Migration of luteinizing hormone-releasing hormone (LHRH) neurons in early human embryos

Journal of Comparative Neurology

Volumn 366, Issue 3, 1996, Pages 547-557

  Schwanzel Fukuda, M ^a   Crossin, K L ^b   Pfaff, D W ^a   Bouloux, P M G ^c   Hardelin, J P ^d   Petit, C ^d  

^a ROCKEFELLER UNIVERSITY   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c ROYAL FREE HOSPITAL   (United Kingdom)

^d INSTITUT PASTEUR   (France)

Author keywords

gonadotropin hormone releasing hormone; Nervus terminalis (terminal nerve); neural cell adhesion molecule; olfactory placode; sialic acid

Indexed keywords

ANTISERUM; GONADORELIN; NERVE CELL ADHESION MOLECULE; POLYSIALIC ACID;

ARTICLE; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; HUMAN; HUMAN TISSUE; IMMUNOREACTIVITY; NERVE CELL; ONTOGENY; PRIORITY JOURNAL;

ANTIBODIES, MONOCLONAL; ANTIBODY SPECIFICITY; BRAIN CHEMISTRY; EMBRYO; GONADOTROPIN-RELEASING HORMONE; HUMANS; NEURAL CELL ADHESION MOLECULES; NEURONS; NOSE; POLYSACCHARIDES; SIALIC ACIDS;

EID: 0030068102     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19960311)366:3<547::AID-CNE12>3.0.CO;2-M     Document Type: Article

References (34)

1. Boehm, N., J. Roos, and B. Gasser (1994) Luteinizing hormone-releasing hormone (LHRH)-expressing cells in the nasal septum of human fetuses. Dev. Brain Res. 52:175-180
2. Bonfanti, L., S. Olive, D.A. Poulain, and D.T, Theodosis (1992) Mapping of the distribution of polysialated neural cell adhesion molecule throughout the central nervous system of the adult rat: an immunohistochemical study. Neuroscience 49:419-436.
3. Bossy, J. (1980) Development of olfactory and related structures in staged human embryos. Anat. Embryol. (Berl.) 161:225-236.
4. Chiba, A., S. Oka, and Y Honma (1994) Ontogenetic development of gonadotropin-releasing hormone-like immunoreaetive neurons in the brain of the chum salmon, Oncorhynchus keta. Neurosci. Lett. 178:51-54.
5. Chuong, C -M., D.A. McClain, P. Street, and G.M. Edelman (1982) Neural cell adhesion molecules in rodent brains isolated by monoclonal antibodies with cross-species reactivity Proc Natl. Acad. Sci. U.S.A. 79:4234-4238.
6. Crossin, K.L., G.M Edelman, and B.A. Cunningham (1984) Mapping of three carbohydrate attachment sites in embryonic and adult forms of the neural cell adhesion molecule. J. Cell Biol. 99:1848-1855.
7. Cunningham, B A., S. Hoffman, U. Rutishauser, J.J. Hemperly, and G.M. Edelman (1983) Molecular topography of the neural cell adhesion molecule N-CAM: surface orientation and location of sialic acid-rich and binding regions. Proc Natl. Acad. Sci. U.S.A. 80:3116-3120.
8. Daikoku-Ishido, H., Y. Okamura, N Yanaihara, and S. Daikoku (1990) Development of the hypothalamic luteinizing hormone-releasing hormone-containing neuron system in the rat: in vivo and in vitro transplantation studies. Dev. Biol. 140.374-387.
9. Edelman, G M., and C.-M. Chuong (1982) Embryonic to adult conversion of neural cell adhesion molecules in normal and staggerer mice. Proc. Natl Acad, Sci. U.S.A. 79:7036-7040.
10. Edelman, G.M., and K.L Crossin (1991) Cell adhesion molecules. Annu Rev. Biochem. 60:155-190
11. Hoffman, S., and G.M. Edelman (1983) Kinetics of homophilic binding by E and A forms of the neural cell adhesion molecule. Proc. Natl. Acad Sci U.S.A. 80.5762-5766
12. Miragall, F., G. Kadmon, and M Schactner (1989) Expression of L1 and N-CAM cell adhesion molecules during development of the mouse olfactory system Dev. Biol. 135:272-286.
13. Murakami, S., T. Seki, K Wakabayashi, and Y. Arai (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 polysialated neural cell adhesion molecule. Neurosci. Res. 12:421-431.
14. Muske, L., and F.L. Moore (1990) Ontogeny of gonadotropin-releasing hormone neuronal systems in amphibians. Brain Res. 534:177-187.
15. Nakane, P. (1968) Simultaneous localization of multiple tissue antigens using the peroxidase-labeled method: a study on pituitary glands of the rat. J. Histochem. Cytochem 16:557-560.
16. Norgren, R.B., and M.N Lehman (1991) Neurons that migrate from the olfactory epithelium in the chick express luteinizing hormone-releasing hormone. Endocrinology 128:1676-1678.
17. O'Rahilly, R., and F. Muller (1994) The Embryonic Human Brain: An Atlas of Developmental Stages. New York. Wiley-Liss, John Wiley & Sons, Inc
18. Pahar, I S., M. Iwata, D.W. Pfaff, and M. Schwanzel-Fukuda (1995) Embryonic development of gonadotropin-releasing hormone neurons in the sockeye salmon. J. Comp. Neurol. 562:256-270.
19. Pearson, A.A. (1941) The development of the nervus terminalis in man. J. Comp. Neurol. 75:36-66.
20. Pearson, A.A (1942) The development of the olfactory nerve, the nervus terminalis, and the vomeronasal nerve in man. Ann. Otol. Rhinol. Laryngol. 51:317-333.
21. Pellier, V., and L, Astic (1994) Histochemical and immunocytochemical study of the migration of neurons from the rat olfactory placode. Cell Tissue Res. 275:587-598.
22. Rønnekleiv, O., and J A. Resko (1990) Ontogeny of gonadotropin-releasing hormone-containing neurons in early fetal development of rhesus macaques. Endocrinology 126.498-511
23. Rougon, G., C. Dubois, N. Buckley, J.L, Magnani, and W. Zollinger (1986) A monoclonal antibody against meningococcus group B polysaccharides distinguishes embryonic from adult N-CAM. J. Cell Biol. 103:2429-2437.
24. Rousselot, P., and F. Nottebohm (1995) Expression of polysialylated N-CAM in the central nervous system of adult canaries and its possible relation to function. J Comp. Neurol 356:629-640.
25. Rousselot, P., C. Lois, and A. Alvarez-Buylla (1995) Embryonic (PSA) N-CAM reveals chains of migrating neuroblasts between the lateral ventricle and the olfactory bulb of adult mice. J. Comp. Neurol. 351:51-61
26. Rutishauser, U. (1992) NCAM and its polysialic moiety, a mechanism for pull/push regulation of cell interactions during development? Development [Suppl.] 99-104
27. Rutishauser. U., M. Watanabe, J. Silver, F.A. Troy, and E.R. Vimr (1985) Specific alteration of N-CAM-mediated cell adhesion by an endoneuraminidase. J. Cell Biol. 101:1842-1849.
28. Schwanzel-Fukuda, M., and D.W. Pfaff (1989) Origin of luteinizing hormone-releasing hormone neurons Nature 338:161-164.
29. Schwanzel-Fukuda, M., D. Bick, and D.W. Pfaff (1989) Luteinizing hormone-releasing hormone (LHRH)-expressing cells do not migrate normally in an inherited hypogonadal (Kallmann) syndrome. Mol. Brain Res 6:311-326.
30. Schwanzel-Fukuda, M., S. Abraham, K.L. Crossin, G.M. Edelman, and D.W. Pfaff (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.
31. Sunshine, J., K. Balak, U. Rutishauser, and M. Jacobson (1987) Changes in neural cell adhesion molecule (N-CAM) structure during vertebrate neural development. Proc. Natl. Acad. Sci. U.S.A. 84:5986-5900.
32. Wray, S., P. Grant, and H. Gainer (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. U.S.A. 86:8132-8136.
33. Yoshida, K., G.A. Schwarting, U Rutishauser, and J.E. Crandall (1995) LHRH neuronal migration is disrupted by enzymatic removal of polysialic acid in embryonic mice Soc. Neurosci. Abstr. 21(part 2):1528.
34. Zheng, L.-M., D.W. Pfaff, and M. Schwanzel-Fukuda (1992) Electron microscopic identification of luteinizing hormone-releasing hormone (LHRH)-immunoreactive neurons in the medial olfactory placode and basal forebrain of embryonic mice Neuroscience 46.407-418.