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Protein degradation systems in the skeletal muscles of parr and smolt Atlantic salmon Salmo salar L. and brown trout Salmo trutta L.

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Abstract

Although protein degradation limits the rate of muscle growth in fish, the role of proteolytic systems responsible for degrading myofibrillar proteins in skeletal muscle is not well defined. The study herein aims to evaluate the role of calpains (calcium-activated proteases) and proteasomes (ATP-dependent proteases) in mediating muscle protein turnover at different life stages in wild salmonids. Protease activities were estimated in Atlantic salmon (Salmo salar L.) and brown trout (Salmo trutta L.) parr and smolts from the Indera River (Kola Peninsula, Russia). Calpain and proteasome activities in Atlantic salmon skeletal muscles were lower in smolts as compared with parr. Reduced muscle protein degradation accompanying Atlantic salmon parr-smolt transformation appeared to provide intense muscle growth essential for a minimum threshold size achievement that is required for smoltification. Calpain and proteasome activities in brown trout parr and smolts at age 3+ did not significantly differ. However, calpain activity was higher in smolts brown trout 4+ as compared with parr, while proteasome activity was lower. Results suggest that brown trout smoltification does not correspond with intense muscle growth and is more facultative and plastic in comparison with Atlantic salmon smoltification. Obtained data on muscle protein degradation capacity as well as length-weight parameters of fish reflect differences between salmon and trout in growth and smoltification strategies.

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References

  • Agustsson T, Sundell K, Sakamoto T, Johansson V, Ando M, Björnsson B (2001) Growth hormone endocrinology of Atlantic salmon: pituitary gene expression, hormone storage, secretion, and plasma levels during parr-smolt transformation. J Endocrinol 170:227–234

    Article  CAS  PubMed  Google Scholar 

  • Amaral IP, Johnston IA (2011) Insulin-like growth factor (IGF) signalling and genome-wide transcriptional regulation in fast muscle of zebrafish following a single-satiating meal. J Exp Biol 214:2125–2139. doi:10.1242/jeb.053298

    Article  CAS  PubMed  Google Scholar 

  • Bagliniere JL, Champigneulle A (1986) Population estimates of juvenile Atlantic salmon, Salmo salar, as indices of smolt production in the R. Scorff, Brittany. J Fish Biol 29:467–482

    Article  Google Scholar 

  • Björnsson BT, Bradley TM (2007) Epilogue: past successes, present misconceptions and future milestones in salmon smoltification research. Aquaculture 273:384–391. doi:10.1016/j.aquaculture.2007.10.020

    Article  Google Scholar 

  • Björnsson BT, Johansson V, Benedet S, Einarsdottir IE, Hildahl J, Agustsson T, Jonsson E (2002) Growth hormone endocrinology of salmonids: regulatory mechanisms and mode of action. Fish Physiol Biochem 27:227–242. doi:10.1023/B:FISH.0000032728.91152.10

    Article  Google Scholar 

  • Björnsson BT, Stefansson SO, McCormick SD (2011) Environmental endocrinology of salmon smoltification. Gen Comp Endocrinol 170:290–298. doi:10.1016/j.ygcen.2010.07.003

    Article  PubMed  Google Scholar 

  • Bower NI, Johnston IA (2010) Transcriptional regulation of the IGF signaling pathway by amino acids and insulin-like growth factors during myogenesis in Atlantic salmon. PLoS One 5(6):e11100. doi:10.1371/journal.pone.0011100

    Article  PubMed  PubMed Central  Google Scholar 

  • Bower NI, Li X, Taylor R, Johnston IA (2008) Switching to fast growth: the insulin-like growth factor (IGF) system in skeletal muscle of Atlantic salmon. J Exp Biol 211:3859–3870. doi:10.1242/jeb.024117

    Article  CAS  PubMed  Google Scholar 

  • Bracewell P, Cowx IG, Uglov RF (2004) Effects of handling and electrofishing on plasma glucose and whole blood lactate of Leuciscus cephalus. J Fish Biol 64:65–71. doi:10.1046/j.1095-8649.2003.00281.x

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Cleveland BM, Weber GM (2010) Effects of insulin-like growth factor-I, insulin, and leucine on protein turnover and ubiquitin ligase expression in rainbow trout primary myocytes. Am J Physiol Regul Integr Comp Physiol 298:R341–R350. doi:10.1152/ajpregu.00516.2009

    Article  CAS  PubMed  Google Scholar 

  • Dêbowski P, Dobosz S, Grudniewska J, Kuzmiñski H (2010) Possibilities of using the length differentiation of hatchery sea trout, Salmo trutta m. Trutta L., parr to predict numbers of one-year smolts. Arch Pol Fish 18:51–58. doi:10.2478/v10086-010-0006-z

    Article  Google Scholar 

  • Enns DL, Belcastro AN (2006) Early activation and redistribution of calpain activity in skeletal muscle during hindlimb unweighting and reweighting. Can J Physiol Pharmacol 84:601–609

    Article  CAS  PubMed  Google Scholar 

  • Handeland SO, Porter M, Björnsson BT, Stefansson SO (2003) Osmoregulation and growth in a wild and a selected strain of Atlantic salmon smolts on two photoperiod regimes. Aquaculture 222:29–43. doi:10.1111/jfb.1248

    Article  Google Scholar 

  • Hevrøy EM, Azpeleta C, Shimizu M, Lanzén A, Kaiya H, Espe M, Olsvik PA (2011) Effects of short-term starvation on ghrelin. GH-IGF system, and IGF-binding proteins in Atlantic salmon Fish Physiol Biochem 37:217–232. doi:10.1007/s10695-010-9434-3

    PubMed  Google Scholar 

  • Johnston IA, Bower NI, Macqueen DJ (2011) Growth and the regulation of myotomal muscle mass in teleost fish. J Exp Biol 214:1617–1628. doi:10.1242/jeb.038620

    Article  CAS  PubMed  Google Scholar 

  • Jones DA, Bergman E, Greenberg L (2015) Food availability in spring affects smolting in brown trout (Salmo trutta). Can J Fish Aquat Sci 72:1694–1699. doi:10.1139/cjfas-2015-0106

    Article  Google Scholar 

  • Kaushik SJ, Luquet P (1979) Influence of dietary amino acid patterns on the free amino acid contents of blood and muscle of rainbow trout (Salmo gairdnerii R.) Comp Biochem Physiol B 64:175–180. doi:10.1016/0305-0491(79)90157-3

    Article  CAS  PubMed  Google Scholar 

  • Klemetsen A, Amundsen P-A, Dempson JB, Jonsson B, Jonsson N, O’Connell MF, Mortensen E (2003) Atlantic salmon Salmo salar L., brown trout Salmo trutta L. and Arctic charr Salvelinus alpinus (L.): a review of aspects of their life histories. Ecol Freshw Fish 12:1–59. doi:10.1034/j.1600-0633.2003.00010.x

    Article  Google Scholar 

  • Kolditz C, Borthaire M, Richard N, Corraze G, Panserat S, Vachot C, Lefevre F, Medale F (2008) Liver and muscle metabolic changes induced by dietary energy content and genetic selection in rainbow trout (Oncorhynchus mykiss). Am J Physiol Integr Comp Physiol 294:1154–1164. doi:10.1152/ajpregu.00766.2007

    Article  Google Scholar 

  • Kristinsson JB, Saunders RL, Wiggs AJ (1985) Growth dynamics during the development of bimodal length-frequency distribution in juvenile Atlantic salmon (Salmo salar L.) Aquaculture 45:1–20

    Article  Google Scholar 

  • Leonko AA, Chernitskiy AG (1986) Comparative analysis of smolt migration of Atlantic salmon, Salmo salar, and sea trout, Salmo trutta. J Ichthyol 26:113–118

    Google Scholar 

  • Lysenko LA, Kantserova NP, Krupnova MY, Veselov AE, Nemova NN (2015) Intracellular protein degradation in the development of the Atlantic salmon Salmo salar L. Russ J Bioorg Chem 41(6):645–651. doi:10.1134/S1068162015060096

    Article  CAS  Google Scholar 

  • Marshall WS (2002) Na+, Cl, Ca2+ and Zn2+ transport by fish gills: retrospective review and prospective synthesis. J Exp Zool 293:264–283

    Article  CAS  PubMed  Google Scholar 

  • McCormick SD (1994) Ontogeny and evolution of salinity tolerance in anadromous salmonids: hormones and heterochrony. Estuaries 17:26–33

    Article  CAS  Google Scholar 

  • McCormick SD, Björnsson BT, Sheridan M, Eilertson C, Carey JB, O’Dea M (1995) Increased daylength stimulates plasma growth hormone and gill Na+, K+-ATPase in Atlantic salmon (Salmo salar). J Comp Physiol B 165:245–254

    Article  CAS  Google Scholar 

  • McCormick SD, Hansen LP, Quinn TP, Saunders RL (1998) Movement, migration, and smolting of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 55(1):77–92. doi:10.1139/d98-011

    Article  Google Scholar 

  • McCormick SD, Moriyama S, Björnsson BT (2000) Low temperature limits the photoperiod control of smolting in Atlantic salmon through endocrine mechanisms. Am J Phys 278:R1352–R1361

    CAS  Google Scholar 

  • McCormick SD, Shrimpton JM, Moriyama S, Björnsson BT (2002) Effects of an advanced temperature cycle on smolt development and endocrinology indicate that temperature is not a zeitgeber for smolting in Atlantic salmon. J Exp Biol 205:3553–3560

    PubMed  Google Scholar 

  • Metcalfe NB, Huntingford FA, Thorpe JE (1988) Feeding intensity, growth rates, and the establishment of life-history patterns in juvenile Atlantic salmon Salmo salar. J Anim Ecol 57(2):463–474. doi:10.2307/4918

    Article  Google Scholar 

  • Mommsen TP (2004) Salmon spawning migration and muscle protein metabolism: the August Krogh principle at work. Comp Biochem Physiol B Biochem Mol Biol 139:383–400. doi:10.1016/j.cbpc.2004.09.018

    Article  PubMed  Google Scholar 

  • Nemova NN, Lysenko LA, Kantserova NP (2016) Degradation of the skeletal muscles proteins in salmonid fish growth and development. Rus J Dev Biol 4:161–172. doi:10.1134/S1062360416040068

    Article  Google Scholar 

  • Nicieza AG, Reyesgavilan FG, Brana F (1994) Differentiation in juvenile growth and bimodality patterns berween northern and southern populations of Atlantic salmon (Salmo salar L.) Can J Zool 72:1603–1610. doi:10.1139/z94-213

    Article  Google Scholar 

  • Olsson IC, Greenberg LA, Bergman E, Wysujack K (2006) Environmentally induced migration: the importance of food. Ecol Lett 9(6):645–651. doi:10.1111/j.1461-0248.2006.00909.x

    Article  PubMed  Google Scholar 

  • Overturf K, Gaylord TG (2009) Determination of relative protein degradation activity at different life stages in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol Part B 152(2):150–160. doi:10.1016/j.cbpb.2008.10.012

    Article  Google Scholar 

  • Quigley DTG, Harvey MJ, Hayden TJ, Dowling C, O’ Keane MP (2006) A comparative study of smoltification in sea trout (Salmo trutta L.) and Atlantic salmon (Salmo salar L.): seawater tolerance and thyroid hormone titres. Biology and Environment: Proceedings of the Royal Irish Academy 106B(1):35–47

    Google Scholar 

  • Rodgers KJ, Dean RT (2003) Assessment of proteasome activity in cell lysates and tissue homogenates using peptide substrates. Int J Biochem Cell Biol 35:716–727. doi:10.1016/S1357-2725(02)00391-6

    Article  CAS  PubMed  Google Scholar 

  • Salem M, Kenney B, Killefer J, Nath J (2004) Isolation and characterization of calpains from rainbow trout muscle and their role in texture development. J Muscle Foods 15:245–255

    Article  CAS  Google Scholar 

  • Salem M, Nath J, Rexroad C, Killefer J, Yao J (2005a) Identification and molecular characterization of the rainbow trout calpains (Capn1 and Capn2): their expression in muscle wasting during starvation. Comp Biochem Physiol B 140:63–71. doi:10.1016/j.cbpc.2004.09.007

    Article  PubMed  Google Scholar 

  • Salem M, Yao J, Rexroad C, Kenney B, Semmens K, Killefer J, Nath J (2005b) Characterization of calpastatin gene in fish: its potential role in muscle growth and fillet quality. Comp Biochem Physiol B 141:488–497. doi:10.1016/j.cbpc.2005.05.012

    Article  PubMed  Google Scholar 

  • Schreck C, Whaley R, Bass M, Maughan O, Solazzi M (1976) Physiological responses of rainbow trout (Salmo gairdneri) to electroshock. J Fish Res Board Can 33:76–84

    Article  CAS  Google Scholar 

  • Seear P, Carmichael S, Talbot R, Taggart J, Bron J, Sweeney G (2010) Differential gene expression during smoltification of Atlantic salmon (Salmo salar L.): a first large-scale microarray study. Mar Biotechnol 12:126–140. doi:10.1007/s10126-009-9218-x

    Article  CAS  PubMed  Google Scholar 

  • Seiliez I, Panserat S, Skiba-Cassy S, Fricot A, Vachot C, Kaushik S, Tesseraud S (2008) Feeding status regulates the polyubiquitination step of the ubiquitin-proteasome-dependent proteolysis in rainbow trout (Oncorhynchus mykiss) muscle. J Nutr 138:487–491. doi:10.1186/1743-7075-10-28

    CAS  PubMed  Google Scholar 

  • Sheridan MA (1989) Alterations in lipid metabolism accompanying smoltification and seawater adap tation of salmonid fish. Aquaculture 82:191–203

    Article  CAS  Google Scholar 

  • Shrimpton JM, Bernier N, Randall DJ (1994) Changes in cortisol dynamics in wild and hatchery-reared juvenile coho salmon (Oncorhynchus kisutch) during smoltification. Can J Fish Aquat Sci 54:2179–2187

    Article  Google Scholar 

  • Sower AS, Karlson KH, Fawcett RS (1992) Changes in plasma thyroxine, estradiol-7b, and 17a, 20b-dihydroxy-4-pregnen-3-one during smoltification of coho salmon. Gen Comp Endocrinol 85:278–285

    Article  CAS  PubMed  Google Scholar 

  • Stefansson SO, Björnsson BT, Ebbesson LOE, McCormick SD (2008) Smoltification. In: Finn RN, Kapoor BG (eds) Fish larval physiology. Science Publishers, Enfield, pp 639–681

    Google Scholar 

  • Tanguy JM, Ombredane D, Bagliniere JL, Prunet P (1994) Aspects of parr-smolt transformation in anadromous and resident forms of brown trout (Salmo trutta) in comparison with Atlantic salmon (Salmo salar). Aquaculture 121(1–3):51–63

    Article  Google Scholar 

  • Thorpe JE (1977) Bimodal distribution of length of juvenile Atlantic salmon (Salmo salar L.) under artificial rearing conditions. J Fish Biol 11:175–184

    Article  Google Scholar 

  • Thorpe JE, Talbot C, Villarreal C (1982) Bimodality of growth and smolting in Atlantic salmon, Salmo salar L. Aquaculture 28:123–132

    Article  CAS  Google Scholar 

  • Thorstad EB, Økland F, Finstad B, Rolf S, Plantalech N, Bjørn PA, McKinley RS (2007) Fjord migration and survival of wild and hatchery-reared Atlantic salmon and wild brown trout post-smolts. Hydrobiologia 582:99–107. doi:10.1007/s10750-006-0548-7

    Article  Google Scholar 

  • VanderKooi S, Maule A, Schreck C (2001) The effects of electroshock on immune function and disease progression in juvenile spring chinook salmon. Trans Am Fish Soc 130(3):397–408

    Article  Google Scholar 

  • Winans GA, Nishioka RS (1987) A multivariate description of change in body shape of coho salmon (Oncorhynchus kisutch) during smoltification. Aquaculture 66:35–45

    Article  Google Scholar 

  • Woolmer A, Maxwell E, Lart W (2011) SIPF C0083-effects of electrofishing for Ensis spp. on benthic macrofauna, epifauna and fish species. Seafish Report SR 652:57

    Google Scholar 

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Acknowledgments

Salmonid fish catch and study were conducted in the accordance with a resolution no. 51 2015 03 0119 by Barentsevo-Belomorskoye territorial department of the Federal Agency for Fisheries. We are grateful to Denis Efremov and Mikhail Ruchyev for their assistance in field experiments. The research was supported by the Russian Scientific Foundation, project 14-24-00102 “Salmonids of the northwestern Russia: Ecological and biochemical mechanisms of the early development”.

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Correspondence to Nadezda P. Kantserova.

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Kantserova, N.P., Lysenko, L.A., Veselov, A.E. et al. Protein degradation systems in the skeletal muscles of parr and smolt Atlantic salmon Salmo salar L. and brown trout Salmo trutta L.. Fish Physiol Biochem 43, 1187–1194 (2017). https://doi.org/10.1007/s10695-017-0364-1

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