Pituitary Growth Hormone Secretion in the Turbot, a Phylogenetically Recent Teleost, Is Regulated by a Species-Specific Pattern of Neuropeptides

Abstract

In mammals, growth hormone (GH) is under a dual hypothalamic control exerted by growth hormone-releasing hormone (GHRH) and somatostatin (SRIH). We investigated GH release in a pleuronectiform teleost, the turbot (Psetta maxima), using a serum-free primary culture of dispersed pituitary cells. Cells released GH for up to 12 days in culture, indicating that turbot somatotropes do not require releasing hormone for their regulation. SRIH dose-dependently inhibited GH release up to a maximal inhibitory effect of 95%. None of the potential stimulators tested induced any change in basal GH release. Also, neither forskolin, an activator of adenylate cyclase, nor phorbol ester (TPA), an activator of protein kinase C, were able to modify GH release, suggesting that spontaneous basal release already represents the maximal secretory capacity of turbot somatotropes. In contrast, forskolin and TPA were able to increase GH release in the presence of SRIH. In this condition (coincubation with SRIH), pituitary adenylate cyclase-activating polypeptide (PACAP) stimulated GH release, whereas none of the other neuropeptides tested (GHRHs; sea bream or salmon or chicken II GnRHs; TRH; CRH) had any significant effect. These data indicate that inhibitory control by SRIH may be the basic control of GH production in teleosts and lower vertebrates, while PACAP may represent the ancestral growth hormone-releasing factor in teleosts, a role taken over in higher vertebrates by GHRH.

Evidence of a reproduction-related function for pituitary adenylate cyclase-activating polypeptide-related peptide in an Anabantidae fish

“…PRP can stimulate GH release from pituitary cells in several teleosts: goldfish (Vaughan et al 1992), rainbow trout (Luo et al 1990), and sockeye salmon (Parker et al 1997), and a synthetic hexapeptide of PRP increased the cell number of rat GH-secreting cells (Goth et al 1992). In contrast, in turbot (Psetta maxima) and zfGHRH-R-transfected CHO cells, PRP did not stimulate GH release (Montero et al 2000, Rousseau et al 2001.…”

Expression and in vitro regulation of pituitary adenylate cyclase-activating polypeptide (pacap38) and its type I receptor (pac1-r) in the gonads of tilapia (Oreochromis mossambicus)

“…Concurrent with the wide range of tissue distribution in mammals, Pacap is considered to be pleiotropic , Wong et al 2000, Small & Nonneman 2001. PACAP 1) effectively stimulates the secretion of GH (Parker et al 1997, Montero et al 1998, Wong et al 1998, 2000, Wirachowsky et al 2000, Rousseau et al 2001 and gonadotropin (Chang et al 2001); 2) it functions in the gut by affecting contractions of the intestine (Matsuda et al 2000, Olsson & Holmgren 2000; 3) it can trigger catecholamine secretion from chromaffin cells (Montpetit & Perry 2000); 4) it controls the differentiation and proliferation of cells during zebrafish ontogeny (Mathieu et al 2004); 5) it is essential for brain development in zebrafish (Sherwood & Wu 2005, Sherwood et al 2007; and 6) it enhances the maturation rate of rat and zebrafish oocytes (Apa et al 1997, Wang et al 2003.…”

Genomic structure, polymorphism and expression analysis of growth hormone-releasing hormone and pituitary adenylate cyclase activating polypeptide genes in the half-smooth tongue sole (Cynoglossus semilaevis)

“…While in fish, initial studies analyzing the potential role of GHRH-like peptide in the control of GH release did not show similar results, either consistent with the previous studies in mammals or failed to demonstrate a major stimulatory action in releasing GH in vitro (Luo and McKeown, 1991;Parker et al, 1997;Rousseau et al, 2001). However, recent identifications showed that authentic GHRH mRNA of goldfish (C. auratus) was detected mostly in the brain, whereas GHRH receptor mRNA was found in both brain and pituitary.…”

“…Evidence indicates that both forms of PACAP are derived from the same gene and mRNA precursor (Arimura and Shioda, 1995). In fish, PACAP is a pleiotropic hormone as an enhancer which potently stimulates the release of GH (Wong et al, 2000;Rousseau et al, 2001), gonadotropin (Wong et al, 2000), prolactin, adrenocorticotrophic hormone (ACTH) and luteinizing hormone (LH) (Fradinger and Sherwood, 2000). The PACAP mRNA precursor also encodes PACAP-related peptide (PRP), which also enhances the growth rates like PACAP as reported in fish (Lugo et al, 2008).…”