Regulation of metabolism by dietary carbohydrates in two lines of rainbow trout divergently selected for muscle fat content

Journal of Experimental Biology

Volumn 215, Issue 15, 2012, Pages 2567-2578

  Kamalam, Biju Sam ^a   Medale, Françoise ^a   Kaushik, Sadasivam ^a   Polakof, Sergio ^a,b   Skiba Cassy, Sandrine ^a   Panserat, Stephane ^a  

^a UR1067 Nutrition Metabolism Aquaculture   (France)

^b CRNH AUVERGNE   (France)

Author keywords

Carbohydrates; Fish nutrition; Gene expression; Genetic selection; Metabolism

Indexed keywords

ADENYLATE KINASE; FATTY ACID; MESSENGER RNA; PROTEIN KINASE B; S6 KINASE; TRANSCRIPTION FACTOR;

ADIPOSE TISSUE; ANIMAL; ARTICLE; BLOOD; CARBOHYDRATE DIET; DRUG EFFECT; ENZYMOLOGY; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; GENETICS; GLUCONEOGENESIS; GLYCOLYSIS; GROWTH, DEVELOPMENT AND AGING; LIPOGENESIS; LIVER; METABOLISM; MUSCLE; OXIDATION REDUCTION REACTION; PHOSPHORYLATION; POSTPRANDIAL STATE; RAINBOW TROUT; WESTERN BLOTTING;

ADENYLATE KINASE; ADIPOSE TISSUE; ANIMALS; BLOTTING, WESTERN; DIETARY CARBOHYDRATES; FATTY ACIDS; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCONEOGENESIS; GLYCOLYSIS; LIPOGENESIS; LIVER; MUSCLES; ONCORHYNCHUS MYKISS; OXIDATION-REDUCTION; PHOSPHORYLATION; POSTPRANDIAL PERIOD; PROTO-ONCOGENE PROTEINS C-AKT; RIBOSOMAL PROTEIN S6 KINASES; RNA, MESSENGER; TRANSCRIPTION FACTORS;

ONCORHYNCHUS MYKISS; SALMONIDAE;

EID: 84863932363     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.070581     Document Type: Article

References (75)

1. Alvarez, M., Diez, A., Lopez-Bote, C., Gallego, M. and Bautista, J. (2000). Shortterm modulation of lipogenesis by macronutrients in rainbow trout (Oncorhynchus mykiss) hepatocytes. Br. J. Nutr. 84, 619-628.
2. Assifi, M. M., Suchankova, G., Constant, S., Prentki, M., Saha, A. K. and Ruderman, N. B. (2005). AMP-activated protein kinase and coordination of hepatic fatty acid metabolism of starved/carbohydrate-refed rats. Am. J. Physiol. Endocrinol. Metab. 289, E794-E800.
3. Austreng, E., Risa, S., Edwards, D. and Hvidsten, H. (1977). Carbohydrate in rainbow trout diets. II. Influence of carbohydrate levels on chemical composition and feed utilization of fish from different families. Aquaculture 11, 39-50.
4. Bergot, F. (1979). Effects of dietary carbohydrates and of their mode of distribution on glycaemia in rainbow trout (Salmo gairdneri Richardson). Comp. Biochem. Physiol. 64A, 543-547.
5. Blanc, J. (2002). Interaction between diet and genetic aptitude for weight and growth in juvenile rainbow trout, Oncorhynchus mykiss (Walbaum). Aquac. Res. 33, 563568.
6. Brauge, C., Corraze, G. and Medale, F. (1995). Effects of dietary levels of carbohydrate and lipid on glucose oxidation and lipogenesis from glucose in rainbow trout, Oncorhynchus mykiss, reared in freshwater or in seawater. Comp. Biochem. Physiol. 111A, 117-124.
7. Cowey, C. B. and Walton, M. J. (1989). Intermediary metabolism. In Fish Nutrition, 2nd edn (ed. J. E. Halver), pp. 259-329. New York: Academic Press.
8. Dentin, R., Denechaud, P. D., Benhamed, F., Girard, J. and Postic, C. (2006). Hepatic gene regulation by glucose and polyunsaturated fatty acids: a role for ChREBP. J. Nutr. 136, 1145-1149.
9. Eberle, D., Hegarty, B., Bossard, P., Ferre, P. and Foufelle, F. (2004). SREBP transcription factors: master regulators of lipid homeostasis. Biochimie 86, 839-848.
10. Edwards, D., Austreng, E., Risa, S. and Gjedrem, T. (1977). Carbohydrate in rainbow trout diets. I. Growth of fish of different families fed diets containing different proportions of carbohydrate. Aquaculture11, 31-38.
11. Enes, P., Panserat, S., Kaushik, S. and Oliva-Teles, A. (2009). Nutritional regulation of hepatic glucose metabolism in fish. Fish Physiol. Biochem. 35, 519-539.
12. Ferre, P. and Foufelle, F. (2007). SREBP-1c transcription factor and lipid homeostasis: clinical perspective. Horm. Res. Paediatr. 68, 72-82.
13. Figueiredo-Silva, A., Corraze, G., Borges, P. and Valente, L. (2010). Dietary protein/lipid level and protein source effects on growth, tissue composition and lipid metabolism of blackspot seabream (Pagellus bogaraveo). Aquac. Nutr. 16, 173-187.
14. Folch, J., Lees, M. and Sloane-Stanley, G. (1957). A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226, 497-509.
15. Gjedrem, T. (2000). Genetic improvement of cold-water fish species. Aquac. Res. 31, 25-33.
16. Hemre, G. I. and Kahrs, F. (1997). 14C-glucose injection in Atlantic cod, Gadus morhua, metabolic responses and excretion via the gill membrane. Aquac. Nutr. 3, 3-8.
17. Hemre, G. I., Mommsen, T. P. and Krogdahl, A. (2002). Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes. Aquac. Nutr. 8, 175-194.
18. Henryon, M., Jokumsen, A., Berg, P., Lund, I., Pedersen, P. B., Olesen, N. J. and Slierendrecht, W. J. (2002). Genetic variation for growth rate, feed conversion efficiency, and disease resistance exists within a farmed population of rainbow trout. Aquaculture 209, 59-76.
19. Hilton, J. W. and Atkinson, J. L. (1982). Response of rainbow trout (Salmo gairdneri) to increased levels of available carbohydrate in practical trout diets. Br. J. Nutr. 47, 597-607.
20. Hilton, J. W., Atkinson, J. L. and Slinger, S. J. (1987). Evaluation of the net energy value of glucose (cerelose) and maize starch in diets for rainbow trout (Salmo gairdneri). Br. J. Nutr. 58, 453-461.
21. Kaushik, S., Medale, F., Fauconneau, B. and Blanc, D. (1989). Effect of digestible carbohydrates on protein/energy utilization and on glucose metabolism in rainbow trout (Salmo gairdneri R.). Aquaculture 79, 63-74.
22. Kaushik, S. J. and de Oliva Teles, A. (1985). Effect of digestible energy on nitrogen and energy balance in rainbow trout. Aquaculture 50, 89-101.
23. Keppler, D. and Decker, K. (1974). Glycogen determination with amyloglucosidase. In Methods of Enzymatic Analysis (ed. H. U. Bergmeyer), pp. 1127-1131. New York: Academic Press.
24. Kim, J. and Kaushik, S. (1992). Contribution of digestible energy from carbohydrates and estimation of protein/energy requirements for growth of rainbow trout (Oncorhynchus mykiss). Aquaculture 106, 161-169.
25. Kirchner, S., Kaushik, S. and Panserat, S. (2003). Effect of partial substitution of dietary protein by a single gluconeogenic dispensable amino acid on hepatic glucose metabolism in rainbow trout (Oncorhynchus mykiss). Comp. Biochem. Physiol. 134A, 337-347.
26. Kirchner, S., Panserat, S., Lim, P., Kaushik, S. and Ferraris, R. (2008). The role of hepatic, renal and intestinal gluconeogenic enzymes in glucose homeostasis of juvenile rainbow trout. J. Comp. Physiol. 178B, 429-438.
27. Kolditz, C. I., Borthaire, M., Richard, N., Corraze, G., Panserat, S., Vachot, C., Lefevre, F. and Medale, F. (2008a). 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.
28. Kolditz, C. I., Paboeuf, G., Borthaire, M., Esquerre, D., SanCristobal, M., Lefevre, F. and Medale, F. (2008b). Changes induced by dietary energy intake and divergent selection for muscle fat contentin rainbow trout (Oncorhynchus mykiss), assessed by transcriptome and proteome analysis of the liver. BMC Genomics 9, 506-521.
29. Lansard, M., Panserat, S., Seiliez, I., Polakof, S., Plagnes-Juan, E., Geurden, I., Medale, F., Kaushik, S., Corraze, G. and Skiba-Cassy, S. (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, 1564-1573.
30. Likimani, T. A. and Wilson, R. P. (1982). Effects of diet on lipogenic enzyme activities in channel catfish hepatic and adipose tissue. J. Nutr. 112, 112-117.
31. Lin, H., Romsos, D. R., Tack, P. I. and Leveille, G. A. (1977a). Influence of diet on in vitro and in vivo rates of fatty acid synthesis in coho salmon [Oncorhynchus kisutch (Walbaum)]. J. Nutr. 107, 1677-1682.
32. Lin, H., Romsos, D. R., Tack, P. I. and Leveille, G. A. (1977b). Influence of dietary lipid on lipogenic enzyme activities in coho salmon, Oncorhynchus kisutch (Walbaum). J. Nutr. 107, 846-854.
33. Mazur, C. N., Higgs, D., Plisetskaya, E. and March, B. (1992). Utilization of dietary starch and glucose tolerance in juvenile chinook salmon (Oncorhynchus tshawytscha) of different strains in seawater. Fish Physiol. Biochem. 10, 303-313.
34. Mommsen, T. and Plisetskaya, E. (1991). Insulin in fishes and agnathans: history, structure, and metabolic regulation. Rev. Aquat. Sci. 4, 225-259.
35. Moon, T. W. (2001). Glucose intolerance in teleost fish: fact or fiction? Comp. Biochem. Physiol. 129B, 243-249.
36. Moore, S. (1968). Amino acid analysis: aqueous dimethyl sulfoxide as solvent for the ninhydrin reaction. J. Biol. Chem. 243, 6281-6283.
37. Morais, S., Pratoomyot, J., Taggart, J., Bron, J., Guy, D., Bell, J. and Tocher, D. (2011a). Genotype-specific responses in Atlantic salmon (Salmo salar) subject to dietary fish oil replacement by vegetable oil: a liver transcriptomic analysis. BMC Genomics 12, 255-271.
38. Morais, S., Pratoomyot, J., Torstensen, B. E., Taggart, J. B., Guy, D. R., Gordon Bell, J. and Tocher, D. R. (2011b). Diet x genotype interactions in hepatic cholesterol and lipoprotein metabolism in Atlantic salmon (Salmo salar) in response to replacement of dietary fish oil with vegetable oil. Br. J. Nutr. 106, 1457-1469.
39. Navarro, I., Leibush, B., Moon, T., Plisetskaya, E., Banos, N., Mendez, E., Planas, J. and Gutierrez, J. (1999). Insulin, insulin-like growth factor-I (IGF-I) and glucagon: the evolution of their receptors. Comp. Biochem. Physiol. 122B, 137-153.
40. Naylor, R. L., Goldburg, R. J., Primavera, J. H., Kautsky, N., Beveridge, M. C. M., Clay, J., Folke, C., Lubchenco, J., Mooney, H. and Troell, M. (2000). Effect of aquaculture on world fish supplies. Nature 405, 1017-1024.
41. Ntambi, J. M., Miyazaki, M. and Dobrzyn, A. (2004). Regulation of stearoyl-CoA desaturase expression. Lipids 39, 1061-1065.
42. Olsvik, P., Lie, K., Jordal, A. E., Nilsen, T. and Hordvik, I. (2005). Evaluation of potential reference genes in real-time RT-PCR studies of Atlantic salmon. BMC Mol. Biol. 6, 21-29.
43. Panserat, S., Medale, F., Blin, C., Breque, J., Vachot, C., Plagnes-Juan, E., Gomes, E., Krishnamoorthy, R. and Kaushik, S. (2000a). Hepatic glucokinase is induced by dietary carbohydrates in rainbow trout, gilthead seabream, and common carp. Am. J. Physiol. Regul. Integr. Comp. Physiol. 278, R1164-R1170.
44. Panserat, S., Medale, F., Breque, J., Plagnes-Juan, E. and Kaushik, S. (2000b). Lack of significant long-term effect of dietary carbohydrates on hepatic glucose-6-phosphatase expression in rainbow trout (Oncorhynchus mykiss). J. Nutr. Biochem. 11, 22-29.
45. Panserat, S., Plagnes-Juan, E., Breque, J. and Kaushik, S. (2001a). Hepatic phosphoenolpyruvate carboxykinase gene expression is not repressed by dietary carbohydrates in rainbow trout (Oncorhynchus mykiss). J. Exp. Biol. 204, 359-365.
46. Panserat, S., Plagnes-Juan, E. and Kaushik, S. (2001b). Nutritional regulation and tissue specificity of gene expression for proteins involved in hepatic glucose metabolism in rainbow trout (Oncorhynchus mykiss). J. Exp. Biol. 204, 2351-2360.
47. Panserat, S., Plagnes-Juan, E. and Kaushik, S. (2002). Gluconeogenic enzyme gene expression is decreased by dietary carbohydrates in common carp (Cyprinus carpio) and gilthead seabream (Sparus aurata). Biochim. Biophys. Acta 1579, 35-42.
48. Panserat, S., Skiba-Cassy, S., Seiliez, I., Lansard, M., Plagnes-Juan, E., Vachot, C., Aguirre, P., Larroquet, L., Chavernac, G., Medale, F. et al. (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.
49. Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
50. Pilkis, S. and Granner, D. (1992). Molecular physiology of the regulation of hepatic gluconeogenesis and glycolysis. Annu. Rev. Physiol. 54, 885-909.
51. Planas, J. V., Capilla, E. and Gutierrez, J. (2000). Molecular identification of a glucose transporter from fish muscle1. FEBS Lett. 481, 266-270.
52. Polakof, S., Skiba-Cassy, S. and 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, R1769-R1776.
53. Polakof, S., Mommsen, T. P. and Soengas, J. L. (2011a). Glucosensing and glucose homeostasis: from fish to mammals. Comp. Biochem. Physiol. 160B, 123-149.
54. Polakof, S., Medale, F., Larroquet, L., Vachot, C., Corraze, G. and Panserat, S. (2011b). Regulation of de novo hepatic lipogenesis by insulin infusion in rainbow trout fed a high-carbohydrate diet. J. Anim. Sci. 89, 3079-3088.
55. Polakof, S., Panserat, S., Craig, P. M., Martyres, D. J., Plagnes-Juan, E., Savari, S., Aris-Brosou, S. and Moon, T. W. (2011c). The metabolic consequences of hepatic AMP-kinase phosphorylation in rainbow trout. PloS ONE 6, e20228.
56. Polakof, S., Medale, F., Larroquet, L., Vachot, C., Corraze, G. and Panserat, S. (2011d). Insulin stimulates lipogenesis and attenuates beta-oxidation in white adipose tissue of fed rainbow trout. Lipids 46, 189-199.
57. Quillet, E., Le Guillou, S., Aubin, J. and Fauconneau, B. (2005). Two-way selection for muscle lipid content in pan-size rainbow trout (Oncorhynchus mykiss). Aquaculture 245, 49-61.
58. Quillet, E., Le Guillou, S., Aubin, J., Labbe, L., Fauconneau, B. and Medale, F. (2007). Response of a lean muscle and a fat muscle rainbow trout (Oncorhynchus mykiss) line on growth, nutrient utilization, body composition and carcass traits when fed two different diets. Aquaculture 269, 220-231.
59. Randle, P. J. (1998). Regulatory interactions between lipids and carbohydrates: the glucose fatty acid cycle after 35 years. Diabetes Metab. Rev. 14, 263-283.
60. Refstie, T. and Austreng, E. (1981). Carbohydrate in rainbow trout diets. III. Growth and chemical composition of fish from different families fed four levels of carbohydrate in the diet. Aquaculture 25, 35-49.
61. Rutter, G. A., Xavier, G. D. S. and Leclerc, I. (2003). Roles of 5-AMP-activated protein kinase (AMPK) in mammalian glucose homoeostasis. Biochem. J. 375, 1-16.
62. Seiliez, I., Panserat, S., Kaushik, S. and Bergot, P. (2001). Cloning, tissue distribution and nutritional regulation of a A6-desaturase-like enzyme in rainbow trout. Comp. Biochem. Physiol. 130B, 83-93.
63. Seiliez, I., Gabillard, J. C., Skiba-Cassy, S., Garcia-Serrana, D., Gutierrez, J., Kaushik, S., Panserat, S. and Tesseraud, S. (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.
64. Seiliez, I., Panserat, S., Lansard, M., Polakof, S., Plagnes-Juan, E., Surget, A., Dias, K., Larquier, M., Kaushik, S. and 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, 733-743.
65. Shaw, R. J. (2009). LKB1 and AMP-activated protein kinase control of mTOR signalling and growth. Acta Physiol. 196, 65-80.
66. Skiba-Cassy, S., Lansard, M., Panserat, S. and 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, R1421-R1429.
67. Stone, D. A. J. (2003). Dietary carbohydrate utilization by fish. Rev. Fish. Sci. 11, 337370.
68. Tacon, A. G. J. and Metian, M. (2008). Global overview on the use of fish meal and fish oil in industrially compounded aquafeeds: trends and future prospects. Aquaculture 285, 146-158.
69. Tocher, D., Leaver, M. and Hodgson, P. (1998). Recent advances in the biochemistry and molecular biology of fatty acyl desaturases. Prog. Lipid Res. 37, 73-117.
70. Towle, H. C., Kaytor, E. N. and Shih, H. M. (1997). Regulation of the expression of lipogenic enzyme genes by carbohydrate. Annu. Rev. Nutr. 17, 405-433.
71. Vagner, M. and Santigosa, E. (2010). Characterization and modulation of gene expression and enzymatic activity of delta-6 desaturase in teleosts: a review. Aquaculture 315, 131-143.
72. West, T., Schulte, P. and Hochachka, P. (1994). Implications of hyperglycemia for post-exercise resynthesis of glycogen in trout skeletal muscle. J. Exp. Biol. 189, 6984.
73. Wilson, R. (1994). Utilization of dietary carbohydrate by fish. Aquaculture124, 67-80.
74. Wullschleger, S., Loewith, R. and Hall, M. N. (2006). TOR signaling in growth and metabolism. Cell124, 471-484.
75. Yamada, K. and Noguchi, T. (1999). Nutrient and hormonal regulation of pyruvate kinase gene expression. Biochem. J. 337, 1-11.