Gonadotropin-releasing hormone (GnRH) neuron migration: Initiation, maintenance and cessation as critical steps to ensure normal reproductive function

Frontiers in Neuroendocrinology

Volumn 32, Issue 1, 2011, Pages 43-52

  Wierman, Margaret E ^a,b   Kiseljak Vassiliades, Katja ^a,b   Tobet, Stuart ^c  

^a UCD   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

G protein coupled receptors; GnRH; Neuronal migration; Receptor kinases; Reproduction

Indexed keywords

4 AMINOBUTYRIC ACID; CELL SURFACE PROTEIN; CHEMOKINE RECEPTOR CXCR4; CHOLECYSTOKININ; EPHRIN; FIBROBLAST GROWTH FACTOR 8; FIBROBLAST GROWTH FACTOR RECEPTOR 1; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 54; GONADORELIN; GROWTH FACTOR; HELIX LOOP HELIX PROTEIN; KISSPEPTIN; NETRIN 1; NEUROPILIN 2; NEUROTRANSMITTER; PLEXIN; PROKINETICIN 2 RECEPTOR; PROTEIN AXL; PROTEIN NHLH2; PROTEIN TYROSINE KINASE; PROTEINTYRO3; REELIN; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; SEMAPHORIN; STROMAL CELL DERIVED FACTOR 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EBF2; UNCLASSIFIED DRUG;

CELL MIGRATION; CELLULAR DISTRIBUTION; CHILD DEVELOPMENT; DEVELOPMENTAL STAGE; EMBRYO DEVELOPMENT; FOREBRAIN; GENE MUTATION; GENE OVEREXPRESSION; GENE SILENCING; GONADOTROPIN RELEASING HORMONE NEURON; GONADOTROPIN SECRETING CELL; HORMONE ACTION; HORMONE DEFICIENCY; HUMAN; HYPOGONADOTROPIC HYPOGONADISM; HYPOPHYSIS GONAD SYSTEM; HYPOTHALAMUS; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; PUBERTY; REPRODUCTION; REVIEW; VOMERONASAL ORGAN;

ANIMALS; CELL MOVEMENT; GONADOTROPIN-RELEASING HORMONE; HUMANS; MICE; MODELS, BIOLOGICAL; NEUROGENESIS; NEURONS; OLFACTORY PATHWAYS; REPRODUCTION;

EID: 78651413983     PISSN: 00913022     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yfrne.2010.07.005     Document Type: Review

References (122)

1. Albuisson J., Pecheux C., Carel J.C., Lacombe D., Leheup B., Lapuzina P., Bouchard P., Legius E., Matthijs G., Wasniewska M., Delpech M., Young J., Hardelin J.P., Dode C. Kallmann syndrome: 14 novel mutations in KAL1 and FGFR1 (KAL2). Hum. Mutat. 2005, 25:98-99.
2. Allen M.P., Zeng C., Schneider K., Xiong X., Meintzer M.K., Bellosta P., Basilico C., Varnum B., Heidenreich K.A., Wierman M.E. Growth arrest-specific gene 6 (Gas6)/adhesion related kinase (Ark) signaling promotes gonadotropin-releasing hormone neuronal survival via extracellular signal-regulated kinase (ERK) and Akt. Mol. Endocrinol. 1999, 13:191-201.
3. Allen M.P., Linseman D.A., Udo H., Xu M., Schaack J.B., Varnum B., Kandel E.R., Heidenreich K.A., Wierman M.E. Novel mechanism for gonadotropin-releasing hormone neuronal migration involving Gas6/Ark signaling to p38 mitogen-activated protein kinase. Mol. Cell. Biol. 2002, 22:599-613.
4. Ballabio A., Camerino G. The gene for X-linked Kallmann syndrome: a human neuronal migration defect. Curr. Opin. Genet. Dev. 1992, 2:417-421.
5. Belmadani A., Tran P.B., Ren D., Assimacopoulos S., Grove E.A., Miller R.J. The chemokine stromal cell-derived factor-1 regulates the migration of sensory neuron progenitors. J. Neurosci. 2005, 25:3995-4003.
6. Bennett K.L., Bradshaw J., Youngman T., Rodgers J., Greenfield B., Aruffo A., Linsley P.S. Deleted in colorectal carcinoma (DCC) binds heparin via its fifth fibronectin type III domain. J. Biol. Chem. 1997, 272:26940-26946.
7. Bilban M., Ghaffari-Tabrizi N., Hintermann E., Bauer S., Molzer S., Zoratti C., Malli R., Sharabi A., Hiden U., Graier W., Knofler M., Andreae F., Wagner O., Quaranta V., Desoye G. Kisspeptin-10, a KiSS-1/metastin-derived decapeptide, is a physiological invasion inhibitor of primary human trophoblasts. J. Cell. Sci. 2004, 117:1319-1328.
8. Bless E.P., Westaway W.A., Schwarting G.A., Tobet S.A. Effects of gamma-aminobutyric acid(A) receptor manipulation on migrating gonadotropin-releasing hormone neurons through the entire migratory route in vivo and in vitro. Endocrinology 2000, 141:1254-1262.
9. Bless E.P., Walker H.J., Yu K.W., Knoll J.G., Moenter S.M., Schwarting G.A., Tobet S.A. Live view of gonadotropin-releasing hormone containing neuron migration. Endocrinology 2005, 146:463-468.
10. Bless E., Raitcheva D., Henion T.R., Tobet S., Schwarting G.A. Lactosamine modulates the rate of migration of GnRH neurons during mouse development. Eur. J. Neurosci. 2006, 24:654-660.
11. Cariboni A., Pimpinelli F., Colamarino S., Zaninetti R., Piccolella M., Rumio C., Piva F., Rugarli E.I., Maggi R. The product of X-linked Kallmann's syndrome gene (KAL1) affects the migratory activity of gonadotropin-releasing hormone (GnRH)-producing neurons. Hum. Mol. Genet. 2004, 13:2781-2791.
12. Cariboni A., Rakic S., Liapi A., Maggi R., Goffinet A., Parnavelas J.G. Reelin provides an inhibitory signal in the migration of gonadotropin-releasing hormone neurons. Development 2005, 132:4709-4718.
13. Cariboni A., Maggi R., Parnavelas J.G. From nose to fertility: the long migratory journey of gonadotropin-releasing hormone neurons. Trends Neurosci. 2007, 30:638-644.
14. Cariboni A., Hickok J., Rakic S., Andrews W., Maggi R., Tischkau S., Parnavelas J.G. Neuropilins and their ligands are important in the migration of gonadotropin-releasing hormone neurons. J. Neurosci. 2007, 27:2387-2395.
15. Catalano P.N., Di Giorgio N., Bonaventura M.M., Bettler B., Libertun C., Lux-Lantos V.A. Lack of functional GABA(B) receptors alters GnRH physiology and sexual dimorphic expression of GnRH and GAD-67 in the brain. Am. J. Physiol. Endocrinol. Metab. 2010, 298:E683-E696.
16. Catalano P.N., Bonaventura M.M., Silveyra P., Bettler B., Libertun C., Lux-Lantos V.A. GABA(B1) knockout mice reveal alterations in prolactin levels, gonadotropic axis, and reproductive function. Neuroendocrinology 2005, 82:294-305.
17. Caviness V.S., So D.K., Sidman R.L. The hybrid reeler mouse. J. Hered. 1972, 63:241-246.
18. Cheng M.Y., Bullock C.M., Li C., Lee A.G., Bermak J.C., Belluzzi J., Weaver D.R., Leslie F.M., Zhou Q.Y. Prokineticin 2 transmits the behavioural circadian rhythm of the suprachiasmatic nucleus. Nature 2002, 417:405-410.
19. Ciofi P., Garret M., Lapirot O., Lafon P., Loyens A., Prevot V., Levine J.E. Brain-endocrine interactions: a microvascular route in the mediobasal hypothalamus. Endocrinology 2009, 150:5509-5519.
20. Cogliati T., Delgado-Romero P., Norwitz E.R., Guduric-Fuchs J., Kaiser U.B., Wray S., Kirsch I.R. Pubertal impairment in Nhlh2 null mice is associated with hypothalamic and pituitary deficiencies. Mol. Endocrinol. 2007, 21:3013-3027.
21. Cole L.W., Sidis Y., Zhang C., Quinton R., Plummer L., Pignatelli D., Hughes V.A., Dwyer A.A., Raivio T., Hayes F.J., Seminara S.B., Huot C., Alos N., Speiser P., Takeshita A., Van Vliet G., Pearce S., Crowley W.F., Zhou Q.Y., Pitteloud N. Mutations in prokineticin 2 and prokineticin receptor 2 genes in human gonadotrophin-releasing hormone deficiency: molecular genetics and clinical spectrum. J. Clin. Endocrinol. Metab. 2008, 93:3551-3559.
22. Corradi A., Croci L., Broccoli V., Zecchini S., Previtali S., Wurst W., Amadio S., Maggi R., Quattrini A., Consalez G.G. Hypogonadotropic hypogonadism and peripheral neuropathy in Ebf2-null mice. Development 2003, 130:401-410.
23. Daniel D., Rossel M., Seki T., Konig N. Stromal cell-derived factor-1 (SDF-1) expression in embryonic mouse cerebral cortex starts in the intermediate zone close to the pallial-subpallial boundary and extends progressively towards the cortical hem. Gene Expr. Patterns 2005, 5:317-322.
24. de Seranno S., d'Anglemont de Tassigny X., Estrella C., Loyens A., Kasparov S., Leroy D., Ojeda S.R., Beauvillain J.C., Prevot V. Role of estradiol in the dynamic control of tanycyte plasticity mediated by vascular endothelial cells in the median eminence. Endocrinology 2010, 151:1760-1772.
25. Deng C.X., Wynshaw-Boris A., Shen M.M., Daugherty C., Ornitz D.M., Leder P. Murine FGFR-1 is required for early postimplantation growth and axial organization. Genes Dev. 1994, 8:3045-3057.
26. Dode C., Hardelin J.P. Kallmann syndrome: fibroblast growth factor signaling insufficiency?. J. Mol. Med. 2004, 82:725-734.
27. Dode C., Teixeira L., Levilliers J., Fouveaut C., Bouchard P., Kottler M.L., Lespinasse J., Lienhardt-Roussie A., Mathieu M., Moerman A., Morgan G., Murat A., Toublanc J.E., Wolczynski S., Delpech M., Petit C., Young J., Hardelin J.P. Kallmann syndrome: mutations in the genes encoding prokineticin-2 and prokineticin receptor-2. PLoS Genet. 2006, 2:e175.
28. Dubois L., Vincent A. The COE-Collier/Olf1/EBF - transcription factors: structural conservation and diversity of developmental functions. Mech. Dev. 2001, 108:3-12.
29. Ebens A., Brose K., Leonardo E.D., Hanson M.G., Bladt F., Birchmeier C., Barres B.A., Tessier-Lavigne M. Hepatocyte growth factor/scatter factor is an axonal chemoattractant and a neurotrophic factor for spinal motor neurons. Neuron 1996, 17:1157-1172.
30. Falardeau J., Chung W.C., Beenken A., Raivio T., Plummer L., Sidis Y., Jacobson-Dickman E.E., Eliseenkova A.V., Ma J., Dwyer A., Quinton R., Na S., Hall J.E., Huot C., Alois N., Pearce S.H., Cole L.W., Hughes V., Mohammadi M., Tsai P., Pitteloud N. Decreased FGF8 signaling causes deficiency of gonadotropin-releasing hormone in humans and mice. J. Clin. Invest. 2008, 118:2822-2831.
31. Fang Z., Xiong X., James A., Gordon D.F., Wierman M.E. Identification of novel factors that regulate GnRH gene expression and neuronal migration. Endocrinology 1998, 139:3654-3657.
32. Ferrara N., LeCouter J., Lin R., Peale F. EG-VEGF and Bv8: a novel family of tissue-restricted angiogenic factors. Biochim. Biophys. Acta 2004, 1654:69-78.
33. Franco B., Guioli S., Pragliola A., Incerti B., Bardoni B., Tonlorenzi R., Carrozzo R., Maestrini E., Pieretti M., Taillon-Miller P., et al. A gene deleted in Kallmann's syndrome shares homology with neural cell adhesion and axonal path-finding molecules. Nature 1991, 353:529-536.
34. Fueshko S.M., Key S., Wray S. GABA inhibits migration of luteinizing hormone-releasing hormone neurons in embryonic olfactory explants. J. Neurosci. 1998, 18:2560-2569.
35. Gamble J.A., Karunadasa D.K., Pape J.R., Skynner M.J., Todman M.G., Bicknell R.J., Allen J.P., Herbison A.E. Disruption of ephrin signaling associates with disordered axophilic migration of the gonadotropin-releasing hormone neurons. J. Neurosci. 2005, 25:3142-3150.
36. Giacobini P., Wray S. Cholecystokinin directly inhibits neuronal activity of primary gonadotropin-releasing hormone cells through cholecystokinin-1 receptor. Endocrinology 2007, 148:63-71.
37. Giacobini P., Giampietro C., Fioretto M., Maggi R., Cariboni A., Perroteau I., Fasolo A. Hepatocyte growth factor/scatter factor facilitates migration of GN-11 immortalized LHRH neurons. Endocrinology 2002, 143:3306-3315.
38. Giacobini P., Kopin A.S., Beart P.M., Mercer L.D., Fasolo A., Wray S. Cholecystokinin modulates migration of gonadotropin-releasing hormone-1 neurons. J. Neurosci. 2004, 24:4737-4748.
39. Giacobini P., Messina A., Wray S., Giampietro C., Crepaldi T., Carmeliet P., Fasolo A. Hepatocyte growth factor acts as a motogen and guidance signal for gonadotropin hormone-releasing hormone-1 neuronal migration. J. Neurosci. 2007, 27:431-445.
40. Giacobini P., Messina A., Morello F., Ferraris N., Corso S., Penachioni J., Giordano S., Tamagnone L., Fasolo A. Semaphorin 4D regulates gonadotropin hormone-releasing hormone-1 neuronal migration through Plexin B1-Met complex. J. Cell Biol. 2008, 183:555-566.
41. Giger R.J., Cloutier J.F., Sahay A., Prinjha R.K., Levengood D.V., Moore S.E., Pickering S., Simmons D., Rastan S., Walsh F.S., Kolodkin A.L., Ginty D.D., Geppert M. Neuropilin-2 is required in vivo for selective axon guidance responses to secreted semaphorins. Neuron 2000, 25:29-41.
42. Gill J.C., Tsai P.S. Expression of a dominant negative FGF receptor in developing GNRH1 neurons disrupts axon outgrowth and targeting to the median eminence. Biol. Reprod. 2006, 74:463-472.
43. Gonzalez-Martinez D., Kim S.H., Hu Y., Guimond S., Schofield J., Winyard P., Vannelli G.B., Turnbull J., Bouloux P.M. Anosmin-1 modulates fibroblast growth factor receptor 1 signaling in human gonadotropin-releasing hormone olfactory neuroblasts through a heparan sulfate-dependent mechanism. J. Neurosci. 2004, 24:10384-10392.
44. Good D.J., Porter F.D., Mahon K.A., Parlow A.F., Westphal H., Kirsch I.R. Hypogonadism and obesity in mice with a targeted deletion of the Nhlh2 gene. Nat. Genet. 1997, 15:397-401.
45. Heger S., Seney M., Bless E., Schwarting G.A., Bilger M., Mungenast A., Ojeda S.R., Tobet S.A. Overexpression of glutamic acid decarboxylase-67 (GAD-67) in gonadotropin-releasing hormone neurons disrupts migratory fate and female reproductive function in mice. Endocrinology 2003, 144:2566-2579.
46. Herbison A.E., Porteous R., Pape J.R., Mora J.M., Hurst P.R. Gonadotropin-releasing hormone neuron requirements for puberty, ovulation, and fertility. Endocrinology 2008, 149:597-604.
47. Hori A., Honda S., Asada M., Ohtaki T., Oda K., Watanabe T., Shintani Y., Yamada T., Suenaga M., Kitada C., Onda H., Kurokawa T., Nishimura O., Fujino M. Metastin suppresses the motility and growth of CHO cells transfected with its receptor. Biochem. Biophys. Res. Commun. 2001, 286:958-963.
48. Hudson M.L., Kinnunen T., Cinar H.N., Chisholm A.D. C. elegans Kallmann syndrome protein KAL-1 interacts with syndecan and glypican to regulate neuronal cell migrations. Dev. Biol. 2006, 294:352-365.
49. Ieraci A., Forni P.E., Ponzetto C. Viable hypomorphic signaling mutant of the Met receptor reveals a role for hepatocyte growth factor in postnatal cerebellar development. Proc. Natl. Acad. Sci. USA 2002, 99:15200-15205.
50. Jay P., Rougeulle C., Massacrier A., Moncla A., Mattei M.G., Malzac P., Roeckel N., Taviaux S., Lefranc J.L., Cau P., Berta P., Lalande M., Muscatelli F. The human necdin gene, NDN, is maternally imprinted and located in the Prader-Willi syndrome chromosomal region. Nat. Genet. 1997, 17:357-361.
51. Kastenhuber E., Kern U., Bonkowsky J.L., Chien C.B., Driever W., Schweitzer J. Netrin-DCC, Robo-Slit, and heparan sulfate proteoglycans coordinate lateral positioning of longitudinal dopaminergic diencephalospinal axons. J. Neurosci. 2009, 29:8914-8926.
52. Kauffman A. Coming of age in the Kisspeptin Era: sex differences, development and puberty. Mol. Cell. Endocrinol. 2010, 324:51-63.
53. Kawauchi S., Shou J., Santos R., Hebert J.M., McConnell S.K., Mason I., Calof A.L. FGF8 expression defines a morphogenetic center required for olfactory neurogenesis and nasal cavity development in the mouse. Development 2005, 132:5211-5223.
54. Kim S.H., Hu Y., Cadman S., Bouloux P. Diversity in fibroblast growth factor receptor 1 regulation: learning from the investigation of Kallmann syndrome. J. Neuroendocrinol. 2008, 20:141-163.
55. Klein R.S., Rubin J.B., Gibson H.D., DeHaan E.N., Alvarez-Hernandez X., Segal R.A., Luster A.D. SDF-1 alpha induces chemotaxis and enhances Sonic hedgehog-induced proliferation of cerebellar granule cells. Development 2001, 128:1971-1981.
56. J.G. Knoll, T. Henion, G.A. Schwarting, S.A. Tobet, Sex differences in kisspeptin mRNA expression during murine development, Endocrine Society, San Francisco, CA P1-680, 2008.
57. Knox AJ X.M., Plummer L., Slavov D., Taylor D., Pitteloud N., Crowley W.F., Wierman M.E. Analysis of Mutations in Axl and Tyro3 in Probands with Kallman Syndrome and Idiopathic Hypogonadotropic Hypogonadism 2009, The Endocrine Society Meeting, Washington, DC.
58. Kramer P.R., Wray S. Novel gene expressed in nasal region influences outgrowth of olfactory axons and migration of luteinizing hormone-releasing hormone (LHRH) neurons. Genes Dev. 2000, 14:1824-1834.
59. Lai C., Lemke G. An extended family of protein-tyrosine kinase genes differentially expressed in the vertebrate nervous system. Neuron 1991, 6:691-704.
60. LeCouter J., Lin R., Tejada M., Frantz G., Peale F., Hillan K.J., Ferrara N. The endocrine-gland-derived VEGF homologue Bv8 promotes angiogenesis in the testis: localization of Bv8 receptors to endothelial cells. Proc. Natl. Acad. Sci. USA 2003, 100:2685-2690.
61. Lee J.M., Tiong J., Maddox D.M., Condie B.G., Wray S. Temporal migration of gonadotrophin-releasing hormone-1 neurones is modified in GAD67 knockout mice. J. Neuroendocrinol. 2008, 20:93-103.
62. Legouis R., Hardelin J.P., Levilliers J., Claverie J.M., Compain S., Wunderle V., Millasseau P., Le Paslier D., Cohen D., Caterina D., et al. The candidate gene for the X-linked Kallmann syndrome encodes a protein related to adhesion molecules. Cell 1991, 67:423-435.
63. Lemke G., Rothlin C.V. Immunobiology of the TAM receptors. Nat. Rev. Immunol. 2008, 8:327-336.
64. Li M., Bullock C.M., Knauer D.J., Ehlert F.J., Zhou Q.Y. Identification of two prokineticin cDNAs: recombinant proteins potently contract gastrointestinal smooth muscle. Mol. Pharmacol. 2001, 59:692-698.
65. Linger R.M.A., Keating A.K., Earp H.S., Graham D.K. TAM receptor tyrosine kinases: biologic functions, signaling, and potential therapeutic targeting in human cancer. Adv. Cancer. Res. 2008, 100:35-83.
66. Lutz B., Kuratani S., Rugarli E.I., Wawersik S., Wong C., Bieber F.R., Ballabio A., Eichele G. Expression of the Kallmann syndrome gene in human fetal brain and in the manipulated chick embryo. Hum. Mol. Genet. 1994, 3:1717-1723.
67. Ma Q., Jones D., Borghesani P.R., Segal R.A., Nagasawa T., Kishimoto T., Bronson R.T., Springer T.A. Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc. Natl. Acad. Sci. USA 1998, 95:9448-9453.
68. MacDonald H.R., Wevrick R. The necdin gene is deleted in Prader-Willi syndrome and is imprinted in human and mouse. Hum. Mol. Genet. 1997, 6:1873-1878.
69. Maina F., Hilton M.C., Ponzetto C., Davies A.M., Klein R. Met receptor signaling is required for sensory nerve development and HGF promotes axonal growth and survival of sensory neurons. Genes Dev. 1997, 11:3341-3350.
70. Matsumoto S., Yamazaki C., Masumoto K.H., Nagano M., Naito M., Soga T., Hiyama H., Matsumoto M., Takasaki J., Kamohara M., Matsuo A., Ishii H., Kobori M., Katoh M., Matsushime H., Furuichi K., Shigeyoshi Y. Abnormal development of the olfactory bulb and reproductive system in mice lacking prokineticin receptor PKR2. Proc. Natl. Acad. Sci. USA 2006, 103:4140-4145.
71. Meyers E.N., Lewandoski M., Martin G.R. An FGF8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat. Genet. 1998, 18:136-141.
72. Miller N.L., Wevrick R., Mellon P.L. Necdin, a Prader-Willi syndrome candidate gene, regulates gonadotropin-releasing hormone neurons during development. Hum. Mol. Genet. 2009, 18:248-260.
73. Miura K., Acierno J.S., Seminara S.B. Characterization of the human nasal embryonic LHRH factor gene, NELF, and a mutation screening among 65 patients with idiopathic hypogonadotropic hypogonadism (IHH). J. Hum. Genet. 2004, 49:265-268.
74. Monnier C., Dode C., Fabre L., Teixeira L., Labesse G., Pin J.P., Hardelin J.P., Rondard P. PROKR2 missense mutations associated with Kallmann syndrome impair receptor signalling activity. Hum. Mol. Genet. 2009, 18:75-81.
75. Murakami S., Arai Y. Migration of LHRH neurons into the spinal cord: evidence for axon-dependent migration from the transplanted chick olfactory placode. Eur. J. Neurosci. 2002, 16:684-692.
76. Muscatelli F., Abrous D.N., Massacrier A., Boccaccio I., Le Moal M., Cau P., Cremer H. Disruption of the mouse necdin gene results in hypothalamic and behavioral alterations reminiscent of the human Prader-Willi syndrome. Hum. Mol. Genet. 2000, 9:3101-3110.
77. Ng K.L., Li J.D., Cheng M.Y., Leslie F.M., Lee A.G., Zhou Q.Y. Dependence of olfactory bulb neurogenesis on prokineticin 2 signaling. Science 2005, 308:1923-1927.
78. Ohtaki T., Shintani Y., Honda S., Matsumoto H., Hori A., Kanehashi K., Terao Y., Kumano S., Takatsu Y., Masuda Y., Ishibashi Y., Watanabe T., Asada M., Yamada T., Suenaga M., Kitada C., Usuki S., Kurokawa T., Onda H., Nishimura O., Fujino M. Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature 2001, 411:613-617.
79. Oliveira L.M., Seminara S.B., Beranova M., Hayes F.J., Valkenburgh S.B., Schipani E., Costa E.M., Latronico A.C., Crowley W.F., Vallejo M. The importance of autosomal genes in Kallmann syndrome: genotype-phenotype correlations and neuroendocrine characteristics. J. Clin. Endocrinol. Metab. 2001, 86:1532-1538.
80. Oro A.E., Simerly R.B., Swanson L.W. Estrous cycle variations in levels of cholecystokinin immunoreactivity within cells of three interconnected sexually dimorphic forebrain nuclei. Evidence for a regulatory role for estrogen. Neuroendocrinology 1988, 47:225-235.
81. Pallais J.C., Bo-Abbas Y., Pitteloud N., Crowley W.F., Seminara S.B. Neuroendocrine, gonadal, placental, and obstetric phenotypes in patients with IHH and mutations in the G-protein coupled receptor, GPR54. Mol. Cell. Endocrinol. 2006, 254-255:70-77.
82. Pallais J.C., Au M., Pitteloud N., Seminara S., Crowley W.F. Kallman Syndrome 2010, University of Washington, Seattle Washington.
83. Peng H., Huang Y., Rose J., Erichsen D., Herek S., Fujii N., Tamamura H., Zheng J. Stromal cell-derived factor 1-mediated CXCR4 signaling in rat and human cortical neural progenitor cells. J. Neurosci. Res. 2004, 76:35-50.
84. Pierce A., Bliesner B., Xu M., Nielsen-Preiss S., Lemke G., Tobet S., Wierman M.E. Axl and Tyro3 modulate female reproduction by influencing gonadotropin-releasing hormone neuron survival and migration. Mol. Endocrinol. 2008, 22:2481-2495.
85. Pierce A.B.B., Xu M., Tobet S., Lemke G., Wierman M.E. Axl and Tyro3 regulate GnRH Neuron Migration and Modulate Female Reproductive Function 2008, The Endocrine Society Meeting, San Francisco California.
86. Pitteloud N., Meysing A., Quinton R., Acierno J.S., Dwyer A.A., Plummer L., Fliers E., Boepple P., Hayes F., Seminara S., Hughes V.A., Ma J., Bouloux P., Mohammadi M., Crowley W.F. Mutations in fibroblast growth factor receptor 1 cause Kallmann syndrome with a wide spectrum of reproductive phenotypes. Mol. Cell. Endocrinol. 2006, 254-255:60-69.
87. Pitteloud N., Quinton R., Pearce S., Raivio T., Acierno J., Dwyer A., Plummer L., Hughes V., Seminara S., Cheng Y.Z., Li W.P., Maccoll G., Eliseenkova A.V., Olsen S.K., Ibrahimi O.A., Hayes F.J., Boepple P., Hall J.E., Bouloux P., Mohammadi M., Crowley W. Digenic mutations account for variable phenotypes in idiopathic hypogonadotropic hypogonadism. J. Clin. Invest. 2007, 117:457-463.
88. Pitteloud N., Zhang C., Pignatelli D., Li J.D., Raivio T., Cole L.W., Plummer L., Jacobson-Dickman E.E., Mellon P.L., Zhou Q.Y., Crowley W.F. Loss-of-function mutation in the prokineticin 2 gene causes Kallmann syndrome and normosmic idiopathic hypogonadotropic hypogonadism. Proc. Natl. Acad. Sci. USA 2007, 104:17447-17452.
89. Plant T.M. The role of KiSS-1 in the regulation of puberty in higher primates. Eur. J. Endocrinol. 2006, 155(Suppl. 1):S11-S16.
90. Rugarli E.I. Kallmann syndrome and the link between olfactory and reproductive development. Am. J. Hum. Genet. 1999, 65:943-948.
91. Rugarli E.I., Di Schiavi E., Hilliard M.A., Arbucci S., Ghezzi C., Facciolli A., Coppola G., Ballabio A., Bazzicalupo P. The Kallmann syndrome gene homolog in C. elegans is involved in epidermal morphogenesis and neurite branching. Development 2002, 129:1283-1294.
92. Schwanzel-Fukuda M., Pfaff D.W. Origin of luteinizing hormone-releasing hormone neurons. Nature 1989, 338:161-164.
93. Schwanzel-Fukuda M., Bick D., Pfaff D.W. Luteinizing hormone-releasing hormone (LHRH)-expressing cells do not migrate normally in an inherited hypogonadal (Kallmann) syndrome. Brain Res. Mol. Brain Res. 1989, 6:311-326.
94. Schwarting G.A., Kostek C., Bless E.P., Ahmad N., Tobet S.A. Deleted in colorectal cancer (DCC) regulates the migration of luteinizing hormone-releasing hormone neurons to the basal forebrain. J. Neurosci. 2001, 21:911-919.
95. Schwarting G.A., Raitcheva D., Bless E.P., Ackerman S.L., Tobet S. Netrin 1-mediated chemoattraction regulates the migratory pathway of LHRH neurons. Eur. J. Neurosci. 2004, 19:11-20.
96. Schwarting G.A., Henion T.R., Nugent J.D., Caplan B., Tobet S. Stromal cell-derived factor-1 (chemokine C-X-C motif ligand 12) and chemokine C-X-C motif receptor 4 are required for migration of gonadotropin-releasing hormone neurons to the forebrain. J. Neurosci. 2006, 26:6834-6840.
97. Seeburg P.H., Mason A.J., Stewart T.A., Nikolics K. The mammalian GnRH gene and its pivotal role in reproduction. Recent Prog. Horm. Res. 1987, 43:69-98.
98. Seminara S.B. Converging at puberty's hub. Endocrinology 2007, 148:5145-5146.
99. Seminara S.B., Messager S., Chatzidaki E.E., Thresher R.R., Acierno 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 W.F., Aparicio S.A., Colledge W.H. The GPR54 gene as a regulator of puberty. N. Engl. J. Med. 2003, 349:1614-1627.
100. Silveira L.F., Trarbach E.B., Latronico A.C. Genetics basis for GnRH-dependent pubertal disorders in humans. Mol. Cell. Endocrinol. 2010, 324:30-38.
101. Teles M.G., Trarbach E.B., Noel S.D., Guerra-Junior G., Jorge A., Beneduzzi D., Bianco S.D., Mukherjee A., Baptista M.T., Costa E.M., De Castro M., Mendonca B.B., Kaiser U.B., Latronico A.C. A novel homozygous splice acceptor site mutation of KISS1R in two siblings with normosmic isolated hypogonadotropic hypogonadism. Eur. J. Endocrinol. 2010, 163:29-34.
102. Tena-Sempere M. GPR54 and kisspeptin in reproduction. Hum. Reprod. Update 2006, 12:631-639.
103. Tissir F., Wang C.E., Goffinet A.M. Expression of the chemokine receptor Cxcr4 mRNA during mouse brain development. Brain Res. Dev. Brain Res. 2004, 149:63-71.
104. Toba Y., Tiong J.D., Ma Q., Wray S. CXCR4/SDF-1 system modulates development of GnRH-1 neurons and the olfactory system. Dev. Neurobiol. 2008, 68:487-503.
105. Tobet S.A., Schwarting G.A. Minireview: recent progress in gonadotropin-releasing hormone neuronal migration. Endocrinology 2006, 147:1159-1165.
106. Tobet S.A., Chickering T.W., King J.C., Stopa E.G., Kim K., Kuo-Leblank V., Schwarting G.A. Expression of gamma-aminobutyric acid and gonadotropin-releasing hormone during neuronal migration through the olfactory system. Endocrinology 1996, 137:5415-5420.
107. Tobet S.A., Bless E.P., Schwarting G.A. Developmental aspect of the gonadotropin-releasing hormone system. Mol. Cell Endocrinol. 2001, 185:173-184.
108. Todman M.G., Han S.K., Herbison A.E. Profiling neurotransmitter receptor expression in mouse gonadotropin-releasing hormone neurons using green fluorescent protein-promoter transgenics and microarrays. Neuroscience 2005, 132:703-712.
109. Trarbach E.B., Baptista M.T., Garmes H.M., Hackel C. Molecular analysis of KAL-1, GnRH-R, NELF and EBF2 genes in a series of Kallmann syndrome and normosmic hypogonadotropic hypogonadism patients. J. Endocrinol. 2005, 187:361-368.
110. Tsai P.S., Gill J.C. Mechanisms of disease: insights into X-linked and autosomal-dominant Kallmann syndrome. Nat. Clin. Pract. Endocrinol. Metab. 2006, 2:160-171.
111. Tsai P.S., Moenter S.M., Postigo H.R., El Majdoubi M., Pak T.R., Gill J.C., Paruthiyil S., Werner S., Weiner R.I. Targeted expression of a dominant-negative fibroblast growth factor (FGF) receptor in gonadotropin-releasing hormone (GnRH) neurons reduces FGF responsiveness and the size of GnRH neuronal population. Mol. Endocrinol. 2005, 19:225-236.
112. Vanderhaeghen J.J., Signeau J.C., Gepts W. New peptide in the vertebrate CNS reacting with antigastrin antibodies. Nature 1975, 257:604-605.
113. Vijayan E., Samson W.K., McCann S.M. In vivo and in vitro effects of cholecystokinin on gonadotropin, prolactin, growth hormone and thyrotropin release in the rat. Brain Res. 1979, 172:295-302.
114. Wierman M.E., Pawlowski J.E., Allen M.P., Xu M., Linseman D.A., Nielsen-Preiss S. Molecular mechanisms of gonadotropin-releasing hormone neuronal migration. Trends Endocrinol. Metab. 2004, 15:96-102.
115. Wray S., Hoffman G. Postnatal morphological changes in rat LHRH neurons correlated with sexual maturation. Neuroendocrinology 1986, 43:93-97.
116. Wray S., Grant P., Gainer H. Evidence that cells expressing luteinizing hormone-releasing hormone mRNA in the mouse are derived from progenitor cells in the olfactory placode. Proc. Natl. Acad. Sci. USA 1989, 86:8132-8136.
117. Xu N., Bhagavath B., Kim H.G., Halvorson L., Podolsky R.S., Chorich L.P., Prasad P., Xiong W.C., Cameron R.S., Layman L.C. NELF is a nuclear protein involved in hypothalamic GnRH neuronal migration. Mol. Cell Endocrinol. 2009.
118. Yamaguchi T.P., Harpal K., Henkemeyer M., Rossant J. Fgfr-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation. Genes Dev. 1994, 8:3032-3044.
119. Yoshida K., Tobet S.A., Crandall J.E., Jimenez T.P., Schwarting G.A. The migration of luteinizing hormone-releasing hormone neurons in the developing rat is associated with a transient, caudal projection of the vomeronasal nerve. J. Neurosci. 1995, 15:7769-7777.
120. Yoshida K., Rutishauser U., Crandall J.E., Schwarting G.A. Polysialic acid facilitates migration of luteinizing hormone-releasing hormone neurons on vomeronasal axons. J. Neurosci. 1999, 19:794-801.
121. Zhu Y., Yu T., Zhang X.C., Nagasawa T., Wu J.Y., Rao Y. Role of the chemokine SDF-1 as the meningeal attractant for embryonic cerebellar neurons. Nat. Neurosci. 2002, 5:719-720.
122. Zou Y.R., Kottmann A.H., Kuroda M., Taniuchi I., Littman D.R. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 1998, 393:595-599.