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Estrogen-induced yolk precursors in European sea bass, Dicentrarchus labrax: Status and perspectives on multiplicity and functioning of vitellogenins Ozlem Yilmaz a,b,⇑, Francisco Prat c,d, Antonio José Ibáñez c,e, Haruna Amano f, Sadi Koksoy g, Craig V. Sullivan h,i a
Akdeniz University, Fisheries Faculty, Antalya 07070, Turkey National Institute of Agrinomic Research, Campus de Beaulieu, 35000 Rennes Cedex, France1 c Institute of Aquaculture of Torre de la Sal (CSIC), 12595 Castellón, Spain d Institute of Marine Sciences of Andalucía (CSIC), 11510 Cádiz, Spain1 e Electron and Confocal Microscopy Service, University of Valencia, 46100 Valencia, Spain1 f School of Marine Biosciences, Kitasato University, 1-15-1 Kitasato, Minami, Sagamihara, Kanagawa 252-0373, Japan g Faculty of Medicine, Akdeniz University, Antalya 07070, Turkey h Department of Biology, North Carolina State University, Raleigh, NC 27695-7617, USA i Carolina AquaGyn, P.O. Box 12914, Raleigh, NC 27605, USA1 b
a r t i c l e
i n f o
Article history: Available online xxxx Keywords: Teleost Reproduction Lipoprotein Vitellogenin Oocyte Yolk
a b s t r a c t The estrogen-inducible egg yolk precursor, vitellogenin, of the European sea bass (Dicentrarchus labrax) has received considerable scientific attention by virtue of its central importance in determination of oocyte growth and egg quality in this important aquaculture species. However, the multiplicity of vitellogenins in the sea bass has only recently been examined. Recent cloning and homology analyses have revealed that the sea bass possesses the three forms of vitellogenin, VtgAa, VtgAb and VtgC, reported to occur in some other highly evolved teleosts. Progress has been made in assessing the relative abundance and special structural features of the three Vtgs and their likely roles in oocyte maturation and embryonic nutrition. This report discusses these findings in the context of our prior knowledge of vitellogenesis in this species and of the latest advances in our understanding of the evolution and function of multiple Vtgs in acanthomorph fishes. Ó 2015 Published by Elsevier Inc.
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1. Introduction
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In oviparous vertebrates, vitellogenin (Vtg) is synthesized by the liver in response to estrogen and is secreted into the blood, from where it is taken up by growing oocytes via receptor-mediated endocytosis and enzymatically processed by cathepsin D into the major yolk proteins (review: Polzonetti-Magni et al., 2004; Babin et al., 2007). These yolk proteins (YPs) include lipovitellin (Lv; heavy chain [LvH], light chain [LvL]), phosvitin (Pv), b0 -compo-
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Abbreviations: ELISA, enzyme-linked immunosorbent assay; LDL, low-density lipoprotein; RT-PCR, reverse transcription-polymerase chain reaction; RT-qPCR, real-time quantitative PCR; SDS–PAGE, sodium dodecylsulphate polyacrylamide gel electrophoresis; Vldlr, very low density lipoprotein receptor. ⇑ Corresponding author at: National Institute of Agronomic Research (INRA), UR1037 Laboratory of Fish Physiology and Genomics, Campus de Beaulieu, 35042 Rennes Cedex, France. E-mail address: [email protected] (O. Yilmaz). 1 Present address.
nent (b0 c), and C-terminal peptide (Ct) (reviews: Finn, 2007a,b). The largest is Lv, an apoprotein delivering mainly phospholipids into growing oocytes (review: Romano et al., 2004). The smallest is Pv, which largely consists of phosphorylated serine residues thought to stabilize nascent Vtg structure during lipid loading and to enhance solubility of Vtg in the blood (Finn, 2007b). The b0 c and Ct are small cleavage products of a YP domain homologous to von Willebrand factor type D (VWFD) that contains a highly conserved motif of repeated cysteine residues postulated to stabilize the Vtg dimer for cellular recognition and receptor binding, and to protect Vtg or its product YPs from premature or inappropriate proteolysis (Wallace et al., 1990; Finn, 2007b). In the most recently evolved group of teleosts (Acanthomorpha), the tripartite Vtg system generally includes two complete Vtg paralogs (VtgAa and VtgAb) bearing all YP domains, and an incomplete Vtg (VtgC) lacking Pv and much of the C-terminus (b0 c/Ct) (reviews: Finn and Kristoffersen, 2007; Reading and Sullivan, 2011). The different forms of Vtg appear to disparately bind to
http://dx.doi.org/10.1016/j.ygcen.2015.01.018 0016-6480/Ó 2015 Published by Elsevier Inc.
Please cite this article in press as: Yilmaz, O., et al. Estrogen-induced yolk precursors in European sea bass, Dicentrarchus labrax: Status and perspectives on
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different forms of Vtg receptor (Vtgr) (reviews: Hiramatsu et al., 2013, this volume) and they and their product YPs undergo different degrees of proteolysis by various cathepsins during oocyte growth and oocyte maturation (OM) (Carnevali et al., 2006). In some marine teleosts spawning pelagic eggs, virtually all YPs derived from VtgAa may be proteolytically cleaved into free amino acids (FAAs) during OM, whereas the major products of VtgAb (LvHAb) and VtgC (LvHC) remain largely intact. The FAAs act as osmotic effectors of oocyte hydration (review: Cerdà et al., 2007) and serve as diffusible nutrients selectively utilized by early embryos, while the large lipoproteins derived from VtgAb and VtgC are utilized later by the larvae (review: Matsubara et al., 1999, 2003). Thus, the multiple Vtg system provides for proper adjustment of egg buoyancy and delivers the appropriate types of nutrients for each stage of early development. The degree to which dysfunction of multiple Vtg systems is involved in poor egg quality, which is widespread in finfish aquaculture (Bromage, 1995) and the subject of intensive investigation (Brooks et al., 1997; Cerdà et al., 2008; Bobe and Labbé, 2010), has not previously been explored. Vitellogenins and vitellogenesis have received some prior study in European sea bass (Dicentrarchus labrax), an acanthomorph teleost spawning pelagic eggs in seawater that is highly prized in marine fisheries and aquaculture (Carrillo et al., 1995; Saillant et al., 2003). However, multiplicity of Vtgs in this species has been heretofore unknown. This review covers prior research on the biochemistry and physiology of vitellogenesis in sea bass relevant to egg quality in farmed fish, and then presents results of recent research on multiplicity of Vtgs in this species, emphasizing observations relevant to the evolution and functioning of the different forms of Vtg.
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2. Vitellogenesis and yolk formation in sea bass
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Sea bass Vtg has been purified using a two-step chromatography process that, based on our present knowledge of the biochemistry of multiple Vtgs in Moronidae (see Hiramatsu et al., 2002c; see also Reading et al., 2011, Supplemental Fig. 1), would have resulted in the loss of VtgC in the pass-through fraction during the second ion-exchange procedure (Mañanós et al., 1994a). The resulting Vtg preparation, likely a mixture of the A-type Vtgs (VtgAa and VtgAb), exhibited an apparent molecular weight in gel filtration and an amino acid composition similar to those reported for complete forms of teleost Vtg from other teleosts. A rabbit antibody raised against the sea bass Vtg was employed in immunocytochemistry to localize the protein in the liver and ovary and in Western blotting to verify induction of vitellogenesis in estrogentreated males, the presence of the Vtgs in the plasma of naturally vitellogenic females, and the existence of corresponding Vtgderived yolk proteins in ovulated egg extracts (Mañanós et al., 1994a). The apparent mass of the sea bass VtgA monomer(s) (180 kDa) in SDS- PAGE is in close agreement with that reported for other members of the family Moronidae, striped bass, Morone saxatilis (A-type Vtg 170 kDa; Tao et al., 1993) and white perch, M. americana (VtgAa and VtgAb 180 kDa; Hiramatsu et al., 2002b), and the induction of vitellogenesis in males by estrogen was confirmed by homologous ELISA to be dose-dependent. The ELISA was later used to describe annual variations in plasma Vtg levels in farmed adults held at natural seasonal temperature and day length in Torre de la Sal, Spain (Mañanós et al., 1994b). The Vtg levels corresponded well to the progression of oocyte growth revealed by histology, with plasma Vtg rising at the onset of vitellogenesis in October, peaking at over 3 mg/ml in December, and dropping thereafter to intermediate values (1.5 mg/ml) that were sustained through May, approximately until the end of the natural spawning season. Strikingly similar profiles of plasma Vtg have
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been reported for other Moronidae family members, including striped bass (Tao et al., 1993; Woods and Sullivan, 1993), white perch (Jackson and Sullivan, 1995), and white bass, Morone chrysops (Berlinsky et al., 1995). Annual plasma Vtg profiles were also assessed in captive females maturing under natural or experimentally altered photothermal cycles (Mañanós et al., 1997b). In all groups, changes in plasma Vtg levels were positively correlated with estradiol-17b (E2) levels, oocyte growth, and spawning time. Profiles of plasma Vtg in control fish were as seen before, with high Vtg levels (1.6–1.9 mg/ml) being sustained during the entire spawning period together with the presence of vitellogenic oocytes, suggesting the existence of several waves of oocyte growth in the ovary and, thus, several spawns per female. In general, the annual Vtg profiles were shifted and compressed in females exposed to experimental day length cycles that advanced or delayed spawning time. The sea bass Vtg ELISA was also employed to evaluate the influence of broodstock ration on plasma Vtg and E2 levels and reproductive performance of females (Cerdà et al., 1994). In adult females fed a natural trash fish (Boops boops) diet at either 1.04% or 0.45% body weight/day for 6 months before spawning, the lower ration was associated with decreased growth rates, condition factor and plasma E2 levels, and a delay in the onset of vitellogenesis and spawning. However, the profiles of plasma Vtg levels were similar between the two groups as were egg quality (% buoyant eggs) and biochemical composition, and also larval hatching rates and survival for 40 days. The influence of dietary lipid composition on plasma levels of Vtg, E2, and GtH II (FSH) and reproductive performance was also investigated (Navas et al., 1998). When fish were fed the natural control diet of trash fish, a commercially available pelleted diet with 10% lipid content, or the commercial diet supplemented to 22% lipid content with refined fish oil enriched with n-3 fatty acids, fish fed the pelleted diets exhibited a greater decrease in plasma Vtg levels during the middle of the spawning period, and this was correlated with a decrease in reproductive performance (egg viability, hatching rate). Collectively, the results of these studies illustrate the reliability of plasma Vtg levels as indicators of the status and progression of oogenesis and the potential gamete quality of sea bass held under various experimental conditions. A more remarkable linkage of vitellogenesis to egg quality was made by Carnevali et al. (2001), who evaluated lysosomal enzyme activities in sea bass eggs and embryos. As in other marine pelagic spawners, floating sea bass eggs have the potential to produce viable embryos whereas sinking eggs do not and, as noted, the acquisition of egg buoyancy is related to the generation of FAAs via proteolysis of Vtg during OM (review Cerdà et al., 2007). It was found that cathepsin D was present at significantly higher levels in sinking sea bass eggs, whereas cathepsin L was more abundant in the floating eggs (Carnevali et al., 2001), and a relationship of cathepsin gene expression or enzyme activity to egg quality was subsequently verified in several studies of a variety of species (review: Carnevali et al., 2006). Vitellogenin receptors (Vtgrs) have been detected in sea bass using the preparation of A-type Vtgs in ‘grind and bind’ studies employing 125I-Vtg as the tracer and solubilized ovarian membrane proteins as the receptor preparation (Mañanós et al., 1997a). Ligand blots revealed a 100 kDa receptor protein that specifically bound Vtg, and filter binding assays indicated that the binding was specific and saturable with a Kd in the mid nM range. Based upon its apparent mass and binding characteristics, the identified Vtgr likely corresponds to the ‘classical’ Vtgr that has been described in striped bass and white perch (Tao et al., 1996; Reading et al., 2011), which preferentially binds the major form of Vtg (VtgAb) to mediate its uptake into growing oocytes (reviews: Hiramatsu et al., 2013, this volume). This Vtgr is also described as the
Please cite this article in press as: Yilmaz, O., et al. Estrogen-induced yolk precursors in European sea bass, Dicentrarchus labrax: Status and perspectives on
Q1 multiplicity and functioning of vitellogenins. Gen. Comp. Endocrinol. (2015), http://dx.doi.org/10.1016/j.ygcen.2015.01.018
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LR8- receptor because it has 8 class-A ligand-binding repeats (LR) at its N-terminus and lacks the distal O-linked sugar domain that is present in the twin Vldlr (LR8+) sequence present in other teleosts, of which the Vtgr is a splice variant. Full-length cDNAs encoding Moronidae LR8- Vtgrs have been obtained for sea bass (Prat, Martínez-Rodríguez, Shaw, Sánchez, Ibáñez, Cerdá-Reverter, Gómez, and Zanuy, unpublished data; Genbank SbsVtgr FR717659.1; Sánchez et al., 2004) and white perch (Hiramatsu et al., 2004). Expression of the sea bass vtgr mRNA in isolated ovarian follicles was shown by RT-qPCR to be highest in previtellogenic stages, decreasing to low levels during vitellogenesis (García-López et al., 2011), a pattern also seen in white perch ovaries (Hiramatsu et al., 2004) that indicates most receptors are synthesized at early stages of oocyte development and stored for later mobilization to support oocyte growth. In addition to these investigations relevant to egg quality in sea bass, the aforementioned ELISA has been utilized to measure Vtg in this species as a biomarker for exposure of the fish to environmental pollutants with estrogenic activity, such as certain alkylphenols (e.g. Fernandes et al., 2008, 2009).
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3. Multiplicity of sea bass vitellogenins
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Three complete sea bass vtg cDNAs were assembled from contiguous partial sequences obtained by RT-PCR and cloning and the obtained full-length cDNA sequences have been deposited in GenBank (SbsvtgAa, JQ283441; SbsvtgAb, JQ283442; SbsvtgC, JQ341410). The deduced polypeptide products encoded by these cDNAs were classified via alignment of their sequences to those of other teleost Vtgs, which revealed homologies across a broad
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array of taxa and definitively identified them as sea bass VtgAa, VtgAb and VtgC (Yilmaz, 2013). As in other acanthomorph teleosts, the two A-type Vtg paralogs are complete, possessing all Vtgderived yolk protein (YP) domains, and the VtgC lacks a Pv domain and the two C-terminal YP domains (b0 c and Ct). The three forms of Vtg and their derived YPs were detected by label-free quantitative mass spectrometry and quantified in blood plasma and ovary of postvitellogenic females based on normalized counts of tryptic peptide spectra mapped to their parent Vtg polypeptide sequences (Yilmaz et al., 2013). The VtgAb appears to be the dominant form of Vtg in sea bass, being 3-fold more abundant in the plasma than VtgAa and 8-fold more abundant than VtgC. However, all three forms of Vtg make a substantial contribution to the egg yolk, with the postvitellogenic ovarian YPAa:YPAb:YPC ratio being 1.5:3.0:1. Similar disparities between abundance ratios of the Vtgs in plasma and the corresponding YP ratios in oocytes or eggs have been observed in several other teleosts, including striped bass (see Hiramatsu et al., this volume; Table 1), leading researchers to speculate that there may be receptor-based mechanisms for disparate accumulation of the different forms of Vtg by growing oocytes. In the Moronidae species, multiple ovarian membrane proteins with different affinities for VtgAa and VtgAb have been discovered (Reading et al., 2011). In addition to the classical LR8- Vtgr (Hiramatsu et al., 2004), which preferentially binds VtgAb in white perch, there is a novel receptor initially termed ‘‘LR7+1’’ based the unusual structure of its ligand-binding domain(s), which includes 7 N-terminal and one distal LR. This receptor appears to preferentially bind VtgAa in white perch (Reading et al., 2011) and was subsequently classified as a new type of low-density lipoprotein receptor-related protein (Lrp) named Lrp13 (Reading et al., 2014). Interestingly, while the VtgC does not appear to bind to ovarian
Table 1 Oocyte hydration and maturational proteolysis of lipovitellins in Moronidae and some other teleosts whose multiple vitellogenin systems have been investigated. Lv, lipovitellin; LvH, Lv heavy chain; LvL, Lv light chain: VtgAc, Clupea harengus Vtg. Number superscripts indicate references for oocyte and egg diameter values used to calculate oocyte and egg volumes (see footnote). Species SW pelagic Goldsinny wrasse Haddock1 Atlantic halibut1 Barfin flounder2 SW benthi Mummichog3 Atlantic herring4 Moronidae Sea bass5 Striped bass
6
White perch White bass8 1 2 3 4 5 6 7 8 *
7
Egg type
Oocyte volume (mm3)
Egg volume (mm3)
Percent change
Fold change
Lipovitellin (Lv) proteolysis
References for Lv proteolysis
SW pelagic SW pelagic SW pelagic SW pelagic
0.05
0.33
547
6.47X
LvHAa
Kolarevic et al. (2008)
0.23
1.38
500
6.00X
LvHAa LvHAb
Reith et al. (2001)
3.42
15.30
347
4.47X
Finn (2007a)
0.68
2.81
313
4.13X
LvHAa LvHAb, LvLAb LvHAa LvHAb, LvLA
SW demersal SW demersal
1.30
2.90
123
2.23X
LvHAa
La Fleur et al. (2005)
0.54
0.85
57
1.57X
VtgAc1’VtgAc2
Kristoffersen et al. (2009)
SW pelagic FW pelagic FW demersal FW demersal
0.27
0.80
196
2.96X
LvHAa’LvHAb’LvC
This study
0.34
0.76
124
2.24X
LvHAa’LvHAb’LvC
Williams et al. (2014)
*
0.15
0.30
100
2.00X
LvHAa+LvHAb, LvC
0.16
0.35
119
2.19X
LvHAa+LvHAb, LvC*
Matsubara et al. (1999)
Reading et al. (2009) and Hiramatsu et al. (2002a,b) Hiramatsu et al. (2002b) and Reading et al. (2009)
Finn et al. (2000). Matsubara and Koya (1997). Greeley et al. (1991). Kristoffersen and Finn (2008). Mayer et al. (1988). Mylonas et al. (1997). Jackson and Sullivan (1995). Hiramatsu et al. (2002c); see References for Latin binomial species names. Degree of VtgC proteolysis unknown, LvH proteolysis inferred from comparisons of white bass and/or perch with striped bass (see text for details).
Please cite this article in press as: Yilmaz, O., et al. Estrogen-induced yolk precursors in European sea bass, Dicentrarchus labrax: Status and perspectives on
Q1 multiplicity and functioning of vitellogenins. Gen. Comp. Endocrinol. (2015), http://dx.doi.org/10.1016/j.ygcen.2015.01.018
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membrane proteins in white perch and has been speculated to enter oocytes in the fluid phase or via some other means, a least two unidentified receptors bind VtgC in the cutthroat trout, Oncorhynchus clarki (Hiramatsu et al., this volume). We compared the predicted 3-dimensional (3-D) structures, conserved glycine and proline residues, and conserved charged residues of the 85 residue receptor-binding domain (Li et al., 2003) present on the N-sheet of sea bass A- and C-type Vtgs (see Finn, 2007a). Glycine and proline have unique properties that make them particularly important to the secondary structure of proteins (review: Betts and Russell, 2003) and it is thought that binding of ligands to the Ldlr- family lipoprotein receptors is mediated by electrostatic interactions between positively charged residues on the ligand and negatively charged residues (e.g. SDE) present on LRs of the receptor (Huang et al., 2010). Some results of the analysis are shown for sea bass VtgAb and VtgC in Fig. 1. The predicted 3-D structures of the two receptor-binding domains are strikingly different, as is the distribution of positively and negatively charged residues on their surfaces. The structural differences may be due, in part, to massive substitution of glycine and proline residues in sea bass VtgC that are highly conserved among A-type Vtgs, with these substitutions occurring in almost all teleost VtgCs examined (Yilmaz, Prat and Sullivan, unpublished data). Also, in addition to the non-conservative substitution of a glutamine [Q] for the lysine [K181] residue found by Li et al. (2003) to be essential for receptor binding and reported by Reading et al. (2009) to be highly conserved in A-type Vtgs, the cysteines forming one of two disulfide bonds present in the receptor-binding domain of all A-type Vtgs (C204–C207 in sea bass VtgAb) are substituted in sea bass VtgC and in virtually all other teleost VtgCs examined (Fig. 1). These structural changes may explain the inability of Moronidae VtgC to bind to the A-type Vtg receptors. The different types of sea bass Vtg were also compared with regard to the proteolytic fates of their product Lvs during oocyte maturation. Western blotting performed using Vtg-type specific
antisera raised against purified gray mullet (Mugil cephalus) LvAa, LvAb, and LvC (Amano et al., 2008) confirmed the presence of the three Vtgs and their derived Lvs in blood plasma and ovary, respectively, and revealed that all three forms of sea bass LvH are partially degraded during oocyte maturation, as evidenced by the de novo appearance in Western blots of egg extracts of multiple immunoreactive bands with a lower apparent mass than the respective LvH (Yilmaz et al., 2013). Similar findings based on Western blotting using Vtg-type specific antisera raised against white perch Vtgs were recently made for the three forms of LvH in striped bass (Williams et al., 2014; Reading et al., 2009) and can be postulated for white bass based upon the gradual (incomplete) disappearance of the heaviest YP band (110 kDa) seen in SDS–PAGE of oocyte extracts, which contains a mixture of A-type LvHs (Hiramatsu et al., 2002a), with concomitant appearance of lower molecular weight bands as the oocytes matured in vivo or in vitro (Hiramatsu et al., 2002c). However, the broad degradation of all three forms of LvH seen in sea bass is unusual for a highly evolved marine teleost spawning pelagic eggs, in which preferential proteolysis of LvHAa appears to be the norm (Table 1). Moronidae is a monophyletic assemblage of very closely related species (Williams et al., 2012) and the similarity of Vtgs and vitellogenesis among these species, which includes an extraordinary degree of homology among their deduced Vtg polypeptide sequences (Fig. 2), is not entirely surprising. The LvH sequences of striped bass and white perch Vtgs are 95.1–95.8% identical and 97.5–98.1% similar to the corresponding sequences in sea bass; for LvL, these figures are 89.5–96.5% and 94.1–98.0%, respectively, and the b0 c and Ct domains are equally well conserved. Even for the Pvs, which are less conserved among teleosts, the Morone sequences are 68.1–86.2% identical and 68.1–88.8% similar to their counterparts in sea bass. However, when we consider the very different reproductive life histories and egg types among the Moronidae (Table 1), the high homologies and the similar pattern of LvH proteolysis during OM present something of a conundrum.
Fig. 1. Predicted three-dimensional surface distribution of highly conserved charged amino acid residues in the 85 amino acid receptor binding domains of sea bass VtgAa and VtgC. Geno3D (Combet et al., 2002) was used to model the molecular structures using aligned residues from the crystallographically resolved structure of lamprey Lv (Anderson et al., 1998) as the template and the PyMol molecular visualization system (http://www.pymol.org/) was employed for imaging. Conservation of residues was judged from results of an Evolutionary Trace (ET) analysis (Litcharge et al., 1996) obtained by the entering lamprey (I. unicuspis) Lv sequence Protein Data Bank (PDB) identifier 1lsh into the ET Report Maker. Note the substantial differences in predicted surface charge distribution and structure between the receptor-binding sites of the two types of Vtg. Arrows indicate the position of cysteine residues involved in the conserved disulfide bond present in sea bass VtgAb (C204–C207) that are substituted in the VtgC of sea bass and other teleosts. See text for details.
Please cite this article in press as: Yilmaz, O., et al. Estrogen-induced yolk precursors in European sea bass, Dicentrarchus labrax: Status and perspectives on
Q1 multiplicity and functioning of vitellogenins. Gen. Comp. Endocrinol. (2015), http://dx.doi.org/10.1016/j.ygcen.2015.01.018
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Fig. 2. Conservation of vitellogenin (Vtg) polypeptide sequences in the family Moronidae. The domain structure of each form of sea bass (D. labrax) Vtg is shown: (A) VtgAa; (B) VtgAb; (C) VtgC. Beneath each domain, the percent identity of the corresponding sequence in striped bass (M. saxatilis) and white perch (M. americana) is shown in boldface type with the percent similarity indicated below in plain typeface set in parentheses. For each form of Vtg, before calculating the identity and similarity values, the homologous sequences from the three Moronidae species were aligned using ClustalW (Thompson et al., 1994). Sp, signal peptide; LvH, lipovitellin heavy chain; Pv, phosvitin; LvL, lipovitellin light chain; b0 c, b0 -component; Ct, C-terminal component.
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As noted, sea bass spawn pelagic eggs in seawater (SW), while the striped bass is a fresh water (FW) spawner of eggs that are pelagic only in turbulent waters, and the white perch and white bass both spawn demersal eggs in FW. These differences are reflected to only a limited extent by the degree to which the oocytes hydrate and increase in volume during OM (Table 1). The fold increase in volume of maturing sea bass oocytes (3X) falls at the lower end of the range for marine pelagic spawners in which LvHAa is preferentially hydrolyzed during OM, and it is only slightly greater than that of the mummichog (SW demersal), the striped bass (FW pelagic), and the other two Morone species (FW demersal) (Table 1). In the sea bass, while oocyte constituents other than water, notably lipids, may make the major contribution to egg buoyancy, minor adjustments of buoyancy seemingly involve maturational proteolysis of all three forms of LvH (and perhaps other YPs), and these adjustments are probably important, as evidenced by the linkage of cathepsin D and cathepsin L activities to egg buoyancy in this species (Carnevali et al., 2006).
Confirmation of these hypotheses will require further studies in which the maturational proteolysis of YPs is described in more detail and the quantities and profiles of free amino acids in the eggs are measured and mapped to their parent YPs (e.g. Finn, 2007a).
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4. Conclusion
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In the European sea bass, plasma Vtg levels and profiles are an established indicator of the status and progress of maturation and, in some cases, they and Vtg-processing enzyme (cathepsin) activities may predict the quality of the resulting eggs. The sea bass produces all three forms of Vtg described for acanthomorph teleosts. The VtgAb is the dominant form of Vtg in this species, but all three types of Vtg contribute significantly to the store of YPs deposited in eggs. Observed differences in deposition of A- and C-type Vtgs and the lack of receptor binding by VtgC are likely due to extensive
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Please cite this article in press as: Yilmaz, O., et al. Estrogen-induced yolk precursors in European sea bass, Dicentrarchus labrax: Status and perspectives on
Q1 multiplicity and functioning of vitellogenins. Gen. Comp. Endocrinol. (2015), http://dx.doi.org/10.1016/j.ygcen.2015.01.018
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modification of the 3-D structure of the receptor-binding domain in VtgC, including the distribution of charged residues across its surface. Although hydration of the oocytes during OM is limited in sea bass compared to other marine fish spawning pelagic eggs, all three types of sea bass LvH undergo noticeable proteolysis during this time and likely contribute to the store of FAAs involved in oocyte hydration and early embryo nutrition. The obtained Vtg sequences and mass spectrometry methods employed in the cited studies set the stage for discovery of the role(s) that the multiple Vtg system plays in determining egg quality in farmed sea bass.
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Acknowledgments
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The research on multiple sea bass Vtgs is, in part, included in the doctoral dissertation of O.Y. at the Faculty of Fisheries, Postgraduate School of Natural and Applied Sciences, Akdeniz University, Antalya, Turkey (Yilmaz, 2013). This research was supported by an Akdeniz University Scientific Research Coordinating Unit Ph.D. research grant (2009.03.0121.008) and a Fulbright Doctoral Research fellowship granted to O.Y., and by awards from the North Carolina Sea Grant Program (award number R/12-SSS-3), the North Carolina Agricultural Foundation, Inc., and Carolina AquaGyn to CVS. These supporters had no role in the design, execution, reporting or decision to publish the research. Some results of this study were reported at the 6th Fish and Shellfish Larviculture Symposium (LARVI 2013), 2–5 September, 2013, Ghent, Belgium, or were presented at the 10th International Symposium on Reproductive Physiology of Fish, Olhão, Portugal, 25–30 May, 2014.
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References
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Amano, H., Fujita, T., Hiramatsu, N., Kagawa, H., Matsubara, T., Sullivan, C.V., Hara, A., 2008. Multiple vitellogenin-derived yolk proteins in gray mullet (Mugil cephalus): disparate proteolytic patterns associated with ovarian follicle maturation. Mol. Reprod. Dev. 75, 1307–1317. Anderson, T.A., Levitt, D.G., Banaszak, L.J., 1998. The structural basis of lipid interactions in lipovitellin, a soluble lipoprotein. Structure 6, 895–909. Babin, P.J., Carnevali, O., Lubzens, E., Schneider, W.J., 2007. Molecular aspects of oocyte vitellogenesis in fish. In: Babin, P.J., Cerdà, J., Lubzens, E. (Eds.), The Fish Oocyte: from Basic Studies to Biotechnological Applications. Springer, Netherlands, pp. 39–76, Chapter 2. Berlinsky, D.L., Jackson, L.F., Sullivan, C.V., 1995. The annual reproductive cycle of white bass, Morone chrysops. J. World Aquaculture Soc. 26, 252–260. Betts, M.J., Russell, R.B., 2003. Amino acid properties and consequences of substitutions. In: Barnes, M.R., Gray, I.C. (Eds.), Bioinformatics for Geneticists. John Wiley and Sons Ltd., West Sussex, England, pp. 289–316, Chapter 14. Bobe, J., Labbé, C., 2010. Egg and sperm quality in fish. Gen. Comp. Endocrinol. 165, 535–548. Bromage, N., 1995. Broodstock management and seed quality: general considerations. In: Bromage, N.R., Roberts, R.J. (Eds.), Broodstock Management and Egg and Larval Quality. Blackwell Science, Oxford, UK, pp. 1–24, Chapter 1. Brooks, S., Tyler, C.R., Sumpter, J.P., 1997. Egg quality in fish: what makes a good egg? Rev. Fish Biol. Fish. 7, 387–416. Carnevali, O., Mosconi, G., Cambi, A., Ridolfi, S., Zanuy, S., Polzonetti-Magni, A.M., 2001. Changes of lysosomal enzyme activities in sea bass (Dicentrarchus labrax) eggs and developing embryos. Aquaculture 202, 249–256. Carnevali, O., Cionna, C., Tosti, L., Lubzens, E., Maradonna, F., 2006. Role of cathepsins in ovarian follicle growth and maturation. Gen. Comp. Endocrinol. 146, 195–203. Carrillo, M., Zanuy, S., Prat, F., Cerdá, J., Ramos, J., Mañanós, E., Bromage, N., 1995. Sea bass (Dicentrarchus labrax). In: Bromage, N.R., Roberts, R.J. (Eds.), Broodstock Management and Egg and Larval Quality. Blackwell Science, Oxford, UK, pp. 138–168, Chapter 7. Cerdà, J., Bobe, J., Babin, P.J., Admon, A., Lubzens, E., 2008. Functional genomics and proteomic approaches for the study of gamete formation and viability in farmed finfish. Rev. Fish. Sci. 16, 56–72. Cerdà, J., Carrillo, M., Zanuy, S., Ramos, J., 1994. Effect of food ration on estrogen and vitellogenin plasma levels, fecundity and larval survival in captive sea bass Dicentrarchus labrax: preliminary observations. Aquat. Living Resour. 7, 255– 256. Cerdà, J., Fabra, M., Raldúa, D., 2007. Physiological and molecular basis of fish oocyte hydration. In: Babin, P.J., Cerdà, J., Lubzens, E. (Eds.), The Fish Oocyte: from Basic Studies to Biotechnological Applications. Springer, Dordrecht, The Netherlands, pp. 349–396, Chapter 12. Combet, C., Jambon, M., Deléage, G., Geourjon, C., 2002. Geno3D: automatic comparative molecular modeling of protein. Bioinformatics 18, 213–214.
367 368 369 370 371 372 373 374 375
379 380 381 382 383 384 385 386 387 388 389 390 391
Fernandes, D., Zanuy, S., Bebianno, M.J., Porte, C., 2008. Chemical and biochemical tools to assess pollution exposure in cultured fish. Environ. Pollut. 152, 138– 146. Fernandes, D., Bebianno, M.J., Porte, C., 2009. Assessing pollutant exposure in cultured and wild sea bass (Dicentrarchus labrax) from the Iberian Peninsula. Ecotoxicology 18, 1043–1050. Finn, R.N., Fyhn, H.J., Norberg, B., Munholland, J., Reith, M., 2000. Oocyte hydration as a key feature in the adaptive evolution of teleost fishes to seawater. In: Norberg, B., Kjesbu, O.S., Taranger, G.L., Andersson, E., Stefansson, S.O. (Eds.), Proceedings of the 6th International Symposium on the Reproductive Physiology of Fish. University of Bergen, Bergen, Norway, pp. 289–291. Finn, R.N., 2007a. The maturational disassembly and differential proteolysis of paralogous vitellogenins in a marine pelagophil teleost: a conserved mechanism of oocyte hydration. Biol. Reprod. 76, 936–948. Finn, R.N., 2007b. Vertebrate yolk complexes and the functional implications of phosvitins and other subdomains in vitellogenins. Biol. Reprod. 76, 926–935. Finn, R.N., Kristoffersen, B.A., 2007. Vertebrate vitellogenin gene duplication in relation to the ‘‘3R hypothesis’’: correlation to the pelagic egg and the oceanic radiation of teleosts. PLoS One 2, e169. García-López, A., Sánchez-Amaya, M.I., Prat, F., 2011. Targeted gene expression profiling in European sea bass (Dicentrarchus labrax, L.) follicles from primary growth to late vitellogenesis. Comp. Biochem. Physiol. A 160, 374–380. Greeley, M.S., Hols, H., Wallace, R.A., 1991. Changes in size, hydration and low molecular weight osmotic effectors during meiotic maturation of Fundulus oocytes in vivo. Comp. Biochem. Physiol. 100A, 639–647. Hiramatsu, N., Chapman, R.W., Lindzey, J.K., Haynes, M.R., Sullivan, C.V., 2004. Molecular characterization and expression of vitellogenin receptor from white perch (Morone americana). Biol. Reprod. 70, 720–1730. Hiramatsu, N., Hara, A., Hiramatsu, K., Fukada, H., Weber, G.M., Denslow, N.D., Sullivan, C.V., 2002a. Vitellogenin-derived yolk proteins of white perch, Morone americana: purification, characterization and vitellogenin-receptor binding. Biol. Reprod. 67, 655–667. Hiramatsu, N., Luo, W., Reading, B.J., Sullivan, C.V., Mizuta, H., Ryu, Y.-W., Nishimiya, O., Todo, T., Hara, A., 2013. Ovarian lipoprotein receptors in teleosts. Fish Physiol. Biochem. 39, 29–32. Hiramatsu, N., Matsubara, T., Hara, A., Donato, D.M., Hiramatsu, K., Denslow, N.D., Sullivan, C.V., 2002b. Identification, purification and classification of multiple forms of vitellogenin from white perch (Morone americana). Fish Physiol. Biochem. 26, 355–370. Hiramatsu, N., Matsubara, T., Weber, G.M., Sullivan, C.V., Hara, A., 2002c. Vitellogenesis in aquatic animals. Fish. Sci. 68, 694–699. Hiramatsu, N., Todo, T., Sullivan, C.V., Schilling, J., Reading, B.J., Matsubara, Ryu Y.W., Mizuta, H., Luo, W., Nishimiya, O., Wu, M., Mushirobira, M., Yilmaz, O., Hara, A. Ovarian yolk formation in fishes: molecular mechanisms underlying formation of lipid droplets and vitellogenin-derived yolk proteins (this volume). Huang, S., Henry, L., Ho, H.-K., Pownall, H.J., Rudenko, G., 2010. Mechanism of LDL binding and release probed by structure-based mutagenesis of the LDL receptor. J. Lipid Res. 2010 (51), 297–308. Jackson, L.F., Sullivan, C.V., 1995. Reproduction of white perch (Morone americana): the annual gametogenic cycle. Trans. Am. Fish. Soc. 124, 563–577. Kolarevic, J., Nerland, A., Nilsen, F., Finn, R.N., 2008. Goldsinny wrasse (Ctenolabrus rupestris) is an extreme vtgAa-type pelagophil teleost. Mol. Reprod. Dev. 75, 1011–1020. Kristoffersen, B.A., Finn, R.N., 2008. Major osmolyte changes during oocyte hydration of a clupeocephalan marine benthophil: Atlantic herring (Clupea harengus). Mar. Biol. 154, 683–692. Kristoffersen, B.A., Nerland, A., Nilsen, F., Kolarevic, J., Finn, R.N., 2009. Genomic and proteomic analyses reveal non-neofunctionalized vitellogenins in a basal clupeocephalan, the Atlantic herring, and point to the origin of maturational yolk proteolysis in marine teleosts. Mol. Biol. Evol. 26, 1029–1044. La Fleur Jr., G.J., Raldúa, D., Fabra, M., Carnevali, O., Denslow, N., Wallace, R.A., Cerdà, J., 2005. Derivation of major yolk proteins from parental vitellogenins and alternative processing during oocyte maturation in Fundulus heteroclitus. Biol. Reprod. 73, 815–824. Li, A., Sadasivam, M., Ding, J.L., 2003. Receptor-ligand interaction between vitellogenin receptor (VtgR) and vitellogenin (Vtg), implications on low density lipoprotein receptor and apolipoprotein B/E. J. Biol. Chem. 278, 2799– 2806. Litcharge, O., Bourne, H.R., Cohen, F.E., 1996. An evolutionary trace method defines binding surfaces common to protein families. J. Mol. Biol. 257, 342–358. Mañanós, E.L., Zanuy, S., Le Menn, F., Carrillo, M., Núñez, J., 1994a. Sea bass (Dicentrarchus labrax) vitellogenin. I – Induction, purification, and partial characterization. Comp. Biochem. Physiol. B 107, 205–216. Mañanós, E.L., Núñez, J., Zanuy, S., Carrillo, M., Le Menn, F., 1994b. Sea bass (Dicentrarchus labrax) vitellogenin. II – validation of an enzyme-linked immunosorbent assay (ELISA). Comp. Biochem. Physiol. B 107, pp. 217–213. Mañanós, E.L., Núñez Rodríguez, J., le Menn, F., Zanuy, S., Carillo, M., 1997a. Identification of vitellogenin receptors in the ovary of a teleost fish, the Mediterranean sea bass (Dicentrarchus labrax). Reprod. Nutr. Dev. 37, 51–61. Mañanós, E.L., Zanuy, S., Carrillo, M., 1997b. Photoperiodic manipulations of the reproductive cycle of sea bass (Dicentrarchus labrax) and their effects on gonadal development, and plasma 17ß-estradiol and vitellogenin levels. Fish Physiol. Biochem. 16, 211–222. Matsubara, T., Koya, Y., 1997. Course of proteolytic cleavage in three classes of yolk proteins during oocyte maturation in barfin flounder, Verasper moseri, a marine teleost spawning pelagic eggs. J. Exp. Zool. 278, 189–200.
Please cite this article in press as: Yilmaz, O., et al. Estrogen-induced yolk precursors in European sea bass, Dicentrarchus labrax: Status and perspectives on
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Matsubara, T., Ohkubo, N., Andoh, T., Sullivan, C.V., Hara, A., 1999. Two forms of vitellogenin, yielding two distinct lipovitellins, play different roles during oocyte maturation and early development of barfin flounder, Verasper moseri, a marine teleost spawning pelagic eggs. Dev. Biol. 213, 18–32. Matsubara, T., Nagae, M., Ohkubo, N., Andoh, T., Sawaguchi, S., Hiramatsu, N., Sullivan, C.V., Hara, A., 2003. Multiple vitellogenins and their unique roles in marine teleosts. Fish Physiol. Biochem. 28, 295–299. Mayer, I., Shackley, S.E., Ryland, J.S., 1988. Aspects of the reproductive biology of the bass, Dicentrarchus labrax L. I: an histological and histochemical study of oocyte development. J. Fish Biol. 33, 609–622. Mylonas, C.C., Woolds III, L.C., Zohar, Y., 1997. Cyto-histological examination of post-vitellogenesis and final oocyte maturation in captive-reared striped bass. J. Fish Biol. 50, 34–49. Navas, J.M., Mañanós, E.L., Thrush, M., Ramos, J., Zanuy, S., Carillo, M., Zohar, Y., Bromage, N., 1998. Effect of dietary lipid composition on vitellogenin, 17bestradiol and gonadotropin plasma levels and spawning performance in captive sea bass (Dicentrarchus labrax L.). Aquaculture 165, 65–79. Polzonetti-Magni, A.M., Mosconi, G., Soverchia, L., Kikuyama, S., Carnevali, O., 2004. Multihormonal control of vitellogenesis in lower vertebrates. Int. Rev. Cytol. 239, 1–45. Reading, B.J., Hiramatsu, N., Sawaguchi, S., Matsubara, T., Hara, A., Lively, M.O., Sullivan, C.V., 2009. Conserved and variant molecular and functional features of multiple vitellogenins in white perch (Morone americana) and other teleosts. Mar. Biotechnol. 11, 169–187. Reading, B.J., Hiramatsu, N., Schilling, J., Molloy, K.T., Glassbrook, N., Mizuta, H., Luo, W., Baltzegar, D.A., Williams, V.N., Hara, A., Sullivan, C.V., 2014. Lrp13 is a novel vertebrate lipoprotein receptor that binds vitellogenins in teleost fishes. J. Lipid Res. 55, 2287–2295. Reading, B.J., Hiramatsu, N., Sullivan, C.V., 2011. Disparate binding of three types of vitellogenin to multiple forms of vitellogenin receptor in white perch. Biol. Reprod. 84, 392–399. Reading, B.J., Sullivan, C.V., 2011. Vitellogenesis in fishes. In: Farrell, A.P., Stevens, E.D., , Cech, J.J., Jr., Richards, J.G. (Eds.), Encyclopedia of Fish Physiology: from Genome to Environment. Elsevier, Maryland Heights, Missouri, USA, pp. 635– 646, Chapter 257. Reith, M., Munholland, J., Kelly, J., Finn, R.N., Fyhn, H.J., 2001. Lipovitellins derived from two forms of vitellogenin are differentially processed during oocyte maturation in haddock (Melanogrammus aeglefinus). J. Exp. Zool. 291, 58–67. Romano, M., Rosanova, P., Anteo, C., Limatola, E., 2004. Vertebrate yolk proteins: a review. Mol. Reprod. Dev. 69, 109–116.
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Saillant, E., Fostier, A., Haffray, P., Menu, B., Chatain, B., 2003. Saline preferendum for the European sea bass, Dicentrarchus labrax, larvae and juveniles: effect of salinity on early development and sex determination. J. Exp. Mar. Biol. Ecol. 287, 103–117. Sánchez, E., Ibáñez, A.J., Shaw, M., Martínez-Rodríguez, G., Zanuy, S., Carrillo, M., Prat, F., 2004. The vitellogenin receptor of European sea bass (Dicentrarchus labrax L.): cloning, molecular characterization and developmental expression. Proceedings of the 5th International Symposium on Fish Endocrinology, September 5–9, Castellón, Spain. Abstract No. P88. Tao, Y., Berlinsky, D.L., Sullivan, C.V., 1996. Characterization of a vitellogenin receptor in white perch (Morone americana). Biol. Reprod. 55, 646–656. Tao, Y., Hara, A., Hodson, R.G., Woods III, L.C., Sullivan, C.V., 1993. Purification, characterization and immunoassay of striped bass (Morone saxatilis) vitellogenin. Fish Physiol. Biochem. 12, 31–46. Thompson, J.D., Higgins, D.G., Gibson, T.J., 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680. Wallace, R.A., Hoch, K., Carnevali, O., 1990. Placement of small lipovitellin subunits with in the vitellogenin precursor in Xenopus laevis. J. Mol. Biol. 213, 407–409. Williams, E.P., Peer, A.C., Miller, T.J., Secor, D.H., Place, A.R., 2012. A phylogeny of the temperate seabasses (Moronidae) characterized by a translocation of the mtnd6 gene. J. Fish Biol. 80, 110–130. Williams, V.N., Reading, B.J., Hiramatsu, N., Amano, H., Glassbrook, N., Hara, A., Sullivan, C.V., 2014. Multiple vitellogenins and product yolk proteins in striped bass, Morone saxatilis: molecular characterization and processing during oocyte growth and maturation. Fish Physiol. Biochem. 40, 395–415. Woods III, L.C., Sullivan, C.V., 1993. Reproduction of striped bass (Morone saxatilis) broodstock: monitoring maturation and hormonal induction of spawning. J. Aquacult. Fish. Manage. 24, 213–224. Yilmaz, O., 2013. Characterization of vitellogenin genes in European sea bass (Dicentrarchus labrax) (Ph.D. dissertation). Akdeniz University, Postgraduate School of Natural and Applied Sciences. Antalya, Turkey. 136 p. Yilmaz, O., Prat, F., Ibáñez, A., Amano, H., Koksoy, S., Sullivan, C.V., 2013. Multiple vitellogenin yolk precursors in European sea bass (Dicentrarchus labrax): molecular cloning, biochemical characterization, quantification in plasma, oocytes and eggs, and potential significance to acquisition of egg buoyancy and to embryonic and larval nutrition. In: C.I. Hendry (Ed.), Proceedings of the 6th Fish and Shellfish Larviculture Symposium (LARVI 2013), 2–5 September, 2013, Ghent, Belgium. European Aquaculture Society, Special Publication No. 505-508, Oostende, Belgium, 2013.
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Estrogen-induced yolk precursors in European sea bass, Dicentrarchus labrax: Status and perspectives on multiplicity and functioning of vitellogenins Ozlem Yilmaz a,b,⇑, Francisco Prat c,d, Antonio José Ibáñez c,e, Haruna Amano f, Sadi Koksoy g, Craig V. Sullivan h,i a
Akdeniz University, Fisheries Faculty, Antalya 07070, Turkey National Institute of Agrinomic Research, Campus de Beaulieu, 35000 Rennes Cedex, France1 c Institute of Aquaculture of Torre de la Sal (CSIC), 12595 Castellón, Spain d Institute of Marine Sciences of Andalucía (CSIC), 11510 Cádiz, Spain1 e Electron and Confocal Microscopy Service, University of Valencia, 46100 Valencia, Spain1 f School of Marine Biosciences, Kitasato University, 1-15-1 Kitasato, Minami, Sagamihara, Kanagawa 252-0373, Japan g Faculty of Medicine, Akdeniz University, Antalya 07070, Turkey h Department of Biology, North Carolina State University, Raleigh, NC 27695-7617, USA i Carolina AquaGyn, P.O. Box 12914, Raleigh, NC 27605, USA1 b
a r t i c l e
i n f o
Article history: Available online xxxx Keywords: Teleost Reproduction Lipoprotein Vitellogenin Oocyte Yolk
a b s t r a c t The estrogen-inducible egg yolk precursor, vitellogenin, of the European sea bass (Dicentrarchus labrax) has received considerable scientific attention by virtue of its central importance in determination of oocyte growth and egg quality in this important aquaculture species. However, the multiplicity of vitellogenins in the sea bass has only recently been examined. Recent cloning and homology analyses have revealed that the sea bass possesses the three forms of vitellogenin, VtgAa, VtgAb and VtgC, reported to occur in some other highly evolved teleosts. Progress has been made in assessing the relative abundance and special structural features of the three Vtgs and their likely roles in oocyte maturation and embryonic nutrition. This report discusses these findings in the context of our prior knowledge of vitellogenesis in this species and of the latest advances in our understanding of the evolution and function of multiple Vtgs in acanthomorph fishes. Ó 2015 Published by Elsevier Inc.
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1. Introduction
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In oviparous vertebrates, vitellogenin (Vtg) is synthesized by the liver in response to estrogen and is secreted into the blood, from where it is taken up by growing oocytes via receptor-mediated endocytosis and enzymatically processed by cathepsin D into the major yolk proteins (review: Polzonetti-Magni et al., 2004; Babin et al., 2007). These yolk proteins (YPs) include lipovitellin (Lv; heavy chain [LvH], light chain [LvL]), phosvitin (Pv), b0 -compo-
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Abbreviations: ELISA, enzyme-linked immunosorbent assay; LDL, low-density lipoprotein; RT-PCR, reverse transcription-polymerase chain reaction; RT-qPCR, real-time quantitative PCR; SDS–PAGE, sodium dodecylsulphate polyacrylamide gel electrophoresis; Vldlr, very low density lipoprotein receptor. ⇑ Corresponding author at: National Institute of Agronomic Research (INRA), UR1037 Laboratory of Fish Physiology and Genomics, Campus de Beaulieu, 35042 Rennes Cedex, France. E-mail address: [email protected] (O. Yilmaz). 1 Present address.
nent (b0 c), and C-terminal peptide (Ct) (reviews: Finn, 2007a,b). The largest is Lv, an apoprotein delivering mainly phospholipids into growing oocytes (review: Romano et al., 2004). The smallest is Pv, which largely consists of phosphorylated serine residues thought to stabilize nascent Vtg structure during lipid loading and to enhance solubility of Vtg in the blood (Finn, 2007b). The b0 c and Ct are small cleavage products of a YP domain homologous to von Willebrand factor type D (VWFD) that contains a highly conserved motif of repeated cysteine residues postulated to stabilize the Vtg dimer for cellular recognition and receptor binding, and to protect Vtg or its product YPs from premature or inappropriate proteolysis (Wallace et al., 1990; Finn, 2007b). In the most recently evolved group of teleosts (Acanthomorpha), the tripartite Vtg system generally includes two complete Vtg paralogs (VtgAa and VtgAb) bearing all YP domains, and an incomplete Vtg (VtgC) lacking Pv and much of the C-terminus (b0 c/Ct) (reviews: Finn and Kristoffersen, 2007; Reading and Sullivan, 2011). The different forms of Vtg appear to disparately bind to
http://dx.doi.org/10.1016/j.ygcen.2015.01.018 0016-6480/Ó 2015 Published by Elsevier Inc.
Please cite this article in press as: Yilmaz, O., et al. Estrogen-induced yolk precursors in European sea bass, Dicentrarchus labrax: Status and perspectives on
Q1 multiplicity and functioning of vitellogenins. Gen. Comp. Endocrinol. (2015), http://dx.doi.org/10.1016/j.ygcen.2015.01.018
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different forms of Vtg receptor (Vtgr) (reviews: Hiramatsu et al., 2013, this volume) and they and their product YPs undergo different degrees of proteolysis by various cathepsins during oocyte growth and oocyte maturation (OM) (Carnevali et al., 2006). In some marine teleosts spawning pelagic eggs, virtually all YPs derived from VtgAa may be proteolytically cleaved into free amino acids (FAAs) during OM, whereas the major products of VtgAb (LvHAb) and VtgC (LvHC) remain largely intact. The FAAs act as osmotic effectors of oocyte hydration (review: Cerdà et al., 2007) and serve as diffusible nutrients selectively utilized by early embryos, while the large lipoproteins derived from VtgAb and VtgC are utilized later by the larvae (review: Matsubara et al., 1999, 2003). Thus, the multiple Vtg system provides for proper adjustment of egg buoyancy and delivers the appropriate types of nutrients for each stage of early development. The degree to which dysfunction of multiple Vtg systems is involved in poor egg quality, which is widespread in finfish aquaculture (Bromage, 1995) and the subject of intensive investigation (Brooks et al., 1997; Cerdà et al., 2008; Bobe and Labbé, 2010), has not previously been explored. Vitellogenins and vitellogenesis have received some prior study in European sea bass (Dicentrarchus labrax), an acanthomorph teleost spawning pelagic eggs in seawater that is highly prized in marine fisheries and aquaculture (Carrillo et al., 1995; Saillant et al., 2003). However, multiplicity of Vtgs in this species has been heretofore unknown. This review covers prior research on the biochemistry and physiology of vitellogenesis in sea bass relevant to egg quality in farmed fish, and then presents results of recent research on multiplicity of Vtgs in this species, emphasizing observations relevant to the evolution and functioning of the different forms of Vtg.
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2. Vitellogenesis and yolk formation in sea bass
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Sea bass Vtg has been purified using a two-step chromatography process that, based on our present knowledge of the biochemistry of multiple Vtgs in Moronidae (see Hiramatsu et al., 2002c; see also Reading et al., 2011, Supplemental Fig. 1), would have resulted in the loss of VtgC in the pass-through fraction during the second ion-exchange procedure (Mañanós et al., 1994a). The resulting Vtg preparation, likely a mixture of the A-type Vtgs (VtgAa and VtgAb), exhibited an apparent molecular weight in gel filtration and an amino acid composition similar to those reported for complete forms of teleost Vtg from other teleosts. A rabbit antibody raised against the sea bass Vtg was employed in immunocytochemistry to localize the protein in the liver and ovary and in Western blotting to verify induction of vitellogenesis in estrogentreated males, the presence of the Vtgs in the plasma of naturally vitellogenic females, and the existence of corresponding Vtgderived yolk proteins in ovulated egg extracts (Mañanós et al., 1994a). The apparent mass of the sea bass VtgA monomer(s) (180 kDa) in SDS- PAGE is in close agreement with that reported for other members of the family Moronidae, striped bass, Morone saxatilis (A-type Vtg 170 kDa; Tao et al., 1993) and white perch, M. americana (VtgAa and VtgAb 180 kDa; Hiramatsu et al., 2002b), and the induction of vitellogenesis in males by estrogen was confirmed by homologous ELISA to be dose-dependent. The ELISA was later used to describe annual variations in plasma Vtg levels in farmed adults held at natural seasonal temperature and day length in Torre de la Sal, Spain (Mañanós et al., 1994b). The Vtg levels corresponded well to the progression of oocyte growth revealed by histology, with plasma Vtg rising at the onset of vitellogenesis in October, peaking at over 3 mg/ml in December, and dropping thereafter to intermediate values (1.5 mg/ml) that were sustained through May, approximately until the end of the natural spawning season. Strikingly similar profiles of plasma Vtg have
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been reported for other Moronidae family members, including striped bass (Tao et al., 1993; Woods and Sullivan, 1993), white perch (Jackson and Sullivan, 1995), and white bass, Morone chrysops (Berlinsky et al., 1995). Annual plasma Vtg profiles were also assessed in captive females maturing under natural or experimentally altered photothermal cycles (Mañanós et al., 1997b). In all groups, changes in plasma Vtg levels were positively correlated with estradiol-17b (E2) levels, oocyte growth, and spawning time. Profiles of plasma Vtg in control fish were as seen before, with high Vtg levels (1.6–1.9 mg/ml) being sustained during the entire spawning period together with the presence of vitellogenic oocytes, suggesting the existence of several waves of oocyte growth in the ovary and, thus, several spawns per female. In general, the annual Vtg profiles were shifted and compressed in females exposed to experimental day length cycles that advanced or delayed spawning time. The sea bass Vtg ELISA was also employed to evaluate the influence of broodstock ration on plasma Vtg and E2 levels and reproductive performance of females (Cerdà et al., 1994). In adult females fed a natural trash fish (Boops boops) diet at either 1.04% or 0.45% body weight/day for 6 months before spawning, the lower ration was associated with decreased growth rates, condition factor and plasma E2 levels, and a delay in the onset of vitellogenesis and spawning. However, the profiles of plasma Vtg levels were similar between the two groups as were egg quality (% buoyant eggs) and biochemical composition, and also larval hatching rates and survival for 40 days. The influence of dietary lipid composition on plasma levels of Vtg, E2, and GtH II (FSH) and reproductive performance was also investigated (Navas et al., 1998). When fish were fed the natural control diet of trash fish, a commercially available pelleted diet with 10% lipid content, or the commercial diet supplemented to 22% lipid content with refined fish oil enriched with n-3 fatty acids, fish fed the pelleted diets exhibited a greater decrease in plasma Vtg levels during the middle of the spawning period, and this was correlated with a decrease in reproductive performance (egg viability, hatching rate). Collectively, the results of these studies illustrate the reliability of plasma Vtg levels as indicators of the status and progression of oogenesis and the potential gamete quality of sea bass held under various experimental conditions. A more remarkable linkage of vitellogenesis to egg quality was made by Carnevali et al. (2001), who evaluated lysosomal enzyme activities in sea bass eggs and embryos. As in other marine pelagic spawners, floating sea bass eggs have the potential to produce viable embryos whereas sinking eggs do not and, as noted, the acquisition of egg buoyancy is related to the generation of FAAs via proteolysis of Vtg during OM (review Cerdà et al., 2007). It was found that cathepsin D was present at significantly higher levels in sinking sea bass eggs, whereas cathepsin L was more abundant in the floating eggs (Carnevali et al., 2001), and a relationship of cathepsin gene expression or enzyme activity to egg quality was subsequently verified in several studies of a variety of species (review: Carnevali et al., 2006). Vitellogenin receptors (Vtgrs) have been detected in sea bass using the preparation of A-type Vtgs in ‘grind and bind’ studies employing 125I-Vtg as the tracer and solubilized ovarian membrane proteins as the receptor preparation (Mañanós et al., 1997a). Ligand blots revealed a 100 kDa receptor protein that specifically bound Vtg, and filter binding assays indicated that the binding was specific and saturable with a Kd in the mid nM range. Based upon its apparent mass and binding characteristics, the identified Vtgr likely corresponds to the ‘classical’ Vtgr that has been described in striped bass and white perch (Tao et al., 1996; Reading et al., 2011), which preferentially binds the major form of Vtg (VtgAb) to mediate its uptake into growing oocytes (reviews: Hiramatsu et al., 2013, this volume). This Vtgr is also described as the
Please cite this article in press as: Yilmaz, O., et al. Estrogen-induced yolk precursors in European sea bass, Dicentrarchus labrax: Status and perspectives on
Q1 multiplicity and functioning of vitellogenins. Gen. Comp. Endocrinol. (2015), http://dx.doi.org/10.1016/j.ygcen.2015.01.018
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LR8- receptor because it has 8 class-A ligand-binding repeats (LR) at its N-terminus and lacks the distal O-linked sugar domain that is present in the twin Vldlr (LR8+) sequence present in other teleosts, of which the Vtgr is a splice variant. Full-length cDNAs encoding Moronidae LR8- Vtgrs have been obtained for sea bass (Prat, Martínez-Rodríguez, Shaw, Sánchez, Ibáñez, Cerdá-Reverter, Gómez, and Zanuy, unpublished data; Genbank SbsVtgr FR717659.1; Sánchez et al., 2004) and white perch (Hiramatsu et al., 2004). Expression of the sea bass vtgr mRNA in isolated ovarian follicles was shown by RT-qPCR to be highest in previtellogenic stages, decreasing to low levels during vitellogenesis (García-López et al., 2011), a pattern also seen in white perch ovaries (Hiramatsu et al., 2004) that indicates most receptors are synthesized at early stages of oocyte development and stored for later mobilization to support oocyte growth. In addition to these investigations relevant to egg quality in sea bass, the aforementioned ELISA has been utilized to measure Vtg in this species as a biomarker for exposure of the fish to environmental pollutants with estrogenic activity, such as certain alkylphenols (e.g. Fernandes et al., 2008, 2009).
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3. Multiplicity of sea bass vitellogenins
226
Three complete sea bass vtg cDNAs were assembled from contiguous partial sequences obtained by RT-PCR and cloning and the obtained full-length cDNA sequences have been deposited in GenBank (SbsvtgAa, JQ283441; SbsvtgAb, JQ283442; SbsvtgC, JQ341410). The deduced polypeptide products encoded by these cDNAs were classified via alignment of their sequences to those of other teleost Vtgs, which revealed homologies across a broad
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array of taxa and definitively identified them as sea bass VtgAa, VtgAb and VtgC (Yilmaz, 2013). As in other acanthomorph teleosts, the two A-type Vtg paralogs are complete, possessing all Vtgderived yolk protein (YP) domains, and the VtgC lacks a Pv domain and the two C-terminal YP domains (b0 c and Ct). The three forms of Vtg and their derived YPs were detected by label-free quantitative mass spectrometry and quantified in blood plasma and ovary of postvitellogenic females based on normalized counts of tryptic peptide spectra mapped to their parent Vtg polypeptide sequences (Yilmaz et al., 2013). The VtgAb appears to be the dominant form of Vtg in sea bass, being 3-fold more abundant in the plasma than VtgAa and 8-fold more abundant than VtgC. However, all three forms of Vtg make a substantial contribution to the egg yolk, with the postvitellogenic ovarian YPAa:YPAb:YPC ratio being 1.5:3.0:1. Similar disparities between abundance ratios of the Vtgs in plasma and the corresponding YP ratios in oocytes or eggs have been observed in several other teleosts, including striped bass (see Hiramatsu et al., this volume; Table 1), leading researchers to speculate that there may be receptor-based mechanisms for disparate accumulation of the different forms of Vtg by growing oocytes. In the Moronidae species, multiple ovarian membrane proteins with different affinities for VtgAa and VtgAb have been discovered (Reading et al., 2011). In addition to the classical LR8- Vtgr (Hiramatsu et al., 2004), which preferentially binds VtgAb in white perch, there is a novel receptor initially termed ‘‘LR7+1’’ based the unusual structure of its ligand-binding domain(s), which includes 7 N-terminal and one distal LR. This receptor appears to preferentially bind VtgAa in white perch (Reading et al., 2011) and was subsequently classified as a new type of low-density lipoprotein receptor-related protein (Lrp) named Lrp13 (Reading et al., 2014). Interestingly, while the VtgC does not appear to bind to ovarian
Table 1 Oocyte hydration and maturational proteolysis of lipovitellins in Moronidae and some other teleosts whose multiple vitellogenin systems have been investigated. Lv, lipovitellin; LvH, Lv heavy chain; LvL, Lv light chain: VtgAc, Clupea harengus Vtg. Number superscripts indicate references for oocyte and egg diameter values used to calculate oocyte and egg volumes (see footnote). Species SW pelagic Goldsinny wrasse Haddock1 Atlantic halibut1 Barfin flounder2 SW benthi Mummichog3 Atlantic herring4 Moronidae Sea bass5 Striped bass
6
White perch White bass8 1 2 3 4 5 6 7 8 *
7
Egg type
Oocyte volume (mm3)
Egg volume (mm3)
Percent change
Fold change
Lipovitellin (Lv) proteolysis
References for Lv proteolysis
SW pelagic SW pelagic SW pelagic SW pelagic
0.05
0.33
547
6.47X
LvHAa
Kolarevic et al. (2008)
0.23
1.38
500
6.00X
LvHAa LvHAb
Reith et al. (2001)
3.42
15.30
347
4.47X
Finn (2007a)
0.68
2.81
313
4.13X
LvHAa LvHAb, LvLAb LvHAa LvHAb, LvLA
SW demersal SW demersal
1.30
2.90
123
2.23X
LvHAa
La Fleur et al. (2005)
0.54
0.85
57
1.57X
VtgAc1’VtgAc2
Kristoffersen et al. (2009)
SW pelagic FW pelagic FW demersal FW demersal
0.27
0.80
196
2.96X
LvHAa’LvHAb’LvC
This study
0.34
0.76
124
2.24X
LvHAa’LvHAb’LvC
Williams et al. (2014)
*
0.15
0.30
100
2.00X
LvHAa+LvHAb, LvC
0.16
0.35
119
2.19X
LvHAa+LvHAb, LvC*
Matsubara et al. (1999)
Reading et al. (2009) and Hiramatsu et al. (2002a,b) Hiramatsu et al. (2002b) and Reading et al. (2009)
Finn et al. (2000). Matsubara and Koya (1997). Greeley et al. (1991). Kristoffersen and Finn (2008). Mayer et al. (1988). Mylonas et al. (1997). Jackson and Sullivan (1995). Hiramatsu et al. (2002c); see References for Latin binomial species names. Degree of VtgC proteolysis unknown, LvH proteolysis inferred from comparisons of white bass and/or perch with striped bass (see text for details).
Please cite this article in press as: Yilmaz, O., et al. Estrogen-induced yolk precursors in European sea bass, Dicentrarchus labrax: Status and perspectives on
Q1 multiplicity and functioning of vitellogenins. Gen. Comp. Endocrinol. (2015), http://dx.doi.org/10.1016/j.ygcen.2015.01.018
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membrane proteins in white perch and has been speculated to enter oocytes in the fluid phase or via some other means, a least two unidentified receptors bind VtgC in the cutthroat trout, Oncorhynchus clarki (Hiramatsu et al., this volume). We compared the predicted 3-dimensional (3-D) structures, conserved glycine and proline residues, and conserved charged residues of the 85 residue receptor-binding domain (Li et al., 2003) present on the N-sheet of sea bass A- and C-type Vtgs (see Finn, 2007a). Glycine and proline have unique properties that make them particularly important to the secondary structure of proteins (review: Betts and Russell, 2003) and it is thought that binding of ligands to the Ldlr- family lipoprotein receptors is mediated by electrostatic interactions between positively charged residues on the ligand and negatively charged residues (e.g. SDE) present on LRs of the receptor (Huang et al., 2010). Some results of the analysis are shown for sea bass VtgAb and VtgC in Fig. 1. The predicted 3-D structures of the two receptor-binding domains are strikingly different, as is the distribution of positively and negatively charged residues on their surfaces. The structural differences may be due, in part, to massive substitution of glycine and proline residues in sea bass VtgC that are highly conserved among A-type Vtgs, with these substitutions occurring in almost all teleost VtgCs examined (Yilmaz, Prat and Sullivan, unpublished data). Also, in addition to the non-conservative substitution of a glutamine [Q] for the lysine [K181] residue found by Li et al. (2003) to be essential for receptor binding and reported by Reading et al. (2009) to be highly conserved in A-type Vtgs, the cysteines forming one of two disulfide bonds present in the receptor-binding domain of all A-type Vtgs (C204–C207 in sea bass VtgAb) are substituted in sea bass VtgC and in virtually all other teleost VtgCs examined (Fig. 1). These structural changes may explain the inability of Moronidae VtgC to bind to the A-type Vtg receptors. The different types of sea bass Vtg were also compared with regard to the proteolytic fates of their product Lvs during oocyte maturation. Western blotting performed using Vtg-type specific
antisera raised against purified gray mullet (Mugil cephalus) LvAa, LvAb, and LvC (Amano et al., 2008) confirmed the presence of the three Vtgs and their derived Lvs in blood plasma and ovary, respectively, and revealed that all three forms of sea bass LvH are partially degraded during oocyte maturation, as evidenced by the de novo appearance in Western blots of egg extracts of multiple immunoreactive bands with a lower apparent mass than the respective LvH (Yilmaz et al., 2013). Similar findings based on Western blotting using Vtg-type specific antisera raised against white perch Vtgs were recently made for the three forms of LvH in striped bass (Williams et al., 2014; Reading et al., 2009) and can be postulated for white bass based upon the gradual (incomplete) disappearance of the heaviest YP band (110 kDa) seen in SDS–PAGE of oocyte extracts, which contains a mixture of A-type LvHs (Hiramatsu et al., 2002a), with concomitant appearance of lower molecular weight bands as the oocytes matured in vivo or in vitro (Hiramatsu et al., 2002c). However, the broad degradation of all three forms of LvH seen in sea bass is unusual for a highly evolved marine teleost spawning pelagic eggs, in which preferential proteolysis of LvHAa appears to be the norm (Table 1). Moronidae is a monophyletic assemblage of very closely related species (Williams et al., 2012) and the similarity of Vtgs and vitellogenesis among these species, which includes an extraordinary degree of homology among their deduced Vtg polypeptide sequences (Fig. 2), is not entirely surprising. The LvH sequences of striped bass and white perch Vtgs are 95.1–95.8% identical and 97.5–98.1% similar to the corresponding sequences in sea bass; for LvL, these figures are 89.5–96.5% and 94.1–98.0%, respectively, and the b0 c and Ct domains are equally well conserved. Even for the Pvs, which are less conserved among teleosts, the Morone sequences are 68.1–86.2% identical and 68.1–88.8% similar to their counterparts in sea bass. However, when we consider the very different reproductive life histories and egg types among the Moronidae (Table 1), the high homologies and the similar pattern of LvH proteolysis during OM present something of a conundrum.
Fig. 1. Predicted three-dimensional surface distribution of highly conserved charged amino acid residues in the 85 amino acid receptor binding domains of sea bass VtgAa and VtgC. Geno3D (Combet et al., 2002) was used to model the molecular structures using aligned residues from the crystallographically resolved structure of lamprey Lv (Anderson et al., 1998) as the template and the PyMol molecular visualization system (http://www.pymol.org/) was employed for imaging. Conservation of residues was judged from results of an Evolutionary Trace (ET) analysis (Litcharge et al., 1996) obtained by the entering lamprey (I. unicuspis) Lv sequence Protein Data Bank (PDB) identifier 1lsh into the ET Report Maker. Note the substantial differences in predicted surface charge distribution and structure between the receptor-binding sites of the two types of Vtg. Arrows indicate the position of cysteine residues involved in the conserved disulfide bond present in sea bass VtgAb (C204–C207) that are substituted in the VtgC of sea bass and other teleosts. See text for details.
Please cite this article in press as: Yilmaz, O., et al. Estrogen-induced yolk precursors in European sea bass, Dicentrarchus labrax: Status and perspectives on
Q1 multiplicity and functioning of vitellogenins. Gen. Comp. Endocrinol. (2015), http://dx.doi.org/10.1016/j.ygcen.2015.01.018
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Fig. 2. Conservation of vitellogenin (Vtg) polypeptide sequences in the family Moronidae. The domain structure of each form of sea bass (D. labrax) Vtg is shown: (A) VtgAa; (B) VtgAb; (C) VtgC. Beneath each domain, the percent identity of the corresponding sequence in striped bass (M. saxatilis) and white perch (M. americana) is shown in boldface type with the percent similarity indicated below in plain typeface set in parentheses. For each form of Vtg, before calculating the identity and similarity values, the homologous sequences from the three Moronidae species were aligned using ClustalW (Thompson et al., 1994). Sp, signal peptide; LvH, lipovitellin heavy chain; Pv, phosvitin; LvL, lipovitellin light chain; b0 c, b0 -component; Ct, C-terminal component.
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As noted, sea bass spawn pelagic eggs in seawater (SW), while the striped bass is a fresh water (FW) spawner of eggs that are pelagic only in turbulent waters, and the white perch and white bass both spawn demersal eggs in FW. These differences are reflected to only a limited extent by the degree to which the oocytes hydrate and increase in volume during OM (Table 1). The fold increase in volume of maturing sea bass oocytes (3X) falls at the lower end of the range for marine pelagic spawners in which LvHAa is preferentially hydrolyzed during OM, and it is only slightly greater than that of the mummichog (SW demersal), the striped bass (FW pelagic), and the other two Morone species (FW demersal) (Table 1). In the sea bass, while oocyte constituents other than water, notably lipids, may make the major contribution to egg buoyancy, minor adjustments of buoyancy seemingly involve maturational proteolysis of all three forms of LvH (and perhaps other YPs), and these adjustments are probably important, as evidenced by the linkage of cathepsin D and cathepsin L activities to egg buoyancy in this species (Carnevali et al., 2006).
Confirmation of these hypotheses will require further studies in which the maturational proteolysis of YPs is described in more detail and the quantities and profiles of free amino acids in the eggs are measured and mapped to their parent YPs (e.g. Finn, 2007a).
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4. Conclusion
357
In the European sea bass, plasma Vtg levels and profiles are an established indicator of the status and progress of maturation and, in some cases, they and Vtg-processing enzyme (cathepsin) activities may predict the quality of the resulting eggs. The sea bass produces all three forms of Vtg described for acanthomorph teleosts. The VtgAb is the dominant form of Vtg in this species, but all three types of Vtg contribute significantly to the store of YPs deposited in eggs. Observed differences in deposition of A- and C-type Vtgs and the lack of receptor binding by VtgC are likely due to extensive
358
Please cite this article in press as: Yilmaz, O., et al. Estrogen-induced yolk precursors in European sea bass, Dicentrarchus labrax: Status and perspectives on
Q1 multiplicity and functioning of vitellogenins. Gen. Comp. Endocrinol. (2015), http://dx.doi.org/10.1016/j.ygcen.2015.01.018
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modification of the 3-D structure of the receptor-binding domain in VtgC, including the distribution of charged residues across its surface. Although hydration of the oocytes during OM is limited in sea bass compared to other marine fish spawning pelagic eggs, all three types of sea bass LvH undergo noticeable proteolysis during this time and likely contribute to the store of FAAs involved in oocyte hydration and early embryo nutrition. The obtained Vtg sequences and mass spectrometry methods employed in the cited studies set the stage for discovery of the role(s) that the multiple Vtg system plays in determining egg quality in farmed sea bass.
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Acknowledgments
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The research on multiple sea bass Vtgs is, in part, included in the doctoral dissertation of O.Y. at the Faculty of Fisheries, Postgraduate School of Natural and Applied Sciences, Akdeniz University, Antalya, Turkey (Yilmaz, 2013). This research was supported by an Akdeniz University Scientific Research Coordinating Unit Ph.D. research grant (2009.03.0121.008) and a Fulbright Doctoral Research fellowship granted to O.Y., and by awards from the North Carolina Sea Grant Program (award number R/12-SSS-3), the North Carolina Agricultural Foundation, Inc., and Carolina AquaGyn to CVS. These supporters had no role in the design, execution, reporting or decision to publish the research. Some results of this study were reported at the 6th Fish and Shellfish Larviculture Symposium (LARVI 2013), 2–5 September, 2013, Ghent, Belgium, or were presented at the 10th International Symposium on Reproductive Physiology of Fish, Olhão, Portugal, 25–30 May, 2014.
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References
394 395 396 397 398 399 400 401 402 403 404 405 406 407 408 409 410 411 412 413 414 415 416 417 418 419 420 421 422 423 424 425 426 427 428 429 430 431 432 433 434 435 436 437 438
Amano, H., Fujita, T., Hiramatsu, N., Kagawa, H., Matsubara, T., Sullivan, C.V., Hara, A., 2008. Multiple vitellogenin-derived yolk proteins in gray mullet (Mugil cephalus): disparate proteolytic patterns associated with ovarian follicle maturation. Mol. Reprod. Dev. 75, 1307–1317. Anderson, T.A., Levitt, D.G., Banaszak, L.J., 1998. The structural basis of lipid interactions in lipovitellin, a soluble lipoprotein. Structure 6, 895–909. Babin, P.J., Carnevali, O., Lubzens, E., Schneider, W.J., 2007. Molecular aspects of oocyte vitellogenesis in fish. In: Babin, P.J., Cerdà, J., Lubzens, E. (Eds.), The Fish Oocyte: from Basic Studies to Biotechnological Applications. Springer, Netherlands, pp. 39–76, Chapter 2. Berlinsky, D.L., Jackson, L.F., Sullivan, C.V., 1995. The annual reproductive cycle of white bass, Morone chrysops. J. World Aquaculture Soc. 26, 252–260. Betts, M.J., Russell, R.B., 2003. Amino acid properties and consequences of substitutions. In: Barnes, M.R., Gray, I.C. (Eds.), Bioinformatics for Geneticists. John Wiley and Sons Ltd., West Sussex, England, pp. 289–316, Chapter 14. Bobe, J., Labbé, C., 2010. Egg and sperm quality in fish. Gen. Comp. Endocrinol. 165, 535–548. Bromage, N., 1995. Broodstock management and seed quality: general considerations. In: Bromage, N.R., Roberts, R.J. (Eds.), Broodstock Management and Egg and Larval Quality. Blackwell Science, Oxford, UK, pp. 1–24, Chapter 1. Brooks, S., Tyler, C.R., Sumpter, J.P., 1997. Egg quality in fish: what makes a good egg? Rev. Fish Biol. Fish. 7, 387–416. Carnevali, O., Mosconi, G., Cambi, A., Ridolfi, S., Zanuy, S., Polzonetti-Magni, A.M., 2001. Changes of lysosomal enzyme activities in sea bass (Dicentrarchus labrax) eggs and developing embryos. Aquaculture 202, 249–256. Carnevali, O., Cionna, C., Tosti, L., Lubzens, E., Maradonna, F., 2006. Role of cathepsins in ovarian follicle growth and maturation. Gen. Comp. Endocrinol. 146, 195–203. Carrillo, M., Zanuy, S., Prat, F., Cerdá, J., Ramos, J., Mañanós, E., Bromage, N., 1995. Sea bass (Dicentrarchus labrax). In: Bromage, N.R., Roberts, R.J. (Eds.), Broodstock Management and Egg and Larval Quality. Blackwell Science, Oxford, UK, pp. 138–168, Chapter 7. Cerdà, J., Bobe, J., Babin, P.J., Admon, A., Lubzens, E., 2008. Functional genomics and proteomic approaches for the study of gamete formation and viability in farmed finfish. Rev. Fish. Sci. 16, 56–72. Cerdà, J., Carrillo, M., Zanuy, S., Ramos, J., 1994. Effect of food ration on estrogen and vitellogenin plasma levels, fecundity and larval survival in captive sea bass Dicentrarchus labrax: preliminary observations. Aquat. Living Resour. 7, 255– 256. Cerdà, J., Fabra, M., Raldúa, D., 2007. Physiological and molecular basis of fish oocyte hydration. In: Babin, P.J., Cerdà, J., Lubzens, E. (Eds.), The Fish Oocyte: from Basic Studies to Biotechnological Applications. Springer, Dordrecht, The Netherlands, pp. 349–396, Chapter 12. Combet, C., Jambon, M., Deléage, G., Geourjon, C., 2002. Geno3D: automatic comparative molecular modeling of protein. Bioinformatics 18, 213–214.
367 368 369 370 371 372 373 374 375
379 380 381 382 383 384 385 386 387 388 389 390 391
Fernandes, D., Zanuy, S., Bebianno, M.J., Porte, C., 2008. Chemical and biochemical tools to assess pollution exposure in cultured fish. Environ. Pollut. 152, 138– 146. Fernandes, D., Bebianno, M.J., Porte, C., 2009. Assessing pollutant exposure in cultured and wild sea bass (Dicentrarchus labrax) from the Iberian Peninsula. Ecotoxicology 18, 1043–1050. Finn, R.N., Fyhn, H.J., Norberg, B., Munholland, J., Reith, M., 2000. Oocyte hydration as a key feature in the adaptive evolution of teleost fishes to seawater. In: Norberg, B., Kjesbu, O.S., Taranger, G.L., Andersson, E., Stefansson, S.O. (Eds.), Proceedings of the 6th International Symposium on the Reproductive Physiology of Fish. University of Bergen, Bergen, Norway, pp. 289–291. Finn, R.N., 2007a. The maturational disassembly and differential proteolysis of paralogous vitellogenins in a marine pelagophil teleost: a conserved mechanism of oocyte hydration. Biol. Reprod. 76, 936–948. Finn, R.N., 2007b. Vertebrate yolk complexes and the functional implications of phosvitins and other subdomains in vitellogenins. Biol. Reprod. 76, 926–935. Finn, R.N., Kristoffersen, B.A., 2007. Vertebrate vitellogenin gene duplication in relation to the ‘‘3R hypothesis’’: correlation to the pelagic egg and the oceanic radiation of teleosts. PLoS One 2, e169. García-López, A., Sánchez-Amaya, M.I., Prat, F., 2011. Targeted gene expression profiling in European sea bass (Dicentrarchus labrax, L.) follicles from primary growth to late vitellogenesis. Comp. Biochem. Physiol. A 160, 374–380. Greeley, M.S., Hols, H., Wallace, R.A., 1991. Changes in size, hydration and low molecular weight osmotic effectors during meiotic maturation of Fundulus oocytes in vivo. Comp. Biochem. Physiol. 100A, 639–647. Hiramatsu, N., Chapman, R.W., Lindzey, J.K., Haynes, M.R., Sullivan, C.V., 2004. Molecular characterization and expression of vitellogenin receptor from white perch (Morone americana). Biol. Reprod. 70, 720–1730. Hiramatsu, N., Hara, A., Hiramatsu, K., Fukada, H., Weber, G.M., Denslow, N.D., Sullivan, C.V., 2002a. Vitellogenin-derived yolk proteins of white perch, Morone americana: purification, characterization and vitellogenin-receptor binding. Biol. Reprod. 67, 655–667. Hiramatsu, N., Luo, W., Reading, B.J., Sullivan, C.V., Mizuta, H., Ryu, Y.-W., Nishimiya, O., Todo, T., Hara, A., 2013. Ovarian lipoprotein receptors in teleosts. Fish Physiol. Biochem. 39, 29–32. Hiramatsu, N., Matsubara, T., Hara, A., Donato, D.M., Hiramatsu, K., Denslow, N.D., Sullivan, C.V., 2002b. Identification, purification and classification of multiple forms of vitellogenin from white perch (Morone americana). Fish Physiol. Biochem. 26, 355–370. Hiramatsu, N., Matsubara, T., Weber, G.M., Sullivan, C.V., Hara, A., 2002c. Vitellogenesis in aquatic animals. Fish. Sci. 68, 694–699. Hiramatsu, N., Todo, T., Sullivan, C.V., Schilling, J., Reading, B.J., Matsubara, Ryu Y.W., Mizuta, H., Luo, W., Nishimiya, O., Wu, M., Mushirobira, M., Yilmaz, O., Hara, A. Ovarian yolk formation in fishes: molecular mechanisms underlying formation of lipid droplets and vitellogenin-derived yolk proteins (this volume). Huang, S., Henry, L., Ho, H.-K., Pownall, H.J., Rudenko, G., 2010. Mechanism of LDL binding and release probed by structure-based mutagenesis of the LDL receptor. J. Lipid Res. 2010 (51), 297–308. Jackson, L.F., Sullivan, C.V., 1995. Reproduction of white perch (Morone americana): the annual gametogenic cycle. Trans. Am. Fish. Soc. 124, 563–577. Kolarevic, J., Nerland, A., Nilsen, F., Finn, R.N., 2008. Goldsinny wrasse (Ctenolabrus rupestris) is an extreme vtgAa-type pelagophil teleost. Mol. Reprod. Dev. 75, 1011–1020. Kristoffersen, B.A., Finn, R.N., 2008. Major osmolyte changes during oocyte hydration of a clupeocephalan marine benthophil: Atlantic herring (Clupea harengus). Mar. Biol. 154, 683–692. Kristoffersen, B.A., Nerland, A., Nilsen, F., Kolarevic, J., Finn, R.N., 2009. Genomic and proteomic analyses reveal non-neofunctionalized vitellogenins in a basal clupeocephalan, the Atlantic herring, and point to the origin of maturational yolk proteolysis in marine teleosts. Mol. Biol. Evol. 26, 1029–1044. La Fleur Jr., G.J., Raldúa, D., Fabra, M., Carnevali, O., Denslow, N., Wallace, R.A., Cerdà, J., 2005. Derivation of major yolk proteins from parental vitellogenins and alternative processing during oocyte maturation in Fundulus heteroclitus. Biol. Reprod. 73, 815–824. Li, A., Sadasivam, M., Ding, J.L., 2003. Receptor-ligand interaction between vitellogenin receptor (VtgR) and vitellogenin (Vtg), implications on low density lipoprotein receptor and apolipoprotein B/E. J. Biol. Chem. 278, 2799– 2806. Litcharge, O., Bourne, H.R., Cohen, F.E., 1996. An evolutionary trace method defines binding surfaces common to protein families. J. Mol. Biol. 257, 342–358. Mañanós, E.L., Zanuy, S., Le Menn, F., Carrillo, M., Núñez, J., 1994a. Sea bass (Dicentrarchus labrax) vitellogenin. I – Induction, purification, and partial characterization. Comp. Biochem. Physiol. B 107, 205–216. Mañanós, E.L., Núñez, J., Zanuy, S., Carrillo, M., Le Menn, F., 1994b. Sea bass (Dicentrarchus labrax) vitellogenin. II – validation of an enzyme-linked immunosorbent assay (ELISA). Comp. Biochem. Physiol. B 107, pp. 217–213. Mañanós, E.L., Núñez Rodríguez, J., le Menn, F., Zanuy, S., Carillo, M., 1997a. Identification of vitellogenin receptors in the ovary of a teleost fish, the Mediterranean sea bass (Dicentrarchus labrax). Reprod. Nutr. Dev. 37, 51–61. Mañanós, E.L., Zanuy, S., Carrillo, M., 1997b. Photoperiodic manipulations of the reproductive cycle of sea bass (Dicentrarchus labrax) and their effects on gonadal development, and plasma 17ß-estradiol and vitellogenin levels. Fish Physiol. Biochem. 16, 211–222. Matsubara, T., Koya, Y., 1997. Course of proteolytic cleavage in three classes of yolk proteins during oocyte maturation in barfin flounder, Verasper moseri, a marine teleost spawning pelagic eggs. J. Exp. Zool. 278, 189–200.
Please cite this article in press as: Yilmaz, O., et al. Estrogen-induced yolk precursors in European sea bass, Dicentrarchus labrax: Status and perspectives on
Q1 multiplicity and functioning of vitellogenins. Gen. Comp. Endocrinol. (2015), http://dx.doi.org/10.1016/j.ygcen.2015.01.018
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Matsubara, T., Ohkubo, N., Andoh, T., Sullivan, C.V., Hara, A., 1999. Two forms of vitellogenin, yielding two distinct lipovitellins, play different roles during oocyte maturation and early development of barfin flounder, Verasper moseri, a marine teleost spawning pelagic eggs. Dev. Biol. 213, 18–32. Matsubara, T., Nagae, M., Ohkubo, N., Andoh, T., Sawaguchi, S., Hiramatsu, N., Sullivan, C.V., Hara, A., 2003. Multiple vitellogenins and their unique roles in marine teleosts. Fish Physiol. Biochem. 28, 295–299. Mayer, I., Shackley, S.E., Ryland, J.S., 1988. Aspects of the reproductive biology of the bass, Dicentrarchus labrax L. I: an histological and histochemical study of oocyte development. J. Fish Biol. 33, 609–622. Mylonas, C.C., Woolds III, L.C., Zohar, Y., 1997. Cyto-histological examination of post-vitellogenesis and final oocyte maturation in captive-reared striped bass. J. Fish Biol. 50, 34–49. Navas, J.M., Mañanós, E.L., Thrush, M., Ramos, J., Zanuy, S., Carillo, M., Zohar, Y., Bromage, N., 1998. Effect of dietary lipid composition on vitellogenin, 17bestradiol and gonadotropin plasma levels and spawning performance in captive sea bass (Dicentrarchus labrax L.). Aquaculture 165, 65–79. Polzonetti-Magni, A.M., Mosconi, G., Soverchia, L., Kikuyama, S., Carnevali, O., 2004. Multihormonal control of vitellogenesis in lower vertebrates. Int. Rev. Cytol. 239, 1–45. Reading, B.J., Hiramatsu, N., Sawaguchi, S., Matsubara, T., Hara, A., Lively, M.O., Sullivan, C.V., 2009. Conserved and variant molecular and functional features of multiple vitellogenins in white perch (Morone americana) and other teleosts. Mar. Biotechnol. 11, 169–187. Reading, B.J., Hiramatsu, N., Schilling, J., Molloy, K.T., Glassbrook, N., Mizuta, H., Luo, W., Baltzegar, D.A., Williams, V.N., Hara, A., Sullivan, C.V., 2014. Lrp13 is a novel vertebrate lipoprotein receptor that binds vitellogenins in teleost fishes. J. Lipid Res. 55, 2287–2295. Reading, B.J., Hiramatsu, N., Sullivan, C.V., 2011. Disparate binding of three types of vitellogenin to multiple forms of vitellogenin receptor in white perch. Biol. Reprod. 84, 392–399. Reading, B.J., Sullivan, C.V., 2011. Vitellogenesis in fishes. In: Farrell, A.P., Stevens, E.D., , Cech, J.J., Jr., Richards, J.G. (Eds.), Encyclopedia of Fish Physiology: from Genome to Environment. Elsevier, Maryland Heights, Missouri, USA, pp. 635– 646, Chapter 257. Reith, M., Munholland, J., Kelly, J., Finn, R.N., Fyhn, H.J., 2001. Lipovitellins derived from two forms of vitellogenin are differentially processed during oocyte maturation in haddock (Melanogrammus aeglefinus). J. Exp. Zool. 291, 58–67. Romano, M., Rosanova, P., Anteo, C., Limatola, E., 2004. Vertebrate yolk proteins: a review. Mol. Reprod. Dev. 69, 109–116.
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Saillant, E., Fostier, A., Haffray, P., Menu, B., Chatain, B., 2003. Saline preferendum for the European sea bass, Dicentrarchus labrax, larvae and juveniles: effect of salinity on early development and sex determination. J. Exp. Mar. Biol. Ecol. 287, 103–117. Sánchez, E., Ibáñez, A.J., Shaw, M., Martínez-Rodríguez, G., Zanuy, S., Carrillo, M., Prat, F., 2004. The vitellogenin receptor of European sea bass (Dicentrarchus labrax L.): cloning, molecular characterization and developmental expression. Proceedings of the 5th International Symposium on Fish Endocrinology, September 5–9, Castellón, Spain. Abstract No. P88. Tao, Y., Berlinsky, D.L., Sullivan, C.V., 1996. Characterization of a vitellogenin receptor in white perch (Morone americana). Biol. Reprod. 55, 646–656. Tao, Y., Hara, A., Hodson, R.G., Woods III, L.C., Sullivan, C.V., 1993. Purification, characterization and immunoassay of striped bass (Morone saxatilis) vitellogenin. Fish Physiol. Biochem. 12, 31–46. Thompson, J.D., Higgins, D.G., Gibson, T.J., 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680. Wallace, R.A., Hoch, K., Carnevali, O., 1990. Placement of small lipovitellin subunits with in the vitellogenin precursor in Xenopus laevis. J. Mol. Biol. 213, 407–409. Williams, E.P., Peer, A.C., Miller, T.J., Secor, D.H., Place, A.R., 2012. A phylogeny of the temperate seabasses (Moronidae) characterized by a translocation of the mtnd6 gene. J. Fish Biol. 80, 110–130. Williams, V.N., Reading, B.J., Hiramatsu, N., Amano, H., Glassbrook, N., Hara, A., Sullivan, C.V., 2014. Multiple vitellogenins and product yolk proteins in striped bass, Morone saxatilis: molecular characterization and processing during oocyte growth and maturation. Fish Physiol. Biochem. 40, 395–415. Woods III, L.C., Sullivan, C.V., 1993. Reproduction of striped bass (Morone saxatilis) broodstock: monitoring maturation and hormonal induction of spawning. J. Aquacult. Fish. Manage. 24, 213–224. Yilmaz, O., 2013. Characterization of vitellogenin genes in European sea bass (Dicentrarchus labrax) (Ph.D. dissertation). Akdeniz University, Postgraduate School of Natural and Applied Sciences. Antalya, Turkey. 136 p. Yilmaz, O., Prat, F., Ibáñez, A., Amano, H., Koksoy, S., Sullivan, C.V., 2013. Multiple vitellogenin yolk precursors in European sea bass (Dicentrarchus labrax): molecular cloning, biochemical characterization, quantification in plasma, oocytes and eggs, and potential significance to acquisition of egg buoyancy and to embryonic and larval nutrition. In: C.I. Hendry (Ed.), Proceedings of the 6th Fish and Shellfish Larviculture Symposium (LARVI 2013), 2–5 September, 2013, Ghent, Belgium. European Aquaculture Society, Special Publication No. 505-508, Oostende, Belgium, 2013.
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Q1 multiplicity and functioning of vitellogenins. Gen. Comp. Endocrinol. (2015), http://dx.doi.org/10.1016/j.ygcen.2015.01.018
