Marine Biotechnology

, Volume 17, Issue 6, pp 753–767 | Cite as

Food Shortage Causes Differential Effects on Body Composition and Tissue-Specific Gene Expression in Salmon Modified for Increased Growth Hormone Production

  • Jason Abernathy
  • Stéphane Panserat
  • Thomas Welker
  • Elisabeth Plagne-Juan
  • Dionne Sakhrani
  • David A. Higgs
  • Florence Audouin
  • Robert H. Devlin
  • Ken Overturf
Original Article

Abstract

Growth hormone (GH) transgenic salmon possesses markedly increased metabolic rate, appetite, and feed conversion efficiency, as well as an increased ability to compete for food resources. Thus, the ability of GH-transgenic fish to withstand periods of food deprivation as occurs in nature is potentially different than that of nontransgenic fish. However, the physiological and genetic effects of transgenic GH production over long periods of food deprivation remain largely unknown. Here, GH-transgenic coho salmon (Oncorhynchus kisutch) and nontransgenic, wild-type coho salmon were subjected to a 3-month food deprivation trial, during which time performance characteristics related to growth were measured along with proximate compositions. To examine potential genetic effects of GH-transgenesis on long-term food deprivation, a group of genes related to muscle development and liver metabolism was selected for quantitative PCR analysis. Results showed that GH-transgenic fish lose weight at an increased rate compared to wild-type even though proximate compositions remained relatively similar between the groups. A total of nine genes related to muscle physiology (cathepsin, cee, insulin-like growth factor, myostatin, murf-1, myosin, myogenin, proteasome delta, tumor necrosis factor) and five genes related to liver metabolism (carnitine palmitoyltransferase, fatty acid synthase, glucose-6-phosphatase, glucose-6-phosphate dehydrogenase, glucokinase) were shown to be differentially regulated between GH-transgenic and wild-type coho salmon over time. These genetic and physiological responses assist in identifying differences between GH-transgenic and wild-type salmon in relation to fitness effects arising from elevated growth hormone during periods of long-term food shortage.

Keywords

Oncorhynchus kisutch Coho salmon Transgenic Liver Metabolism Muscle Proximate analysis Gene expression Network analysis 

References

  1. Albalat A, Liarte C, MacKenzie S, Tort L, Planas JV, Navarro I (2005) Control of adipose tissue lipid metabolism by tumor necrosis factor-alpha in rainbow trout (Oncorhynchus mykiss). J Endocrinol 184:527–534CrossRefPubMedGoogle Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefPubMedGoogle Scholar
  3. Berge GM, Ruyter B, Åsgård T (2004) Conjugated linoleic acid in diets for juvenile Atlantic salmon (Salmo salar); effects on fish performance, proximate composition, fatty acid and mineral content. Aquaculture 237:365–380CrossRefGoogle Scholar
  4. Biga PR, Meyer J (2009) Growth hormone differentially regulates growth and growth-related gene expression in closely related fish species. Comp Biochem Physiol A Mol Integr Physiol 154:465–473CrossRefPubMedGoogle Scholar
  5. Biga PR et al (2004) Growth hormone differentially regulates muscle myostatin1 and −2 and increases circulating cortisol in rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 138:32–41CrossRefPubMedGoogle Scholar
  6. Blasco J, Fernàndez-Borràs J, Marimon I, Requena A (1996) Plasma glucose kinetics and tissue uptake in brown trout in vivo: effect of an intravascular glucose load. J Comp Physiol B 165:534–541CrossRefGoogle Scholar
  7. Bodin N et al (2008) Threonine requirements for rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar) at the fry stage are similar. Aquaculture 274:353–365CrossRefGoogle Scholar
  8. Broussard SR et al (2003) Cytokine-hormone interactions: tumor necrosis factor alpha impairs biologic activity and downstream activation signals of the insulin-like growth factor I receptor in myoblasts. Endocrinology 144:2988–2996CrossRefPubMedGoogle Scholar
  9. Brudeseth BE et al (2013) Status and future perspectives of vaccines for industrialised fin-fish farming. Fish Shellfish Immunol 35:1759–1768CrossRefPubMedGoogle Scholar
  10. Cleveland BM, Weber GM, Blemings KP, Silverstein JT (2009) Insulin-like growth factor-I and genetic effects on indexes of protein degradation in response to feed deprivation in rainbow trout (Oncorhynchus mykiss). Am J Physiol Regul Integr Comp Physiol 297:R1332–R1342CrossRefPubMedGoogle Scholar
  11. Cook JT, McNiven MA, Richardson GF, Sutterlin AM (2000a) Growth rate, body composition and feed digestibility/conversion of growth-enhanced transgenic Atlantic salmon (Salmo salar). Aquaculture 188:15–32CrossRefGoogle Scholar
  12. Cook JT, Sutterlin AM, McNiven MA (2000b) Effect of food deprivation on oxygen consumption and body composition of growth-enhanced transgenic Atlantic salmon (Salmo salar). Aquaculture 188:47–63CrossRefGoogle Scholar
  13. de Alvaro C, Teruel T, Hernandez R, Lorenzo M (2004) Tumor necrosis factor alpha produces insulin resistance in skeletal muscle by activation of inhibitor kappaB kinase in a p38 MAPK-dependent manner. J Biol Chem 279:17070–17078CrossRefPubMedGoogle Scholar
  14. De Larichaudy J et al (2012) TNF-alpha- and tumor-induced skeletal muscle atrophy involves sphingolipid metabolism. Skelet Muscle 2:2PubMedCentralCrossRefPubMedGoogle Scholar
  15. del Aguila LF, Claffey KP, Kirwan JP (1999) TNF-alpha impairs insulin signaling and insulin stimulation of glucose uptake in C2C12 muscle cells. Am J Physiol 276:E849–E855PubMedGoogle Scholar
  16. Deng L, Zhang WM, Lin HR, Cheng CH (2004) Effects of food deprivation on expression of growth hormone receptor and proximate composition in liver of black seabream Acanthopagrus schlegeli. Comp Biochem Physiol B Biochem Mol Biol 137:421–432CrossRefPubMedGoogle Scholar
  17. Devlin RH, Yesaki TY, Biagi CA, Donaldson EM, Swanson P, Chan W-K (1994) Extraordinary salmon growth. Nature 371:209–210CrossRefGoogle Scholar
  18. Devlin RH, Yesaki TY, Donaldson EM, Du SJ, Hew C-L (1995) Production of germline transgenic Pacific salmonids with dramatically increased growth performance. Can J Fish Aquat Sci 52:1376–1384CrossRefGoogle Scholar
  19. Devlin RH, Biagi CA, Yesaki TY, Smailus DE, Byatt JC (2001) Growth of domesticated transgenic fish. Nature 409:781–782CrossRefPubMedGoogle Scholar
  20. Devlin RH, Biagi CA, Yesaki TY (2004a) Growth, viability and genetic characteristics of GH transgenic coho salmon strains. Aquaculture 236:607–632CrossRefGoogle Scholar
  21. Devlin RH, D'Andrade M, Uh M, Biagi CA (2004b) Population effects of growth hormone transgenic coho salmon depend on food availability and genotype by environment interactions. Proc Natl Acad Sci U S A 101:9303–9308PubMedCentralCrossRefPubMedGoogle Scholar
  22. Devlin RH, Sundstrom LF, Muir WM (2006) Interface of biotechnology and ecology for environmental risk assessments of transgenic fish. Trends Biotechnol 24:89–97CrossRefPubMedGoogle Scholar
  23. Du SJ, Gong ZY, Fletcher GL, Shears MA, King MJ, Idler DR, Hew CL (1992) Growth enhancement in transgenic Atlantic salmon by the use of an "all fish" chimeric growth hormone gene construct. Biotechnology (N Y) 10:176–181CrossRefGoogle Scholar
  24. FAO (2015) Fisheries and Aquaculture Department. http://www.fao.org/fishery/aquaculture/en. Accessed 20 Jan 2015
  25. Grisdale-Helland B, Gatlin DM, Corrent E, Helland SJ (2011) The minimum dietary lysine requirement, maintenance requirement and efficiency of lysine utilization for growth of Atlantic salmon smolts. Aquac Res 42:1509–1529CrossRefGoogle Scholar
  26. Guttridge DC, Mayo MW, Madrid LV, Wang CY, Baldwin AS Jr (2000) NF-kappaB-induced loss of MyoD messenger RNA: possible role in muscle decay and cachexia. Science 289:2363–2366CrossRefPubMedGoogle Scholar
  27. Haeffner A et al (1997) Inhibitory effect of growth hormone on TNF-alpha secretion and nuclear factor-kappaB translocation in lipopolysaccharide-stimulated human monocytes. J Immunol 158:1310–1314PubMedGoogle Scholar
  28. Handeland SO, Imsland AK, Stefansson SO (2008) The effect of temperature and fish size on growth, feed intake, food conversion efficiency and stomach evacuation rate of Atlantic salmon post-smolts. Aquaculture 283:36–42CrossRefGoogle Scholar
  29. Hershberger WK, Myers JM, Iwamoto RN, McAuley WC, Saxton AM (1990) Genetic changes in the growth of coho salmon (Oncorhynchus kisutch) in marine net-pens, produced by ten years of selection. Aquaculture 85:187–197CrossRefGoogle Scholar
  30. Higgs DA, Balfry SK, Oakes JD, Rowshandeli M, Skura BJ, Deacon G (2006) Efficacy of an equal blend of canola oil and poultry fat as an alternate dietary lipid source for Atlantic salmon (Salmo salar L.) in sea water. I: effects on growth performance, and whole body and fillet proximate and lipid composition. Aquac Res 37:180–191CrossRefGoogle Scholar
  31. Higgs DA et al (2009) Influence of dietary concentrations of protein, lipid and carbohydrate on growth, protein and energy utilization, body composition, and plasma titres of growth hormone and insulin-like growth factor-1 in non-transgenic and growth hormone transgenic coho salmon, Oncorhynchus kisutch (Walbaum). Aquaculture 286:127–137CrossRefGoogle Scholar
  32. Hornick JL, Van Eenaeme C, Gerard O, Dufrasne I, Istasse L (2000) Mechanisms of reduced and compensatory growth. Domest Anim Endocrinol 19:121–132CrossRefPubMedGoogle Scholar
  33. Huang da W, Sherman BT, Lempicki RA (2009a) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37:1–13PubMedCentralCrossRefPubMedGoogle Scholar
  34. Huang da W, Sherman BT, Lempicki RA (2009b) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44–57CrossRefPubMedGoogle Scholar
  35. Johansen KA, Overturf K (2006) Alterations in expression of genes associated with muscle metabolism and growth during nutritional restriction and refeeding in rainbow trout. Comp Biochem Physiol B Biochem Mol Biol 144:119–127CrossRefPubMedGoogle Scholar
  36. Johnsson JI, Bohlin T (2006) The cost of catching up: increased winter mortality following structural growth compensation in the wild. Proc Biol Sci 273:1281–1286PubMedCentralCrossRefPubMedGoogle Scholar
  37. Johnston IA (2006) Environment and plasticity of myogenesis in teleost fish. J Exp Biol 209:2249–2264CrossRefPubMedGoogle Scholar
  38. Johnston IA, Bower NI, Macqueen DJ (2011) Growth and the regulation of myotomal muscle mass in teleost fish. J Exp Biol 214:1617–1628CrossRefPubMedGoogle Scholar
  39. Jones KK, Cornwell TJ, Bottom DL, Campbell LA, Stein S (2014) The contribution of estuary-resident life histories to the return of adult Oncorhynchus kisutch. J Fish Biol 85:52–80CrossRefPubMedGoogle Scholar
  40. Knight JD, Kothary R (2011) The myogenic kinome: protein kinases critical to mammalian skeletal myogenesis. Skelet Muscle 1:29PubMedCentralCrossRefPubMedGoogle Scholar
  41. Kodama M, Hard J, Naish K (2012) Temporal variation in selection on body length and date of return in a wild population of coho salmon, Oncorhynchus kisutch. BMC Evol Biol 12:116PubMedCentralCrossRefPubMedGoogle Scholar
  42. Lansard M et al (2009) Hepatic protein kinase B (Akt)-target of rapamycin (TOR)-signalling pathways and intermediary metabolism in rainbow trout (Oncorhynchus mykiss) are not significantly affected by feeding plant-based diets. Br J Nutr 102:1564–1573CrossRefPubMedGoogle Scholar
  43. Larsson T, Morkore T, Kolstad K, Ostbye TK, Afanasyev S, Krasnov A (2012) Gene expression profiling of soft and firm Atlantic salmon fillet. PLoS One 7:e39219PubMedCentralCrossRefPubMedGoogle Scholar
  44. Lecker SH, Goldberg AL, Mitch WE (2006) Protein degradation by the ubiquitin-proteasome pathway in normal and disease states. J Am Soc Nephrol 17:1807–1819CrossRefPubMedGoogle Scholar
  45. Leggatt RA, Raven PA, Mommsen TP, Sakhrani D, Higgs D, Devlin RH (2009) Growth hormone transgenesis influences carbohydrate, lipid and protein metabolism capacity for energy production in coho salmon (Oncorhynchus kisutch). Comp Biochem Physiol B Biochem Mol Biol 154:121–133CrossRefPubMedGoogle Scholar
  46. Merico D, Isserlin R, Stueker O, Emili A, Bader GD (2010) Enrichment map: a network-based method for gene-set enrichment visualization and interpretation. PLoS One 5:e13984PubMedCentralCrossRefPubMedGoogle Scholar
  47. Overturf K, Sakhrani D, Devlin RH (2010) Expression profile for metabolic and growth-related genes in domesticated and transgenic coho salmon (Oncorhynchus kisutch) modified for increased growth hormone production. Aquaculture 307:111–122CrossRefGoogle Scholar
  48. Panserat S, Kamalam BS, Fournier J, Plagnes-Juan E, Woodward K, Devlin RH (2014) Glucose metabolic gene expression in growth hormone transgenic coho salmon. Comp Biochem Physiol A Mol Integr Physiol 170:38–45CrossRefPubMedGoogle Scholar
  49. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45PubMedCentralCrossRefPubMedGoogle Scholar
  50. Polakof S, Medale F, Skiba-Cassy S, Corraze G, Panserat S (2010) Molecular regulation of lipid metabolism in liver and muscle of rainbow trout subjected to acute and chronic insulin treatments. Domest Anim Endocrinol 39:26–33CrossRefPubMedGoogle Scholar
  51. Polakof S, Panserat S, Soengas J, Moon T (2012) Glucose metabolism in fish: a review. J Comp Physiol B 182:1015–1045CrossRefPubMedGoogle Scholar
  52. Raso S, Anderson TA (2003) Effects of dietary fish oil replacement on growth and carcass proximate composition of juvenile barramundi (Lates calcarifer). Aquac Res 34:813–819CrossRefGoogle Scholar
  53. Raven PA, Devlin RH, Higgs DA (2006) Influence of dietary digestible energy content on growth, protein and energy utilization and body composition of growth hormone transgenic and non-transgenic coho salmon (Oncorhynchus kisutch). Aquaculture 254:730–747CrossRefGoogle Scholar
  54. Raven PA et al (2008) Endocrine effects of growth hormone overexpression in transgenic coho salmon. Gen Comp Endocrinol 159:26–37CrossRefPubMedGoogle Scholar
  55. Rise ML et al (2006) Multiple microarray platforms utilized for hepatic gene expression profiling of GH transgenic coho salmon with and without ration restriction. J Mol Endocrinol 37:259–282CrossRefPubMedGoogle Scholar
  56. Roberts SB, McCauley LA, Devlin RH, Goetz FW (2004) Transgenic salmon overexpressing growth hormone exhibit decreased myostatin transcript and protein expression. J Exp Biol 207:3741–3748CrossRefPubMedGoogle Scholar
  57. Rønsholdt B, McLean E (2004) Effect of growth hormone and salbutamol on growth performance, fillet proximate composition and pigmentation of rainbow trout (Oncorhynchus mykiss). Aquaculture 229:225–238CrossRefGoogle Scholar
  58. 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 138:487–491PubMedGoogle Scholar
  59. Shannon P et al (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504PubMedCentralCrossRefPubMedGoogle Scholar
  60. Starks HA, Clemento AJ, Garza JC (2015) Discovery and characterization of single nucleotide polymorphisms in coho salmon, Oncorhynchus kisutch. Mol Ecol Resour. doi:10.1111/1755-0998 PubMedGoogle Scholar
  61. Sundström LF, Devlin R (2011) Increased intrinsic growth rate is advantageous even under ecologically stressful conditions in coho salmon (Oncorhynchus kisutch). Evol Ecol 25:447–460CrossRefGoogle Scholar
  62. Takagi K, Saito Y, Sawada J (2001) Proteasome inhibitor enhances growth hormone-binding protein release. Mol Cell Endocrinol 182:157–163CrossRefPubMedGoogle Scholar
  63. Tibbetts SM, Wall CL, Barbosa-Solomieu V, Bryenton MD, Plouffe DA, Buchanan JT, Lall SP (2013) Effects of combined ‘all-fish’ growth hormone transgenics and triploidy on growth and nutrient utilization of Atlantic salmon (Salmo salar L.) fed a practical grower diet of known composition. Aquaculture 406–407:141–152CrossRefGoogle Scholar
  64. Tymchuk WE, Devlin RH (2005) Growth differences among first and second generation hybrids of domesticated and wild rainbow trout (Oncorhynchus mykiss). Aquaculture 245:295–300CrossRefGoogle Scholar
  65. van Kerkhof P, Govers R, Alves dos Santos CM, Strous GJ (2000) Endocytosis and degradation of the growth hormone receptor are proteasome-dependent. J Biol Chem 275:1575–1580CrossRefPubMedGoogle Scholar
  66. Vraskou Y, Roher N, Diaz M, Antonescu CN, MacKenzie SA, Planas JV (2011) Direct involvement of tumor necrosis factor alpha in the regulation of glucose uptake in rainbow trout muscle cells. Am J Physiol Regul Integr Comp Physiol 300:R716–R723CrossRefPubMedGoogle Scholar
  67. Warde-Farley D et al (2010) The GeneMANIA prediction server: biological network integration for gene prioritization and predicting gene function. Nucleic Acids Res 38:W214–W220PubMedCentralCrossRefPubMedGoogle Scholar
  68. Won ET, Borski RJ (2013) Endocrine regulation of compensatory growth in fish. Front Endocrinol (Lausanne) 4:74Google Scholar

Copyright information

© Springer Science+Business Media New York (outside the USA) 2015

Authors and Affiliations

  • Jason Abernathy
    • 1
  • Stéphane Panserat
    • 2
  • Thomas Welker
    • 1
  • Elisabeth Plagne-Juan
    • 2
  • Dionne Sakhrani
    • 3
  • David A. Higgs
    • 3
  • Florence Audouin
    • 3
  • Robert H. Devlin
    • 3
  • Ken Overturf
    • 1
  1. 1.USDA-ARS, Hagerman Fish Culture Experiment StationHagermanUSA
  2. 2.INRA, UR1067 Nutrition Metabolism AquacultureSaint-Pée-sur-NivelleFrance
  3. 3.Fisheries and Oceans CanadaWest VancouverCanada

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