Nitric oxide signaling in ghrelin-induced LH release from goldfish pituitary cells

General and Comparative Endocrinology

Volumn 183, Issue , 2013, Pages 7-13

  Grey, Caleb L ^a   Chang, John P ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Goldfish ghrelin; Maturational gonadotropin GTH II; Nitric oxide synthase isoform selective inhibitors; Primary goldfish pituitary cell culture; Signal transduction

Indexed keywords

7 NITROINDAZOLE; AMINOGUANIDINE; AMINOGUANIDINE HEMISULFATE; GHRELIN; INDUCIBLE NITRIC OXIDE SYNTHASE; ISOENZYME; LUTEINIZING HORMONE; N [3 (AMINOMETHYL)BENZYL]ACETAMIDINE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; NITROPRUSSIDE SODIUM; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL STIMULATION; CONTROLLED STUDY; FEMALE; GOLDFISH; HORMONAL REGULATION; HORMONE ACTION; HORMONE RELEASE; HYPOPHYSIS CELL; INTRACELLULAR SIGNALING; MALE; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL;

EID: 84871760294     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2012.11.022     Document Type: Article

References (50)

1. Bellefontaine N., Hanchate N.K., Parkash J., Campagne C., de Seranno S., Clasadonte J., d'Anglemont de Tassigny X., Prevot V. Nitric oxide as key mediator of neuron-to-neuron and endothelia-to-glia communication involved in the neuroendocrine control of reproduction. Neuroendocrinology 2011, 93:74-89.
2. Chang J.P., Cook H., Freedman G.L., Wiggs A.J., Somoza G.M., de Leeuw R., Peter R.E. Use of a pituitary cell dispersion method and primary culture system for the studies of gonadotropin-releasing hormone action in the goldfish, Carassius auratus. I. Initial morphological, static, and cell column perifusion studies. Gen. Comp. Endocrinol. 1990, 77:256-273.
3. Chang J.P., Habibi H.R., Yu Y., Moussavi M., Grey C.L., Pemberton J.G. Calcium and other signalling pathways in neuroendocrine regulation of somatotroph functions. Cell Calcium 2011, 51:240-252.
4. Chang J.P., Johnson J.D., Sawisky G.R., Grey C.L., Mitchell G., Booth M., Volk M.M., Parks S.K., Thompson E., Goss G.G., Klausen C., Habibi H.R. Signal transduction in multifactorial neuroendocrine control of gonadotropin secretion and synthesis in teleosts-studies on the goldfish model. Gen. Comp. Endocrinol. 2009, 161:42-52.
5. Chang J.P., Sawisky G.R., Mitchell G., Uretsky A.D., Kwong P., Grey C.L., Meints A.N., Booth M. PACAP stimulation of maturational gonadotropin secretion in goldfish involves extracellular signal-regulated kinase, but not nitric oxide or guanylate cyclase, signaling. Gen. Comp. Endocrinol. 2010, 165:127-135.
6. 2+ stores in dopamine- and PACAP-evoked growth hormone release in goldfish. Mol. Cell. Endocrinol. 2003, 206:63-74.
7. Dubey P.K., Tripathi V., Singh R.P., Saikumar G., Nath A., Pratheesh, Gade N., Sharma G.T. Expression of nitric oxide synthase isoforms in different stages of buffalo (Bubalus bubalis) ovarian follicles: effect of nitric oxide on in vitro development of preantral follicle. Theriogenology 2012, 77:280-291.
8. Dubey P.K., Tripathi V., Singh R.P., Sharma G.T. Influence of nitric oxide on in vitro growth, survival, steroidogenesis, and apoptosis of follicle stimulating hormone stimulated buffalo (Bubalus bubalis) preantral follicles. J. Vet. Sci. 2011, 12:257-265.
9. Ducsay C.A., Myers D.A. ENOS activation and NO function: differential control of steroidogenesis by nitric oxide and its adaptation with hypoxia. J. Endocrinol. 2011, 210:259-269.
10. Fernandez-Fernandez R., Tena-Sempere M., Navarro V.M., Barreiro M.L., Castellano J.M., Aguilar E., Pinilla L. Effects of ghrelin upon gonadotropin-releasing hormone and gonadotropin secretion in adult female rats: in vivo and in vitro studies. Neuroendocrinology 2005, 82:245-255.
11. Fernandez-Fernandez R., Tena-Sempere M., Roa J., Castellano J.M., Navarro V.M., Aguilar E., Pinilla L. Direct stimulatory effect of ghrelin on pituitary release of LH through a nitric oxide-dependent mechanism that is modulated by estrogen. Reproduction 2007, 133:1223-1232.
12. Forbes S., Li X.F., Kinsey-Jones J., O'Byrne K. Effects of ghrelin on Kisspeptin mRNA expression in the hypothalamic medial preoptic area and pulsatile luteinising hormone secretion in the female rat. Neurosci. Lett. 2009, 460:143-147.
13. Furuta M., Funabashi T., Kimura F. Intracerebroventricular administration of ghrelin rapidly suppresses pulsatile luteinizing hormone secretion in ovariectomized rats. Biochem. Biophys. Res. Commun. 2001, 288:780-785.
14. Grey C.L., Chang J.P. Differential involvement of protein kinase C and protein kinase A in ghrelin-induced growth hormone and gonadotrophin release from goldfish (Carassius auratus) pituitary cells. J. Neuroendocrinol. 2011, 23:1273-1287.
15. Grey C.L., Chang J.P. Ghrelin-induced growth hormone release from goldfish pituitary cells is nitric oxide dependent. Gen. Comp. Endocrinol. 2012, 179:152-158.
16. 2+ channels. Mol. Cell. Endocrinol. 2010, 317:64-77.
17. Griffiths M.J., Messent M., MacAllister R.J., Evans T.W. Aminoguanidine selectively inhibits inducible nitric oxide synthase. Br. J. Pharmacol. 1993, 110:963-968.
18. Hogg N., Singh R.J., Joseph J., Neese F., Kalyanaraman B. Reactions of nitric oxide with nitronyl nitroxides and oxygen: prediction of nitrite and nitrate formation by kinetic simulation. Free Radic. Res. 1995, 22:47-56.
19. Kaiya H., Miyazato M., Kangawa K., Peter R.E., Unniappan S. Ghrelin: a multifunctional hormone in non-mammalian vertebrates. Comp. Biochem. Physiol. Part A: Mol. Integr. Physiol. 2008, 149:109-128.
20. Kang K.S., Yahashi S., Matsuda K. Central and peripheral effects of ghrelin on energy balance, food intake and lipid metabolism in teleost fish. Peptides 2011, 32:2242-2247.
21. Klatt P., Schmid M., Leopold E., Schmidt K., Werner E.R., Mayer B. The pteridine binding site of brain nitric oxide synthase. Tetrahydrobiopterin binding kinetics, specificity, and allosteric interaction with the substrate domain. J. Biol. Chem. 1994, 269:13861-13866.
22. Kleppisch T., Feil R. CGMP signalling in the mammalian brain: role in synaptic plasticity and behaviour. Handb. Exp. Pharmacol. 2009, 549-579.
23. Levavi-Sivan B., Bogerd J., Mañanós E.L., Gómez A., Lareyre J.J. Perspectives on fish gonadotropins and their receptors. Gen. Comp. Endocrinol. 2010, 165:412-437.
24. Lorenzi T., Meli R., Marzioni D., Morroni M., Baragli A., Castellucci M., Gualillo O., Muccioli G. Ghrelin: a metabolic signal affecting the reproductive system. Cytokine Growth Factor Rev. 2009, 20:137-152.
25. Meints A.N., Pemberton J.G., Chang J.P. Nitric oxide and guanylate cyclase signalling are differentially involved in gonadotrophin (LH) release responses to two endogenous GnRHs from goldfish pituitary cells. J. Neuroendocrinol. 2012, 24:1166-1181.
26. Miura T., Maruyama K., Kaiya H., Miyazato M., Kangawa K., Uchiyama M., Shioda S., Matsuda K. Purification and properties of ghrelin from the intestine of the goldfish, Carassius auratus. Peptides 2009, 30:758-765.
27. Muccioli G., Lorenzi T., Lorenzi M., Ghe C., Arnoletti E., Raso G.M., Castellucci M., Gualillo O., Meli R. Beyond the metabolic role of ghrelin: a new player in the regulation of reproductive function. Peptides 2011, 32:2514-2521.
28. Naor Z. Signaling by G-protein-coupled receptor (GPCR): studies on the GnRH receptor. Front. Neuroendocrinol. 2009, 30:10-29.
29. Ogata R., Matsuzaki T., Iwasa T., Kiyokawa M., Tanaka N., Kuwahara A., Yasui T., Irahara M. Hypothalamic ghrelin suppresses pulsatile secretion of luteinizing hormone via beta-endorphin in ovariectomized rats. Neuroendocrinology 2009, 90:364-370.
30. 2+ elevation. Neurochem. Res. 1995, 20:779-784.
31. Parmentier S., Bohme G.A., Lerouet D., Damour D., Stutzmann J.M., Margaill I., Plotkine M. Selective inhibition of inducible nitric oxide synthase prevents ischaemic brain injury. Br. J. Pharmacol. 1999, 127:546-552.
32. Peter R.E., Nahorniak C.S., Chang J.P., Crim L.W. Gonadotropin release from the pars distalis of goldfish, Carassius auratus, transplanted beside the brain or into the brain ventricles: additional evidence for gonadotropin-release-inhibitory factor. Gen. Comp. Endocrinol. 1984, 55:337-346.
33. Potter L.R. Guanylyl cyclase structure, function and regulation. Cell. Signal. 2011, 23:1921-1926.
34. Rodríguez-Pacheco F., Luque R.M., Tena-Sempere M., Malagón M.M., Castaño J.P. Ghrelin induces growth hormone secretion via a nitric oxide/cGMP signalling pathway. J. Neuroendocrinol. 2008, 20:406-412.
35. Shepperd E., Peng C., Unniappan S. Ghrelinergic system in fish ovaries and ghrelin inhibition of germinal vesicle breakdown in zebrafish oocytes. Gen. Comp. Endocrinol. 2012, 176:426-431.
36. Slomiany B.L., Slomiany A. Helicobacter pylori induces disturbances in gastric mucosal Akt activation through inducible nitric oxide synthase-dependent S-nitrosylation: effect of ghrelin. ISRN Gastroenterol. 2011, 2011:1-8.
37. Sokołowska-Mikołajczyk M., Socha M., Szczerbik P., Epler P. The effects of ghrelin on the in vitro spontaneous and sGnRH-A stimulated luteinizing hormone (LH) release from the pituitary cells of common carp (Cyprinus carpio L.). Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2009, 153:386-390.
38. Sudar E., Dobutovic B., Soskic S., Mandusic V., Zakula Z., Misirkic M., Vucicevic L., Janjetovic K., Trajkovic V., Mikhailidis D.P., Isenovic E.R. Regulation of inducible nitric oxide synthase activity/expression in rat hearts from ghrelin-treated rats. J. Physiol. Biochem. 2010, 67:195-204.
39. Trudeau V.L. Neuroendocrine regulation of gonadotrophin II release and gonadal growth in the goldfish, Carassius auratus. Rev. Reprod. 1997, 2:55-68.
40. Unniappan S. Ghrelin: an emerging player in the regulation of reproduction in non-mammalian vertebrates. Gen. Comp. Endocrinol. 2010, 167:340-343.
41. Unniappan S., Canosa L.F., Peter R.E. Orexigenic actions of ghrelin in goldfish: feeding-induced changes in brain and gut mRNA expression and serum levels, and responses to central and peripheral injections. Neuroendocrinology 2004, 79:100-108.
42. Unniappan S., Lin X., Cervini L., Rivier J., Kaiya H., Peter R.E. Goldfish ghrelin: molecular characterization of the complementary deoxyribonucleic acid, partial gene structure and evidence for its stimulatory role in food intake. Endocrinology 2002, 143:4143-4146.
43. Unniappan S., Peter R. In vitro and in vivo effects of ghrelin on luteinizing hormone and growth hormone release in goldfish. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004, 286:R1093-R1101.
44. Uretsky A.D., Chang J.P. Evidence that nitric oxide is involved in the regulation of growth hormone secretion in goldfish. Gen. Comp. Endocrinol. 2000, 118:461-470.
45. Uretsky A.D., Weiss B.L., Yunker W.K., Chang J.P. 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. Neuroendocrinol. 2003, 15:667-676.
46. Van Goor F., Goldberg J.I., Chang J.P. Dopamine-D2 actions on voltage-dependent calcium current and gonadotropin-II secretion in cultured goldfish gonadotrophs. J. Neuroendocrinol. 1998, 10:175-186.
47. Villanueva C., Giulivi C. Subcellular and cellular locations of nitric oxide synthase isoforms as determinants of health and disease. Free Radic. Biol. Med. 2010, 49:307-316.
48. Volkoff H., Xu M., MacDonald E., Hoskins L. Aspects of the hormonal regulation of appetite in fish with emphasis on goldfish, Atlantic cod and winter flounder: notes on actions and responses to nutritional, environmental and reproductive changes. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2009, 153:8-12.
49. Wong A.O., Chang J.P., Peter R.E. Dopamine stimulates growth hormone release from the pituitary of goldfish, Carassius auratus, through the dopamine D1 receptors. Endocrinology 1992, 130:1201-1210.
50. 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. Mol. Cell. Endocrinol. 2011, 332:283-292.