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Pituitary Gland in Vitro: Evects of Somatostatin-14, Insulin-Like Growth Factor-I, and Nutritional Status

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Pituitary Gland in Vitro: Evects of Somatostatin-14, Insulin-Like Growth Factor-I, and Nutritional Status General and Comparative Endocrinology 141 (2005) 93–100 www.elsevier.com/locate/ygcen Growth hormone secretion from the Arctic charr (Salvelinus alpinus) pituitary gland in vitro: eVects of somatostatin-14, insulin-like growth factor-I, and nutritional status C. Camerona,¤, R.D. Mocciab, J.F. Leatherlanda a Department of Biomedical Sciences, University of Guelph, Guelph, Ont., Canada N1G 2W1 b Department of Animal and Poultry Science, University of Guelph, Guelph, Ont., Canada N1G 2W1 Received 27 February 2004; revised 3 November 2004; accepted 29 November 2004 Available online 8 January 2005 Abstract This study investigated the inXuence of nutritional status on the growth hormone (GH)/insulin-like growth factor-I (IGF-I) axis in Arctic charr (Salvelinus alpinus). The objectives were to study the regulation of GH secretion in vitro by somatostatin-14 (SRIF) and hIGF-I, and to determine whether pituitary sensitivity to these factors is dependent upon nutritional status. Arctic charr were fed at three diVerent ration levels (0, 0.35, and 0.70% BW d¡1), and pituitary glands were harvested at 1, 2, and 5 weeks for in vitro study. Both SRIF and hIGF-I inhibited GH secretion from Arctic charr pituitary tissue in long-term (18 h) static hemipituitary cul- ture, as well as after acute exposure in a pituitary fragment perifusion system. This response appeared to be dose-dependent for SRIF in static culture over the range of 0.01–1 nM, but not for hIGF-I. The acute inhibitory action of hIGF-I on GH release in the perifusion system suggests an action that is initially independent of any eVects on GH gene expression or protein synthesis. Nutri- tional status did not aVect the sensitivity of Arctic charr pituitary tissue to either SRIF or hIGF-I in vitro, indicating that changes in abundance of pituitary SRIF or IGF-I receptors may not explain the alterations in plasma GH levels found during dietary restriction. 2004 Elsevier Inc. All rights reserved. Keywords: Growth hormone; Insulin-like growth factor-I; Ration level; Pituitary hormone secretion; Somatostatin; Arctic charr 1. Introduction peptide has been conWrmed in several teleost species (Holloway et al., 1997; Lin and Peter, 2001). Insulin-like The regulation of growth hormone (GH) secretion in growth factor-I (IGF-I), the mediator of many of the Wshes is multifactorial, with inputs from both neuroen- actions of GH, is another inhibitor of GH secretion, pro- docrine and circulating sources. Several members of the viding negative feedback on pituitary GH secretion in somatostatin family of peptides have been identiWed as many vertebrate species. This function has also been inhibitors of GH secretion, and this function, as well as conWrmed in several Wsh species (Blaise et al., 1995; peptide structure, has been highly conserved across the Fruchtman et al., 2000, 2002; Huang et al., 1997; Pérez- vertebrates (Lin et al., 1998). Somatostatin-14 (SRIF) Sánchez et al., 1992; Rousseau et al., 1997). has been conserved with identical primary structure in It is unclear from the studies in Wshes whether the all vertebrates, and the inhibition of GH release by this inhibition of GH secretion by IGF-I in vitro is a result of an instantaneous change in the rate of hormone secre- * Corresponding author. Fax: +1 613 562 5486. tion, changes in GH gene expression, or a combination E-mail address: [email protected] (C. Cameron). of these possibilities. Striped bass hybrid (Morone 0016-6480/$ - see front matter 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.ygcen.2004.11.019 94 C. Cameron et al. / General and Comparative Endocrinology 141 (2005) 93–100 saxatilis £ M. chrysops) somatotroph GH content and does not appear to be as potent in salmonid Wshes (Hol- protein synthesis are reduced after 18–20 h of exposure loway and Leatherland, 1998). of to IGF-I (Fruchtman et al., 2000), and tilapia (Ore- The purpose of the present study was to investigate ochromis mossambicus) pituitary glands treated with the eVects of SRIF and IGF-I on GH secretion from IGF-I for 24 h have reduced levels of GH mRNA, Arctic charr pituitary glands in vitro, and to determine if although GH secretion does not diVer signiWcantly after nutritional status has an inXuence on pituitary sensitiv- 4h (Kajimura et al., 2002). Conversely, injection of IGF- ity to these factors. Static hemipituitary gland culture I into catheterized rainbow trout (Oncorhynchus mykiss) was used to study changes in GH secretion after long- resulted in rapid (<60 min) reductions in plasma GH term exposure to peptides, whereas pituitary gland peri- concentrations (Blaise et al., 1995). In rat pituitary cells, fusion was used for acute exposures. IGF-I inhibits GH secretion and reduces levels of GH mRNA expression by somatotrophs in vitro (Niiori- Onishi et al., 1999; Yamashita and Melmed, 1986). In 2. Materials and methods addition, IGF-I may also act at the hypothalamic level, to stimulate the release of SRIF (Berelowitz et al., 1981), 2.1. Animals increase SRIF mRNA synthesis, and decrease GH releasing-hormone (GHRH) mRNA synthesis (Sato and All experimental protocols used in this study were Frohman, 1993). There are many potential sites of action approved by the University of Guelph Animal Care of IGF-I on pituitary GH secretion, and it is unclear Committee. Arctic charr (Salvelinus alpinus) of the Lab- from the previous studies in Wshes at which level(s) this rador strain were obtained from the Alma Aquaculture may be occurring. Research Station (Alma, Ont.). Fish had been main- The changes in the GH/IGF-I axis following dietary tained outdoors in 10 m circular tanks, with a water restriction have been described in mammals (Straus, temperature of 8.5 °C, and were fed a standard commer- 1994), and there is evidence to suggest a similar control cial diet (Martin Mills, Elmira, Ont.) using demand in Wshes (Duan, 1998). In several Wsh species, the reduc- feeders. tion in growth following dietary restriction is character- ized by elevated plasma GH concentrations (Duan and 2.2. Experimental design Plisetskaya, 1993; Farbridge and Leatherland, 1992; Fukada et al., 2004; Sumpter et al., 1991), a decreased Approximately 900 male and female Arctic charr level of hepatic IGF-I mRNA (Duan and Plisetskaya, (average weight D 397.9 g) were randomly distributed 1993), and a reduced plasma IGF-I concentration among nine 2 m tanks with a target initial stocking den- (Pérez-Sánchez et al., 1994a,b). It has been demon- sity of 40 kg m¡3. The tanks were located indoors under strated that hepatic GH-binding and GH-receptor a natural photoperiod. Water Xow rates were adjusted mRNA expression is reduced during dietary restriction to 30 L min¡1; water temperature was 8.5 °C; dissolved in Wshes (Fukada et al., 2004; Gray et al., 1992; Pérez- oxygen was monitored regularly and remained within Sánchez et al., 1994a). It is generally accepted that the normal limits for the duration of the study (8.5– reduction in negative feedback by circulating IGF-I 10 mg L¡1). contributes to increases in GH secretion and plasma After three days, the Wsh in all tanks were fed the GH. same commercial diet at 0.70% BWd¡1 via automatic There is evidence in Wshes that pituitary sensitivity to belt feeders. This was maintained for a period of 12 the factors that regulate the synthesis and secretion of weeks during which growth and feed conversion GH are inXuenced by reproductive and hormonal status eYciency were monitored. At the beginning of the study (Cardenas et al., 2003; Holloway and Leatherland, 1998; (March 11 2002) the tanks were randomly assigned to Peng and Peter, 1997). However, there is currently little one of three ration groups (0, 0.35, or 0.70% BWd¡1; 3 information on the eVects of changes in nutritional sta- tanks/ration level). The 0.70% BW d¡1 ration was tus on pituitary sensitivity to various GH secretagogues. selected as a full ration as the apparent feed conversion The changes in plasma GH concentrations related to eYciencies observed during the 12 week acclimation nutritional status could be explained by altered pituitary period indicated that a portion of this ration remained sensitivity to factors that inhibit GH secretion, such as uneaten in some tanks (data not shown). The experimen- SRIF or IGF-I. Pituitary sensitivity to these factors tal ration levels were maintained for a period of Wve depends on the abundance of SRIF or IGF-I receptors, weeks. and changes in the abundance of these receptors has A sample of 12 Wsh was taken from each tank after 1, been observed in relation to nutritional and hormonal 2, and 5 weeks. Fish were removed from the tanks in the status of Wsh (Pesek and Sheridan, 1996; Planas et al., morning prior to feeding (8:30–10:30) and euthanized 2000). Sensitivity to hypothalamic factors that stimulate with MS-222 (>125 mgL¡1). Pituitary glands were GH secretion may also be important, however, GHRH removed from each Wsh and placed in ice-cold 80% C. Cameron et al. / General and Comparative Endocrinology 141 (2005) 93–100 95 HBSS (Gibco-BRL, Canadian Life Technologies, Bur- 2.5. Assays lington, Ont.; with 4.17 mM NaHCO3, 0.1% BSA, pH 7.5, diluted to 80%). For measurement of GH secreted in vitro, a non-com- petitive enzyme-linked immunosorbent assay (ELISA) 2.3. Static hemipituitary gland culture developed for oncorhynchid species (Farbridge and Lea- therland, 1991), modiWed by Holloway and Leatherland Pituitary glands were dissected along the sagittal axis (1997), and validated for use in Arctic charr (Cameron et into two equal parts. The hemipituitaries were then al., 2002), was used.
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