Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Polish Journal of Food and Nutrition Sciences

The Journal of Institute of Animal Reproduction and Food Research of Polish Academy of Sciences in Olsztyn

4 Issues per year

IMPACT FACTOR 2016: 1.276

CiteScore 2016: 1.56

SCImago Journal Rank (SJR) 2016: 0.397
Source Normalized Impact per Paper (SNIP) 2016: 0.951

Open Access
See all formats and pricing
More options …

Enzymes in Tenderization of Meat - The System of Calpains and Other Systems - a Review

Dariusz Nowak
  • Department and Chair of Nutrition and Dietetics, Faculty of Health Science, Collegium Medicum, Nicholas Copernicus University, ul. Dębowa 3, 85-626 Bydgoszcz, Poland
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2011-10-21 | DOI: https://doi.org/10.2478/v10222-011-0025-5

Enzymes in Tenderization of Meat - The System of Calpains and Other Systems - a Review

Tenderness of meat is considered as the most important feature of meat quality. Three proteolytic systems present in a muscle were examined as those which can play a role in the postmortem proteolysis and tenderization: the system of calpains, lysosomal cathepsins and MCP (multicatalytic proteinase complex). There are several theories (enzymatic or non-enzymatic) explaining the tenderization process. The calpain theory of tenderization was recognized as the most probable. During tenderization the main structures of a cytoskeleton are degraded as well as myofibril and cytoskeletal proteins. Meat becomes soft and the process of tenderization is accompanied by changes in the ultrastructure (degradation of the Z-line and the I-band). Many studies show that the system of calpains (especially calpain I and calpastatin) plays a major role in postmortem proteolysis and meat tenderization. However, recent studies show that proteasomes and caspases may be responsible for this process as well. This paper includes the characterization of calpains as well as describes the construction and functioning of the system of calpains. Additionally, this article presents factors influencing the activity of calpains. It was also mentioned that other systems, such as proteasomes and caspases, may be involved in postmortem tenderization of meat.

Keywords: meat tenderization; calpain; calpastatin; system of calpains

  • Bernard C., Cassar-Malek I., Le Cunff M., Dubroeucq H., Renard G., Hocquette J. F., New indicators of beef sensory quality revealed by expression of specific genes. J. Agr. Food Chem., 2007, 55, 5229-5237.CrossrefGoogle Scholar

  • Boehm M. L., Kendall T. L., Thompson V. F., Goll D. E., Changes in the calpains and calpastatin during post mortem storage of bovine muscle. J. Anim. Sci., 1998, 76, 2415-2434.Google Scholar

  • Boleman S. J., Boleman S. L., Bidner T. D., Mc Millin K. W., Monlezun C. J., Effects of postmortem time of calcium chloride injection on beef tenderness and drip, cooking and total loss. Meat Sci., 1995, 39, 35-41.CrossrefPubMedGoogle Scholar

  • Boleman S. J., Boleman S. L., Miller R. K., Taylor J. F., Cross H. R., Wheeler T. L., Koohmaraie M., Shackelford S. D., Miller M. F., West R. L., Johnson D. D., Savell J. W., Consumer evaluation of beef of known categories of tenderness. J. Anim. Sci., 1997, 75, 1521-1524.Google Scholar

  • Camou J. P., Mares S. W., Marchello J. A., Vazquez R., Taylor M., Thompson V. F., Goll D. E., Isolation and characterization of μ-calpain, m-calpain, and calpastatin from postmortem muscle. I. Initial steps. J. Anim. Sci., 2007, 85, 3400-3414.Google Scholar

  • Carragher N. O., Frame M. C., Calpain: a role in cell transformation and migration. Int. J. Biochem. Cell Biol., 2002, 34, 1539-1543.CrossrefGoogle Scholar

  • Casas E., White S. N., Wheeler T. L., Shackelford S. D., Koohmaraie M., Riley D. G., Chase C. C., Johnson D. D., Smith T. P. L., Effects of calpastatin and μ-calpain markers in beef cattle on tenderness traits. J. Anim. Sci., 2006, 84, 520-525.Google Scholar

  • Chen L., Feng X. C., Lu F., Xu X. L., Zhou G. H., Li Q. Y., Guo X. Y., Effects of camptothecin, etoposide and Ca2+ on caspase-3 activity and myofibrillar disruption of chicken during postmortem ageing. Meat Sci., 2011, 87, 165-174.CrossrefPubMedGoogle Scholar

  • Dahlmann B., Ruppert T., Kloetzel P. M., Kuehn L., Subtypes of 20S proteasomes from skeletal muscle. Biochimie, 2001, 83, 295-299.CrossrefGoogle Scholar

  • Destefanis G., Brugiapaglia A., Barge M. T., Dal Molin E., Relationship between beef consumer tenderness perception and Warner-Bratzler shear force. Meat Sci., 2008, 78, 153-156.CrossrefPubMedGoogle Scholar

  • Dransfield E., Wakefield D. K., Parkman I. D., Modelling postmortem tenderisation - I: Texture of electrically stimulated and non-stimulated beef. Meat Sci., 1992a, 31, 57-73.PubMedCrossrefGoogle Scholar

  • Dransfield E., Etherington D. J., Taylor M. A. J., Modelling post-mortem tenderisation - II: Enzyme changes during storage of electrically stimulated and non-stimulated beef. Meat Sci., 1992b, 31, 75-84.PubMedCrossrefGoogle Scholar

  • Dransfield E., Modelling post-mortem tenderisation - III: Role of calpain I in conditioning. Meat Sci., 1992c, 31, 85-94.CrossrefPubMedGoogle Scholar

  • Dransfield E., Optimisation of tenderisation, ageing and tenderness. Meat Sci., 1994a, 36, 105-121.CrossrefPubMedGoogle Scholar

  • Dransfield E., Modelling post-mortem tenderisation - V: Inactivation of calpains. Meat Sci., 1994b, 37, 391-409.CrossrefGoogle Scholar

  • Dransfield E., Meat tenderness-the μ-calpain hypothesis. 1999, in: 45th ICoMST, pp. 220-228.Google Scholar

  • Dutaud D., Aubry L., Sentandreu M. A., Ouali A., Bovine muscle 20S proteasome: I. Simple purification procedure and enzymatic characterization in relation with postmortem conditions. Meat Sci., 2006, 74, 327-336.CrossrefGoogle Scholar

  • Feldkamp T. J., Schroeder T. C., Lusk J. L., Determining consumer valuation of differentiated beef steak quality attributes. J. Muscle Foods, 2005, 16, 1-15.CrossrefGoogle Scholar

  • Frylinck L., van Wyk G. L., Smith T. P. L., Strydom P. E., van Marle-Köster E., Webb E. C., Koohmaraie M., Smith M. F., Evaluation of biochemical parameters and genetic markers for association with meat tenderness in South African feedlot cattle. Meat Sci., 2009, 83, 657-665.CrossrefGoogle Scholar

  • Geesink G. H., Koohmaraie M., Postmortem proteolysis and calpain/calpastatin activity in callipyge and normal lamb biceps femoris during extended postmortem storage. J. Anim. Sci., 1999, 77, 1490-1501.Google Scholar

  • Geesink G. H., Taylor R. G., Bekhit A. E. D., Bickerstaffe R., Evidence against the non-enzymatic calcium theory of tenderization. Meat Sci., 2001, 59, 417-422.PubMedCrossrefGoogle Scholar

  • Geesink G. H., Taylor R. G., Koohmaraie M., Calpain 3/p94 is not involved in postmortem proteolysis. J. Anim. Sci., 2005, 83, 1646-1652.Google Scholar

  • Geesink G. H., Kuchay S., Chishti A. H., Koohmaraie M., μ-Calpain is essential for postmortem proteolysis of muscle proteins. J. Anim. Sci., 2006, 84, 2834-2840.Google Scholar

  • Goll D. E., Thompson V. F., Li H., Wei W., Cong J., The calpain system. Physiol. Rev., 2003, 83, 731-801.PubMedGoogle Scholar

  • Hanna R. A., Campbell R. L., Davies P. L., Calcium-bound structure of calpain and its mechanism of inhibition by calpastatin. Nature, 2008, 456, 409-412.PubMedCrossrefGoogle Scholar

  • Homma N., Ikeuchi Y., Suzuki A., Levels of calpain and calpastatin in meat subjected to high pressure. Meat Sci., 1995, 41, 251-260.PubMedCrossrefGoogle Scholar

  • Hope-Jones M., Strydom P. E., Frylinck L, Webb E. C., The efficiency of electrical stimulation to counteract the negative effects of β-agonists on meat tenderness of feedlot cattle. Meat Sci., 2010, 86, 699-705.CrossrefGoogle Scholar

  • Hopkins D. L., Thompson J. M., Inhibition of protease activity 2. Degradation of myofibrillar proteins, myofibril examination of free calcium levels. Meat Sci., 2001, 59, 199-209.PubMedGoogle Scholar

  • Houbak M. B., Ertbjerg P., Therkildsen M., In vitro study to evaluate the degradation of bovine muscle proteins post-mortem by proteasome and microcalpain. Meat Sci., 2008, 79, 77-85.CrossrefGoogle Scholar

  • 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 Chem., 2009, 115, 181-186.CrossrefGoogle Scholar

  • Huff-Lonergan E., Mitsuhashi T., Beekman D. D., Parrish F. C., Olson D. G., Robson R. M., Proteolysis of specific muscle structural proteins by μ-calpain at low pH and temperature is similar to degradation in post mortem bovine muscle. J. Anim. Sci., 1996, 74, 993-1008.Google Scholar

  • Hughes M. C., Geary S., Dransfield E., Mc Sweeney P. L. H., O'Neill E. E., Characterization of peptides released from rabbit skeletal muscle troponin-T by μ-calpain under conditions of low temperature and high ionic strength. Meat Sci., 2001, 59, 61-69.CrossrefPubMedGoogle Scholar

  • Hwang I. H., Thompson J. M., The effect of time and type of electrical stimulation on the calpain system and meat tenderness in beef longissimus dorsi muscle. Meat Sci., 2001, 58, 135-144.PubMedCrossrefGoogle Scholar

  • Ilian M. A., Morton J. D., Kent M. P., Le Couteur C. E., Hickford J., Cowley R., Bickerstaffe R., Intermuscular variation in tenderness: Association with the ubiquitous and muscle-specific calpains. J. Anim. Sci. 2001, 79, 122-132.Google Scholar

  • Ilian M. A., Bekhit A. E., Bickerstaffe R., The relationship between meat tenderization, myofibril fragmentation and autolysis of calpain 3 during post-mortem ageing. Meat Sci., 2004a, 66, 387-397.PubMedCrossrefGoogle Scholar

  • Ilian M. A., Bekhit A. E., Stevenson B., Morton J. D., Isherwood P., Bickerstaffe R., Up- and down- regulation of longissimus tenderness parallels changes in the myofibril-bound calpain 3 protein. Meat Sci., 2004b, 67, 433-445.PubMedCrossrefGoogle Scholar

  • Ilian M. A., Bickerstaffe R., Greaser M. L., Postmortem changes in myofibrillar-bound calpain 3 revealed by immunofluorescence microscopy. Meat Sci. 2004c, 66, 231-240.CrossrefPubMedGoogle Scholar

  • Jakubiec-Puka A., The role of proteolytic calpain system in animal cell. Post. Biochem., 1993, 39, 251-258 (in Polish).Google Scholar

  • Jeacocke R. E., The concentrations of free magnesium and free calcium ions both increase in skeletal muscle fibres entering rigor mortis. Meat Sci., 1993, 35, 27-45.CrossrefPubMedGoogle Scholar

  • Kanawa R., Ji J.-R., Takahashi K., Inactivity of μ-calpain throughout post mortem aging of meat. J. Food Sci., 2002, 67, 635-638.CrossrefGoogle Scholar

  • 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. J. Anim. Sci., 2006, 84, 2841-2846.Google Scholar

  • Kemp C. M., Sensky P. L., Bardsley R. G., Buttery P. J., Parr T., Tenderness - An enzymatic view. Meat Sci., 2010, 84, 248-256.CrossrefPubMedGoogle Scholar

  • Kent M. P., Spencer M. J., Koohmaraie M., Postmortem proteolysis is reduced in transgenic mice overexpressing calpastatin. J. Anim. Sci., 2004, 82, 794-801.Google Scholar

  • Kołczak T., Influence postmortem factors on beef tenderness. Gosp. Mięsna, 2000, 5, 28-31 (in Polish).Google Scholar

  • Koohmaraie M., The role of endogenous proteases in meat tenderness. 1988, in: Proceedings of 41st Annual Reciprocal Meat Conference, Wyoming, USA, pp. 89-100.Google Scholar

  • Koohmaraie M., The role of Ca+2 - dependent proteases (calpains) in post mortem proteolysis and meat tenderness. Biochimie, 1992, 74, 239-245.CrossrefGoogle Scholar

  • Koohmaraie, M., Ovine skeletal muscle multicatalytic proteinase complex (proteasome): purification, characterization, and comparison of its effect on myofibrils with μ-calpain. J. Anim. Sci., 1992b, 70, 3697-3708.Google Scholar

  • Koohmaraie M., Muscle proteinases and meat ageing. Meat Sci., 1994, 36, 93-104.PubMedCrossrefGoogle Scholar

  • Koohmaraie M., Biochemical factors regulating the toughening and tenderisation processes of meat. Meat Sci., 1996, 43, 193-201.CrossrefGoogle Scholar

  • Koohmaraie M., Kent M. P., Shackelford S. D., Veiseth E., Wheeler T. L., Meat tenderness and muscle growth: is there any relationship? Meat Sci., 2002, 62, 345-352.PubMedCrossrefGoogle Scholar

  • 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 Sci., 2006, 74, 34-43.CrossrefPubMedGoogle Scholar

  • Korzeniewska-Dyl I., Caspases - structure and function. Pol. Merk. Lek., 2007, 138, 403-407 (in Polish).Google Scholar

  • Korzeniowski W., Nowak D., Ostoja H., The role of proteolytic enzymes to improve the meat tenderness. Gosp. Mięsna, 1998, 8, 40-43 (in Polish).Google Scholar

  • Kumamoto T., Kleese W. C., Cong J., Goll D. E., Pierce P. R., Allen R. E., Localization of the Ca+2 - dependent proteinases and their inhibitor in normal, fasted and denervated rat skeletal muscle. Anat. Rec., 1992, 232, 60-77.CrossrefPubMedGoogle Scholar

  • Kurebayashi N., Harkins A. B., Baylor S.,M., Use of fura red as an intracellular calcium indicator in frog skeletal muscle fibers. Biophys. J., 1993, 64, 1934-1960.Google Scholar

  • Lee S., Polidori P., Kaufman R. G., Kim B. C., Low-voltage electrical stimulation effects on proteolysis and lamb tenderness. J. Food Sci., 2000, 65, 786-790.CrossrefGoogle Scholar

  • Lusk J. L., Fox J. A., Schroeder T. C., Mintert J., Koohmaraie M., In-store valuation of steak tenderness. Am. J. Agr. Econ., 2001, 83, 539-550.Google Scholar

  • Maribo H., Ertbjerg P., Andersson M., Barton-Gade P., Møller A. J., Electrical stimulation of pigs - effect on pH fall, meat quality and Cathepsin B+L activity. Meat Sci., 1999, 52, 179-187.PubMedCrossrefGoogle Scholar

  • Meyers S. N., Beever J. E., Investigating the genetic basis of pork tenderness: Genomic analysis of porcine CAST. Anim. Genet., 2008, 39, 531-543.Google Scholar

  • Miller M. F., Carr M. F., Ramsey C. B., Crockett K. L., Hoover L. C., Consumer thresholds for establishing the value of beef tenderness. J. Anim. Sci., 2001, 79, 3062-3068.Google Scholar

  • Moldoveanu T., Gehring K., Green D. R., Concerted multi-pronged attack by calpastatin to occlude the catalytic cleft of heterodimeric calpains. Nature, 2008, 456, 404-408.Google Scholar

  • Moudilou E. N., Mouterfi N., Exbrayat J. M., Brun C., Calpains expression during Xenopus laevis development. Tissue Cell, 2010, 42, 275-281.CrossrefGoogle Scholar

  • Morgan J. B., Miller R. K., Mendez F. M., Hale D. S., Savell J. W., Using calcium chloride injection to improve tenderness of beef from mature cows. J. Anim. Sci., 1991, 69, 4469-4476.Google Scholar

  • Morton J. D., Bickerstaffe R., Kent M. P., Dransfield E., Keeley G. M., Calpain-calpastatin and toughness in M. Longissimus from electrically stimulated lamb and beef carcasses. Meat Sci., 1999, 52, 71-79.CrossrefGoogle Scholar

  • Neath K. E., Del Barrio A. N., Lapitan R. M., Herrera J. R. V., Cruz L. C., Fujihara T., Muroya S., Chikuni K., Hirabayashi M., Kanai Y., Protease activity higher in postmortem water buffalo meat than Brahman beef. Meat Sci., 2007, 77, 389-396.PubMedCrossrefGoogle Scholar

  • Northcutt J. K., Pringle T. D., Dickens J. A., Buhr R. J., Young L. L., Effects of age and tissue type on the calpain proteolytic system in turkey skeletal muscle. Poultry Sci., 1998, 77, 367-372.Google Scholar

  • Nowak D., Korzeniowski W., Influence modified conditions of ripening on meat tenderness and structural changes in skeletal muscle. Fleischwirtschaft, 2004, 10, 100-103 (in German, English abstract).Google Scholar

  • Nowak D., Methods for improving the tenderness of beef - influence metal ions and temperatures. Fleischwirtschaft, 2005, 11, 109-111 (in German, English abstract).Google Scholar

  • Olsson U., Hertzman C., Tornberg E., The influence of low temperature, type of muscle and electrical stimulation on the course of rigor mortis, ageing and tenderness of beef muscles. Meat Sci., 1994, 37, 115-131.CrossrefPubMedGoogle Scholar

  • Ouali A., Hernan Herrera-Mendez C., Coulis G., Becila S., Boudjellal A., Aubry L., Sentandreu M. A., Revisiting the conversion of muscle into meat and the underlying mechanisms. Meat Sci., 2006, 74, 44-58.PubMedCrossrefGoogle Scholar

  • Parr T., Sensky P. L., Scothern G. P., Bardsley R. G., Buttery P. J., Wood J. D., Warkup C., Relationship between skeletal muscle - specific calpain and tenderness of conditioned porcine longissimus muscle. J. Anim. Sci., 1999, 77, 661-668.Google Scholar

  • Purslow P. P., Ertbjerg P., Baron C. P., Christensen M., Lawson M. A., Patterns of variation in enzyme activity and cytoskeletal proteolysis in muscle. 2001, in: 47th ICoMST, pp. 38-43.Google Scholar

  • Rees M. P., Trout G. R., W arner R. D., Effect of calcium infusion on tenderness and ageing rate of pork m. longissimus thoracis et lumborum after accelerated boning. Meat Sci., 2002, 61, 169-179.CrossrefGoogle Scholar

  • Sentandreu M. A., Coulis G., Ouali A., Role of muscle endopeptidases and their inhibitors in meat tenderness. Trends Food Sci. Tech., 2002, 13, 400-421.CrossrefGoogle Scholar

  • Shackelford S. D., Wheeler T. L., Meade M. K., Reagan J. O., Byrnes B. L., Koohmaraie M., Consumer impressions of Tender Select beef. J. Anim. Sci., 2001, 79, 2605-2614.Google Scholar

  • Soares G. J. D., Areas J. A. G., Effect of electrical stimulation on post mortem biochemical characteristics and quality of longissimus dorsi thoracis muscle from buffalo (Bubalus bubalis). Meat Sci., 1995, 41, 369-379.CrossrefGoogle Scholar

  • Steen D., Claeys E., Uytterhaegen L., De Smet S., Demeyer D., Early post-mortem conditions and the calpain/calpastatin system in relation to tenderness of double-muscled beef. Meat Sci., 1997, 45, 307-319.PubMedCrossrefGoogle Scholar

  • Takahashi K., Structural weakening of skeletal muscle tissue during post-mortem ageing of meat: the non-enzymatic mechanism of meat tenderization. Meat Sci., 1996, 43, 67-80.CrossrefGoogle Scholar

  • Taylor R. G., Geesing G. H., Thompson V. F., Koohmaraie M., Goll D. E., Is Z-disk degradation responsible for post mortem tenderization? J. Anim. Sci., 1995a, 73, 1351-1367.Google Scholar

  • Taylor R. G., Tassy C., Briand M., Robert N., Briand Y., Ouali A., Proteolytic activity of proteasome on myofibrillar structures. Mol. Biol. Rep., 1995b, 21, 71-73.PubMedCrossrefGoogle Scholar

  • Thomson B. C., Dobbie P. M., Singh K., Speck P. A., Post-mortem kinetics of meat tenderness and the components of the calpain system in bull skeletal muscle. Meat Sci., 1996, 44, 151-157.PubMedCrossrefGoogle Scholar

  • Tornberg E., Biophysical aspects of meat tenderness. Meat Sci., 43, 1996, 175-191.Google Scholar

  • Veeramuthu G. I., Sams A. R., Post mortem pH, myofibrillar fragmentation, and calpain activity in Pectoralis from electrically stimulated and muscle tensioned broiler carcasses. Poultry Sci., 1999, 78, 272-276.Google Scholar

  • Whipple G., Koohmaraie M., Degradation of myofibril proteins by extractable lysosomal enzymes and m-calpain, and the effects of zinc chloride. J. Anim. Sci., 1991, 69, 4449-4460.Google Scholar

  • White S. N., Casas E., Wheeler T. L., Shackelford S. D., Koohmaraie M., Riley D. G., Chase C. C., Johnson D. D., Keele J. W., Smith T. P. L., 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., 2005, 83, 2001-2008.Google Scholar

  • Xian-Xing Xu, Xue Shui, Zhi-Hang Chen, Cheng-Qi Shan, Yu-Nan Hou, Yuan-Guo Cheng, Development and application of a real-time PCR method for pharmacokinetic and biodistribution studies of recombinant adenovirus. Mol Biotechnol., 2009, 43, 130-137.Google Scholar

  • Zór K., Ortiz R., Saatci E., Bardsley R., Parr T., Csöregi E., Nistor M., Label free capacitive immunosensor for detecting calpastatin - a meat tenderness biomarker. Bioelectrochemistry, 2009, 76, 93-99.PubMedCrossrefGoogle Scholar

About the article

Published Online: 2011-10-21

Published in Print: 2011-12-01

Citation Information: Polish Journal of Food and Nutrition Sciences, Volume 61, Issue 4, Pages 231–237, ISSN (Online) 2083-6007, ISSN (Print) 1230-0322, DOI: https://doi.org/10.2478/v10222-011-0025-5.

Export Citation

This content is open access.

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

Changyu Zhou, Ying Wang, Daodong Pan, Yangying Sun, and Jinxuan Cao
Food Research International, 2016, Volume 90, Page 1
Alessandro Lana and Lello Zolla
Trends in Food Science & Technology, 2015, Volume 46, Number 2, Page 231

Comments (0)

Please log in or register to comment.
Log in