DOI QR코드

DOI QR Code

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)
  • Received : 2012.06.28
  • Accepted : 2012.09.15
  • Published : 2013.03.01

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

References

  1. Bar, A. and D. Pette. 1988. Three fast myosin heavy chains in adult rat skeletal muscle. FEBS Lett. 235:153-155. https://doi.org/10.1016/0014-5793(88)81253-5
  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. https://doi.org/10.1016/j.meatsci.2007.07.031
  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. https://doi.org/10.1016/j.nmd.2008.08.005
  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. https://doi.org/10.1021/jf063372l
  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. 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. https://doi.org/10.1038/nsb0797-532
  8. 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.
  9. 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. https://doi.org/10.1016/0309-1740(95)80005-0
  10. Brooke, M. H. and K. K. Kaiser. 1970. Muscle fiber types: How many and what kind? Arch. Neurol. 23:369-379. https://doi.org/10.1001/archneur.1970.00480280083010
  11. 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. https://doi.org/10.1016/j.biochi.2010.09.003
  12. 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. https://doi.org/10.2527/jas.2009-2678
  13. 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. https://doi.org/10.2527/jas.2007-0164
  14. 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.
  15. 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. https://doi.org/10.1161/hh1001.090876
  16. 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.
  17. 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.
  18. 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. https://doi.org/10.1074/jbc.273.1.660
  19. 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. https://doi.org/10.1590/S1415-47572007000600006
  20. 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. https://doi.org/10.1016/j.meatsci.2006.06.021
  21. Croall, D. E. and G. N. DeMartino. 1991. Calcium-activated neutral protease (calpain) system: Structure, function, and regulation. Physiol. Rev. 71:813-847.
  22. Croall, D. E. and K. Ersfeld. 2007. The calpains: Modular designs and functional diversity. Genome Biol. 8: 218. https://doi.org/10.1186/gb-2007-8-6-218
  23. 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. https://doi.org/10.1016/j.meatsci.2007.05.031
  24. 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.
  25. Dransfield, E. 1994. Modelling post-mortem tenderization-V: Inactivation of calpains. Meat Sci. 37:391-409. https://doi.org/10.1016/0309-1740(94)90055-8
  26. 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. https://doi.org/10.1016/j.meatsci.2006.03.027
  27. Eisenberg, D., R. M. Weiss, T. C. Terwilliger and W. Wilcox. 1982. Hydrophobic moments and protein structure. Faraday Symp. Chem. Soc. 17:109-120. https://doi.org/10.1039/fs9821700109
  28. 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.
  29. 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. https://doi.org/10.1083/jcb.106.5.1563
  30. 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. https://doi.org/10.1074/jbc.M007493200
  31. 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. https://doi.org/10.1006/geno.1997.5160
  32. 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. https://doi.org/10.1016/j.meatsci.2011.02.031
  33. Garcia Diaz, B. E., S. Gauthier and P. L. Davies. 2006. $Ca^{2+}$ dependency of calpain 3 (p94) activation. Biochemistry 45:3714-3722. https://doi.org/10.1021/bi051917j
  34. 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.
  35. 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.
  36. 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.
  37. 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. https://doi.org/10.1111/j.1745-4514.1983.tb00795.x
  38. Goll, D. E., V. F. Thompson, H. Li, W. Wei and J. Cong. 2003. The calpain system. Physiol. Rev. 83:731-801.
  39. Gollasch, M. and M. T. Nelson. 1997. Voltage-dependent $Ca^{2+}$ channels in arterial smooth muscle cells. Kidney Blood Press. Res. 20:355-371. https://doi.org/10.1159/000174250
  40. 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.
  41. Guroff, G. 1964. A neutral, calcium-activated proteinase from the soluble fraction of rat brain. J. Biol. Chem. 239:149-155.
  42. 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. https://doi.org/10.1002/mus.10465
  43. 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. https://doi.org/10.1038/nature07451
  44. 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.
  45. 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. https://doi.org/10.1093/emboj/18.24.6880
  46. 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. https://doi.org/10.1016/j.meatsci.2005.04.022
  47. 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.
  48. 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.
  49. 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. https://doi.org/10.1016/j.meatsci.2010.05.004
  50. 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. https://doi.org/10.1016/S0925-4773(96)00631-4
  51. 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. https://doi.org/10.1016/S0309-1740(02)00271-1
  52. 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. https://doi.org/10.1016/S0309-1740(03)00125-6
  53. 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. https://doi.org/10.1016/j.meatsci.2003.11.016
  54. 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. https://doi.org/10.1016/S0309-1740(03)00096-2
  55. 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. https://doi.org/10.1021/jf0010026
  56. 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.
  57. 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. https://doi.org/10.1021/bi00421a022
  58. 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. https://doi.org/10.1016/0167-4781(91)90139-D
  59. 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. https://doi.org/10.5713/ajas.2011.90407
  60. Karlsson, A. H., R. E. Klont and X. Fernandez. 1999. Skeletal muscle fibres as factors for pork quality. Livest. Prod. Sci. 60: 255-269. https://doi.org/10.1016/S0301-6226(99)00098-6
  61. 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. https://doi.org/10.1016/j.meatsci.2009.06.008
  62. 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.
  63. 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.
  64. 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. https://doi.org/10.1016/S0891-0618(02)00102-3
  65. Koohmaraie, M. 1992. The role of $Ca^{2+}$-dependent proteases(calpains) in post mortem proteolysis and meat tenderness. Biochimie 74:239-245. https://doi.org/10.1016/0300-9084(92)90122-U
  66. Koohmaraie, M. 1996. Biochemical factors regulating the toughening and tenderization processes of meat. Meat Sci. 43 (Supp. 1):193-201. https://doi.org/10.1016/0309-1740(96)00065-4
  67. 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. https://doi.org/10.2527/jas.2006-122
  68. 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.
  69. 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. https://doi.org/10.1016/j.meatsci.2006.04.025
  70. 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. https://doi.org/10.1111/j.1365-2621.1988.tb07717.x
  71. 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.
  72. 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. https://doi.org/10.1093/hmg/ddh153
  73. 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. https://doi.org/10.1128/MCB.01296-06
  74. 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. https://doi.org/10.1093/hmg/ddn223
  75. 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. https://doi.org/10.1093/hmg/ddp257
  76. 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. https://doi.org/10.1021/jf025555n
  77. 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.
  78. 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. https://doi.org/10.3382/ps.2007-00296
  79. Lefaucheur, L. 2010. A second look into fibre typing-relation to meat quality. Meat Sci. 84:257-270. https://doi.org/10.1016/j.meatsci.2009.05.004
  80. 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.
  81. 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. https://doi.org/10.1038/nsb0797-539
  82. 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. https://doi.org/10.1111/j.1365-2052.2009.01903.x
  83. Locker, R. H. and C. J. Hagyard. 1963. A cold shortening effect in beef muscles. J. Sci. Food Agric. 14:787-793. https://doi.org/10.1002/jsfa.2740141103
  84. 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.
  85. 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.
  86. McCormick, R. J. 2009. Collagen, applied muscle biology and meat science. In: CRC Press, Boca Raton, FL, pp. 129-148.
  87. Mellgren, R. L. 2008. Structural biology: Enzyme knocked for a loop. Nature 456:337-338.
  88. 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.
  89. 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. https://doi.org/10.1111/j.1365-2052.2008.01765.x
  90. 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. https://doi.org/10.1016/j.meatsci.2009.06.023
  91. 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. https://doi.org/10.1038/nature07353
  92. 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.
  93. 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. https://doi.org/10.1111/j.1365-2052.2006.01483.x
  94. Moudilou, E. N., N. Mouterfi, J. M. Exbrayat and C. Brun. 2010. Calpains expression during Xenopus Laevis development. Tissue Cell 42:275-281. https://doi.org/10.1016/j.tice.2010.07.001
  95. 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. https://doi.org/10.2108/zsj.19.755
  96. 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. https://doi.org/10.1016/j.meatsci.2007.04.010
  97. 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.
  98. 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. https://doi.org/10.1159/000132937
  99. 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. https://doi.org/10.1074/jbc.M308789200
  100. 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. https://doi.org/10.1074/jbc.M110.126946
  101. 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.
  102. 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.
  103. 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.
  104. Peaston, A. E. and E. Whitelaw. 2006. Epigenetics and phenotypic variation in mammals. Mamm. Genome 17:365-374. https://doi.org/10.1007/s00335-005-0180-2
  105. Pette, D. and R. S. Staron. 2000. Myosin isoforms, muscle fiber types, and transitions. Microsc. Res. Techniq. 50: 500-509. https://doi.org/10.1002/1097-0029(20000915)50:6<500::AID-JEMT7>3.0.CO;2-7
  106. 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. https://doi.org/10.4238/vol9-3gmr881
  107. 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. https://doi.org/10.1016/j.meatsci.2008.03.019
  108. 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.
  109. 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. https://doi.org/10.1111/j.1742-4658.2008.06833.x
  110. 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. https://doi.org/10.1042/BJ20041821
  111. 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. https://doi.org/10.1016/S0309-1740(01)00181-4
  112. 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.
  113. Roberts, N., B. Palmer, J. G. H. Hickford and R. Bickerstaffe. 1996. PCR-SSCP in the ovine calpastatin gene. Anim. Genet. 27:211.
  114. 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. https://doi.org/10.1093/hmg/ddg020
  115. 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.
  116. 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. https://doi.org/10.1007/BF01739810
  117. Schiaffino, S. and C. Reggiani. 1994. Myosin isoforms in mammalian skeletal muscle. J. Appl. Physiol. 77:493-501.
  118. Schiaffino, S. and C. Reggiani. 1996. Molecular diversity of myofibrillar proteins: Gene regulation and functional significance. Physiol. Rev. 76:371-423.
  119. 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. https://doi.org/10.1111/j.1745-4557.1989.tb00308.x
  120. 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. https://doi.org/10.1016/S0924-2244(02)00188-7
  121. 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.
  122. 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. https://doi.org/10.1016/j.meatsci.2009.08.038
  123. 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. https://doi.org/10.1016/j.meatsci.2008.05.006
  124. 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. https://doi.org/10.1016/j.livsci.2009.10.015
  125. 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.
  126. 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. https://doi.org/10.1074/jbc.270.52.31158
  127. 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.
  128. 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. https://doi.org/10.1073/pnas.97.2.588
  129. 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. https://doi.org/10.1074/jbc.M109.063966
  130. 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. https://doi.org/10.1515/bchm3.1995.376.9.523
  131. 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.
  132. 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. https://doi.org/10.1006/bbrc.2001.4279
  133. 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. https://doi.org/10.1042/0264-6021:3430467
  134. 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. https://doi.org/10.1083/jcb.151.2.235
  135. 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.
  136. 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. https://doi.org/10.1016/j.meatsci.2004.05.015
  137. 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. https://doi.org/10.1083/jcb.96.2.562
  138. 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. https://doi.org/10.1083/jcb.107.6.2199
  139. 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.
  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. https://doi.org/10.1007/s12033-009-9173-9
  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. https://doi.org/10.1016/j.bioelechem.2009.06.001

Cited by

  1. Ultrasound as an Alternative to Conventional Marination: Acceptability and Mass Transfer vol.2017, pp.1745-4557, 2017, https://doi.org/10.1155/2017/8675720
  2. Modification of Food Systems by Ultrasound vol.2017, pp.1745-4557, 2017, https://doi.org/10.1155/2017/5794931
  3. Effect of negative dietary cation-anion differences on carcass characteristics and beef tenderness of Japanese Black steers pp.13443941, 2017, https://doi.org/10.1111/asj.12918
  4. High intensity ultrasound homogenizes and improves quality of beef longissimus dorsi pp.0101-2061, 2018, https://doi.org/10.1590/fst.05218
  5. Gene Co-expression Analysis Indicates Potential Pathways and Regulators of Beef Tenderness in Nellore Cattle vol.9, pp.1664-8021, 2018, https://doi.org/10.3389/fgene.2018.00441
  6. Integrated analysis of lncRNA and mRNA expression in rainbow trout families showing variation in muscle growth and fillet quality traits vol.8, pp.1, 2018, https://doi.org/10.1038/s41598-018-30655-8
  7. Does altered protein metabolism interfere with postmortem degradation analysis for PMI estimation? vol.132, pp.5, 2018, https://doi.org/10.1007/s00414-018-1814-8
  8. The impact of muscle and aging time on meat tenderness in the carcasses of Limousin × Holstein-Friesian crossbred bulls vol.42, pp.6, 2018, https://doi.org/10.1111/jfpp.13619
  9. A comprehensive transcriptome analysis of skeletal muscles in two Polish pig breeds differing in fat and meat quality traits vol.41, pp.1, 2018, https://doi.org/10.1590/1678-4685-gmb-2016-0101
  10. Expression analyses of candidate genes related to meat quality traits in squabs from two breeds of meat-type pigeon vol.102, pp.3, 2018, https://doi.org/10.1111/jpn.12869
  11. MiRNAs differentially expressed in skeletal muscle of animals with divergent estimated breeding values for beef tenderness vol.20, pp.1, 2019, https://doi.org/10.1186/s12867-018-0118-3