Minireview: Recent progress in gonadotropin-releasing hormone neuronal migration

Endocrinology

Volumn 147, Issue 3, 2006, Pages 1159-1165

  Tobet, Stuart A ^a   Schwarting, Gerald A ^a,b  

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

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GONADORELIN;

BRAIN; CELL MIGRATION; CELL POPULATION; FOREBRAIN; GANGLION; HORMONE SYNTHESIS; HUMAN; MOLECULAR DYNAMICS; NERVE CELL MEMBRANE; NONHUMAN; OLFACTORY SYSTEM; PHENOTYPE; PRIORITY JOURNAL; SHORT SURVEY; SIGNAL TRANSDUCTION; SURFACE PROPERTY;

ANIMALS; BRAIN; CELL MOVEMENT; CYTOSKELETON; GONADOTROPIN-RELEASING HORMONE; HUMANS; MICE; MODELS, BIOLOGICAL; NEURAL PATHWAYS; NEURONS; OLFACTORY BULB; OLFACTORY PATHWAYS; PHENOTYPE; PROSENCEPHALON; SIGNAL TRANSDUCTION;

EID: 32644439915     PISSN: 00137227     EISSN: None     Source Type: Journal    
DOI: 10.1210/en.2005-1275     Document Type: Short Survey

References (91)

1. Schwanzel-Fukuda M, Pfaff DW 1989 Origin of luteinizing hormone-releasing hormone neurons. Nature 338:161-164
2. Wray S, Grant P, Gainer H 1989 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 86:8132-8136
3. King JC, Sower SA, Anthony EL 1988 Neuronal systems immunoreactive with antiserum to lamprey gonadotropin-releasing hormone in the brain of Petromyzon marinus. Cell Tissue Res 253:1-8
4. Tobet SA, Chickering TW, Sower SA 1996 Relationship of gonadotropin-releasing hormone (GnRH) neurons to the olfactory system in developing lamprey (Petromyzon marinus). J Comp Neurol 376:97-111
5. Gorbman A, Sower SA 2003 Evolution of the role of GnRH in animal (Metazoan) biology. Gen Comp Endocrinol 134:207-213
6. Amano M, Okubo K, Yamanome T, Oka Y, Kawaguchi N, Aida K, Yamamori K 2004 Ontogenic development of three GnRH systems in the brain of a pleuronectiform fish, barfin flounder. Zool Sci 21:311-317
7. Wierman ME, Pawlowski JE, Allen MP, Xu M, Linseman DA, Nielsen-Preiss S 2004 Molecular mechanisms of gonadotropin-releasing hormone neuronal migration. Trends Endocrinol Metab 15:96-102
8. Wray S 2001 Development of luteinizing hormone releasing hormone neurones. J Neuroendocrinol 13:3-11
9. Tobet SA, Bless EP, Schwarting GA 2001 Developmental aspect of the gonadotropin-releasing hormone system. Mol Cell Endocrinol 185:173-184
10. el Amraoui A, Dubois PM 1993 Experimental evidence for an early commitment of gonadotropin-releasing hormone neurons, with special regard to their origin from the ectoderm of nasal cavity presumptive territory. Neuroendocrinology 57:991-1002
11. Whitlock KE, Wolf CD, Boyce ML 2003 Gonadotropin-releasing hormone (GnRH) cells arise from cranial neural crest and adenohypophyseal regions of the neural plate in the zebrafish, Danio rerio. Dev Biol 257:140-152
12. Yoshida K, Tobet SA, Crandall JE, Jimenez TP, Schwarting GA 1995 Migration of luteinizing hormone-releasing hormone neurons in the developing rat is associated with a transient, caudal projection of the vomeronasal nerve. J Neurosci 15:7769-7777
13. A receptor manipulation on migrating gonadotropin-releasing hormone neurons through the entire migratory route in vivo and in vitro. Endocrinology 141:254-262
14. Marin O, Rubenstein JL 2003 Cell migration in the forebrain. Annu Rev Neurosci 26:441-483
15. Ronnekleiv OK, Resko JA 1990 Ontogeny of gonadotropin-releasing hormone-containing neurons in early fetal development of rhesus macaques. Endocrinology 126:498-511
16. Tobet SA, Crandall JE, Schwarting GA 1993 Relationship of migrating luteinizing hormone-releasing hormone neurons to unique olfactory system glycoconjugates in embryonic rats. Dev Biol 155:471-482
17. Murakami S, Arai Y 1994 Direct evidence for the migration of LHRH neurons from the nasal region to the forebrain in the chick embryo: a carbocyanine dye analysis. Neurosci Res 19:331-338
18. Akutsu S, Takada M, Ohki-Hamazaki H, Murakami S, Arai Y 1992 Origin of luteinizing hormone-releasing hormone (LHRH) neurons in the chick embryo: effect of the olfactory placode ablation. Neurosci Lett 142:241-244
19. Murakami S Kikuyama S, Arai Y 1992 The origin of the luteinizing hormone-releasing hormone (LHRH) neurons in newts (Cynops pyrrhogaster): the effect of olfactory placode ablation. Cell Tissue Res 269:21-27
20. Norgren RB Jr., Gao C, Ji Y, Fritzsch B 1995 Tangential migration of luteinizing hormone-releasing hormone (LHRH) neurons in the medial telencephalon in association with transient axons extending from the olfactory nerve. Neurosci Lett 202:9-12
21. Fang Z, Xiong X, James A, Gordon DF, Wierman ME 1998 Identification of novel factors that regulate GnRH gene expression and neuronal migration. Endocrinology 139:3654-3657
22. Allen MP, Linseman DA, Udo H, Xu M, Schaack JB, Varnum B, Kandel ER, Heidenreich KA, Wierman ME 2002 Novel mechanism for gonadotropin-releasing hormone neuronal migration involving Gas6/Ark signaling to p38 mitogen-activated protein kinase. Mol Cell Biol 22:599-613
23. Giampietro C, Luzzati F, Gambarotta G, Giacobini P, Boda E, Fasolo A, Perroteau I 2005 Stathmin expression modulates migratory properties of GN-11 neurons in vitro. Endocrinology 146:1825-1834
24. Terasawa E, Quanbeck CD, Schulz CA, Burich AJ, Luchansky LL, Claude P 1993 A primary cell culture system of luteinizing hormone releasing hormone neurons derived from embryonic olfactory placode in the rhesus monkey. Endocrinology 133:2379-2390
25. Fueshko S, Wray S 1994 LHRH cells migrate on peripherin fibers in embryonic olfactory explant cultures: an in vitro model for neurophilic neuronal migration. Dev Biol 166:331-348
26. Tobet SA, Hanna IK, Schwarting, GA 1996 Migration of neurons containing gonadotropin releasing hormone (GnRH) in slices from embryonic nasal compartment and forebrain. Dev Brain Res 97:287-292
27. Tobet SA, Walker HJ, Seney ML, Yu KW 2003 Viewing cell movements in the developing neuroendocrine brain. Integr Comp Biol 43:794-801
28. Suter KJ, Song WJ, Sampson TL, Wuarin JP, Saunders JT, Dudek FE, Moenter SM 2000 Genetic targeting of green fluorescent protein to gonadotropin-releasing hormone neurons: characterization of whole-cell electrophysiological properties and morphology. Endocrinology 141:412-419
29. Bless EP, Walker HJ, Yu KW, Knoll JG, Moenter SM, Schwarting GA, Tobet SA 2005 Live view of gonadotropin-releasing hormone containing neuron migration. Endocrinology 146:463-468
30. Wray S, Key S, Qualls R, Fueshko SM 1994 A subset of peripherin positive olfactory axons delineates the luteinizing hormone releasing hormone neuronal migratory pathway in developing mouse. Dev Biol 166:349-354
31. Livne I, Gibson MJ, Silverman AJ 1993 Biochemical differentiation and intercellular interactions of migratory gonadotropin-releasing hormone (GnRH) cells in the mouse. Dev Biol 159:643-656
32. Schwarting GA, Kostek C, Bless EP, Ahmad N, Tobet SA 2001 Deleted in colorectal cancer (DCC) regulates the migration of luteinizing hormone-releasing hormone neurons to the basal forebrain. J Neurosci 21:911-919
33. Schwarting GA, Raitcheva D, Bless EP, Ackerman SL, Tobet S 2004 Netrin 1-mediated chemoattraction regulates the migratory pathway of LHRH neurons. Eur J Neurosci 19:11-20
34. Anderson SA, Eisenstat DD, Shi L, Rubenstein JL 1997 Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278:474-476
35. Nadarajah B, Parnavelas JG 2002 Modes of neuronal migration in the developing cerebral cortex. Nat Rev Neurosci 3:423-432
36. Ang ES Jr., Haydar TF, Gluncic V, Rakic P 2003 Four-dimensional migratory coordinates of GABAergic interneurons in the developing mouse cortex. J Neurosci 23:5805-5815
37. Xu Q, de la Cruz E, Anderson SA 2003 Cortical interneuron fate determination: diverse sources for distinct subtypes? Cereb Cortex 13:670-676
38. Tobet SA, Chickering TW, King JC, Stopa EG, Kim K, Kuo-Leblank V, Schwarting GA 1996 Expression of γ-aminobutyric acid and gonadotropin-releasing hormone during neuronal migration through the olfactory system. Endocrinology 137:5415-5420
39. Soria JM, Valdeolmillos M 2002 Receptor-activated calcium signals in tangentially migrating cortical cells. Cereb Cortex 12:831-839
40. Lujan R, Shigemoto R, Lopez-Bendito G 2005 Glutamate and GABA receptor signalling in the developing brain. Neuroscience 130:567-580
41. Fueshko SM, Key S, Wray S 1998 GABA inhibits migration of luteinizing hormone-releasing hormone neurons in embryonic olfactory explants. J Neurosci 18:2560-2569
42. Trainor PA 2005 Specification of neural crest cell formation and migration in mouse embryos. Semin Cell Dev Biol 16:683-693
43. Robinson V, Smith A, Flenniken AM, Wilkinson DG 1997 Roles of Eph receptors and ephrins in neural crest pathfinding. Cell Tissue Res 290:265-274
44. Gamble JA, Karunadasa DK, Pape JR, Skynner MJ, Todman MG, Bicknell RJ, Allen JP, Herbison AE 2005 Disruption of ephrin signaling associates with disordered axophilic migration of the gonadotropin-releasing hormone neurons. J Neurosci 25:3142-3150
45. Jiang Y, Liu MT, Gershon MD 2003 Netrins and DCC in the guidance of migrating neural crest-derived cells in the developing bowel and pancreas. Dev Biol 258:364-384
46. Trokovic R, Trokovic N, Hernesniemi S, Pirvola U, Vogt Weisenhorn DM, Rossant J, McMahon AP, Wurst W, Partanen J 2003 FGFR1 is independently required in both developing mid- and hindbrain for sustained response to isthmic signals. EMBO J 22:1811-1823
47. Dode C, Levilliers J, Dupont JM, De Paepe A, Le Du N, Soussi-Yanicostas N, Coimbra RS, Delmaghani S, Compain-Nouaille S, Baverel F, Pecheux C, Le Tessier D, Cruaud C, Delpech M, Speleman F, Vermeulen S, Amalfitano A, Bachelot Y, Bouchard P, Cabrol S, Carel JC, Delemarre-van de Waal H, Goulet-Salmon B, Kottler ML, Richard O, Sanchez-Franco F, Saura R, Young J, Petit C, Hardelin JP 2003 Loss-of-function mutations in FGFR1 cause autosomal dominant Kallmann syndrome. Nat Genet 33:463-465
48. Glogarova K, Buckiova D 2004 Changes in sialylation in homozygous Sp2H mouse mutant embryos. Birth Defects Res A Clin Mol Teratol 70:142-152
49. Yoshida K, Rutishauser U, Crandall JE, Schwarting GA 1999 Polysialic acid facilitates migration of luteinizing hormone-releasing hormone neurons on vomeronasal axons. J Neurosci 19:794-801
50. Givens ML, Rave-Harel N, Goonewardena VD, Kurotani R, Berdy SE, Swan CH, Rubenstein JL, Robert B, Mellon PL 2005 Developmental regulation of gonadotropin-releasing hormone gene expression by the MSX and DLX homeodomain protein families. J Biol Chem 280:19156-19165.
51. Romanelli RG, Barni T, Maggi M, Luconi M, Failli P, Pezzatini A, Morelli A, Maggi R, Zaninetti R, Salerno R, Ambrosini S, Marini M, Rotella CM, Vannelli GB 2005 Role of endothelin-1 in the migration of human olfactory gonadotropin-releasing hormone-secreting neuroblasts. Endocrinology 146:4321-4330
52. A) receptor subunit mRNA expression in postnatal gonadotropin-releasing hormone (GnRH) neurons of the male mouse with single cell RTPCR. Neuroendocrinology 74:300-308
53. Parhar IS, Ogawa S, Sakuma Y 2004 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 145:3613-3618
54. Todman MG, Han SK, Herbison AE 2005 Profiling neurotransmitter receptor expression in mouse gonadotropin-releasing hormone neurons using green fluorescent protein-promoter transgenics and microarrays. Neuroscience 132:703-712
55. Temple JL, Wray S 2005 Developmental changes in GABA receptor subunit composition within the gonadotrophin-releasing hormone-1 neuronal system. J Neuroendocrinol 17:591-599
56. Woods CG 2004 Neuroscience. Crossing the midline. Science 304:1455-1456
57. Murakami S, Kamiya M, Akutsu S, Seki T, Kuwabara Y, Arai, Y 1995 Straying phenomenon of migrating LHRH neurons and highly polysialylated NCAM in the chick embryo. Neurosci Res 22:109-115
58. Schwanzel-Fukuda M, Bick D, Pfaff DW 1989 Luteinizing hormone-releasing hormone (LHRH)-expressing cells do not migrate normally in an inherited hypogonadal (Kallmann) syndrome. Mol Brain Res 6:311-326
59. Pronina T, Ugrumov M, Calas A, Seif I, Tramu G 2003 Influence of monoamines on differentiating gonadotropin-releasing hormone neurones in foetal mice. J Neuroendocrinol 15:925-932
60. Giacobini P, Kopin AS, Beart PM, Mercer LD, Fasolo A, Wray S 2004 Cholecystokinin modulates migration of gonadotropin-releasing hormone-1 neurons. J Neurosci 24:4737-4748
61. Gibson MJ, Ingraham L, Dobrjansky A 2000 Soluble factors guide gonadotropin-releasing hormone axonal targeting to the median eminence. Endocrinology 141:3065-3071
62. Gill JC, Moenter SM, Tsai PS 2004 Developmental regulation of gonadotropin-releasing hormone neurons by fibroblast growth factor signaling. Endocrinology 145:3830-3839
63. Tsai PS, Moenter SM, Postigo HR, El Majdoubi M, Pak TR, Gill JC, Paruthiyil S, Werner S, Weiner RI 2005 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 19:225-236
64. Cronin AS, Horan TL, Spergel DJ, Brooks AN, Hastings MH, Ebling FJ 2004 Neurotrophic effects of BDNF on embryonic gonadotropin-releasing hormone (GnRH) neurons. Eur J Neurosci 20:338-344
65. Wong K, Park HT, Wu JY, Rao Y 2002 Slit proteins: molecular guidance cues for cells ranging from neurons to leukocytes. Curr Opin Genet Dev 12:583-591
66. 2+ transients control CNS neuronal migration. Cell Calcium 37:387-393
67. Toba Y, Pakiam JG, Wray S 2005 Voltage-gated calcium channels in developing GnRH-1 neuronal system in the mouse. Eur J Neurosci 22:79-92
68. Bolteus AJ, Bordey A 2004 GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. J Neurosci 24:7623-7631
69. Romanelli RG, Barni T, Maggi M, Luconi M, Failli P, Pezzatini A, Pelo E, Torricelli F, Crescioli C, Ferruzzi P, Salerno R, Marini M, Rotella CM, Vannelli GB 2004 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 279:117-126
70. Lazarini F, Tham TN, Casanova P, Arenzana-Seisdedos F, Dubois-Dalcq M 2003 Role of the α-chemokine stromal cell-derived factor (SDF-1) in the developing and mature central nervous system. Glia 42:139-148
71. Belmadani A, Tran PB, Ren D, Assimacopoulos S, Grove EA, Miller RJ 2005 The chemokine stromal cell-derived factor-1 regulates the migration of sensory neuron progenitors. J Neurosci 25:3995-4003
72. Tran PB, Ren D, Veldhouse TJ, Miller RJ 2004 Chemokine receptors are expressed widely by embryonic and adult neural progenitor cells. J Neurosci Res 76:20-34
73. Schaar BT, McConnell SK 2005 Cytoskeletal coordination during neuronal migration. Proc Natl Acad Sci USA 102:13652-13657
74. Gonzalez-Martinez D, Hu Y, Bouloux PM 2004 Ontogeny of GnRH and olfactory neuronal systems in man: novel insights from the investigation of inherited forms of Kallmann's syndrome. Front Neuroendocrinol 25:108-130
75. Franco B, Guioli S, Pragliola A, Incerti B, Bardoni B, Tonlorenzi R, Carrozzo R, Maestrini E, Pieretti M, Taillon-Miller P, Brown CJ, Willard HF, Lawrence C, Persico MG, Camarino G, Ballabio A 1991 A gene deleted in Kallmann's syndrome shares homology with neural cell adhesion and axonal path-finding molecules. Nature 353:529-536
76. Soussi-Yanicostas N, Faivre-Sarrailh C, Hardelin JP, Levilliers J, Rougon G, Petit C 1998 Anosmin-1 underlying the X chromosome-linked Kallmann syndrome is an adhesion molecule that can modulate neurite growth in a cell-type specific manner. J Cell Sci 111:2953-2965
77. Gonzalez-Martinez D, Kim SH, Hu Y, Guimond S, Schofield J, Winyard P, Vannelli GB, Turnbull J, Bouloux PM 2004 Anosmin-1 modulates fibroblast growth factor receptor 1 signaling in human gonadotropin-releasing hormone olfactory neuroblasts through a heparan sulfate-dependent mechanism. J Neurosci 24:10384-10392
78. Cariboni A, Pimpinelli F, Colamarino S, Zaninetti R, Piccolella M, Rumio C, Piva F, Rugarli EI, Maggi R 2004 The product of X-linked Kallmann's syndrome gene (KAL1) affects the migratory activity of gonadotropin-releasing hormone (GnRH)-producing neurons. Hum Mol Genet 13:2781-2791
79. Pitteloud N, Acierno JS, Meysing A, Metzger D, Hayes FJ, Dwyer AA, Hughes VA, Yialamas M, Hall JE, Grant E, Mohammadi M, Crowley Jr WF, Mutations in fibroblast growth factor receptor 1 cause both Kallmann syndrome and normosmic idiopathic hypogonadotropic hypogonadism. Proc Natl Acad Sci, USA, in press
80. Giacobini P, Giampietro C, Fioretto M, Maggi R, Cariboni A, Perroteau I, Fasolo A 2002 Hepatocyte growth factor/scatter factor facilitates migration of GN-11 immortalized LHRH neurons. Endocrinology 143:3306-3315
81. Simonian SX, Herbison AE 2001 Differing spatially restricted roles of ionotropic glutamate receptors in regulating the migration of GnRH neurons during embryogenesis. J Neurosci 21:934-943
82. Kramer PR, Wray S 2000 Novel gene expressed in nasal region influences outgrowth of olfactory axons and migration of luteinizing hormone-releasing hormone (LHRH) neurons. Genes Dev 14:1824-1834
83. Allen MP, Xu M, Zeng C, Tobet SA, Wierman ME 2000 Myocyte enhancer factors-2B and -2C are required for adhesion related kinase repression of neuronal gonadotropin releasing hormone gene expression. J Biol Chem 275:39662-39670
84. Lawson MA, Mellon PL 1998 Expression of GATA-4 in migrating gonadotropin-releasing neurons of the developing mouse. Mol Cell Endocrinol 140:157-161
85. Wolfe A, Kim HH, Tobet S, Stafford DE, Radovick S 2002 Identification of a discrete promoter region of the human GnRH gene that is sufficient for directing neuron-specific expression: a role for POU homeodomain transcription factors. Mol 16:435-449
86. Corradi A, Croci L, Broccoli V, Zecchini S, Previtali S, Wurst W, Amadio S, Maggi R, Quattrini A, Consalez GG 2003 Hypogonadotropic hypogonadism and peripheral neuropathy in Ebf2-null mice. Development 130:401-410
87. Kruger M, Ruschke K, Braun T 2004 NSCL-1 and NSCL-2 synergistically determine the fate of GnRH-1 neurons and control necdin gene expression. EMBO J 23:4353-4364
88. Sharifi N, Reuss AE, Wray S 2002 Prenatal LHRH neurons in nasal explant cultures express estrogen receptor-β transcript. Endocrinology 143:2503-2507
89. Martinez-Fuentes AJ, Hu L, Krsmanovic LZ, Catt KJ 2004 Gonadotropin-releasing hormone (GnRH) receptor expression and membrane signaling in early embryonic GnRH neurons: role in pulsatile neurosecretion. Mol Endocrinol 18:1808-1817
90. Key S, Wray S 2000 Two olfactory placode derived galanin subpopulations: luteinizing hormone-releasing hormone neurones and vomeronasal cells. J Neuroendocrinol 12:535-545
91. Dellovade TL, Davis AM, Ferguson C, Sieghart W, Homanics GE, Tobet SA 2001 GABA influences the development of the ventromedial nucleus of the hypothalamus. J Neurobiol 49:264-276