Lipids

, Volume 46, Issue 2, pp 189–199 | Cite as

Insulin Stimulates Lipogenesis and Attenuates Beta-Oxidation in White Adipose Tissue of Fed Rainbow Trout

  • S. Polakof
  • F. Médale
  • L. Larroquet
  • C. Vachot
  • G. Corraze
  • S. Panserat
Original Article

Abstract

As lipid deposition tissue in fish, the white adipose tissue (WAT) has important functions related to reproduction and the challenges of long-term fasting. In the study reported here, we infused fish fed a high-carbohydrate diet with two doses of insulin for 5 days in order to explore the effects of this hormone on lipogenesis and beta-oxidation-related enzymes. We demonstrated the presence of some of the main lipogenic enzymes at molecular, protein and activity levels (ATP-citrate lyase and fatty acid synthase). However, while ATP-citrate lyase was unexpectedly down-regulated, fatty acid synthase was up-regulated (at protein and activity levels) in an insulin dose-dependent manner. The main enzymes acting as NADPH donors for lipogenesis were also characterized at biochemical and molecular levels, although there was no evidence of their regulation by insulin. On the other hand, lipid oxidation potential was found in this tissue through the measurement of gene expression of enzymes involved in β-oxidation, highlighting two carnitine palmitoyltransferase isoforms, both down-regulated by insulin infusion. We found that insulin acts as an important regulator of trout WAT lipid metabolism, inducing the final stage of lipogenesis at molecular, protein and enzyme activity levels and suppressing β-oxidation at least at a molecular level. These results suggest that WAT in fish may have a role that is important not only as a lipid deposition tissue but also as a lipogenic organ (with possible involvement in glucose homeostasis) that could also be able to utilize the lipids stored as a local energy source.

Keywords

Insulin Fish Dietary carbohydrates White adipose tissue Lipogenesis Lipid oxidation 

Abbreviations

6PGDH

6-Phosphogluconate dehydrogenase

ACLY

ATP citrate lyase

CPT

Carnitine palmitoyltransferase

EF1α

Elongation factor 1 alpha

FFA

Free fatty acids

G6PDH

Glucose 6-phosphate dehydrogenase

HOAD

3-Hydroxyacyl-CoA dehydrogenase

HSL

Hormone-sensitive lipase

ICDH

Isocitrate dehydrogenase

LPL

Lipoprotein lipase

ME

Malic enzyme

NAPDH

Nicotine adenine dinucleotide phosphate, reduced

TAG

Triacylglycerols

TNF

Tumor necrosis factor-alpha

WAT

White adipose tissue

Notes

Acknowledgments

This study was supported by research grants from the Agence Nationale de la Recherche (ANR-08-JCJC-0025-01) and INRA PHASE Department. SP was recipient of a postdoctoral fellowship from the Xunta de Galicia (Program Ángeles Alvariño). We thank the technical stuff (Y. Hontang, F. Sandres, and F. Terrier) of the INRA experimental fish farm of Donzacq for supplying the experimental animals.

References

  1. 1.
    Bezaire V, Langin D (2009) Regulation of adipose tissue lipolysis revisited. Proc Nutr Soc 68:350–360CrossRefPubMedGoogle Scholar
  2. 2.
    Minehira K, Bettschart V, Vidal H, Vega N, Di Vetta V, Rey V, Schneiter P, Tappy L (2003) Effect of carbohydrate overfeeding on whole body and adipose tissue metabolism in humans. Obes Res 11:1096–1103CrossRefPubMedGoogle Scholar
  3. 3.
    Zang Y, Wang T, Xie W, Wang-Fischer YL, Getty L, Han J, Corkey BE, Guo W (2005) Regulation of acetyl CoA carboxylase and carnitine palmitoyl transferase-1 in rat adipocytes. Obes Res 13:1530–1539CrossRefPubMedGoogle Scholar
  4. 4.
    Frayn KN (2002) Adipose tissue as a buffer for daily lipid flux. Diabetologia 45:1201–1210CrossRefPubMedGoogle Scholar
  5. 5.
    Sheridan MA (1988) Lipid dynamics in fish: aspects of absorption, transportation, deposition and mobilization. Comp Biochem Physiol B Biochem Mol Biol 90:679–690CrossRefGoogle Scholar
  6. 6.
    Sheridan MA, Harmon JS (1994) Adipose tissue. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fishes, vol 3. Elsevier, Amsterdam, pp 305–311Google Scholar
  7. 7.
    Navarro I, Gutiérrez J (1995) Fasting and starvation. In: Hochachka PW, Mommsen TP (eds) Metabolic biochemistry, vol 4. Elsevier, Amsterdam, pp 394–434Google Scholar
  8. 8.
    Company R, Calduch-Giner JA, Kaushik S, Pérez-Sánchez J (1999) Growth performance and adiposity in gilthead sea bream (Sparus aurata): risks and benefits of high energy diets. Aquaculture 171:279–292CrossRefGoogle Scholar
  9. 9.
    Sheridan MA (1989) Alterations in lipid metabolism accompanying smoltification and seawater adaptation of salmonid fish. Aquaculture 82:191–203CrossRefGoogle Scholar
  10. 10.
    Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11:107–184CrossRefGoogle Scholar
  11. 11.
    Albalat A, Sánchez-Gurmaches J, Gutiérrez J, Navarro I (2006) Regulation of lipoprotein lipase activity in rainbow trout (Oncorhynchus mykiss) tissues. Gen Comp Endocrinol 146:226–235CrossRefPubMedGoogle Scholar
  12. 12.
    Albalat A, Saera-Vila A, Capilla E, Gutiérrez J, Pérez-Sánchez J, Navarro I (2007) Insulin regulation of lipoprotein lipase (LPL) activity and expression in gilthead sea bream (Sparus aurata). Comp Biochem Physiol B Biochem Mol Biol 148:151–159CrossRefPubMedGoogle Scholar
  13. 13.
    Cruz-Garcia L, Saera-Vila A, Navarro I, Calduch-Giner J, Perez-Sanchez J (2009) Targets for TNFalpha-induced lipolysis in gilthead sea bream (Sparus aurata L.) adipocytes isolated from lean and fat juvenile fish. J Exp Biol 212:2254–2260CrossRefPubMedGoogle Scholar
  14. 14.
    Harmon JS, Rieniets LM, Sheridan MA (1993) Glucagon and insulin regulate lipolysis in trout liver by altering phosphorylation of triacylglycerol lipase. Am J Physiol Regul Integr Comp Physiol 265:R255–R260Google Scholar
  15. 15.
    Aster PL, Moon TW (1981) Influence of fasting and diet on lipogenic enzymes in the American eel, Anguilla rostrata LeSueur. J Nutr 111:346–354PubMedGoogle Scholar
  16. 16.
    Likimani TA, Wilson RP (1982) Effects of diet on lipogenic enzyme activities in channel catfish hepatic and adipose tissue. J Nutr 112:112–117PubMedGoogle Scholar
  17. 17.
    Lin H, Romsos DR, Tack PI, Leveille GA (1977) Influence of dietary lipid on lipogenic enzyme activities in coho salmon, Oncorhynchus kisutch (Walbaum). J Nutr 107:846–854PubMedGoogle Scholar
  18. 18.
    Bouraoui L, Sánchez-Gurmaches J, Cruz-Garcia L, Gutiérrez J, Benedito-Palos L, Pérez-Sánchez J, Navarro I (2010) Effect of dietary fish meal and fish oil replacement on lipogenic and lipoprotein lipase activities and plasma insulin in gilthead sea bream (Sparus aurata) Aquacult Nut 17:54–63. doi:  10.1111/j.1365-2095.2009.00706.x Google Scholar
  19. 19.
    Henderson RJ, Sargent JR (1981) Lipid biosynthesis in rainbow trout, Salmo gairdneri, fed diets of differing lipid content. Comp Biochem Physiol C Comp Pharmacol 69:31–37CrossRefGoogle Scholar
  20. 20.
    Henderson RJ, JR Sargent (1985) Fatty acid metabolism in fish. In: Cowey CB, Mackie AM, Bell JG (eds) Nutrition and feeding in fish. Academic Press, New York, pp 349–364Google Scholar
  21. 21.
    Todorcevic M, Kjaer MA, Djakovic N, Vegusdal A, Torstensen BE, Ruyter B (2009) N-3 HUFAs affect fat deposition, susceptibility to oxidative stress, and apoptosis in Atlantic salmon visceral adipose tissue. Comp Biochem Physiol B Biochem Mol Biol 152:135–143CrossRefPubMedGoogle Scholar
  22. 22.
    Todorcevic M, Vegusdal A, Gjoen T, Sundvold H, Torstensen BE, Kjaer MA, Ruyter B (2008) Changes in fatty acids metabolism during differentiation of Atlantic salmon preadipocytes; effects of n-3 and n-9 fatty acids. Biochim Biophys Acta 1781:326–335PubMedGoogle Scholar
  23. 23.
    Gutieres S, Damon M, Panserat S, Kaushik S, Medale F (2003) Cloning and tissue distribution of a carnitine palmitoyltransferase I gene in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol B Biochem Mol Biol 135:139–151PubMedGoogle Scholar
  24. 24.
    Torstensen B, Nanton D, Olsvik P, Sundvold H, Stubhaug I (2009) Gene expression of fatty acid-binding proteins, fatty acid transport proteins (cd36 and FATP) and β-oxidation-related genes in Atlantic salmon (Salmo salar L.) fed fish oil or vegetable oil. Aquac Nutr 15:440–451CrossRefGoogle Scholar
  25. 25.
    Boukouvala E, Leaver MJ, Favre-Krey L, Theodoridou M, Krey G (2010) Molecular characterization of a gilthead sea bream (Sparus aurata) muscle tissue cDNA for carnitine palmitoyltransferase 1B (CPT1B). Comp Biochem Physiol B Biochem Mol Biol 157:189–197CrossRefPubMedGoogle Scholar
  26. 26.
    Mingarro M, Vega-Rubín de Celis S, Astola A, Pendon C, Valdivia MM, Pérez-Sánchez J (2002) Endocrine mediators of seasonal growth in gilthead sea bream (Sparus aurata): the growth hormone and somatolactin paradigm. Gen Comp Endocrinol 128:102–111CrossRefPubMedGoogle Scholar
  27. 27.
    Harmon JS, Sheridan MA (1992) Effects of nutritional state, insulin, and glucagon on lipid mobilization in rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 87:214–221CrossRefPubMedGoogle Scholar
  28. 28.
    Vianen GJ, Obels PP, van den Thillart GE, Zaagsma J (2002) Beta-adrenoceptors mediate inhibition of lipolysis in adipocytes of tilapia (Oreochromis mossambicus). Am J Physiol Endocrinol Metab 282:E318–E325PubMedGoogle Scholar
  29. 29.
    Albalat A, Liarte C, MacKenzie S, Tort L, Planas JV, Navarro I (2005) Control of adipose tissue lipid metabolism by tumor necrosis factor-α in rainbow trout (Oncorhynchus mykiss). J Endocrinol 184:527–534CrossRefPubMedGoogle Scholar
  30. 30.
    Navarro I, Capilla E, Castillo A, Albalat A, Díaz M, Gallardo M A, Blasco J, Planas JV, Gutiérrez J (2006) Insulin metabolic effects in fish tissues. In: Reinecke M, Zaccone G, Kapoor BG (eds) Fish endocrinology Science Publishers Inc., Enfield, pp 15–48Google Scholar
  31. 31.
    Albalat A, Gutiérrez J, Navarro I (2005) Regulation of lipolysis in isolated adipocytes of rainbow trout (Oncorhynchus mykiss): the role of insulin and glucagon. Comp Biochem Physiol B Biochem Mol Biol 142:347–354Google Scholar
  32. 32.
    Mommsen TP, Plisetskaya EM (1991) Insulin in fishes and agnathans: history, structure, and metabolic regulation. Rev Aquat Sci 4:225–259Google Scholar
  33. 33.
    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
  34. 34.
    Planas JV, Méndez E, Banos N, Capilla E, Navarro I, Gutiérrez J (2000) Insulin and IGF-I receptors in trout adipose tissue are physiologically regulated by circulating hormone levels. J Exp Biol 203:1153–1159PubMedGoogle Scholar
  35. 35.
    Polakof S, Skiba-Cassy S, Choubert G, Panserat S (2010) Insulin-induced hypoglycaemia is co-ordinately regulated by liver and muscle during acute and chronic insulin stimulation in rainbow trout (Oncorhynchus mykiss). J Exp Biol 213:1443–1452CrossRefPubMedGoogle Scholar
  36. 36.
    Dias J, Álvarez MJ, Díez A, Arzel J, Corraze G, Bautista JM, Kaushik S (1998) Regulation of hepatic lipogenesis by dietary protein/energy in juvenile European seabass (Dicentrarchus labrax). Aquaculture 161:169–186CrossRefGoogle Scholar
  37. 37.
    Lin H, Romsos DR, Tack PI, Leveille GA (1977) Effects of fasting and feeding various diets on hepatic lipogenic enzyme activities in coho salmon (Oncorhynchus kisutch (Walbaum)). J Nutr 107:1477–1483PubMedGoogle Scholar
  38. 38.
    Panserat S, Skiba-Cassy S, Seiliez I, Lansard M, Plagnes-Juan E, Vachot C, Aguirre P, Larroquet L, Chavergnac G, Médale F, Corraze G, Kaushik S, Moon TW (2009) Metformin improves postprandial glucose homeostasis in rainbow trout fed dietary carbohydrates: a link with the induction of hepatic lipogenic capacities? Am J Physiol Regul Integr Comp Physiol 293:707–715Google Scholar
  39. 39.
    Polakof S, Skiba-Cassy S, Panserat S (2009) Glucose homeostasis is impaired by a paradoxical interaction between metformin and insulin in carnivorous rainbow trout. Am J Physiol Regul Integr Comp Physiol 297:1769–1776Google Scholar
  40. 40.
    Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45CrossRefPubMedGoogle Scholar
  41. 41.
    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 Regul Integr Comp Physiol 294:R1154–R1164PubMedGoogle Scholar
  42. 42.
    Figueiredo-Silva AC, Corraze G, Borges P, Valente LMP (2010) Dietary protein/lipid level and protein source effects on growth, tissue composition and lipid metabolism of blackspot seabream (Pagellus bogaraveo). Aquac Nutr 16:173–187CrossRefGoogle Scholar
  43. 43.
    Mommsen TP, Osachoff HL, Elliott ME (2003) Metabolic zonation in teleost gastrointestinal tract effects of fasting and cortisol in tilapia. J Comp Physiol B Biochem Syst Environ Physiol 173:409–418CrossRefGoogle Scholar
  44. 44.
    Álvarez MJ, Díez A, López-Bote C, Gallego M, Bautista JM (2000) Short-term modulation of lipogenesis by macronutrients in rainbow trout (Oncorhynchus mykiss) hepatocytes. Br J Nutr 84:619–628PubMedGoogle Scholar
  45. 45.
    Bouraoui L, Capilla E, Gutierrez J, Navarro I (2010) Insulin and insulin-like growth factor I signaling pathways in rainbow trout (Oncorhynchus mykiss) during adipogenesis and their implication in glucose uptake. Am J Physiol Regul Integr Comp Physiol 299:33–41Google Scholar
  46. 46.
    Berggreen C, Gormand A, Omar B, Degerman E, Goransson O (2009) Protein kinase B activity is required for the effects of insulin on lipid metabolism in adipocytes. Am J Physiol Endocrinol Metab 296:E635–E646CrossRefPubMedGoogle Scholar
  47. 47.
    Strable MS, Ntambi JM (2010) Genetic control of de novo lipogenesis: role in diet-induced obesity. Crit Rev Biochem Mol Biol 45:199–214CrossRefPubMedGoogle Scholar
  48. 48.
    Towle HC, Kaytor EN, Shih HM (1997) Regulation of the expression of lipogenic enzyme genes by carbohydrate. Annu Rev Nutr 17:405–433CrossRefPubMedGoogle Scholar
  49. 49.
    Saggerson ED, McAllister TW, Baht HS (1988) Lipogenesis in rat brown adipocytes effects of insulin and noradrenaline, contributions from glucose and lactate as precursors and comparisons with white adipocytes. Biochem J 251:701–709PubMedGoogle Scholar
  50. 50.
    Fukuda H, Iritani N (1999) Regulation of ATP citrate-lyase gene expression in hepatocytes and adipocytes in normal and genetically obese rats. J Biochem 126:437–444PubMedGoogle Scholar
  51. 51.
    Skiba-Cassy S, Lansard M, Panserat S, Medale F (2009) Rainbow trout genetically selected for greater muscle fat content display increased activation of liver TOR signaling and lipogenic gene expression. Am J Physiol Regul Integr Comp Physiol 297:1421–1429Google Scholar
  52. 52.
    Potapova IA, El-Maghrabi MR, Doronin SV, Benjamin WB (2000) Phosphorylation of recombinant human ATP:citrate lyase by cAMP-dependent protein kinase abolishes homotropic allosteric regulation of the enzyme by citrate and increases the enzyme activity. Allosteric activation of ATP: citrate lyase by phosphorylated sugars. Biochemistry 39:1169–1179CrossRefPubMedGoogle Scholar
  53. 53.
    Cusin I, Terrettaz J, Rohner-Jeanrenaud F, Jeanrenaud B (1990) Metabolic consequences of hyperinsulinaemia imposed on normal rats on glucose handling by white adipose tissue, muscles and liver. J.Biochem 267:99–103Google Scholar
  54. 54.
    Larue-Achagiotis C, Goubern M, Laury MC (1988) Concomitant food intake and adipose tissue responses under chronic insulin infusion in rats. Physiol Behav 44:95–100CrossRefPubMedGoogle Scholar
  55. 55.
    Moon TW (2001) Glucose intolerance in teleost fish: fact or fiction? Comp Biochem Physiol B Biochem Mol Biol 129:243–249CrossRefPubMedGoogle Scholar
  56. 56.
    Louet JF, Le May C, Pegorier JP, Decaux JF, Girard J (2001) Regulation of liver carnitine palmitoyltransferase I gene expression by hormones and fatty acids. Biochem Soc Trans 29:310–316CrossRefPubMedGoogle Scholar
  57. 57.
    Morash AJ, Bureau DP, McClelland GB (2009) Effects of dietary fatty acid composition on the regulation of carnitine palmitoyltransferase (CPT) I in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol B Biochem Mol Biol 152:85–93CrossRefPubMedGoogle Scholar
  58. 58.
    Esser V, Brown NF, Cowan AT, Foster DW, McGarry JD (1996) Expression of a cDNA isolated from rat brown adipose tissue and heart identifies the product as the muscle isoform of carnitine palmitoyltransferase I (M-CPT I): M-CPT I is the predominant CPT I isoform expressed in both white (epididymal) and brown adipocytes. J Biol Chem 271:6972–6977CrossRefPubMedGoogle Scholar
  59. 59.
    Plisetskaya EM, Sheridan MA, Mommsen TP (1989) Metabolic changes in Coho and Chinook salmon resulting from acute insufficiency in pancreatic hormones. J Exp Zool 249:158–164CrossRefPubMedGoogle Scholar

Copyright information

© AOCS 2011

Authors and Affiliations

  • S. Polakof
    • 1
    • 2
  • F. Médale
    • 1
  • L. Larroquet
    • 1
  • C. Vachot
    • 1
  • G. Corraze
    • 1
  • S. Panserat
    • 1
  1. 1.INRA, UMR1067 Nutrition Aquaculture et Génomique, Pôle d’hydrobiologie, CD918Saint-Pée-sur-NivelleFrance
  2. 2.Laboratorio de Fisioloxía Animal, Departamento de Bioloxía Funcional e Ciencias da SaúdeFacultade de Bioloxía, Universidade de VigoVigoSpain

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