Origin and migration of luteinizing hormone-releasing hormone neurons in mammals

Microscopy Research and Technique

Volumn 44, Issue 1, 1999, Pages 2-10

  Schwanzel Fukuda, Marlene ^a  

^a SUNY DOWNSTATE MEDICAL CENTER   (United States)

Author keywords

GnRH; Olfactory placode; Terminal nerve; Vomeronasal nerve

Indexed keywords

BRAIN; CELL ADHESION; CELLS; MAMMALS; SCAFFOLDS (BIOLOGY);

CELL MIGRATION; CENTRAL NERVOUS SYSTEMS; GNRH; HYPOTHALAMIC NEURON; LUTEINIZING HORMONE RELEASING HORMONES; NEURAL CELL ADHESION MOLECULES; OLFACTORY EPITHELIUMS; OLFACTORY PLACODE; TERMINAL NERVE; VOMERONASAL NERVE;

NEURONS;

LUTEINIZING HORMONE;

ARTICLE; BRAIN MATURATION; CELL DIFFERENTIATION; CELL MIGRATION; CLINICAL FEATURE; HYPOGONADOTROPIC HYPOGONADISM; KALLMANN SYNDROME; LUTEINIZING HORMONE RELEASE; NERVE CELL DIFFERENTIATION; NONHUMAN; OLFACTORY NERVE; PATHOGENESIS; PRIORITY JOURNAL; VOMERONASAL ORGAN;

EID: 0032929821     PISSN: 1059910X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0029(19990101)44:1<2::AID-JEMT2>3.0.CO;2-4     Document Type: Article

References (69)

1. Arai Y, Murakami S, Seki T, Miyakawa M, Kamiya M. 1997. Origin and migration on GnRH neurons in the chick embryo: an experimental study. In: Pahar IS, Sakuma Y, editors. GnRH Neurons: Gene to Behavior. Tokyo: Brain Shuppan, p 181-195.
2. Barry J. 1976. Characterization and topography of LHRH neurons in the human brain. Neurosci Lett 3:287-291.
3. Boehm N, Roos J, Gasser B. 1994. Luteinizing hormone-releasing hormone (LHRH)-expressing cells in the nasal septum of human fetuses. Dev Brain Res 82:175-180.
4. Bojsen-Moller F. 1975. Demonstration of the terminalis, olfactory, trigeminal and perivascular nerves in the rat nasal septum. J Comp Neurol 159:245-246.
5. Burr HS. 1916. The effects of removal of the olfactory pits in Amblystoma embryos, J Exp Zool 20:27-51.
6. Chiba A, Oka S, Honma Y. 1994. Ontogenetic development of gonadotropin-releasing hormone-like immunoreactive neurons in the brain of chum salmon, Oncorhynchus keta. Neurosci Lett 178:51-54.
7. Cremer H, Lange R, Christoph A, Plomann M, Vopper G, Roes J, Brown R, Baldwin S, Kraemer P, Scheff S, Barthels D, Rajewsky K, Wille W. 1994. Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 367:455-459.
8. Cummings D, Brunjes P. 1995. Migrating luteinizing hormone-releasing hormone (LHRH) neurons and processes are associated with a substrate that expresses S100. Dev Brain Res 88:148-157.
9. Daikoku-Ishido H, Okamura Y, Yanaihara N, Daikoku S. 1990. Development of the hypothalamic luteinizing hormone-releasing hormone-containing neuron system in the rat: in vivo and in transplantation studies. Dev Biol 140:374-387.
10. Dellovade TL, King JA, Millar RP, Rissman EF. 1993. Differential regional distribution of mammalian and chicken-II gonadotropin releasing hormones in musk shrew brain. Neuroendocrinology 58:166-177.
11. Dellovade TL, Hardelin J-P, Soussi-Yanicostas N, Pfaff DW, Schwanzel-Fukuda M, Petit C. 1998. Anosmin-I-immunoreactivity during embryogenesis in a primitive eutherian mammal. Proc Natl Acad Sci USA submitted.
12. Demski LS. 1986. The evolution of neuroanatomical substrates of reproductive behavior: sex steroid and LHRH-specific pathways including the terminal nerve. Am Zool 24:809-830.
13. Demski LS. 1993. Terminal nerve complex. Acta Anat 148:81-95.
14. Demski L, Northcutt RG. 1983. The terminal nerve: a new chemosensory system in vertebrates? Science 220:435-437.
15. Duke VM, Winyard PJ, Thorogood P, Soothill P, Bouloux PMG, Woolf AS. 1995. KAL, a gene mutated in Kallmann's syndrome, is expressed in the first trimester of human development. Mol Cell Endocrinol 110:73-79.
16. 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, Camerino 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.
17. Graziadei PPC, Monti Graziadei GA. 1979. Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Differentiation and structural organization of the olfactory sensory neurons. J Neurocytol 8:1-18.
18. Guillemin R. 1978. Peptides in the brain: The new endocrinology of the neuron. Science 202:390-402.
19. Halpern-Sebold L, Schreibman MP. 1983. Ontogeny of centers containing luteinizing hormone-releasing hormone in the brain of the platyfish (Xiphophorus maculatus) as determined by immunocytochemistry. Cell Tissue Res 229:75-84.
20. Huber GC, Guild RS. 1913. Observation on the peripheral distribution of the nervus terminalis in mammalia. Anat Rec 7:253-272.
21. Jennes L, Stumpf WE. 1980. Luteinizing hormone-releasing hormone (LHRH) systems in the brain of the golden hamster. Cell Tissue Res 209:239-256.
22. Kallmann F, Schoenfeld WA, Barrera SE. 1944. The genetic aspects of primary eunuchoidism. Am J Ment Defic 48:203-236.
23. Kuenzel WJ, Blahser S. 1991. The distribution of gonadotropin-releasing hormone (GnRH) neurons and fibers throughout the chick brain (Gallus domesticus). Cell Tissue Res 264:481-495.
24. Larsell O. 1918. Studies on the nervus terminalis: Mammals. J Comp Neurol 30:3-68.
25. Larsell O. 1950. The nervus terminalis. Ann Otol Rhinol Laryngol 59:414-435.
26. Legouis R, Hardelin J-P, Levilliers J, Claverie J-M, Compain S, Wunderle V, Millasseau P, Le Paslier D, Cohen D, Caterina D, Bougueleret L, Delemarre-Van de Waal H, Lutfalla G, Weissenbach J, Petit C. 1991. The candidate gene for the X-linked Kallmann syndrome encodes a protein related to adhesion molecules. Cell 67:423-435.
27. Locy WA. 1905. On a newly recognized nerve connected with the forebrain of the selachian. Anat Anz 26:33-63.
28. Lutz B, Rugarli EI, Eichele G, Ballabio A. 1993. X-linked Kallmann syndrome: a neuronal targeting defect in the olfactory system? FEBS Lett 325:128-134.
29. Moss RL, McCann SM. 1973. Induction of mating behavior in rats by luteinizing hormone-releasing factor. Science 181:177-179.
30. Munz H, Claas B. 1987. The terminal nerve and its development in teleost fishes. In: Demski LS, Schwanzel-Fukuda M, editors. The terminal nerve (Nervus Terminalis): structure, function and evolution. Ann NY Acad Sci 519:50-59.
31. Murakami S, Seki K, Wakabayashi K, Arai Y. 1991. The ontogeny of luteinizing hormone-releasing hormone (LHRH producing neurons in the chick embryo: possible evidence for migrating LHRH neurons from the olfactory epithelium expressing a highly polysialyated neural cell adhesion molecule. Neurosci Res 12:421-431.
32. Murakami S, Kikuyama S, Arai Y. 1992. The origin of luteinizing hormone-releasing hormone (LHRH) neurons in newts (Cynops pyrrhogaster): the effect of olfactory placode ablation. Cell Tissue Res 269:21-27.
33. Muske L. 1993. Evolution of gonadotropin-releasing hormone (GnRH) neuronal systems. Brain Behav Evol 42:215-230.
34. Muske L, Moore FL. 1987. Luteinizing hormone-releasing hormone immunoreactive neurons in the amphibian brain are distributed along the course of the nervus terminalis. In: Demski LS, Schwanzel-Fukuda M, editors. The terminal nerve (Nervus Terminalis): structure, function and evolution. Ann NY Acad Sci 519:433-446.
35. Muske L, Moore FL. 1988. The nervus terminalis in amphibians: anatomy, chemistry, and relationship with the hypothalamic gonadotropin-releasing hormone system. Brain Behav Evol 32:141-148.
36. Norgren RB, Lehman MN. 1991. Neurons that migrate from the olfactory epithelium in the chick express luteinizing hormone-releasing hormone. Endocrinology 128:1676-1678.
37. Norgren RB, Brackenbury R. 1993. Cell adhesion molecules and the migration of LHRH neurons during development. Dev Biol 160:377-387.
38. Oelschlager HA. 1987. Development of the nervus terminalis in mammals including toothed whales and humans. In: Demski LS, Schwanzel-Fukuda M, editors. The terminal nerve (Nervus Terminalis): structure, function and evolution. Ann NY Acad Sci 519:447-464.
39. Pahar IS, Pfaff DW, Schwanzel-Fukuda M. 1996. Gonadotropin-releasing hormone gene expression in teleosts. Mol Brain Res 41:216-227.
40. Paulin C, Dubois MP, Barry J, Dubois PM. 1977. Immunofluorescence study of LH-RH producing cells in the human fetal hypothalamus. Cell Tissue Res 182:341-345.
41. Pearson AA. 1941. The development of the nervus terminalis in man. J Comp Neurol 75:39-66.
42. Pfaff DW. 1973. Luteinizing hormone-releasing factor potentiates lordosis behavior in hypophysectomized ovariectomized female rats. Science 182:1148-1149.
43. Ronnekleiv O, Resko JA. 1990. Ontogeny of gonadotropin-releasing hormone-containing neurons in early fetal development of rhesus macaques. Endocrinology 126:498-511.
44. Schally AV, Arimura A, Kastin AJ, Matsuo H, Baba Y, Redding TW, Nair RMG, Debelchuk L. 1971. Gonadotropin-releasing hormone: One polypeptide secretion of luteinizing hormone-releasing hormone and follicle stimulating hormone. Science 173:1036-1038.
45. Schwanzel-Fukuda M, Pfaff DW. 1989. Origin of luteinizing hormone-releasing hormone neurons. Nature 338:161-164.
46. Schwanzel-Fukuda M, Pfaff DW. 1995. The structure and function of the nervus terminalis. In: Doty RL, editor. The handbook of clinical olfaction and gustation. New York: Marcel Dekker, Inc., p 835-864.
47. Schwanzel-Fukuda M, Silverman A-J. 1980. The nervus terminalis of the guinea pig: A new luteinizing hormone-releasing hormone neuronal system. J Comp Neurol 191:213-225.
48. Schwanzel-Fukuda M, Robinson JA, Silverman A-J. 1981. The fetal development of the luteinizing hormone-releasing hormone (LHRH) neuronal systems of the guinea pig brain. Brain Res Bull 7:293-315.
49. Schwanzel-Fukuda M, Morrell JI, Pfaff DW. 1985. Ontogenesis of neurons producing luteinizing hormone-releasing hormone (LHRH) in the nervus terminalis of the rat. J Comp Neurol 238:348-364.
50. Schwanzel-Fukuda M, Fadem BH, Garcia MS, Pfaff DW. 1988. Immunocytochemical localization of luteinizing hormone-releasing hormone (LHRH) in the brain and nervus terminalis of the adult and early neonatal gray short-tailed opossum (Monodelphis domestica). J Comp Neurol 276:44-60.
51. 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.
52. Schwanzel-Fukuda M, Abraham S, Crossin KL, Edelman GM, Pfaff DW. 1992. Immunocytochemical demonstration of neural cell adhesion molecule (NCAM) along the migration route of luteinizing hormone-releasing hormone (LHRH) neurons in mice. J Comp Neurol 321:1-18.
53. Schwanzel-Fukuda M, Abraham S, Reinhard GR, Crossin KL, Edelman GM, Pfaff DW. 1994a. Antibody to neural cell adhesion molecule (NCAM) can disrupt the migration of luteinizing hormone-releasing hormone (LHRH) neurons into the mouse brain. J Comp Neurol 342:174-185.
54. Schwanzel-Fukuda M, Pfaff DW, Crossin KL, Cremer H, Hardelin J-P, Petit C. 1995 Luteinizing hormone-releasing hormone (LHRH) neurons migrate normallin neural cell adhesion molecule (N-CAM)-deficient mice. Chemical Senses. Association for Chemoreception Sciences Meeting. Abstract.
55. Schwanzel-Fukuda M, Pfaff DW, Bouloux PMG, Hardelin J-P, Petit C. 1996. Migration of LHRH neurons in early human embryos: association with neural cell adhesion molecules. J Comp Neurol 366:547-557
56. Schwanzel-Fukuda M, Dellovade TL. 1998. Ultrastructure of the nasal mesenchyme during vasculogenesis and formation of the migration route of LHRH neurons originating from the olfactory placode of embryonic mice. Soc Neurosci Abstr. 24:1279.
57. Silverman A-J. 1988. The gonadotropin-releasing hormone neuronal systems: immunocytochemistry. In: Knobil E, Neill J, editors. The physiology of reproduction. New York: Raven Press, p 1283-1304.
58. Soussi-Yanicostas N, Hardelin J-P, Arroyo-Jimenez M, Ardoouin O, Legouis R, Levilliers J, Traincard J, Betton J-M, Cabanie L, Petit C. 1996. Initial characterization of anosmin-1, a putative extracellular matrix protein synthesized by definitive neuronal cell populations in the central nervous system. J Cell Sci 109:1749-1757.
59. Sullivan K, Silverman A-J. 1993. Ontogeny of gonadotropin-releasing hormone in the chick. Neuroendocrinology 58:597-608.
60. Terasawa E, Quanbeck CD, Schultz CA, Burich AJ, Luchansky LL, Claude P. 1993. A primary cell culture system of luteinizing hormone-releasing hormone neurons derived from enbryonic olfactory placode in the rhesus monkey. Endocrinology 133:2379-2390.
61. Von Bartheld CS, Lindorfer HW, Meyer DL. 1987. The nervus terminalis also exists in cyclostomes and birds. Cell Tissue Res 250:431-434.
62. Wirsig CR, Leonard CM. 1987. Terminal nerve damage impairs the mating behavior of the male hamster. Brain Res 417:293-303.
63. Wirsig CR, Getchell TV. 1986. Amphibian terminal nerve: Distribution revealed LHRH and AChe markers. Brain Res 385:10-21.
64. Witkin JW. 1987. Luteinizing hormone-releasing hormone (LHRH) in olfactory systems in primates. In: Demski LS, Schwanzel-Fukuda M, editors. The terminal nerve (Nervus Terminalis): structure, function and evolution. Ann NY Acad Sci 519:174-183.
65. Witkin JW, Silverman A-J. 1983. Luteinizing hormone-releasing hormone in rat olfactory systems. J Comp Neurol 218:426-432.
66. Wray S, Nieburgs A, Elkabes S. 1989a. Spatiotemporal cell expression of luteinizing hormone-releasing hormone in the prenatal mouse: evidence for an embryonic origin in the olfactory placode. Dev Brain Res 46:309-318.
67. Wray S, Grant P, Gainer H. 1989b. Evidence that cells expressing luteinizing hormone-releasing hormone mRNA are derived from progenitor cells in the olfactory placode. Proc Natl Acad Sci USA 86:8132-8136.
68. Wray S, Key S, Qualls R, Fueshko SM. 1994. Rapid communication: a subset of peripherin positive olfactory axons delineates the luteinizing hormone-releasing hormone neuronal migratory pathway in developing mouse. Dev Biol 166:349-354.
69. Wright DE, Demski LS. 1990. Gonadotropin hormone-releasing hormone (GnRH)-immunoreactivity in the brains of primitive bony fishes. Soc Neurosci Abstr 16:127.