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Degradation of skeletal muscle protein during growth and development of salmonid fish

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Abstract

Published data and the results of the authors’ own studies on the role of intracellular proteolytic enzymes and the metabolic and signaling processes regulated by these enzymes at certain stages of growth and development of salmonid fishes are analyzed in the present review. The major pathways of intracellular proteolysis relying on autophagy, proteasome activity, and calpain activity are considered, as well as the relative contribution of these pathways to proteolysis in skeletal muscle of the fish. Skeletal muscle accounts for more than half of the weight of the fish and undergoes the most significant changes due to the action of anabolic and catabolic signals. Special attention is paid to the intensity of protein degradation during the active growth period characterized by a high rate of protein synthesis and metabolism in fish, as well as to protein degradation during the reproductive period characterized by predomination of catabolic processes in contrast to the growth period. Skeletal muscle plays a unique role as a source of plastic and energy substrates in fish, and, therefore, the process of muscle protein degradation is regarded as a key mechanism for the regulation of growth intensity in juvenile salmon and for maintenance of viability and reproductive capacity of salmonid fish during the maturation of gametes, starvation, and migration related to spawning. The possibility of using a set of parameters of intracellular proteolysis to characterize the early development of salmonids is demonstrated in the review.

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References

  • Alami-Durante, H., Médale, F., Cluzeaud, M., and Kaushik, S.J., Skeletal muscle growth dynamics and expression of related genes in white and red muscles of rainbow trout fed diets with graded levels of a mixture of plant protein sources as substitutes for fishmeal, Aquaculture, 2010, vol. 303, pp. 50–58.

    Article  CAS  Google Scholar 

  • Alsop, D.H., Kieffer, J.D., and Wood, C.M., The effects of temperature and swimming speed on instantaneous fuel use and nitrogenous waste excretion of the Nile tilapia, Physiol. Biochem. Zool., 1999, vol. 72, pp. 474–483.

    Article  CAS  PubMed  Google Scholar 

  • Ando, S., Hatano, M., and Zama, K., Protein degradation and protease activity of chum salmon (Oncorhynchus keta) muscle during spawning migration, Fish Physiol. Biochem., 1986, vol. 1, pp. 17–26.

    Article  CAS  PubMed  Google Scholar 

  • Ardley, H.C. and Robinson, P.A., E3 ubiquitin ligases. The ubiquitin-proteasome system, Essays Biochem., 2005, vol. 41, pp. 15–30.

    Article  CAS  PubMed  Google Scholar 

  • Attaix, D., Combaret, L., and Taillandier, D., Mechanisms and regulation in protein degradation, in Protein Metabolism and Nutrition, Lobley, G.E., Ed., Proceedings VIII, Purdue University Press, 1999, pp. 51–67.

    Google Scholar 

  • Aussanasuwannakul, A., Kenney, P.B., Weber, G.M., et al., Effect of sexual maturation on growth, fillet composition, and texture of female rainbow trout (Oncorhynchus mykiss) on a high nutritional plane, Aquaculture, 2011, vol. 317, pp. 79–88.

    Article  Google Scholar 

  • Bahuaud, D., Gaarder, M., Veiseth-Kent, E., and Thomassen, M., Fillet texture and protease activities in different families of farmed Atlantic salmon (Salmo salar L.), Aquaculture, 2010, vol. 310, pp. 213–220.

    Article  CAS  Google Scholar 

  • Belcastro, A.N., Shewchuk, L.D., and Raj, D.A., Exerciseinduces muscle injury: a calpain hypothesis, Mol. Cell. Biochem., 1998, vol. 179, pp. 135–145.

    Article  CAS  PubMed  Google Scholar 

  • Björnsson, B.T. and Bradley, T.M., Epilogue: past successes, present misconceptions and future milestones in salmon smoltification research, Aquaculture, 2007, vol. 273, pp. 384–391.

    Article  Google Scholar 

  • Blazevich, A.J. and Sharp, N.C., Understanding muscle architectural adaptation: macro- and micro-level research, Cells Tissues Organs, 2005, vol. 181, no. 1, pp. 1–10.

    Article  PubMed  Google Scholar 

  • Bohley, P., Intracellular proteolysis, in Hydrolytic Enzymes, Biomedical division, 1987, pp. 307–332.

    Chapter  Google Scholar 

  • Bradford, R.G., Differential utilization of storage lipids and storage proteins by northwest Atlantic herring (Clupea harengus harengus), J. Fish. Biol., 1993, vol. 43, pp. 811–824.

    Article  CAS  Google Scholar 

  • Bureau, D.P., Hua, K., and Cho, C.Y., Effect of feeding level on growth and nutrient deposition in rainbow trout (Oncorhynchus mykiss) growing from 150 to 600 g, Aquac. Res., 2006, vol. 37, pp. 1090–1098.

    Article  CAS  Google Scholar 

  • Busconi, L., Folco, E.J., Studdert, C., and Sanchez, J.J., Purification and characterization of a latent form of multicatalytic proteinase from fish muscle, Comp. Biochem. Physiol. B, 1992, vol. 102, pp. 303–309.

    CAS  PubMed  Google Scholar 

  • Carnevali, O. and Maradonna, F., Exposure to xenobiotic compounds: looking for new biomarkers, Gen. Comp. Endocrinol., 2003, vol. 131, pp. 203–208.

    Article  CAS  PubMed  Google Scholar 

  • Carruth, L.L., Dores, R.M., Maldonado, T.A., et al., Elevation of plasma cortisol during the spawning migration of landlocked kokanee salmon (Oncorhynchus nerka kennerlyi), Comp. Biochem. Physiol. C, 2000, vol. 127, pp. 123–131.

    Article  CAS  Google Scholar 

  • Cavailles, V., Augereau, P., and Rochefort, H., Cathepsin D gene of human MCF7 cells contains estrogenresponsive sequences in its 5' proximal flanking region, Biochem. Biophys. Res. Commun., 1991, vol. 174, no. 2, pp. 816–824.

    Article  CAS  PubMed  Google Scholar 

  • Chen, Y. and Klionsky, D.J., The regulation of autophagy— unanswered questions, J. Cell. Sci., 2011, vol. 124, pp. 161–170.

    Article  CAS  PubMed  Google Scholar 

  • Churova, M.V., Meshcheryakova, O.V., Veselov, A.E., and Nemova, N.N., Activity of enzymes involved in the energy and carbohydrate metabolism and the level of some molecular-genetic characteristics in young salmons (Salmo salar L.) with different age and weight, Russ. J. Dev. Biol., 2015, vol. 46, no. 5, pp. 254–262.

    Article  CAS  Google Scholar 

  • Ciechanover, A., Intracellular protein degradation: from a vague idea through the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting, Bioorg. Med. Chem., 2013, vol. 21, no. 12, pp. 3400–3410.

    Article  CAS  PubMed  Google Scholar 

  • Cleveland, B.M. and Burr, G.S., Proteolytic response to feeding level in rainbow trout (Oncorhynchus mykiss), Aquaculture, 2011, vol. 319, pp. 194–204.

    Article  CAS  Google Scholar 

  • Cleveland, B.M. and Evenhuis, J.P., Molecular characterization of atrogin-1/Fbox protein-32 (FBXO32) and F-box protein-25 (FBXO25) in rainbow trout (Oncorhynchus mykiss): expression across tissues in response to feed deprivation, Comp. Biochem. Physiol. B, 2010, vol. 157, pp. 248–257.

    Article  PubMed  Google Scholar 

  • Cleveland, B.M. and Weber, G.M., Effects of sex steroids on indices of protein turnover in rainbow trout (Oncorhynchus mykiss) white muscle, Gen. Comp. Endocrinol., 2011, vol. 174, pp. 132–142.

    Article  CAS  PubMed  Google Scholar 

  • Codogno, P. and Meijer, A.J., Autophagy and signaling: their role in cell survival and cell death, Cell Death Differ., 2005, vol. 12, pp. 1509–1518.

    Article  CAS  PubMed  Google Scholar 

  • Cottin, P., Brustis, J.J., and Poussard, S., Ca2+-dependent proteinases (calpains) and muscle cell differentiation, Biochim. Biophys. Acta, 1994, vol. 1223, pp. 170–178.

    Article  CAS  PubMed  Google Scholar 

  • Cuervo, A.M. and Dice, J.F., Lysosomes, a meeting point of proteins, chaperones, and proteases, J. Mol. Med., 1998, vol. 76, pp. 6–12.

    Article  CAS  PubMed  Google Scholar 

  • von der Decken, A., Physiological changes of skeletal muscle by maturation-spawning of non-migrating female Atlantic salmon, Salmo salar, Comp. Biochem. Physiol. B, 1992, vol. 101, pp. 299–301.

    Google Scholar 

  • Dobly, A., Martin, S.A., Blaney, S.C., and Houlihan, D.F., Protein growth rate in rainbow trout (Oncorhynchus mykiss) is negatively correlated to liver 20S proteasome activity, Comp. Biochem. Physiol., A, 2004, vol. 137, pp. 75–85.

    Article  CAS  Google Scholar 

  • Du, M., Zhu, M.J., Means, W.J., et al., Effect of nutrient restriction on calpain and calpastatin content of skeletal muscle from cows and fetuses, J. Anim. Sci., 2004, vol. 82, no. 9, pp. 2541–2547.

    CAS  PubMed  Google Scholar 

  • Emery, P.W., Cotellessa, L., Holness, M., et al., Different patterns of protein turnover in skeletal and gastrointestinal smooth muscle and the production of N taumethylhistidine during fasting in the rat, Biosci. Rep., 1986, vol. 6, no. 2, pp. 143–153.

    Article  CAS  PubMed  Google Scholar 

  • Ezaki, J., Matsumoto, N., Takeda-Ezaki, M., et al., Liver autophagy contributes to the maintenance of blood glucose and amino acid levels, Autophagy, 2011, vol. 7, pp. 727–736.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Froehlich, J.M., Fowler, Z.G., Galt, N.J., et al., Sarcopenia and piscines: the case for indeterminate-growing fish as unique genetic model organisms in aging and longevity research, Front. Genet., 2013, vol. 4, p. 159.

    Article  PubMed  PubMed Central  Google Scholar 

  • Glass, D.J., Signaling pathways perturbing muscle mass, Curr. Opin. Clin. Nutr. Metab. Care, 2010, vol. 13, pp. 225–229.

    Article  CAS  PubMed  Google Scholar 

  • Goll, D.E., Thompson, V.F., Li, H., et al., The calpain system, Physiol. Rev., 2003, vol. 83, pp. 731–801.

    Article  CAS  PubMed  Google Scholar 

  • Goll, D.E., Neti, G., Mares, S.W., and Thompson, V.F., Myofibrillar protein turnover: the proteasome and the calpains, J. Anim. Sci., 2008, vol. 86, pp. E19–35.

    Article  CAS  PubMed  Google Scholar 

  • Guderley, H., Lapointe, D., Bédard, M., and Dutil, J.-D., Metabolic priorities during starvation: enzyme sparing in liver and white muscle of Atlantic cod, Gadus morhua L., Comp. Biochem. Physiol., A, 2003, vol. 135, pp. 347–356.

    Article  Google Scholar 

  • Haas, K.F., Woodruff, E., III, and Broadie, K., Proteasome function is required to maintain muscle cellular architecture, Biol. Cell, 2007, vol. 99, pp. 615–626.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hershko, A., Ciechanover, A., and Varshavsky, A., Basic medical research award. The ubiquitin system, Nat. Med., 2000, vol. 6, pp. 1073–1081.

    Article  CAS  PubMed  Google Scholar 

  • Huang, J. and Forsberg, N.E., Role of calpain in skeletalmuscle protein degradation, Proc. Natl. Acad. Sci. U. S. A., 1998, vol. 95, pp. 12100–12105.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hutchings, J. and Jones, M., Life history variation and growth rate thresholds for maturity in Atlantic salmon, Salmo salar, Can. J. Fish. Aquat. Sci., 1998, vol. 55, pp. 22–47.

    Article  Google Scholar 

  • Ito, K., Toyohara, H., and Sakaguchi, H., Disintegration of the pericellular connective tissue of ayu muscle in the spawning season relevant to softening, Nippon Suissan Gakkaishi, 1992, vol. 58, p. 1553.

    Google Scholar 

  • Jackman, R.W. and Kandarian, S.C., The molecular basis of skeletal muscle atrophy, Am. J. Physiol. Cell Ph., 2004, vol. 287, pp. 834–843.

    Article  Google Scholar 

  • Jékely, G. and Friedrich, P., The evolution of the calpain family as reflected in paralogous chromosome regions, J. Mol. Evol., 1999, vol. 49, pp. 272–281.

    Article  PubMed  Google Scholar 

  • Johnston, I.A., Environment and plasticity of myogenesis in teleost fish, J. Exp. Biol., 2006, vol. 209, pp. 2249–2264.

    Article  CAS  PubMed  Google Scholar 

  • Kasperek, G.J. and Snider, R.D., Total and myofibrillar protein degradation in isolated soleus muscles after exercise, Am. J. Physiol., 1989, vol. 257, pt. 1, pp. E1–E5.

    CAS  PubMed  Google Scholar 

  • Kuma, A., Hatano, M., Matsui, M., et al., The role of autophagy during the early neonatal starvation period, Nature, 2004, vol. 432, no. 7020, pp. 1032–1036.

    Article  CAS  PubMed  Google Scholar 

  • Lecker, S.H., Jagoe, R.T., Gilbert, A., et al., Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression, FASEB J., 2004, vol. 18, pp. 39–51.

    Article  CAS  PubMed  Google Scholar 

  • Lubzens, E., Young, G., Bobe, J., and Cerda, J., Oogenesis in teleosts: how eggs are formed, Gen. Comp. Endocrinol., 2010, vol. 165, pp. 367–389.

    Article  CAS  PubMed  Google Scholar 

  • Lysenko, L.A., Nemova, N.N., and Kantserova, N.P., Proteoliticheskaya regulyatsiya biologicheskikh protsessov (Proteolytic Regulation of Biological Processes), Petrozavodsk: Karel. Nauch. Tsentr RAN, 2011.

    Google Scholar 

  • Lysenko, L.A., Kantserova, N.P., Ushakova, N.V., and Nemova, N.N., Proteinases of the calpain family in water invertebrates and fishes, Russ. J. Bioorg. Chem., 2012a, vol. 38, no. 3, pp. 282–289.

    Article  CAS  Google Scholar 

  • Lysenko, L.A., Kantserova, N.P., Kaivarainen, E.I., et al., Osmotic balance in marine organisms: adaptation through protein degradation, Comp. Biochem. Physiol., A, 2012b, vol. 163, suppl., pp. S29–S30.

    Article  Google Scholar 

  • Lysenko, L., Kantserova, N.P., Krupnova, M.Yu., and Nemova, N.N., Protein degradation systems in the control of salmonid fish growth, Protein Sci., 2015A, vol. 24, p. 262.

    Google Scholar 

  • Lysenko, L.A., Kantserova, N.P., Krupnova, M.Yu., et al., Intracellular protein degradation in the development of the Atlantic salmon Salmo salar L., Russ. J. Bioorg. Chem., 2015b, vol. 41, no. 6, pp. 645–651.

    Article  CAS  Google Scholar 

  • Martin, S.A., Blaney, S., Bowman, A.S., and Houlihan, D.F., Ubiquitin-proteasome-dependent proteolysis in rainbow trout (Oncorhynchus mykiss): effect of food deprivation, Pflugers Arch., 2002, vol. 445, pp. 257–266.

    Article  CAS  PubMed  Google Scholar 

  • Masiero, E., Agatea, L., Mammucari, C., et al., Autophagy is required to maintain muscle mass, Cell. Metab., 2009, vol. 10, pp. 507–515.

    Article  CAS  PubMed  Google Scholar 

  • Mizushima, N. and Klionsky, D.J., Protein turnover via autophagy: implications for metabolism, Annu. Rev. Nutr., 2007, vol. 27, pp. 19–40.

    Article  CAS  PubMed  Google Scholar 

  • Mommsen, T.P., Paradigms of growth in fish, Comp. Biochem. Physiol. B, 2004, vol. 129, pp. 207–219.

    Article  Google Scholar 

  • Mommsen, T.P., Salmon spawning migration and muscle protein metabolism: the August Krogh principle at work, Comp. Biochem. Physiol. B, 2004, vol. 139, no. 3, pp. 383–400.

    Article  PubMed  Google Scholar 

  • Morata, P., Vargas, A.M., Sanchez-Medina, F., et al., Evolution of gluconeogenic enzyme activities during starvation in liver and kidney of the rainbow trout (Salmo gairdneri), Comp. Biochem. Physiol. B, 1982, vol. 71, no. 1, pp. 65–70.

    Article  CAS  PubMed  Google Scholar 

  • Neifakh, A.A. and Timofeeva, M.Ya., Molekulyarnaya biologiya protsessov razvitiya (Molecular Biology of Development Processes), Moscow: Nauka, 1977.

    Google Scholar 

  • Nemova, N.N., Krupnova, M.Yu., Efremov, D.A., and Veselov, A.E., Activity of lysosomal proteases (cathepsins B and D) in muscles of young (0+, 1+, 2+) Atlantic salmon from the Varzuga River, Trudy KarNTs RAN, Ser. Eksp. Biol., 2015, no. 11, pp. 85–91.

    Google Scholar 

  • Nemova, N.N., Kyaivyaryainen, E.I., Nefedova, Z.A., and Veselov, A.E., Calcium-dependent proteases (calpains) in yearlings (0+) of Atlantic salmon Salmo salar L. from two habitats of the Varzuga River, Uch. Zap. Petrozavodsk. Gos. Univ., Ser. Estestv. Tekhn. Nauki, 2014, vol. 1, no. 8 (145), pp. 7–11.

    Google Scholar 

  • Nemova, N.N., Sidorov, V.S., and Ripatti, P.O., Lysosomal digestion of proteins of salmon Salmo salar L. organs during starvation in cages in the prespawning period, Vopr. Ikhtiol., 1980, vol. 120, pp. 180–182.

    Google Scholar 

  • Nemova, N.N., Vnutrikletochnye proteoliticheskie fermenty u ryb (Intracellular Proteolytic Enzymes in Fish), Petrozavodsk: Karel. Nauch. Tsentr RAN, 1996.

    Google Scholar 

  • Nemova, N.N., Lysenko, L.A., and Kantserova, N.P., Proteases of the calpain family: structure and functions, Russ. J. Dev. Biol., 2010, vol. 41, no. 5, pp. 318–325.

    Article  Google Scholar 

  • Nielsen, L.B. and Nielsen, H.H., Purification and characterization of cathepsin D from herring muscle (Clupea harengus), Comp. Biochem. Physiol. B, 2001, vol. 128, pp. 351–363.

    Article  CAS  PubMed  Google Scholar 

  • Noakes, D.J. and Beamish, R.J., Shifting the balance: towards sustainable salmon populations and fisheries of the future, in Sustainable Fisheries: Multi-Level Approaches to a Global Problem, Taylor, W.W., Lynch, A.J., and Schechter, M.G., Eds., Bethesda, Maryland: American Fisheries Society, 2011, pp. 23–50.

    Google Scholar 

  • Olin, T., Westman, A., and Decken, A., Response of epaxial muscle and liver to 17b estradiol in fed and starved Atlantic salmon (Salmo salar), Aquaculture, 1991, vol. 99, pp. 179–191.

    Article  CAS  Google Scholar 

  • Ono, Y. and Sorimachi, H., Calpains—an elaborate proteolytic system, Biochim. Biophys. Acta, 2012, vol. 1824, pp. 224–236.

    Article  CAS  PubMed  Google Scholar 

  • Overturf, K. and Gaylord, T.G., Determination of relative protein degradation activity at different life stages in rainbow trout (Oncorhynchus mykiss), Comp. Biochem. Physiol. B, 2009, vol. 152, no. 2, pp. 150–160.

    Article  PubMed  Google Scholar 

  • Peragon, J., Barroso, J.B., Garcia-Salguero, L., et al., Selective changes in the protein-turnover rates and nature of growth induced in trout liver by long-term starvation followed by re-feeding, Mol. Cell. Biochem., 1999, vol. 201, nos. 1–2, pp. 1–10.

    Article  CAS  PubMed  Google Scholar 

  • Preziosa, E., Liu, S., Terova, G., et al., Effect of nutrient restriction and re-feeding on calpain family genes in skeletal muscle of channel catfish (Ictalurus punctatus), PLoS One, 2013, vol. 8, no. 3, p. e59404.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Purintrapiban, J., Wang, M.C., and Forsberg, N.E., Degradation of sarcomeric and cytoskeletal proteins in cultured skeletal muscle cells, Comp. Biochem. Physiol. B, 2003, vol. 136, pp. 393–401.

    Article  PubMed  Google Scholar 

  • Saito, M., Sato, K., Kunisaki, N., and Kimura, S., Characterization of a rainbow trout matrix metalloproteinase capable of degrading type i collagen, Eur. J. Biochem., 2000, vol. 267, pp. 6943–6950.

    Article  CAS  PubMed  Google Scholar 

  • Salem, M., Nath, J., Rexroad, C.E., et al., Identification and molecular characterization of the rainbow trout calpains (Capn1 and Capn2): their expression in muscle wasting during starvation, Comp. Biochem. Physiol. B, 2005a, vol. 140, no. 1, pp. 63–71.

    Article  PubMed  Google Scholar 

  • Salem, M., Yao, J., Rexroad, C., et al., Characterization of calpastatin gene in fish: its potential role in muscle growth and fillet quality, Comp. Biochem. Physiol. B, 2005b, vol. 141, pp. 488–497.

    Article  PubMed  Google Scholar 

  • Salem, M., Kenney, P.B., Rexroad, C.E., and Yao, J., Molecular characterization of muscle atrophy and proteolysis associated with spawning in rainbow trout, Comp. Biochem. Physiol., D, 2006, vol. 1, no. 2, pp. 227–237.

    Google Scholar 

  • Salem, M., Silverstein, J., Rexroad, C.E., and Yao, J., Effect of starvation on global gene expression and proteolysis in rainbow trout (Oncorhynchus mykiss), BMC Genomics, 2007, vol. 8, p. 328.

    Article  PubMed  PubMed Central  Google Scholar 

  • Salmerón, C., García de la Serrana, D., Jiménez-Amilburu, V., et al., Characterisation and expression of calpain family members in relation to nutritional status, diet composition and flesh texture in gilthead sea bream (Sparus aurata), PLoS One, 2013, vol. 8, no. 9, p. e75349.

    Article  PubMed  PubMed Central  Google Scholar 

  • Salmerón, C., Navarro, I., Johnston, I.A., et al., Characterisation and expression analysis of cathepsins and ubiquitin-proteasome genes in gilthead sea bream (Sparus aurata) skeletal muscle, BMC Res. Notes, 2015, vol. 8, p. 149.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sandri, M., Autophagy in skeletal muscle, FEBS Lett., 2010, vol. 584, pp. 1411–1416.

    Article  CAS  PubMed  Google Scholar 

  • Seear, P.J., Carmichael, S.N., Talbot, R., et al., Differential gene expression during smoltification of Atlantic salmon (Salmo salar L.): a first large-scale microarray study, Mar. Biotechnol., 2010, vol. 12, pp. 126–140.

    Article  CAS  PubMed  Google Scholar 

  • Seiliez, I., Panserat, S., Skiba-Cassy, S., et al., Feeding status regulates the polyubiquitination step of the ubiquitin proteasome-dependent proteolysis in rainbow trout (Oncorhynchus mykiss) muscle, J. Nutr., 2008, vol. 138, pp. 487–491.

    CAS  PubMed  Google Scholar 

  • Seiliez, I., Gabillard, J.C., Riflade, M., et al., Amino acids downregulate the expression of several autophagyrelated genes in rainbow trout myoblasts, Autophagy, 2012, vol. 8, pp. 364–375.

    Article  CAS  PubMed  Google Scholar 

  • Seiliez, I., Dias, K., and Cleveland, B.M., Contribution of the autophagy-lysosomal and ubiquitin-proteasomal proteolytic systems to total proteolysis in rainbow trout (Oncorhynchus mykiss) myotubes, Am. J. Physiol. Regul. Integr. Comp. Physiol., 2014, vol. 307, pp. R1330–R1337.

    Article  CAS  PubMed  Google Scholar 

  • Silva, L.A., Silveira, P.C.L., Ronsani, M.M., et al., Taurine supplementation decreases oxidative stress in skeletal muscle after eccentric exercise, Cell. Biochem. Funct., 2011, vol. 29, pp. 43–49.

    Article  CAS  PubMed  Google Scholar 

  • Solomon, V., Lecker, S.H., and Goldberg, A.L., The Nend rule pathway catalyzes a major fraction of the protein degradation in skeletal muscle, J. Biol. Chem., 1998, vol. 273, pp. 25216–25222.

    Article  CAS  PubMed  Google Scholar 

  • Somero, G.N. and Yancey, P.H., Osmolytes and cell-volume regulation: physiological and evolutionary principles, Compr. Physiol., 2011, pp. 441–484.

    Google Scholar 

  • Sorimachi, H., Imajoh-Ohmi, S., Emori, Y., et al., 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., 1989, vol. 264, pp. 20106–20111.

    CAS  PubMed  Google Scholar 

  • Sorimachi, H. and Ono, Y., Regulation and physiological roles of the calpain system in muscular disorders, Cardiovasc. Res., 2012, vol. 96, pp. 11–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka, K. and Ichihara, A., Autodegradation of rat liver proteasomes (large multicatalytic proteinase complexes), Biochem. Biophys. Res. Commun., 1989, vol. 158, no. 2, pp. 548–554.

    Article  CAS  PubMed  Google Scholar 

  • Temm-Grove, C.J., Wert, D., Thompson, V.F., et al., Microinjection of calpastatin inhibits fusion in myoblasts, Exp. Cell Res., 1999, vol. 247, pp. 293–303.

    Article  CAS  PubMed  Google Scholar 

  • van den Thillart, G., Energy metabolism of swimming trout (Salmo gairdneri). Oxidation rates of palmitate, glucose, lactate, alanine, leucine and glutamate, J. Comp. Physiol. B, 1986, vol. 156, pp. 511–520.

    Article  Google Scholar 

  • Toyohara, H., Ito, K., Ando, M., et al., Effect of maturation on activities of various proteases and protease inhibitors in the muscle of ayu (Plecoglossus altivelis), Comp. Biochem. Physiol. B, 1991, vol. 99, pp. 419–424.

    Article  CAS  PubMed  Google Scholar 

  • Tripathi, G. and Verma, P., Starvation-induced impairment of metabolism in a freshwater catfish, Z. Naturforsch., A: Phys. Sci., 2003, vol. 58, pp. 446–451.

    CAS  Google Scholar 

  • Verrez-Bagnis, V., Ladrat, C., Noëlle, J., and Fleurence, J., In vitro proteolysis of myofibrillar and sarcoplasmic proteins of European sea bass (Dicentrarchus labrax L.) by an endogenous m-calpain, J. Sci. Food Agric., 2002, vol. 82, pp. 1256–1262.

    Article  CAS  Google Scholar 

  • Veselov, A.E. and Kalyuzhin, S.M., Ekologiya, povedenie i raspredelenie molodi atlanticheskogo lososya (Ecology, Behavior, and Distribution of Juvenile Atlantic Salmon), Petrozavodsk: Kareliya, 2001.

    Google Scholar 

  • Yamashita, M. and Konagaya, S., Differentiation and localization of catheptic proteinases responsible for extensive autolysis of mature chum salmon muscle (Oncorhynchus keta), Comp. Biochem. Physiol. B, 1992, vol. 103, no. 4, pp. 999–1003.

    Google Scholar 

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  1. Institute of Biology, Karelian Research Center, Russian Academy of Sciences, ul. Pushkinskaya, 11, Petrozavodsk, 185910, Russia

    N. N. Nemova, L. A. Lysenko & N. P. Kantserova

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  1. N. N. Nemova
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Original Russian Text © N.N. Nemova, L.A. Lysenko, N.P. Kantserova, 2016, published in Ontogenez, 2016, Vol. 47, No. 4, pp. 197–208.

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Nemova, N.N., Lysenko, L.A. & Kantserova, N.P. Degradation of skeletal muscle protein during growth and development of salmonid fish. Russ J Dev Biol 47, 161–172 (2016). https://doi.org/10.1134/S1062360416040068

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  • DOI: https://doi.org/10.1134/S1062360416040068

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