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Inhibition of post-mortem fish muscle softening and degradation using legume seed proteinase inhibitors

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Abstract

Inhibitors that control muscle softening are important for regulating the activities of specific proteinases in meat. Proteolytic activity of endogenous proteinases in postmortem fish leads to the deterioration of myofibres. Calpain proteolytic enzyme system in skeletal muscles is mainly responsible for the post-mortem proteolysis. Soluble sarcoplasmic serine proteinase and the insoluble myofibrillar serine proteinase fractions contribute to the modori effects in surimi gels while myosin heavy chains contribute to gel strength. Proteolytic degenerative processes negatively affect the entire quality spectrum of the fish as food. Legume seeds are a good source of proteinase inhibitors with the potential to emerge as a promising tool in fish meat quality management. Many workers have studied the potent inhibitory effect of the seed flour from various legume crops on the flesh, surimi gels and visceral proteinases of fishes. The present review provides collective information about proteolysis in fish and its control by using legume seed flour as a natural source of proteinase inhibitors. Use of legume seed flour can reduce the dependence of the meat processing industry on the non-renewable synthetic chemical agents. Moreover, the use of natural products from sustainable resources also leads to the improved economics of meat production.

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References

  1. Ahmed Z, Donkor O, Street WA, Vasiljevic T (2015) Calpains-and cathepsins-induced myofibrillar changes in post-mortem fish: impact on structural softening and release of bioactive peptides. Trends Food Sci Technol 45(1):130–146

  2. Alderton AL, Means WJ, Kalchayanand N, McCormick RJ, Miller KW (2004) Bovine metalloprotease characterization and in vitro connective tissue degradation. J Animal Sci 82(5):1475–1481

  3. Ando M, Toyohara H, Sakaguchi M (1992) Post-mortem tenderization of rainbow trout muscle caused by the disintegration of collagen fibers in the pericellular connective tissue. Nippon Suisan Gakk 58(3):567–570

  4. Béné C, Barange M, Subasinghe R, Pinstrup-Andersen P, Merino G, Hemre GI, Williams M (2015) Feeding 9 billion by 2050—putting fish back on the menu. Food Secur 7(2):261–274

  5. Benhabiles MS, Abdi N, Drouiche N, Lounici H, Pauss A, Goosen MFA, Mameri N (2012) Fish protein hydrolysate production from sardine solid waste by crude pepsin enzymatic hydrolysis in a bioreactor coupled to an ultrafiltration unit. Mat Sci Eng C 32(4):922–928

  6. Benjakul S, Karoon S, Suwanno A (1999) Inhibitory effects of legume seed extracts on fish proteinases. J Sci Food Agric 79(13):1875–1881

  7. Benjakul S, Visessanguan W, Thummaratwasik P (2000) Inhibition of gel weakening of threadfin bream surimi using Thai legume seed proteinase inhibitors. J Food Biochem 24(5):363–380

  8. Boye SW, Lanier TC (1988) Effects of heat-stable alkaline protease activity of Atlantic menhaden (Brevoorti tyrannus) on surimi gels. J Food Sci 53(5):1340–1342

  9. Cao MJ, Hara K, Osatomi K, Tachibana K, Izumi T, Ishihara T (1999) Myofibril-Bound Serine Proteinase (MBP) and its degradation of myofibrillar proteins. J Food Sci 64(4):644–647

  10. Chéret R, Delbarre-Ladrat C, de Lamballerie-Anton M, Verrez-Bagnis V (2007) Calpain and cathepsin activities in post mortem fish and meat muscles. Food Chem 101(4):1474–1479

  11. D’Alessandro A, Zolla L (2013) Meat science: from proteomics to integrated omics towards system biology. J Proteomics 78:558–577

  12. Delbarre-Ladrat C, Verrez-Bagnis V, Noël J, Fleurence J (2004) Relative contribution of calpain and cathepsins to protein degradation in muscle of sea bass (Dicentrarchus labrax L.). Food Chem 88(3):389–395

  13. Delbarre-Ladrat C, Chéret R, Taylor R, Verrez-Bagnis V (2006) Trends in postmortem aging in fish: understanding of proteolysis and disorganization of the myofibrillar structure. Crit Rev Food Sci Nutr 46(5):409–421

  14. Elliott PR, Pei XY, Dafforn TR, Lomas DA (2000) Topography of a 2.0 Å structure of α 1-antitrypsin reveals targets for rational drug design to prevent conformational disease. Protein Sci 9(7):1274–1281

  15. Fowler MR, Park JW (2015) Salmon blood plasma: effective inhibitor of protease-laden Pacific whiting surimi and salmon mince. Food Chem 176:448–454

  16. García-Carreño FL, Navarrete del Toro MA, Díaz-López M, Hernandez-Cortes MP, Ezquerra JM (1996) Proteinase inhibition of fish muscle enzymes using legume seed extracts. J Food Prot 59(3):312–318

  17. Geesink GH, Kuchay S, Chishti AH, Koohmaraie M (2006) μ-Calpain is essential for postmortem proteolysis of muscle proteins. J Anim Sci 84(10):2834–2840

  18. Ghaly AE, Dave D, Budge S, Brooks MS (2010) Fish spoilage mechanisms and preservation techniques: review. Am J Appl Sci 7:846–864

  19. Ho ML, Chen GH, Jiang ST (2000) Effects of mackerel cathepsins L, L-like and calpain on the degradation of mackerel surimi. Fish Sci 66(3):558–568

  20. Hopkins DL, Thompson JM (2002) The degradation of myofibrillar proteins in beef and lamb using denaturing electrophoresis-an overview. J Muscle Foods 13(2):81–102

  21. Hossain MI, Itoh Y, Morioka K, Obatake A (2001) Inhibiting effect of polymerization and degradation of myosin heavy chain during preheating at 30 °C and 50 °C on the gel-forming ability of Walleye pollack surimi. Fisheries Sci 67(4):718–725

  22. Hu Y, Morioka K, Itoh Y (2010) Participation of cysteine protease cathepsin L in the gel disintegration of red bulleye (Priacanthus macracanthus) surimi gel paste. J Sci Food Agric 90:370–375

  23. Hu Y, Yu H, Dong K, Yang S, Ye X, Chen S (2014) Analysis of the tenderisation of jumbo squid (Dosidicus gigas) meat by ultrasonic treatment using response surface methodology. Food Chem 160:219–225

  24. Huang M, Huang F, Xu X, Zhou G (2009) Influence of caspase3 selective inhibitor on proteolysis of chicken skeletal muscle proteins during post mortem aging. Food Chem 115(1):181–186

  25. Ishida N, Yamashita M, Koizumi N, Terayama M, Ineno T, Minami T (2003) Inhibition of post-mortem muscle softening following in situ perfusion of protease inhibitors in tilapia. Fisheries Sci 69(3):632–638

  26. Kemp CM, Sensky PL, Bardsley RG, Buttery PJ, Parr T (2010) Tenderness—an enzymatic view. Meat Sci 84(2):248–256

  27. Klomklao S, Benjakul S (2015) Effect of trypsin inhibitor in adzuki bean (Vigna angularis) on proteolysis and gel properties of threadfin bream (Nemipterus bleekeri). LWT - Food Sci Technol 63(2):906–911

  28. Koohmaraie M, Geesink GH (2006) Contribution of postmortem muscle biochemistry to the delivery of consistent meat quality with particular focus on the calpain system. Meat Sci 74(1):34–43

  29. Kristoffersen S, Tobiassen T, Esaiassen M, Olsson GB, Godvik LA, Seppola MA, Olsen RL (2006) Effects of pre-rigour filleting on quality aspects of Atlantic cod (Gadus morhua L.). Aquac Res 37(15):1556–1564

  30. Kudre T, Benjakul S, Kishimura H (2013) Effects of protein isolates from black bean and mungbean on proteolysis and gel properties of surimi from sardine (Sardinella albella). LWT - Food Sci Technol 50:511–518

  31. Kunimoto M, Hamada-Sato N, Kato N (2016) Main protein components in frozen surimi contributed to heat-induced gel formation. Int Food Res J 23(5):1939–1948

  32. Lafarga T, Hayes M (2014) Bioactive peptides from meat muscle and by-products: generation, functionality and application as functional ingredients. Meat Sci 98(2):227–239

  33. Law RH, Zhang Q, McGowan S, Buckle AM, Silverman GA, Wong W, Rosado CJ, Langendorf CG, Pike RN, Bird PI, Whisstock JC (2006) An overview of the serpin superfamily. Genome Biol 7(5):216

  34. Lonergan EH, Zhang W, Lonergan SM (2010) Biochemistry of postmortem muscle—lessons on mechanisms of meat tenderization. Meat Sci 86(1):184–195

  35. López FM, Dıaz IM, López MD, López FA (1999) Inhibition of digestive proteases by vegetable meals in three fish species; seabream (Sparus aurata), tilapia (Oreochromis niloticus) and African sole (Solea senegalensis). Comp Biochem Physiol B: Biochem Mol Biol 122(3):327–332

  36. Luo Y, Kuwahara R, Kaneniwa M, Murata Y, Yokoyama M (2004) Effect of soy protein isolate on gel properties of Alaska pollock and common carp surimi at different setting conditions. J Sci Food Agric 84(7):663–671

  37. Martín-Cabrejas MA, Aguilera Y, Pedrosa MM, Cuadrado C, Hernández T, Díaz S, Esteban RM (2009) The impact of dehydration process on antinutrients and protein digestibility of some legume flours. Food Chem 114(3):1063–1068

  38. Mazorra-Manzano MA, Ramírez-Suárez JC, Moreno-Hernández JM, Pacheco-Aguilar R (2018) Seafood proteins. In: Yada RY (ed) Proteins in food processing. Woodhead Publishing, Cambridge, pp 445–475

  39. Ohkubo M, Miyagawa K, Osatomi K, Hara K, Nozaki Y, Ishihara T (2004) Purification and characterization of myofibril-bound serine protease from lizard fish (Saurida undosquamis) muscle. Comp Biochem Physiol B: Biochem Mol Biol 137(1):139–150

  40. Olson ST, Gettins PG (2011) Regulation of proteases by protein inhibitors of the serpin superfamily. Prog Mol Biol Transl Sci 99:185–240

  41. Ouali A, Herrera-Mendez CH, Coulis G, Becila S, Boudjellal A, Aubry L, Sentandreu MA (2006) Revisiting the conversion of muscle into meat and the underlying mechanisms. Meat Sci 74(1):44–58

  42. Ouali A, Gagaoua M, Boudida Y, Becila S, Boudjellal A, Herrera-Mendez CH, Sentandreu MA (2013) Biomarkers of meat tenderness: present knowledge and perspectives in regards to our current understanding of the mechanisms involved. Meat Sci 95(4):854–870

  43. Oujifard A, Benjakul S, Ahmad M, Seyfabadi J (2012) Effect of bambara groundnut protein isolate on autolysis and gel properties of surimi from threadfin bream (Nemipterus bleekeri). LWT - Food Sci Technol 47:261–266

  44. Pereira PMDCC, Vicente AFDRB (2013) Meat nutritional composition and nutritive role in the human diet. Meat Sci 93(3):586–592

  45. Prato E, Biandolino F (2015) The contribution of fish to the Mediterranean diet. In: Preedy VR, Watson RR (eds) The Mediterranean diet. Academic Press, Cambridge, pp 165–174

  46. Prato E, Biandolino F, Parlapiano I, Giandomenico S, Denti G, Calò M, Spada L, Di Leo A (2019) Proximate, fatty acids and metals in edible marine bivalves from Italian market: beneficial and risk for consumers health. Sci Total Environ 648:153–163

  47. Pushparajan N, Varadharajan D, Soundarapandian P (2013) Microbial studies of prepared curries stored in tin free steel cans. J Food Process Technol 4(6):1000238

  48. Ramírez JA, García-Carreño EL, Morales OG, Sanchez A (2002) Inhibition of Modori-associated proteinases by legume seed extracts in surimi production. J Food Sci 67(2):578–581

  49. Schechter NM, Plotnick MI (2004) Measurement of the kinetic parameters mediating protease–serpin inhibition. Methods 32(2):159–168

  50. Sentandreu MA, Coulis G, Ouali A (2002) Role of muscle endopeptidases and their inhibitors in meat tenderness. Trends Food Sci Technol 13(12):400–421

  51. Silverman GA, Bird PI, Carrell RW, Coughlin PB, Gettins PG, Irving JI, Lomas DA, Luke CJ, Moyer RW, Pemberton PA, Remold-O’Donnell E, Salvesen GS, Travis J, Whisstock JC (2001) The serpins are an expanding superfamily of structurally similar but funtionally diverse proteins: evolution, mechanism of inhibition, novel functions, and a revised nomenclature. J Biol Chem 276(36):33293–33296

  52. Singh A, Benjakul S (2018) Proteolysis and its control using protease inhibitors in fish and fish products: a review. Compr Rev Food Sci Food Saf 17:496–509

  53. Singh B, Singh JP, Shevkani K, Singh N, Kaur A (2017a) Bioactive constituents in pulses and their health benefits. J Food Sci Technol 54(4):858–870

  54. Singh B, Singh JP, Kaur A, Singh N (2017b) Phenolic composition and antioxidant potential of grain legume seeds: a review. Food Res Int 101:1–16

  55. Singh B, Singh JP, Singh N, Kaur A (2017c) Saponins in pulses and their health promoting activities: a review. Food Chem 233:540–549

  56. Sriket C (2014) Proteases in fish and shellfish: role on muscle softening and prevention. Int Food Res J 21:433–445

  57. Sriket C, Benjakul S, Visessanguan W, Kishimura H (2011a) Collagenolytic serine protease in fresh water prawn (Macrobrachium rosenbergii): characteristics and its impact on muscle during iced storage. Food Chem 124(1):29–35

  58. Sriket C, Benjakul S, Visessanguan W, Hara K (2011b) Effect of legume seed extracts on the inhibition of proteolytic activity and muscle degradation of fresh water prawn (Macrobrachium rosenbergii). Food Chem 129(3):1093–1099

  59. Stoknes I, Rustad T (1995) Proteolytic activity in muscle from Atlantic salmon (Salmo salar). J Food Sci 60(4):711–714

  60. Suarez MD, Abad M, Ruiz-Cara T, Estrada JD, García-Gallego M (2005) Changes in muscle collagen content during post mortem storage of farmed sea bream (Sparus aurata): influence on textural properties. Aquac Int 13(4):315–325

  61. Sulikowski T, Bauer BA, Patston PA (2002) α1-Proteinase inhibitor mutants with specificity for plasma kallikrein and C1 s but not C1. Protein Sci 11(9):2230–2236

  62. Suwansakornkul P, Itoh Y, Hara S, Obatake A (1993) Identification of proteolytic activities of gel-degradation factors in three lizard fish species. Nippon Suisan Gakk 59(6):1039–1045

  63. Tacon AG, Metian M (2013) Fish matters: importance of aquatic foods in human nutrition and global food supply. Rev Fish Sci 21(1):22–38

  64. Taylor R, Fjaera S, Skjervold P (2002) Salmon fillet texture is determined by myofiber–myofiber and myofiber–myocommata attachment. J Food Sci 67(6):2067–2071

  65. Tsuchiya H, Seki N (1991) Action of calpain on α-actinin within and isolated from carp myofibrils. Nippon Suisan Gakk 57(6):1133–1139

  66. Wu JL, Lu BJ, Du MH, Liu GM, Hara KJ, Su WJ, Cao MJ (2008) Purification and characterization of gelatinase-like proteinases from the dark muscle of common carp (Cyprinus carpio). J Agric Food Chem 56(6):2216–2222

  67. Wu GP, Chen SH, Liu GM, Yoshida A, Zhang LJ, Su WJ, Cao MJ (2010) Purification and characterization of a collagenolytic serine proteinase from the skeletal muscle of red sea bream (Pagrus major). Comp Biochem Physiol B: Biochem Mol Biol 155(3):281–287

  68. Xiong GY, Zhang LL, Zhang W, Wu J (2012) Influence of ultrasound and proteolytic enzyme inhibitors on muscle degradation, tenderness and cooking loss of hens during aging. Czech J Food Sci 30(3):195–205

  69. Yamashita M, Konagaya S (1991) Hydrolytic action of salmon cathepsins B and L to muscle structural proteins in respect of muscle softening. Nippon Suisan Gakk 57(10):1917–1922

  70. Yongsawatdigul J, Park JW, Virulhakul P, Viratchakul S (2000) Proteolytic degradation of tropical tilapia surimi. J Food Sci 65(1):129–133

  71. Yu D, Wu L, Regenstein JM, Jiang Q, Yang F, Xu Y, Xia W (2019) Recent advances in quality retention of non-frozen fish and fishery products: a review. Crit Rev Food Sci Nutr. https://doi.org/10.1080/10408398.2019.1596067

  72. Zamora F, Aubry L, Sayd T, Lepetit J, Lebert A, Sentandreu MA, Ouali A (2005) Serine peptidase inhibitors, the best predictor of beef ageing amongst a large set of quantitative variables. Meat Sci 71(4):730–742

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Correspondence to Balwinder Singh.

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Singh, J., Singh, B. Inhibition of post-mortem fish muscle softening and degradation using legume seed proteinase inhibitors. J Food Sci Technol 57, 1–11 (2020) doi:10.1007/s13197-019-04044-6

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Keywords

  • Proteolytic inhibitors
  • Softening
  • Legume seeds
  • Endogenous proteases
  • SERPINS