Hostname: page-component-76fb5796d-2lccl Total loading time: 0 Render date: 2024-04-26T13:45:25.731Z Has data issue: false hasContentIssue false
  • English
  • Français

Dietary levels of all-trans retinol affect retinoid nuclear receptor expression and skeletal development in European sea bass larvae

Published online by Cambridge University Press:  08 March 2007

Laure Villeneuve ,
Enric Gisbert ,
Hervé Le Delliou ,
Chantal L. Cahu  and
Jose L. Zambonino-Infante
Laure Villeneuve*
Affiliation:
Unité Mixte de Nutrition des Poissons IFREMER-INRA, IFREMER, 29 280, Plouzané, France
Enric Gisbert
Affiliation:
Unité Mixte de Nutrition des Poissons IFREMER-INRA, IFREMER, 29 280, Plouzané, France Centre d'aqüicultura, Institut de Recerca i Tecnologia Agroalimentaries (IRTA), Aptat. Correus 200, 43540 Sant Carles de la Ràpita, Tarragona, Spain
Hervé Le Delliou
Affiliation:
Unité Mixte de Nutrition des Poissons IFREMER-INRA, IFREMER, 29 280, Plouzané, France
Chantal L. Cahu
Affiliation:
Unité Mixte de Nutrition des Poissons IFREMER-INRA, IFREMER, 29 280, Plouzané, France
Jose L. Zambonino-Infante
Affiliation:
Unité Mixte de Nutrition des Poissons IFREMER-INRA, IFREMER, 29 280, Plouzané, France
*
*Corresponding author: Dr Laure Villeneuve, fax +33 298884363, email lvillene@ifremer.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.

European sea bass larvae were fed different dietary vitamin A levels. Growth, skeletal development and the expression of genes involved in larval morphogenesis were evaluated. From 7 to 42 d post-hatching, larvae were fed five isoproteic and isolipidic compound diets with graded levels of retinyl acetate (RA; RA0, RA10, RA50, RA250 and RA1000, containing 0, 10, 50, 250 and 1000 mg RA/kg DM, respectively), resulting in an incorporation of 12, 13, 31, 62 and 196 mg all-trans retinol/kg DM. Larvae fed extreme levels of RA had weights 19 % and 27 % lower than those of the RA50 group. The RA1000 diet induced a fall in growth with an increase of circulating and storage retinol forms in larvae, revealing hypervitaminosis. High levels of RA affected maturation of the pancreas and intestine. These data indicated that the optimal RA level was close to 31 mg/kg DM. Inappropriate levels of dietary RA resulted in an alteration of head organisation characterised by the abnormal development of the splanchnocranium and neurocranium, and scoliotic fish. Of the larvae fed RA1000, 78·8 % exhibited skeletal abnormalities, whereas the RA50 group presented with 25 % malformations. A linear correlation between vitamin A level and malformation percentage was observed and mainly associated with an upregulation of retinoic acid receptor-γ expression in the RA1000 group during the 2 first weeks after hatching. The expression of retinoid X receptor-α decreased during normal larval development when that of the retinoic acid receptors increased. This work highlights the involvement of retinoid pathways in the appearance of dietary-induced skeletal malformations during post-hatching development in sea bass.

Keywords

RetinolEuropean sea bassSkeletal malformationsRetinoic acid nuclear receptors (RAR, RXR)Growth factors (BMP-4, IGF-1)
Type
Research Article
Information
British Journal of Nutrition , Volume 93 , Issue 6 , June 2005 , pp. 791 - 801
Copyright
Copyright © The Nutrition Society 2005

References

Allan, GJ, Zannoni, AMcKinnel, IOho, WR, Holzenberger, M, Flint, DJ & Patel, K (2003) Major components of the insulin-like growth factor axis are expressed early in chicken embryogenesis, with IGF binding protein (IGFBP)-5 expression subject to regulation by Sonic Hedgehog. Anat Embryol 207, 73–84.CrossRefGoogle ScholarPubMed
Balmer, JE & Blomhoff, R (2002) Gene expression regulation by retinoic acid. J Lipid Res 43, 1773–1808.CrossRefGoogle ScholarPubMed
Barnabé, G, Boulineau-Coatanea, F & Rene, F (1976) Chronologie de la morphogenèse chez le loup ou bar Dicentrarchus labrax (L.) (Pisces Serranidae) obtenu par reproduction artificielle. Aquaculture 8, 351–363.CrossRefGoogle Scholar
Bessey, OA, Lowry, OH & Brock, MJ (1946) Rapid coloric method for determination of alkaline phosphatase in five cubic millimeters of serum. J Biol Chem 164, 321–329.CrossRefGoogle Scholar
Bradford, MM (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.CrossRefGoogle ScholarPubMed
Cahu, CL & Zambonino, Infante JL (1994) Early weaning of sea bass (Dicentrarchus labrax) larvae with a compound diet: effect on digestive enzymes. Comp Biochem Physiol 109A, 213–222.CrossRefGoogle Scholar
Cahu, CL & Zambonino, Infante JL (2001) Substitution of live food by formulated diets in marine fish larvae. Aquaculture 200, 161–180.CrossRefGoogle Scholar
Cahu, CLZambonino, Infante JL & Barbosa, V (2003a) Effect 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 90, 21–28.CrossRefGoogle ScholarPubMed
Cahu, C, Zambonino, Infante J & Takeuchi, T (2003b) Nutritional components affecting skeletal development in fish larvae. Aquaculture 227, 245–258.CrossRefGoogle Scholar
Cohlan, SQ (1953) Excessive intakes of vitamin A as a cause of congenital anomalies in the rat. Science 117, 535–536.CrossRefGoogle ScholarPubMed
Conlon, RA (1995) Retinoic acid and pattern formation in vertebrates. Trends Genet 11, 314–319.CrossRefGoogle ScholarPubMed
Crane, RK, Boge, G & Rigal, A (1979) Isolation of brush border membranes in vesicular form from the intestinal spiral valve of the small dogfish (Scyliorhinus canicula). Biochim Biophys Acta 554, 264–267.CrossRefGoogle ScholarPubMed
Dagnelie, P (1975) Les méthodes de l'inférence statistique. In Théorie et méthodes statistiques, Vol. 2, pp. 1–463 [Ducolot, J, editor]. Gembloux, Belgium: Les Presses Agronomiques de Gembloux.Google Scholar
Dahlqvist, A (1970) Assay of intestinal disaccharidase. Enzym Biol Clin 11, 52–56.CrossRefGoogle Scholar
Dedi, J, Takeuchi, T, Seikai, T, Watanabe, T & Hosaya, K (1997) Hypervitaminosis A during vertebral morphogenesis in larval Japanese flounder. Fish Sci 63, 466–473.CrossRefGoogle Scholar
Fu, Z, Noguchi, T & Kato, H (2001) Vitamin A deficiency reduces insulin-like growth factor (IGF)-I gene expression and increases IGF-I receptor and insulin receptor gene expression in tissues of Japanese Quail (Coturnix coturnix japonica). J Nutr 131, 1189–1194.CrossRefGoogle ScholarPubMed
Gabbitas, B & Canalis, E (1997) Retinoic acid regulates the expression of insulin-like growth factors I and II in osteoblasts. J Cell Physiol 172, 253–264.3.0.CO;2-A>CrossRefGoogle Scholar
Gause, WC & Adamovicz, J (1994) The use of the PCR to quantitate gene expression. PCR Methods Appl 3, 123–135.CrossRefGoogle ScholarPubMed
Gouillou-Coustans, MF & Guillaume, J (2001) Vitamin nutrition. In Nutrition and Feeding of Fish and Crustaceans, pp. 145–166 [Guillaume, J, Kaushik, SJ, Bergot, P and Metallier, R, editors]. Chichester: Springer-Praxis.Google Scholar
Gouillou-Coustans, MF, Bergot, P & Kaushik, SJ (1998) Dietary ascorbic acid needs of common carp (Cyprinus carpio) larvae. Aquaculture 161, 453–461.CrossRefGoogle Scholar
Grolier, P, Agoudavi, S & Azais-Braesco, V (1995) Comparative bioavailability of diet-, oil- and emulsion-based preparations of vitamin A and b-carotene in rat. Nutrition Res 15, 1507–1516.CrossRefGoogle Scholar
Haga, Y, Suzuki, T, Kagechika, H & Takeuchi, T (2003) A retinoic acid receptor-selective agonist causes jaw deformity in the Japanese flounder. Paralichthys olivaceus. Aquaculture 221, 381–392.CrossRefGoogle Scholar
Haga, Y, Suzuki, T & Takeuchi, T (2002) Retinoic acid isomers produce malformations in postembryonic development of the Japanese flounder, Paralichthys olivaceus. Zool Sci 19, 1105–1112.CrossRefGoogle ScholarPubMed
Helms, JA, Kim, CH, Hu, D, Minkoff, R, Thaller, C & Eichele, G (1997) Sonic hedgehog participates in cranofacial morphogenesis and is down-regulated by teratogenic doses of retinoic acid. Dev Biol 187, 25–35.CrossRefGoogle Scholar
Henning, SJ (1987) Functional development of the gastrointestinal tract. In Physiology of the Gastrointestinal Tract, pp. 285–300 [Johnson, LR, editor]. New York: Raven Press.Google Scholar
Hogan, BL (1996) Bone morphogenic proteins: multifunctional regulators of vertebrate development. Gene Dev 10, 1580–1594.CrossRefGoogle Scholar
Holm, H, Hanssen, LE, Krogdahl, A & Florholmen, J (1988) High and low inhibitor soybean meals affect human duodenal proteinase activity differently: in vivo comparison with bovine serum albumin. J Nutr 118, 515–520.CrossRefGoogle ScholarPubMed
Joore, J, Van, D, Lans, GBLJ, Lanser, PH, Vervaart, JM, Zivkovic, D, Speksnijder, JE & Kruijer, W (1994) Effects of retinoic acid on the expression of retinoic acid receptors during zebrafish embryogenesis. Mech Dev 46, 137–150.CrossRefGoogle ScholarPubMed
Kaushik, SJ, Gouillou-Coustans, MF & Cho, CY (1998) Application of the recommendations on vitamin requirements of finfish by NRC (1993) to salmonids and sea bass using practical and purified diets. Aquaculture 161, 463–474.CrossRefGoogle Scholar
Kimmel, CB, Ballard, WW, Kimmel, SR, Ullman, B & Schilling, TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203, 253–310.CrossRefGoogle ScholarPubMed
Kobayashi, H, Spilde, TL, Bhatia, AM, Scita, GDeLuca, LMTaira, M, Levin, AA, Ozato, K & David, IB (2002) Retinoid signaling controls mouse pancreatic exocrine lineage selection through epithelial-mesenchymal interactions. Gastroenterology 123, 1331–1340.CrossRefGoogle ScholarPubMed
Krumlauf, R (1994) Hox genes in vertebrate development. Cell 78, 191–201.CrossRefGoogle ScholarPubMed
Lee, SH, Fu, KK, Hui, JN & Richma, JM (2001) Noggin and retinoic acid transform the identity of avian facial prominences. Nature 414, 909–912.CrossRefGoogle ScholarPubMed
Li, H, Bartold, PM, Zhang, CZ, Clarkson, RW, Young, WG & Waters, MJ (1998) Growth hormone and insulin-like growth factor I induce bone morphogenetic proteins 2 and 4: a mediator role in bone and tooth formation? Endocrinology 139, 3855–3862.CrossRefGoogle ScholarPubMed
Maroux, S, Louvard, D & Baratti, J (1973) The aminopeptidase from hog-intestinal brush border. Biochim Biophys Acta 321, 282–295.CrossRefGoogle ScholarPubMed
Minucci, S, Saint-Jeannet, JP, Toyama, R, Bichingham, BB, Hembree, MJ, Prasadan, K, Preuett, BL, Imamurea, M & Gittes, GK (1996) Retinoic X receptor-selective ligands produce malformations in Xenopus embryos. Proc Natl Acad Sci U S A 93, 1803–1807.CrossRefGoogle ScholarPubMed
National Research Council (1985) Guide for the Care and Use of the Laboratory Animals. Publication no. 85–23 (rev.). Bethesda, MD: National Institutes of Health.Google Scholar
National Research Council (1993) Nutrient Requirements of Fish. Washington, DC: National Academy Press.Google Scholar
Ornsrud, R, Graff, IE, Hoie, S, Totland, GK & Hemre, GI (2002) Hypervitaminosis A in first-feeding fry of the Atlantic salmon (Salmo salar L.). Aquac Nutr 8, 7–13.CrossRefGoogle Scholar
Péres, AZambonino, Infante JL & Cahu, CL (1998) Dietary regulation of activities and mRNA levels of trypsin and amylase in sea bass (Dicentrarchus labrax) larvae. Fish Physiol Biochem 19, 145–152.CrossRefGoogle Scholar
Pfaffl, MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29, 2002–2007.CrossRefGoogle ScholarPubMed
Pfaffl, MW, Horgan, GW & Dempfle, L (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30, 9–36.CrossRefGoogle Scholar
Qin, P, Cimildoro, R, Kochhar, DM, Soprano, KJ & Robert, Soprano D (2002) PBX, MEIS, and IGF-I are potential mediators of retinoic acid-induced proximodistal limb reduction defects. Teratology 66, 224–234.CrossRefGoogle ScholarPubMed
Raul, F, Noriega, R, Doffoel, M, Grenier, JF & Haffen, K (1982) Modifications of brush border enzyme activities during starvation in the jejunum and ileum of adult rats. Enzyme 28, 328–335.CrossRefGoogle ScholarPubMed
Reifen, R, Zaiger, G & Uni, Z (1998) Effect of vitamin A on small intestinal brush border enzymes in a rat. Int J Vitam Nutr Res 68, 281–286.Google ScholarPubMed
Ross, SA, McCaffery, PJ, Drager, UC & De Luca, LM (2000) Retinoids in embryonal development. Physiol Rev 80, 1021–1054.CrossRefGoogle ScholarPubMed
Suzuki, T, Oohara, I & Kurokawa, T (1998) Hoxd-4 expression during pharyngeal arch development in flounder (Paralichthys olivaceus) embryos and effects of retinoic acid on expression. Zool Sci 15, 57–67.CrossRefGoogle ScholarPubMed
Suzuki, T, Srivastava, AS & Kurokawa, T (2000) Experimental induction of jaw, gill and pectoral fin malformations in Japanese flounder, Paralichthys olivaceus, larvae. Aquaculture 185, 175–187.CrossRefGoogle Scholar
Uni, Z, Zaiger, GGal-Garber, OPines, M, Rozenboim, I & Reifen, R (2000) Vitamin A deficiency interferes with proliferation and maturation of cells in the chicken small intestine. Br Poult Sci 41, 410–415.CrossRefGoogle ScholarPubMed
Yates, KE, Troulis, MJ, Kaban, LB & Glowacki, J (2002) IGF-I, TGF-β, and BMP-4 are expressed during distraction osteogenesis of the pig mandible. Int J Oral Maxillofac Surg 31, 173–178.CrossRefGoogle ScholarPubMed
Yu, VC, Delsert, C, Andersen, B, Holloway, JM, Devary, OV, Näär, AMKim, SY, Boutin, JM, Glass, CK & Rosenfeld, MG (1991) RXRβ: a coregulator that enhances binding of retinoic acid, thyroid hormone, and vitamin D receptors to their cognate response elements. Cell 67, 1251–1266.CrossRefGoogle Scholar
Zambonino, Infante JL & Cahu, CL (1999) High dietary lipids levels enhance digestive tract maturation and improve Dicentrarchus labrax larval development. J Nutr 129, 1195–1200.CrossRefGoogle Scholar
Zambonino, Infante JL, Cahu, CL & Péres, A (1997) Partial substitution of di- and tripeptides for native protein in sea bass diet improves Dicentrarchus labrax larval development. J Nutr 127, 604–614.Google Scholar
Zizola, CF, Balaña, ME, Sandoval, M & Calvo, JC (2002) Changes in IGF-I receptor and IGF-I mRNA during differentiation of 3T3-L1 preadipocytes. Biochimie 84, 975–980.CrossRefGoogle ScholarPubMed