doi:

DOI: 10.3724/SP.J.1231.2013.38776

Journal of Fisheries of China (水产学报) 2013/37:12 PP.1863-1872

Mechanisms of actions of somatostatin on the regulation of pituitary growth hormone release in fish


Abstract:
Somatostatin is a multifunctional tetradecapeptide which is involved in growth,development,metabolism and reproductive processes,via the specific seven α helical transmembrane G-protein-coupled receptors(GPCRs).This review briefly summarizes the progress of research on somatostatin and its receptors,with special emphasis on the intracellular signaling mechanisms mediating somatostatin actions on the regulation of pituitary growth hormone release in fish.To date,six somatostatin genes and four somatostatin receptors have been characterized in fish.The diversity of the somatostatin peptide family is due to the existence of multiple somatostatin genes as well as the tissue-specific differential processing of preprosomatostatin.The subtypes of somatostatin receptors are complex due to the polyploidization that occurred during fish lineage evolution.Information on the mechanisms of somatostatin suppression of GH secretion in teleosts is mainly derived from studies in goldfish,which indicates that cAMP formation,Ca2+ mobilization,and PKC activation may be involved in the mechanism through which somatostatin regulates GH secretion.However,the intricate web of intracellular signals is still far from being fully understood.In addition,species-specific differences in the mechanisms of GH release do exist in diverse models.The somatostatin genes,receptors and the mechanism of actions of somatostatin on pituitary GH release await further studies in teleosts.

Key words:fish,somatostatin,somatostatin receptors,growth hormone,signal transduction

ReleaseDate:2015-04-19 11:27:17



[1] Brazeau P,Vale W,Burgus R,et al.Hypothalamic polypeptide that inhibits the secretion of immunoreactive pituitary growth hormone[J].Science,1973,179(68):77-79.

[2] Patel Y C.Somatostatin and its receptor family[J].Front Neuroendocrinol,1999,20(3):157-198.

[3] Lin X,Peter R E.Somatostatins and their receptors in fish[J].Comp Biochem Physiol-Part B:Biochem Mol Biol,2001,129(2-3):543-550.

[4] Gahete M D,Cordoba-Chacon J,Duran-Prado M,et al.Somatostatin and its receptors from fish to mammals[J].Ann N Y Acad Sci,2010,1200:43-52.

[5] Kumar U,Grant M.Somatostatin and somatostatin receptors[J].Results Probl Cell Differ,2010,50:137-184.

[6] Hobart P,Crawford R,Shen L P,et al.Cloning and sequence analysis of cDNAs encoding two distinct somatostatin precursors found in the endocrine pancreas of anglerfish[J].Nature,1980,288(5787):137-141.

[7] Lin X W,Otto C J,Peter R E.Evolution of neuroendocrine peptide systems:gonadotropin-releasing hormone and somatostatin[J].Comp Biochem Physiol-Part C:Pharmacol Toxicol Endocrinol,1998,119(3):375-388.

[8] Lin X W,Otto C J,Peter R E.Expression of three distinct somatostatin messenger ribonucleic acids(mRNAs)in goldfish brain:characterization of the complementary deoxyribonucleic acids,distribution and seasonal variation of the mRNAs,and action of a somatostatin-14 variant[J].Endocrinology,1999,140(5):2089-2099.

[9] Uesaka T,Yano K,Yamasaki M,et al.Somatostatin-,vasoactive intestinal peptide-,and granulin-like peptides isolated from intestinal extracts of goldfish,Carassius auratus[J].General and Comparative Endocrinology,1995,99(3):298-306.

[10] Ye X,Li W S,Lin H R.Polygenic expression of somatostatin in orange-spotted grouper(Epinephelus coioides):molecular cloning and distribution of the mRNAs encoding three somatostatin precursors[J].Mol Cell Endocrinol,2005,241(1-2):62-72.

[11] Klein S E,Sheridan M A.Somatostatin signaling and the regulation of growth and metabolism in fish[J].Mol Cell Endocrinol,2008,286(1-2):148-154.

[12] Chang J P,Habibi H R,Yu Y,et al.Calcium and other signalling pathways in neuroendocrine regulation of somatotroph functions[J].Cell Calcium,2011,51(3-4):240-252.

[13] Samson W K,Zhang J V,Avsian-Kretchmer O,et al.Neuronostatin encoded by the somatostatin gene regulates neuronal,cardiovascular,and metabolic functions[J].J Biol Chem,2008,283(46):31949-31959.

[14] Liu Y,Lu D,Zhang Y,et al.The evolution of somatostatin in vertebrates[J].Gene,2010,463(1-2):21-28.

[15] Tostivint H,Quan F B,Bougerol M,et al.Impact of gene/genome duplications on the evolution of the urotensin II and somatostatin families[J].Gen Comp Endocrinol,2013,118(1):110-117.

[16] Yamada Y,Post S R,Wang K,et al.Cloning and functional characterization of a family of human and mouse somatostatin receptors expressed in brain,gastrointestinal tract,and kidney[J].Proc Natl Acad Sci USA,1992:251-255.

[17] Dong H Y,Li W S,Lin H R.Comparative analyses of sequence structure,evolution,and expression of four somatostatin receptors in orange-spotted grouper(Epinephelus coioides)[J].Mol Cell Endocrinol,2010,323(2):125-136.

[18] Muller E E,Locatelli V,Cocchi D.Neuroendocrine control of growth hormone secretion[J].Physiol Rev,1999,79(2):511-607.

[19] Cordoba-Chacon J,Gahete M D,Duran-Prado M,et al.Truncated somatostatin receptors as new players in somatostatin-cortistatin pathophysiology[J].Ann N Y Acad Sci,2010,1220(1):6-15.

[20] Duran-Prado M,Gahete M D,Martinez-Fuentes A J,et al.Identification and characterization of two novel truncated but functional isoforms of the somatostatin receptor subtype 5 differentially present in pituitary tumors[J].J Clin Endocrinol Metab,2009,94(7):2634-2643.

[21] Cordoba-Chacon J,Gahete M D,Duran-Prado M,et al.Identification and characterization of new functional truncated variants of somatostatin receptor subtype 5 in rodents[J].Cell Mol Life Sci,2009,67(7):1147-63.

[22] Kumar U,Laird D,Srikant C B,et al.Expression of the five somatostatin receptor(SSTR1-5)subtypes in rat pituitary somatotrophes:quantitative analysis by double-layer immunofluorescence confocal microscopy[J].Endocrinology,1997,138(10):4473-4476.

[23] Rohrer S P,Birzin E T,Mosley R T,et al.Rapid identification of subtype-selective agonists of the somatostatin receptor through combinatorial chemistry[J].Science,1998,282(5389):737-740.

[24] Nelson L E,Sheridan M A.Regulation of somatostatins and their receptors in fish[J].Gen Comp Endocrinol,2005,142(1-2):117-133.

[25] Cervia D,Bagnoli P.An update on somatostatin receptor signaling in native systems and new insights on their pathophysiology[J].Pharmacol Ther,2007,116(2):322-341.

[26] Ben-Shlomo A,Melmed S.Pituitary somatostatin receptor signaling[J].Trends Endocrinol Metab,2010,21(3):123-133.

[27] Kao Y,Youson J H,Holmes J A,et al.Effects of somatostatin on lipid metabolism of larvae and metamorphosing landlocked sea lamprey,Petromyzon marinus[J].Gen Comp Endocrind,1998,111(2):177-185.

[28] Yada T,Hirano T.Inhibition of growth hormone synthesis by somatostatin in cultured pituitary of rainbow trout[J].Journal of Comparative Physiology B,1992,162:575-580.

[29] Melamed P,Gur G,Elizur A,et al.Differential effects of gonadotropin-releasing hormone,dopamine and somatostatin and their second messengers on the mRNA levels of gonadotropin II beta subunit and growth hormone in the teleost fish,tilapia[J].Neuroendocrinology,1996,64(4):320-328.

[30] Rousseau K,Dufour S.Phylogenetic evolution of the neuroendocrine control of growth hormone:contribution from teleosts[J].Cybium,2004,28(3):181-198.

[31] Simard J,Labrie F,Gossard F.Regulation of growth hormone mRNA and pro-opiomelanocortin mRNA levels by cyclic AMP in rat anterior pituitary cells in culture[J].DNA,1986,5(4):263-270.

[32] Sugihara H,Minami S,Okada K,et al.Somatostatin reduces transcription of the growth hormone gene in rats[J].Endocrinology,1993,132(3):1225-1229.

[33] Chang J P,Johnson J D,Van Goor F,et al.Signal transduction mechanisms mediating secretion in goldfish gonadotropes and somatotropes[J].Biochem Cell Biol,2000,78(3):139-153.

[34] Kwong P,Chang J P.Somatostatin inhibition of growth hormone release in goldfish:possible targets of intracellular mechanisms of action[J].Gen Comp Endocrinol,1997,108(3):446-456.

[35] Yunker W K,Chang J P.Somatostatin actions on a protein kinase C-dependent growth hormone secretagogue cascade[J].Mol Cell Endocrinol,2001,175(1-2):193-204.

[36] Donoghue D J,Scanes C G.Possible involvement of adenylyl cyclase-cAMP-protein kinase a pathway in somatostatin inhibition of growth hormone release from chicken pituitary cells[J].Gen Comp Endocrinol,1991,81(1):113-119.

[37] Tanner J W,Davis S K,McArthur N H,et al.Modulation of growth hormone(GH)secretion and GH mRNA levels by GH-releasing factor,somatostatin and secretagogues in cultured bovine adenohypophysial cells[J].J Endocrinol,1990,125(1):109-115.

[38] Ramirez J L,Torronteras R,Castano J P,et al.Somatostatin plays a dual,stimulatory/inhibitory role in the control of growth hormone secretion by two somatotrope subpopulations from porcine pituitary[J].J Neuroendocrinol,1997,9(11):841-848.

[39] Cordoba-Chacon J,Gahete M D,Culler M D,et al.Somatostatin dramatically stimulates growth hormone release from primate somatotropes acting at low doses via sst5 and cAMP[J].J Neuroendocrinol,2012,24(3):453-463.

[40] Ramirez J L,Gracia-Navarro F,S.Garcia-Navarro,et al.Somatostatin stimulates GH secretion in two porcine somatotrope subpopulations through a cAMP-dependent pathway[J].Endocrinology,2002,143(3):889-897.

[41] Brunetti L.Nitric oxide:a gas as a modulator of neuroendocrine secretions[J].Clin Ter,1994,144(2):147-153.

[42] Koesling D,Russwurm M,Mergia E,et al.Nitric oxide-sensitive guanylyl cyclase:structure and regulation[J].Neurochem Int,2004,45(6):813-819.

[43] Rettori V,Belova N,Yu W H,et al.Role of nitric oxide in control of growth hormone release in the rat[J].Neuroimmunomodulation,1994,1(3):195-200.

[44] Tena-Sempere M,Pinilla L,Gonzalez D,et al.Involvement of endogneous nitric oxide in the control of pituitary responsiveness to different elicitors of growth hormone release in prepubertal rats[J].Neuroendocrinology,1996,64(2):146-152.

[45] Pinilla L,Tena-Sempere M,Aguilar E.Nitric oxide stimulates growth hormone secretion in vitro through a calcium- and cyclic guanosine monophosphate-independent mechanism[J].Horm Res,1999,51(5):242-247.

[46] Baratta M,Saleri R,Mainardi G L,et al.Leptin regulates GH gene expression and secretion and nitric oxide production in pig pituitary cells[J].Endocrinology,2002,143(2):551-557.

[47] Luque R M,Rodriguez-Pacheco F,Tena-Sempere M,et al.Differential contribution of nitric oxide and cGMP to the stimulatory effects of growth hormone-releasing hormone and low-concentration somatostatin on growth hormone release from somatotrophs[J].J Neuroendocrinology,2005,17(9):577-582.

[48] Valverde I,Penalva A,Ghigo E,et al.Involvement of nitric oxide in the regulation of growth hormone secretion in dogs[J].Neuroendocrinology,2001,74(4):213-229.

[49] Cuttica C M,Giusti M,Bocca L,et al.Nitric oxide modulates in vivo and in vitro growth hormone release in acromegaly[J].Neuroendocrinology,1997,66(6):426-431.

[50] Rubinek T,Rubinfeld H,Hadani M,et al.Nitric oxide stimulates growth hormone secretion from human fetal pituitaries and cultured pituitary adenomas[J].Endocrine,2005,28(2):209-216.

[51] Kato M.Involvement of nitric oxide in growth hormone(GH)-releasing hormone-induced GH secretion in rat pituitary cells[J].Endocrinology,1992,131(5):2133-2138.

[52] Tsumori M,Murakami Y,Koshimura K,et al.Endogenous nitric oxide inhibits growth hormone secretion through cyclic guanosine monophosphate-dependent mechanisms in GH3 cells[J].Endocr J,1999,46(6):779-785.

[53] Korbonits M,Trainer P J,Fanciulli G,et al.L-arginine is unlikely to exert neuroendocrine effects in humans via the generation of nitric oxide[J].Eur J Endocrinol,1996,135(5):543-547.

[54] Fisker S,Nielsen S,Ebdrup L,et al.The role of nitric oxide in L-arginine-stimulated growth hormone release[J].J Endocrinol Invest,1999,22(5 Suppl.):89-93.

[55] Bocca L,Valenti S,Cuttica C M,et al.Nitric oxide biphasically modulates GH secretion in cultured cells of GH-secreting human pituitary adenomas[J].Minerva Endocrinol,2000,25(3-4):55-59.

[56] Uretsky A D,Chang J P.Evidence that nitric oxide is involved in the regulation of growth hormone secretion in goldfish[J].Gen Comp Endocrinol,2000,118(3):461-470.

[57] Uretsky A D,Weiss B L,Yunker W K,et al.Nitric oxide produced by a novel nitric oxide synthase isoform is necessary for gonadotropin-releasing hormone-induced growth hormone secretion via a cGMP-dependent mechanism[J].J Neuroendocrinol,2003,15(7):667-676.

[58] Mitchell G,Sawisky G R,Grey C L,et al.Differential involvement of nitric oxide signaling in dopamine and PACAP stimulation of growth hormone release in goldfish[J].Gen Comp Endocrinol,2008,155(2):318-327.

[59] Yu Y,Chang J P.Involvement of protein kinase C and intracellular Ca2+ in goldfish brain somatostatin-28 inhibitory action on growth hormone release in goldfish[J].Gen Comp Endocrinol,2010,168(1):71-81.

[60] Cervia D,Petrucci C,Bluet-Pajot M T,et al.Inhibitory control of growth hormone secretion by somatostatin in rat pituitary GC cells:sst(2)but not sst(1)receptors are coupled to inhibition of single-cell intracellular free calcium concentrations[J].Neuroendocrinology,2002,76(2):99-110.

[61] Sims S M,Lussier B T,Kraicer J.Somatostatin activates an inwardly rectifying K+ conductance in freshly dispersed rat somatotrophs[J].J Physiol,1991,441:615-637.

[62] Yunker W K,Smith S,Graves C,et al.Endogenous hypothalamic somatostatins differentially regulate growth hormone secretion from goldfish pituitary somatotropes in vitro[J].Endocrinology,2003,144(9):4031-4041.

[63] Yunker W K,Chang J P.Somatostatin-14 actions on dopamine- and pituitary adenylate cyclase-activating polypeptide-evoked Ca2+ signals and growth hormone secretion[J].J Neuroendocrinol,2004,16(8):684-694.

[64] Yu Y,Chang J P.Goldfish brain somatostatin-28 differentially affects dopamine- and pituitary adenylate cyclase-activating polypeptide-induced GH release and Ca(2+)and cAMP signals[J].Mol Cell Endocrinol,2011,332(1-2):283-292.

[65] Marchant T A,Fraser R A,Andrews P C,et al.The influence of mammalian and teleost somatostatins on the secretion of growth hormone from goldfish(Carassius auratus L.)pituitary fragments in vitro[J].Regul Pept,1987,17(1):41-52.

[66] Oyama H,Bradshaw R A,Bates O J,et al.Amino acid sequence of catfish pancreatic somatostatin I[J].J Biol Chem,1980,255(6):2251-2254.

[67] Castano J P,Torronteras R,Ramirez J L,et al.Somatostatin increases growth hormone(GH)secretion in a subpopulation of porcine somatotropes:evidence for functional and morphological heterogeneity among porcine GH-producing cells[J].Endocrinology,1996,137(1):129-136.

[68] Reindl K M,Sheridan M A.Peripheral regulation of the growth hormone-insulin-like growth factor system in fish and other vertebrates[J].Comp Biochem Physiol-Part A:Mol Integr Physiol,2012,163(3-4):231-245.