Selection for high muscle fat in rainbow trout induces potentially higher chylomicron synthesis and PUFA biosynthesis in the intestine

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 164, Issue 2, 2013, Pages 417-427

  Kamalam, Biju Sam ^a   Panserat, Stephane ^a   Aguirre, Peyo ^a   Geurden, Inge ^a   Fontagné Dicharry, Stéphanie ^a   Médale, Françoise ^a  

^a UR1067 Nutrition Metabolism Aquaculture   (France)

Author keywords

Carbohydrates; Digestibility; Fatty acid bioconversion; Fish nutrition; Gene expression; Genetic selection; Intestine; Nutrient transport

Indexed keywords

APOLIPOPROTEIN A1; APOLIPOPROTEIN A4; CHYLOMICRON; FAT; FATTY ACID; GLUCOSE TRANSPORTER 2; MESSENGER RNA; SODIUM GLUCOSE COTRANSPORTER 1; STARCH;

ANIMAL TISSUE; ARTICLE; BIOTRANSFORMATION; BLOOD; CECUM; CONTROLLED STUDY; DIETARY INTAKE; FATTY ACID METABOLISM; GENETIC SELECTION; GENOTYPE; INTESTINE; LIPOPROTEIN SYNTHESIS; MEAL; MIDGUT; NONHUMAN; NUCLEOTIDE SEQUENCE; NUTRIENT UPTAKE; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PYLORUS; RAINBOW TROUT;

ONCORHYNCHUS MYKISS; SALMONIDAE;

EID: 84871653701     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2012.11.020     Document Type: Article

References (73)

1. Adibi S.A. Regulation of expression of the intestinal oligopeptide transporter (Pept-1) in health and disease. Am. J. Physiol. Gastrointest. Liver Physiol. 2003, 285:G779-G788.
2. Bakke A.M., Glover C., Krogdahl Å. Feeding, digestion and absorption of nutrients. Fish Physiol. 2011, 30:57-110.
3. Bakke-McKellep A., Nordrum S., Krogdahl Å., Buddington R. Absorption of glucose, amino acids, and dipeptides by the intestines of Atlantic salmon (Salmo salar L.). Fish Physiol. Biochem. 2000, 22:33-44.
4. Bell M., Dick J., Porter A.E.A. Pyloric ceca are significant sites of newly synthesized 22:6 n-3 in rainbow trout (Oncorhynchus mykiss). Lipids 2003, 38:39-44.
5. Bergot F. Digestibility of native starches of various botanical origins by rainbow trout (Oncorhynchus mykiss). Fish Nutrition in Practice 1993, 857-865. INRA, Paris. S.J. Kaushik, P. Luquet (Eds.).
6. Black D.D. Development and physiological regulation of intestinal lipid absorption. I. Development of intestinal lipid absorption: cellular events in chylomicron assembly and secretion. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 293:G519-G524.
7. Buddington R.K. Does the natural diet influence the intestine's ability to regulate glucose absorption?. J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 1987, 157:677-688.
8. Buddington R.K., Hilton J.W. Intestinal adaptations of rainbow trout to changes in dietary carbohydrate. Am. J. Physiol. Gastrointest. Liver Physiol. 1987, 253:G489-G496.
9. Buddington R.K., Krogdahl A., Bakke-McKellep A.M. The intestines of carnivorous fish: structure and functions and the relations with diet. Acta Physiol. Scand. Suppl. 1997, 638:67-80.
10. Choubert G., De La Noüe J., Luquet P. Digestibility in fish: improved device for the automatic collection of feces. Aquaculture 1982, 29:185-189.
11. Collie N.L., Ferraris R.P. Nutrient fluxes and regulation in fish intestine. Biochem. Mol. Biol. Fish. 1995, 4:221-239.
12. Cui X.L., Jiang L., Ferraris R.P. Regulation of rat intestinal GLUT2 mRNA abundance by luminal and systemic factors. Biochim. Biophys. Acta Biomembr. 2003, 1612:178-185.
13. Daniel H. Molecular and integrative physiology of intestinal peptide transport. Annu. Rev. Physiol. 2004, 66:361-384.
14. De Verdal H., Mignon-Grasteau S., Jeulin C., Le Bihan-Duval E., Leconte M., Mallet S., Martin C., Narcy A. Digestive tract measurements and histological adaptation in broiler lines divergently selected for digestive efficiency. Poult. Sci. 2010, 89:1955-1961.
15. Denstadli V., Vegusdal A., Krogdahl Å., Bakke-McKellep A., Berge G., Holm H., Hillestad M., Ruyter B. Lipid absorption in different segments of the gastrointestinal tract of Atlantic salmon (Salmo salar L.). Aquaculture 2004, 240:385-398.
16. Fan Y.K., Croom W.J., Daniel L.R., Bird A.R., Black B.L., Eisen E.J., McBride B.W. Selection for body composition does not affect energetic efficiency of jejunal glucose uptake in mice. J. Nutr. 1996, 126:2861-2866.
17. Fan Y., Croom W., Christensen V., Bird A., Daniel L., McBride B., Eisen E. Apparent energetic efficiency of jejunal glucose uptake in young adult turkeys selected for rapid growth. Can. J. Anim. Sci. 1998, 78:301-306.
18. Fang X., Wei Y., Liu Y., Wang J., Dai J. The identification of apolipoprotein genes in rare minnow (Gobiocypris rarus) and their expression following perfluorooctanoic acid exposure. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 2010, 151:152-159.
19. Ferraris R.P., Ahearn G.A. Sugar and amino acid transport in fish intestine. Comp. Biochem. Physiol. A Physiol. 1984, 77:397-413.
20. Ferraris R.P., Diamond J.M. Specific regulation of intestinal nutrient transporters by their dietary substrates. Annu. Rev. Physiol. 1989, 51:125-141.
21. Folch J., Lees M., Sloane-Stanley G. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 1957, 226:497-509.
22. Herd R., Arthur P. Physiological basis for residual feed intake. J. Anim. Sci. 2009, 87:E64-E71.
23. Hernandez-Blazquez F.J., Guerra R.R., Kfoury J.R., Bombonato P.P., Cogliati B., Silva J.R.M.C. Fat absorptive processes in the intestine of the Antarctic fish Notothenia coriiceps (Richardson, 1844). Polar Biol. 2006, 29:831-836.
24. Holtta-Vuori M., Salo V., Nyberg L., Brackmann C., Enejder A., Panula P., Ikonen E. Zebrafish: gaining popularity in lipid research. Biochem. J. 2010, 429:235-242.
25. Hussain M.M., Kedees M.H., Singh K., Athar H., Jamali N.Z. Signposts in the assembly of chylomicrons. Front. Biosci. 2001, 6:D320-D331.
26. Hussain M.M., Nijstad N., Franceschini L. Regulation of microsomal triglyceride transfer protein. Clin. Lipidol. 2011, 6:293-303.
27. Kamalam B.S., Medale F., Kaushik S., Polakof S., Skiba-Cassy S., Panserat S. Regulation of metabolism by dietary carbohydrates in two lines of rainbow trout divergently selected for muscle fat content. J. Exp. Biol. 2012, 215:2567-2578.
28. Karasov W.H., Diamond J.M. Interplay between physiology and ecology in digestion. Bioscience 1988, 38:602-611.
29. Kennedy S.R., Bickerdike R., Berge R.K., Dick J.R., Tocher D.R. Influence of conjugated linoleic acid (CLA) or tetradecylthioacetic acid (TTA) on growth, lipid composition, fatty acid metabolism and lipid gene expression of rainbow trout (Oncorhynchus mykiss L.). Aquaculture 2007, 272:489-501.
30. Kim K.Y., Cho Y.S., Bang I.C., Nam Y.K. Isolation and characterization of the apolipoprotein multigene family in Hemibarbus mylodon (Teleostei: Cypriniformes). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2009, 152:38-46.
31. Kirchner S., Panserat S., Lim P.L., Kaushik S., Ferraris R.P. The role of hepatic, renal and intestinal gluconeogenic enzymes in glucose homeostasis of juvenile rainbow trout. J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 2008, 178:429-438.
32. Kolditz C., Borthaire M., Richard N., Corraze G., Panserat S., Vachot C., Lefèvre F., Médale F. 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. 2008, 294:R1154-R1164.
33. Kolditz C.I., Paboeuf G., Borthaire M., Esquerré D., SanCristobal M., Lefèvre F., Médale F. Changes induced by dietary energy intake and divergent selection for muscle fat content in rainbow trout (Oncorhynchus mykiss), assessed by transcriptome and proteome analysis of the liver. BMC Genomics 2008, 9:506.
34. Kondo H., Morinaga K., Misaki R., Nakaya M., Watabe S. Characterization of the pufferfish Takifugu rubripes apolipoprotein multigene family. Gene 2005, 346:257-266.
35. Krasnov A., Teerijoki H., Mölsä H. Rainbow trout (Oncorhynchus mykiss) hepatic glucose transporter. Biochim. Biophys. Acta Gene Struct. Expr. 2001, 1520:174-178.
36. Krogdahl Å., Sundby A., Olli J.J. Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss) digest and metabolize nutrients differently. Effects of water salinity and dietary starch level. Aquaculture 2004, 229:335-360.
37. Krogdahl Å., Hemre G.I., Mommsen T. Carbohydrates in fish nutrition: digestion and absorption in postlarval stages. Aquacult. Nutr. 2005, 11:103-122.
38. Leaver M.J., Bautista J.M., Björnsson B.T., Jönsson E., Krey G., Tocher D.R., Torstensen B.E. Towards fish lipid nutrigenomics: current state and prospects for fin-fish aquaculture. Rev. Fish. Sci. 2008, 16:73-94.
39. Leaver M.J., Taggart J.B., Villeneuve L., Bron J.E., Guy D.R., Bishop S.C., Houston R.D., Matika O., Tocher D.R. Heritability and mechanisms of n-3 long chain polyunsaturated fatty acid deposition in the flesh of Atlantic salmon. Comp. Biochem. Physiol. Part D Genomics Proteomics 2011, 6:62-69.
40. Medale F. Relation between growth and utilization of energy substrates in three rainbow trout strains. Fish Nutrition in Practice 1993, 37-48. INRA, Paris. S.J. Kaushik, P. Luquet (Eds.).
41. Mignon-Grasteau S., Muley N., Bastianelli D., Gomez J., Peron A., Sellier N., Millet N., Besnard J., Hallouis J., Carré B. Heritability of digestibilities and divergent selection for digestion ability in growing chicks fed a wheat diet. Poult. Sci. 2004, 83:860-867.
42. Mitchell M., Smith M. The effects of genetic selection for increased growth rate on mucosal and muscle weights in the different regions of the small intestine of the domestic fowl (Gallus domesticus). Comp. Biochem. Physiol. A Physiol. 1991, 99:251-258.
43. Mithieux G. The new functions of the gut in the control of glucose homeostasis. Curr. Opin. Clin. Nutr. Metab. Care 2005, 8:445-449.
44. Moon T.W. Glucose intolerance in teleost fish: fact or fiction?. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2001, 129:243-249.
45. Mooradian A.D., Wong N.C.N., Shah G.N. Apolipoprotein A1 expression in young and aged rats is modulated by dietary carbohydrates. Metabolism 1997, 46:1132-1136.
46. Mooradian A.D., Haas M.J., Wong N.C.W. Transcriptional control of apolipoprotein AI gene expression in diabetes. Diabetes 2004, 53:513-520.
47. Moore S. Amino acid analysis: aqueous dimethyl sulfoxide as solvent for the ninhydrin reaction. J. Biol. Chem. 1968, 243:6281-6283.
48. Morais S., Pratoomyot J., Taggart J., Bron J., Guy D., Bell J., Tocher D. Genotype-specific responses in Atlantic salmon (Salmo salar) subject to dietary fish oil replacement by vegetable oil: a liver transcriptomic analysis. BMC Genomics 2011, 12:255.
49. Morais S., Silva T., Cordeiro O., Rodrigues P., Guy D.R., Bron J.E., Taggart J.B., Bell J.G., Tocher D.R. Effects of genotype and dietary fish oil replacement with vegetable oil on the intestinal transcriptome and proteome of Atlantic salmon (Salmo salar). BMC Genomics 2012, 13:448.
50. Olsen R., Henderson R., Ringø E. The digestion and selective absorption of dietary fatty acids in Arctic charr, Salvelinus alpinus. Aquacult. Nutr. 1998, 4:13-22.
51. Olsvik P., Lie K., Jordal A.E., Nilsen T., Hordvik I. Evaluation of potential reference genes in real-time RT-PCR studies of Atlantic salmon. BMC Mol. Biol. 2005, 6:21.
52. Ostaszewska T., Kamaszewski M., Grochowski P., Dabrowski K., Verri T., Aksakal E., Szatkowska I., Nowak Z., Dobosz S. The effect of peptide absorption on PepT1 gene expression and digestive system hormones in rainbow trout (Oncorhynchus mykiss). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2010, 155:107-114.
53. Pajor A., Hirayama B.A., Wright E.M. Molecular biology approaches to comparative study of Na (+)-glucose cotransport. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1992, 263:R489-R495.
54. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45.
55. Polakof S., Álvarez R., Soengas J.L. Gut glucose metabolism in rainbow trout: implications in glucose homeostasis and glucosensing capacity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 299:R19-R32.
56. Quillet E., Le Guillou S., Aubin J., Fauconneau B. Two-way selection for muscle lipid content in pan-size rainbow trout (Oncorhynchus mykiss). Aquaculture 2005, 245:49-61.
57. Rasmussen R.S., Jokumsen A. Digestibility in selected rainbow trout families and relation to growth and feed utilisation. Aquacult. Int. 2009, 17:187-197.
58. Rougière N., Malbert C.H., Rideau N., Cognié J., Carré B. Comparison of gizzard activity between chickens from genetic D+ and D- lines selected for divergent digestion efficiency. Poult. Sci. 2012, 91:460-467.
59. Rungruangsak-Torrissen K., Stien L.H., Daae B.S., Vågseth T., Thorsheim G.B., Tobin D., Ritola O. Different dietary levels of protein to lipid ratio affected digestive efficiency, skeletal growth, and muscle protein in rainbow trout families. Sch. Res. Exch. 2009, 2009:1-13.
60. Seiliez I., Panserat S., Kaushik S., Bergot P. Cloning, tissue distribution and nutritional regulation of a [Delta] 6-desaturase-like enzyme in rainbow trout. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2001, 130:83-93.
61. Sire M., Lutton C., Vernier J. New views on intestinal absorption of lipids in teleostean fishes: an ultrastructural and biochemical study in the rainbow trout. J. Lipid Res. 1981, 22:81-94.
62. Skiba-Cassy S., Lansard M., Panserat S., Médale F. 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. 2009, 297:R1421-R1429.
63. Soengas J.L., Moon T.W. Transport and metabolism of glucose in isolated enterocytes of the black bullhead Ictalurus melas: effects of diet and hormones. J. Exp. Biol. 1998, 201:3263-3273.
64. Spannhof L., Plantikow H. Studies on carbohydrate digestion in rainbow trout. Aquaculture 1983, 30:95-108.
65. Storebakken T., Shearer K.D., Refstie S., Lagocki S., McCool J. Interactions between salinity, dietary carbohydrate source and carbohydrate concentration on the digestibility of macronutrients and energy in rainbow trout (Oncorhynchus mykiss). Aquaculture 1998, 163:347-359.
66. Tocher D.R. Metabolism and functions of lipids and fatty acids in teleost fish. Rev. Fish. Sci. 2003, 11:107-184.
67. Tocher D.R., Fonseca-Madrigal J., Bell J.G., Dick J.R., Henderson R.J., Sargent J.R. Effects of diets containing linseed oil on fatty acid desaturation and oxidation in hepatocytes and intestinal enterocytes in Atlantic salmon (Salmo salar). Fish Physiol. Biochem. 2002, 26:157-170.
68. Valente L.M.P., Fauconneau B., Gomes E.F.S. Voluntary feed intake, feed and nutrient utilisation in slow and fast growing rainbow trout strains. Aquat. Living Resour. 1998, 11:93-99.
69. Vayro S., Wood I.S., Dyer J., Shirazi-Beechey S.P. Transcriptional regulation of the ovine intestinal Na+/glucose cotransporter SGLT1 gene. Eur. J. Biochem. 2001, 268:5460-5470.
70. Verri T., Kottra G., Romano A., Tiso N., Peric M., Maffia M., Boll M., Argenton F., Daniel H., Storelli C. Molecular and functional characterisation of the zebrafish (Danio rerio) PEPT1-type peptide transporter. FEBS Lett. 2003, 549:115-122.
71. Verri T., Romano A., Barca A., Kottra G., Daniel H., Storelli C. Transport of di-and tripeptides in teleost fish intestine. Aquacult. Res. 2009, 41:641-653.
72. Wilson J., Castro L. Morphological diversity of the gastrointestinal tract in fishes. Fish Physiol. 2011, 30:1-55.
73. Wright E.M. The intestinal Na+/glucose cotransporter. Annu. Rev. Physiol. 1993, 55:575-589.