Enhancement by Proopiomelanocortin-Derived Peptides of Growth Hormone and Prolactin Secretion by Bullfrog Pituitary Cells

doi:10.1006/gcen.1999.7289

General and Comparative Endocrinology

Volume 115, Issue 1, July 1999, Pages 101-109

https://doi.org/10.1006/gcen.1999.7289 Get rights and content

Abstract

Corticotrophs in the bullfrog (Rana catesbeiana) are situated mainly in the rostral region of the anterior lobe of the pituitary gland, which receives its blood supply primarily from the portal vessel. On the assumption that the proopiomelanocortin (POMC)-derived peptides released into the pituitary circulation may influence the function of other pituitary cells situated downstream, the effects of three POMC-derived peptides, namely, N-terminal peptide of POMC (NPP), adrenocorticotropic hormone (ACTH), and joining peptide (JP), on the secretion of growth hormone (GH) and prolactin (PRL) by bullfrog dispersed anterior pituitary cells were examined. NPP and ACTH, but not JP, stimulated the release of GH and PRL in a concentration-dependent manner. It was also found that ACTH_1–17, but not α-melanocyte-stimulating hormone, was effective in enhancing GH and PRL release. A marked difference between the response to NPP and ACTH and the response to thyrotropin-releasing hormone employed as a reference secretagogue in terms of the time required for stimulating the release of GH and PRL was noted. Northern blot analysis of GH and PRL mRNA levels and radioimmunoassay for GH and PRL in the cultured cells revealed that ACTH increases the syntheses of both pituitary hormones as well. The possibility that NPP and ACTH act on neighboring cells to maintain their overall secretory function is discussed.

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It was also demonstrated that both fNPP and fACTH, but not α-MSH, enhanced the release of PRL and GH from the bullfrog anterior pituitary cells in vitro. In this respect, fACTH1–17 (identical with human ACTH1–17) was as effective as authentic fACTH1–39 (Aida et al., 1999b). Thus, corticotropes were considered to play a role in maintaining the secretory function of some neighboring cells in addition to stimulating the adrenal cortex.
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In addition, the major factor from the bullfrog hypothalamus that exhibits PRL-releasing activity has been characterized as TRH (Nakajima et al., 1993), These observations indicate that TRH is likely a physiological regulator of pituitary lactotrope cells. TRH also stimulates GH secretion from the pituitary of R. catesbeiana (Hall and Chadwick, 1984; Aida et al., 1999; Yamamoto et al., 2000), R. perezi (Pelophylax perezi) (Gracia-Navarro et al., 1991; Castaño et al., 1993), R. pipiens (Hall and Chadwick, 1984) and X. laevis (Hall and Chadwick, 1984). Finally, TRH is a very potent stimulator of α-melanocyte-stimulating hormone (α-MSH) secretion from melanotrope cells in R. ridibunda (Vaudry et al., 1977; Tonon et al., 1980, 1983; Leroux et al., 1982, 1983; Adjeroud et al., 1986; Lamacz et al., 1987, 1988; Louiset et al., 1989; Gonzalez de Aguilar et al., 1997; Galas et al., 1998, 1999), R. pipiens (Kraicer, 1977) and X. laevis (Verburg-van Kemenade et al., 1987; Dotman et al., 1997).
Thyrotropin-releasing hormone (TRH) is the first hypothalamic hypophysiotropic neuropeptide whose sequence has been chemically characterized. The primary structure of TRH (pGlu-His-Pro-NH₂) has been fully conserved across the vertebrate phylum. TRH is generated from a large precursor protein that contains multiple repeats of the TRH progenitor tetrapeptide Gln-His-Pro-Gly. In all tetrapods, TRH-expressing neurons located in the hypothalamus project towards the external zone of the median eminence while in teleosts they directly innervate the pars distalis of the pituitary. In addition, in frogs and teleosts, a bundle of TRH-containing fibers terminate in the neurointermediate lobe of the pituitary gland. Although TRH was originally named for its ability to trigger the release of thyroid-stimulating hormone (TSH) in mammals, it later became apparent that it exerts multiple, species-dependent hypophysiotropic activities. Thus, in fish TRH stimulates growth hormone (GH) and prolactin (PRL) release but does not affect TSH secretion. In amphibians, TRH is a marginal stimulator of TSH release in adult frogs, not in tadpoles, and a major releasing factor for GH and PRL. In birds, TRH triggers TSH and GH secretion. In mammals, TRH stimulates TSH, GH and PRL release. In fish and amphibians, TRH is also a very potent stimulator of α-melanocyte-stimulating hormone release. Because the intermediate lobe of the pituitary of amphibians is composed by a single type of hormone-producing cells, the melanotrope cells, it is a suitable model in which to investigate the mechanism of action of TRH at the cellular and molecular level. The occurrence of large amounts of TRH in the frog skin and high concentrations of TRH in frog plasma suggests that, in amphibians, skin-derived TRH may exert hypophysiotropic functions.
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The possible effect of proopiomelanocortin-derived peptide, β-endorphin on frog gonadotrope cells was investigated. Binding and internalization of β-endorphin to pituitary pars distalis cultured cells were visualized by immunofluorescence and analyzed by means of confocal laser scanning microscopy. Using biotinylated endorphin, the time-course of β-binding showed that this opioid was internalized through receptor-mediated endocytosis, the mechanism in which actin and clathrin were involved; then, the lysosomal degradation program occurred at later stages. The β-endorphin binding was well antagonized by Naloxone, the opiate receptor antagonist, and up-regulated since more rapid response was obtained in the previously primed cells. The double immunostaining reaction for β-endorphin and LH β-subunit revealed that half the β-endorphin labeled cell population was positively immunostained for LH β-subunit, and β-endorphin was able to induce an increasing trend of LH secretion in cultured pars distalis cells. Therefore, it seems that β-endorphin acts directly on pituitary pars distalis and influences gonadotropin secretion through the interaction with its own receptor.
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These results indicate that the regulatory mechanism governing GH secretion by GHRH exists in the frog. In addition, thyrotropin-releasing hormone (27), proopiomelanocortin-derived peptides (27), pituitary adenylate cyclase-activating polypeptide (34), and endothelin (35) are involved in GH release in the frog. These facts indicate that the stimulation of GH secretion in frog is governed by a complicated hypothalamic hormonal regulation.
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Regular ArticleEnhancement by Proopiomelanocortin-Derived Peptides of Growth Hormone and Prolactin Secretion by Bullfrog Pituitary Cells

Abstract

J. Biol. Chem.

Comp. Biochem. Physiol. C

Biochem. Biophys. Res. Commun.

Peptides

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

J. Biol. Chem.

Life Sci.

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

FEBS Lett.

J. Biol. Chem.

Gen. Comp. Endocrinol.

Cloning of a bullfrog proopiomelanocortin cDNA

Zool. Sci.

Stimulation by proopiomelanocortin-derived peptides of LH release by bullfrog dispersed anterior pituitary cells

Zool. Sci.

Effects of proopiomelanocortin (POMC)-derived peptides on pituitary function in the bullfrog, Rana catesbeiana

Proc. 3rd International Symp. Asia Oceania Soc. Comp. Endocrinol.

Complete structure of the porcine proopiomelanocortin mRNA derived from the nucleotide sequence of cloned cDNA

Nucleic Acids Res.

Inhibition of luteinizing hormone release by morphine and endogenous opiates in cultured pituitary cells

Endocrinology

Cell-to-cell communication in peptide target cells of the anterior pituitary

Methods Enzymol.

Regular Article
Enhancement by Proopiomelanocortin-Derived Peptides of Growth Hormone and Prolactin Secretion by Bullfrog Pituitary Cells