Journal of Comparative Physiology B

, Volume 182, Issue 4, pp 507–516 | Cite as

Glucose and lipid metabolism in the pancreas of rainbow trout is regulated at the molecular level by nutritional status and carbohydrate intake

  • Sergio Polakof
  • Sandrine Skiba-Cassy
  • Sadasivam Kaushik
  • Iban Seiliez
  • Jose Luis Soengas
  • Stephane Panserat
Original Paper

Abstract

Glucose and lipid metabolism in pancreatic islet organs is poorly characterized. In the present study, using as a model the carnivorous rainbow trout, a glucose-intolerant fish, we assessed mRNA expression levels of several genes involved in glucose and lipid metabolism (including ATP-citrate lyase; carnitine palmitoyltransferase-1 isoforms, CPT; the mitochondrial isoform of the phosphoenolpyrutave carboxykinase, mPEPCK and pyruvate kinase, PK) and glucosensing (glucose transporter type 2, Glut2; glucokinase, GK and the potassium channel, KATP) in Brockmann bodies. We evaluated the response of these parameters to changes in feeding status (food deprived vs. fed fish) as well as to changes in the amount of carbohydrate (dextrin) in the diet. A general inhibition of the glycolytic (including the glucosensing marker GK) and β-oxidation pathways was found when comparing fed versus food-deprived fish. When comparing fish feeding on either low- or high-carbohydrate diets, we found that some genes related to lipid metabolism were more controlled by the feeding status than by the carbohydrate content (fatty acid synthase, CPTs). Findings are discussed in the context of pancreatic regulation of glucose and lipid metabolism in fish, and show that while trout pancreatic metabolism can partially adapt to a high-carbohydrate diet, some of the molecular actors studied seem to be poorly regulated (KATP) and may contribute to the glucose intolerance observed in this species when fed high-carbohydrate diets.

Keywords

Glucose and lipid metabolism Dietary carbohydrates Brockmann bodies Fish 

Notes

Acknowledgments

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

References

  1. Assimacopoulos-Jeannet F, Thumelin S, Roche E, Esser V, McGarry JD, Prentki M (1997) Fatty acids rapidly induce the carnitine palmitoyltransferase I gene in the pancreatic beta-cell line INS-1. J Biol Chem 272:1659–1664PubMedCrossRefGoogle Scholar
  2. Berne C (1975) The metabolism of lipids in mouse pancreatic islets. The biosynthesis of triacylglycerols and phospholipids. Biochem J 152:667–673PubMedGoogle Scholar
  3. Brun T, Roche E, Kim KH, Prentki M (1993) Glucose regulates acetyl-CoA carboxylase gene expression in a pancreatic beta-cell line (INS-1). J Biol Chem 268:18905–18911PubMedGoogle Scholar
  4. Carneiro MN, Eilertson C, Sheridan MA (1996) Lipid-stimulated somatostatin secretion in rainbow trout, Oncorhynchus mykiss. Fish Physiol Biochem 15:447–452CrossRefGoogle Scholar
  5. Chen S, Ogawa A, Ohneda M, Unger RH, Foster DW, McGarry JD (1994) More direct evidence for a malonyl-CoA-carnitine palmitoyltransferase I interaction as a key event in pancreatic beta-cell signaling. Diabetes 43:878–883PubMedCrossRefGoogle Scholar
  6. Cooperstein SJ, Lazarow A (1969) Uptake of glucose by islet of Langerhans and other tissues of toadfish (Opsanus tau). Am J Physiol 217:1784–1788PubMedGoogle Scholar
  7. Ehrman MM, Melroe GT, Kittilson D, Sheridan MA (2000) The expression of presomatostatin II mRNAs in the Brockmann bodies of rainbow trout, Oncorhynchus mykiss, is regulated by glucose. Gen Comp Endocrinol 118:150–160PubMedCrossRefGoogle Scholar
  8. Ehrman MM, Melroe GT, Moore CA, Kittilson JD, Sheridan MA (2002) Nutritional regulation of somatostatin expression in rainbow trout, Oncorhynchus mykiss. Fish Physiol Biochem 26:309–314CrossRefGoogle Scholar
  9. 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 135:139–151PubMedCrossRefGoogle Scholar
  10. Hamilton JA, Kamp F (1999) How are free fatty acids transported in membranes? Is it by proteins or by free diffusion through the lipids? Diabetes 48:2255–2269PubMedCrossRefGoogle Scholar
  11. Hobart P, Crawford R, Shen L, Pictet R, Rutter WJ (1980) Cloning and sequence analysis of cDNAs encoding two distinct somatostatin precursors found in the endocrine pancreas of anglerfish. Nature 288:137–141PubMedCrossRefGoogle Scholar
  12. Humbel RE, Renold AE, Williams AK (1963) Studies on isolated islets of Langerhans (Brockmann bodies) of teleost fishes I. Metabolic activity in vitro. Biochim Biophys Acta 74:84–95PubMedCrossRefGoogle Scholar
  13. Iynedjian PB, Jotterand D, Nouspikel T, Asfari M, Pilot PR (1989) Transcriptional induction of glucokinase gene by insulin in cultured liver cells and its repression by the glucagon-cAMP system. J Biol Chem 264:21824–21829PubMedGoogle Scholar
  14. Joy P (2002) Cloning, sequencing and expression of the tilapia glucokinase. M.Sc. Thesis, Department of Biology, Dalhousie UniversityGoogle Scholar
  15. Kittilson JD, Moore CA, Sheridan MA (1999) Polygenic expression of somatostatin in rainbow trout, Oncorhynchus mykiss: evidence of a preprosomatostatin encoding somatostatin-14. Gen Comp Endocrinol 114:88–96PubMedCrossRefGoogle Scholar
  16. Liang Y, Jetton TL, Zimmerman EC, Najafi H, Berner DK, Matschinsky FM, Magnuson MA (1994) Effects of glucose on insulin secretion, glucokinase activity, and transgene expression in transgenic mouse islets containing an upstream glucokinase promoter-human growth hormone fusion gene. Diabetes 43:1138–1145PubMedCrossRefGoogle Scholar
  17. Liang Y, Matschinsky FM (1991) Content of CoA-esters in perifused rat islets stimulated by glucose and other fuels. Diabetes 40:327–333PubMedCrossRefGoogle Scholar
  18. MacDonald MJ, Dobrzyn A, Ntambi J, Stoker SW (2008) The role of rapid lipogenesis in insulin secretion: insulin secretagogues acutely alter lipid composition of INS-1 832/13 cells. Arch Biochem Biophys 470:153–162PubMedCrossRefGoogle Scholar
  19. Macleod JJR (1922) The source of insulin. A study of the effect produced on blood sugar by extracts of the pancreas and principal islets of fishes. J Metab Res 2:149–172Google Scholar
  20. Magnuson MA, Matschinsky FM (2004) Glucokinase as a glucose sensor: past, present and future. In: Matschinsky FM, Magnuson MA (eds) Glucokinase and glycemic disease: from basics to novel therapeutics. Krager, Basel, pp 1–17CrossRefGoogle Scholar
  21. Matschinsky FM (1990) Perspectives in diabetes: glucokinase as glucose sensor and metabolic signal generator in pancreatic β-cells and hepatocytes. Diabetes 39:647–652PubMedCrossRefGoogle Scholar
  22. Melroe GT, Ehrman MM, Kittilson JD, Sheridan MA (2000) Glucose regulates pancreatic preprosomatostatin I expression. FEBS Lett 465:115–118PubMedCrossRefGoogle Scholar
  23. Modaressi S, Brechtel K, Christ B, Jungermann K (1998) Human mitochondrial phosphoenolpyruvate carboxykinase 2 gene. Structure, chromosomal localization and tissue-specific expression. Biochem J 333(Pt 2):359–366PubMedGoogle Scholar
  24. Mommsen TP, Busby ER (2006) Glucagon and friends. In: Reinecke M, Zaccone G, Kapoor BG (eds) Fish endocrinology. Science Publishers, Enfield, pp 223–256CrossRefGoogle Scholar
  25. Mommsen TP, Plisetskaya EM (1991) Insulin in fishes and agnathans: history, structure, and metabolic regulation. Rev Aquat Sci 4:225–259Google Scholar
  26. Moore CA, Kittilson JD, Ehrman MM, Sheridan MA (1999) Rainbow trout (Oncorhynchus mykiss) possess two somatostatin mRNAs that are differentially expressed. Am J Physiol Regul Integr Comp Physiol 277:1553–1561Google Scholar
  27. Moore S (1968) Amino acid analysis: aqueous dimethyl sulfoxide as solvent for the ninhydrin reaction. J Biol Chem 243:6281–6283PubMedGoogle Scholar
  28. Moritz W, Leech CA, Ferrer J, Habener JF (2001) Regulated expression of adenosine triphosphate-sensitive potassium channel subunits in pancreatic beta-cells. Endocrinology 142:129–138PubMedCrossRefGoogle Scholar
  29. Newgard CB, McGarry JD (1995) Metabolic coupling factors in pancreatic beta-cell signal transduction. Annu Rev Biochem 64:689–719PubMedCrossRefGoogle Scholar
  30. Newsholme P, Gaudel C, McClenaghan N (2010) Nutrient regulation of insulin secretion and β-cell functional integrity. In: Islam MS (ed) The islets of Langerhans. Springer, DordrechtGoogle Scholar
  31. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucl Acids Res 29:e45PubMedCrossRefGoogle Scholar
  32. Plisetskaya EM, Duguay S, Schrgibman MP, Scanes CE, Pang P (1993) Pancreatic hormones and metabolism in ectotherm vertebrates: current views. In: Schreibman MP, Scanes CG, Pang PKT Jr (eds) The endocrinology of growth. Development and metabolism in vertebrates. Academic Press, New York, pp 266–287Google Scholar
  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 39:26–33PubMedCrossRefGoogle Scholar
  34. Polakof S, Míguez JM, Moon TW, Soengas JL (2007a) Evidence for the presence of a glucosensor in hypothalamus, hindbrain, and Brockmann bodies of rainbow trout. Am J Physiol Regul Integr Comp Physiol 292:R1657–R1666PubMedCrossRefGoogle Scholar
  35. Polakof S, Míguez JM, Soengas JL (2007b) In vitro evidences for glucosensing capacity and mechanisms in hypothalamus, hindbrain, and Brockmann bodies of rainbow trout. Am J Physiol Regul Integr Comp Physiol 293:R1410–R1420PubMedCrossRefGoogle Scholar
  36. Polakof S, Míguez JM, Soengas JL (2008a) Dietary carbohydrates induce changes in glucosensing capacity and food intake of rainbow trout. Am J Physiol Regul Integr Comp Physiol 295:R478–R489PubMedCrossRefGoogle Scholar
  37. Polakof S, Mommsen TP, Soengas JL (2011) Glucosensing and glucose homeostasis: from fish to mammals. Comp Biochem Physiol A Mol Integr Physiol 160:123–149Google Scholar
  38. Polakof S, Panserat S, Plagnes-Juan E, Soengas JL (2008b) Altered dietary carbohydrates significantly affect gene expression of the major glucosensing components in Brockmann bodies and hypothalamus of rainbow trout. Am J Physiol Regul Integr Comp Physiol 295:R1077–R1088PubMedCrossRefGoogle Scholar
  39. Polakof S, Soengas JL (2008) Involvement of lactate in glucose metabolism and glucosensing function in selected tissues of rainbow trout. J Exp Biol 211:1075–1086PubMedCrossRefGoogle Scholar
  40. Prentki M, Vischer S, Glennon MC, Regazzi R, Deeney JT, Corkey BE (1992) Malonyl-CoA and long chain acyl-CoA esters as metabolic coupling factors in nutrient-induced insulin secretion. J Biol Chem 267:5802–5810PubMedGoogle Scholar
  41. Rennie J, Fraser T (1907) The islets of Langerhans in relation to diabetes. Biochem J 2:7–19PubMedGoogle Scholar
  42. Roca B, Fernandez-Valencia R, Arilla E (1988) Effects of fasting and refeeding on somatostatin concentration and binding to cytosol from rabbit gastric mucosa. Gut 29:642–646PubMedCrossRefGoogle Scholar
  43. Roche E, Assimacopoulos-Jeannet F, Witters LA, Perruchoud B, Yaney G, Corkey B, Asfari M, Prentki M (1997) Induction by glucose of genes coding for glycolytic enzymes in a pancreatic β-cell line (INS-1). J Biol Chem 272:3091–3098PubMedCrossRefGoogle Scholar
  44. Roche E, Farfari S, Witters LA, Assimacopoulos-Jeannet F, Thumelin S, Brun T, Corkey BE, Saha AK, Prentki M (1998) Long-term exposure of beta-INS cells to high glucose concentrations increases anaplerosis, lipogenesis, and lipogenic gene expression. Diabetes 47:1086–1094PubMedCrossRefGoogle Scholar
  45. Rubi B, Antinozzi PA, Herrero L, Ishihara H, Asins G, Serra D, Wollheim CB, Maechler P, Hegardt FG (2002) Adenovirus-mediated overexpression of liver carnitine palmitoyltransferase I in INS1E cells: effects on cell metabolism and insulin secretion. Biochem J 364:219–226PubMedGoogle Scholar
  46. Schuit F, De Vos A, Farfari S, Moens K, Pipeleers D, Brun T, Prentki M (1997) Metabolic fate of glucose in purified islet cells. Glucose-regulated anaplerosis in beta cells. J Biol Chem 272:18572–18579PubMedCrossRefGoogle Scholar
  47. Seiliez I, Panserat S, Lansard M, Polakof S, Plagnes-Juan E, Surget A, Dias K, Larquier M, Kaushik S, Skiba-Cassy S (2011) Dietary carbohydrate to protein ratio affects TOR signaling and metabolism-related gene expression in the liver and muscle of rainbow trout after a single meal. Am J Physiol Regul Integr Comp Physiol 300:R733–R743PubMedCrossRefGoogle Scholar
  48. Sheridan MA, Hagemeister AL (2010) Somatostatin and somatostatin receptors in fish growth. Gen Comp Endocrinol 167:360–365PubMedCrossRefGoogle Scholar
  49. Sheridan MA, Kittilson JD (2004) The role of somatostatins in the regulation of metabolism in fish. Comp Biochem Physiol B Biochem Mol Biol 138:323–330PubMedCrossRefGoogle Scholar
  50. Sladky KK, Swanson CR, Stoskopf MK, Loomis MR, Lewbart GA (2001) Comparative efficacy of tricaine methanesulfonate and clove oil for use as anesthetics in red pacu (Piaractus brachypomus). Am J Vet Res 62:337–342PubMedCrossRefGoogle Scholar
  51. Smith AJ, Partridge CJ, Asipu A, Mair LA, Hunter M, Sivaprasadarao A (2006) Increased ATP-sensitive K+ channel expression during acute glucose deprivation. Biochem Biophys Res Commun 348:1123–1131PubMedCrossRefGoogle Scholar
  52. Soengas JL, Polakof S, Chen X, Sangiao-Alvarellos S, Moon TW (2006) Glucokinase and hexokinase expression and activities in rainbow trout tissues: changes with food deprivation and refeeding. Am J Physiol Regul Integr Comp Physiol 291:R810–R821PubMedCrossRefGoogle Scholar
  53. Stark R, Pasquel F, Turcu A, Pongratz RL, Roden M, Cline GW, Shulman GI, Kibbey RG (2009) Phosphoenolpyruvate cycling via mitochondrial phosphoenolpyruvate carboxykinase links anaplerosis and mitochondrial GTP with insulin secretion. J Biol Chem 284:26578–26590PubMedCrossRefGoogle Scholar
  54. Staub A, Sinn L, Behrens OK (1953) Purification and crystallization of hyperglycemic glycogenolytic factor (HGF). Science 117:628–629PubMedCrossRefGoogle Scholar
  55. Tranulis MA, Christophersen B, Borrebaek B (1997) Glucokinase in Atlantic halibut (Hippoglossus hipoglossus) Brockmann bodies. Comp Biochem Physiol B Biochem Mol Biol 116:367–370CrossRefGoogle Scholar
  56. Tranulis MA, Dregni O, Christophersen B, Krogdahl A, Borrebaek B (1996) A glucokinase-like-enzyme in the liver of Atlantic salmon (Salmo salar). Comp Biochem Physiol A Physiol 114:35–39CrossRefGoogle Scholar
  57. Waeber G, Thompson N, Haefliger JA, Nicod P (1994) Characterization of the murine high K m glucose transporter GLUT2 gene and its transcriptional regulation by glucose in a differentiated insulin-secreting cell line. J Biol Chem 269:26912–26919PubMedGoogle Scholar
  58. Wilson RP (1994) Utilization of dietary carbohydrate by fish. Aquaculture 124:67–80CrossRefGoogle Scholar
  59. Youson JH, Al-Mahrouki AA (1999) Ontogenetic and phylogenetic development of the endocrine pancreas (islet organ) in fish. Gen Comp Endocrinol 116:303–335PubMedCrossRefGoogle Scholar
  60. Youson JH, Al-Mahrouki AA, Anemiya Y, Graham LC, Montpetit CJ, Irwin DM (2006) The fish endocrine pancreas: research update and future directions in ontogenic and phylogenetic development. Gen Comp Endocrinol 148:105–115PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Sergio Polakof
    • 1
    • 2
    • 3
    • 4
  • Sandrine Skiba-Cassy
    • 1
  • Sadasivam Kaushik
    • 1
  • Iban Seiliez
    • 1
  • Jose Luis Soengas
    • 2
  • Stephane Panserat
    • 1
  1. 1.INRA, UR1067 Nutrition Metabolisme Aquaculture, Pôle d’hydrobiologie, CD918St-Pée-sur-NivelleFrance
  2. 2.Laboratorio de Fisioloxía Animal, Departamento de Bioloxía Funcional e Ciencias da Saude Facultade de BioloxíaUniversidade de VigoVigoSpain
  3. 3.INRA, UMR 1019, UNH, CRNH AuvergneClermont-FerrandFrance
  4. 4.Clermont Université, Université d’Auvergne, Unité de Nutrition HumaineClermont-FerrandFrance

Personalised recommendations