Nasal embryonic LHRH factor plays a role in the developmental migration and projection of gonadotropin-releasing hormone 3 neurons in zebrafish

Developmental Dynamics

Volumn 238, Issue 1, 2009, Pages 66-75

  Palevitch, Ori ^a   Abraham, Eytan ^b   Borodovsky, Natalya ^c   Levkowitz, Gil ^c   Zohar, Yonathan ^b   Gothilf, Yoav ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

GnRH; Kallmann syndrome; NELF; Neuronal migration; Zebrafish

Indexed keywords

COMPLEMENTARY DNA; GONADORELIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MATURATION; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GENE; NELF GENE; NERVE CELL; NERVE FIBER; NERVE FIBER GROWTH; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIKARYON; PRIORITY JOURNAL; ZEBRA FISH;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BRAIN; CELL MOVEMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKDOWN TECHNIQUES; GONADOTROPIN-RELEASING HORMONE; HUMANS; IN SITU HYBRIDIZATION; MOLECULAR SEQUENCE DATA; NEURONS; PYRROLIDONECARBOXYLIC ACID; SEQUENCE ALIGNMENT; TRANSCRIPTION FACTORS; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 58149242345     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21823     Document Type: Article

References (34)

1. Abraham E, Palevitch O, Ijiri S, Du S-J, Gothilf Y, Zohar Y. 2008. Early development of forebrain gonadotropin-releasing hormone neurones and the role of GnRH as an autocrine migration factor. J Neuroendocrinol 20:394-405.
2. Bhagavath B, Layman LC. 2007. The genetics of hypogonadotropic hypogonadism. Semin Reprod Med 25:272-286.
3. Cadman SM, Kim SH, Hu Y, Gonzalez-Martinez D, Bouloux PM. 2007. Molecular pathogenesis of Kallmann's syndrome. Horm Res 67:231-242.
4. Cariboni A, Maggi R, Parnavelas JG. 2007. From nose to fertility: the long migratory journey of gonadotropin-releasing hormone neurons. Trends Neurosci 30:638-644.
5. Dubois EA, Zandbergen MA, Peute J, Goos HJ. 2002. Evolutionary development of three gonadotropin-releasing hormone (GnRH) systems in vertebrates. Brain Res Bull 57:413-418.
6. Gao C, Noden DM, Norgren RB Jr. 2000. LHRH neuronal migration: heterotypic transplantation analysis of guidance cues. J Neurobiol 42:95-103.
7. Gore AC. 2002. GnRH: the master molecule of reproduction. Norwell, MA: Kluwer Academic Publishers.
8. Kallmann FJ, Schoenfeld WA, Barrera SE. 1944. The genetic aspects of primary eunuchoidism. Am J Ment Defic 158:203-236.
9. 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.
10. Kramer PR, Wray S. 2001. Nasal embryonic LHRH factor (NELF) expression within the CNS and PNS of the rodent. Brain Res Gene Expr Patterns 1:23-26.
11. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567-580.
12. Kuo MW, Lou SW, Postlethwait J, Chung BC. 2005. Chromosomal organization, evolutionary relationship, and expression of zebrafish GnRH family members. J Biomed Sci 12:629-639.
13. Marín O, Rubenstein JL. 2003. Cell migration in the forebrain. Annu Rev Neurosci 26:441-483.
14. Miura K, Acierno JS Jr, Seminara SB. 2004. 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 49:265-268.
15. Murakami S, Seki T, Rutishauser U, Arai Y. 1998. LHRH neurons migrate into the trigeminal nerve when the developing olfactory nerve fibers are physically interrupted in chick embryos. Gen Comp Endocrinol 112:312-321.
16. Naftolin F, Harris GW, Bobrow M. 1971. Effect of purified luteinizing hormone releasing factor on normal and hypogonadotrophic anosmic men. Nature 232:496-497.
17. Nasevicius A, Ekker SC. 2000. Effective targeted gene 'knockdown' in zebrafish. Nat Genet 26:216-220.
18. Okubo K, Nagahama Y. 2008. Structural and functional evolution of gonadotropin-releasing hormone in vertebrates. Acta Physiol (Oxf) 193:3-15.
19. Palevitch O, Kight K, Abraham E, Wray S, Zohar Y, Gothilf Y. 2007. Ontogeny of the GnRH systems in zebrafish brain: in situ hybridization and promoter-reporter expression analyses in intact animals. Cell Tissue Res 327:313-322.
20. Pitteloud N, Quinton R, Pearce S, Raivio T, Acierno J, Dwyer A, Plummer L, Hughes V, Seminara S, Cheng YZ, Li WP, Maccoll G, Eliseenkova AV, Olsen SK, Ibrahimi OA, Hayes FJ, Boepple P, Hall JE, Bouloux P, Mohammadi M, Crowley W. 2007. Digenic mutations account for variable phenotypes in idiopathic hypogonadotropic hypogonadism. J Clin Invest 117:457-463.
21. Powell JF, Krueckl SL, Collins PM, Sherwood NM. 1996. Molecular forms of GnRH in three model fishes: rockfish, medaka and zebrafish. J Endocrinol 150:17-23.
22. Schwanzel-Fukuda M. 1999. Origin and migration of luteinizing hormone-releasing hormone neurons in mammals. Microsc Res Tech 44:2-10.
23. Schwanzel-Fukuda M, Pfaff DW. 1989. Origin of luteinizing hormone-releasing hormone neurons. Nature 338:161-164.
24. 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. Brain Res Mol Brain Res 6:311-326.
25. Schwarting GA, Wierman ME, Tobet SA. 2007. Gonadotropin-releasing hormone neuronal migration. Semin Reprod Med 25:305-312.
26. Steven C, Lehnen N, Kight K, Ijiri S, Klenke U, Harris WA, Zohar Y. 2003. Molecular characterization of the GnRH system in zebrafish (Danio rerio): cloning of chicken GnRH-II, adult brain expression patterns and pituitary content of salmon GnRH and chicken GnRH-II. Gen Comp Endocrinol 133:27-37.
27. Tobet SA, Schwarting GA. 2006. Minireview: recent progress in gonadotropin-releasing hormone neuronal migration. Endocrinology 147:1159-1165.
28. Torgersen J, Nourizadeh-Lillabadi R, Husebye H, Aleström P. 2002. In silico and in situ characterization of the zebrafish (Danio rerio) gnrh3 (sGnRH) gene. BMC Genom 3:25.
29. Westerfield M. 1995. The zebrafish book. Oregon: University of Oregon Press.
30. White RB, Fernald RD. 1998. Genomic structure and expression sites of three gonadotropin-releasing hormone genes in one species. Gen Comp Endocrinol 112:17-25.
31. Whitlock KE, Illing N, Brideau NJ, Smith KM, Twomey S. 2006. Development of GnRH cells: setting the stage for puberty. Mol Cell Endocrinol 25:39-50.
32. Wray S. 2002. Development of gonadotropin-releasing hormone-1 neurons. Front Neuroendocrinol 23:292-316.
33. 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 U S A 86:8132-8136.
34. Yamamoto N, Uchiyama H, Ohki-Hamazaki H, Tanaka H, Ito H. 1996. Migration of GnRH-immunoreactive neurons from the olfactory placode to the brain: a study using avian embryonic chimeras. Brain Res Dev Brain Res 95:234-244.