Hostname: page-component-7c8c6479df-hgkh8 Total loading time: 0 Render date: 2024-03-29T14:26:08.429Z Has data issue: false hasContentIssue false

Intake of high levels of vitamin A and polyunsaturated fatty acids during different developmental periods modifies the expression of morphogenesis genes in European sea bass (Dicentrarchus labrax)

Published online by Cambridge University Press:  08 March 2007

Laure A. N. Villeneuve*
Affiliation:
UMR1067, Nutrition Aquaculture Génomique, IFREMER, 29 280 Plouzané, France
Enric Gisbert
Affiliation:
Centre d'Aqüicultura, Institut de Recerca i Tecnologia Agroalimentaries (IRTA), Aptat. Correus 200, 43 540 Sant Carles de la Ràpita, Tarragona, Spain
Jacques Moriceau
Affiliation:
UMR1067, Nutrition Aquaculture Génomique, IFREMER, 29 280 Plouzané, France
Chantal L. Cahu
Affiliation:
UMR1067, Nutrition Aquaculture Génomique, IFREMER, 29 280 Plouzané, France
José L. Zambonino Infante
Affiliation:
UMR1067, Nutrition Aquaculture Génomique, IFREMER, 29 280 Plouzané, France
*
*Corresponding author: Dr Laure A. N. Villeneuve, fax +33 298224366, email villeneuvelan@yahoo.fr
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The effect of the feeding period on larval development was investigated in European sea bass larvae by considering the expression level of some genes involved in morphogenesis. Larvae were fed a control diet except during three different periods (period A: from 8 to 13d post-hatching (dph); period B: from 13 to 18dph; period C: from 18 to 23dph) with two compound diets containing high levels of vitamin A or PUFA. European sea bass morphogenesis was affected by these two dietary nutrients during the early stages of development. The genes involved in morphogenesis could be modulated between 8 and 13dph, and our results indicated that retinoids and fatty acids influenced two different molecular pathways that in turn implicated two different gene cascades, resulting in two different kinds of malformation. Hypervitaminosis A delayed development, reducing the number of vertebral segments and disturbing bone formation in the cephalic region. These malformations were correlated to an upregulation of retinoic acid receptor γ, retinoid X receptor (RXR) α and bone morphogenetic protein (BMP)4. An excess of PUFA accelerated the osteoblast differentiation process through the upregulation of RXRα and BMP4, leading to a supernumerary vertebra. These results suggest that the composition of diets devoted to marine fish larvae has a particularly determining effect before 13dph on the subsequent development of larvae and juvenile fish.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2006

References

Balmer, JE & Blomhoff, RGene expression regulation by retinoic acid. J Lipid Res (2002) 43, 17731808.CrossRefGoogle ScholarPubMed
Barnabé, G, Boulineau-Coatanea, F & Rene, FChronologie de la morphogenèse chez le loup ou bar Dicentrarchus labrax (L.) (Pisces, Serranidae) obtenu par reproduction artificielle. Aquaculture (1976) 8, 351363.CrossRefGoogle Scholar
Bessey, OA, Lowry, OH & Brock, MJA method for the rapid determination of alkaline phosphatase with five cubic millimeters of serum. J Biol Chem (1946) 164, 321329.CrossRefGoogle ScholarPubMed
Bradford, MMA rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem (1976) 72, 248254.CrossRefGoogle ScholarPubMed
Cahu, C & Zambonino Infante, JLSubstitution of live food by formulated diets in marine fish larvae. Aquaculture (2001) 200, (1–2), Special issue,161180.CrossRefGoogle Scholar
Cahu, CL, Zambonino Infante, JL& Barbosa, VEffect of dietary phospholipid level and phospholipid: neutral lipid value on the development of sea bass (Dicentrarchus labrax) larvae fed a compound diet. Br J Nutr (2003) 90, 2128.CrossRefGoogle ScholarPubMed
Crane, KK, Boge, G & Rigal, AIsolation of brush border membranes in vesicular form from the intestinal spiral valve of the small dogfish (Scyliorhinus canicula). Biomembranes (1979) 554, 264267.CrossRefGoogle ScholarPubMed
Dagnelie, PLes méthodes de l'inférence statistique. In Théorie et méthodes statistiques, pp. 1463 [Ducolot, J, editor]. Gambloux, Belgium: Les Presses Agronomiques de Gembloux (1975)Google Scholar
Folch, J, Lees, M & Stanley, GHSA simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem (1957) 226, 497509.CrossRefGoogle ScholarPubMed
Gabbitas, B & Canalis, ERetinoic acid regulates the expression of insulin-like growth factors I and II in osteoblasts. J Cell Physiol (1997) 172, 253264.3.0.CO;2-A>CrossRefGoogle Scholar
Gause, WC & Adamovicz, JThe use of the PCR to quantitate gene expression. PCR Methods Appl (1994) 3, 123135.CrossRefGoogle ScholarPubMed
Gisbert, E, Villeneuve, L, Zambonino Infante, JL, Quazuguel, P & Cahu, CLDietary phospholipids are more efficient than neutral lipids for long-chain polyunsaturated fatty acid supply in European sea bass Dicentrarchus labrax larval development. Lipids (2005) 40, 609618.CrossRefGoogle ScholarPubMed
Glozak, MA & Rogers, MBBMP4- and RA-induced apoptosis is mediated through the activation of retinoic acid receptor [alpha] and [gamma] in P19 embryonal carcinoma cells. Exp Cell Res (1998) 242, 165173.CrossRefGoogle ScholarPubMed
Haga, Y, Suzuki, T, Kagechika, H & Takeuchi, TA retinoic acid receptor-selective agonist causes jaw deformity in the Japanese flounder, Paralichthys olivaceus. Aquaculture (2003) 221, 381392.CrossRefGoogle Scholar
Haga, Y, Suzuki, T & Takeuchi, TRetinoic acid isomers produce malformations in postembryonic development of the Japanese flounder, Paralichthys olivaceus. Zool Sci (2002) 19, 11051112.CrossRefGoogle ScholarPubMed
Hogan, BLBone morphogenic proteins: multifunctional regulators of vertebrate development. Gene Dev (1996) 10, 15801594.CrossRefGoogle Scholar
Holm, H, Hanssen, LE, Krogdahl, A & Florholmen, JHigh and low inhibitor soybean meals affect human duodenal proteinase activity differently: in vivo comparison with bovine serum albumin. J Nutr (1988) 118, 515520.CrossRefGoogle ScholarPubMed
Juaneda, P & Roquelin, GRapid and convenient separation of phospholipid and non phosphorus lipids from rat heart using silica cartridges. Lipids (1985) 20, 4041.CrossRefGoogle ScholarPubMed
Kacem, A, Meunier, FJ, Aubin, J & Haffray, PCaractérisation histo-morphologique des malformations du squelette vertébral chez la truite arc-en-ciel (Oncorhynchus mykiss) après différents traitements de triploïdisation. Cybium (2004) 28, 1523.Google Scholar
Keller, H, Dreyer, C, Medin, J, Mahfoudi, A, Ozato, K & Wahli, WFatty acids and retinoids control lipid metabolism through activation of peroxisome proliferator-activated receptor-retinoid X receptor heterodimers. PNAS (1993) 90, 21602164.CrossRefGoogle ScholarPubMed
Krumlauf, RHox genes in vertebrate development. Cell (1994) 78, 191201.CrossRefGoogle ScholarPubMed
Lewis, LM, Lall, sp & Eckhard Witten, PMorphological descriptions of the early stages of spine and vertebral development in hatchery-reared larval and juvenile Atlantic halibut (Hippoglossus hippoglossus). Aquaculture (2004) 241, 4759.CrossRefGoogle Scholar
Mata de Urquiza, A, Liu, S, Sjöberg, M, Zetterström, RH, Griffiths, W, Sjövall, J & Perlmann, TDocosahexaenoic acid, a ligand for the retinoid X receptor in mouse brain. Science (2000) 290, 21402144.CrossRefGoogle Scholar
Métais, P & Bieth, JDétermination de l'a-amylase par une microtechnique. Ann Biol Clin-Paris (1968) 26, 133142.Google Scholar
National Research Council Guide for the Care and Use of the Laboratory Animals. Publication No. 85–23 (rev.). Bethesda, MD: National Institutes of Health. (1985)Google Scholar
Péres, A, Zambonino Infante, JL & Cahu, CDietary regulation of activities and mRNA levels of trypsin and amylase in sea bass (Dicentrarchus labrax) larvae. Fish Physiol Biochem (1998) 19, 145152.CrossRefGoogle Scholar
Pfaffl, MWA new mathematical model for relative quantifi- cation in real-time RT-PCR. Nucleic Acids Res (2001) 29, e45.CrossRefGoogle Scholar
Pfaffl, MW, Horgan, GW & Dempfle, LRelative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res (2002) 30, 936.CrossRefGoogle Scholar
Ribeiro, L, Zambonino Infante, JL, Cahu, C & Dinis, MTDigestive enzymes profile of Solea senegalensis post larvae fed Artemia and a compound diet. Fish Physiol Biochem (2002) 27, (1–2), 6169.CrossRefGoogle Scholar
Ross, SA, McCaffery, PJ, Drager, UC & De Luca, LMRetinoids in embryonal development. Physiol Rev (2000) 80, 10211054.CrossRefGoogle ScholarPubMed
Sargent, J, McEvoy, L, Estevez, A, Bell, G, Bell, M, Henderson, J & Tocher, DLipid nutrition of marine fish during early development: current status and future directions. Aquaculture (1999) 179, 217229.CrossRefGoogle Scholar
Skillington, J, Choy, L & Derynck, RBone morphogenetic protein and retinoic acid signaling cooperate to induce osteoblast differentiation of preadipocytes. J Cell Biol (2002) 159, 135146.CrossRefGoogle ScholarPubMed
Solheim, EGrowth factors in bone. Int Orthop (1998) 22, 410416.CrossRefGoogle ScholarPubMed
Suzuki, T, Oohara, I & Kurokawa, TRetinoic acid given at late embryonic stage depresses sonic hedgehog and Hoxd-4 expression in the pharyngeal area and induces skeletal malformation in flounder (Paralichthys olivaceus) embryos. Develop Growth Differ (1999) 41, 143152.CrossRefGoogle ScholarPubMed
Suzuki, T, Srivastava, AS & Kurokawa, TExperimental induction of jaw, gill and pectoral fin malformations in Japanese flounder, Paralichthys olivaceus, larvae. Aquaculture (2000) 185, 175187.CrossRefGoogle Scholar
Thompson, DL, Gerlach-Banck, LM, Barald, KF & Koenig, RJRetinoic acid repression of bone morphogenetic protein 4 in inner ear development. Mol Cell Biol (2003) 23, 22772286.CrossRefGoogle ScholarPubMed
Villeneuve, L, Gisbert, E, Cahu, CL, Gall, MM & Zambonino-Infante, JLExpression and localization of some retinoid receptors during European sea bass (Dicentrarchus labrax) larvae development. Aquaculture (2004) 242, 537551.CrossRefGoogle Scholar
Villeneuve, L, Gisbert, E, Le Delliou, H, Cahu, CL & Zambonino-Infante, JDietary levels of all-trans retinol affect retinoid nuclear receptor expression and skeletal development in European sea bass larvae. Br J Nutr (2005 a) 93, 112.CrossRefGoogle ScholarPubMed
Villeneuve, L, Gisbert, E, Zambonino-Infante, JL, Quazuguel, P & Cahu, CLEffects of lipids on European sea bass morphogenesis: implication of retinoid receptors. Br J Nutr (2005 b) 94, 877884.CrossRefGoogle ScholarPubMed
Yu, VC, Delsert, C, Andersen, B, Holloway, JM, Devary, OV, Näär, AMKim, SY, Boutin, JM, Glass, CK & Rosenfeld, MGRXRb: a coregulator that enhances binding of retinoic acid, thyroid hormone, and vitamin D receptors to their cognate response elements. Cell (1991) 67, 12511266.CrossRefGoogle Scholar
Zambonino Infante, J & Cahu, CLOntogeny of the gastrointestinal tract of marine fish larvae. Comp Biochem Physiol C (2001) 130, 477487.Google ScholarPubMed
Zambonino-Infante, JL, Cahu, CL & Péres, APartial substitution of di- and tripeptides for native protein in sea bass diet improves Dicentrarchus labrax larval development. J Nutr (1997) 127, 604614.CrossRefGoogle ScholarPubMed
Zizola, CF, Balana, ME, Sandoval, M &Calvo, JCChanges in IGF-I receptor and IGF-I mRNA during differentiation of 3T3- L1 preadipocytes. Biochimie (2002) 84, 975980.CrossRefGoogle ScholarPubMed