Regulation of de novo hepatic lipogenesis by insulin infusion in rainbow trout fed a high-carbohydrate diet

Journal of Animal Science

Volumn 89, Issue 10, 2011, Pages 3079-3088

  Polakof, S ^a,b   Medale F ^a   Larroquet, L ^a   Vachot, C ^a   Corraze, G ^a   Panserat, S ^a  

^a UR1067 Nutrition Metabolism Aquaculture   (France)

^b UNIVERSITY OF VIGO   (Spain)

Author keywords

Dietary carbohydrate; Fish; Insulin; Lipogenesis; Liver

Indexed keywords

INSULIN;

ANIMAL; ANIMAL DISEASE; ANIMAL FOOD; ARTICLE; CARBOHYDRATE DIET; DIET; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; LIPOGENESIS; LIVER; METABOLISM; PHYSIOLOGY; RAINBOW TROUT;

ANIMAL FEED; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; DIET; DIETARY CARBOHYDRATES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; INSULIN; LIPOGENESIS; LIVER; ONCORHYNCHUS MYKISS;

BOVINAE; ONCORHYNCHUS MYKISS; SALMONIDAE;

EID: 80052982254     PISSN: 00218812     EISSN: 15253163     Source Type: Journal    
DOI: 10.2527/jas.2010-3733     Document Type: Article

References (51)

1. Álvarez, M. J., A. Díez, C. López-Bote, M. Gallego, and J. M. Bautista. 2000. Short-term modulation of lipogenesis by macronutrients in rainbow trout (Oncorhynchus mykiss) hepatocytes. Br. J. Nutr. 84:619-628.
2. Aster, P. L., and T. W. Moon. 1981. Influence of fasting and diet on lipogenic enzymes in the american eel, Anguilla rostrata LeSueur. J. Nutr. 111:346-354.
3. Baldwin, J., and K. C. Reed. 1976. Cytoplasmic sources of NADPH for fat synthesis in rainbow trout liver: Effect of thermal acclimation on enzyme activities. Comp. Biochem. Physiol. B 54:527-529.
4. Bradford, M. M. 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.
5. Cowley, D. J., and M. A. Sheridan. 1993. Insulin stimulates hepatic lipogenesis in rainbow trout, Oncorhynchus mykiss. Fish Physiol. Biochem. 11:421-428.
6. Ducasse-Cabanot, S., J. Zambonino-Infante, N. Richard, F. Médale, G. Corraze, M. Mambrini, J. Robin, C. Cahu, S. Kaushik, and S. Panserat. 2007. Reduced lipid intake leads to changes in digestive enzymes in the intestine but has minor effect on key enzymes of hepatic intermediary metabolism in rainbow trout (Oncorhynchus mykiss). Animal 1:1272-1282.
7. Figueiredo-Silva, A. C., G. Corraze, P. Borges, and L. M. P. Valente. 2010. Dietary protein/lipid level and protein source effects on growth, tissue composition and lipid metabolism of blackspot seabream (Pagellus bogaraveo). Aquacult. Nutr. 16:173-187.
8. Fukuda, H., and N. Iritani. 1999. Regulation of ATP citrate-lyase gene expression in hepatocytes and adipocytes in normal and genetically obese rats. J. Biochem. 126:437-444.
9. Griffin, M. J., and H. S. Sul. 2004. Insulin regulation of fatty acid synthase gene transcription: Roles of USF and SREBP-1c. IUBMB Life 56:595-600.
10. Gutières, S., M. Damon, S. Panserat, S. Kaushik, and F. Medale. 2003. Cloning and tissue distribution of a carnitine palmitoyltransferase I gene in rainbow trout (Oncorhynchus mykiss). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 135:139-151.
11. Gutiérrez, J., I. Navarro, J. V. Planas, N. Montserrat, P. Rojas, J. Castillo, O. V. Chystiakova, J. C. Gabillard, A. Smith, S. J. Chan, and B. N. Leibush. 2006. Insulin and IGF receptors in fish. Pages 131-165 in Fish Endocrinology. M. Reinecke, G. Zaccone, and B. G. Kapoor, ed. Science Publishers, Enfield, NH.
12. Harmon, J. S., C. D. Eilertson, M. A. Sheridan, and E. M. Plisetskaya. 1991. Insulin suppression is associated with hypersomatostatinemia and hyperglucagonemia in glucose-injected rainbow trout. Am. J. Physiol. 261:R609-R613.
13. Harmon, J. S., and M. A. Sheridan. 1992. Glucose stimulated lipolysis in rainbow trout, Oncorhynchus mykiss, liver. Fish Physiol. Biochem. 10:189-199.
14. Henderson, R. J., and J. R. Sargent. 1985. Fatty acid metabolism in fish. Pages 349-364 in Nutrition and Feeding in Fish. C. B. Cowey, ed. Academic Press, New York, NY.
15. Higgs, D. A., J. N. Sutton, H. Kim, J. D. Oakes, J. Smith, C. Biagi, M. Rowshandeli, and R. H. Devlin. 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 286:127-137.
16. Hung, S. S. O., and T. Storebakken. 1994. Carbohydrate utilization by rainbow trout is affected by feeding strategy. J. Nutr. 124:223-230.
17. Ide, T., H. Kobayashi, L. Ashakumary, I. A. Rouyer, Y. Takahashi, T. Aoyama, T. Hashimoto, and M. Mizugaki. 2000. Comparative effects of perilla and fish oils on the activity and gene expression of fatty acid oxidation enzymes in rat liver. Biochim. Biophys. Acta 1485:23-35.
18. Kersten, S. 2001. Mechanisms of nutritional and hormonal regulation of lipogenesis. EMBO Rep. 2:282-286.
19. Kolditz, C., M. Borthaire, N. Richard, G. Corraze, S. Panserat, C. Vachot, F. Lefevre, and F. Medale. 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-R1164.
20. Lansard, M., S. Panserat, E. Plagnes-Juan, I. Seiliez, and S. Skiba-Cassy. 2010. Integration of insulin and amino acid signals that regulate hepatic metabolism-related gene expression in rainbow trout: Role of TOR. Amino Acids 39:801-810.
21. Lin, H., D. R. Romsos, P. I. Tack, and G. A. Leveille. 1977a. Effects of fasting and feeding various diets on hepatic lipogenic enzyme activities in coho salmon (Oncorhynchus kisutch (Walbaum)). J. Nutr. 107:1477-1483.
22. Lin, H., D. R. Romsos, P. I. Tack, and G. A. Leveille. 1977b. Influence of dietary lipid on lipogenic enzyme activities in coho salmon, Oncorhynchus kisutch (Walbaum). J. Nutr. 107:846-854.
23. Machado, C. R., M. R. Garofalo, J. E. S. Roselino, I. C. Kettelhut, and R. H. Migliorini. 1988. Effects of starvation, refeeding, and insulin on energy-linked metabolic processes in catfish Rhamdia hilarii) adapted to a carbohydrate-rich diet. Gen. Comp. Endocrinol. 71:429-437.
24. Mommsen, T. P., H. L. Osachoff, and M. E. Elliott. 2003. Metabolic zonation in teleost gastrointestinal tract. Effects of fasting and cortisol in tilapia. J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 173:409-418.
25. Nakai, N., G. R. Collier, Y. Sato, Y. Oshida, N. Fujitsuka, and Y. Shimomura. 1997. Activities of liver pyruvate dehydrogenase complex and 3-hydroxyacyl-CoA dehydrogenase in sand rat (Psammomys obesus). Life Sci. 60:51-55.
26. Navarro, I., E. Capilla, A. Castillo, A. Albalat, M. Díaz, M. A. Gallardo, J. Blasco, J. V. Planas, and J. Gutiérrez. 2006. Insulin metabolic effects in fish tissues. Pages 15-48 in Fish Endocrinology. M. Reinecke, G. Zaccone, and B. G. Kapoor, ed. Science Publishers Inc., Enfield, NH.
27. Nepokroeff, C. M., M. R. Lakshmanan, G. C. Ness, R. A. Muesing, D. A. Kleinsek, and J. W. Porter. 1974. Coordinate control of rat liver lipogenic enzymes by insulin. Arch. Biochem. Biophys. 162:340-344.
28. Novello, F., J. A. Gumaa, and P. Mclean. 1969. The pentose phosphate pathway of glucose metabolism. Hormonal and dietary control of the oxidative and non-oxidative reactions of the cycle in liver. Biochem. J. 111:713-725.
29. Panserat, S., S. Skiba-Cassy, I. Seiliez, M. Lansard, E. Plagnes-Juan, C. Vachot, P. Aguirre, L. Larroquet, G. Chavergnac, F. Médale, G. Corraze, S. Kaushik, and T. W. Moon. 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. 297:R707-R715.
30. Pérez-Sánchez, J. 1988. Metabolismo intermediario en juveniles de lubina: Hormonas pancreáticas, control de la glucemia y efecto ''sparing''. PhD Diss. Instituto de Acuicultura de Torre la Sal (CSIC), Barcelona.
31. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.
32. Plagnes-Juan, E., M. Lansard, I. Seiliez, F. Medale, G. Corraze, S. Kaushik, S. Panserat, and S. Skiba-Cassy. 2008. Insulin regulates the expression of several metabolism-related genes in the liver and primary hepatocytes of rainbow trout (Oncorhynchus mykiss). J. Exp. Biol. 211:2510-2518.
33. Plisetskaya, E. M., S. Duguay, M. P. Schrgibman, C. E. Scanes, and P. Pang. 1993. Pancreatic hormones and metabolism in ectotherm vertebrates: Current views. Pages 266-287 in The Endocrinology of Growth, Development and Metabolism in Vertebrates. M. P. Schreibman, C. G. Scanes, and P. K. T. Pang Jr., ed. Academic Press, New York, NY.
34. Polakof, S., F. Medale, L. Larroquet, C. Vachot, G. Corraze, and S. Panserat. 2011a. Insulin stimulates lipogenesis and attenuates β-oxidation in white adipose tissue of fed rainbow trout. Lipids 46:189-199.
35. Polakof, S., F. Medale, S. Skiba-Cassy, G. Corraze, and S. Panserat. 2010a. Molecular regulation of lipid metabolism in liver and muscle of rainbow trout subjected to acute and chronic insulin treatments. Domest. Anim. Endocrinol. 39:26-33.
36. Polakof, S., T. W. Moon, P. Aguirre, S. Skiba-Cassy, and S. Panserat. 2010b. Effects of insulin infusion on glucose homeostasis and glucose metabolism in rainbow trout fed a high-carbohydrate diet. J. Exp. Biol. 213:4151-4157.
37. Polakof, S., T. W. Moon, P. Aguirre, S. Skiba-Cassy, and S. Panserat. 2011b. Glucose homeostasis in rainbow trout fed a high carbohydrate diet: Metformin and insulin interact in a tissuedependent manner. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300:R166-R174.
38. Polakof, S., S. Skiba-Cassy, G. Choubert, and S. Panserat. 2010c. 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. 213:1443-1452.
39. Polakof, S., S. Skiba-Cassy, and S. Panserat. 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:R1769-R1776.
40. Potapova, I. A., M. R. El-Maghrabi, S. V. Doronin, and W. B. Benjamin. 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 39:1169-1179.
41. Radenne, A., M. Akpa, C. Martel, S. Sawadogo, D. Mauvoisin, and C. Mounier. 2008. Hepatic regulation of fatty acid synthase by insulin and T3: Evidence for T3 genomic and nongenomic actions. Am. J. Physiol. Endocrinol. Metab. 295:E884-E894.
42. Rollin, X., F. Médale, S. Gutieres, D. Blanc, and S. J. Kaushik. 2003. Short- and long-term nutritional modulation of acetyl-CoA carboxylase activity in selected tissues of rainbow trout (Oncorhynchus mykiss). Br. J. Nutr. 89:803-810.
43. Rozen, S., and H. J. Skaletsky. 2000. Primer3 on the WWW for general users and for biologist programmers. Pages 365-386 in S. Krawetz and S. Misener, ed. Bioinformatics Methods and Pro-tocols: Methods in Molecular Biology. Humana Press, Totowa, NJ.
44. Schwarz, J. M., P. Linfoot, D. Dare, and K. Aghajanian. 2003. Hepatic de novo lipogenesis in normoinsulinemic and hyperinsulinemic subjects consuming high-fat, low-carbohydrate and lowfat, high-carbohydrate isoenergetic diets. Am. J. Clin. Nutr. 77:43-50.
45. Seiliez, I., J. C. Gabillard, S. Skiba-Cassy, D. García-Serrana, J. Gutiérrez, S. Kaushik, S. Panserat, and S. Tesseraud. 2008. An in vivo and in vitro assessment of TOR signaling cascade in rainbow trout (Oncorhynchus mykiss). Am. J. Physiol. Regul. Integr. Comp. Physiol. 295:R329-R335.
46. Sheridan, M. A., N. Y. S. Woo, and H. A. Bern. 1985. Changes in the rates of glycogenesis, glycogenolysis, lipogenesis, and lipolysis in selected tissues of the coho salmon (Oncorhynchus kisutch) associated with parr-smolt transformation. J. Exp. Zool. 236:35-44.
47. Skiba-Cassy, S., M. Lansard, S. Panserat, and F. Medale. 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:R1421-R1429.
48. Taniguchi, C. M., B. Emanuelli, and C. R. Kahn. 2006. Critical nodes in signalling pathways: Insights into insulin action. Nat. Rev. Mol. Cell Biol. 7:85-96.
49. Walton, M. J., and C. B. Cowey. 1982. Aspects of intermediary metabolism in salmonid fish. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 73:59-79.
50. Warman, A. W. III, and N. R. Bottino. 1978. Lipogenic activity of catfish liver. Lack of response to dietary changes and insulin administration. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 59:153-161.
51. Witters, L. A., and B. E. Kemp. 1992. Insulin activation of acetyl-CoA carboxylase accompanied by inhibition of the 5′-AMPactivated protein kinase. J. Biol. Chem. 267:2864-2867.