Differential effects of gonadotropin-releasing hormone, dopamine and somatostatin and their second messengers on the mRNA levels of gonadotropin IIb subunit and growth hormone in the teleost fish, tilapia
[en] In cultured pituitary cells of tilapia, gonadotropin-releasing hormone (GnRH; 10 nM 4-24 h), elevation of cyclic AMP (by 10 microM forskolin or 0.2 mM 3-isobutyl-1-methylxanthine: IBMX 0.5-36 h) or activation of protein kinase C (PKC; by 12.5 nM tetradecanoyl phorbol-13-acetate: TPA, 0.5-24 h) all increased gonadotropin (GtH) II beta steady state mRNA levels by three to four-fold. The involvement of PKA and PKC in the GnRH stimulatory effect on both GtH release and GtH II beta mRNA levels was corroborated by use of the PKA and PKC inhibitors, H89 and GF109203X, respectively (100 nM) which attenuated the GnRH effect. Incubation with actinomycin D (8 microM, 4-21 h) after preexposure for 24 h to either forskolin (10 microM) or TPA (12.5 nM), revealed that rates of transcript degradation were slower in forskolin-treated cells (T 1/2 = 14.1 h) than in control or TPA-treated cells (T 1/2 = 8.47 or 8.38 h), suggesting a stabilizing effect on the mRNA. Dopamine (DA; 10 microM, 4-36 h) had no apparent effect on steady state mRNA levels of GtH II beta, but reduced GtH release by as much as 75%. Steady state levels of growth hormone (GH) mRNA were not affected by exposure to GnRH (10 nM, 4-24 h), although GH release was more than doubled. Similarly, activation of PKC (by TPA 12.5 nM, 1.5-36 h), which was shown to be essential for the GnRH-stimulatory effect on GH release, did not alter levels of the GH transcript, but increased GH release by more than fivefold. DA (10 microM, 4-24 h) moderately increased GH transcript levels (160%) with similar kinetics but lower potency than direct elevation of cAMP (by 10 microM forskolin or 0.2 mM IBMX, 0.5-36 h) which increased transcript levels by more than fourfold. The involvement of PKA in the DA effect was confirmed when the PKA inhibitor H89 (100 nM, 15 min prior to DA exposure) attenuated the DA effect on GH mRNA levels. Exposure of cells to actinomycin D (8 microM, 2-16 h) after treatment with forskolin (10 microM, 24 h) led to a slower rate of transcript degradation than in control cells (T 1/2 = 6.5 h vs. T 1/2 = 4.36 h), suggesting that cAMP also elicits a stabilizing effect on GH mRNA. Somatostatin (100 nM, 0.5-36 h) had no clear effect on GH transcript levels, but reduced GH release by as much as 90%. These results suggest that activation of either cAMP-PKA or PKC pathways can, possibly by different mechanisms, stimulate mRNA levels of the GtH II beta gene, but that only the cAMP-PKA pathway stimulates GH mRNA levels. It would appear therefore that GnRH, although stimulating GH release, does not regulate GH transcription in this fish.
Differential effects of gonadotropin-releasing hormone, dopamine and somatostatin and their second messengers on the mRNA levels of gonadotropin IIb subunit and growth hormone in the teleost fish, tilapia
Marchant TA, Chang J P, Nahorniak CS, Peter RE: Evidence that gonadotropin releasing hormone also functions as a growth hormone-releasing factor in the goldfish, Endocrinology 1989;124:2509-2518.
Lin X-W, Lin H-R, Peter RE: Growth hormone and gonadotropin secretion in the common carp(Cyprinus carpioL,): In vitro interactions of gonadotropin-releasing hormone, somatostatin, and the dopamine agonist apomorphinc, Gen Comp Endocrinol 1993;89:62-71.
LeGae F, Blaise O, Fostier A, Le Bail P-Y, Loir M, Mourot B, Weil C: Growth hormone (GFI) and reproduction: A review, Fish Physiol Bio-chem 1993;11:219-232.
Melamed P, Eliahu N, Lcvavi-Sivan B, Ofir M, Farchi-Pisanty O, Rentier-Delrue F, Smal J, Yaron Z, Naor Z: Hypothalamic and thyroidal regulation of growth hormone in tilapia, Gen Comp Endocrinol 1995;97:13-30.
Chang JP, Yu K, Wong AOL, Peter RE: Differential actions of dopamine receptor subtypes on gonadotropin and growth hormone release in vitro in goldfish, Neuroendocrinology 1990: 51:664-674.
Wong AOL, Chang JP, Peter RE: Dopamine stimulates growth hormone release from the pituitary' of goldfish, Carassius auralus, through the dopamine D1 receptors, Endocrinology 1992;130:1201-1210.
Levavi-Sivan B, Yaron Z: Gonadotropin secretion from perifused tilapia pituitary in relation to gonadotropin-releasing hormone, extracellular calcium, and activation of protein kinase C, Gen Comp Endocrinol 1989;75:187-194.
Jobin RM, Chang JP: Involvement of protein kinase C in the modulation of gonadotropin and growth hormone secretion from dispersed goldfish pituitary cells, Fish Physiol Biochem 1993;11:35-42.
Jobin RM, Chang JP: Actions of two native GnRHs and protein kinase modulators on goldfish pituitary cells: Studies on intracellular calcium levels and gonadotropin release, Cell Calcium 1992:13:531-540.
van Asselt LAC, Goos HJT, Smit-Van D, Braas J, Roozcndaal M, van Oordt PGWJ: The involvement of calcium and cyclic AMP in gonadotropin secretion in the African catfish, Clarias gariepinus, Gen Comp Endocrinol 1989:74:297.
Levavi-Sivan B, Yaron Z: Involvement of cyclic adenosine monophosphate in the stimulation of gonadotropin secretion from the pituitary of the tcleost fish, tilapia, Mol Cell Endocrinol 1992;85:175-182.
Mukhopadhyay B, Biswas R, Bhallacharya S: Gonadotropin releasing hormone stimulation of cyclic 3',5'-AMP in the pituitary cell of a tcleost(Clianna punctalus, Bloch) requires extracellular calcium: Its relationship to gonadotropin release, Gen Comp Endocrinol 1995:97: 353-365.
Gharib SD, Wierman ME, Shupnik MA, Chin W: Molecular biology of the pituitary gonadotropins, Endocr Rev 1990; 11:177-199.
Ben-Menahem D, Naor Z: Regulation of gonadotropin mRNA levels in cultured rat pituitary' cells by gonadotropin-releasing hormone (GnRH): Role for Ca2* and protein kinase C, Biochemistry 1994:33:3698-3704.
Mercer JE, Chin WW: Regulation of pituitary gonadotropin gene expression, Hum Reprod Update 1995;1:363-384.
Xiong F, Chin R, Gong Z, Suzuki K, Kitching R, Majumdar-Sonnylal S, Elsholtz H, Hew CL: Control of salmon pituitary hormone gene expression, Fish Physiol Biochem 1993:11:63-70.
Xiong F, Liu D, Le Drean Y, Elsholtz HP, Hew CL: Differential recruitment of steroid hormone response elements may dictate the expression of the pituitary gonadotropin II(S subunit gene during salmon maturation, Mol Endocrinol 1994:8:782-793.
Khakoo Z, Bhatia A, Gedainu L, Habibi HR: Functional specificity for salmon gonadotropin-releasing hormone (GnRH) and chicken GnRH-ll coupled to the gonadotropin release and subunit messenger ribonucleic acid level in the goldfish pituitary, Endocrinology 1994; 134:838-847.
Bilezikjian LM, Vale WW: Stimulation of adenosine 3',5'-monophosphate production by-growth hormone releasing factor and its inhibition by somatostatin in anterior pituitary cells in vitro, Endocrinology 1983:113:657-662.
Peter RE, Nahorniak CS, Vale WW, Rivicr JE: Human pancreatic growth hormone releasing factor (hpGRF) stimulates growth hormone release in goldfish, J Exp Zool 1984:231:161-163.
Marchant TA, Peter RE: Hypothalamic peptides influencing growth hormone secretion in the goldfish, Carassius auralus, Fish Physiol Biochem 1989:7:133-139.
Yada T, Urano A, Hirano T: Growth hormone and prolactin gene expression and release in the pituitary of rainbow trout in serum-free culture, Endocrinology 1991:129:1183-1192.
Luo D, McKcown BA: Interaction of carp growth hormone-releasing factor and somatostatin on in vitro release of growth hormone in rainbow trout(Oncorhynchus mykiss), Neu-roendocrinolgy 1991;54:359-364.
Wong AOL, Chang JP, Peter RE: Interactions of somatostatin, gonadotropin-releasing hormone, and the gonads on dopamine-stimulated growth hormone release in the goldfish, Gen Comp Endocrinol 1993:92:366-378.
Wong AOL, van der Kraak G, Chang JP: Cyclic 3',5'-adcnosinc monophosphate mediates dopamine Dl-stimulated growth hormone release from goldfish pituitary cells, Neuroendocrino-logy 1994;60:410-417.
Wong AOL, Van Goor F, Jobin RM, Neumann CM, Chang JP: Interactions of cyclic AMP, protein kinase C and calcium in dopamine- and GnRH-stimulaled growth hormone release in the goldfish, Endocrinology 1994; 135:1593-1604.
Cook H, Bcrkenbosch JW, Femhoul MJ, Yu K-L, Peter RE, Chang JP, Rivier JE: Demonstration of gonadotropin releasing-hormone receptors on gonadotrophs and somatotrophs of the goldfish: An electron microscope study, Regul Peptides 1991;36:369-378.
Melamed P, Eliahu N, Ofir M, Levavi-Sivan B, Rentier-Delrue F, Smal J, Yaron Z: The effects of gonadal development and sex steroids on GH secretion in the male tilapia hybrid, Fish Physiol Biochem 1995:14:267-277.
Mahmoud SS, Moloney MM, Habibi HR: Cloning and sequencing of the goldfish growth hormone cDNA, Gen Comp Endocrinol 1996: 101:139-144.
Elsholtz HP, Majumdar-Sonnvlal S, Xiong F, Gong Z, Hew CL: Phylogenetic specificity of prolactin gene expression with conservation of pit-1 function, Mol Endocrinol 1992:6:515-522.
Argenton F, Vianello S, Bcmardini S, Jac-quemin P, Martial J, Bclayew A, Colombo L, Bortolussi M: The transcriptional regulation of the growth hormone gene is conserved in vertebrate evolution, Biochem Biophys Res Com-mun 1993:192:1360-1366.
Yamada S, Hata J-I, Yamashita S: Molecular cloning of fish pit-1 cDNA and its functional binding to promoter of gene expressed in the pituitary, J Biol Chcrn 1993:268:24361-24366.
Ono M, Mochizuki E, Mori Y, Aizawa A, Hari-gai T: The regulatory region and transcription factor required for the expression of rat and salmon pituitary hormone-encoding genes show cell-type and species specificity, Gene 1995: 153:267-271.
Tlieill LE, Karin M: Transcriptional control of GH expression and anterior pituitary development, Endocr Rev 1993; 14:670-689.
Gutierrez-Hartmann A: Pit-l/GHF-1: A pituitary-specific transcription factor linking general signaling pathways to cell-specific gene expression, Mol Endocrinol 1994:8:1447-1449.
Dana S, Karin M: Induction of human growth hormone promoter activity by the adenosine 3',5'-monophosphate pathway involves a novel responsive clement, Mol Endocrinol 1989:3: 815-821.
Copp RP, Samuels HH: Identification of an adenosine 3',5'-monophosphate (cAMPFre-sponsive region in the rat growth hormone gene: Evidence for independent and synergistic effects of cAMP and thyroid hormone on gene expression, Mol Endocrinol 1989:3:790-796.
Levavi-Sivan B, Ofir M, Yaron Z: Possiblcsitcs of dopaminergic inhibition of gonadotropin release from the pituitary of a tcleost fish, tilapia, Mol Cell Endocrinol 1995; 109:87-95.
Bogomolnaya A, Yaron Z, Hilgc V, Gracsslin D, Lichtenberg V, Abraham M: Isolation and radioimmunoassay of a steroidogenic gonadotropin of tilapia, Isr J Aquacult-Bamidgeh 1989:41:123-136.
Kawauchi H, Suzuki K, Itoh H, Swanson P, Naito N, Nagahama Y, Nozaki M, Nakai Y, Itoh S: The duality of tcleost gonadotropins, Fish Physiol Biochem 1989;7:29-38.
Chomczynski P, Sacchi N: Single step method of RNA isolation by acidguanidinium thiocya-nate-phenol-chloroform extraction, Ann Biochem 1987;162:156-159.
Frohman MA: RACE: Rapid Amplification of cDNA Ends, PCR Protocols: A Guide to Methods and Applications, New York, Academic Press, 1990.
Elizur A, Zmora N, Rosenfeld H, Meiri I, Has-sin S, Gordin H, Zohar Y: p GtH I and p GtH II from the gilthead seabream, Gen Comp Endocrinol 1996;102:39-46.
Rentier-Delrue F, Swennen D, Philippart JC, L'Hoir C, Lion M, Benrubi O, Martial JA: Tilapia growth hormone: Molecular cloning of cDNA and expression inEscherichia coti, DNA 1989;8:271-278.
Andrews WV, Maurer RA, Conn PM: Stimulation of rat luteinizing hormone-P messenger RNA levels by gonadotropin releasing hormone, J Biol Client 1988:263:13755-13761.
Ishizaka K, Tsujii T, Winters SJ: Evidence for a role for the cyclic adenosine 3',5'-monophos-phate/protcin kinasc-A pathway in regulation of the gonadotropin subunit messenger ribonucleic acids, Endocrinology 1993:133:2040-2048.
Curran T, Franza BR: Fos and Jun: The AP-I connection, Cell 1988:55:395-397.
Ccsnjai M, Catt KJ, Stojilkovic SS: Coordinate actions of calcium and protein kinasc-C in the expression of primary response genes in pituitary gonadotrophs, Endocrinology 1994:135: 692-701.
Barinaga M, Bilezikjian LM, Vale WW, Rosen-fcld MG, Evans RM: Independent effects of growth hormone releasing factor on growth hormone release and gene transcription, Nature 1985;314:279-281.
Parker DB, Coe IR, Dixon GH, Sherwood NM: Two salmon neuropeptides encoded by one brain cDNA arc structurally related to members of the glucagon superfamily, Eur J Biochem 1993:215:439-448.
McRory JE, Parker DB, Ngamvongchon S, Sherwood NM: Sequence and expression of cDNA for pituitary adenylate cyclase activating polypeptide (PACAP) and growth hormone-releasing hormone (GHRHFlike peptide in catfish, Mol Cell Endocrinol 1995:108:169-177.
Murphy D, Pardy K, Scah V, Carter D: Post-transcriptional regulation of rat growth hormone gene expression: Increased message stability and nuclear polyadenylation accompany thyroid hormone depletion, Mol Cell Biol 1992; 12:2624-2632.
Imagawa M, Chiu R, Karin M: Transcription factor AP-2 mediates induction by two different signal-transduction pathways: Protein kinase C and cAMP, Cell 1987:51:251-260.
Rocsler WJ, Vandenbark GR, Hanson RW: Cyclic AMP and the induction of eukaryotic gene transcription, J Biol Chem 1988;263: 9063-9066.
Yada T, Hirano T: Inhibition of growth hormone synthesis by somatostatin in cultured pituitarv of rainbow trout, J Comp Phvsiol 1992;162:575-580.
Namba H, Morita S, Melmed S: Insulin-like growth factor-I action on growth hormone secretion and messenger ribonucleic acid levels: Interactions with somatostatin, Endocrinology 1989:24:1794-1799.