Molecular Adaptive Mechanisms in the Cardiac Muscle of Exercised Fish

  • Harald Takle
  • Vicente Castro


This chapter reviews the current knowledge on molecular adaptive mechanisms in the cardiac muscle in response to swimming-induced exercise. Although an impressive and fruitful effort has been committed in the last 50 years to understand the cardiovascular and systemic effects that exercise training produces in fish, very little is known regarding the molecular adaptive mechanisms behind these effects. We present and discuss available information related to mRNA and protein expression adaptations that may further substantiate the exercise training benefits to the cardiac system in fish. In particular, we review molecular mechanisms related to cardiac growth, contractility, energy metabolism, vascularization, and hematopoiesis. In light of the intriguing benefits of exercise training to improve disease resistance in fish, we present an overview of exercise-induced cardiac immune adaptations including inflammatory, complement, and tissue protective responses. Altogether, exercise training seems to promote molecular adaptations that strengthen the overall cardiac capacity and immune competence.


Vascular Endothelial Growth Factor Rainbow Trout Exercise Training Sarcoplasmic Reticulum Proliferate Cell Nuclear Antigen 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Aho E, Vornanen M (2001) Cold acclimation increases basal heart rate but decreases its thermal tolerance in rainbow trout (Oncorhynchus mykiss). J Comp Physiol B 171:173–179PubMedGoogle Scholar
  2. Allen RG, Tresini M (2000) Oxidative stress and gene regulation. Free Radic Biol Med 28:463–499PubMedGoogle Scholar
  3. Alne H, Thomassen MS, Takle H, Terjesen BF, Grammes F, Oehme M, Refstie S, Sigholt T, Berge RK, Rørvik KA (2009) Increased survival by feeding tetradecylthioacetic acid during a natural outbreak of heart and skeletal muscle inflammation in S0 Atlantic salmon, Salmo salar L. J Fish Dis 32:953–961PubMedGoogle Scholar
  4. Anttila K, Manttari S, Jarvilehto M (2006) Effects of different training protocols on Ca2+ handling and oxidative capacity in skeletal muscle of Atlantic salmon (Salmo salar L.). J Exp Biol 209:2971–2978PubMedGoogle Scholar
  5. Anttila K, Jarvilehto M, Manttari S (2008) The swimming performance of brown trout and whitefish: the effects of exercise on Ca2+ handling and oxidative capacity of swimming muscles. J Comput Phys B 178:465–475Google Scholar
  6. Avellini L, Chiaradia E, Gaiti A (1999) Effect of exercise training, selenium and vitamin E on some free radical scavengers in horses (Equus caballus). Comp Biochem Phys B 123:147–154Google Scholar
  7. Bailey JR, West JL, Driedzic WR (1997) Heart growth associated with sexual maturity in male rainbow trout (Oncorhynchus mykiss) is hyperplastic. Comp Biochem Physiol B 188:607–611Google Scholar
  8. Bernardo BC, Weeks KL, Pretorius L, McMullen JR (2010) Molecular distinction between physiological and pathological cardiac hypertrophy: experimental findings and therapeutic strategies. Pharmacol Ther 128:191–227PubMedGoogle Scholar
  9. Bloor CM, Leon AS (1970) Interaction of age and exercise on the heart and its blood supply. Lab Investig 22:160–165PubMedGoogle Scholar
  10. Boshra H, Li J, Sunyer JO (2006) Recent advances on the complement system of teleost fish. Fish Shellfish Immun 20:239–262Google Scholar
  11. Bowie AG, Haga IR (2005) The role of toll-like receptors in the host response to viruses. Mol Immunol 42:859–867PubMedGoogle Scholar
  12. Brown MD (2003) Exercise and coronary vascular remodelling in the healthy heart. Exp Physiol 88:645–658PubMedGoogle Scholar
  13. Bruunsgaard H, Pedersen BK (2003) Age-related inflammatory cytokines and disease. Immunol Allergy Clin 23:15–39Google Scholar
  14. Castro V, Grisdale-Helland B, Helland SJ, Kristensen T, Jørgensen SM, Helgerud J, Claireaux G, Farrell AP, Krasnov A, Takle H (2011) Aerobic training stimulates growth and promotes disease resistance in Atlantic salmon (Salmo salar). Comp Biochem Phys A 160:278–290Google Scholar
  15. Chou CF, Tohari S, Brenner S, Venkatesh B (2004) Erythropoietin gene from a teleost fish, Fugu rubripes. Blood 104:1498–1503PubMedGoogle Scholar
  16. Chu CY, Cheng CH, Yang CH, Huang CJ (2008) Erythropoietins from teleosts. Cell Mol Life Sci 65:3545–3552PubMedGoogle Scholar
  17. Claireaux G, McKenzie DJ, Genge AG, Chatelier A, Aubin J, Farrell AP (2005) Linking swimming performance, cardiac pumping ability and cardiac anatomy in rainbow trout. J Exp Biol 208:1775–1784PubMedGoogle Scholar
  18. Clark RJ, Rodnick KJ (1998) Morphometric and biochemical characteristics of ventricular hypertrophy in male rainbow trout (Oncorhynchus mykiss). J Exp Biol 210:1541–1552Google Scholar
  19. Dane S, Taysi S, Gul M, Akcay F, Gunal A (2008) Acute exercise induced oxidative stress is prevented in erythrocytes of male long distance athletes. Biol Sport 25:115–124Google Scholar
  20. Davie PS, Farrell AP (1991) The coronary and luminal circulations of the myocardium of fishes. Can J Zool 69:1993–2001Google Scholar
  21. Davie PS, Wells RMG, Tetens V (1986) Effects of sustained swimming on rainbow trout muscle structure, blood oxygen transport, and lactate dehydrogenase isozymes: evidence for increased aerobic capacity of white muscle. J Exp Zool 237:159–171PubMedGoogle Scholar
  22. Davison W (1994) Exercise training in the banded wrasse Notolabrus fucicola affects muscle fibre diameter but not muscle mitochondrial morphology. NZ Nat Sci 21:11–16Google Scholar
  23. Davison W (1997) The effects of exercise training on teleost fish, a review of recent literature. Comp Biochem Physiol A 117:67–75Google Scholar
  24. De Caterina R, Basta G (2001) n−3 fatty acids and the inflammatory response-biological background. Eur Heart J Suppl 3D:D42–D49Google Scholar
  25. Ellis AE, Cavaco A, Petrie A, Lockhart K, Snow M, Collet B (2010) Histology, immunocytochemistry and qRT-PCR analysis of Atlantic salmon, Salmo salar L., post-smolts following infection with infectious pancreatic necrosis virus (IPNV). J Fish Dis 33:803–818PubMedGoogle Scholar
  26. Farrell AP (1991) From hagfish to tuna—a perspective on cardiac function in fish. Physiol Zool 64:1137–1164Google Scholar
  27. Farrell AP (2002) Coronary arteriosclerosis in salmon: growing old or growing fast? Comp Biochem Physiol A 132:723–735Google Scholar
  28. Farrell AP, Clutterham SM (2003) On-line venous oxygen tensions in rainbow trout during graded exercise at two acclimation temperatures. J Exp Biol 206:487–496PubMedGoogle Scholar
  29. Farrell AP, Hammons AM, Graham MS, Tibbits GF (1988) Cardiac growth in rainbow trout, Salmo gairdneri. Can J Zool 66:2368–2373Google Scholar
  30. Farrell AP, Johansen JA, Steffensen JF, Moyes CD, West TG, Suarez K (1990) Effects of exercise training and coronary ablation on swimming performance, heart size, and cardiac enzymes in rainbow trout, Oncorhynchus mykiss. Can J Zool 68:1174–1179Google Scholar
  31. Farrell AP, Johansen JA, Suarez RK (1991) Effects of exercise training on cardiac performance and muscle enzymes in rainbow trout, Oncorhynchus mykiss. Fish Physiol Biochem 9:303–312Google Scholar
  32. Ferreira JCB, Bacurau AV, Bueno Junior CR, Cunha TC, Tanaka LY, Jardim MA, Ramires PR, Brum PC (2010) Aerobic exercise training improves Ca2+ handling and redox status of skeletal muscle in mice. Exp Biol Med 235:497–505Google Scholar
  33. Fill M, Copello JA (2002) Ryanodine receptor calcium release channels. Physiol Rev 82:893–922PubMedGoogle Scholar
  34. Gallaugher PE, Thorarensen H, Kiessling A, Farrell AP (2001) Effects of high intensity exercise training on cardiovascular function, oxygen uptake, internal oxygen transport and osmotic balance in Chinook salmon (Oncorhynchus tshawytscha) during critical speed swimming. J Exp Biol 204:2861–2872PubMedGoogle Scholar
  35. Gamperl AK, Farrell AP (2004) Cardiac plasticity in fishes: environmental influences and intraspecific differences. J Exp Biol 207:2539–2550PubMedGoogle Scholar
  36. Gleeson M (2007) Immune function in sport and exercise. J Appl Physiol 103:693–699PubMedGoogle Scholar
  37. Graham MS, Farrell AP (1989) The effect of temperature acclimation and adrenaline on the performance of a perfused trout heart. Physiol Zool 62:38–61Google Scholar
  38. Greer Walker M, Emerson L (1978) Sustained swimming speeds and myotomal muscle function in the trout, Salmo gairdneri. J Fish Biol 13:475–481Google Scholar
  39. Hardie DG, Sakamoto K (2006) AMPK: a key sensor of fuel and energy status in skeletal muscle. Physiology 21:48–60PubMedGoogle Scholar
  40. Hardie DG, Hawley SA, Scott JW (2006) AMP-activated protein kinase—development of the energy sensor concept. J Physiol 574:7–15PubMedGoogle Scholar
  41. Haugland O, Mikalsen AB, Nilsen P, Lindmo K, Thu BJ, Eliassen TM, Roos N, Rode M, Evensen O (2011) Cardiomyopathy syndrome of Atlantic salmon (Salmo salar L.) is caused by a dsRNA virus of the Totiviridae family. J Virol 85:5275–5286PubMedGoogle Scholar
  42. Henry MA, Alexis MN, Fountoulaki E, Nengas I, Rigos G (2009) Effects of a natural parasitical infection (Lernanthropus kroyeri) on the immune system of European sea bass, Dicentrarchus labrax. Parasite Immunol 31:729–740PubMedGoogle Scholar
  43. Hochachka P (1961) Effects of physical training on oxygen debt and glycogen reserves in trout. Can J Zool 39:767–776Google Scholar
  44. Houlihan DF, Laurent P (1987) Effects of exercise training on the performance, growth, and protein-turnover of rainbow-trout (Salmo gardnieri). Can J Fish Aquat Sci 44:1614–1621Google Scholar
  45. Iemitsu A, Maeda S, Jesmin S, Otsuki T, Miyauchi T (2006) Exercise training improves aging-induced downregulation of VEGF angiogenic signaling cascade i hearts. Am J Physiol Heart Circ Physiol 291:H1290–H1298PubMedGoogle Scholar
  46. Iliev DB, Jørgensen SM, Rode M, Krasnov A, Harneshaug I, Jørgensen JB (2010) CpG-induced secretion of MHCIIbeta and exosomes from salmon (Salmo salar) APCs. Dev Comp Immunol 34:29–41PubMedGoogle Scholar
  47. Itoh H, Ohkuwa T, Yamamoto T, Sato Y, Miyamura M, Naoi M (1998) Effects of endurance physical training on hydroxyl radical generation in rat tissues. Life Sci 63:1921–1929PubMedGoogle Scholar
  48. Jager S, Handschin C, St-Pierre J, Spiegelman B (2007) AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1α. Proc Nat Acad Sci 104:12017–12022PubMedGoogle Scholar
  49. Jørgensen SM, Hetland DL, Press CM, Grimholt U, Gjøen T (2007) Effect of early infectious salmon anaemia virus (ISAV) infection on expression of MHC pathway genes and type I and II interferon in Atlantic salmon (Salmo salar L.) tissues. Fish Shellfish Immun 23:576–588Google Scholar
  50. Jørgensen SM, Afanasyev S, Krasnov A (2008) Gene expression analyses in Atlantic salmon challenged with infectious salmon anemia virus reveal differences between individuals with early, intermediate and late mortality. BMC Genomics 9:179PubMedGoogle Scholar
  51. Keen JE, Farrell AP (1994) Maximum prolonged swimming speed and maximum cardiac performance of rainbow trout, Oncorhynchus mykiss, acclimated to two different water temperatures. Comp Biochem Physiol 108A:287–295Google Scholar
  52. Keen JE, Farrell AP, Tibbits GF, Brill RW (1992) Cardiac physiology in tunas. II. Effect of ryanodine calcium and adrenaline on force-frequency relationships in atrial strips from skipjack tuna, Katsuwonus pelamis. Can J Zool 70:1211–1217Google Scholar
  53. Kojda G, Hambrecht R (2005) Molecular mechanisms of vascular adaptations to exercise. Physical activity as an effective antioxidant therapy? Cardiovasc Res 67:187–197PubMedGoogle Scholar
  54. Kristensen T, Haugen TO, Rosten T, Fjellheim A, Atland A, Rosseland BO (2011) Effects of production intensity and production strategies in commercial Atlantic salmon smolt (Salmo salar L.) production on subsequent performance in the early sea stage. Fish Physiol Biochem (in press). doi:  10.1007/s10695-011-9566-0
  55. Lanctin HP, McMorran LG, Driedzic WR (1980) Rates of glucose and lactate oxidation by the perfused isolated trout (Salvelinus fontinalis) heart. Can J Zool 58:1708–1711PubMedGoogle Scholar
  56. Landeira-Fernandez AM, Morrissette JM, Blank JM, Block BA (2004) Temperature dependence of the Ca2+ -ATPase (SERCA2) in the ventricles of tuna and mackerel. Am J Physiol Regul Integr Comp Physiol 286:R398–R404PubMedGoogle Scholar
  57. Lehman JJ, Kelly DP (2002) Transcriptional activation of energy metabolic switches in the developing and hypertrophied heart. Clin Exp Pharmacol P 29:339–345Google Scholar
  58. Lehman JJ, Barger PM, Kovacs A, Saffitz JE, Medeiros DM, Kelly DP (2000) Peroxisome proliferator-activated receptor γ coactivator-1 promotes cardiac mitochondrial biogenesis. J Clin Invest 106:847–856PubMedGoogle Scholar
  59. Leosco D, Rengo, G. Iaccarino G, Golino L, Marchese M, Fortunato F, Zincarelli C, Sanzari E, Ciccarelli M, Galasso G, Altobelli GG, Conti V, Matrone G, Cimini V, Ferrara N, Filipelli A, Koch WJ, Rengo F (2008) Exercise promotes angiogenesis and improves -adrenergic receptor signaling in the post-ischaemic failing rat heart. Cardiovasc Res 78:385–394Google Scholar
  60. Lovoll M, Wiik-Nielsen J, Grove S, Wiik-Nielsen CR, Kristoffersen AB, Faller R, Poppe T, Jung J, Pedamallu CS, Nederbragt AJ, Meyerson M, Rimstad E, Tengs T (2010) A novel totivirus and piscine reovirus (PRV) in Atlantic salmon (Salmo salar) with cardiomyopathy syndrome (CMS). Virol J 7:309. doi: 10.1186/1743-422X-7-309 PubMedGoogle Scholar
  61. Magnoni LJ, Vraskou Y, Palstra AP, Planas JV (2012) AMP-activated protein kinase plays an important evolutionary conserved role in the regulation of glucose metabolism in fish skeletal muscle cells. PLoS ONE 7:e31219. doi: 10.1371/journal.pone.0031219 PubMedGoogle Scholar
  62. Manttari S, Anttila K, Kaakinen M, Jarvilehto M (2006) Effects of low-intensity training on dihydropyridine and ryanodine receptor content in skeletal muscle of mouse. J Physiol Biochem 62:293–302Google Scholar
  63. Mathur N, Pedersen BK (2008) Exercise as a mean to control low-grade systemic inflammation. Mediat Inflamm Art ID. 109502, p 6Google Scholar
  64. Michiels C, Raes M, Toussiant O, Remacle J (1994) Importance of Se-glutathione peroxidase, catalase, and Cu/Zn-SOD for cell survival against oxidative stress. Free Radic Biol Med 17:235–248PubMedGoogle Scholar
  65. Milligan CL, Farrell AP (1991) Lactate utilization by an in situ perfused trout heart: effects of workload and blockers of lactate transport. J Exp Biol 155:357–373Google Scholar
  66. Moran M, Saborido A, Megias A (2003) Ca2+ regulatory systems in rat myocardium are altered by 24 weeks treadmill training. Pflug Arch Eur J Phy 446:161–168Google Scholar
  67. Moyes CD (1996) Cardiac metabolism in high performance fish. Comp Biochem Physiol A 113:69–75Google Scholar
  68. Moyes CD, Mathieu-Costello O, Brill RW, Hochachka PW (1992) Mitochondrial metabolism of cardiac and skeletal muscles from a fast (Katsuwonus pelamis) and a slow (Cyprinus carpio) fish. Can J Zool 70:1246–1253Google Scholar
  69. Murphy K, Travers P, Walport M (2008) Janeway’s immunology, 7th edn. Garland Science, New YorkGoogle Scholar
  70. Navarro A, Gomez C, Lopez-Cepero JM, Boveris A (2004) Beneficial effects of moderate exercise on mice ageing: survival, behavior, oxidative stress, and mitochondrial electron transfer. Am J Physiol Reg Integr Comp Physiol 286:R505–R511Google Scholar
  71. Neely JR, Rovetto MJ, Oram JF (1972) Myocardial utilization of carbohydrate and lipids. Prog Cardiovasc Dis 15:289–329PubMedGoogle Scholar
  72. Neufer PD, Dohm GL (1993) Exercise induces a transient increase in transcription of the GLUT-4 gene in skeletal muscle. Am J Cell Physiol 265:1597–1603Google Scholar
  73. Nielsen JN, Wojtaszewski JFP, Haller RG, Hardie DG, Kemp BE, Richter EA, Vissing J (2002) Role of 5’AMP-activated protein kinase in glycogen synthase activity and glucose utilization: insights from patients with McArdle’s disease. J Physiol 541(3):979–989PubMedGoogle Scholar
  74. Palacios G, Lovoll M, Tengs T, Hornig M, Hutchison S, Hui J, Kongtorp RT, Savji N, Bussetti AV, Solovyov A, Kristoffersen AB, Celone C, Street C, Trifonov V, Hirschberg DL, Rabadan R, Egholm M, Rimstad E, Lipkin WI (2010) Heart and skeletal muscle inflammation of farmed salmon is associated with infection with a novel reovirus. PLoS ONE 5:e11487. doi: 10.1371/journal.pone.0011487 PubMedGoogle Scholar
  75. Pahl HL (1999) Activators and target genes of Rel/NF-κB transcription factors. Oncogene 18:6853–6866PubMedGoogle Scholar
  76. Palstra AP, Planas JV (2011) Fish under exercise. Fish Physiol Biochem 37:259–272PubMedGoogle Scholar
  77. Patey CP, Driedzic WR (1997) Cold acclimation increases activities of mitochondrial long-chain acyl-CoA synthetase and carnitine acyl-CoA transferase I in heart of rainbow trout (Oncorhynchus mykiss). Can J Zool 75:324–331Google Scholar
  78. Peatman E, Terhune J, Baoprasertkul P, Xu P, Nandi S, Wang S, Somridhivej B, Kucuktas H, Li P, Dunham R, Liu Z (2008) Microarray analysis of gene expression in the blue catfish liver reveals early activation of the MHC class I pathway after infection with Edwardsiella ictaluri. Mol Immunol 45:553–566PubMedGoogle Scholar
  79. Polakof S, Panserat S, Craig PM, Martyres DJ, Plagnes-Juan E, Savari S, Aris-Brosou S, Moon TW (2011) The metabolic consequences of hepatic AMP-kinase phosphorylation in rainbow trout. PLoS ONE 6:e20228. doi: 10.1371/journal.pone.0020228 PubMedGoogle Scholar
  80. Poppe TT, Johansen R, Gunnes G, Torud B (2003) Heart morphology in wild and farmed Atlantic salmon Salmo salar and rainbow trout Oncorhynchus mykiss. Dis Aquat Org 57:103–108PubMedGoogle Scholar
  81. Robertsen B (2006) The interferon system of teleost fish. Fish Shellfish Immunol 20:172–191PubMedGoogle Scholar
  82. Robertsen B (2008) Expression of interferon and interferon-induced genes i salmonids in response to virus infection, interferon-inducing compounds and vaccination. Fish Shellfish Immunol 25:351–357PubMedGoogle Scholar
  83. Rolim NPL, Medeiros A, Rosa KT, Mattos KC, Irigoyen MC, Krieger EM, Krieger JE, Negrao CE, Brum PC (2007) Exercise training improves the net balance of cardiac Ca2+ handling protein expression in heart failure. Physiol Genomics 29:246–252PubMedGoogle Scholar
  84. Roy D, Marette A (1996) Exercise induces the translocation of GLUT4 to transverse tubules from an intracellular pool in rat skeletal muscle. Biochem Biophys Res Commun 223:147–152PubMedGoogle Scholar
  85. Saborido A, Molano F, Moro G, Megias A (1995) Regulation of dihydropyridine receptor levels in skeletal and cardiac muscle by exercise training. Pflug Arch Eur J Phys 429:364–369Google Scholar
  86. Samuel CE (2001) Antiviral actions of interferons. Clin Microbiol Rev 14:78–809Google Scholar
  87. Sänger AM, Pötscher U (2000) Endurance exercise training affects fast white axial muscle in the cyprinid species Chalcalburnus chalcoides mento (Agassiz, 1832), cyprinidae, teostei. Basic Appl Myol 10:297–300Google Scholar
  88. Santer RM, Greer Walker M, Emerson L, Witthames PR (1983) On the morphology of the heart ventricle in marine teleost fish (Teleostei). Comp Biochem Physiol A 76:453–457Google Scholar
  89. Satchell GH (1991) Physiology and form of fish circulation. Cambridge University Press, New YorkGoogle Scholar
  90. Sephton DH, Driedzic WR (1995) Low temperature acclimation decreases rates of protein synthesis in rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 14:63–69Google Scholar
  91. Shiels HA, Farrell AP (2000) The effect of ryanodine on isometric tension development in isolated ventricular trabeculae from Pacific mackerel (Scomber japonicus). Comp Biochem Physiol A 125:331–341Google Scholar
  92. Shiels HA, Freund EV, Farrell AP, Block BA (1999) The sarcoplasmic reticulum plays major role in isometric contraction in atrial muscle of yellowfin tuna. J Exp Biol 202:881–890PubMedGoogle Scholar
  93. Silva LA, Pinho CA, Scarabelot KS, Fraga DB, Volpato AMJ, Boeck CR, De Souza CT, Streck EL, Pinho R (2009) Physical exercise increases mitochondrial function and reduces oxidative damage in skeletal muscle. Eur J Appl Physiol 105:861–867PubMedGoogle Scholar
  94. Simonot DL, Farrell AP (2007) Cardiac remodelling in rainbow trout Oncorhynchus mykiss Walbaum in response to phenylhydrazine-induced anaemia. J Exp Biol 210:2574–2584PubMedGoogle Scholar
  95. Simonot DL, Farrell AP (2009) Coronary vascular volume remodeling in rainbow trout Oncorhynchus mykiss. J Fish Biol 75:1762–1772PubMedGoogle Scholar
  96. Skugor S, Jørgensen SM, Gjerde B, Krasnov A (2009) Hepatic gene expression profiling reveals protective responses in Atlantic salmon vaccinated against furunculosis. BMC Genomics 10:503PubMedGoogle Scholar
  97. Smail DA, Bain N, Bruno DW, King JA, Thompson F, Pendrey DJ, Morrice S, Cunningham CO (2006) Infectious pancreatic necrosis virus in Atlantic salmon, Salmo salar L., post-smolts in the Shetland Isles, Scotland: virus identification, histopathology, immunohistochemistry and genetic comparison with Scottish mainland isolates. J Fish Dis 29:31–41PubMedGoogle Scholar
  98. Soonpaa MH, Kim KK, Pajak L, Franklin M, Field LJ (1996) Cardiomyocyte DNA synthesis and binucleation during murine development. Am J Physiol Heart C 271:H2183–H2189Google Scholar
  99. Sun X, Hoage T, Bai P, Ding Y, Chen Z, Zhang R, Huang W, Jahangir A, Paw B, Li YG, Xu X (2009) Cardiac hypertrophy involves both myocyte hypertrophy and hyperplasia in anemic zebrafish. PLoS ONE 4:e6596. doi: 10.1371/journal.pone.0006596 PubMedGoogle Scholar
  100. Thorarensen H, Gallaugher PE, Kiessling AK, Farrell AP (1993) Intestinal blood flow in swimming chinook salmon Oncorhynchus tshawytscha and the effects of haematocrit on blood flow distribution. J Exp Biol 179:115–129Google Scholar
  101. Tibbits GF, Moyes CD, Hove-Madsen L (1992) Excitation-contraction coupling in the teleost heart. In: Hoar WS, Randall DJ, Farrell AP (eds) The cardiovascular system. Academic Press, San Diego, pp 267–304Google Scholar
  102. Timmerhaus G, Krasnov A, Nilsen P, Alarcon M, Afanasyev S, Rode M, Takle H, Jørgensen SM (2011) Transcriptome profiling of immune responses to cardiomyopathy syndrome (CMS) in Atlantic salmon. BMC Genomics 12:459PubMedGoogle Scholar
  103. Tomanek RJ (1970) Effects of age and exercise on the extent of the myocardial capillary bed. Anat Rec 167:55–62PubMedGoogle Scholar
  104. Tota B (1983) Vascular and metabolic zonation in the ventricular myocardium of mammals and fishes. Comp Biochem Physiol A 76:423–437PubMedGoogle Scholar
  105. Urso ML, Clarkson PM (2003) Oxidative stress, exercise, and antioxidant supplementation. Toxicology 189:41–54PubMedGoogle Scholar
  106. Van der Meulen T, Schipper H, van der Boogaart JGM, Huising MO, Kranenbarg S, van Leeuwen JL (2006) Endurance exercise differentially stimulates heart and axial muscle development in zebrafish (Danio rerio). Am J Physiol Reg I 291:R1040–R1048Google Scholar
  107. Vega RB, Huss JM, Kelly DP (2000) The coactivator PGC-1 cooperates with peroxisome proliferator-activated receptor α in transcriptional control of nuclear genes encoding mitochondrial fatty acid oxidation enzymes. Mol Cell Biol 20:1868–1876PubMedGoogle Scholar
  108. Wagner N, Jehl-Pietri C, Giordano C, Schwartz C, Gounon P, Hatem SN, Grimaldi P, Wagner KD (2009) Peroxisome proliferator-activated receptor beta stimulation induces rapid cardiac growth and angiogenesis via direct activation of calcineurin. Cardiovasc Res 83:61–71PubMedGoogle Scholar
  109. Weber JM, Brill RW, Hochachka PW (1986) Mammalian metabolite flux rates in a teleost- lactate and glucose-turnover in tuna. Am J Physiol 250:452–458Google Scholar
  110. West TG, Arthur PG, Suarez RK, Doll CJ, Hochachka P (1993) In vivo utilization of glucose by heart and locomotory muscles of exercising rainbow trout (Oncorhynchus mykiss). J Exp Biol 177:63–79Google Scholar
  111. Yancopoulos GD, Davis S, Gale NW, Rudge JS, Wiegand SJ, Holash J (2000) Vascular-specific growth factors and blood vessel formation. Nature 407:242–248PubMedGoogle Scholar
  112. Zhang Z, Niu C, Storset A, Bøgwald J, Dalmo RA (2011) Comparisson of Aeromonas salmonicida resistance and susceptible salmon families: a high immune response is beneficial for the survival against Aeromonas salmonicida challenge. Fish Shellfish Immunol 31:1–9PubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Nofima ASÅsNorway
  2. 2.AVS Chile S.APuerto VarasChile

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