Browse > Article
http://dx.doi.org/10.5713/ajas.2012.12365

A New Insight into the Role of Calpains in Post-mortem Meat Tenderization in Domestic Animals: A review  

Lian, Ting (College of Animal Science and Technology, Sichuan Agricultural University)
Wang, Linjie (College of Animal Science and Technology, Sichuan Agricultural University)
Liu, Yiping (College of Animal Science and Technology, Sichuan Agricultural University)
Publication Information
Asian-Australasian Journal of Animal Sciences / v.26, no.3, 2013 , pp. 443-454 More about this Journal
Abstract
Tenderness is the most important meat quality trait, which is determined by intracellular environment and extracellular matrix. Particularly, specific protein degradation and protein modification can disrupt the architecture and integrity of muscle cells so that improves the meat tenderness. Endogenous proteolytic systems are responsible for modifying proteinases as well as the meat tenderization. Abundant evidence has testified that calpains (CAPNs) including calpain I (CAPN1) and calpastatin (CAST) have the closest relationship with tenderness in livestock. They are involved in a wide range of physiological processes including muscle growth and differentiation, pathological conditions and post-mortem meat aging. Whereas, Calpain3 (CAPN3) has been established as an important activating enzyme specifically expressed in livestock's skeletal muscle, but its role in domestic animals meat tenderization remains controversial. In this review, we summarize the role of CAPN1, calpain II (CAPN2) and CAST in post-mortem meat tenderization, and analyse the relationship between CAPN3 and tenderness in domestic animals. Besides, the possible mechanism affecting post-mortem meat aging and improving meat tenderization, and current possible causes responsible for divergence (whether CAPN3 contributes to animal meat tenderization or not) are inferred. Only the possible mechanism of CAPN3 in meat tenderization has been confirmed, while its exact role still needs to be studied further.
Keywords
Calpains; Post-mortem Meat tenderization; Proteolysis System; Domestic Animals;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 Bar, A. and D. Pette. 1988. Three fast myosin heavy chains in adult rat skeletal muscle. FEBS Lett. 235:153-155.   DOI   ScienceOn
2 Barbut, S., A. A. Sosnicki, S. M. Lonergan, T. Knapp, D. C. Ciobanu, L. J. Gatcliffe, E. Huff-Lonergan and E. W. Wilson. 2008. Progress in reducing the pale, soft and exudative (PSE) problem in pork and poultry meat. Meat Sci. 79:46-63.   DOI   ScienceOn
3 Barendse, W., B. E. Harrison, R. J. Bunch and M. B. Thomas. 2008. Variation at the calpain 3 gene is associated with meat tenderness in zebu and composite breeds of cattle. BMC Genet. 9:41.
4 Beckmann, J. S. and M. Spencer. 2008. Calpain 3, the "gatekeeper" of proper sarcomere assembly, turnover and maintenance. Neuromuscul. Disord. 18:913-921.   DOI   ScienceOn
5 Bernard, C., I. Cassar-Malek, M. L. Cunff, H. Dubroeucq, G. Renand and J. F. Hocquette. 2007. New indicators of beef sensory quality revealed by expression of specific genes. J. Agric. Food Chem. 55:5229-5237.   DOI   ScienceOn
6 Bickerstaffe, R., K. Gately and J. D. Morton. 2008. The association between polymorphic variations in calpain 3 with the yield and tenderness of retail lamb meat cuts. Proceedings of 54th International Congress of Meat Science and Technology, Helsinki, Finland, 1-4.
7 Destefanis, G., A. Brugiapaglia, M. T. Barge and E. Dal Molin. 2008. Relationship between beef consumer tenderness perception and warner-bratzler shear force. Meat Sci. 78:153-156.   DOI   ScienceOn
8 Doumit, M. E. and M. Koohmaraie. 1999. Immunoblot analysis of calpastatin degradation: Evidence for cleavage by calpain in postmortem muscle. J. Anim. Sci. 77:1467-1473.
9 Dransfield, E. 1994. Modelling post-mortem tenderization-V: Inactivation of calpains. Meat Sci. 37:391-409.   DOI   ScienceOn
10 Dutaud, D., L. Aubry, M. A. Sentandreu and A. Ouali. 2006. Bovine muscle 20S proteasome: I. Simple purification Procedure and Enzymatic Characterization in Relation with Postmortem Conditions. Meat Sci. 74:327-336.   DOI   ScienceOn
11 Eisenberg, D., R. M. Weiss, T. C. Terwilliger and W. Wilcox. 1982. Hydrophobic moments and protein structure. Faraday Symp. Chem. Soc. 17:109-120.   DOI
12 Emori, Y., H. Kawasaki, S. Imajoh, S. Kawashima and K. Suzuki. 1986. Isolation and sequence analysis of cDNA clones for the small subunit of rabbit calcium-dependent protease. J. Biol. Chem. 261:9472-9476.
13 Fürst, D. O., M. Osborn, R. Nave and K. Weber. 1988. The organization of titin filaments in the half-sarcomere revealed by monoclonal antibodies in immunoelectron microscopy: A map of ten nonrepetitive epitopes starting at the Z line extends close to the M line. J. Cell Biol. 106:1563-1572.   DOI   ScienceOn
14 Faulkner, G., A. Pallavicini, A. Comelli, M. Salamon, G. Bortoletto, C. Ievolella, S. Trevisan, S. Koji, F. Dalla Vecchia and P. Laveder. 2000. FATZ, a filamin-, actinin-, and telethonin-binding protein of the Z-disc of skeletal muscle. J. Biol. Chem. 275:41234-41242.   DOI   ScienceOn
15 Koohmaraie, M., M. E. Doumit and T. L. Wheeler. 1996. Meat toughening does not occur when rigor shortening is prevented. J. Anim. Sci. 74:2935-2942.
16 Koohmaraie, M. 1992. The role of $Ca^{2+}$-dependent proteases(calpains) in post mortem proteolysis and meat tenderness. Biochimie 74:239-245.   DOI   ScienceOn
17 Koohmaraie, M. 1996. Biochemical factors regulating the toughening and tenderization processes of meat. Meat Sci. 43 (Supp. 1):193-201.   DOI   ScienceOn
18 Koohmaraie, M., A. H. Chishti, G. H. Geesink and S. Kucha. 2006. $\mu$-Calpain is essential for postmortem proteolysis of muscle proteins. J. Anim. Sci. 84:2834-2840.   DOI   ScienceOn
19 Koohmaraie, M. and G. H. Geesink. 2006. Contribution of postmortem muscle biochemistry to the delivery of consistent meat quality with particular focus on the calpain system. Meat Sci. 74:34-43.   DOI   ScienceOn
20 Koohmaraie, M., S. C. Seideman, J. E. Schollmeyer, T. R. Dutson and A. S. Babiker. 1988. Factors associated with the tenderness of three bovine muscles. J. Food Sci. 53:407-410.   DOI
21 Koohmaraie, M., G. Whipple, D. H. Kretchmar, J. D. Crouse and H. J. Mersmann. 1991. Postmortem proteolysis in longissimus muscle from beef, lamb and pork carcasses. J. Anim. Sci. 69: 617-624.
22 Kramerova, I., E. Kudryashova, J. G. Tidball and M. J. Spencer. 2004. Null mutation of calpain 3 (p94) in mice causes abnormal sarcomere formation in vivo and in vitro. Hum. Mol. Genet. 13:1373-1388.   DOI   ScienceOn
23 Kramerova, I., E. Kudryashova, B. Wu and M. J. Spencer. 2006. Regulation of the M-cadherin-beta-catenin complex by calpain 3 during terminal stages of myogenic differentiation. Mol. Cell Biol. 26:8437- 8447.   DOI   ScienceOn
24 Mayes, P. A. 1993. Metabolism of glycogen. In: Harpers biochemistry 28th. edn. New Jersy: Appleton and Lange Publishing Division of Prentice Hall, Englewood Cliffs, pp. 50-400.
25 Lindholm-Perry, A. K., G. A. Rohrer, J. W. Holl, S. D. Shackelford, T. L. Wheeler, M. Koohmaraie and D. Nonneman. 2009. Relationships among calpastatin single nucleotide polymorphisms, calpastatin expression and tenderness in pork longissimus. Anim. Genet. 40:713-721.   DOI   ScienceOn
26 Locker, R. H. and C. J. Hagyard. 1963. A cold shortening effect in beef muscles. J. Sci. Food Agric. 14:787-793.   DOI
27 Ma, H., C. Fukiage, M. Azuma and T. R. Shearer. 1998. Cloning and expression of mRNA for calpain Lp82 from rat lens: Splice variant of p94. Invest. Ophthalmol. Vis. Sci. 39:454-461.
28 McCormick, R. J. 2009. Collagen, applied muscle biology and meat science. In: CRC Press, Boca Raton, FL, pp. 129-148.
29 Mellgren, R. L. 2008. Structural biology: Enzyme knocked for a loop. Nature 456:337-338.
30 Melody, J. L., S. M. Lonergan, L. J. Rowe, T. W. Huiatt, M. S. Mayes and E. Huff-Lonergan. 2004. Early postmortem biochemical factors influence tenderness and water holding capacity of three porcine muscles. J. Anim. Sci. 82:1195-1205.
31 Meyers, S. N. and J. E. Beever. 2008. Investigating the genetic basis of pork tenderness: Genomic analysis of porcine CAST. Anim. Genet. 39:531-543.   DOI   ScienceOn
32 Moeller, S. J., R. K. Miller, K. K. Edwards, H. N. Zerby, K. E. Logan, T. L. Aldredge, C. A. Stahl, M. Boggess and J. M. Box-Steffensmeier. 2010. Consumer perceptions of pork eating quality as affected by pork quality attributes and end-point cooked temperature. Meat Sci. 84:14-22.   DOI   ScienceOn
33 Ravulapalli, R., B. Garcia Diaz, R. L. Campbell and P. L. Davies. 2005. Homodimerization of calpain 3 penta-EF-hand domain. Biochem. J. 388:585-591.   DOI   ScienceOn
34 Pomponio, L., R. Lametsch, A. H. Karlsson, L. N. Costa, A. Grossi and P. Ertbjerg. 2008. Evidence for post-mortem m-calpain autolysis in porcine muscle. Meat Sci. 80:761-764.   DOI   ScienceOn
35 Poussard, S., M. Duvert, D. Balcerzak, S. Ramassamy, J. J. Brustis, P. Cottin and A. Ducastaing. 1996. Evidence for implication of muscle-specific calpain (p94) in myofibrillar integrity. Cell Growth Differ. 7:1461-1469.
36 Ravulapalli, R., R. Campbell, S. Y. Gauthier, S. Dhe-Paganon and P. L. Davies. 2009. Distinguishing between calpain heterodimerization and homodimerization. FEBS J. 276:973-982.   DOI   ScienceOn
37 Rees, M. P., G. R. Trout and R. D. Warner. 2002. Effect of calcium infusion on tenderness and ageing rate of pork M. Longissimus Thoracis et Lumborum after accelerated boning. Meat Sci. 61: 169-179.   DOI   ScienceOn
38 Riley, D. G., C. C. Chase, T. D. Pringle, R. L. West, D. D. Johnson, T. A. Olson, A. C. Hammond and S. W. Coleman. 2003. Effect of sire on -and m-calpain activity and rate of tenderization as indicated by myofibril fragmentation indices of steaks from Brahman cattle. J. Anim. Sci. 81:2440-2447.
39 Roberts, N., B. Palmer, J. G. H. Hickford and R. Bickerstaffe. 1996. PCR-SSCP in the ovine calpastatin gene. Anim. Genet. 27:211.
40 Salmikangas, P., P. F. M. Van der Ven, M. Lalowski, A. Taivainen, F. Zhao, H. Suila, R. Schr der, P. Lappalainen and D. O. Furst. 2003. Myotilin, the limb-girdle muscular dystrophy 1A (LGMD1A) protein, cross-links actin filaments and controls sarcomere assembly. Hum. Mol. Genet. 12:189-203.   DOI   ScienceOn
41 Van der Ven, P. F. M., S. Wiesner, P. Salmikangas, D. Auerbach, M. Himmel, S. Kempa, K. Haye, D. Pacholsky, A. Taivainen, R. Schroder, O. Carpen and D. O. Furst. 2000. Indications for a novel muscular dystrophy pathway. J. Cell Biol. 151:235-248.   DOI
42 Taylor, R. G., G. H. Geesink, V. F. Thompson, M. Koohmaraie and D. E. Goll. 1995. Is Z-disk degradation responsible for postmortem tenderization? J. Anim. Sci. 73:1351-1367.
43 Tompa, P., Y. Emori, H. Sorimachi, K. Suzuki and P. Friedrich. 2001. Domain III of calpain is a $Ca^{2+}$-regulated phospholipid-binding domain. Biochem. Biophys. Res. Commun. 280:1333-1339.   DOI   ScienceOn
44 Tullio, R. D., M. Passalacqua, M. Averna, F. Salamino, E. Melloni and S. Pontremoli. 1999. Changes in intracellular localization of calpastatin during calpain activation. Biochem. J. 343:467- 472.   DOI
45 Veiseth, E., S. D. Shackelford, T. L. Wheeler and M. Koohmaraie. 2001. Effect of postmortem storage on mu-calpain and m-calpain in ovine skeletal muscle. J. Anim. Sci. 79:1502-1508.
46 Veiseth, E., S. D. Shackelford, T. L. Wheeler and M. Koohmaraie. 2004. Factors regulating lamb longissimus tenderness are affected by age at slaughter. Meat Sci. 68:635-640.   DOI   ScienceOn
47 Wang, K. and R. Ramirez-Mitchell. 1983. A network of transverse and longitudina intermediate filaments is associated with sarcomeres of adult vertebrate skeletal-muscle. J. Cell Biol. 96:562-570.   DOI
48 Wang, K. and J. Wright. 1988. Architecture of the sarcomere matrix of skeletal muscle: immunoelectron microscopic evidence that suggests a set of parallel inextensible nebulin filaments anchored at the Z line. J. Cell Biol. 107:2199-2212.   DOI   ScienceOn
49 Wang, Y. M. and L. F. Li. 1994. The relationship between muscle histology characteristics and meat quality on Yushan pigs of JiangXi. Acta J. X. Agric. Univ. 16:284-287.
50 Blanchard, H., P. Grochulski, Y. Li, J. S. C. Arthur, P. L. Davies, J. S. Elce and M. Cygler. 1997. Structure of a calpain $Ca^{2+}$-binding domain reveals a novel EF-hand and $Ca^{2+}$-induced conformational changes. Nat. Struct. Biol. 4:532-538.   DOI   ScienceOn
51 Blanchard, H., Y. Li, M. Cygler, C. M. Kay, J. S. C. Arthur, P. L. Davies and J. S. Elce. 1996. $Ca^{2+}$-binding domain VI of rat calpain is a homodimer in solution: Hydrodynamic, crystallization and preliminary X-ray diffraction studies. Protein Sci. 5:535-537.
52 Boleman, S. J., S. L. Boleman, T. D. Bidner, K. W. McMillin and C. J. Monlezun. 1995. Effects of postmortem time of calcium chloride injection on beef tenderness and drip, cooking, and total loss. Meat Sci. 39:35-41.   DOI   ScienceOn
53 Brooke, M. H. and K. K. Kaiser. 1970. Muscle fiber types: How many and what kind? Arch. Neurol. 23:369-379.   DOI   ScienceOn
54 Brule, C., E. Dargelos, R. Diallo, A. Listrat, D. Bechet, P. Cottin and S. Poussard. 2010. Proteomic study of calpain interacting proteins during skeletal muscle aging. Biochimie 92:1923-1933.   DOI   ScienceOn
55 Cafe, L. M., B. L. McIntyre, D. L. Robinson, G. H. Geesink, W. Barendse, D. W. Pethick, J. M. Thompson and P. L. Greenwood. 2010. Production and processing studies on calpain-system gene markers for tenderness in brahman cattle:1. Growth, efficiency, temperament, and carcass characteristics. J. Anim. Sci. 88:3047-3058.   DOI   ScienceOn
56 Camou, J. P., J. A. Marchello, V. F. Thompson, S. W. Mares and D. E. Goll. 2007. Effect of postmortem storage on activity of $\mu$-and m-calpain in five bovine muscles. J. Anim. Sci. 85: 2670-2681.   DOI   ScienceOn
57 Casas, E., S. N. White, T. L. Wheeler, S. D. Shackelford, M. Koohmaraie, D. G. Riley, C. C. Chase Jr, D. D. Johnson and T. P. L. Smith. 2006. Effects of calpastatin and $\mu$-calpain markers in beef cattle on tenderness traits. J. Anim. Sci. 84:520-525.
58 Ciobanu, D. C., J. W. M. Bastiaansen, S. M. Lonergan, H. Thomsen, J. C. M. Dekkers, G. S. Plastow and M. F. Rothschild. 2004. New alleles in calpastatin gene are associated with meat quality traits in pigs. J. Anim. Sci. 82: 2829-2839.
59 Cazorla, O., Y. Wu, T. C. Irving and H. Granzier. 2001. Titin-based modulation of calciumsensitivity of active tension in mouse skinned cardiac myocytes. Circ. Res. 88:1028-1035.   DOI   ScienceOn
60 Cheong, H. S., D. H. Yoon, B. L. Park, L. H. Kim, J. S. Bae, S. Namgoong, H. W. Lee, C. S. Han, J. O. Kim and I. C. Cheong. 2008. A single nucleotide polymorphism in CAPN 1 associated with marbling score in Korean cattle. BMC Genet. 9:33.
61 Cong, M., V. F. Thompson, D. E. Goll and P. B. Antin. 1998. The bovine calpastatin gene promoter and a new N-terminal region of the protein are targets for cAMP-dependent protein kinase activity. J. Biol. Chem. 273:660-666.   DOI   ScienceOn
62 Corva, P., L. Soria, A. Schor, E. Villarreal, M. P. Cenci, M. Motter, C. Mezzadra, L. Melucci, C. Miquel, E. Paván, G. Depetris, F. Santini and J. G. Naón. 2007. Association of CAPN1 and CAST gene polymorphisms with meat tenderness in Bos Taurus beef cattle from Argentina. Genet. Mol. Biol. 30:1064-1069.   DOI
63 Costello, S., E. O'Doherty, D. J. Troy, C. W. Ernst, K. S. Kim, P. Stapleton, T. Sweeney and A. M. Mullen. 2007. Association of polymorphisms in the calpain I, calpain II and growth hormone genes with tenderness in bovine M. Longissimus Dorsi. Meat Sci. 75:551-557.   DOI   ScienceOn
64 Croall, D. E. and G. N. DeMartino. 1991. Calcium-activated neutral protease (calpain) system: Structure, function, and regulation. Physiol. Rev. 71:813-847.
65 Croall, D. E. and K. Ersfeld. 2007. The calpains: Modular designs and functional diversity. Genome Biol. 8: 218.   DOI
66 Geesink, G. H., R. G. Taylor and M. Koohmaraie. 2005. Calpain 3/p94 is not involved in postmortem proteolysis. J. Anim. Sci. 83:1646-1652.
67 Fougerousse, F., M. Durand, L. Suel, O. Pourquie, A. L. Delezoide, N. B. Romero, M. Abitbol and J. S. Beckmann. 1998. Expression of genes (CAPN3, SGCA, SGCB, and TTN) involved in progressive muscular dystrophies during early human development. Genomics 48:145-156.   DOI   ScienceOn
68 Gandolfi, G., L. Pomponio, P. Ertbjerg, A. H. Karlsson, L. Nanni Costa, R. Lametsch, V. Russo and R. Davoli. 2011. Investigation on CAST, CAPN1 and CAPN3 porcine gene polymorphisms and expression in relation to post-mortem calpain activity in muscle and meat quality. Meat Sci. 88:694-700.   DOI   ScienceOn
69 Garcia Diaz, B. E., S. Gauthier and P. L. Davies. 2006. $Ca^{2+}$ dependency of calpain 3 (p94) activation. Biochemistry 45:3714-3722.   DOI   ScienceOn
70 Goll, D. E., R. M. Robson and M. H. Stromer. 1984. Skeletal muscle, nervous system, temperature regulation, and special senses. In: Duke's physiol. domestic anim (Ed. M. J. Swensen). Ithaca, N.Y: Cornell University Press. pp. 548-580.
71 Goll, D. E., W. R. Dayton, I. Singh and R. M. Robson. 1991. Studies of the alpha-actinin/actin interaction in the Z-Disk by using calpain. J. Biol. Chem. 266:8501-8510.
72 Goll, D. E., Y. Otsuka, P. A. Nagainis, J. D. Shannon, S. K. Sathe and M. Muguruma. 1983. Role of muscle proteinases in maintenance of muscle integrity and mass. J. Food Biochem. 7:137-177.   DOI
73 Goll, D. E., V. F. Thompson, H. Li, W. Wei and J. Cong. 2003. The calpain system. Physiol. Rev. 83:731-801.
74 Gollasch, M. and M. T. Nelson. 1997. Voltage-dependent $Ca^{2+}$ channels in arterial smooth muscle cells. Kidney Blood Press. Res. 20:355-371.   DOI   ScienceOn
75 Hanna, R. A., R. L. Campbell and P. L. Davies. 2008. Calcium-bound structure of calpain and its mechanism of inhibition by calpastatin. Nature 456:409-412.   DOI   ScienceOn
76 Grobbel, J. P., M. E. Dikeman, M. C. Hunt and G. A. Milliken. 2008. Effects of packaging atmospheres on beef instrumental tenderness, fresh color stability, and internal cooked color. J. Anim. Sci. 86:1191-1199.
77 Guroff, G. 1964. A neutral, calcium-activated proteinase from the soluble fraction of rat brain. J. Biol. Chem. 239:149-155.
78 Guyon, J. R., E. Kudryashova, A. Potts, I. Dalkilic, M. A. Brosius, T. G. Thompson, J. S. Beckmann, L. M. Kunkel and M. J. Spencer. 2003. Calpain 3 cleaves filamin C and regulates its ability to interact with $\gamma$-and $\delta$-sarcoglycans. Muscle Nerve 28: 472-483.   DOI   ScienceOn
79 Herasse, M., Y. Ono, F. Fougerousse, E. Kimura, D. Stockholm, C. Beley, D. Montarras, C. H. Sorimachi, K. Suzuki, J. S. Beckmann and I. Richard. 1999. Expression and functional characteristics of calpain 3 isoforms generated through tissue-specific transcriptional and posttranscriptional events. Mol. Cell Biol. 19:4047-4055.
80 Hosfield, C. M., J. S. Elce, P. L. Davies and Z. C. Jia. 1999. Crystal structure of calpain reveals the structural basis for $Ca^{2+}$-dependent protease activity and a novel mode of enzyme activation. EMBO J. 18:6880-6889.   DOI   ScienceOn
81 Huff-Lonergan, E. and S. M. Lonergan. 2005. Mechanisms of water-holding capacity of meat: The role of postmortem biochemical and structural changes. Meat Sci. 71:194-204.   DOI   ScienceOn
82 Huff-Lonergan, E., T. Mitsuhashi, D. D. Beekman, F. Parrish Jr, D. G. Olson and R. M. Robson. 1996. Proteolysis of specific muscle structural proteins by mu-calpain at low pH and temperature is similar to degradation in postmortem bovine muscle. J. Anim. Sci. 74:993-1008.
83 Hwang, I. H., C. E. Devine and D. L. Hopkins. 2003. The biochemical and physical effects of electrical stimulation on beef and sheep meat tenderness. Meat Sci. 65:677-691.   DOI   ScienceOn
84 Huff-Lonergan, E. and S. M. Lonergan. 1999. Postmortem mechanisms of meat tenderization: The roles of the structural proteins and the calpain system. In: Quality attributes muscle foods (Ed. Y. L. Xiong, C. -T. Ho and F. Shahidi). New York: Kluwer Academic/Plenum Publishers. pp. 229-251.
85 Huff Lonergan, E., W. Zhang and S. M. Lonergan. 2010. Biochemistry of postmortem muscle-Lessons on mechanisms of meat tenderization. Meat Sci. 86:184-195.   DOI   ScienceOn
86 Hughes, S. M., K. Koishi, M. Rudnicki and A. M. Maggs. 1997. MyoD protein differentially accumulated in fast and slow skeletal muscle fibers and required for normal fiber type balance in rodents. Mech. Dev. 61:151-163.   DOI   ScienceOn
87 Ilian, M. A., A. E. D. Bekhit and R. Bickerstaffe. 2004a. The relationship between meat tenderization, myofibril fragmentation and autolysis of calpain 3 during post-mortem aging. Meat Sci. 66:387-397.   DOI   ScienceOn
88 Ilian, M. A., A. E. D. A. Bekhit, B. Stevenson, J. D. Morton, P. Isherwood and R. Bickerstaffe. 2004b. Up-and down-regulation of longissimus tenderness parallels changes in the myofibril-bound calpain 3 protein. Meat Sci. 67:433-445.   DOI   ScienceOn
89 Ilian, M. A., R. Bickerstaffe and M. L. Greaser. 2004c. Postmortem changes in myofibrillar-bound calpain 3 revealed by immunofluorescence microscopy. Meat Sci. 66:231-240.   DOI   ScienceOn
90 Ilian, M. A., J. D. Morton, A. E. D. Bekhit, N. Roberts, B. Palmer, S. Sorimachi and R. Bickerstaffe. 2001. Effect of preslaughter feed withdrawal period on longissimus tenderness and the expression of calpains in the ovine. J. Agric. Food Chem. 49: 1990-1998.   DOI   ScienceOn
91 Jin, X., L. C. Zhang, Z. H. Li, X. H. Liu, H. G. Jin and C. G. Yan. 2011. Association of polymorphisms in the calpain I gene with meat quality traits in Yanbian yellow cattle of China. Asian-Aust. J. Anim. Sci. 24:9-16.   DOI   ScienceOn
92 Ilian, M. A., J. D. Morton, M. P. Kent, C. E. Le Couteur, J. Hickford, R. Cowley and R. Bickerstaffe. 2001. Intermuscular variation in tenderness: Association with the ubiquitous and muscle-specific calpains. J. Anim. Sci. 79:122-132.
93 Imajoh, S., K. Aoki, S. Ohno, Y. Emori, H. Kawasaki, H. Sugihara and K. Suzuki. 1988. Molecular cloning of the cDNA for the large subunit of the high-calcium-requiring form of human calcium-activated neutral protease. Biochemistry 27:8122-8128.   DOI   ScienceOn
94 Ishida, S., Y. Emori and K. Suzuki. 1991. Rat calpastatin has diverged primary sequence from other mammalian calpastatins but retains functionality important sequences. Biochim. Biophys. Acta. 1088:436-438.   DOI   ScienceOn
95 Karlsson, A. H., R. E. Klont and X. Fernandez. 1999. Skeletal muscle fibres as factors for pork quality. Livest. Prod. Sci. 60: 255-269.   DOI   ScienceOn
96 Kemp, C. M., P. L. Sensky, R. G. Bardsley, P. J. Buttery and T. Parr. 2010. Tenderness-An enzymatic view. Meat Sci. 84:248-256.   DOI   ScienceOn
97 Kent, M. P., M. J. Spencer and M. Koohmaraie. 2004. Postmortem proteolysis is reduced in transgenic mice overexpressing calpastatin. J. Anim. Sci. 82:794-801.
98 Kinbara, K., S. Ishiura, S. Tomioka, H. Sorimachi, S. Y. Jeong, S. Amano, H. Kawasaki, B. Kolmerer, S. Kimura, S. Labeit and K. Suzuki. 1998. Purification of native p94, a muscle-specific calpain, and characterization of its autolysis. Biochem. J. 335: 589-596.
99 Konig, N., F. Raynaud, H. Feane, M. Durand, N. NMestre-Frances, M. Rossel, A. Ouali and Y. Benyamin. 2003. Calpain 3 is expressed in astrocytes of rat and microcebus brain. J. Chem. Neuroanat. 25:129-136.   DOI   ScienceOn
100 Kramerova, I., E. Kudryashova, B. Wu, C. Ottenheijm, H. Granzier and M. J. Spencer. 2008. Novel role of calpain-3 in the triad-associated protein complex regulating calcium release in skeletal muscle. Hum. Mol. Genet. 17:3271-3280.   DOI   ScienceOn
101 Kramerova, I., E. Kudryashova, B. Wu, S. Germain, K. Vandenborne, N. Romain, R. G. Haller, M. A. Verity and M. J. Spencer. 2009. Mitochondrial abnormalities, energy deficit and oxidative stress are features of calpain 3 deficiency in skeletal muscle. Hum. Mol. Genet. 18:3194-3205.   DOI   ScienceOn
102 Lametsch, R., P. Roepstorff and E. Bendixen. 2002. Identification of protein degradation during post-mortem storage of pig meat. J. Agric. Food Chem. 50:5508- 5512.   DOI   ScienceOn
103 Larzul, C., L. Lefaucheur, P. Ecolan, J. Gogue, A. Talmant, P. Sellier, P. Le Roy and G. Monin. 1997. Phenotypic and genetic parameters for longissimus muscle fiber characteristics in relation to growth, carcass, and meat quality traits in large white pigs. J. Anim. Sci. 75:3126-3137.
104 Lee, H. L., V. Sante-Lhoutellier, S. Vigouroux, Y. Briand and M. Briand. 2008. Role of calpains in postmortem proteolysis in chicken muscle. Poult. Sci. 87:2126-2132.   DOI   ScienceOn
105 Lefaucheur, L. 2010. A second look into fibre typing-relation to meat quality. Meat Sci. 84:257-270.   DOI   ScienceOn
106 Lefaucheur, L., D. Milan, P. Ecolan and C. Le Callennec. 2004. Myosin heavy chain composition of different skeletal muscles in large white and meishan pigs. J. Anim. Sci. 82:1931-1941.
107 Lin, G. D., D. Chattopadhyay, M. Maki, K. K. Wang, M. Carson, L. Jin, P. W. Yuen, E. Takano, M. Hatanaka, L. J. DeLucas and S. V. Narayana. 1997. Crystal structure of calcium bound domain VI of calpain at 1.9 A resolution and its role in enzyme assembly, regulation, and inhibitor binding. Nat. Struct. Biol. 4:539-547.   DOI   ScienceOn
108 Morris, C. A., N. G. Cullen, S. M. Hickey, M. Dobbie, B. A. Veenvliet, T. R. Manley, W. S. Pitchford, Z. A. Kruk, C. D. K. Bottema and T. Wilson. 2006. Genotypic effects of calpain 1 and calpastatin on the tenderness of cooked M. Longissimus Dorsi steaks from Jersey${\times}$Limousin, Angus and Hereford-cross cattle. Anim. Genet. 37:411-414.   DOI   ScienceOn
109 Moldoveanu, T., K. Gehring and D. R. Green. 2008. Concerted multi-pronged attack by calpastatin to occlude the catalytic cleft of heterodimeric calpains. Nature 456:404- 408.   DOI   ScienceOn
110 Morgan, J. B., R. K. Miller, F. M. Mendez, D. S. Hale and J. W. Savell. 1991. Using calcium chloride injection to improve tenderness of beef from mature cows. J. Anim. Sci. 69:4469-4476.
111 Moudilou, E. N., N. Mouterfi, J. M. Exbrayat and C. Brun. 2010. Calpains expression during Xenopus Laevis development. Tissue Cell 42:275-281.   DOI   ScienceOn
112 Muroya, S., I. Nakajima and K. Chikuni. 2002. Related expression of MyoD and Myf5 with myosin heavy chain isoform types in bovine adult skeletal muscles. Zool. Sci. 19:755-761.   DOI   ScienceOn
113 Neath, K. E., A. N. Del Barrio, R. M. Lapitan, J. R. V. Herrera, L. C. Cruz, T. Fujihara, S. Muroya, K. Chikuni, M. Hirabayashi and Y. Kanai. 2007. Protease activity higher in postmortem water buffalo meat than Brahman beef. Meat Sci. 77:389-396.   DOI   ScienceOn
114 Ohno, S., Y. Emori and E. Suzuki. 1986. Nucleotide sequence of a cDNA coding for the small subunit of human calcium-dependent protease. Nucleic Acids Res. 14:5559.
115 Ohno, S., S. Minoshima, J. Kudoh, R. Fukuyama, Y. Shimizu, S.Ohmi-Imajohs, N. Shimizu and K. Suzuki. 1990. Four genes for the calpain family locate on four distinct human chromosomes. Cytogenet. Genome Res. 53:225-229.   DOI
116 Schiaffino, S. and C. Reggiani. 1996. Molecular diversity of myofibrillar proteins: Gene regulation and functional significance. Physiol. Rev. 76:371-423.
117 Schenkel, F. S., S. P. Miller, Z. Jiang, I. B. Mandell, X. Ye, H. Li and J. W. Wilton. 2006. Association of a single nucleotide polymorphism in the calpastatin gene with carcass and meat quality traits of beef cattle. J. Anim. Sci. 84:291-299.
118 Schiaffino, S., L. Gorza, S. Sartore, L. Saggin, S. Ausoni, M. Vianello, K. Gundersen and T. LOmo. 1989. Three myosin heavy chain isoforms in type 2 skeletal muscle fibres. J. Muscle Res. Cell Motil. 10:197-205.   DOI
119 Schiaffino, S. and C. Reggiani. 1994. Myosin isoforms in mammalian skeletal muscle. J. Appl. Physiol. 77:493-501.
120 Seideman, S. C., H. R. Cross and J. D. Crouse. 1989. Variations in the sensory properties of beef as affected by sex condition, muscle and postmortem aging. J. Food Qual. 12:39-58.   DOI
121 Sentandreu, M. A., G. Coulis and A. Ouali. 2002. Role of muscle endopeptidases and their inhibitors in meat tenderness. Trends Food Sci. Technol. 13:400-421.   DOI   ScienceOn
122 Shackelford, S. D., T. L. Wheeler, M. K. Meade, J. O. Reagan, B. L. Byrnes and M. Koohmaraie. 2001. Consumer impressions of tender select beef. J. Anim. Sci. 79:2605-2614.
123 Sieczkowska, H., A. Zybert, E. Krzecio, K. Antosik, M. Kocwin-Podsiadla, M. Pierzchala and P. Urbanski. 2010. The expression of genes PKM2 and CAST in the muscle tissue of pigs differentiated by glycolytic potential and drip loss, with reference to the genetic group. Meat Sci. 84:137-142.   DOI   ScienceOn
124 Simmons, N. J., C. C. Daly, T. L. Cummings, S. K. Morgan, N. V. Johnson and A. Lombard. 2008. Reassessing the principles of electrical stimulation. Meat Sci. 80:110-122.   DOI   ScienceOn
125 Page, B. T., E. Casas, R. L. Quaas, R. M. Thallman, T. L. Wheeler, S. D. Shackelford, M. Koohmaraie, S. N. White, G. L. Bennett, J. W. Keele, M. E. Dikeman and T. P. Smith. 2004. Association of markers in the bovine CAPN1 gene with meat tenderness in large crossbred populations that sample influential industry sires. J. Anim. Sci. 82:3474-3481.
126 Ono, Y., K. Kakinuma, F. Torii, A. Irie, K. Nakagawa, S. Labeit, K. Abe, K. Suzuki and H. Sorimachi. 2004. Possible regulation of the conventional calpain system by skeletal muscle-specific calpain, p94/calpain 3. J. Biol. Chem. 279:2761-2771.   DOI   ScienceOn
127 Ono, Y., K. Ojima, F. Torii, E. Takaya, N. Doi, K. Nakagawa, S. Hata, K. Abe and H. Sorimachi. 2010. Skeletal muscle-specific calpain is an intracellular $Na^{+}$-dependent protease. J. Biol. Chem. 285:22986-22998.   DOI   ScienceOn
128 Page, B. T., E. Casas, M. P. Heaton, N. G. Cullen, D. L. Hyndman, C. A. Morris, A. M. Crawford, T. L. Wheeler, M. Koohmaraie, J. W. Keele and T. P. L. Smith. 2002. Evaluation of single-nucleotide polymorphisms in CAPN1 for association with meat tenderness in cattle. J. Anim. Sci. 80:3077-3085.
129 Parr, T., P. L. Sensky, G. P. Scothern, R. G. Bardsley, P. J. Buttery, J. D. Wood and C. Warkup. 1999. Relationship between skeletal muscle-specific calpain and tenderness of conditioned porcine longissimus muscle. J. Anim. Sci. 77:661-668.
130 Peaston, A. E. and E. Whitelaw. 2006. Epigenetics and phenotypic variation in mammals. Mamm. Genome 17:365-374.   DOI
131 Pette, D. and R. S. Staron. 2000. Myosin isoforms, muscle fiber types, and transitions. Microsc. Res. Techniq. 50: 500-509.   DOI
132 Pinto, L. F. B, J. B. S. Ferraz, F. V. Meirelles, J. P. Eler, F. M. Rezende, M. E. Carvalho, H. B. Almeida and R. C. G. Silva. 2010. Association of SNPs on CAPN1 and CAST genes with tenderness in Nellore cattle. Genet. Mol. Res. 9:1431-1442.   DOI
133 Sorimachi, H., N. Toyama-Sorimachi, T. C. Saido, H. Kawasaki, H. Sugita, M. Miyasaka, K. Arahata, S. Ishiura and K. Suzuki. 1993. Muscle-specific calpain, p94, is degraded by autolysis immediately after translation, resulting in disappearance from muscle. J. Biol. Chem. 268:10593-10605.
134 Skrlep, M., M. Candek-Potokar, T. Kavar, B. Zlender, M. HortOs, P. Gou, J. Arnau, G. Evans, O. Southwood, A. Diestre and N. Robert. 2010. Association of PRKAG3 and CAST genetic polymorphisms with traits of interest in dry-cured ham production: Comparative study in France, Slovenia and Spain. Livest Sci. 128:60-66.   DOI   ScienceOn
135 Sorimachi, H., S. Imajoh-Ohmi, Y. Emori, H. Kawasaki, S. Ohno, Y. Minami and K. Suzuki. 1989. Molecular cloning of a novel mammalian calcium-dependent protease distinct from both m-and mu-types. Specific expression of the mRNA in skeletal muscle. J. Biol. Chem. 264:20106-20111.
136 Sorimachi, H., K. Kinbara, S. Kimura, M. Takahashi, S. Ishiura, N. Sasagawa, N. Sorimachi, H. Shimada, K. Tagawa, K. Maruyama and K. Suzuki. 1995. Muscle-specific calpain, p94, responsible for limb girdle muscular dystrophy type 2A, associates with connectin through IS2, a p94-specific sequence. J. Biol. Chem. 270:31158-31162.   DOI
137 Strobl, S., C. Fernandez-Catalan, M. Braun, R. Huber, H. Masumoto, K. Nakagawa, A. Irie, H. Sorimachi, G. Bourenkow, H. Bartunik, K. Suzuki and W. Bode. 2000. The crystal structure of calcium-free human m-calpain suggests an electrostatic switch mechanism for activation by calcium. Proc. Natl. Acad. Sci. 97:588-592.   DOI
138 Stuelsatz, P., F. Pouzoulet, Y. Lamarre, E. Dargelos, S. Poussard, S. Leibovitch, P. Cottin and P. Veschambre. 2010. Down-regulation of MyoD by calpain 3 promotes generation of reserve cells in C2C12 myoblasts. J. Biol. Chem. 285:12670-12683.   DOI   ScienceOn
139 Suzuki, K., H. Sorimachi, T. Yoshizawa, K. Kinbara and S. Ishiura. 1995. Calpain: Novel family members, activation, and physiological function. Biol. Chem. Hoppe-Seyler 376:523.   DOI   ScienceOn
140 Wendt, A., V. F. Thompson and D. E. Goll. 2004. Interaction of calpastatin with calpain: A review. Biol. Chem. 385:465-472.
141 Wheeler, T. L. and M. Koohmaraie. 1999. The extent of proteolysis is independent of sarcomere length in lamb longissimus and psoas major. J. Anim. Sci. 77:2444-2451.
142 Wheeler, T. L., S. D. Shackelford and M. Koohmaraie. 2000. Variation in proteolysis, sarcomere length, collagen content, and tenderness among major pork muscles. J. Anim. Sci. 78: 958-965.
143 Whipple, G. and M. Koohmaraie. 1991. Degradation of myofibrillar proteins by extractable lysosomal enzymes and m-calpain, and the effects of zinc chloride. J. Anim. Sci. 69: 4449-4460.
144 White, S. N., E. Casas, T. L. Wheeler, S. D. Shackelford, M. Koohmaraie, D. G. Riley, C. C. Chase, D. D. Johnson, J. W. Keele and T. P. L. Smith. 2005. A new single nucleotide polymorphism in CAPN1 extends the current tenderness marker test to include cattle of Bos Indicus, Bos Taurus, and crossbred descent. J. Anim. Sci. 83:2001-2008.
145 Xu, X. X., X. Shui, Z. H. Chen, C. Q. Shan, Y. N. Hou and Y. G. Cheng. 2009. Development and application of a real-time PCR method for pharmacokinetic and biodistribution studies of recombinant adenovirus. Mol. Biotechnol. 43:130-137.   DOI   ScienceOn
146 Zhang, Z. R., Y. P. Liu, Y. G. Yao, X. S. Jiang, H. R. Du and Q. Zhu. 2009. Identification and association of the single nucleotide polymorphisms in calpain3 (CAPN3) gene with carcass traits in chickens. BMC Genet. 10:10.
147 Zor, K., R. Ortiz, E. Saatci, R. Bardsley, T. Parr, E. Csoregi and M. Nistor. 2009. Label free capacitive immunosensor for detecting calpastatin-A meat tenderness biomarker. Bioelectrochemistry 76:93-99.   DOI   ScienceOn