The GnRH neuron: Molecular aspects of migration, gene expression and regulation

Progress in Brain Research

Volumn 141, Issue , 2002, Pages 243-257

  Wolfe, Andrew ^a   Kim, Helen H ^a   Radovick, Sally ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FOLLITROPIN; GONADORELIN; LUTEINIZING HORMONE;

ALTERNATIVE RNA SPLICING; ANIMAL MODEL; CELL LINE; CELL MIGRATION; CELL POPULATION; CONFERENCE PAPER; GENE EXPRESSION; GENE EXPRESSION REGULATION; HYPOTHALAMUS; MOLECULAR DYNAMICS; NERVE CELL; NEUROANATOMY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION;

EID: 18744410638     PISSN: 00796123     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0079-6123(02)41097-7     Document Type: Conference Paper

References (95)

1. al Shawi, R., Kinnaird, J., Burke, J. and Bishop, J.O. (1990) Expression of a foreign gene in a line of transgenic mice is modulated by a chromosomal position effect. Mol. Cell. Biol., 10: 1192-1198.
2. Allen, M.P., Zeng, C., Schneider, K., Xiong, X., Meintzer, M.K., Bellosta, P., Basilico, C., Vamum, B., Heidenreich, K.A. and Wierman, M.E. (1999) 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., 13: 191-201.
3. Barry, J., Hoffman, G.E. and Wray, S. (1985) LHRH-containing systems. In: A. Björklund and T Hökfelt (Eds.), Handbook of Chemical Neuroanatomy. Vol. 4: GABA and Neuropeptides in the CNS, Part 1. Elsevier, Amsterdam, pp. 166-215.
4. Belsham, D.D. and Mellon, P.L. (2000) Transcription factors Oct-1 and C/EBPbeta (CCAAT/enhancer-binding protein-beta) are involved in the glutamate/nitric oxide/cyclicguanosine 5′-monophosphate-mediated repression of mediated repression of gonadotropin-releasing hormone gene expression. Mol. Endocrinol., 14: 212-228.
5. Bond, C.T., Hayflick, J.S., Seeburg, P.H. and Adelman, J.P. (1989) The rat gonadotropin-releasing hormone: SH locus: Structure and hypothalamic expression. Mol. Endocrinol., 3(8): 1257-1262.
6. Bosma, M.M. (1993) Ion channel properties and episodic activity in isolated immortalized gonadotropin-releasing hormone (GnRH) neurons. J. Membr. Biol., 136: 85-96.
7. Bruder, J.M., Krebs, W.D., Nett, T.M. and Wierman, M.E. (1992) Phorbol ester activation of the protein kinase C pathway inhibits gonadotropin-releasing hormone gene expression. Endocrinology, 131: 2552-2558.
8. Chandran, U.R. and DeFranco, D.B. (1999) Regulation of gonadotropin-releasing hormone gene transcription. Behav. Brain Res., 105: 29-36.
9. Chandran, U.R., Warren, B.S., Baumann, C.T., Hager, G.L. and DeFranco, D.B. (1999) The glucocorticoid receptor is tethered to DNA-bound Oct-1 at the mouse gonadotropin-releasing hormone distal negative glucocorticoid response element. J. Biol. Chem., 274: 2372-2378.
10. Clark, M.E. and Mellon, P.L. (1995) The POU homeodomain transcription factor Oct-1 is essential for activity of the gonadotropin-releasing hormone neuron-specific enhancer. Mol. Cell. Biol., 15(11): 6169-6177.
11. Dong, K.-W., Yu, K.-L. and Roberts, J.L. (1993) Identification of a major up-stream transcription start site for the human progonadotropin-releasing hormone gene used in reproductive tissues and cell lines. Mol. Endocrinol., 7: 1654-1666.
12. Dutlow, C.M., Rachman, J., Jacobs, T.W. and Millar, R.P. (1992) Prepubertal increases in gonadotropin-releasing hormone mRNA, gonadotropin-releasing hormone precursor, and subsequent maturation of precurso processing in male rats. J. Clin. Invest., 90: 2496-2501.
13. Eraly, S.A. and Mellon, P.L. (1995) Regulation of gonadotropin-releasing hormone transcription by protein kinase C is mediated by evolutionarily conserved promoter-proximal elements, Mol. Endocrinol., 9: 848-859.
14. Eraly, S.A., Nelson, S.B., Huang, K.M. and Mellon, P.L. (1998) Oct-1 binds promoter elements required for transcription of the GnRH gene. Mol. Endocrinol., 12: 469-481.
15. Fang, Z., Xiong, X., James, A., Gordon, D.F. and Wierman, M.E. (1998) Identification of novel factors that regulate GnRH gene expression and neuronal migration. Endocrinology, 139: 3654-3657.
16. Fischer, I., Richter-Landsberg, C. and Safaei, R. (1991) Regulation of microtubule associated protein 2 (MAP2) expression by nerve growth factor in PC12 cells. Exp. Cell Res., 194: 195-201.
17. Franco, B., Guioli, S., Pragliola, A., Incerti, B., Bardoni, B., Tonlorenzi, R., Carrozzo, R., Maestrini, E., Pieretti, M. and Taillon-Miller, P. (1991) A gene deleted in Kallmann's syndrome shares homology with neural cell adhesion and axonal path-finding molecules. Nature, 353: 529-536.
18. Fueshko, S.M., Key, S. and Wray, S. (1998) GABA inhibits migration of luteinizing hormone-releasing hormone neurons in embryonic olfactory explants. J. Neurosci., 18: 2560-2569.
19. Goldowitz, D. (1989) The weaver granuloprival phenotype is due to intrinsic action of the mutant locus in granule cells: Evidence from homozygous weaver chimeras. Neuron, 2: 1565-1575.
20. Goldowitz, D. and Mullen, R.J. (1982) Granule cell as a site of gene action in the weaver mouse cerebellum: Evidence from heterozygous mutant chimeras. J. Neurosci., 2: 1474-1485.
21. Gore, A.C. (1998) Diurnal rhythmicity of gonadotropin-releasing hormone gene expression in the rat. Neuroendocrinology, 68: 257-263.
22. Gore, A.C., Ho, A. and Roberts, J.L. (1995) Translational efficiency of gonadotropin-releasing hormone messenger ribonucleic acid is negatively regulated by phorbol ester in GT1-7 cells. Endocrinology, 136: 1620-1625.
23. Gore, A.C., Wu, T.J., Rosenberg, J.J. and Roberts, J.L. (1996) Gonadotropin-releasing hormone and NMDA receptor gene expression and colocalization change during puberty in female rats. J. Neurosci., 16: 5281-5289.
24. Gore, A.C., Roberts, J.L. and Gibson, M.J. (1999) Mechanism for the regulation of gonadotropin-releasing hormone gene expression in the developing mouse. Endocrinology, 140: 2280-2287.
25. Hayflick, J.S., Adelman, J.P. and Seeburg, P.H. (1989) The complete nucleotide sequence of the human gonadotropin-releasing hormone gene. Nucleic Acid Res., 17(15): 6403-6404.
26. He, X., Treacy, M.N., Simmons, D.M., Ingraham, H.A., Swanson, L.W. and Rosenfeld, M.G. (1989) Expression of a large family of POU-domain regulatory genes in mammalian brain development. Nature, 340: 35-41 [erratum appeared in Nature (1989), 340(6235): 662].
27. Hiatt, E.S., Brunetta, P.G., Seiler, G.R., Barney, S.A., Selles, W.D., Wooledge, K.H. and King, J.C. (1992) Subgroups of luteinizing hormone-releasing hormone perikary defined by computer analysis in the basal forebrain of intact female rats. Endocrinology, 130(2): 1030-1043.
28. Hsueh, A.J. and Erickson, G.F. (1979a) Extra-pituitary inhibition of testicular function by luteinising hormone releasing hormone. Nature, 281: 66-67.
29. Hsueh, A.J. and Erickson, G.F. (1979b) Extrapituitary action of gonadotropin-releasing hormone: Direct inhibition ovarian steroidogenesis. Science, 204: 854-855.
30. Kelley, C.G., Lavorgna, G., Clark, M.E., Boncinelli, E. and Mellon, P.L. (2000) The Otx2 homeoprotein regulates expression from the gonadotropin-releasing hormone proximal promoter. Mol. Endocrinol., 14: 1246-1256.
31. Kepa, J.K., Wang, C., Neeley, C.I., Raynolds, M.V., Gordon, D.F., Wood, W.M. and Wierman, M.E. (1992) Structure of the rat gonadotropin-releasing hormone (rGnRH) gene promoter and functional analysis in hypothalamic cells. Nucleic Acid Res., 20(6): 1393-1399.
32. Kepa, J.K., Spaulding, A.J., Jacobsen, B.M., Fang, Z., Xiong, X., Radovick, S. and Wierman, M.E. (1996) Structure of the distal human gonadotropin releasing hormone (hGnrh) gene promoter and functional analysis in Gtl-7 neuronal cells. Nucleic Acids Res., 24: 3614-3620.
33. Kim, H.H., Wolfe, A., Smith, G.R., Tobet, S.A. and Radovick, S. (2002) Promoter sequences targeting tissue-specific gene expression of hypothalamic and ovarian gonadotropin-releasing hormone in vivo. J. Biol. Chem., 277: 5194-5202.
34. King, J.C., Tobet, S.A., Snavely, F.L. and Arimura, A.A. (1982) LHRH Imminopositive Cells and Their Projections to the Median Eminence and Organum Vasculosum of the Lamina Teminalis. J. Comp. Neurol., 209: 287-300.
35. Knecht, M., Ranta, T., Feng, P., Shinohara, O. and Catt, K.J. (1985) Gonadotropin-releasing hormone as a modulator of ovarian function. J. Steroid Biochem., 23: 771-778.
36. Kokoris, G.J., Lam, N.Y., Ferin, M., Silverman, A.J. and Gibson, M.J. (1988) Transplanted gonadotropin-releasing hormone neurons promote pulsatile luteinizing hormone secretion in congenitally hypogonadal (hpg) male mice. Neuroendocrinology, 48: 45-52.
37. Kramer, P.R. and 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.
38. Lawson, M.A. and Mellon, P.L. (1998) Expression of GATA-4 in migrating gonadotropin-releasing neurons of the developing mouse [In Process Citation]. Mol. Cell. Endocrinol., 140: 157-161.
39. Lawson, M.A., Whyte, D.B. and Mellon, P.L. (1996) GATA factors are essential for activity of the neuron-specific enhancer of the gonadotropin-releasing hormone gene. Mol. Cell. Biol. 1996 Jul, 16: 3596-3605.
40. Lawson, M.A., Buhain, A.R., Jovenal, J.C. and Mellon, P.L. (1998) Multiple factors interacting at the GATA sites of the gonadotropin-releasing hormone neuron-specific enhancer regulate gene expression. Mol. Endocrinol., 12: 364-377.
41. Lawson, M.A., Macconell, L.A., Kim, J., Powl, B.T., Nelson, S.B. and Mellon, P.L. (2002) Neuron-specific expression in vivo by defined transcription regulatory elements of the GnRH gene. Endocrinology, 143: 1404-1412.
42. 2+-mobilizing and adenylyl cyclase-coupled receptors. J. Neurosci., 20: 9290-9297.
43. Legouis, R., Hardelin, J.-P., Levilliers, J., Claverie, J.-M., Compain, S., Wunderie, V., Millasseau, P., Le Paslier, D., Cohen, D., Caterina, D., Bougueleret, L., Delemarre-Van de Waal, H., Lutfalla, G., Weissenbach, J. and Petit, C. (1991) The candidate gene for the X-linked Kallmann syndrome encodes a protein related to adhesion molocules. Cell, 423-435.
44. Legouis, R., Cohen-Salmon, M., Del Castillo, I. and Petit, C. (1994) Isolation and characterization of the gene responsible for the X chromosome-linked Kallmann syndrome. Biomed. Pharmacother., 48: 241-246.
45. Levine, J.E. and Ramirez, V.D. (1982) Luteinizing hormone-releasing hormone release during the rat estrous cycle and after ovariectomy, as estimated with push-pull cannulae. Endocrinology, 111: 1439-1448.
46. Livne, I., Gibson, M.J. and Silverman, A.J. (1993a) Biochemical differentiation and intercellular interactions of migratory gonadotropin-releasing hormone (GnRH) cells in the mouse. Dev. Biol., 159: 643-656.
47. Livne, I., Gibson, M.J. and Silverman, A.J. (1993b) Gonadotropin-releasing hormone (GnRH) neurons in the hypogonadal mouse elaborate normal projections despite their biosynthetic deficiency. Neurosci. Lett., 151: 229-233.
48. Martinez, d.I.E., Choi, A.L. and Weiner, R.I. (1992) Generation and synchronization of gonadotropin-releasing hormone (GnRH) pulses: Intrinsic properties of the GT1-1 GnRH neuronal cell line. Proc. Natl. Acad. Sci. USA, 89: 1852-1855.
49. Mason, A.J., Hayflick, J.S., Zoeller, R.T., Young, W.S., Phillips, H.S., Nikolics, K. and Seeburg, P.H. (1986) A deletion truncating the gonadotropin-releasing hormone gene is responsible for hypogonadism in the hpg mouse. Science, 234: 1366-1371.
50. Mavilia, C., Couchie, D., Mattei, M.G., Nivez, M.P. and Nunez, J. (1993) High and low molecular weight tau proteins are differentially expressed from a single gene. J. Neurochem., 61: 1073-1081.
51. Mellon, P.L., Windle, J.J., Goldsmith, P.C., Padula, C.A., Roberts, J.L. and Weiner, R.I. (1990) Immortalization of hypothalamic gnrh neurons by genetically targeted tumorigenesis. Neuron, 5: 1-10.
52. Mitsushima, D., Hei, D.L. and Terasawa, E. (1994) gamma-Aminobutyric acid is an inhibitory neurotransmitter restricting the release of luteinizing hormone-releasing hormone before the onset of puberty. Proc. Natl. Acad. Sci. USA, 91: 395-399.
53. Moenter, S.M., Caraty, A., Locatelli, A. and Karsch, F.J. (1991) Pattern of gonadotropin-releasing hormone (gnrh) secretion leading up to ovulation in the ewe: Existence of a preovulatory GnRH surge, Endocrinology, 129(3): 1175-1182.
54. Nelson, S.B., Lawson, M.A., Kelley, C.G. and Mellon, P.L. (2000) Neuron-specific expression of the rat gonadotropin-releasing hormone gene is conferred by interactions of a defined promoter element with the enhancer in GT1-7 cells. Mol. Endocrinol., 14: 1509-1522.
55. Pape, J.R., Skynner, M.J., Allen, N.D. and Herbison, A.E. (1999) Transgenics identify distal 5′- and 3′-sequences specifying gonadotropin-releasing hormone expression in adult mice. Mol. Endocrinol., 13: 2203-2211.
56. Parfitt, D.B., Thompson, R.C., Richardson, H.N., Romeo, R.D. and Sisk, C.L. (1999) GnRH mRNA increases with puberty in the male syrian hamster brain [In Process Citation]. J. Neuroendocrinol., 11: 621-627.
57. Poletti, A., Melcangi, R.C., Negri-Cesi, P., Maggi, R. and Martini, L. (1994) Steroid binding and metabolism in the luteinizing hormone-releasing hormone-producing neuronal cell line GT1-1. Endocrinology, 135(6): 2623-2628.
58. Poletti, A., Rampoldi, A., Piccioni, F., Volpi, S., Simeoni, S., Zanisi, M. and Martini, L. (2001) 5Alpha-reductase type 2 and androgen receptor expression in gonadotropin releasing hormone GT1-1 cells. J. Neuroendocrinol., 13: 353-357.
59. Porkka-Heiskanen, T., Urban, J.H., Turek, F.W. and Levine, J.E. (1994) Gene expression in a subpopulation of luteinizing hormone-releasing hormone (LHRH) neurons prior to the preovuluatory gonadotropin surge. J. Neurosci., 14(9): 5548-5558.
60. Quinton, R., Hasan, W., Grant, W., Thrasivoulou, C., Quincy, R.E., Besser, G.M. and Bouloux, P.M. (1997) Gonadotropin-releasing hormone immunoreactivity in the nasal epithelia of adults with Kallmann's syndrome and isolated hypogonadotropic hypogonadism and in the early midtrimester human fetus. J, Clin. Endocrinol. Metab., 82: 309-314.
61. Radovick, S., Wondisford, F.E., Nakayama, Y., Yamada, M., Cutler Jr. G.B. and Weintraub, B.D. (1990) Isolation and characterization of the human gonadotropin-releasing hormone gene in the hypothalamus and placenta. Mol. Endocrinol., 4: 476-480.
62. Radovick, S., Wray, S., Lee, E., Nicols, D.K., Nakayama, Y., Weintraub, B.D., Westphal, H., Cutler Jr., G.B. and Wondisford, F.E. (1991) Migratory arrest of gonadotropin-releasing hormone neurons in transgenic mice. Proc. Natl. Acad. Sci. USA, 88: 3402-3406.
63. Rajendren, G. (2001) Subsets of gonadotropin-releasing hormone (GnRH) neurons are activated during a steroid-induced luteinizing hormone surge and mating in mice: A combined retrograde tracing double immunohistochemical study. Brain Res., 918: 74-79.
64. Rakic, P. and Sidman, R.L. (1973a) Sequence of developmental abnormalities leading to granule cell deficit in cerebellar cortex of weaver mutant mice. J. Comp. Neurol., 152: 103-132.
65. Rakic, P. and Sidman, R.L. (1973b) Weaver mutant mouse cerebellum: Defective neuronal migration secondary to abnormality of Bergmann glia. Proc. Natl. Acad. Sci. USA, 70: 240-244.
66. Richards, J.S. (1994) Hormonal control of gene expression in the ovary. Endocrinol. Rev., 15: 725-751.
67. Rogers, M.C., Silverman, A.J. and Gibson, M.J. (1997) Gonadotropin-releasing hormone axons target the median eminence: In vitro evidence for diffusible chemoattractive signals from the mediobasal hypothalamus. Endocrinology, 138: 3956-3966.
68. Rogers, M.C., Silverman, A.J. and Gibson, M.J. (1998) Preoptic area grafts implanted in mammillary bodies of hypogonadal mice: Patterns of GnRH neuronal projections. Exp. Neurol., 151: 265-272.
69. Scholl, F.G., Gamallo, C., Vilaro S. and Quintanilla, M. (1999) Identification of PA2.26 antigen as a novel cell-surface mucin-type glycoprotein that induces plasma membrane extensions and increased motility in keratinocytes. J. Cell Sci., 112: 4601-4613.
70. Schwanzel-Fukuda, M., Garcia, M.S., Morrell, J.I. and Pfaff, D.W. (1987) Distribution of luteinizing hormone-releasing hormone in the nervus terminalis and brain of the mouse detected by immunocytochemistry. J. Comp. Neurol., 255(2): 231-244.
71. Schwanzel-Fukuda, M., Bick, D. and Pfaff, D.W. (1989) Luteinizing hormone-releasing hormone (LHRH)-expressing cells do not migrate normally in an inherited hypogonadal (Kallmann) syndrome. Mol. Brain Res., 6: 311-326.
72. Seeburg, P.H., Mason, A.J., Stewart, T.A. and Nikolics, K. (1987) The mammalian GnRH gene and its pivotal role in reproduction. Rec. Prog. Horm. Res., 41: 69-98.
73. Silverman, A.J., Roberts, J.L., Dong, K.W., Miller, G.M. and Gibson, M.J. (1992) Intrahypothalamic injection of a cell line secreting gonadotropin-releasing hormone results in cellular differentiation and reversal of hypogonadism in mutant mice. Proc. Natl. Acad. Sci. USA, 89: 10668-10672.
74. Skynner, M.J., Slater, R., Sim, J.A., Allen, N.D. and Herbison, A.E. (1999) Promoter transgenics reveal multiple gonadotropin-releasing hormone-I-expressing cell populations of different embryological origin in mouse brain. J. Neurosci., 19: 5955-5966.
75. Sosnowski, R., Mellon, P.L. and Lawson, M.A. (2000) Activation of translation in pituitary gonadotrope cells by gonadotropin-releasing hormone. Mol. Endocrinol., 14: 1811-1819.
76. Suter, K.J., Song, W.J., Sampson, T.L., Wuarin, J.P., Saunders, J.T., Dudek, F.E. and Moenter, S.M. (2000) Genetic targeting of green fluorescent protein to gonadotropin-releasing hormone neurons: Characterization of whole-cell electrophysiological properties and morphology. Endocrinology, 141: 412-419.
77. Terasawa, E., Luchansky, L.L., Kasuya, E. and Nyberg, C.L. (1999) An increase in glutamate release follows a decrease in gamma aminobutyric acid and the pubertal increase in luteinizing hormone releasing hormone release in the female rhesus monkeys. J. Neuroendocrinol., 11: 275-282.
78. Van Goor, F., Krsmanovic, L,Z., Catt, K.J. and Stojilkovic, S.S. (2000) Autocrine regulation of calcium influx and gonadotropin-releasing hormone secretion in hypothalamic neurons. Biochem. Cell. Biol., 78: 359-370.
79. Waldstreicher, J., Seminara, S.B., Jameson, J.L., Geyer, A., Nachtigall, L.B., Boepple, P.A., Holmes, L.B. and Crowley, W.F.J. (1996) The genetic and clinical heterogeneity of gonadotropin-releasing hormone deficiency in the human. J. Clin. Endocrinol. Metab., 81: 4388-4395.
80. Weiner, R.I. and Martinez, d.I.E. (1993) Pulsatile release of gonadotrophin releasing hormone (GnRH) is an intrinsic property of GT1 GnRH neuronal cell lines. Hum. Reprod., 8(2): 13-17.
81. Wetsel, W.C., Mellon, P.L., Weiner, R.I. and Negro-Vilar, A. (1991) Metabolism of pro-luteinizing hormone-releasing hormone in immortalized hypothalamic neurons. Endocrinology. 129: 1584-1595.
82. Whyte, D.B., Lawson, M.A., Belsham, D.D., Eraly, S.A., Bond, C.T., Adelman, J.P. and Mellon, P.L. (1995) A neuron-specific enhancer targets expression of the gonadotropin-releasing hormone gene to hypothalamic neurosecretory neurons. Mol. Endocrinol., 9: 467-477.
83. Wierman, M.E., Kepa, J.K., Sun, W., Gordon, D.F. and Wood, W.M. (1992) Estrogen negatively regulates rat gonadotropin releasing hormone (rGnRH) promoter activity in transfected placental cells. Mol. Cell. Endocrinol., 86: 1-10.
84. Wierman, M.E., Xiong, X., Kepa, J.K., Spaulding, A.J., Jacobsen, B.M., Fang, Z., Nilaver, G. and Ojeda, S.R. (1997) Repression of gonadotropin-releasing hormone promoter activity by the POU homeodomain transcription factor SCIP/Oct-6/ Tst-1: A regulatory mechanism of phenotype expression?. Mol. Cell. Biol., 17: 1652-1665.
85. Wolfe, A.M., Wray, S., Westphal, H. and Radovick, S. (1995) Cell-specific expression of the human gonadotropin-releasing hormone gene in transgenic animals. J. Biol. Chem., 271: 20018-20023.
86. Wolfe, A., Kim, H.S.D., Tobet, S.A. and 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. Endocrinol., 16: 435-449.
87. Wray, S., Grant, P. and 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.
88. Wray, S., Key, S., Qualls, R. and Fueshko, S.M. (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.
89. Wu, T.J., Gibson, M.J., Rogers, M.C. and Silverman, A.J. (1997) New observations on the development of the gonadotropin-releasing hormone system in the mouse. J. Neurobiol., 33: 983-998.
90. Yeo, T.T., Gore, A.C., Jakubowski, M., Dong, K.W., Blum, M. and Roberts, J.L. (1996) Characterization of gonadotropin-releasing hormone gene transcripts in a mouse hypothalamic neuronal GT1 cell line. Brain Res. Mol. Brain Res., 42: 255-262.
91. Yokosaki, Y., Matsuura, N., Higashiyama, S., Murakami, I., Obara, M., Yamakido, M., Shigeto, N., Chen, J. and Sheppard, D. (1998) Identification of the ligand binding site for the integrin alpha9 betal in the third fibronectin type III repeat of tenascin-C. J. Biol. Chem., 273: 11423-11428.
92. Yoshida, K., Rutishauser, U., Crandall, J.E. and Schwarting, G.A. (1999) Polysialic acid facilitates migration of luteinizing hormone-releasing hormone neurons on vomeronasal axons. J. Neurosci., 19: 794-801.
93. Zamorano, P.L., Mahesh, V.B., De Sevilla, L. and Brann, D.W, (1998) Excitatory amino acid receptors and puberty. Steroids, 63: 268-270.
94. Zhen, S., Dunn, I.C., Wray, S., Liu, Y., Chappell, P.E., Levine, J.E. and Radovick, S. (1997a) An alternative gonadotropin- releasing hormone (GnRH) RNA splicing product found in cultured GnRH neurons and mouse hypothalamus. J. Biol. Chem., 272: 12620-12625.
95. Zhen, S., Zakaria, M., Wolfe, A. and Radovick, S. (1997b) Regulation of gonadotropin-releasing hormone (GnRH) gene expression by insulin-like growth factor I in a cultured GnRH-expressing neuronal cell line. Mol. Endocrinol., 11: 1145-1155.