Scientia Agricultura Sinica ›› 2011, Vol. 44 ›› Issue (15): 3214-3222.doi: 10.3864/j.issn.0578-1752.2011.15.017

• STORAGE·FRESH-KEEPING·PROCESSING • Previous Articles     Next Articles

Advances in Research on Postmortem Tenderization Mechanism of Endogenous Proteolytic Enzymes in Muscle

HUANG  Ming, HUANG  Feng, HUANG  Ji-Chao, XU  Bao-Cai, ZHOU  Guang-Hong, XU  Xing-Lian   

  1. 1. 南京农业大学食品科技学院/教育部肉品加工与质量控制重点实验室
    2. 雨润集团肉品加工与质量控制国家重点实验室
  • Received:2010-10-29 Revised:2011-05-20 Online:2011-08-01 Published:2011-05-25

Abstract: The mechanism of postmortem tenderization of muscle has been the focus of meat science for years. It is generally accepted that improvement of meat tenderness during postmortem aging mainly results from limited degradation of myofibrillar proteins by endogenous proteolytic enzymes. Calpains are widely considered to be a major contributor, but not only ones to postmortem improvement of meat tenderness, which is the result of multi-enzymatic interaction. The roles of lysosomal cathepsins, proteasomes and calpains during postmortem tenderization of meat were briefly reviewed in the paper. The characteristics of apoptosis, activating pathways and caspases were introduced, meanwhile the potential contribution of caspases to postmortem tenderization was also discussed. In the last, the possibilities of interactions between caspases and calpains and contribution of both proteases together to meat tenderization were also analyzed in the review.

Key words: postmortem tenderization, calpains, apoptosis, caspases, interaction

[1]Shackelford S D, Wheeler T L, Meade M K, Reagan J O, Koohmaraie M. Consumer impressions of tender select beef. Journal of Animal Science, 2001, 79(10): 2605-2614.

[2]汤晓艳, 周光宏, 徐幸莲, 杨曙明, 钱永忠, 叶志华. 肉嫩度决定因子及牛肉嫩化技术研究进展. 中国农业科学, 2007,  40(12): 2835-2841.

Tang X Y, Zhou G H, Xu X L, Yang S M, Qian Y Z, Ye Z H. Advances of research on factors affecting meat tenderness and techniques for beef tenderization. Scientia Agricultura Sinica, 2007, 40(12): 2835-2841. (in Chinese)

[3]Koohmaraie M, Kent M P, Shackelford S D, Veiseth E, Wheeler T L. Meat tenderness and muscle growth: is there any relationship?. Meat Science, 2002, 62(3): 345-352.

[4]Koohmaraie M, Geesink G H. Contribution of postmortem muscle biochemistry to the delivery of consistent meat quality with particular focus on the calpain system. Meat Science, 2006, 74(1): 34-43.

[5]Hopkins D, Thompson J. The degradation of myofibrillar proteins in beef and lamb using denaturing electrophoresis-An overview. Journal of Muscle Foods, 2002, 13(2): 81-102.

[6]Koohmaraie M. Biochemical factors regulating the toughening and tenderization processes of meat. Meat Science, 1996, 43(Suppl. 1): 193-201.

[7]Ouali A, Herrera-Mendez C H, Coulis G, Becila S, Boudjellal A, Sentandreu M A. Revisiting the conversion of muscle into meat and the underlying mechanisms. Meat Science, 2006, 74(1): 44-58.

[8]Herrera-Mendez C H, Becila S, Boudjellal A, Ouali A. Meat ageing: Reconsideration of the current concept. Trends in Food Science and Technology, 2006, 17(8): 394-405.

[9]黄  明, 赵  莲, 徐幸莲, 周光宏. 钙离子和钙激活酶外源抑制剂对牛肉钙激活酶活性和超微结构的影响. 南京农业大学学报, 2004, 27(4): 101-104.

Huang M, Zhao L, Xu X L, Zhou G H. Effects of calcium ion and exogenous calpains inhibitors on calpains activity and ultrastructure of beef. Journal of Nanjing Agricultural University, 2004, 27(4): 101-104. (in Chinese)

[10]Goll D E, Otsuka Y, Nagainis P A, Shannon J D, Sathe S K, Muguruma M. Role of muscle proteinases in maintenance of muscle integrity and mass. Journal of Food Biochemistry, 1983, 7(3): 137-177.

[11]Costelli P, Reffo P, Penna F, Autelli R, Bonelli G, Baccino F M. Ca2+-dependent proteolysis in muscle wasting. The International Journal of Biochemistry and Cell Biology, 2005, 37(10): 2134-2146.

[12]Sentandreu M A, Coulis G, Ouali A. Role of muscle endopeptidases and their inhibitors in meat tenderness. Trends in Food Science and Technology, 2002, 13(12): 400-421.

[13]Uytterhaegen L, Claeys E, Demeyer D. Effects of exogenous protease effectors on beef tenderness development and myofibrillar degradation and solubility. Journal of Animal Science, 1994, 72(5): 1209-1223.

[14]Whipple G, Koohmaraie M. Degradation of myofibrillar proteins by extractable lysosomal enzymes and m-calpain, and the effects of zinc chloride. Journal of Animal Science, 1991, 69(11): 4449-4460.

[15]Whipple G, Koohmaraie M, Dikeman M, Crouse J, Hunt M, Klemm R. Evaluation of attributes that affect longissimus muscle tenderness in Bos taurus and Bos indicus cattle. Journal of Animal Science, 1990, 68(9): 2716-2728.

[16]Koohmaraie M, Babiker A S, Merkel R A, Dutson T R. Role of Ca2+-dependent proteases and lysosomal enzymes in postmortem changes in bovine skeletal muscle. Journal of Food Science, 1988, 53(5): 1253-1257.

[17]Kubo T, Gerelt B, Han G D, Sugiyama T, Nishiumi T, Suzuki A. Changes in immunoelectron microscopic localization of cathepsin D in muscle induced by conditioning or high-pressure treatment. Meat Science, 2002, 61(4): 415-418.

[18]O'Halloran G R, Troy D J, Buckley D J, Reville W J. The role of endogenous proteases in the tenderisation of fast glycolysing muscle. Meat Science, 1997, 47(3/4): 187-210.

[19]Kemp C M, Sensky P L, Bardsley R G, Parr T. Tenderness - An enzymatic view. Meat Science, 2010, 84(2): 248-256.

[20]Jung S, Ghoul M, de Lamballerie-Anton M. Changes in lysosomal enzyme activities and shear values of high pressure treated meat during ageing. Meat Science, 2000, 56(3): 239-246.

[21]Calkins C, Seideman S. Relationships among calcium-dependent protease, cathepsins B and H, meat tenderness and the response of muscle to aging. Journal of Animal Science, 1988, 66(5): 1186-1193.

[22]Ouali A. Proteolytic and physicocohemical mechanisms involved in meat texture development. Biochimie, 1992, 74(3): 251-265.

[23]Baron C P, Jacobsen S, Purslow P P. Cleavage of desmin by cysteine proteases: Calpains and cathepsin B. Meat Science, 2004, 68(3): 447-456.

[24]Adams J. The proteasome: structure, function, and role in the cell. Cancer Treatment Reviews, 2003, 29(Suppl.): 3-9.

[25]Koohmaraie M. The role of Ca2+-dependent proteases (calpains) in post mortem proteolysis and meat tenderness. Biochimie, 1992, 74(3): 239-245.

[26]Dutaud D, Aubry L, Guignot F, Vignon X, Monin G. Bovine muscle 20S proteasome. II: Contribution of the 20S proteasome to meat tenderization as revealed by an ultrastructural approach. Meat Science, 2006, 74(2): 337-344.

[27]Peters J M, Franke W W, Kleinschmidt J A. Distinct 19 S and 20 S subcomplexes of the 26 S proteasome and their distribution in the nucleus and the cytoplasm. The Journal Biological Chemistry, 1994, 269(10): 7709-7718.

[28]Robert N, Briand M, Taylor R, Briand Y. The effect of proteasome on myofibrillar structures in bovine skeletal muscle. Meat Science, 1999, 51(2): 149-153.

[29]Lamare M, Taylor R G, Farout L, Briand Y, Briand M. Changes in proteasome activity during postmortem aging of bovine muscle. Meat Science, 2002, 61(2): 199-204.

[30]Geesink G H, Taylor R G, Koohmaraie M. Calpain 3/p94 is not involved in postmortem proteolysis. Journal of Animal Science, 2005, 83(7): 1646-1652.

[31]Geesink G H, Kuchay S, Chishti A H, Koohmaraie M. Micro-calpain is essential for postmortem proteolysis of muscle proteins. Journal of Animal Science, 2006, 84(10): 2834-2840.

[32]Kent M P, Spencer M J, Koohmaraie M. Postmortem proteolysis is reduced in transgenic mice overexpressing calpastatin. Journal Animal Science, 2004, 82(3): 794-801.

[33]Huff-Lonergan E, Mitsuhashi T, Beekman D D, Parrish F C, Jr., Olson D G, Robson R M. Proteolysis of specific muscle structural proteins by mu-calpain at low pH and temperature is similar to degradation in postmortem bovine muscle. Journal of Animal Science, 1996, 74(5): 993-1008.

[34]Geesink G H, Koohmaraie M. Effect of calpastatin on degradation of myofibrillar proteins by mu-calpain under postmortem conditions. Journal of Animal Science, 1999, 77(10): 2685-2692.

[35]Koohmaraie M, Whipple G, Kretchmar D, Crouse J, Mersmann H. Postmortem proteolysis in longissimus muscle from beef, lamb and pork carcasses. Journal of Animal Science, 1991, 69(2): 617-624.

[36]Camou J P, Marchello J A, Thompson V F, Mares S W, Goll D E. Effect of postmortem storage on activity of µ- and m-calpain in five bovine muscles. Journal of Animal Science, 2007, 85(10): 2670-2681.

[37]Morgan J B, Wheeler T L, Koohmaraie M, Savell J W, Crouse J D. Meat tenderness and the calpain proteolytic system in longissimus muscle of young bulls and steers. Journal of Animal Science, 1993, 71(6): 1471-1476.

[38]Hopkins D, Thompson J. Factors contributing to proteolysis and disruption of myofibrillar proteins and the impact on tenderisation in beef and sheep meat. Australian Journal of Agricultural Research, 2002, 53(2): 149-166.

[39]Park K M, Pramod A B, Kim J H, Choe H S, Hwang I H. Molecular and biological factors affection skeletal muscle cells after slaughtering and their impact on meat quality: a mini-review. Journal of Muscle Foods, 2010, 21(1): 280-307.

[40]Bhatia M. Apoptosis versus necrosis in acute pancreatitis. American Journal of Physiology Gastrointestinal and Liver Physiology, 2004, 286(2): 189-196.

[41]Wang K K. Calpain and caspase: can you tell the difference?. Trends in Neurosciences, 2000, 23(1): 20-26.

[42]Fadeel B, Orrenius S. Apoptosis: a basic biological phenomenon with wide-ranging implications in human disease. Journal of Internal Medicine, 2005, 258(6): 479-517.

[43]McConkey D. Biochemical determinants of apoptosis and necrosis. Toxicology letters, 1998, 99(3): 157-168.

[44]Adams J M. Ways of dying: multiple pathways to apoptosis. Genes and Development, 2003, 17(20): 2481-2495.

[45]Gupta S, Gollapudi S. Susceptibility of naïve and subsets of memory T cells to apoptosis via multiple signaling pathways. Autoimmunity Reviews, 2007, 6(7): 476-481.

[46]Brunelle J K, Chandel N S. Oxygen deprivation induced cell death: an update. Apoptosis, 2002, 7(6): 475-482.

[47]Becila S, Herrera-Mendez C, Coulis G, Labas R, Astruc T, Picard B, Boudjellal A, Pelissier P, Bremaud L. Postmortem muscle cells die through apoptosis. European Food Research and Technology, 2010, 231(3): 485-493.

[48]Kemp C M, Parr T, Bardsley R G, Buttery P J. Comparison of the relative expression of caspase isoforms in different porcine skeletal muscles. Meat Science, 2006, 73(3): 426-431.

[49]Kemp C M, Bardsley R G, Parr T. Changes in caspase activity during the postmortem conditioning period and its relationship to shear force in porcine longissimus muscle. Journal of Animal Science, 2006, 84(10): 2841-2846.

[50]Bernard C, Cassar-Malek I, Le Cunff M, Dubroeucq H, Renand G, Hocquette J. New indicators of beef sensory quality revealed by expression of specific genes. Journal of Agricultural and Food Chemistry, 2007, 55(13): 5229-5237.

[51]Underwood K R, Means W J, Du M. Caspase 3 is not likely involved in the postmortem tenderization of beef muscle. Journal of Animal Science, 2008, 86(4): 960-966.

[52]Kemp C, Parr T. The effect of recombinant caspase 3 on myofibrillar proteins in porcine skeletal muscle. Animal, 2008, 2(8): 1254-1264.

[53]Huang M, Huang F, Xu X L, Zhou G H. Influence of caspase3 selective inhibitor on proteolysis of chicken skeletal muscle proteins during post mortem aging. Food Chemistry, 2009, 115(1): 181-186.

[54]Harwood S M, Yaqoob M M, Allen D A. Caspase and calpain function in cell death: bridging the gap between apoptosis and necrosis. Annals of Clinical Biochemistry, 2005, 42(6): 415-431.

[55]Neumar R, Xu Y, Gada H, Guttmann R, Siman R. Cross-talk between calpain and caspase proteolytic systems during neuronal apoptosis. The Journal of Biological Chemistry, 2003, 278(16): 14162-14167.

[56]Chua B T, Guo K, Li P. Direct cleavage by the calcium-activated protease calpain can lead to inactivation of caspases. The Journal of Biological Chemistry, 2000, 275(7): 5131-5135.

[57]Hwang I H, Park B Y, Cho S H, Lee J M. Effects of muscle shortening and proteolysis on Warner-Bratzler shear force in beef longissimus and semitendinosus. Meat Science, 2004, 68(3): 497-505.

[58]Pörn-Ares M, Samali A, Orrenius S. Cleavage of the calpain inhibitor, calpastatin, during apoptosis. Cell Death and Differentiation, 1998, 5(12): 1028-1033.

[59]Blomgren K, Zhu C, Wang X, Karlsson J O, Leverin A L, Bahr B. A, Mallard C, Hagberg H. Synergistic activation of Caspase-3 by m-Calpain after neonatal Hypoxia-Ischemia. Journal of Biological Chemistry, 2001, 276(13): 10191-10198.

[60]McGinnis K, Gnegy M, Park Y, Mukerjee N, Wang K. Procaspase-3 and poly (ADP) ribose polymerase (PARP) are calpain substrates. Biochemical and Biophysical Research, 1999, 263(1): 94-99.

[61]Boehm M L, Kendall T L, Thompson V F, Goll D E. Changes in the calpains and calpastatin during postmortem storage of bovine muscle. Journal of Animal Science, 1998, 76(9): 2415-2434.

[62]Delgado E F, Geesink G H, Marchello J A, Goll D E. Properties    of myofibril-bound calpain activity in longissimus muscle of  callipyge and normal sheep. Journal of Animal Science, 2001, 79(8): 2097-2107.
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