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The tilapia prolactin cell: A model for stimulus-secretion coupling

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Abstract

The tilapia prolactin (PRL) cell responds rapidly (10–20 min) to small physiological changes in medium osmotic pressure (OP), releasing increasing quantities of hormone as medium OP is reduced. This release is rapidly (≤ 10 min) inhibited by somatostatin (SRIF). There is now extensive evidence that tilapia PRL cell function is regulated through the second messengers Ca++ and cAMP. Our studies have shown that PRL release is augmented by treatments that lead to increased levels of intracellular Ca++ or cAMP. On the other hand, PRL release is blocked when tissues are incubated in Ca++-depleted medium or upon the addition of Co++, an inhibitor of Ca++-mediated processes. The use of45Ca++ to characterize the movement of Ca++ into PRL cells has provided evidence that an increase in the influx of extracellular Ca++ may participate in PRL release upon exposure to hyposmotic medium. Our studies have also shown that SRIF suppresses the increase in45Ca++ accumulation that is brought about when OP is reduced. We have also examined the effects of OP and SRIF on cAMP levels. The reduction of medium OP did not alter cAMP metabolism during 20 min of incubation. By contrast, cAMP accumulation in the presence of IBMX was enhanced at 1 hr of incubation in reduced OP. Thus, an increase in cAMP turnover may play a role in maintaining PRL release under sustained stimulation. SRIF reduced the accumulation of cAMP during 10 min of incubation with IBMX and also reduced the forskolin-stimulated increase in cAMP. Thus, SRIF may suppress adenylate cyclase activity. Finally, our studies have revealed that the forskolin-stimulated increase in cAMP levels is not dependent upon medium Ca++. The presence of Ca++ in the medium is required, however, for PRL release even when the cAMP messenger system has been activated. Moreover, cAMP accumulation was augmented when intracellular Ca++ was increased. This raises the possibility that reduced OP may stimulate an increase in cAMP turnover indirectly through its action(s) on cytosolic Ca++.

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References cited

  • Berridge, M.J. 1985. The molecular basis of communication within the cell. Sci. Am. 253: 142–152.

    Article  PubMed  CAS  Google Scholar 

  • Bolton, J.P., Collie, N.L., Kawauchi, H. and Hirano, T. 1987. Osmoregulatory actions of growth hormone in rainbow trout (Salmo gairdneri). J. Endocrinol. 112: 63–68.

    Article  PubMed  CAS  Google Scholar 

  • Clarke, W.C. and Bern, H.A. 1980. Comparative endocrinology of prolactin.In Hormonal Proteins and Peptides. Vol. VIII. pp. 105–197. Edited by C.H. Li. Academic Press.

  • Cronin, M.J., Faure, N., Martial, J.A. and Weiner, R.I. 1980. Absence of high affinity dopamine receptors in GH3 cells: A prolactin-secreting clone resistant to the inhibitory action of dopamine. Endocrinology 106: 718–723.

    PubMed  CAS  Google Scholar 

  • Delbeke, D., Scammell, J.G. and Dannies, P.S. 1984. Difference in calcium requirements for forskolin-induced release of prolactin from normal pituitary cells and GH4C1 cells in culture. Endocrinology 114: 1433–1440.

    PubMed  CAS  Google Scholar 

  • Dorflinger, L.J. and Schonbrunn, A. 1983. Somatostatin inhibits vasoactive intestinal peptide-stimulated cyclic adenosine monophosphate accumulation in GH pituitary cells. Endocrinology 113: 1541–1550.

    Article  PubMed  CAS  Google Scholar 

  • Dufy, B. and Barker, J. 1984. Peptide hormone regulate ionic conductances in clonal pituitary cells. Abst. 66th Annual Meeting of the Endocrine Society, Quebec City, Quebec, Canada.

  • Gautvik, K.M. and Kriz, M. 1976. Measurements of prolactin and growth hormone synthesis and secretion by rat pituitary cells in culture. Endocrinology 98: 344–351.

    PubMed  CAS  Google Scholar 

  • Grau, E.G., Nishioka, R.S. and Bern, H.A. 1981. Effects of osmotic pressure and calcium ion on prolactin releasein vitro from the rostral pars distalis of the tilapia,Sarotherodon mossambicus. Gen. Comp. Endocrinol. 45: 406–408.

    Article  PubMed  CAS  Google Scholar 

  • Grau, E.G., Nishioka, R.S. and Bern, H.A. 1982. Effects of somatostatin and urotensin II on tilapia pituitary prolactin release and interactions between somatostatin, osmotic pressure, Ca2+, and adenosine 3′, 5′-monophosphate in prolactin releasein vitro. Endocrinology 110: 910–915.

    PubMed  CAS  Google Scholar 

  • Grau, E.G., Nishioka, R.S., Young, G. and Bern, H.A. 1985. Somatostatin-like immunoreactivity in the brain and pituitary of three teleost fish species. Gen. Comp. Endocrinol. 59: 350–357.

    Article  PubMed  CAS  Google Scholar 

  • Grau, E.G., Shimoda, S.K., Ford, C.A., Helms, L.M.H., Cooke, I.M. and Pang, P.K.T. 1986. The role of calcium in prolactin release from the pituitary of a teleost fishin vitro. Endocrinology 119: 2848–2855.

    PubMed  CAS  Google Scholar 

  • Grau, E.G., Ford, C.A., Helms, L.M.H., Shimoda, S.K. and Cooke, I.M. 1987. Somatostatin and altered medium osmotic pressure elicit rapid changes in prolactin release from the rostral pars distalis of the tilapia,Oreochromis mossambicus in vitro. Gen. Comp. Endocrinol. 65: 12–18.

    Article  PubMed  CAS  Google Scholar 

  • Helms, L.M.H., Grau, E.G., Shimoda, S.K., Nishioka, R.S. and Bern, H.A. 1987. Studies on the regulation of growth hormone release from the proximal pars distalis of the tilapia,Oreochromis mossambicus, in vitro. Gen. Comp. Endocrinol. 65: 48–55.

    Article  PubMed  CAS  Google Scholar 

  • Helms, L.M.H., Grau, E.G. and Shimoda, S.K. 1987. A role for cAMP in the regulation of prolactin release from the pituitary of the tilapia,Oreochromis mossambicus. Am. Zool. 27: 74a.

  • Helms, L.M.H. 1988. The role of the cAMP and Ca++ messenger systems in regulating prolactin release from the pituitary gland of the tilapia,Oreochromis mossambicus. Ph.D. Thesis. University of Hawaii, U.S.A.

  • Holmes, R.L. and Ball, J.N. 1974. The Pituitary Gland: A Comparative Account. Cambridge University Press, London.

    Google Scholar 

  • Koch, B.D., Dorflinger, L.J. and Schonbrunn, A. 1985. Pertussis toxin blocks both cyclic AMP-mediated and cyclic AMP-independent actions of somatostatin. J. Biol. Chem. 260: 13138–13145.

    PubMed  CAS  Google Scholar 

  • Leng, G., Mason, W.T. and Dyer, R.G. 1982. The supraoptic nucleus as an osmoreceptor. Neuroendocrinology 34: 75–82.

    PubMed  CAS  Google Scholar 

  • Levitzki, A. 1986. B-Adrenergic receptors and their mode of coupling to adenylate cyclase. Physiol. Rev. 66: 819–854.

    PubMed  CAS  Google Scholar 

  • Maruyama, T., Shiino, M. and Rennels, E.G. 1981. Calcium-dependent changes in electrical properties of prolactin-secreting anterior pituitary (2B8) clonal cells. Neuroendocrinology 32: 28–32.

    PubMed  CAS  Google Scholar 

  • Nagahama, Y., Nishioka, R.S., Bern, H.A. and Gunther, R.L. 1975. Control of prolactin secretion in teleosts, with special reference toGillichthys mirabilis andTilapia mossambica. Gen. Comp. Endocrinol. 25: 166–188.

    Article  PubMed  CAS  Google Scholar 

  • Olivereau, M., Ollevier, F., Vandesnade, F. and Olivereau, J. 1984. Somatostatin in the brain and the pituitary of some teleosts: Immunocytochemical identification and the effect of starvation. Cell Tiss. Res. 238: 289–296.

    Article  CAS  Google Scholar 

  • Ozawa, R. and Kimura, N. 1979. Membrane potential changes caused by thyrotropin-releasing hormone in the clonal GH3 cell and their relationship to secretion of pituitary hormone. Proc. Nat. Acad. Sci. U.S.A. 76: 6017–6020.

    Article  CAS  Google Scholar 

  • Rawls, R.L. 1987. G-proteins. Chem. Eng. News 65: 26–39.

    Google Scholar 

  • Rasmussen, H. and Barret, P.Q. 1984. Calcium messenger system: an integrated view. Physiol. Rev. 64: 938–984.

    PubMed  CAS  Google Scholar 

  • Rasmussen, H., Kojima, I., Kojima, K., Zawalich, W. and Apfeldorf, W. 1984. Calcium as intracellular messenger: sensitivity modulation, C-kinase pathway and sustained cellular response. Adv. Cyclic Nucleotide Res. 18: 159–193.

    CAS  Google Scholar 

  • Richman, N.H., Ford, C.A., Grau, E.G. and Cooke, I.M. 1986. The effects of osmotic pressure and high [K+] on prolactin (PRL) release and CA2+ efflux from tilapia rostral pars distalis (RPD) in perifusion culture. Am. Zool. 26: 110a.

  • Richman, N.H., Ford, C., Helms, L.M.H., Grau, E.G., Pang, P.K.T. and Cooke, I.M. 1987. Effect of osmotic pressure and depolarizing [K+] on calcium uptake by the rostral pars distalis (RPD) from the tilapia,Oreochromis mossambicus. Am. Zool. 27: 96a.

  • Richman, N.H. and Zaugg, W.S. 1987a. Effects of cortisol and growth hormone on osmoregulation in pre- and desmoltified coho salmon (Oncorhynchus kisutch) Gen. Comp. Endocrinol. 65: 189–198.

    Article  PubMed  CAS  Google Scholar 

  • Richman, N.H., Nishioka, R.S., Young, G. and Bern, H.A. 1987b. Effects of cortisol and growth hormone replacement on osmoregulation in hypophysectomized coho salmon (Oncorhynchus kisutch). Gen. Comp. Endocrinol. 67: 194–201.

    Article  PubMed  CAS  Google Scholar 

  • Ronning, S.A., Heatly, G.A. and Martin, T.F.J. 1982. Thyrotropin-releasing hormone mobilizes Ca2+ from endoplasmic reticulum and mitochondria of GH3 pituitary cells: Characterization of cellular Ca2+ pools by a method based on digitonin permeabilization. Proc. Nat. Acad. Sci. U.S.A. 79: 6294–6298.

    Article  CAS  Google Scholar 

  • Rubin, R.P. 1982. Calcium and Cellular Secretion. Plenum Press, New York.

    Google Scholar 

  • Schlegel, W., Wuarin, F., Wollheim, C.B. and Zahnd, G.R. 1984. Somatostatin lowers the cytosolic free Ca2+ concentration in clonal rat pituitary cells (GH3 cells). Cell Calcium 5: 223–236.

    Article  PubMed  CAS  Google Scholar 

  • Taraskevich, P.S. and Douglas, W.W. 1978. Catecholamines of supposed inhibitory hypophysiotropic function suppress action potentials in prolactin cells. Nature, Lond. 276: 832–834.

    Article  CAS  Google Scholar 

  • Tashjian, A.H., Bancroft, F.C. and Levine, L. 1970. Production of both prolactin and growth hormone by clonal strains of rat pituitary tumor cells: Differential effects of hydrocortisone and tissue extracts. J. Cell Biol. 47: 61–70.

    Article  PubMed  CAS  Google Scholar 

  • Yamashita, N., Shibuya, N. and Ogata, E. 1986. Hyperpolarization of the membrane potential caused by somatostatin in dissociated human pituitary adenoma cells that secrete growth hormone. Proc. Nat. Acad. Sci. U.S.A. 83: 6198–6202.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Zoology and Hawaii Institute of Marine Biology, University of Hawaii, Honolulu, HI, 96822, U.S.A.

    E. Gordon Grau & Lisa M. H. Helms

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  1. E. Gordon Grau
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  2. Lisa M. H. Helms
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Grau, E.G., Helms, L.M.H. The tilapia prolactin cell: A model for stimulus-secretion coupling. Fish Physiol Biochem 7, 11–19 (1989). https://doi.org/10.1007/BF00004685

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