Sex steroids and leptin regulate the "first kiss" (KiSS 1/g-protein-coupled receptor 54 system) in human gonadotropin-releasing-hormone-secreting neuroblasts

Journal of Sexual Medicine

Volumn 5, Issue 5, 2008, Pages 1097-1113

  Morelli, Annamaria ^a   Marini, Mirca ^a   Mancina, Rosa ^a   Luconi, Michaela ^a   Vignozzi, Linda ^a   Fibbi, Benedetta ^a   Filippi, Sandra ^a   Pezzatini, Anna ^a   Forti, Gianni ^a   Vannelli, Gabriella B ^a   Maggi, Mario ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Human GnRH Neuroblasts; KiSS 1 GPR54; Leptin; Puberty; Sex Steroids

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; ANDROSTANOLONE; ESTROGEN; G PROTEIN COUPLED RECEPTOR 54; GONADORELIN; KISSPEPTIN; LEPTIN; LEPTIN RECEPTOR; LETROZOLE; MESSENGER RNA; SEX HORMONE; TESTOSTERONE;

ADIPOCYTE; AROMATIZATION; ARTICLE; CELL MIGRATION; CONFOCAL MICROSCOPY; FETUS; GENE EXPRESSION REGULATION; GONADOTROPIN SECRETING CELL; GONADOTROPIN SECRETING CELL NEUROBLAST; HORMONAL REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; METABOLISM; OLFACTORY EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PUBERTY; REPRODUCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING;

EID: 42949164617     PISSN: 17436095     EISSN: 17436109     Source Type: Journal    
DOI: 10.1111/j.1743-6109.2008.00782.x     Document Type: Article

References (53)

1. M. Schwanzel-Fukuda D. Bick D.W. Pfaff Luteinizing hormone-releasing hormone (LHRH)-expressing cells do not migrate normally in an inherited hypogonadal (Kallmann) syndrome Brain Res Mol Brain Res 6 1989 311 326
2. W.H. Colledge GPR54 and puberty Trends Endocrinol Metab 15 2004 448 453
3. T. Ohtaki Y. Shintani S. Honda H. Matsumoto A. Hori K. Kanehashi Y. Terao S. Kumano Y. Takatsu Y. Masusa Y. Ishibashi T. Watenabe M. Asada T. Yamada M. Suenaga C. Kitada S. Usuki T. Kurakowa H. Onda O. Nishimura M. Fujino Metastasis suppressor gene KISS-1 encodes peptide ligand of a G-protein-coupled receptor Nature 411 2001 613 617
4. A.I. Muir L. Chamberlain N.A. Elshourbagy D. Michalovich D.J. Moore A. Calamari P.G. Szekeres H.M. Sarau J.K. Chambers P. Murdock K. Steplewski U. Shabon J.E. Miller S.E. Middleton J.G. Darker C.G. Larminie S. Wilson D.J. Bergsma P. Emson R. Faull K.L. Philpott D.C. Harrison AXOR12, a novel human G protein-coupled receptor, activated by the peptide KISS1 J Biol Chem 276 2001 28969 28975
5. M. Kotani M. Detheux A. Vandenbogaerde D. Communi J.M. Vanderwinden E. Le Poul S. Brezillon R. Tyldesley N. Suarex-Huerta F. Vandeput C. Blanpain S.N. Schiffmann G. Vassart M. Parmentier The metastasis suppressor gene KISS1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54 J Biol Chem 276 2001 34631 34636
6. J.H. Lee M.E. Miele D.J. Hicks K.K. Philips J.M. Trent B.E. Weissman D.R. Welch KISS1 , a novel human malignant melanoma metastasis-suppressor gene J Natl Cancer Inst 88 1996 1731 1737
7. J.H. Lee D.R. Welch Suppression of metastasis in human breast carcinoma MDA-MB-435 cells after transfection with the metastasis suppressor gene, KISS1 Cancer Res 57 1997 2384 2387
8. M. Bilban N. Ghaffari-Tabrizi E. Hintermann S. Bauer S. Molzer C. Zoratti R. Malli U. Hiden W. Graier M. Knofler F. Andrete O. Wagner V. Quaranta G. Desoye Kisspeptin-10, a KISS1/metastin-derived decapeptide, is a physiological invasion inhibitor of primary human trophoblasts J Cell Sci 117 2004 1319 1328
9. J.L. Janneau J. Maldonado-Estrada G. Tachdjian I. Miran N. Motte P. Saulnier J.C. Sabourin J.F. Cote B. Simon R. Frydman G. Chaouat D. Bellet Transcriptional expression of genes involved in cell invasion and migration by normal and tumoral trophoblast cells J Clin Endocrinol Metab 87 2002 5336 5339
10. N. De Roux E. Genin J.C. Carel F. Matsuda J.L. Chaussain E. Milgrom Hypogonadotropic hypogonadism due to a loss of function of the KISS1-derived peptide receptor GPR54 Proc Natl Acad Sci USA 100 2003 10972 10976
11. S.B. Seminara S. Messager E.E. Chatzidaki R.R. Thresher J.S. Acierno J.K. Shagoury Y. Bo-Abbas W. Kuohung K.M. Schwinof A.G. Hendrick D. Zahn J. Dixon U.B. Kaiser S.A. Slaugenhaupt J.F. Gusella S. O'Rahilly M.B.L. Carlton W.F. Crowley S.A.J.R. Aparicio W.H. Colledge The GPR54 is a regulator of puberty N Engl J Med 349 2003 1614 1627
12. S. Funes J.A. Hedrick G. Vassileva L. Markowitz S. Abbondanzo A. Golovko S. Yang F.J. Monmsa E.L. Gustafson The KISS1 receptor GPR54 is essential for the development of the murine reproductive system Biochem Biophys Res Commun 312 2003 1357 1363
13. V.M. Navarro J.M. Castellano R. Fernandez-Fernandez M.L. Barreiro J. Roa J.E. Sanchez-Criado E. Aguilar C. Dieguez L. Pinilla M. Tena-Sampere Developmental and hormonally regulated messenger ribonucleic acid expression of Kiss-1 and its putative receptor, GPR54, in rat hypotalamus and potent luteinizing hormone-releasing activity of Kiss-1 peptide Endocrinology 145 2004 4565 4574
14. M.S. Irwig G.S. Fraley J.T. Smith B.V. Acohido S.M. Popa M.J. Cunningham M.L. Gottsch D.K. Clifton R.A. Steiner Kisspeptin activation of gonadotropin releasing hormone neurone and regulation of KISS1 mRNA in the male rat Neuroendocrinology 80 2004 264 272
15. M. Shahab C. Mastronardi S.B. Seminara W.F. Crowley S.R. Ojeda T.M. Plant Increased hypotalamic GPR54 signaling: A potential mechanism for initiation of puberty in primates Proc Natl Acad Sci USA 102 2005 2129 2134
16. J.T. Smith M.J. Cunningham E.F. Rissman D.K. Clifton R.A. Steiner Regulation of Kiss-1 gene expression in the brain of the female mouse Endocrinology 146 2005 3686 3692
17. J.T. Smith H.M. Dungan E.A. Stoll M.L. Gottsch R.E. Braun S.M. Eacker D.K. Clifton R.A. Steiner Differential regulation of Kiss-1 mRNA expression by sex steroids in the brain of the male mouse Endocrinology 146 2005 2976 2984
18. H. Matsui Y. Takatsu S. Kumano H. Matsumoto T. Ohtaki Peripheral administration of metastin induces marked gonadotropin release and ovulation in the rat Biochem Biophys Res Commun 320 2004 383 388
19. M.L. Gottsch M.J. Cunningham J.T. Smith S.M. Popa B.V. Acohido W.F. Crowley S. Seminara D.K. Clifton R.A. Steiner A role of kisspeptin in the regulation of gonadotropin secretion in the mouse Endocrinology 145 2004 4073 4077
20. E.L. Thompson M. Patterson K.G. Murphy K.L. Smith W.S. Dillo J.F. Todd M.A. Ghatei S.R. Bloom Central and peripheral administration of kisspeptin-10 stimulates the hypothalamic–pituitary–gonadal axis J Neuroendocrinol 16 2004 850 858
21. V.M. Navarro J.M. Castellano R. Fernandez-Fernandez S. Tovar J. Roa A. Mayen R. Nogueiras M.J. Vazquez M.L. Barreiro P. Magni E. Aguilar C. Dieguez L. Pinilla M. Tena-Sampere Characterization of the potent luteinizing hormone-releasing activity of KISS-1 peptide, the natural ligand of GPR54 Endocrinology 146 2005 156 163
22. V.M. Navarro J.M. Castellano R. Fernandez-Fernandez S. Tovar J. Roa A. Mayen M.L. Barreiro F.F. Casanueva E. Aguilar C. Dieguez L. Pinilla M. Tena-Sampere Effects of KISS-1 peptide, the natural ligand of GPR54, on follicle-stimulating hormone secretion in the rat Endocrinology 146 2005 1689 1697
23. S. Messager E.E. Chatzidaki D. Ma A.G. Hendrick D. Zahn J. Dixon R.R. Thresher I. Malinge D. Lomet M.B.L. Carlton W.H. Colledge A. Caraty S.A.J.R. Aparicho Kisspeptin directly stimulates gonadotropin releasing hormone release via G protein-coupled receptor 54 Proc Natl Acad Sci USA 102 2005 1761 1766
24. W.S. Dhillo O.B. Chaundhri M. Patterson E.L. Thompson K.G. Murphy M.K. Barman B.M. McGowan V. Amber S. Patel M.A. Ghatei S.R. Bloom Kisspeptin-54 stimulates gonadal axis in human males J Clin Endocrinol Metab 90 2005 6609 6615
25. J. Roa E. Vigo J.M. Castellano V.M. Navarro R. Fernandez-Fernandez F.F. Casanueva C. Dieguez E. Aguilar L. Pinilla M. Tena-Sempere Hypothalamic expression of KiSS-1 system and gonadotropin-releasing effects of kisspeptin in different reproductive states of the female rat Endocrinology 147 2006 2864 2878
26. H.M. Dungan D.K. Clifton R.A. Steiner Minireview: Kisspeptin neurons as central processors in the regulation of gonadotropin-releasing hormone secretion Endocrinology 147 2006 1154 1158
27. G.B. Vannelli E. Ensoli R. Zonefrati Y. Kubota A. Arcangeli A. Becchetti G. Camici T. Barni C.J. Thiele G.C. Balboni Neuroblast long-term cell cultures from human fetal olfactory epithelium respond to odors J Neurosci 15 1995 4382 4394
28. T. Barni M. Maggi G. Fantoni S. Granchi R. Mancina M. Gulisano F. Marra E. Marcosini M. Luconi C.M. Rotella M. Serio G.C. Balboni G.B. Vannelli Sex steroids and odorants modulate gonadotropin-releasing hormone secretion in primary cultures of human olfactory cells J Clin Endocrinol Metab 84 1999 4266 4273
29. F. Ensoli V. Fiorelli B. Vannelli T. Barni M. De Cristofaro B. Ensoli C.J. Thiele Basic fibroblast growth factor supports human olfactory neurogenesis by autocrine/paracrine mechanisms Neuroscience 86 1998 881 893
30. M. Maggi T. Barni G. Fantoni R. Mancina C. Pupilli M. Luconi C. Crescioli M. Serio G.B. Vannelli Expression of biological effects of endothelin-1 in human gonadotropin-releasing hormone-secreting neurons J Clin Endocrinol Metab 85 2000 1658 1665
31. R.G. Romanelli T. Barni M. Maggi M. Luconi P. Failli A. Pezzatini E. Pelo F. Torricelli C. Crescioli P. Ferruzzi R. Salerno M. Marini C.M. Rotella G.B. Vannelli Expression and function of gonadotropin-releasing hormone (GnRH) receptor in human olfactory GnRH-secreting neurons: An autocrine GnRH loop underlies neuronal migration J Biol Chem 279 2004 117 126
32. R.G. Romanelli T. Barni M. Maggi M. Luconi P. Failli A. Pezzatini A. Morelli R. Maggi R. Zaninetti R. Salerno S. Ambrosini M. Marini C.M. Rotella G.B. Vannelli Role of endothelin-1 in the migration of human olfactory gonadotropin-releasing hormone-secreting neuroblasts Endocrinology 146 2005 4321 4330
33. I.J. Clarke B.A. Henry Leptin and reproduction Rev Reprod 4 1999 48 55
34. M.J. Cunningham D.K. Clifton R.A. Steiner Leptin's action on the reproductive axis: Perspectives and mechanisms Biol Reprod 60 1999 216 222
35. D. Gonzalez-Martinez S.H. Kim Y. Hu S. Guimond J. Schofield P. Winyard G.B. Vannelli J. Turnbull P.M. Bouloux Anosmin-1 modulates fibroblast growth factor receptor 1 signaling in human gonadotropin-releasing hormone olfactory neuroblasts through a heparan sulfate-dependent mechanism J Neurosci 24 2004 10384 10392
36. L. Vignozzi S. Filippi M. Luconi A. Morelli R. Mancina M. Marini G.B. Vannelli S. Granchi C. Orlando S. Gelmini F. Ledda G. Forti M. Maggi Oxytocin receptor is expressed in the penis and mediates an estrogen-dependent smooth muscle contractility Endocrinology 145 2004 1823 1834
37. A. De Lean P.J. Munson D. Rodbard Simultaneous analysis of families of sigmoidal curves: Application to biossay, radioligand assay, and physiological dose-response curves Am J Physiol 235 1978 E97
38. M.L. Gottsch D.K. Clifton R.A. Steiner Kisspeptin–GPR54 signaling in the neuroendocrine reproductive axis Mol Cell Endocrinol 254 255 2006 91 96
39. I.S. Parhar S. Ogawa Y. Sakuma Laser-captured single digoxigenin-labeled neurons of gonadotropin-releasing hormone types reveal a novel G protein-coupled receptor (GPR54) during maturation in cichlid fish Endocrinology 45 2004 3613 3618
40. X. D'Anglemont De Tassigny L.A. Fagg J.P. Dixon K. Day H.G. Leitch A.G. Hendrick D. Zahn I. Franceschini A. Caraty M.B. Carlton S.A. Aparicio W.H. Colledge Hypogonadotropic hypogonadism in mice lacking a functional Kiss1 gene Proc Natl Acad Sci USA 104 2007 10714 10719
41. J.T. Smith S.M. Popa D.K. Clifton G.E. Hoffman R.A. Steiner Kiss1 neurons in the forebrain as central processors for generating the preovulatory luteinizing hormone surge J Neurosci 26 2006 6687 6694
42. G.A. Bray J.S. Fisler D.A. York Neuroendicrine control of the development of obesity: Understanding gained from studies of experimental models of obesity Front Neuroendocrinol 4 1990 128 181
43. I.S. Farooqi T. Wangensteen S. Collins W. Kimber G. Matarese J.M. Keogh E. Lank B. Bottomley J. Lopez-Fernandez I. Ferraz-Amaro M.T. Dattani O. Ercan A.G. Myhre L. Retterstol R. Stanhope J.A. Edge S. McKenzie N. Lessan M. Ghodsi V. De Rosa F. Perna S. Fontana I. Barroso D.E. Undlien S. O'Rahilly Clinical and molecular genetic spectrum of congenital deficiency of the leptin receptor N Engl J Med 356 2007 237 247
44. I.S. Farooqi G. Matarese G.M. Lord J.M. Keogh E. Lawrence C. Agwu V. Sanna S.A. Jebb F. Perna S. Fontana R.I. Lechler A.M. DePaoli S. O'Rahilly Beneficial effects of leptin on obesity, T cell hyporesponsiveness, and neuroendocrine/metabolic dysfunction of human congenital leptin deficiency J Clin Invest 110 2002 1093 1103
45. P. Magni R. Vettor C. Pagano A. Calcagno E. Beretta E. Messi M. Zanisi L. Martini M. Motta Expression of a leptin receptor in immortalized gonadotropin-releasing hormone-secreting neurons Endocrinology 140 1999 1581 1585
46. M. Gamba F.P. Pralong Control of GnRH neuronal activity by metabolic factors: The role of leptin and insulin Mol Cell Endocrinol 254 255 2006 133 139
47. J.M. Castellano V.M. Navarro R. Fernandez-Fernandez R. Nogueiras S. Tovar J. Roa M.J. Vazquez E. Vigo F.F. Casanueva E. Aguilar L. Pinilla C. Dieguez M. Tena-Sampere Changes in hypothalamic KISS1 system and restoration of pubertal activation of the reproductive axis by kisspeptin in undernutrition Endocrinology 146 2005 3917 3925
48. V.M. Navarro R. Fernandez-Fernandez J.M. Castellano J. Roa A. Mayen M.L. Barreiro F. Gaytan E. Aguilar C. Dieguez L. Pinilla M. Tena-Sampere Advanced vaginal opening and precocious activation of the reproductive axis by KISS-1 peptide, the endogenous ligand of GPR54 J Physiol 561 2004 379 386
49. J.T. Smith B.V. Acohido D.K. Clifton R.A. Steiner KISS-1 neurones are direct target of leptin in ob/ob mouse J Neuroendocrinol 18 2006 298 303
50. M.M. Grumbach D.M. Styne Puberty: Ontogeny, neuroendocrinology, physiology and disorders Larsen P.R. Kronenberg H.M. Melmed S. Polonsky K.S. Williams textbook of endocrinology 10th edition 2003 Saunders Philadelphia, PA 1115 1286
51. Y. Miwa T. Kaneda O. Yokoyama Correlation between the aging males' symptoms scale and sex steroids, gonadotropins, dehydroepiandrosterone sulfate, and growth hormone levels in ambulatory men J Sex Med 3 2006 723 726
52. N. Pitteloud J.S. Acierno Jr A.U. Meysing A.A. Dwyer F.J. Hayes W.F. Crowley Jr Reversible Kallmann syndrome, delayed puberty, and isolated anosmia occurring in a single family with a mutation in the fibroblast growth factor receptor 1 gene J Clin Endocrinol Metab 90 2005 1317 1322
53. G. Vogel Reproductive biology. A powerful first KiSS-1 Science 309 2005 551 552