Kisspeptin increases GnRH mRNA expression and secretion in GnRH secreting neuronal cell lines

Molecular and Cellular Endocrinology

Volumn 311, Issue 1-2, 2009, Pages 126-134

  Novaira, Horacio J ^a   Ng, Yewade ^a   Wolfe, Andrew ^a   Radovick, Sally ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Estradiol; GN11 cells; GPR54; GT1 7 cells

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; ESTRADIOL; G PROTEIN COUPLED RECEPTOR 54; GONADORELIN; KISSPEPTIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE B;

ANIMAL CELL; ARTICLE; CELL LINE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GONADOTROPIN SECRETING CELL; HORMONE RELEASE; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TIME; WESTERN BLOTTING;

1-PHOSPHATIDYLINOSITOL 3-KINASE; CELL LINE; ENZYME ACTIVATION; ESTRADIOL; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GONADOTROPIN-RELEASING HORMONE; MAP KINASE SIGNALING SYSTEM; NEURONS; OLIGOPEPTIDES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, G-PROTEIN-COUPLED; RNA, MESSENGER; TIME FACTORS;

EID: 69249219124     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2009.06.011     Document Type: Article

References (69)

1. Bourguignon J.P., Gerard A., Debougnoux G., Rose J., and Franchimont P. Pulsatile release of gonadotropin-releasing hormone (GnRH) from the rat hypothalamus in vitro: calcium and glucose dependency and inhibition by superactive GnRH analogs. Endocrinology 1213 (1987) 993-999
2. Bustin S.A., Benes V., Nolan T., and Pfaffl M.W. Quantitative real-time RT-PCR-a perspective. Journal of Molecular Endocrinology 343 (2005) 597-601
3. Caraty A., and Franceschini I. Basic aspects of the control of GnRH and LH secretions by kisspeptin: potential applications for better control of fertility in females. Reproduction in Domestic Animals = Zuchthygiene 43 Suppl. 2 (2008) 172-178
4. Castellano J.M., Navarro V.M., Fernandez-Fernandez R., Nogueiras R., Tovar S., Roa J., Vazquez M.J., Vigo E., Casanueva F.F., Aguilar E., Pinilla L., Dieguez C., and Tena-Sempere M. Changes in hypothalamic KiSS-1 system and restoration of pubertal activation of the reproductive axis by kisspeptin in undernutrition. Endocrinology 1469 (2005) 3917-3925
5. Castellano J.M., Navarro V.M., Fernandez-Fernandez R., Castano J.P., Malagon M.M., Aguilar E., Dieguez C., Magni P., Pinilla L., and Tena-Sempere M. Ontogeny and mechanisms of action for the stimulatory effect of kisspeptin on gonadotropin-releasing hormone system of the rat. Molecular and Cellular Endocrinology 257-258 (2006) 75-83
6. Clarkson J., d'Anglemont de Tassigny X., Moreno A.S., Colledge W.H., and Herbison A.E. Kisspeptin-GPR54 signaling is essential for preovulatory gonadotropin-releasing hormone neuron activation and the luteinizing hormone surge. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience 2835 (2008) 8691-8697
7. d'Anglemont de Tassigny X., Fagg L.A., Dixon J.P., Day K., Leitch H.G., Hendrick A.G., Zahn D., Franceschini I., Caraty A., Carlton M.B., Aparicio S.A., and Colledge W.H. Hypogonadotropic hypogonadism in mice lacking a functional Kiss1 gene. Proceedings of the National Academy of Sciences of the United States of America 10425 (2007) 10714-10719
8. d'Anglemont de Tassigny X., Fagg L.A., Carlton M.B., and Colledge W.H. Kisspeptin can stimulate gonadotropin-releasing hormone (GnRH) release by a direct action at GnRH nerve terminals. Endocrinology 1498 (2008) 3926-3932
9. de Roux N., Genin E., Carel J.C., Matsuda F., Chaussain J.L., and Milgrom E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proceedings of the National Academy of Sciences of the United States of America 10019 (2003) 10972-10976
10. Dungan H.M., Gottsch M.L., Zeng H., Gragerov A., Bergmann J.E., Vassilatis D.K., Clifton D.K., and Steiner R.A. The role of kisspeptin-GPR54 signaling in the tonic regulation and surge release of gonadotropin-releasing hormone/luteinizing hormone. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience 2744 (2007) 12088-12095
11. El Majdoubi M., Sahu A., and Plant T.M. Effect of estrogen on hypothalamic transforming growth factor alpha and gonadotropin-releasing hormone gene expression in the female rhesus monkey. Neuroendocrinology 674 (1998) 228-235
12. Funes S., Hedrick J.A., Vassileva G., Markowitz L., Abbondanzo S., Golovko A., Yang S., Monsma F.J., and Gustafson E.L. The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochemical and Biophysical Research Communications 3124 (2003) 1357-1363
13. Gottsch M.L., Clifton D.K., and Steiner R.A. Kisspepeptin-GPR54 signaling in the neuroendocrine reproductive axis. Molecular and Cellular Endocrinology 254-255 (2006) 91-96
14. Han S.K., Gottsch M.L., Lee K.J., Popa S.M., Smith J.T., Jakawich S.K., Clifton D.K., Steiner R.A., and Herbison A.E. Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience 2549 (2005) 11349-11356
15. Herbison A.E. Multimodal influence of estrogen upon gonadotropin-releasing hormone neurons. Endocrine Reviews 193 (1998) 302-330
16. Hrabovszky E., Shughrue P.J., Merchenthaler I., Hajszan T., Carpenter C.D., Liposits Z., and Petersen S.L. Detection of estrogen receptor-beta messenger ribonucleic acid and 125I-estrogen binding sites in luteinizing hormone-releasing hormone neurons of the rat brain. Endocrinology 1419 (2000) 3506-3509
17. Herbison A.E., and Pape J.R. New evidence for estrogen receptors in gonadotropin-releasing hormone neurons. Frontiers in Neuroendocrinology 224 (2001) 292-308
18. Herbison A.E. Estrogen positive feedback to gonadotropin-releasing hormone (GnRH) neurons in the rodent: the case for the rostral periventricular area of the third ventricle (RP3 V). Brain Research Reviews 572 (2008) 277-287
19. Irwig M.S., Fraley G.S., Smith J.T., Acohido B.V., Popa S.M., Cunningham M.J., Gottsch M.L., Clifton D.K., and Steiner R.A. Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat. Neuroendocrinology 804 (2004) 264-272
20. Jacobi J.S., Martin C., Nava G., Jeziorski M.C., Clapp C., and Martinez de la Escalera G. 17-Beta-estradiol directly regulates the expression of adrenergic receptors and kisspeptin/GPR54 system in GT1-7 GnRH neurons. Neuroendocrinology 864 (2007) 260-269
21. Kauffman A.S., Clifton D.K., and Steiner R.A. Emerging ideas about kisspeptin-GPR54 signaling in the neuroendocrine regulation of reproduction. Trends in Neurosciences 3010 (2007) 504-511
22. Kinoshita M., Tsukamura H., Adachi S., Matsui H., Uenoyama Y., Iwata K., Yamada S., Inoue K., Ohtaki T., Matsumoto H., and Maeda K. Involvement of central metastin in the regulation of preovulatory luteinizing hormone surge and estrous cyclicity in female rats. Endocrinology 14610 (2005) 4431-4436
23. Kotani M., Detheux M., Vandenbogaerde A., Communi D., Vanderwinden J.M., Le Poul E., Brezillon S., Tyldesley R., Suarez-Huerta N., Vandeput F., Blanpain C., Schiffmann S.N., Vassart G., and Parmentier M. The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. The Journal of Biological Chemistry 27637 (2001) 34631-34636
24. Liu X., Lee K., and Herbison A.E. Kisspeptin excites gonadotropin-releasing hormone neurons through a phospholipase C/calcium-dependent pathway regulating multiple ion channels. Endocrinology 1499 (2008) 4605-4614
25. Martinez-Fuentes A.J., Hu L., Krsmanovic L.Z., and Catt K.J. Gonadotropin-releasing hormone (GnRH) receptor expression and membrane signaling in early embryonic GnRH neurons: role in pulsatile neurosecretion. Molecular Endocrinology (Baltimore, MD) 187 (2004) 1808-1817
26. Matsui H., Takatsu Y., Kumano S., Matsumoto H., and Ohtaki T. Peripheral administration of metastin induces marked gonadotropin release and ovulation in the rat. Biochemical and Biophysical Research Communications 3202 (2004) 383-388
27. Mellon P.L., Windle J.J., Goldsmith P.C., Padula C.A., Roberts J.L., and Weiner R.I. Immortalization of hypothalamic GnRH neurons by genetically targeted tumorigenesis. Neuron 51 (1990) 1-10
28. Messager S., Chatzidaki E.E., Ma D., Hendrick A.G., Zahn D., Dixon J., Thresher R.R., Malinge I., Lomet D., Carlton M.B., Colledge W.H., Caraty A., and Aparicio S.A. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proceedings of the National Academy of Sciences of the United States of America 1025 (2005) 1761-1766
29. Moenter S.M., Caraty A., and Karsch F.J. The estradiol-induced surge of gonadotropin-releasing hormone in the ewe. Endocrinology 1273 (1990) 1375-1384
30. Morelli A., Marini M., Mancina R., Luconi M., Vignozzi L., Fibbi B., Filippi S., Pezzatini A., Forti G., Vannelli G.B., and Maggi M. Sex steroids and leptin regulate the "first kiss" (KiSS 1/G-protein-coupled receptor 54 system) in human gonadotropin-releasing-hormone-secreting neuroblasts. The Journal of Sexual Medicine 55 (2008) 1097-1113
31. Navarro V.M., Castellano J.M., Fernandez-Fernandez R., Barreiro M.L., Roa J., Sanchez-Criado J.E., Aguilar E., Dieguez C., Pinilla L., and Tena-Sempere M. Developmental and hormonally regulated messenger ribonucleic acid expression of KiSS-1 and its putative receptor, GPR54, in rat hypothalamus and potent luteinizing hormone-releasing activity of KiSS-1 peptide. Endocrinology 14510 (2004) 4565-4574
32. Navarro V.M., Castellano J.M., Fernandez-Fernandez R., Tovar S., Roa J., Mayen A., Nogueiras R., Vazquez M.J., Barreiro M.L., Magni P., Aguilar E., Dieguez C., Pinilla L., and Tena-Sempere M. Characterization of the potent luteinizing hormone-releasing activity of KiSS-1 peptide, the natural ligand of GPR54. Endocrinology 1461 (2005) 156-163
33. Navarro V.M., Castellano J.M., Fernandez-Fernandez R., Tovar S., Roa J., Mayen A., Barreiro M.L., Casanueva F.F., Aguilar E., Dieguez C., Pinilla L., and Tena-Sempere M. Effects of KiSS-1 peptide, the natural ligand of GPR54, on follicle-stimulating hormone secretion in the rat. Endocrinology 1464 (2005) 1689-1697
34. Nazian S.J. Role of metastin in the release of gonadotropin-releasing hormone from the hypothalamus of the male rat. Journal of Andrology 273 (2006) 444-449
35. Ng Y., Wolfe A., Novaira H.J., and Radovick S. Estrogen regulation of gene expression in GnRH neurons. Molecular and Cellular Endocrinology 3031 2 (2009) 25-33
36. Petersen S.L., Ottem E.N., and Carpenter C.D. Direct and indirect regulation of gonadotropin-releasing hormone neurons by estradiol. Biology of Reproduction 696 (2003) 1771-1778
37. Pielecka-Fortuna J., Chu Z., and Moenter S.M. Kisspeptin acts directly and indirectly to increase gonadotropin-releasing hormone neuron activity and its effects are modulated by estradiol. Endocrinology 1494 (2008) 1979-1986
38. Plant T.M., and Barker-Gibb M.L. Neurobiological mechanisms of puberty in higher primates. Human Reproduction Update 101 (2004) 67-77
39. Plant T.M., and Witchel S.F. Puberty in nonhuman primates and humans. In: Neil J.D. (Ed). Knobil and Neill's Physiology of Reproduction. 3rd ed. (2006), Elsevier Science, San Diego pp. 2177-2230
40. Plant T.M. Hypothalamic control of the pituitary-gonadal axis in higher primates: key advances over the last two decades. Journal of Neuroendocrinology 206 (2008) 719-726
41. Prentice L.M., Klausen C., Kalloger S., Kobel M., McKinney S., Santos J.L., Kenney C., Mehl E., Gilks C.B., Leung P., Swenerton K., Huntsman D.G., and Aparicio S.A. Kisspeptin and GPR54 immunoreactivity in a cohort of 518 patients defines favourable prognosis and clear cell subtype in ovarian carcinoma. BMC Medicine 5 (2007) 33
42. Quaynor S., Hu L., Leung P.K., Feng H., Mores N., Krsmanovic L.Z., and Catt K.J. Expression of a functional G protein-coupled receptor 54-kisspeptin autoregulatory system in hypothalamic gonadotropin-releasing hormone neurons. Molecular Endocrinology 21 (2007) 3062-3070
43. Radovick S., Ticknor C.M., Nakayama Y., Notides A.C., Rahman A., Weintraub B.D., Cutler Jr. G.B., and Wondisford F.E. Evidence for direct estrogen regulation of the human gonadotropin-releasing hormone gene. The Journal of Clinical Investigation 885 (1991) 1649-1655
44. Radovick S., Wray S., Lee E., Nicols D.K., Nakayama Y., Weintraub B.D., Westphal H., Cutler Jr. G.B., and Wondisford F.E. Migratory arrest of gonadotropin-releasing hormone neurons in transgenic mice. Proceedings of the National Academy of Sciences of the United States of America 888 (1991) 3402-3406
45. Radovick S., Wray S., Muglia L., Westphal H., Olsen B., Smith E., Patriquin E., and Wondisford F.E. Steroid hormone regulation and tissue-specific expression of the human GnRH gene in cell culture and transgenic animals. Hormones and Behavior 284 (1994) 520-529
46. Ringel M.D., Hardy E., Bernet V.J., Burch H.B., Schuppert F., Burman K.D., and Saji M. Metastin receptor is overexpressed in papillary thyroid cancer and activates MAP kinase in thyroid cancer cells. The Journal of Clinical Endocrinology and Metabolism 875 (2002) 2399
47. Roa J., Vigo E., Castellano J.M., Navarro V.M., Fernandez-Fernandez R., Casanueva F.F., Dieguez C., Aguilar E., Pinilla L., and Tena-Sempere M. Hypothalamic expression of KiSS-1 system and gonadotropin-releasing effects of kisspeptin in different reproductive states of the female rat. Endocrinology 1476 (2006) 2864-2878
48. Roa J., Aguilar E., Dieguez C., Pinilla L., and Tena-Sempere M. New frontiers in kisspeptin/GPR54 physiology as fundamental gatekeepers of reproductive function. Frontiers in Neuroendocrinology 291 (2008) 48-69
49. Roa J., Castellano J.M., Navarro V.M., Handelsman D.J., Pinilla L., and Tena-Sempere M. Kisspeptins and the control of gonadotropin secretion in male and female rodents. Peptides 30 (2009) 57-66
50. Roa J., Vigo E., Castellano J.M., Gaytan F., Navarro V.M., Aguilar E., Dijcks F.A., Ederveen A.G., Pinilla L., van Noort P.I., and Tena-Sempere M. Opposite roles of estrogen receptor (ER)-alpha and ERbeta in the modulation of luteinizing hormone responses to kisspeptin in the female rat: implications for the generation of the preovulatory surge. Endocrinology 1494 (2008) 1627-1637
51. Roy D., Angelini N.L., and Belsham D.D. Estrogen directly respresses gonadotropin-releasing hormone (GnRH) gene expression in estrogen receptor-alpha (ERalpha)- and ERbeta-expressing GT1-7 GnRH neurons. Endocrinology 14011 (1999) 5045-5053
52. Sarkar D.K., and Fink G. Luteinizing hormone releasing factor in pituitary stalk plasma from long-term ovariectomized rats: effects of steroids. The Journal of Endocrinology 863 (1980) 511-524
53. Seminara S.B., Messager S., Chatzidaki E.E., Thresher R.R., Acierno Jr. J.S., Shagoury J.K., Bo-Abbas Y., Kuohung W., Schwinof K.M., Hendrick A.G., Zahn D., Dixon J., Kaiser U.B., Slaugenhaupt S.A., Gusella J.F., O'Rahilly S., Carlton M.B., Crowley Jr. W.F., Aparicio S.A., and Colledge W.H. The GPR54 gene as a regulator of puberty. The New England Journal of Medicine 34917 (2003) 1614-1627
54. Seminara S.B., Dipietro M.J., Ramaswamy S., Crowley Jr. W.F., and Plant T.M. Continuous human metastin 45-54 infusion desensitizes G protein-coupled receptor 54-induced gonadotropin-releasing hormone release monitored indirectly in the juvenile male rhesus monkey (Macaca mulatta): a finding with therapeutic implications. Endocrinology 1475 (2006) 2122-2126
55. Seminara S.B., and Crowley Jr. W.F. Kisspeptin and GPR54: discovery of a novel pathway in reproduction. Journal of Neuroendocrinology 206 (2008) 727-731
56. Shahab M., Mastronardi C., Seminara S.B., Crowley W.F., Ojeda S.R., and Plant T.M. Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. Proceedings of the National Academy of Sciences of the United States of America 1026 (2005) 2129-2134
57. Skynner M.J., Sim J.A., and Herbison A.E. Detection of estrogen receptor alpha and beta messenger ribonucleic acids in adult gonadotropin-releasing hormone neurons. Endocrinology 14011 (1999) 5195-5201
58. Skinner D.C., and Dufourny L. Oestrogen receptor beta-immunoreactive neurones in the ovine hypothalamus: distribution and colocalisation with gonadotropin-releasing hormone. Journal of Neuroendocrinology 171 (2005) 29-39
59. Smith J.T., Dungan H.M., Stoll E.A., Gottsch M.L., Braun R.E., Eacker S.M., Clifton D.K., and Steiner R.A. Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse. Endocrinology 1467 (2005) 2976-2984
60. Smith J.T., Cunningham M.J., Rissman E.F., Clifton D.K., and Steiner R.A. Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 1469 (2005) 3686-3692
61. Smith J.T., Clifton D.K., and Steiner R.A. Regulation of the neuroendocrine reproductive axis by kisspeptin-GPR54 signaling. Reproduction (Cambridge, England) 1314 (2006) 623-630
62. Smith J.T., Popa S.M., Clifton D.K., Hoffman G.E., and Steiner R.A. Kiss1 neurons in the forebrain as central processors for generating the preovulatory luteinizing hormone surge. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience 2625 (2006) 6687-6694
63. Stathatos N., Bourdeau I., Espinosa A.V., Saji M., Vasko V.V., Burman K.D., Stratakis C.A., and Ringel M.D. KiSS-1/G protein-coupled receptor 54 metastasis suppressor pathway increases myocyte-enriched calcineurin interacting protein 1 expression and chronically inhibits calcineurin activity. The Journal of Clinical Endocrinology and Metabolism 909 (2005) 5432-5440
64. Suarez-Quian C.A., Wynn P.C., and Catt K.J. Receptor-mediated endocytosis of GnRH analogs: differential processing of gold-labeled agonist and antagonist derivatives. Journal of Steroid Biochemistry 241 (1986) 183-192
65. Tena-Sempere M. GPR54 and kisspeptin in reproduction. Human Reproduction Update 125 (2006) 631-639
66. Terasawa E., and Fernandez D.L. Neurobiological mechanisms of the onset of puberty in primates. Endocrine Reviews 221 (2001) 111-151
67. Wintermantel T.M., Campbell R.E., Porteous R., Bock D., Grone H.J., Todman M.G., Korach K.S., Greiner E., Perez C.A., Schutz G., and Herbison A.E. Definition of estrogen receptor pathway critical for estrogen positive feedback to gonadotropin-releasing hormone neurons and fertility. Neuron 522 (2006) 271-280
68. Wong M.L., and Medrano J.F. Real-time PCR for mRNA quantitation. BioTechniques 391 (2005) 75-85
69. Xia L., Van Vugt D., Alston E.J., Luckhaus J., and Ferin M. A surge of gonadotropin-releasing hormone accompanies the estradiol-induced gonadotropin surge in the rhesus monkey. Endocrinology 1316 (1992) 2812-2820