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Original Articles

Serine Protease Inhibitors as Good Predictors of Meat Tenderness: Which Are They and What Are Their Functions?

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REFERENCES

  • Archibald, A. L., Couperwhite, S., Mellink, C. H., Lahbib-Mansais, Y. and Gellin, J. (1996). Porcine alpha-1-antitrypsin (PI): cDNA sequence, polymorphism and assignment to chromosome 7q2.4- > q2.6. Anim. Genet. 27:85–89.
  • Arrigo, A. P. (2005). Heat shock proteins as molecular chaperones. M S-Med. Sci. 21:619–625.
  • Baker, J. B., Low, D. A., Simmer, R. L. and Cunningham, D. D. (1980). Protease-nexin: A cellular component that links thrombin and plasminogen activator and mediates their binding to cells. Cell. 21:37–45.
  • Becila, S., Herrera-Mendez, C. H., Coulis, G., Labas, R., Astruc, T., Picard, B., Boudjellal, A., Pelissier, P., Bremaud, L. and Ouali, A. (2010). Postmortem muscle cells die through apoptosis. Eur. Food Res. Technol. 231:485–493.
  • Beere, H. M. (2005). Death versus survival: Functional interaction between the apoptotic and stress-inducible heat shock protein pathways. J. Clin. Invest. 115:2633–2639.
  • Bevers, E. M., Comfurius, P. and Zwaal, R. F. (1996). Regulatory mechanisms in maintenance and modulation of transmembrane lipid asymmetry: Pathophysiological implications. Lupus. 5:480–487.
  • Bieth, J. G. (1980). Pathophysiological interpretation of kinetic constants of protease inhibitors. Bull. Eur. Physiopathol. Respir. 16:183–197.
  • Bige, L., Ouali, A. and Valin, C. (1985). Purification and characterization of a low molecular weight cysteine proteinase inhibitor from bovine muscle. Biochim. Biophys. Acta. 843:269–275.
  • Billingsley, G. D., Walter, M. A., Hammond, G. L. and Cox, D. W. (1993). Physical mapping of four serpin genes: Alpha 1-antitrypsin, alpha 1-antichymotrypsin, corticosteroid-binding globulin, and protein C inhibitor, within a 280-kb region on chromosome I4q32.1. Am. J. Hum. Genet. 52:343–353.
  • Blanchet, X., Pere-Brissaud, A., Duprat, N., Pinault, E., Delourme, D., Ouali, A., Combet, C., Maftah, A., Pelissier, P. and Bremaud, L. (2012). Mutagenesis of the bovSERPINA3-3 demonstrates the requirement of aspartate-371 for intermolecular interaction and formation of dimers. Protein Sci. 21:977–986.
  • Businaro, R., Nori, S. L., Toesca, A., De Renzis, G., Ortolani, F., De Santis, E. and Fumagalli, L. (1995). Immunohistochemical detection of three serum protease inhibitors in mouse skeletal muscle by confocal laser scanning microscopy. Ital. J. Anat. Embryol. 100 Suppl 1:123–130.
  • Cassens, U., Lewinski, G., Samraj, A. K., von Bernuth, H., Baust, H., Khazaie, K. and Los, M. (2003). Viral modulation of cell death by inhibition of caspases. Arch. Immunol. Ther. Exp. (Warsz). 51:19–27.
  • Cavanaugh, K. P., Gurwitz, D., Cunningham, D. D. and Bradshaw, R. A. (1990). Reciprocal modulation of astrocyte stellation by thrombin and protease nexin-1. J. Neurochem. 54:1735–1743.
  • Chinni, C., de Niese, M. R., Tew, D. J., Jenkins, A. L., Bottomley, S. P. and Mackie, E. J. (1999). Thrombin, a survival factor for cultured myoblasts. J. Biol. Chem. 274:9169–9174.
  • Citron, B. A., Smirnova, I. V., Zoubine, M. N. and Festoff, B. W. (1997). Quantitative PCR analysis reveals novel expression of prothrombin mRNA and regulation of its levels in developing mouse muscle. Thromb. Res. 87:303–313.
  • De Duve, C., Pressman, B. C., Gianetto, R., Wattiaux, R. and Appelmans, F. (1955). Tissue fractionation studies. 6. Intracellular distribution patterns of enzymes in rat-liver tissue. Biochem. J. 60:604–617.
  • Dean, E. J., Ranson, M., Blackhall, F., Holt, S. V. and Dive, C. (2007). Novel therapeutic targets in lung cancer: Inhibitor of apoptosis proteins from laboratory to clinic. Cancer Treat. Rev. 33:203–212.
  • Deveraux, Q. L. and Reed, T. C. (1999). IAP family proteins - suppressors of apoptosis. Genes Dev. 13:239–252.
  • Dobo, J., Swanson, R., Salvesen, G. S., Olson, S. T. and Gettins, P. G. (2006). Cytokine response modifier a inhibition of initiator caspases results in covalent complex formation and dissociation of the caspase tetramer. J. Biol. Chem. 281:38781–38790.
  • Dutaud, D., Aubry, L., Sentandreu, M. A. and Ouali, A. (2006). Bovine Muscle 20s Proteasome: I. Simple Purification Procedure and Enzymatic Characterization in Relation With Postmortem Conditions. Meat. Sci. 74:337–344.
  • Elliott, P. R., Pei, X. Y., Dafforn, T. R. and Lomas, D. A. (2000). Topography of a 2.0 A structure of alpha1-antitrypsin reveals targets for rational drug design to prevent conformational disease. Protein Sci. 9:1274–1281.
  • Engh, R., Lobermann, H., Schneider, M., Wiegand, G., Huber, R. and Laurell, C. B. (1989). The S variant of human alpha 1-antitrypsin, structure and implications for function and metabolism. Protein Eng. 2:407–415.
  • Farrell, D. H., Van Nostrand, W. E. and Cunningham, D. D. (1986). A simple two-step purification of protease nexin. Biochem. J. 237:907–912.
  • Fenton, J. W. (1986). Thrombin. Ann. NY Acad. Sci. 485:5–15.
  • Forsyth, S., Horvath, A. and Coughlin, P. (2003). A review and comparison of the murine alpha1-antitrypsin and alpha1-antichymotrypsin multigene clusters with the human clade A serpins. Genomics. 81:336–345.
  • Fuentes-Prior, P. and Salvesen, G. S. (2004). The protein structures that shape caspase activity, specificity, activation and inhibition. Biochem. J. 384:201–232.
  • Gagaoua, M., Boudida, Y., Becila, S., Picard, B., Boudjellal, A., Sentandreu, M. A. and Ouali, A. (2012). New Caspases’ inhibitors belonging to the serpin superfamily: A novel key control point of apoptosis in mammalian tissues. Adv. Biosci. Biotechnol. 3(6):740–750.
  • Gettins, P. G. (2002). Serpin structure, mechanism, and function. Chem. Rev. 102:4751–4804.
  • Grand, R. J., Grabham, P. W., Gallimore, M. J. and Gallimore, P. H. (1989). Modulation of morphological differentiation of human neuroepithelial cells by serine proteases: Independence from blood coagulation. Embo. J. 8:2209–2215.
  • Guroff, G. (1964). A Neutral, Calcium-activated Proteinase from the Soluble Fraction of Rat Brain. J. Biol. Chem. 239:149–155.
  • Gurwitz, D. and Cunningham, D. D. (1988). Thrombin modulates and reverses neuroblastoma neurite outgrowth. Proc. Natl. Acad. Sci. U S A. 85:3440–3444.
  • Guttridge, D. C., Lau, A., Tran, L. and Cunningham, D. D. (1997). Thrombin causes a marked delay in skeletal myogenesis that correlates with the delayed expression of myogenin and p21CIP1/WAF1. J. Biol. Chem. 272:24117–24120.
  • Herrera-Mendez, C. H., Becila, S., Blanchet, X., Pelissier, P., Delourme, D., Coulis, G., Sentandreu, M. A., Boudjellal, A., Bremaud, L. and Ouali, A. (2009). Inhibition of human initiator caspase 8 and effector caspase 3 by cross-class inhibitory bovSERPINA3-1 and A3-3. FEBS Lett. 583:2743–2748.
  • Herrera-Mendez, C. H., Becila, S., Boudjellal, A. and Ouali, A. (2006a). Meat ageing : Reconsideration of the current concept. Trends Food Sci. Technol. 17:394–405.
  • Herrera-Mendez, C. H., Becila, S., Coulis, G., Sentandreu, M. A., Aubry, L. and Ouali, A. (2010). Purification and partial characterization of antithrombin III from bovine skeletal muscle and possible role of thrombin in postmortem apoptosis development and in efficiency of low voltage electrical stimulation. Food Res. Int. 43:356–363.
  • Herrera-Mendez, C. H., Bremaud, L., Coulis, G., Pelissier, P., Sentandreu, M. A., Aubry, L., Delourme, D., Chambon, C., Maftah, A., Leveziel, H. and Ouali, A. (2006b). Purification of the skeletal muscle protein Endopin 1B and characterization of the genes encoding Endopin 1A and 1B isoforms. FEBS Lett. 580:3477–3484.
  • Horvath, A. J., Forsyth, S. L. and Coughlin, P. B. (2004). Expression patterns of murine antichymotrypsin-like genes reflect evolutionary divergence at the serpina3 locus. J. Mol. Evol. 59:488–497.
  • Horvath, A. J., Lu, B. G., Pike, R. N. and Bottomley, S. P. (2011). Methods to measure the kinetics of protease inhibition by serpins. Methods Enzymol. 501:223–235.
  • Huntington, J. A., Read, R. J. and Carrell, R. W. (2000). Structure of a serpin-protease complex shows inhibition by deformation. Nature. 407:923–926.
  • Jalink, K. and Moolenaar, W. H. (1992). Thrombin receptor activation causes rapid neural cell rounding and neurite retraction independent of classic second messengers. J. Cell Biol. 118:411–419.
  • Jeremiah, L. E. and Gibson, L. L. (2003). The effects of postmortem product handling and aging time on beef palatability. Food Res. Int. 36:929–941.
  • Kelvin, D. J., Simard, G., Sue, A. Q. A. and Connolly, J. A. (1989). Growth factors, signaling pathways, and the regulation of proliferation and differentiation in BC3H1 muscle cells. II. Two signaling pathways distinguished by pertussis toxin and a potential role for the ras oncogene. J. Cell Biol. 108:169–176.
  • Kemp, C. M. and Parr, T. (2012). Advances in apoptotic mediated proteolysis in meat tenderisation. Meat. Sci. 92:252–259.
  • Kemp, C. M., Sensky, P. L., Bardsley, R. G., Buttery, P. J. and Parr, T. (2010). Tenderness–an enzymatic view. Meat. Sci. 84:248–256.
  • Lamkanfi, M., Festjens, N., Declercq, W., Vanden Berghe, T. and Vandenabeele, P. (2007). Caspases in cell survival, proliferation and differentiation. Cell Death. Differ. 14:44–55.
  • Law, R. H., Zhang, Q., McGowan, S., Buckle, A. M., Silverman, G. A., Wong, W., Rosado, C. J., Langendorf, C. G., Pike, R. N., Bird, P. I. and Whisstock, J. C. (2006). An overview of the serpin superfamily. Genome. Biol. 7:216.
  • Liu, Y., Fields, R. D., Festoff, B. W. and Nelson, P. G. (1994). Proteolytic Action of Thrombin Is Required for Electrical Activity-Dependent Synapse Reduction. Proc. Natl. Acad. Sci. U S A. 91:10300–10304.
  • Majumder, R., Weinreb, G. and Lentz, B. R. (2005). Efficient thrombin generation requires molecular phosphatidylserine, not a membrane surface. Biochemistry. 44:16998–17006.
  • Mann, K. G. (1999). Biochemistry and physiology of blood coagulation. Thromb. Haemost. 82:165–174.
  • Musilova, P., Lahbib-Mansais, Y., Yerle, M., Cepica, S., Stratil, A., Coppieters, W. and Rubes, J. (1995). Assignment of pig alpha 1-antichymotrypsin (AACT or PI2) gene to chromosome region 7q23-q26. Mamm Genome. 6:445.
  • Nelson, R. B. and Siman, R. (1990). Thrombin and its inhibitors regulate morphological and biochemical differentiation of astrocytes in vitro. Brain Res. Dev. Brain Res. 54:93–104.
  • O'Riordan, M. X., Bauler, L. D., Scott, F. L. and Duckett, C. S. (2008). Inhibitor of apoptosis proteins in eukaryotic evolution and development: A model of thematic conservation. Dev. Cell. 15:497–508.
  • Olson, S. T. and Gettins, P. G. (2011). Regulation of proteases by protein inhibitors of the serpin superfamily. Prog. Mol. Biol. Transl. Sci. 99:185–240.
  • Orlowski, M. and Wilk, S. (1981). A multicatalytic protease complex from pituitary that forms enkephalin and enkephalin containing peptides. Biochem. Biophys. Res. Commun. 101:814–822.
  • Ouali, A. (1990). Meat Tenderization: Possible Causes and Mechanisms. A Review. J. Muscle Foods. 1:129–165.
  • Ouali, A., Bige, L., Obled, A., Lacourt, A. and Valin, C. (1986). Small and high molecular weigth protease inhibitors from bovine skeletal muscle.in Cysteine Proteinases and their Inhibitors. Walter de Gruyter and Co., Berlin (Turk, V., ed.), :545–554. [Ce: check journal title abberviation]
  • Ouali, A., Herrera-Mendez, C. H., Coulis, G., Becila, S., Boudjellal, A., Aubry, L. and Sentandreu, M. A. (2006). Revisiting the conversion of muscle into meat and the underlying mechanisms. Meat. Sci. 74:44–58.
  • Ouali, A., Herrera-Mendez, C. H., Coulis, G., Samira, B., Boudjellal, A., Harhoura, K., Aubry, L. and Sentandreu, M. A. (2007). Meat tenderisation and muscle cell death, two highly related events. Tehnologija Mesa. 48:1–15.
  • Ouali, A., Rouchon, P., Zabari, M., Berri, M., Zamora, F. and Tassy, C. (1995). Natural serine and cysteine proteinase inhibitors in bovine skeletal muscle. In Expression of tissue proteinases and regulation of protein degradation as related to meat quality Edited by: Ouali A, Demeyer D, Smulders FJM. Utrecht (NL): ECCEAMST 173–198. [Ce: check style?]
  • Ouali, A. and Talmant, A. (1990). Calpains and calpastatin distribution in bovine, porcine and ovine skeletal muscles. Meat. Sci. 28:331–348.
  • Pejler, G., Abrink, M., Ringvall, M. and Wernersson, S. (2007). Mast cell proteases. Adv. Immunol. 95:167–255.
  • Pelissier, P., Delourme, D., Germot, A., Blanchet, X., Becila, S., Maftah, A., Leveziel, H., Ouali, A. and Bremaud, L. (2008). An original SERPINA3 gene cluster: Elucidation of genomic organization and gene expression in the Bos taurus 21q24 region. BMC Genomics. 9:151.
  • Philchenkov, A. (2004). Caspases: Potential targets for regulating cell death. J. Cell Mol. Med. 8:432–444.
  • Rosenberg, R. D. and Damus, P. S. (1973). The purification and mechanism of action of human antithrombin-heparin cofactor. J. Biol. Chem. 248:6490–6505.
  • Schechter, N. M. and Plotnick, M. I. (2004). Measurement of the kinetic parameters mediating protease-serpin inhibition. Methods. 32:159–168.
  • Sentandreu, M. A., Coulis, G. and Ouali, A. (2002). Role of muscle endopeptidases and their inhibitors in meat tenderness. Trends Food Sci. Technol. 13:400–421.
  • Shackelford, S. D., Koohmaraie, M., Miller, M. F., Crouse, J. D. and Reagan, J. O. (1991). An evaluation of tenderness of the longissimus muscle of Angus by Hereford versus Brahman crossbred heifers. J. Anim. Sci. 69:171–177.
  • Silverman, G. A., Bird, P. I., Carrell, R. W., Church, F. C., Coughlin, P. B., Gettins, P. G., Irving, J. A., Lomas, D. A., Luke, C. J., Moyer, R. W., Pemberton, P. A., Remold-O'Donnell, E., Salvesen, G. S., Travis, J. and Whisstock, J. C. (2001). The serpins are an expanding superfamily of structurally similar but functionally diverse proteins. Evolution, mechanism of inhibition, novel functions, and a revised nomenclature. J. Biol. Chem. 276:33293–33296.
  • Silverman, G. A., Whisstock, J. C., Bottomley, S. P., Huntington, J. A., Kaiserman, D., Luke, C. J., Pak, S. C., Reichhart, J. M. and Bird, P. I. (2010). Serpins flex their muscle: I. Putting the clamps on proteolysis in diverse biological systems. J. Biol. Chem. 285:24299–24305.
  • Stauber, W. T., Fritz, V., Dahlmann, B. and Reinauer, H. (1983a). Immunohistochemical localization of two proteinases in skeletal muscle. J. Histochem. Cytochem. 31:827–830.
  • Stauber, W. T., Ong, S. H., Fritz, V. K., Esnard, F. and Gauthier, F. (1983b). Protease inhibitor localization in control and streptozotocin-diabetic skeletal muscles. Histochem. J. 15:1079–1086.
  • Stennicke, H. R., Ryan, C. A. and Salvesen, G. S. (2002). Reprieval from execution: The molecular basis of caspase inhibition. Trends Biochem. Sci. 27:94–101.
  • Suidan, H. S., Niclou, S. P., Dreessen, J., Beltraminelli, N. and Monard, D. (1996). The thrombin receptor is present in myoblasts and its expression is repressed upon fusion. J. Biol. Chem. 271:29162–29169.
  • Suidan, H. S., Stone, S. R., Hemmings, B. A. and Monard, D. (1992). Thrombin Causes Neurite Retraction in Neuronal Cells through Activation of Cell-Surface Receptors. Neuron. 8:363–375.
  • Swanson, R., Raghavendra, M. P., Zhang, W. Q., Froelich, C., Gettins, P. G. W. and Olson, S. T. (2007). Serine and cysteine proteases are translocated to similar extents upon formation of covalent complexes with serpins - Fluorescence perturbation and fluorescence resonance energy transfer mapping of the protease binding site in CrmA complexes with granzyme B and caspase-1. J. Biol. Chem. 282:2305–2313.
  • Tassy, C. (1998). Purification et caractérisation d'un inhibiteur de sérine protéinases à partir de muscle squelettique de bovin. PhD Thesis, EPHE, Paris.
  • Tassy, C., Herrera-Mendez, C. H., Sentandreu, M. A., Aubry, L., Bremaud, L., Pelissier, P., Delourme, D., Brillard, M., Gauthier, F., Leveziel, H. and Ouali, A. (2005). Muscle endopin 1, a muscle intracellular serpin which strongly inhibits elastase: Purification, characterization, cellular localization and tissue distribution. Biochem. J. 388:273–280.
  • Taylor, R. C., Cullen, S. P. and Martin, S. J. (2008). Apoptosis: Controlled demolition at the cellular level. Nat. Rev. Mol. Cell Biol. 9:231–241.
  • Whisstock, J. C., Silverman, G. A., Bird, P. I., Bottomley, S. P., Kaiserman, D., Luke, C. J., Pak, S. C., Reichhart, J. M. and Huntington, J. A. (2010). Serpins flex their muscle: II. Structural insights into target peptidase recognition, polymerization, and transport functions. J. Biol. Chem. 285:24307–24312.
  • Ye, S., Cech, A. L., Belmares, R., Bergstrom, R. C., Tong, Y., Corey, D. R., Kanost, M. R. and Goldsmith, E. J. (2001). The structure of a Michaelis serpin-protease complex. Nat. Struct. Biol. 8:979–983.
  • Zamora, F., Aubry, L., Sayd, T., Lepetit, J., Lebert, A., Sentandreu, M. A. and Ouali, A. (2005). Serine peptidase inhibitors, the best predictor of beef ageing amongst a large set of quantitative variables. Meat. Sci. 71:730–742.
  • Zamora, F., Debiton, E., Lepetit, J., Lebert, A., Dransfield, E. and Ouali, A. (1996). Predicting variability of ageing and toughness in beef M. Longissimus lumborum et thoracis. Meat. Sci. 43:321–333.
  • Zoubine, M. N., Ma, J. Y., Smirnova, I. V., Citron, B. A. and Festoff, B. W. (1996). A molecular mechanism for synapse elimination: Novel inhibition of locally generated thrombin delays synapse loss in neonatal mouse muscle. Dev. Biol. 179:447–457.

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