Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-15T05:19:03.407Z Has data issue: false hasContentIssue false
  • English
  • Français

Regulation of the somatotropic axis by dietary factors in rainbow trout (Oncorhynchus mykiss)

Published online by Cambridge University Press:  08 March 2007

Pedro Gómez-Requeni ,
Josep Calduch-Giner ,
Silvia Vega-Rubín de Celis ,
Françoise Médale ,
Sadasivam J. Kaushik  and
Jaume Pérez-Sánchez
Pedro Gómez-Requeni
Affiliation:
Instituto de Acuicultura de Torre de la Sal (CSIC), 12 595 Ribera de Cabanes, Castellón, Spain
Josep Calduch-Giner
Affiliation:
Instituto de Acuicultura de Torre de la Sal (CSIC), 12 595 Ribera de Cabanes, Castellón, Spain
Silvia Vega-Rubín de Celis
Affiliation:
Instituto de Acuicultura de Torre de la Sal (CSIC), 12 595 Ribera de Cabanes, Castellón, Spain
Françoise Médale
Affiliation:
Laboratoire de Nutrition des Poissons, Unité Mixte INRA-IFREMER, 64 310 Saint-Pée-sur-Nivelle, France
Sadasivam J. Kaushik
Affiliation:
Laboratoire de Nutrition des Poissons, Unité Mixte INRA-IFREMER, 64 310 Saint-Pée-sur-Nivelle, France
Jaume Pérez-Sánchez*
Affiliation:
Laboratoire de Nutrition des Poissons, Unité Mixte INRA-IFREMER, 64 310 Saint-Pée-sur-Nivelle, France
*
*Corresponding author: Dr Jaume Pérez-Sánchez, fax +34 964319509, email [email protected]
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 activity of the somatotropic axis was analysed in juvenile rainbow trout (Oncorhynchus mykiss) fed either a fishmeal-based diet (FM) or graded levels of plant proteins to replace 50 % (PP50 diet), 75 % (PP75 diet) or 100 % (PP100 diet) of the fishmeal protein. For this purpose, partial cloning and sequencing of the gene encoding rainbow trout growth hormone receptor (GHR) was first accomplished by RT-PCR, using degenerate primers based on the sequences of non-salmonid fish GHR. Growth rates and energy retention were lowered by the PP75 and PP100 diets and a concurrent and progressive increase in plasma levels of growth hormone (GH) was found. However, no changes in hepatic GH binding and total plasma insulin-like growth factor (IGF)-I levels were observed among the four experimental groups. This fact agrees with the lack of changes in hepatic measurements of GHR and IGF-I transcripts. No consistent changes in IGF transcripts were found in peri-visceral adipose tissue and skeletal muscle, but GHR mRNA was up-regulated in the peri-visceral adipose tissue of fish fed the PP75 and PP100 diets, which would favour the lipolytic action of GH. Two specific bands (47 and 33 kDa) of IGF-binding proteins were found in the plasma of all analysed fish, but the sum of the two integrated areas increased progressively with plant protein supply, which might reflect a reduced free IGF availability. Therefore, in our experimental model, the growth impairment could be due, at least in part, to a lowered availability of biologically active IGF (free IGF fraction) rather than to liver GH desensitization or defect in IGF synthesis and release at the systemic and/or paracrine–autocrine level.

Keywords

Rainbow troutPlant proteinsGrowth hormoneGrowth hormone receptorInsulin-like growth factor
Type
Research Article
Information
British Journal of Nutrition , Volume 94 , Issue 3 , September 2005 , pp. 353 - 361
Copyright
Copyright © The Nutrition Society 2005

References

Association of Official Analytical Chemist, (1990) Official Methods of Analysis, 684 [Heldrich, K, editor]. Arlington, VA: AOAC.Google Scholar
Behncken, SN & Waters, MJ (1999) Molecular recognition events involved in the activation of the growth hormone receptor by growth hormone. J Mol Recognit 12, 355–362.Google Scholar
Björnsson, BT (1997) The biology of salmon growth hormone: from daylight to dominance. Fish Physiol Biochem 17, 9–24.Google Scholar
Björnsson, BT, Johansson, V, Benedet, S, Einarsdottir, IE, Hldahj, J, Ágústsson, T & Jönsson, E (2002) Growth hormone endocrinology of salmonids: regulatory mechanisms and mode of action. Fish Physiol Biochem 27 227–242 Special Issue ‘Fish Growth and Metabolism. Experimental, Nutritional and Hormonal Regulation’ [ Plisetskaya, EM, editor] (published in 2004)CrossRefGoogle Scholar
Bolin, DW, King, RP & Klosterman, EW (1952) A simplified method for the determination of chromic oxide (Cr 2 O 3 ) when used as an index substance. Science 116, 634–635.CrossRefGoogle Scholar
Bunn, RC & Fowlkes, JL (2003) Insulin-like growth factor binding protein proteolysis. Trends Endocrinol Metab 14, 176–181.Google Scholar
Calduch-Giner, JA, Duval, H, Chesnel, F, Boeuf, G, Pérez-Sánchez, J & Boujard, D (2001) Fish growth hormone receptor: molecular characterization of two membrane-anchored forms. Endocrinology 142, 3269–3273.Google Scholar
Calduch-Giner, JA, Mingarro, M, Vega-Rubí, n, de Celis, S, Boujard, D & Pérez-Sánchez, J (2003) Molecular cloning and characterization of gilthead sea bream ( Sparus aurata ) growth hormone receptor (GHR). Assessment of alternative splicing. Comp Biochem Physiol 136B 1–13.Google ScholarPubMed
Chen, TT, Shamblott, M, Lin, CM, Tang, Y-L, Chan, K-M, Cheng, CL, Yang, B-Y & Marsh, A (1994) Structure and evolution of growth hormone and insulin like growth factor genes. In Perspectives in Comparative Endocrinology, pp.352–364 [Davey, KG, Peter, RE, Tobe, SS, editor] Ottawa, Ont.: National Research Council of Canada.Google Scholar
Cheng, R, Chang, KM & Wu, JL (2002) Different temporal expressions of tilapia ( Oreochromis mossambicus ) insulin-like growth factor-I and IGF binding protein-3 after growth hormone induction. Mar Biotechnol 4, 218–225.Google Scholar
Chomczynski, P & Sacchi, N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction. Anal Biochem 162, 156–159.Google Scholar
Choubert, G, De la Noue, J & Luquet, P (1982) Digestibility in fish: improved device for the automatic collection of feces. Aquaculture 29, 185–189.Google Scholar
Combes, S, Louveau, I & Bonneau, M (1997) Moderate feed restriction affects skeletal muscle and liver growth hormone receptors differently in pigs. J Nutr 127, 1944–1949.Google Scholar
Company, R, Astola, A, Pendón, C, Valdivia, MM & Pérez-Sánchez, J (2001) Somatotropic regulation of fish growth and adiposity: growth hormone (GH) and somatolactin (SL) relationship. Comp Biochem Physiol 130B, 435–445.Google Scholar
Duan, C, Ding, J, Li, Q, Tsai, W & Pozios, K, (1999) Insulin-like growth factor binding protein 2 is a growth inhibitory protein conserved in zebrafish. Proc Natl Acad Sci USA 96, 15274–15279.Google Scholar
Firth, SM & Baxter, RC (2002) Cellular actions of the insulin-like growth factor binding proteins. Endocr Rev 23, 824–854.CrossRefGoogle ScholarPubMed
Fukada, H, Ozaki, Y, Pierce, AL, Adachi, S, Yamauchi, K, Hara, A, Swanson, P & Dickhoff, WW (2004) Salmon growth hormone receptor: molecular cloning, ligand specificity, and response to fasting. Gen Comp Endocrinol 139, 61–71.Google Scholar
Funkenstein, B, Tsai, W, Maures, T & Duan, C (2002) Ontogeny, tissue distribution, and hormonal regulation of insulin-like growth factor binding protein-2 (IGFBP-2) in a marine fish, Sparus aurata. Gen Comp Endocrinol 128, 112–122.CrossRefGoogle Scholar
Gómez-Requeni, P, Mingarro, M & Kirchner, S (2003) Effects of dietary amino acid profile on growth performance, key metabolic enzymes and somatotropic axis responsiveness of gilthead sea bream ( Sparus aurata ). Aquaculture 220, 749–767.Google Scholar
Gómez-Requeni, P, Mingarro, M, Calduch-Giner, JA, Médale, F, Martin, SAM, Houlihan, DF, Kaushik, SPérez-Sánchez, J (2004) Protein growth performance, amino acid utilisation and somatotropic axis responsiveness to fish meal replacement by plant protein sources in gilthead sea bream ( Sparus aurata ). Aquaculture 232, 493–510.CrossRefGoogle Scholar
Johnsson, JI, Jönsson, E & Björnsson, BT (1996) Dominance, nutritional state, and growth hormone levels in rainbow trout ( Oncorhynchus mykiss ). Horm Behav 30, 13–21.CrossRefGoogle ScholarPubMed
Kelley, KM, Siharath, K & Bern, HA (1992) Identification of insulin-like growth factor-binding protein in the circulation of four teleost fish species. J Exp Zool 263, 220–224.Google Scholar
Kelley, KM, Haigwood, JT, & Perez, M & Galima, MM (2001) Serum insulin-like growth factor binding proteins (IGFBPs) as markers for anabolic/catabolic condition in fishes. Comp Biochem Physiol 129B, 229–236.Google Scholar
Kelley, KM, Schmidt, KE, Berg, L, Sak, K, Galima, MM, Gillespie, C, Balogh, L, Hawayek, A, Reyes, JA & Jamison, M (2002) Comparative endocrinology of the insulin-like growth factor-binding protein. J Endocrinol 175, 3–18.CrossRefGoogle ScholarPubMed
Kumar, S, Tamura, K. Jakobsen, IB & Nei, M (2001) MEGA2: Molecular Evolutionary Genetics Analysis software. Bio informatics 17, 1244–1245.Google ScholarPubMed
Lee, LT, Nong, G, Chan, YH, Tse, DL & Cheng, CH (2001) Molecular cloning of a teleost growth hormone receptor and its functional interaction with human growth hormone. Gene 270, 121–129.Google Scholar
Livak, KJ & Schmittgen, TD (2001) Analysis of real time gene expression data using real time quantitative PCR and the 2 (T) (Delta–Delta C) method. Methods 25, 402–408.Google Scholar
Maures, TJ & Duan, C (2002) Structure, developmental expression, and physiological regulation of zebrafish IGF binding protein-1. Endocrinology 143, 2722–2731.Google Scholar
Maynard, LA & Loosli, JK (1969) Animal Nutrition, 6th ed. pp.613, New York: McGraw-Hill Book Co. Inc.Google Scholar
National Research Council. (1993) Nutrient Requirements of Fish, pp.124. Washington, DC: National Academy Press.Google Scholar
Niu, D, Le, B & Bail, P-Y (1993) Presence of insulin-like growth factor binding-protein (IGF-BP) in rainbow trout ( Oncorhynchus mykiss ) serum. Exp Zool 265, 627–636.Google Scholar
Park, R, Sheperd, BS, Nishioka, RS, Grau, EG & Bern, HA (2000) Effects of homologous pituitary hormone treatment on serum insulin-like growth factor-binding proteins (IGFBPs) in hypophysectomized tilapia, Oreochromis mossambicus, with special reference to a novel 20-kDa IGFBP. Gen Comp Endocrinol 117, 404–412.CrossRefGoogle ScholarPubMed
Pérez-Sánchez, J (2000) The involvement of growth hormone in growth regulation, energy homeostasis and immune function in the gilthead sea bream ( Sparus aurata ): a short review. Fish Physiol Biochem 22, 135–144.Google Scholar
Pérez-Sánchez, J & Le Bail, P-Y (1999) Growth hormone axis as marker of nutritional status and growth performance in fish. Aquaculture 177, 117–128.Google Scholar
Pérez-Sánchez, J, Martí-Palanca, H & Kaushik, S (1995) Ration size and protein intake affect circulating growth hormone concentration, hepatic growth hormone binding and plasma insulin-like growth factor-I immunoreactivity in a marine teleost, the gilthead sea bream ( Sparus aurata ). J Nutr 125, 546–552.Google Scholar
Pérez-Sánchez, J, Calduch-Giner, JA, Mingarro, M, Vega-Rubí, n, de Celis, S, Gómez-Requeni, P, Saera-Vila, A, Astola, A & Valdivia, MM (2002) Overview of fish growth hormone family. New insights in genomic organization and heterogeneity of growth hormone receptors. Fish Physiol Biochem 27, 243 –258 Special Issue ‘Fish Growth and Metabolism. Experimental, Nutritional and HormonalHormonal Regulation’ [Plisetskaya, EM, editor] (published in 2004)Google Scholar
Peterson, BC & Small, BC (2004) Effects of fasting on circulating IGF-binding proteins, glucose, and cortisol in channel catfish ( Ictalurus punctatus ). Domest Anim Endocrinol 26, 231–240.Google Scholar
Pottinger, TG, Rand-Weaver, M & Sumpter, JP (2003) Overwinter fasting and re-feeding in rainbow trout: plasma growth hormone and cortisol levels in relation to energy mobilisation. Comp Biochem Physiol, 136B, 403–417.CrossRefGoogle Scholar
Saera-Vila, A, Calduch-Giner, JA & Pérez-Sánchez, J (2005) Duplication of growth hormone receptor (GHR) in fish genome. Gene organization and transcriptional regulation of GHR type I and Type II in gilthead sea bream ( Sparus aurata ). Gen Comp Endocrinol, 142, 193–203.Google Scholar
Shimizu, M, Swanson, P & Dickhoff, WW (1999) Free and protein-bound insulin-like growth factor-I (IGF-I) and IGF-binding proteins in plasma of coho salmon, Oncorhynchus kisutch. Gen Comp Endocrinol 115, 398–405.Google Scholar
Shimizu, M, Swanson, P, Hara, A & Dickhoff, WW (2003) Purification of a 41 kDa insulin-like growth factor binding protein from serum of Chinook salmon, Oncorhynchus tshawytscha. Gen Comp Endocrinol 132, 103–111.CrossRefGoogle ScholarPubMed
Small, BC, Soares, JH, Woods, LC III & Dahl, GE (2002) Effect of fasting on pituitary growth hormone expression and circulating growth hormone levels in striped bass. North Am J Aquacult 64, 278–283.Google Scholar
Thompson, JD, Higgins, DG & Gibson, TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673–4680.Google Scholar
Tse, DLY, Tse, MCL, Chan, CB, Deng, L, Zhang, WM, Lin, HR & Cheng, CHK (2003) Sea bream growth hormone receptor: molecular cloning and functional studies of the full length cDNA, and tissue expression of two alternatively spliced forms. Biochim Biophys Acta 1265, 64–76.Google Scholar
Tusnády, GE & Simon, I (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics 17, 849–850.CrossRefGoogle ScholarPubMed
Varnavsky, VS, Sakamoto, T & Hirano, T (1995) Effects of premature seawater transfer and fasting on plasma growth hormone levels of yearling coho salmon ( Oncorhynchus kisutch ) parr. Aquaculture 135, 141–145.CrossRefGoogle Scholar
Vega-Rubí, n, de Celis, S, Gómez, P, Calduch-Giner, JA, Médale, F & Pérez-Sánchez, J (2003) Expression and characterization of European sea bass ( Dicentrarchus labrax ) somatolactin: assessment of in vivo metabolic effects. Mar Biotechnol 5, 92–101.Google Scholar
Weber, GM & Grau, EG (1999) Changes in serum concentrations and pituitary content of the two prolactins and growth hormone during the reproductive cycle in female tilapia, Oreochromis mossambicus, compared with changes during fasting. Comp Biochem Physiol 124C, 323–335.Google Scholar
Yao, K, Niu, P-D, Le Gac, F, Le, B & ail, P-Y (1991) Presence of specific growth hormone binding sites in rainbow trout ( Oncorhynchus mykiss ) tissues: characterization of the hepatic receptor. Gen Comp Endocrinol 81, 72–82.Google Scholar
Zhu, T, Goh, ELK, Graichen, R, Ling, L & Lobie, PE (2001) Signal transduction via the growth hormone receptor. Cell Signal 13, 599–616.Google Scholar