Cell Calcium 56 (2014) 467–471
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Organellar mechanosensitive channels involved in hypo-osmoregulation in fission yeast Yoshitaka Nakayama a , Hidetoshi Iida b,∗ a b
Victor Chang Cardiac Research Institute, Darlinghurst, New South Wales 2010, Australia Department of Biology, Tokyo Gakugei University, 4-1-1 Nukui Kita-machi, Koganei-shi, Tokyo 184-8501, Japan
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Article history: Received 1 July 2014 Received in revised form 1 October 2014 Accepted 4 October 2014 Available online 4 November 2014 Keywords: MscS-like protein Mechanosensitive channel Endoplasmic reticulum Osmotic response Ca2+ signal Fission yeast
a b s t r a c t MscS and MscL, bacterial mechanosensitive channels, play crucial roles in the hypo-osmotic shock response. However, only MscS has homologs in eukaryotes. These homologs are called MscS-like proteins or MSL proteins. MSL proteins have changed both structurally and functionally during evolution and are now localized not only to the membrane of the chloroplast, which is thought to be a descendant of an ancient, free-living bacterium, but also the cell membrane and the endoplasmic reticulum (ER) membrane, suggesting that the role of MSL proteins has diverged. In this brief review, we mainly focus on two MSL proteins in the fission yeast Schizosaccharomyces pombe that are localized in the ER membrane and protect cells from hypo-osmotic shock-induced death by regulating intracellular Ca2+ concentrations. We also discuss Arabidopsis thaliana MSL proteins and other yeast ion channels in terms of osmoregulation in eukaryotes. © 2014 Elsevier Ltd. All rights reserved.
1. Introduction In the natural environment, rainfall must be a danger for yeasts because, for example, in yeasts growing in damaged grapes with a high glucose concentration, it causes a rapid drop in osmotic pressure. Water levels consequently increase due to the influx of water into yeast cells, which subsequently expand, thereby increasing cell volume and turgor pressure. Yeasts must have evolved mechanisms to sense hypo-osmotic shock and avoid cell rupture. In the model yeast Saccharomyces cerevisiae, hypo-osmotic shock has been shown to induce the release of Ca2+ from intracellular stores and then the influx of Ca2+ from the external medium to cause transient increases in the concentration of cytoplasmic Ca2+ , [Ca2+ ]cyt , within seconds [1], which activates the protein kinase C (Pkc1)-mediated cell wall integrity MAP kinase pathway within minutes [2], and stimulates the efflux of intracellular glycerol through the Fps1 glycerol transporter [3]. Although S. cerevisiae cells have a homolog of transient receptor potential (TRP) channels, TRPY1 or Yvc1, in their vacuolar membranes, it only responds to hyper-osmotic shock, not hypo-osmotic shock, to raise [Ca2+ ]cyt [4]. Thus, although the mechanism underlying the hypo-osmotic
∗ Corresponding author. Tel.: +81 42 329 7517; fax: +81 42 329 7517. E-mail address: [email protected] (H. Iida). http://dx.doi.org/10.1016/j.ceca.2014.10.001 0143-4160/© 2014 Elsevier Ltd. All rights reserved.
shock response in S. cerevisiae has been elucidated in detail, how hypo-osmotic shock is sensed by ion channels remains unknown. On the other hand, the mechanism responsible for sensing hypo-osmotic shock by ion channels has been clarified in bacterial and mammalian cells. Bacteria have two main mechanosensitive channels in their cell membranes: mechanosensitive channels of small conductance (MscS) and large conductance (MscL), which are involved in osmoregulation by releasing intracellular osmolytes, such as ions and small organic compounds (see below). MscS and MscL are of great interest as sensing mechanisms because both directly sense membrane stretching caused by turgor pressure and release intracellular osmolytes [5–7]. In other words, MscS and MscL do not appear to require intracellular regulatory mechanisms to open. Mammalian cells have developed distinct mechanisms; they swell when challenged with hypo-osmotic shock, which induces an increase in [Ca2+ ]cyt , and this is followed by the active recovery of cell volume, called regulatory volume decrease (RVD), thereby enabling cells to avoid cell rupture [8]. RVD requires the loss of ions, such as K+ and Cl− , and water. Recent studies reported that the increase in [Ca2+ ]cyt was mediated by some members of the TRP channel family, including plasma membrane-localized TRPV4 [9] and TRPM7 [10]. Mammalian TRP channels may be regulated by cellular components, including the actin cytoskeleton, integrins, and receptor tyrosine kinases, which differs from the regulation of bacterial MscS and MscL [11].
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Fig. 1. Structure and membrane topology of MscS, Msy1 and Msy2. (A) Ribbon diagram of MscS based on the crystal structure, PDB 2OAU. (B) Electrostatic surface view of MscS generated by Pymol software. Hydrophobicity is shown in red. The positions of four out of seven side portals and one axial portal are shown schematically. (C) Membrane topology of MscS (top) and predicted membrane topology of Msy1 (middle) and Msy2 (bottom). White rods represent transmembrane helices, while gray rods show pore-forming helices. Black rods represent a predicted EF-hand motif, coiled-coil domain (DUF2040) and Geminivirus C4 family domain. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Another group of ion channels that may be involved in osmoregulation is the eukaryotic MscS-like (MSL) protein family. MSL proteins resemble bacterial MscS in their transmembrane segment and vicinity [12,13]. Proteins similar to MscL have not been detected in eukaryotes. A notable feature of MSL proteins is that they are present in eukaryotes with a cell wall, such as plants, fungi, and protists. From an evolutionary perspective, MSL genes are considered to have been produced by the incorporation of the mscS gene into the genome of the ancestor of these eukaryotes. MSL proteins are of great interest from the viewpoint of function because some of these proteins are localized in organellar membranes, such as chloroplast membranes, in plants, while bacterial MscS is localized in the cell membrane. In addition, fungal MSL proteins are also attracting attention because fungi have no chloroplasts. This diversity in subcellular localization should reflect functional diversity. In this context, we examined the MSL proteins of Schizosaccharomyces pombe, another model yeast. We herein provide a brief overview of our recent advances in the study of S. pombe MSL proteins in consideration of bacterial MscS and plant MSL proteins.
2. Bacterial MscS as a model channel of eukaryotic MSL proteins As described above, MscS and MscL directly sense membrane tension upon hypo-osmotic shock and open to reduce turgor pressure by releasing intracellular osmolytes. Therefore, both mechanosensitive channels act as ‘osmotic safety valves’ to avoid cell rupture. Escherichia coli possesses one MscL and six MscS
paralogs: archetypal MscS (yggB), potassium-dependent MscK (KefA), MscM (YjeP), YbdG, YbiO, and YnaI [14]. X-ray crystallography revealed that the crystal structure of archetypal MscS (PDB: 2OAU – EcMscS, PDB) had a homoheptamer consisting of subunits with three transmembrane domains and a large cytoplasmic domain, termed the “vestibule” [15]. MscS is known to be slightly anion-selective, the TM3 helix forms a hydrophobic channel pore, and the vestibule contains seven side portals and an axial portal formed by a hydrophobic -barrel for the passage of ions (Fig. 1A and B). The vestibule functions as an ion-selective filter. Negatively charged residues proximal to the seven side portals trap cations such as K+ and Ca2+ and generate “ion clouds” by electrostatic interactions to facilitate the passage of anions through MscS [16,17]. Archetypal MscS, in addition to its role as an osmotic safety valve, acts as a conduit for the entry of Ca2+ into E. coli cells, and bacterial mechanosensitive channels function to produce Ca2+ transients in the osmotic response [17]. The expression of mechanosensitive channels in E. coli is regulated by the stress sigma factor RpoS in a manner that is dependent on osmotic pressure [18]. These findings suggest that Ca2+ has important physiological roles in osmotic responses in bacteria. Since MSL proteins are found exclusively in cell-walled organisms, we speculated that these channels might have evolved from a common ancestor of these organisms for osmoregulation. MSL proteins have been grouped into two classes based on sequence similarities in the conserved domain of the MscS family [19,20]: Classes I and II. Class I MSL proteins contain predicted targeting sequences to mitochondria or chloroplasts. On the other hand, Class II MSL proteins do not have a targeting sequence and are found in
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organisms lacking chloroplasts. MSL proteins are also structurally diverse and have been classified into 15 subfamilies [21]. A number of MSL proteins have extra domain structures in the N- and C-termini over archetypal MscS, suggesting that these structures regulate channel activation and/or inactivation. This also highlights the functional diversity of MSL proteins.
3. Fungal MSL proteins A bioinformatics approach in fungal genomes revealed that many, but not all, ascomycetes and basidiomycetes have MSL proteins that belong to Class II. For example, the fission yeast S. pombe has MSL proteins, while the budding yeast S. cerevisiae does not. The structural features of fungal MSL proteins include the presence of one EF-hand Ca2+ -binding motif upstream of a channel pore helix and several N-terminal transmembrane segments (Fig. 1C). Therefore, these homologs are grouped into the EF-MSL family [21], suggesting that cytoplasmic Ca2+ regulates their channel activities. S. pombe has two EF-MSLs, Msy1 and Msy2, and these channels control cytoplasmic Ca2+ levels and cell volume in response to hypo-osmotic shock [13]. The msy1− msy2− mutant cannot survive upon hypo-osmotic shock. Interestingly, this cell death is not caused by cell rupture, suggesting that some impairment is brought about by hypo-osmotic shock in the cells. Single-cell Ca2+ imaging with Yellow Cameleon shows that cell swelling is followed by a cytoplasmic Ca2+ increase upon hypo-osmotic shock and the msy1− msy2− mutant exhibits an abnormally large cytoplasmic Ca2+ increase. Moreover, the cell death of the msy1− msy2− mutant is enhanced by the influx of extracellular calcium. Hypo-osmoticshocked msy1− msy2− cells have two abnormally enlarged vacuoles and cracks between the outer and inner nuclear membranes [22]. These observations suggest that irregular Ca2+ increase induced by cell swelling causes the cell death. The overexpression of either wild-type Msy1 or Msy2 protein can complement this death phenotype, indicative of functional redundancy between Msy1 and Msy2. However, the overexpression of Msy1 with a mutation in the EF hand motif did not complement the msy1− msy2− mutation, while that of the mutant Msy2 did completely, suggesting that this EF-hand motif is necessary for the function of Msy1, and also that the EF-hand motif regulates Msy1 and Msy2 differently. Although the EF-hand motif seems to be important for channel function, it remains to be elucidated electrophysiologically whether the EF-MSLs are Ca2+ -selective for permeation and Ca2+ -sensitive for gating. Other structural features are that Msy1 and Msy2 have a larger C-terminal domain than archetypal MscS, and that Msy1 possesses a predicted coiled-coil domain (DUF2040) that is conserved from fungi to humans and a predicted Geminivirus C4 family domain, which consists of the N-terminal region of Geminivirus C4 proteins necessary for efficient spreading of the virus in tomato plants [23]. The function of the C-terminal region of the fungal MSL channel currently remains unknown. In contrast to bacterial MscS and its paralogs, which are localized in the cell membrane, Msy1 and Msy2 are localized in the perinuclear and cortical ER membranes, respectively, although these channels do not appear to have a signal sequence [13]. Hypoosmotic shock is suggested to activate primarily a Ca2+ channel in organellar membranes to trigger an immediate [Ca2+ ]cyt increase in S. cerevisiae cells [1], and this mechanism also seems to apply to S. pombe cells [13]. Notably, the hypo-osmotic shock-induced [Ca2+ ]cyt increase is much higher in msy1− cells than in wildtype cells and lower in msy2− cells than in wild-type cells. This suggests that Msy1 is involved in the sequestration of cytoplasmic Ca2+ into the perinuclear ER and Msy2 is involved in Ca2+ release from the cortical ER after hypo-osmotic stimulation (Fig. 2).
Fig. 2. Distinct subcellular localization and physiological roles of Msy1 and Msy2. When cells of fission yeast are exposed to hypo-osmotic shock, Msy2 localized in the cortical ER membrane participates in the release of Ca2+ from the ER lumen, while Msy1 localized in the periplasmic ER membrane takes part in the sequestration of cytosolic Ca2+ to the ER lumen [13].
Electrophysiological characterization with E. coli spheroplasts suggests that Msy1 displays mechanosensitive channel activity with a conductance of 300 pS. This finding supports Msy1 being activated by tension in perinuclear ER membranes under hypo-osmotic shock. A number of fungi contain highly conserved EF-MSL proteins, which suggests that these channels are physiologically important. Neurospora crassa has two EF-MSL proteins (NCU09595 and NCU04207). The NCU09595-deletion mutant has significantly more depolarized resting potential than the wild type because of the passive distribution of ions across the plasma membrane [24]. The regulation of increased cytoplasmic Ca2+ concentrations is essential for maintaining viability. The subcellular localization of EF-MSL proteins in N. crassa has yet to be explored; nevertheless, EF-MSL proteins appear to be critically involved in Ca2+ homeostasis. 4. Algal and plant MSL proteins Algae and plants have both Class I and Class II MSL proteins in their genomes. Arabidopsis has 10 MSL genes (MSL1-10); MSL13 have been classified into Class I and MSL4-10 into Class II, and these channels have been detected in chloroplast and cell membranes, respectively. Two Class I MSL proteins, MSL2 and MSL3, were previously shown to be involved in the division of chloroplasts and protected chloroplasts from hypo-osmotic stress under normal growth conditions [25]. These channels were localized at the poles of chloroplasts and were found to control the placement of the division ring, FtsZ [26]. On the other hand, two Class II MSL proteins, MSL9 and MSL10, have been detected in the plasma membranes of roots [27]. Chlamydomonas has three MSL proteins, one of which, MSC1, is a Class II MSL that is a strongly anion-selective mechanosensitive channel present in the chloroplast membrane and is involved in chlorophyll localization [28]. The presence of MSL proteins in chloroplasts indicates that an evolutionary endosymbiotic event occurred. The regulation of osmolyte concentration is important to maintain the turgor of cells; therefore, turgor pressure in the cytoplasm and organelles must be regulated in the osmotic shock response. MSL2 and MSL3 serve as osmotic release valves in plastids to mediate the flux of osmolytes from the plastid stroma in response to an increase in membrane tension upon hypo-osmotic shock. Therefore, the msl2 msl3 mutant responds constitutively to hypo-osmotic stress even under normal growth conditions and has abnormally high stromal solutes in the cytoplasm, such as proline, which is induced by the stress hormone abscisic acid [29]. These findings suggest the existence of a signal cascade triggered by an osmotic imbalance between the plastid and cytoplasm. Although plants, algae, and fungi share similar signal transduction mechanisms as cell-walled organisms in general, osmoregulation through MSL channels seems to differ among them. Algal and plant MSL channels
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Table 1 Ion channels and subunits involved in stress responses in fission yeast. Channel/subunit
Localization
Physiological function
Ref.
Msy1 Msy2 Pkd2
Perinuclear ER Cortical ER Golgi and Intracellular membranes? plasma Plasma mem- membrane? Plasma brane membrane Plasma membrane
Ca2+ and osmotic regulation Ca2+ and osmotic regulation Cell shape regulation Cell wall synthesis Ca2+ regulation n.d. Ca2+ influx Ca2+ influx
[13] [13] [35]
TRP1322 TRP663 Cch1 Yam8
[36] [36] [36] [36]
n.d., not determined.
mainly allow the passage of chloride ions. Unlike fungal MSL channels, they have no Ca2+ -binding motif. This may provide an insight into the different mechanisms underlying organellar osmoregulation between the ER and plastids.
5. Ion channels apart from MSL proteins that are involved in the hypo-osmotic response Although the hypo-osmotic shock response is important for cell survival under stressful conditions in both S. pombe and S. cerevisiae, a limited number of studies have been conducted on this issue [1–3,30–32]. Thus, little is known about the channels or transporters involved in this response besides S. pombe Msy1 and Msy2 (Table 1). Kung and colleagues electrophysiologically detected mechanosensitive channels that were activated by pressure on the plasma membranes of S. cerevisiae [33] and S. pombe [34] more than 20 years ago using patch-clamp techniques. However, the molecular identities of these channels have not yet been revealed. As described above, the S. cerevisiae TRP channel homolog TRPY1 (or Yvc1) is present in the vacuolar membrane and activated to release Ca2+ from the vacuole following hyper-osmotic, but not hypo-osmotic, shock [4]. S. pombe has three TRP channel homologs: Pkd2, which is the most similar to the polycystickidney-disease-related ion channel, as well as Trp1322 and Trp663 [35,36]. Pkd2 is predominantly localized in the Golgi membrane and also in the plasma membrane, being a key signaling component in the regulation of cell shape and cell wall synthesis [35]. Although the channel activity of Pkd2 has not yet been shown, it is conceivable that it senses mechanical stresses caused by cellular events accompanying changes in cell shape. Pkd2 and Trp1322 were previously reported to be involved in an increase in [Ca2+ ]cyt following the exposure of cells to high concentrations of CaCl2 (up to 100 mM) and 200 mM NaCl plus FK506 (a calcineurin inhibitor that potentially activates the cell membrane Ca2+ influx channel Cch1) [36]. It currently remains unclear whether these high concentrations of ions act as an ionic or high-osmolality stress. Fission yeast has a Ca2+ channel in the plasma membrane that is composed of Cch1 and Yam 8, which are homologs of animal voltage-gated Ca2+ channel (VGCC) ␣1 and ␣2 /␦ subunits, respectively [36]. It remains unknown whether this channel can sense a change in osmolality. S. cerevisiae has an ortholog of Yam8, Mid1 [37,38]. This protein is localized in both plasma and ER membranes and exhibits stretch-activated channel activity when expressed in mammalian cells, possibly because it activates an intrinsic VGCC ␣1 subunit [39]. Further studies are needed to clarify the involvement of the Ca2+ channel composed of Cch1 and Yam8 or Cch1 and Mid1 subunits in hypo-osmotic and hyper-osmotic shock responses. It would be interesting to investigate possible functional coordination between the Msy1/Msy2 channels and the Cch1/Yam8 channels.
6. Conclusion The study of fission yeasts Msy1 and Msy2 has provided novel insight into the molecular mechanisms underlying the hypoosmotic shock response. Since both channels are localized in the ER membrane, it has become clear that hypo-osmotic shock can be sensed in organelle membranes, even in cells that are protected by a cell wall. A previous study demonstrated that Msy1 and Msy2 were localized in the perinuclear and cortical ER membranes, respectively [13], which clearly suggests that these two mechanosensitive channels take part in osmoregulation. Because of the ease of molecular genetic analysis for fission yeast, the msy1− msy2− mutant could serve as a tool for investigating the roles of the MSL channels of other organisms in osmoregulation at the molecular level. Conflicts of interests The authors declare no conflicts of interest. Acknowledgements We thank Ms. Yumiko Higashi for her secretarial assistance. This work was supported by Grants-in-Aid for Scientific Research on Priority Area No. 21026009 (to H.I.), No. 23120509 (to H.I.) and No. 25120708 (to H.I.) from the Ministry of Education, Culture, Sports, Science and Technology of Japan, a Grants-in-Aid for Scientific Research B No. 21370017 (to H.I.) and No. 26291026 (to H.I.) from the Japan Society for the Promotion of Science (JSPS), and a Grant-in-Aid for JSPS Fellows No. 10J02008 (to Y.N.) and JSPS Postdoctoral Fellowships for Research Abroad (to Y.N.). References [1] A.F. Batiza, T. Schulz, P.H. Masson, Yeast respond to hypotonic shock with a calcium pulse, J. Biol. Chem. 271 (1996) 23357–23362. [2] J.J. Heinisch, A. Lorberg, H.P. Schmitz, J.J. Jacoby, The protein kinase C-mediated MAP kinase pathway involved in the maintenance of cellular integrity in Saccharomyces cerevisiae, Mol. Microbiol. 32 (1999) 671–680. [3] D. Ahmadpour, C. Geijer, M.J. Tamás, K. Lindkvist-Petersson., Yeast reveals unexpected roles and regulatory features of aquaporins and aquaglyceroporins, Biochim. Biophys. Acta 1840 (2014) 1482–1491. [4] V. Denis, M.S. Cyert, Internal Ca2+ release in yeast is triggered by hypertonic shock and mediated by a TRP channel homologue, J. Cell Biol. 156 (2002) 29–34. [5] K. Okada, P.C. Moe, P. Blount, Functional design of bacterial mechanosensitive channels. Comparison and contrasts illuminated by random mutagenesis, J. Biol. Chem. 277 (2002) 27682–27688. [6] S. Sukharev, Purification of the small mechanosensitive channel of Escherichia coli (MscS): the subunit structure, conduction, and gating characteristics in liposomes, Biophys. J. 83 (2002) 290–298. [7] S.I. Sukharev, P. Blount, B. Martinac, F.R. Blattner, C. Kung, A large conductance mechanosensitive channel in E. coli encoded by mscL alone, Nature 368 (1994) 265–268. [8] Y. Okada, E. Maeno, T. Shimizu, K. Dezaki, J. Wang, S. Morishima, Receptormediated control of regulatory volume decrease (RVD) and apoptotic volume decrease (AVD), J. Physiol. 532 (2001) 3–16. [9] D. Becker, C. Blasé, J. Bereiter-Hahn, M. Jendrach, TRPV4 exhibits a functional role in cell-volume regulation, J. Cell Sci. 118 (2005) 2435–2440.
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Cell Calcium journal homepage: www.elsevier.com/locate/ceca
Organellar mechanosensitive channels involved in hypo-osmoregulation in fission yeast Yoshitaka Nakayama a , Hidetoshi Iida b,∗ a b
Victor Chang Cardiac Research Institute, Darlinghurst, New South Wales 2010, Australia Department of Biology, Tokyo Gakugei University, 4-1-1 Nukui Kita-machi, Koganei-shi, Tokyo 184-8501, Japan
a r t i c l e
i n f o
Article history: Received 1 July 2014 Received in revised form 1 October 2014 Accepted 4 October 2014 Available online 4 November 2014 Keywords: MscS-like protein Mechanosensitive channel Endoplasmic reticulum Osmotic response Ca2+ signal Fission yeast
a b s t r a c t MscS and MscL, bacterial mechanosensitive channels, play crucial roles in the hypo-osmotic shock response. However, only MscS has homologs in eukaryotes. These homologs are called MscS-like proteins or MSL proteins. MSL proteins have changed both structurally and functionally during evolution and are now localized not only to the membrane of the chloroplast, which is thought to be a descendant of an ancient, free-living bacterium, but also the cell membrane and the endoplasmic reticulum (ER) membrane, suggesting that the role of MSL proteins has diverged. In this brief review, we mainly focus on two MSL proteins in the fission yeast Schizosaccharomyces pombe that are localized in the ER membrane and protect cells from hypo-osmotic shock-induced death by regulating intracellular Ca2+ concentrations. We also discuss Arabidopsis thaliana MSL proteins and other yeast ion channels in terms of osmoregulation in eukaryotes. © 2014 Elsevier Ltd. All rights reserved.
1. Introduction In the natural environment, rainfall must be a danger for yeasts because, for example, in yeasts growing in damaged grapes with a high glucose concentration, it causes a rapid drop in osmotic pressure. Water levels consequently increase due to the influx of water into yeast cells, which subsequently expand, thereby increasing cell volume and turgor pressure. Yeasts must have evolved mechanisms to sense hypo-osmotic shock and avoid cell rupture. In the model yeast Saccharomyces cerevisiae, hypo-osmotic shock has been shown to induce the release of Ca2+ from intracellular stores and then the influx of Ca2+ from the external medium to cause transient increases in the concentration of cytoplasmic Ca2+ , [Ca2+ ]cyt , within seconds [1], which activates the protein kinase C (Pkc1)-mediated cell wall integrity MAP kinase pathway within minutes [2], and stimulates the efflux of intracellular glycerol through the Fps1 glycerol transporter [3]. Although S. cerevisiae cells have a homolog of transient receptor potential (TRP) channels, TRPY1 or Yvc1, in their vacuolar membranes, it only responds to hyper-osmotic shock, not hypo-osmotic shock, to raise [Ca2+ ]cyt [4]. Thus, although the mechanism underlying the hypo-osmotic
∗ Corresponding author. Tel.: +81 42 329 7517; fax: +81 42 329 7517. E-mail address: [email protected] (H. Iida). http://dx.doi.org/10.1016/j.ceca.2014.10.001 0143-4160/© 2014 Elsevier Ltd. All rights reserved.
shock response in S. cerevisiae has been elucidated in detail, how hypo-osmotic shock is sensed by ion channels remains unknown. On the other hand, the mechanism responsible for sensing hypo-osmotic shock by ion channels has been clarified in bacterial and mammalian cells. Bacteria have two main mechanosensitive channels in their cell membranes: mechanosensitive channels of small conductance (MscS) and large conductance (MscL), which are involved in osmoregulation by releasing intracellular osmolytes, such as ions and small organic compounds (see below). MscS and MscL are of great interest as sensing mechanisms because both directly sense membrane stretching caused by turgor pressure and release intracellular osmolytes [5–7]. In other words, MscS and MscL do not appear to require intracellular regulatory mechanisms to open. Mammalian cells have developed distinct mechanisms; they swell when challenged with hypo-osmotic shock, which induces an increase in [Ca2+ ]cyt , and this is followed by the active recovery of cell volume, called regulatory volume decrease (RVD), thereby enabling cells to avoid cell rupture [8]. RVD requires the loss of ions, such as K+ and Cl− , and water. Recent studies reported that the increase in [Ca2+ ]cyt was mediated by some members of the TRP channel family, including plasma membrane-localized TRPV4 [9] and TRPM7 [10]. Mammalian TRP channels may be regulated by cellular components, including the actin cytoskeleton, integrins, and receptor tyrosine kinases, which differs from the regulation of bacterial MscS and MscL [11].
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Fig. 1. Structure and membrane topology of MscS, Msy1 and Msy2. (A) Ribbon diagram of MscS based on the crystal structure, PDB 2OAU. (B) Electrostatic surface view of MscS generated by Pymol software. Hydrophobicity is shown in red. The positions of four out of seven side portals and one axial portal are shown schematically. (C) Membrane topology of MscS (top) and predicted membrane topology of Msy1 (middle) and Msy2 (bottom). White rods represent transmembrane helices, while gray rods show pore-forming helices. Black rods represent a predicted EF-hand motif, coiled-coil domain (DUF2040) and Geminivirus C4 family domain. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Another group of ion channels that may be involved in osmoregulation is the eukaryotic MscS-like (MSL) protein family. MSL proteins resemble bacterial MscS in their transmembrane segment and vicinity [12,13]. Proteins similar to MscL have not been detected in eukaryotes. A notable feature of MSL proteins is that they are present in eukaryotes with a cell wall, such as plants, fungi, and protists. From an evolutionary perspective, MSL genes are considered to have been produced by the incorporation of the mscS gene into the genome of the ancestor of these eukaryotes. MSL proteins are of great interest from the viewpoint of function because some of these proteins are localized in organellar membranes, such as chloroplast membranes, in plants, while bacterial MscS is localized in the cell membrane. In addition, fungal MSL proteins are also attracting attention because fungi have no chloroplasts. This diversity in subcellular localization should reflect functional diversity. In this context, we examined the MSL proteins of Schizosaccharomyces pombe, another model yeast. We herein provide a brief overview of our recent advances in the study of S. pombe MSL proteins in consideration of bacterial MscS and plant MSL proteins.
2. Bacterial MscS as a model channel of eukaryotic MSL proteins As described above, MscS and MscL directly sense membrane tension upon hypo-osmotic shock and open to reduce turgor pressure by releasing intracellular osmolytes. Therefore, both mechanosensitive channels act as ‘osmotic safety valves’ to avoid cell rupture. Escherichia coli possesses one MscL and six MscS
paralogs: archetypal MscS (yggB), potassium-dependent MscK (KefA), MscM (YjeP), YbdG, YbiO, and YnaI [14]. X-ray crystallography revealed that the crystal structure of archetypal MscS (PDB: 2OAU – EcMscS, PDB) had a homoheptamer consisting of subunits with three transmembrane domains and a large cytoplasmic domain, termed the “vestibule” [15]. MscS is known to be slightly anion-selective, the TM3 helix forms a hydrophobic channel pore, and the vestibule contains seven side portals and an axial portal formed by a hydrophobic -barrel for the passage of ions (Fig. 1A and B). The vestibule functions as an ion-selective filter. Negatively charged residues proximal to the seven side portals trap cations such as K+ and Ca2+ and generate “ion clouds” by electrostatic interactions to facilitate the passage of anions through MscS [16,17]. Archetypal MscS, in addition to its role as an osmotic safety valve, acts as a conduit for the entry of Ca2+ into E. coli cells, and bacterial mechanosensitive channels function to produce Ca2+ transients in the osmotic response [17]. The expression of mechanosensitive channels in E. coli is regulated by the stress sigma factor RpoS in a manner that is dependent on osmotic pressure [18]. These findings suggest that Ca2+ has important physiological roles in osmotic responses in bacteria. Since MSL proteins are found exclusively in cell-walled organisms, we speculated that these channels might have evolved from a common ancestor of these organisms for osmoregulation. MSL proteins have been grouped into two classes based on sequence similarities in the conserved domain of the MscS family [19,20]: Classes I and II. Class I MSL proteins contain predicted targeting sequences to mitochondria or chloroplasts. On the other hand, Class II MSL proteins do not have a targeting sequence and are found in
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organisms lacking chloroplasts. MSL proteins are also structurally diverse and have been classified into 15 subfamilies [21]. A number of MSL proteins have extra domain structures in the N- and C-termini over archetypal MscS, suggesting that these structures regulate channel activation and/or inactivation. This also highlights the functional diversity of MSL proteins.
3. Fungal MSL proteins A bioinformatics approach in fungal genomes revealed that many, but not all, ascomycetes and basidiomycetes have MSL proteins that belong to Class II. For example, the fission yeast S. pombe has MSL proteins, while the budding yeast S. cerevisiae does not. The structural features of fungal MSL proteins include the presence of one EF-hand Ca2+ -binding motif upstream of a channel pore helix and several N-terminal transmembrane segments (Fig. 1C). Therefore, these homologs are grouped into the EF-MSL family [21], suggesting that cytoplasmic Ca2+ regulates their channel activities. S. pombe has two EF-MSLs, Msy1 and Msy2, and these channels control cytoplasmic Ca2+ levels and cell volume in response to hypo-osmotic shock [13]. The msy1− msy2− mutant cannot survive upon hypo-osmotic shock. Interestingly, this cell death is not caused by cell rupture, suggesting that some impairment is brought about by hypo-osmotic shock in the cells. Single-cell Ca2+ imaging with Yellow Cameleon shows that cell swelling is followed by a cytoplasmic Ca2+ increase upon hypo-osmotic shock and the msy1− msy2− mutant exhibits an abnormally large cytoplasmic Ca2+ increase. Moreover, the cell death of the msy1− msy2− mutant is enhanced by the influx of extracellular calcium. Hypo-osmoticshocked msy1− msy2− cells have two abnormally enlarged vacuoles and cracks between the outer and inner nuclear membranes [22]. These observations suggest that irregular Ca2+ increase induced by cell swelling causes the cell death. The overexpression of either wild-type Msy1 or Msy2 protein can complement this death phenotype, indicative of functional redundancy between Msy1 and Msy2. However, the overexpression of Msy1 with a mutation in the EF hand motif did not complement the msy1− msy2− mutation, while that of the mutant Msy2 did completely, suggesting that this EF-hand motif is necessary for the function of Msy1, and also that the EF-hand motif regulates Msy1 and Msy2 differently. Although the EF-hand motif seems to be important for channel function, it remains to be elucidated electrophysiologically whether the EF-MSLs are Ca2+ -selective for permeation and Ca2+ -sensitive for gating. Other structural features are that Msy1 and Msy2 have a larger C-terminal domain than archetypal MscS, and that Msy1 possesses a predicted coiled-coil domain (DUF2040) that is conserved from fungi to humans and a predicted Geminivirus C4 family domain, which consists of the N-terminal region of Geminivirus C4 proteins necessary for efficient spreading of the virus in tomato plants [23]. The function of the C-terminal region of the fungal MSL channel currently remains unknown. In contrast to bacterial MscS and its paralogs, which are localized in the cell membrane, Msy1 and Msy2 are localized in the perinuclear and cortical ER membranes, respectively, although these channels do not appear to have a signal sequence [13]. Hypoosmotic shock is suggested to activate primarily a Ca2+ channel in organellar membranes to trigger an immediate [Ca2+ ]cyt increase in S. cerevisiae cells [1], and this mechanism also seems to apply to S. pombe cells [13]. Notably, the hypo-osmotic shock-induced [Ca2+ ]cyt increase is much higher in msy1− cells than in wildtype cells and lower in msy2− cells than in wild-type cells. This suggests that Msy1 is involved in the sequestration of cytoplasmic Ca2+ into the perinuclear ER and Msy2 is involved in Ca2+ release from the cortical ER after hypo-osmotic stimulation (Fig. 2).
Fig. 2. Distinct subcellular localization and physiological roles of Msy1 and Msy2. When cells of fission yeast are exposed to hypo-osmotic shock, Msy2 localized in the cortical ER membrane participates in the release of Ca2+ from the ER lumen, while Msy1 localized in the periplasmic ER membrane takes part in the sequestration of cytosolic Ca2+ to the ER lumen [13].
Electrophysiological characterization with E. coli spheroplasts suggests that Msy1 displays mechanosensitive channel activity with a conductance of 300 pS. This finding supports Msy1 being activated by tension in perinuclear ER membranes under hypo-osmotic shock. A number of fungi contain highly conserved EF-MSL proteins, which suggests that these channels are physiologically important. Neurospora crassa has two EF-MSL proteins (NCU09595 and NCU04207). The NCU09595-deletion mutant has significantly more depolarized resting potential than the wild type because of the passive distribution of ions across the plasma membrane [24]. The regulation of increased cytoplasmic Ca2+ concentrations is essential for maintaining viability. The subcellular localization of EF-MSL proteins in N. crassa has yet to be explored; nevertheless, EF-MSL proteins appear to be critically involved in Ca2+ homeostasis. 4. Algal and plant MSL proteins Algae and plants have both Class I and Class II MSL proteins in their genomes. Arabidopsis has 10 MSL genes (MSL1-10); MSL13 have been classified into Class I and MSL4-10 into Class II, and these channels have been detected in chloroplast and cell membranes, respectively. Two Class I MSL proteins, MSL2 and MSL3, were previously shown to be involved in the division of chloroplasts and protected chloroplasts from hypo-osmotic stress under normal growth conditions [25]. These channels were localized at the poles of chloroplasts and were found to control the placement of the division ring, FtsZ [26]. On the other hand, two Class II MSL proteins, MSL9 and MSL10, have been detected in the plasma membranes of roots [27]. Chlamydomonas has three MSL proteins, one of which, MSC1, is a Class II MSL that is a strongly anion-selective mechanosensitive channel present in the chloroplast membrane and is involved in chlorophyll localization [28]. The presence of MSL proteins in chloroplasts indicates that an evolutionary endosymbiotic event occurred. The regulation of osmolyte concentration is important to maintain the turgor of cells; therefore, turgor pressure in the cytoplasm and organelles must be regulated in the osmotic shock response. MSL2 and MSL3 serve as osmotic release valves in plastids to mediate the flux of osmolytes from the plastid stroma in response to an increase in membrane tension upon hypo-osmotic shock. Therefore, the msl2 msl3 mutant responds constitutively to hypo-osmotic stress even under normal growth conditions and has abnormally high stromal solutes in the cytoplasm, such as proline, which is induced by the stress hormone abscisic acid [29]. These findings suggest the existence of a signal cascade triggered by an osmotic imbalance between the plastid and cytoplasm. Although plants, algae, and fungi share similar signal transduction mechanisms as cell-walled organisms in general, osmoregulation through MSL channels seems to differ among them. Algal and plant MSL channels
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Table 1 Ion channels and subunits involved in stress responses in fission yeast. Channel/subunit
Localization
Physiological function
Ref.
Msy1 Msy2 Pkd2
Perinuclear ER Cortical ER Golgi and Intracellular membranes? plasma Plasma mem- membrane? Plasma brane membrane Plasma membrane
Ca2+ and osmotic regulation Ca2+ and osmotic regulation Cell shape regulation Cell wall synthesis Ca2+ regulation n.d. Ca2+ influx Ca2+ influx
[13] [13] [35]
TRP1322 TRP663 Cch1 Yam8
[36] [36] [36] [36]
n.d., not determined.
mainly allow the passage of chloride ions. Unlike fungal MSL channels, they have no Ca2+ -binding motif. This may provide an insight into the different mechanisms underlying organellar osmoregulation between the ER and plastids.
5. Ion channels apart from MSL proteins that are involved in the hypo-osmotic response Although the hypo-osmotic shock response is important for cell survival under stressful conditions in both S. pombe and S. cerevisiae, a limited number of studies have been conducted on this issue [1–3,30–32]. Thus, little is known about the channels or transporters involved in this response besides S. pombe Msy1 and Msy2 (Table 1). Kung and colleagues electrophysiologically detected mechanosensitive channels that were activated by pressure on the plasma membranes of S. cerevisiae [33] and S. pombe [34] more than 20 years ago using patch-clamp techniques. However, the molecular identities of these channels have not yet been revealed. As described above, the S. cerevisiae TRP channel homolog TRPY1 (or Yvc1) is present in the vacuolar membrane and activated to release Ca2+ from the vacuole following hyper-osmotic, but not hypo-osmotic, shock [4]. S. pombe has three TRP channel homologs: Pkd2, which is the most similar to the polycystickidney-disease-related ion channel, as well as Trp1322 and Trp663 [35,36]. Pkd2 is predominantly localized in the Golgi membrane and also in the plasma membrane, being a key signaling component in the regulation of cell shape and cell wall synthesis [35]. Although the channel activity of Pkd2 has not yet been shown, it is conceivable that it senses mechanical stresses caused by cellular events accompanying changes in cell shape. Pkd2 and Trp1322 were previously reported to be involved in an increase in [Ca2+ ]cyt following the exposure of cells to high concentrations of CaCl2 (up to 100 mM) and 200 mM NaCl plus FK506 (a calcineurin inhibitor that potentially activates the cell membrane Ca2+ influx channel Cch1) [36]. It currently remains unclear whether these high concentrations of ions act as an ionic or high-osmolality stress. Fission yeast has a Ca2+ channel in the plasma membrane that is composed of Cch1 and Yam 8, which are homologs of animal voltage-gated Ca2+ channel (VGCC) ␣1 and ␣2 /␦ subunits, respectively [36]. It remains unknown whether this channel can sense a change in osmolality. S. cerevisiae has an ortholog of Yam8, Mid1 [37,38]. This protein is localized in both plasma and ER membranes and exhibits stretch-activated channel activity when expressed in mammalian cells, possibly because it activates an intrinsic VGCC ␣1 subunit [39]. Further studies are needed to clarify the involvement of the Ca2+ channel composed of Cch1 and Yam8 or Cch1 and Mid1 subunits in hypo-osmotic and hyper-osmotic shock responses. It would be interesting to investigate possible functional coordination between the Msy1/Msy2 channels and the Cch1/Yam8 channels.
6. Conclusion The study of fission yeasts Msy1 and Msy2 has provided novel insight into the molecular mechanisms underlying the hypoosmotic shock response. Since both channels are localized in the ER membrane, it has become clear that hypo-osmotic shock can be sensed in organelle membranes, even in cells that are protected by a cell wall. A previous study demonstrated that Msy1 and Msy2 were localized in the perinuclear and cortical ER membranes, respectively [13], which clearly suggests that these two mechanosensitive channels take part in osmoregulation. Because of the ease of molecular genetic analysis for fission yeast, the msy1− msy2− mutant could serve as a tool for investigating the roles of the MSL channels of other organisms in osmoregulation at the molecular level. Conflicts of interests The authors declare no conflicts of interest. Acknowledgements We thank Ms. Yumiko Higashi for her secretarial assistance. This work was supported by Grants-in-Aid for Scientific Research on Priority Area No. 21026009 (to H.I.), No. 23120509 (to H.I.) and No. 25120708 (to H.I.) from the Ministry of Education, Culture, Sports, Science and Technology of Japan, a Grants-in-Aid for Scientific Research B No. 21370017 (to H.I.) and No. 26291026 (to H.I.) from the Japan Society for the Promotion of Science (JSPS), and a Grant-in-Aid for JSPS Fellows No. 10J02008 (to Y.N.) and JSPS Postdoctoral Fellowships for Research Abroad (to Y.N.). References [1] A.F. Batiza, T. Schulz, P.H. Masson, Yeast respond to hypotonic shock with a calcium pulse, J. Biol. Chem. 271 (1996) 23357–23362. [2] J.J. Heinisch, A. Lorberg, H.P. Schmitz, J.J. Jacoby, The protein kinase C-mediated MAP kinase pathway involved in the maintenance of cellular integrity in Saccharomyces cerevisiae, Mol. Microbiol. 32 (1999) 671–680. [3] D. Ahmadpour, C. Geijer, M.J. Tamás, K. Lindkvist-Petersson., Yeast reveals unexpected roles and regulatory features of aquaporins and aquaglyceroporins, Biochim. Biophys. Acta 1840 (2014) 1482–1491. [4] V. Denis, M.S. Cyert, Internal Ca2+ release in yeast is triggered by hypertonic shock and mediated by a TRP channel homologue, J. Cell Biol. 156 (2002) 29–34. [5] K. Okada, P.C. Moe, P. Blount, Functional design of bacterial mechanosensitive channels. Comparison and contrasts illuminated by random mutagenesis, J. Biol. Chem. 277 (2002) 27682–27688. [6] S. Sukharev, Purification of the small mechanosensitive channel of Escherichia coli (MscS): the subunit structure, conduction, and gating characteristics in liposomes, Biophys. J. 83 (2002) 290–298. [7] S.I. Sukharev, P. Blount, B. Martinac, F.R. Blattner, C. Kung, A large conductance mechanosensitive channel in E. coli encoded by mscL alone, Nature 368 (1994) 265–268. [8] Y. Okada, E. Maeno, T. Shimizu, K. Dezaki, J. Wang, S. Morishima, Receptormediated control of regulatory volume decrease (RVD) and apoptotic volume decrease (AVD), J. Physiol. 532 (2001) 3–16. [9] D. Becker, C. Blasé, J. Bereiter-Hahn, M. Jendrach, TRPV4 exhibits a functional role in cell-volume regulation, J. Cell Sci. 118 (2005) 2435–2440.
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