Meat Science 109 (2015) 48–55

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Role of extracellular matrix in development of skeletal muscle and postmortem aging of meat Takanori Nishimura ⁎ Muscle Biology and Meat Science Laboratory, Research Faculty of Agriculture, Hokkaido University, Sapporo, Japan

a r t i c l e

i n f o

Article history: Received 15 February 2015 Received in revised form 15 May 2015 Accepted 16 May 2015 Available online 20 May 2015 Keywords: Extracellular matrix Intramuscular connective tissue Skeletal muscle Myogenesis Meat Postmortem aging

a b s t r a c t The integrity of skeletal muscle is maintained by the intramuscular connective tissues (IMCTs) that are composed of extracellular matrix (ECM) molecules such as collagens, proteoglycans, and glycoproteins. The ECM plays an important role not only in providing biomechanical strength of the IMCT, but also in regulating muscle cell behavior. Some ECM molecules, such as decorin and laminin, modulate the activity of myostatin that regulates skeletal muscle mass. Furthermore, it has been shown that decorin activates Akt downstream of insulin-like growth factor-I receptor (IGF-IR) and enhances the differentiation of myogenic cells, suggesting that decorin acts as a signaling molecule to myogenic cells. With animal growth, the structural integrity of IMCT increases; collagen fibrils within the endomysium associate more closely with each other, and the collagen fibers in the perimysium become increasingly thick and their wavy pattern grows more regular. These changes increase the mechanical strength of IMCT, contributing to the toughening of meat. However, in highly marbled beef cattle like Wagyu, intramuscular fat deposits mainly in the perimysium between muscle fiber bundles during the fattening period. The development of adipose tissues appears to disorganize the structure of IMCT and contributes to the tenderness of Wagyu beef. The IMCT was considered to be rather immutable compared to myofibrils during postmortem aging of meat. However, several studies have shown that collagen networks in the IMCT are disintegrated and proteoglycan components are degraded during postmortem aging. These changes in ECM appear to reduce the mechanical strength of IMCT and contribute to the tenderness of uncooked meat or cooked meat at low temperature. Thus, the ECM plays a multifunctional role in skeletal muscle development and postmortem aging of meat. © 2015 Elsevier Ltd. All rights reserved.

1. Introduction From a consumer standpoint, texture is the most important factor in determining the quality of meat (Dransfield et al., 1984). Meat texture depends on the structure and composition of skeletal muscle, which is mainly composed of muscle fibers and surrounding intramuscular connective tissues (IMCTs). Muscle fibers consist of myofibrils, which are composed of numerous proteins including actin and myosin that are major proteins of thin and thick filaments respectively. The integrity of skeletal muscle is maintained by three layers of IMCT: 1) the endomysium, which encloses individual muscle fibers; 2) the perimysium, which bundles groups of muscle fibers; and 3) the epimysium, which ensheathes the whole muscle. The IMCT is composed of extracellular matrix (ECM) macromolecules such as collagens, proteoglycans (PGs), and glycoproteins. These ECM macromolecules interact with each other and form a supermolecular network that can both withstand

⁎ Muscle Biology and Meat Science Laboratory, Research Faculty of Agriculture, Hokkaido University, Kita, Sapporo 060-8589, Japan. E-mail address: [email protected].

http://dx.doi.org/10.1016/j.meatsci.2015.05.015 0309-1740/© 2015 Elsevier Ltd. All rights reserved.

and transmit the contractile forces generated by muscle fibers (Fig. 1, Voermans et al., 2008). Skeletal muscle contains collagen types I, III, IV, V, VI, XII, and XIV (Listrat, Picard & Geay, 1999; Listrat et al., 2000; Nishimura, Ojima, Hattori & Takahashi, 1997). The major types of collagen in skeletal muscle are type I and III (Bailey & Light, 1989), which align into a quarterstagger array to form fibrils in tissues. Proteoglycan is composed of a central core protein with covalently attached glycosaminoglycan (GAG) chains. The GAG is a polymer of disaccharide repeats that are highly sulfated and negatively charged. Typical GAGs attached to the core protein of PGs are chondroitin sulfate (CS), dermatan sulfate (DS), and heparan sulfate (HS). In skeletal muscle, there are several types of PGs with various sizes of core protein and kinds of GAG chain (Brandan, Fuentes & Andrade, 1992; Nishimura, Hattori & Takahashi, 1996b; Parthasarathy, Chandrasekaran & Tanzer, 1991). Decorin is one of the most studied members of the small leucine-rich proteoglycan (SLRP) family (Kresse & Schönherr, 2001). The decorin molecule is composed of a core-protein to which a CS/DS chain and small number oligosaccharides are covalently attached. Decorin associates with fibrillar collagen, types I, II, and III collagens (Scott, 1988; Vogel & Trotter, 1987), and has been identified in various tissues

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Fig. 1. Schematic representation of the ECM surrounding skeletal muscle. Individual molecules are depicted at their approximate location in relation to the sarcolemma. Well-established molecular interactions between individual ECM molecules are portrayed. From Voermans et al. (2008).

including skeletal muscle (Eggen, Malmstrom & Kolset, 1994; Lennon, Carrino, Baber & Caplan, 1991; Parthasarathy et al., 1991). Danielson et al. (1997) demonstrated that targeted disruption of decorin in mice leads to abnormal collagen fibril morphology and skin fragility, suggesting that decorin plays an important role in collagen fibril formation and organization of fibril networks. Decorin also participates in cell growth by modulating some growth factors (Li, McFarland & Velleman, 2008; Riquelme et al., 2001; Yamaguchi, Mann & Ruoslahti, 1990) and by signaling directly to cells (Schönherr, Sunderkotter, Iozzo & Schaefer, 2005; Suzuki, Kishioka, Wakamatsu & Nishimura, 2013). This article aims to provide a review of roles of ECM in muscle cell growth and the organization of IMCT during skeletal muscle development, and also changes of ECM during the postmortem aging of meat. 2. Role of ECM in myogenesis The ECM supports cells and provides tissues with mechanical strength and elastic properties. In addition to the maintenance of tissue structure, ECM has also been recognized as an important regulator of cell growth, either through modulation of growth factor activities or through direct involvement in cell signaling. Kanematsu et al. (2004) have shown that type I collagen interacts with basic Fibroblast Growth Factor (bFGF) and that collagen matrix can control the release of bFGF, resulting in regulation of its activity. Furthermore, collagen has been reported to serve as a ligand via the discoidin domain receptor (Hou, Vogel & Bendeck, 2001; Shrivastava et al., 1997; Vogel, Gish, Alves & Pawson, 1997). These studies suggest that collagen plays an important role not only in providing shape and biomechanical strength to organs and tissues, but also in regulating cell behavior. In fact, the inhibition of collagen synthesis suppresses the differentiation of myoblasts in vitro, suggesting that collagen is necessary for myogenesis (Nandan, Clarke, Ball & Sanwal, 1990; Saitoh, Periasamy, Kan & Matsuda, 1992). Proteoglycans have been similarly recognized not only as an organizer of ECM but also a modulator of growth factor activities (Kresse & Schönherr, 2001). Perlecan, a HSPG, which is an intrinsic constituent

of basement membranes, participates in the activation of tyrosine kinase receptors by bFGF, a strong inhibitor of myogenic differentiation (Larraín, Alvarez, Hassell & Brandan, 1997). The membraneassociated HSPGs, glypican-1 and syndecan-4, are expressed in myogenic satellite cells (Powell, McFarland, Cowieson, Muir & Velleman, 2014) and affect the expression of myogenic regulatory factors, MyoD, myogenin, and MRF4 (Harthan, McFarland & Velleman, 2013). Syndecan-4 and glypican-1 regulate muscle cell proliferation and differentiation by modulating cellular responsiveness to fibroblast growth factor 2 (FGF2) (Velleman, 2012). Decorin is a small leucine-rich PG containing a single covalently attached CS or DS to the core protein. The induced expression of decorin in Chinese hamster ovary cells leads to an inhibition of cell proliferation (Yamaguchi & Ruoslahti, 1988), which might result from inhibition of transforming growth factor-β1 (TGF-β1) activity (Yamaguchi et al., 1990). Decorin binds to TGF-β through its coreprotein (Schönherr, Broszat, Brandan, Bruckner & Kresse, 1998) and sequesters TGF-β by trapping it in the ECM (Markmann, Hausser, Schönherr & Kresse, 2000). TGF-β1 is a strong inhibitor of both the proliferation and differentiation of myogenic cells. Li et al. (2008) showed that over-expression of decorin in skeletal muscle satellite cells significantly increases cell proliferation by decreasing sensitivity to TGF-β1 signaling. However, Riquelme et al. (2001) showed that decorin prevents the terminal differentiation of C2C12 muscle cells by increasing sensitivity to TGF-β1 signaling. Decorin stimulates TGF-β-dependent signaling via lipoprotein-receptor related protein (LRP-1) in non-differentiated myoblasts, but inhibits signaling by sequestering TGF-β in differentiated myotubes that express low levels of LRP-1 (Cabello-Verrugio & Brandan, 2007; Droguett, Cabello-Verrugio, Riquelme & Brandan, 2006). These results suggest that decorin has differential effects on TGF-β-dependent signaling at the early and late stages in differentiation. Thus, decorin plays important roles in myogenic cell growth by regulating cellular responsiveness to TGF-β1. Several growth factors including HGF, IGF, FGF, and the TGF-β superfamily are involved in controlling the proliferation and differentiation of

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myoblasts, and thus contribute to the regulation of muscle mass. Myostatin was discovered as a new TGF-β superfamily member that negatively regulates skeletal muscle mass (McPherron, Lawler & Lee, 1997). Transgenic mice carrying a null mutation in the myostatin gene exhibit a dramatic increase in muscle mass secondary to a combination of muscle cell hyperplasia and hypertrophy (McPherron et al., 1997). Additionally, natural mutations of the myostatin gene are responsible for the double-muscled phenotype of some cattle breeds such as the Belgian Blue and Piedmontese (Kambadur, Sharma, Smith & Bass, 1997; McPherron & Lee, 1997). Myostatin is the most effective growth factor in the negative control of skeletal mass and is very important for meat production in domestic animals. Most of the mechanisms by which myostatin controls these myogenic events have been elucidated (Thomas et al., 2000). However, the regulation of myostatin activity after its secretion in the ECM remains unclear. Miura et al. (2006) and Miura, Kishioka, Wakamatsu, Hattori and Nishimura (2010) investigated the interaction between myostatin and some ECM molecules by surface plasmon resonance assay, and showed that decorin, fibromodulin, laminin, and fibronectin interacted with myostatin, but biglycan and keratocan did not. Immobilized decorin in the collagen matrix sequesters myostatin within the ECM, preventing it from inhibiting myoblast proliferation (Miura et al., 2006). Furthermore, Kishioka et al. (2008) demonstrated that decorin enhances the differentiation of myoblasts by suppressing myostatin activity. Immunohistochemical analysis demonstrated that myostatin was located in the muscle fibers, and that decorin was located in the periphery of muscle fibers in fetal rat skeletal muscle (Nishimura, Oyama, Kishioka, Wakamatsu & Hattori, 2007). Albrecht et al. (2011) showed that myostatin is located in close proximity to decorin in intermyocellular space. These results suggest possible interactions between myostatin and decorin in the ECM between muscle fibers. Albrecht et al. (2011) also showed that decorin protein level is lower in semitendinosus muscle than in longissimus muscle, although myostatin level is roughly equal in two muscles. Semitendinosus muscle has more fast fibers, less slow fibers, and less intramuscular fat than longissimus muscle. The decorin expression level may affect the biological activity of myostatin in different types of muscle and contribute to the determination of muscle composition. Furthermore, Yasaka et al. (2013) showed that laminin has potential to regulate myostatin activity by binding to myostatin and/or its receptor ActRIIB. These results suggest that the ECM plays an important role in skeletal muscle development through regulation of growth factor activity. Other functions of decorin have also been identified. In A431 squamous carcinoma cells, decorin binds to, and activates, the epidermal growth factor receptor (EGFR) (Iozzo, Moscatello, McQuillan & Eichstetter, 1999; Patel, Santra, McQuillan, Iozzo & Thomas, 1998), leading to the activation of the MAPK signaling pathway (Moscatello et al., 1998). In addition, decorin can disrupt TGF-β/Smad-signaling in human mesangial cells through an intracellular cross-talk mechanism by mobilizing Ca2+ and activating Ca2+/calmodulin-dependent protein kinases (Abdel-Wahab, Wicks, Mason & Chantry, 2002). Furthermore, decorin interacts with IGF-IR and induces Akt phosphorylation and p21 expression in endothelial cells (Schönherr et al., 2005). These results suggest that decorin acts as a signaling molecule in some cell types. However there were no reports that decorin acts directly on myogenic cells as a signaling molecule. Thus, our group investigated the effect of decorin on the differentiation of myoblasts and signaling via IGFIR in myogenic cells. Suzuki et al. (2013) showed that IGF-IR is expressed in myoblasts and myotubes, and that Akt, which is downstream of IGF-IR, is more phosphorylated in myoblasts cultured in media containing decorin than in those cultured without decorin. These results demonstrate that decorin activates Akt downstream of IGF-IR and enhances the differentiation of myogenic cells. This suggests that decorin acts on myogenic cells as a signaling molecule. Thus, ECM is not only a scaffold for muscle cells (fibers) but also a regulator of muscle cell growth (Fig. 2).

3. Structure and organization of IMCT 3.1. Structural changes in IMCT during animal development The thermal and mechanical stability of IMCT increases with animal growth (Bailey & Light, 1989; McCormick, 1994; Nishimura, Ojima, Liu, Hattori & Takahashi, 1996) and is related to the chemical nature of the covalent intermolecular crosslinks of collagen (Lepetit, 2007; Nishiumi, Kunishima, Nishimura & Yoshida, 1995; Tanzer, 1973). Most crosslinks are in the unstable Schiff base form and are labile to acids and heat in connective tissues of young animals (Bailey & Shimokomaki, 1971; Shimokomaki, Elsden & Bailey, 1972). The reducible crosslinks are transformed into more stable non-reducible compounds with animal aging (Bailey & Shimokomaki, 1971; Robins, Shimokomaki & Bailey, 1973). This brings about a decrease in collagen solubility (Dikeman, Tuma & Beecher, 1971), contributing to the toughness of meat from aged animals. The mechanical stability of IMCT depends not only on intermolecular crosslinks of collagen but also on the size and arrangement of collagen fibrils (Rowe, 1981). Nishimura et al. (1996) showed that collagen fibrils in the endomysium bound more closely with each other, collagen fibers in the perimysium increased in thickness, and the wavy pattern of collagen fibers became more regular during development of bovine skeletal muscle. These structural changes in the IMCT seem to be closely related to an increase in the mechanical strength of the IMCT during development of bovine skeletal muscle. Passerieux et al. (2006) showed that each perimysial collagen fiber formed a plexus in close proximity to muscle surface and attached adjacent myofibers at the level of specific domains that they call the perimysium junction plate (PJP). The PJP and associated intracellular subdomains may participate in the lateral transmission of contractile forces as well as mechanosensing. These structures can be defined as contact region between the endomysium and the perimysium. The mechanical strength of the endomysial–perimysial junctions is low compared to that of the perimysium (Lewis & Purslow, 1990). This might be due to a relative fragile structure of PIP compared to the regular network of collagen fibers in the perimysium. Thus, the three-dimensional architecture of IMCT must be an important factor in the rigidity of skeletal muscle and the determination of meat texture. When and how is the IMCT constructed during the early stage of skeletal muscle development? Nishimura, Futami, Taneichi, Mori, and Hattori (2002) investigated the structural changes in the IMCT during bovine fetal growth and found that the relatively integrated structure of the perimysium had already been formed at 2.5 months of fetal growth, when muscle fibers were loosely assembled and the surrounding endomysium was discontinuous and not well organized. The formation of perimysium during early muscle development might be needed to retain the space in which muscle fibers can increase in number and size, and assemble to form a muscle fiber bundle. On the other hand, the sheath structure of connective tissue, which is characteristic of the endomysium in adult animals, was not observed until 6 months of fetal development. In skeletal muscle after 7.5 months of fetal growth, the endomysium consisted of cylindrical sheaths displaying a honeycomb structure, and the perimysium consisted of thick layers of collagen fibers. These structures are essentially the same as those in adult animals (Nishimura, Hattori & Takahashi, 1994). Because neonatal calves need to stand and walk immediately after birth, the IMCTs must already have sufficient strength to support skeletal muscle and to transmit the forces generated by contraction to the bone. Types I, III, V, and VI collagens are already expressed in the endomysium and perimysium of 7-month fetuses and their localization remains unchanged throughout the prenatal and postnatal growth of cattle (Nishimura et al., 1997). It seems likely that these types of collagen are essential for forming and maintaining the structure of the endomysium and the perimysium. Listrat et al. (1999) showed that

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Fig. 2. Role of extracellular matrix in skeletal muscle. The extracellular matrix supports muscle fibers and provides skeletal muscle with mechanical strength. In addition to maintenance of muscular tissue structure, the extracellular matrix plays an important role in regulation of muscle cell growth either through modulation of growth factors activities or through direct involvement in cell signaling.

types I, III, IV, V, and VI are present in the perimysium and types I, IV, V, and VI are present in the IMCT from 110 days of fetal development in several bovine muscles. Types XII and XIV collagens are collocated in the perimysium, which are fibril-associated collagen with interrupted triple helix (FACIT) linking devices between fibrillar collagen and other ECM components (Listrat et al., 2000). Types XII and XIV collagens may also participate in morphogenesis of IMCT, especially the perimysium. Decorin interacts with fibrillar collagen such as types I and III collagens (Scott, 1988; Vogel, Paulsson & Heinegard, 1984; Vogel & Trotter,

1987) and participates in the stabilization of collagen fibrils (Scott & Thomlinson, 1998). Danielson et al. (1997) have shown that decorin regulates collagen fibril formation in connective tissues. Nishimura et al. (2002) found that decorin is already expressed in the perimysium by 2.5 months of bovine fetal development, when collagen fibrils assemble to form perimysial sheets. Taken together, it is likely that decorin plays an important role in morphogenesis of the IMCT during bovine skeletal muscle development. Decorin expression in chick skeletal muscle increases from day 14 to day 19 of embryonic growth, and

Fig. 3. Effect of intramuscular fat deposition on the structure of intramuscular connective tissue during fattening of Wagyu. During the growing period, the structural integrity of the intramuscular connective tissue increases, contributing to the toughening of beef. The intramuscular fat deposits mainly between muscle fiber bundles during the fattening period, resulting in the disorganization of the perimysium. This causes the remodeling of extracellular matrix and reduces the mechanical strength of intramuscular connective tissue, contributing to the tenderization of beef. Adapted from Nishimura (2010).

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decreases thereafter (Velleman & Coy, 1997). Decrease in the decorin expression level prior to hatching are necessary for collagen elongation ant tissue maturation during chick tendon development (Brick, Nurminskaya & Zycband, 1995). In the muscle of chicken with a genetic disorder decorin expression level is higher than that in normal muscle just before hatching, which might cause a change in collagen fibril organization (Velleman, 1999). There is no significant decrease in decorin mRNA levels in skeletal muscle during the late stage of bovine fetal development (Nishimura et al., 2002). The difference of decorin expression pattern between chicken and bovine muscle during embryonic growth may reflect the degree of muscle development before birth between fowls and mammals. 3.2. Effect of intramuscular fat deposition on IMCT structure and meat tenderness Marbling (intramuscular fat) is one of the most important factors in determining meat quality, especially with respect to texture and flavor. Most of the earlier studies have demonstrated small positive relationships between the degree of marbling and sensory tenderness, and a small inverse relationship with the shear force value of cooked beef (Pearson, 1966; Smith, Berry, Savel & Cross, 1988). The degree of marbling accounts for only 3 to 10% of the variation in sensory tenderness of beef (Campion, Crouse & Dikeman, 1975; Crouse, Smith & Mandigo, 1978; Tatum et al., 1980). On the other hand, May, Dolezal, Gill, Ray, and Buchanan (1992) have shown that the marbling score is moderately related to sensory panel tenderness and shear force in Angus × Hereford steers, which are known for a relatively high ability to marble. Japanese Black cattle are characterized by the ability to deposit very large amounts of intramuscular fat (Zembayashi, 1994; Gotoh et al., 2009; Albrecht et al., 2011; Albrecht et al., 2011). Nishimura, Hattori, and Takahashi (1999) have shown that the shear force value of the longissimus muscle in Japanese Black steers decreases after 20 months of age, concomitant with a rapid increase in crude fat content, and there is a high and inverse correlation coefficient between the crude fat content and shear force value of raw longissimus muscle in Japanese Black cattle after 20 months of age. A greater level of marbling is most likely closely related to meat tenderness. Why is highly marbled beef extremely tender? Little is known about the fine structure of the IMCT in highly marbled beef, or about the structural changes that occur in IMCT during the development of intramuscular adipose tissues induced by fattening. Nishimura et al. (1999) have demonstrated structural changes in the IMCT during fattening of Japanese Black steers using the cell maceration method for scanning electron microscopy. During the early fattening period, from 9 to 20 months of age, collagen fibrils within the endomysium in the longissimus muscle associate more closely with each other, and the collagen fibers in the perimysium become increasingly thick and their wavy pattern grows more regular. These changes are closely related to the increased mechanical strength of the IMCT, resulting in toughening of the beef during this period. The shear force value of the longissimus muscle decreases after 20 months of age, concomitant with a rapid increase in the crude fat content. Scanning electron micrographs of the longissimus muscle dissected from 32-month-old steers clearly showed that the adipose tissues formed between the muscle fiber bundles, the honeycomb structure of the endomysium was partially broken, and the perimysium separated into thinner collagen fibers. By contrast, in the semitendinosus muscle, which has a comparatively lower crude fat content, the structure within the intramuscular connective tissue remained rigid at 32 months of age, and the shear force value of the muscle continued to increase, even during the late fattening period from 20 to 32 months of age. Thus, the development of adipose tissues in the longissimus muscle appears to disrupt the structure of the IMCT and remodel the ECM (Nishimura, 2010). This structural change in the IMCT would bring about the extreme tenderness of highly marbled beef from Japanese Black cattle (Fig. 3).

The role of ECM in adipogenesis may be multi-faceted (Hausman, 2012). Laminin appear to provide a superior substratum for preadipocytes to adhere and spread, or migrate on (Hausman, Wright & Richardson, 1996). Types IV and V collagens play an important role in the differentiation of bovine intramuscular preadipocytes (Nakajima, Muroya, Tanabe & Chikuni, 2002a,b). The growth of intramuscular adipose tissue may be dependent on collagen newly synthesized and organized by the adipocytes per se. Many types of MMP are expressed by preadipocytes and adipocytes (Bouloumie, Sengenes, Portolan, Galitzky & Lafontan, 2001). Specific inhibition of MMP-9 drastically reduces adipogenesis in vitro (Bourlier et al., 2005). MMPs and other proteases, such as adamalysins (ADAMS) and cathepsins, could regulate turnover of ECM macromolecules that participate in the regulation of preadipocyte growth, which contributes to adipose tissue development in skeletal muscle. 4. Structural changes in IMCT during postmortem aging of meat Postmortem aging of meat is the process in which meat toughened by rigor mortis is naturally tenderized. The structural integrity of myofibrils changes during postmortem aging, which contributes to the tenderness of aged meat (Dransfield et al., 1984; Takahashi, 1996). While the IMCT contribution to meat texture is certainly important, it has been thought to be rather immutable compared to myofibrils during postmortem aging of meat. In the 70s, connective tissue was supposed to be immutable during postmortem aging. Scientists thought that the collagen solubility was affected neither by temperature nor time of postmortem aging (Chizzolini, Ledward & Lawrie, 1977; Pierson & Fox, 1976), suggesting that collagen remains unchanged at the molecular level during postmortem aging. On the other hand, Stanton and Light (1987, 1988, 1990) showed that perimysial collagen is damaged and partially solubilized during postmortem aging. Judge and Aberle (1982) have shown that the thermal shrinkage temperature of bovine intramuscular collagen decreases by 7–8 °C within 7 days postmortem. The isometric tension of the intramuscular collagen decreases at 21 days postmortem in beef (Etherington, 1987). Lewis, Purslow, and Rice (1991) revealed that the breaking strength of the perimysial connective tissue in raw beef decreases during postmortem aging. Our group has shown that the structural integrity of the IMCT decreases during postmortem aging of chicken (Liu, Nishimura & Takahashi, 1994, 1995), beef (Nishimura, Hattori & Takahashi, 1995), and pork (Nishimura, Fang, Ito, Wakamatsu & Takahashi, 2008). These structural changes are closely related to the mechanical strength of meat as demonstrated by shear measurements on raw muscle or uncooked IMCT structures (Nishimura, Liu, Hattori & Takahashi, 1998). The mechanism by which IMCT is weakened has not been clarified. Although collagen is degraded by metalloproteinases and lysosomal enzymes in vitro (Alexander & Werb, 1991; Bailey & Light, 1989), it is not clear whether these enzymes under the conditions of postmortem muscle can disintegrate collagen fibrils that are densely packed in the IMCT. β-Glucuronidase, which is known to attack PGs, is released from lysosomes in postmortem muscle (Moeller, Fields, Dutson, Landmann & Carpenter, 1976). The activity of free βglucuronidase increases with postmortem aging, concomitant with an increase in the tenderness of beef (Dutson & Lawrie, 1974). Nishimura, Hattori, and Takahashi (1996a) have shown that the amount of PGs in bovine semitendinosus muscle decreases with time postmortem, and that collagen fibril-associated PGs in the perimysium disappear almost entirely during postmortem aging of beef. Etherington (1987) showed that the type and quantity of associated PGs are important in determining the level of susceptibility of collagen to enzymatic digestion. Furthermore, Wu, Dutson, and Carpenter (1981) have demonstrated that collagen solubility increases due to the combined action of collagenase with β-glucuronidase or hyaluronidase. Taken together, there is a possibility that lysosomal glycosidases expose collagen fibrils from surrounding PGs and facilitate

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Fig. 4. Schematic representation of changes in the intramuscular connective tissues during postmortem aging. Immediately postmortem, proteoglycans link collagen fibrils and stabilize the intramuscular connective tissues. During postmortem aging, proteoglycans are degraded and the linkage between collagen fibrils is weakened. This structural change in the intramuscular connective tissues contributes to the tenderization of aged meat. Adapted from Nishimura, Hattori, and Takahashi (1996a).

their degradation by collagenase, resulting in the disintegration of IMCT during postmortem aging of meat (Fig. 4). PGs may stabilize collagen fibrils and fibers of the IMCT in living muscle, and may protect the collagen matrix in the IMCT during the early stages of postmortem aging of meat. Bouton and Harris (1972) showed that the connective tissue toughness is unaffected by extensive postmortem aging when followed by cooking. Lewis et al. (1991) demonstrated that there is a reduction in strength of IMCT with postmortem aging in raw meat, whereas, these effects are negated after cooking to temperatures of 60 °C and above,

where both aged and unaged perimysial IMCTs have the same strength. Purslow (2005) strongly pointed out that the properties of IMCT in raw meat and degradations during postmortem aging do not directly reflect cooked meat texture. Recently, Purslow (2014) proposed a new hypothesis to explain the effects of proteolysis and cooking on collagen fibril strength in IMCT. This hypothesis speculated that there are two populations (pools) of collagen molecules, with a weak pool being easily degraded by proteolysis and cooking, and a strong pool being more resistant to both (Fig. 5). Purslow mentioned in his review that this hypothesis explains the controversial interaction of postmortem aging and

Fig. 5. A new hypothesis to explain the effects of proteolysis and cooking on collagen fibril strength in intramuscular connective tissue (IMCT). Collagen that is not easily extracted forms two populations of molecules: a (gray) weak pool and a (brown) strong pool. These may be divided into different fibrils as shown here for convenience, or, more likely, comingled in each fibril. (a) The changes expected due to aging (top row versus bottom row) and cooking (left versus right). The weak pool is degraded by both proteolysis in aging and cooking. The remaining structures after cooking, in both the aged and unaged cases, define the remaining strength of the IMCT. (b) The effects of temperature on measured IMCT strength. From Purslow (2014). (Reproduced with permission from Annual Reviews.)

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cooking on the strength of IMCT. Future work is needed to verify two populations of collagen molecules and interactions between these collagens and other ECM macromolecules. 5. Conclusions Skeletal muscle development is a highly organized process regulated by complicated interactions between muscle fibers (cells) and the surrounding ECM. During embryonic development, ECM plays an important role in regulation of muscle cell growth, either through modulation of growth factor activities or through direct involvement in cell signaling. During fetal development, the IMCT forms synchronously with muscle fiber formation and assembly. With postnatal growth, the IMCT must be reconstructed with muscle hypertrophy and intramuscular fat deposition. These structural changes affect the mechanical strength of the IMCT and contribute to variation of meat texture. The IMCT consists of collagen fibrils and fibers, the formation and stability of which are regulated by PGs such as decorin. Thus, the turnover and remodeling of ECM in skeletal muscle must be a future target for manipulation of meat texture. During the postmortem aging of meat, PG components of the IMCT are degraded, which causes the disintegration of the structure of the IMCT network. These structural changes in the ECM decrease the mechanical strength of IMCT in raw meat. Thus, the role of ECM is multifaceted in skeletal muscle development and postmortem aging of meat. References Abdel-Wahab, N., Wicks, S.J., Mason, R.M., & Chantry, A. (2002). Decorin suppresses transforming growth factor-beta-induced expression of plasminogen activator inhibitor-1 in human mesangial cells through a mechanism that involves Ca2+dependent phosphorylation of Smad2 at serine-240. Biochemical Journal, 362, 643–649. Albrecht, E., Gotoh, T., Ebara, F., Xu, J.X., Viergutz, T., Nuernberg, G., Maak, S., & Wegner, J. (2011). Cellular conditions for intramuscular fat deposition in Japanese Black and Holstein steers. Meat Science, 89, 13–20. Albrecht, E., Liu, X., Yang, X., Zhao, R., Jonas, L., & Maak, S. (2011). Colocalization of myostatin and decorin in bovine skeletal muscle. Archiv Tierzucht Archives Animal Breeding, 54, 147–156. Alexander, C.M., & Werb, Z. (1991). Extracellular matrix degradation. In E.D. Hay (Ed.), Cell biology of extracellular matrix (pp. 255–302) (2nd edn.). New York: Plenum Press. Bailey, A.J., & Light, N.D. (1989). Connective tissue in meat and meat products. London: Elsevier Applied Science, London. Bailey, A.J., & Shimokomaki, M.S. (1971). Age related changes in the reducible cross-links of collagen. FEBS Letters, 16, 86–89. Bouloumie, A., Sengenes, C., Portolan, G., Galitzky, J., & Lafontan, M. (2001). Adipocyte produces matrix metalloproteinases 2 and 9: Involvement in adipose differentiation. Diabetes, 50, 2080–2086. Bourlier, V., Zakaroff-Girard, A., De Barros, S., Pizzacalla, C., de Saint Front, V.D., Lafontan, M., Bouloumie, A., & Galitzky, J. (2005). Protease inhibitor treatments reveal specific involvement of matrix metalloproteinase-9 in human adipocyte differentiation. Journal of Pharmacology and Experimental Therapeutics, 312, 1272–1279. Bouton, P.E., & Harris, P.V. (1972). The effects of some post-slaughter treatments on the mechanical properties of bovine and ovine muscle. Journal of Food Science, 37, 539–543. Brandan, E., Fuentes, M.E., & Andrade, W. (1992). Decorin, a chondroitin/dermatan sulfate proteoglycan is under neural control in rat skeletal muscle. Journal of Neuroscience Research, 32, 51–59. Brick, D.E., Nurminskaya, M.V., & Zycband, E.I. (1995). Collagen fibrillogenesis in situ: Fibril segments undergo post-depositional modifications resulting in linear and lateral growth during matrix development. Developmental Dynamics, 202, 229–243. Cabello-Verrugio, C., & Brandan, E. (2007). A novel modulatory mechanism of transforming growth factor-beta signaling through decorin and LRP-1. Journal of Biological Chemistry, 282, 18842–18850. Campion, D.R., Crouse, J.D., & Dikeman, M.E. (1975). Predictive value of USDA beef quality grade factors for cooked meat palatability. Journal of Food Science, 40, 1225–1228. Chizzolini, R., Ledward, D.A., & Lawrie, R.A. (1977). Note on the effect of ageing on the neutral salt and acid soluble collagen from the intramuscular connective tissue of various species. Meat Science, 1, 111–117. Crouse, J.D., Smith, G.M., & Mandigo, R.W. (1978). Relationship of selected beef carcass traits with meat palatability. Journal of Food Science, 43, 152–157. Danielson, K.G., Balibault, H., Holmes, D.F., Graham, H., Kadle, K.E., & Iozzo, R.V. (1997). Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. Journal of Cell Biology, 136, 729–743. Dikeman, M.E., Tuma, H.J., & Beecher, G.R. (1971). Bovine muscle tenderness as related to protein solubility. Journal of Food Science, 36, 190–193.

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Role of extracellular matrix in development of skeletal muscle and postmortem aging of meat.

The integrity of skeletal muscle is maintained by the intramuscular connective tissues (IMCTs) that are composed of extracellular matrix (ECM) molecul...
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