Androgen receptor gene expression in the developing and adult zebrafish brain

Developmental Dynamics

Volumn 237, Issue 10, 2008, Pages 2987-2995

  Gorelick, Daniel A ^a,b   Watson, William ^a   Halpern, Marnie E ^a  

^a GEOPHYSICAL LABORATORY   (United States)

^b NONE   (United States)

Author keywords

Androgen; Embryo; Hypothalamus; Olfactory placode; Pronephros

Indexed keywords

ANDROGEN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN REGION; GENE EXPRESSION; GENETIC TRANSCRIPTION; IN SITU HYBRIDIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; SEX DIFFERENCE; SEXUAL BEHAVIOR; ZEBRA FISH;

AGING; ANIMALS; BRAIN; EMBRYO, NONMAMMALIAN; ENDOCRINE SYSTEM; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GERM CELLS; HUMANS; LARVA; RECEPTORS, ANDROGEN; ZEBRAFISH;

DANIO RERIO; MAMMALIA; VERTEBRATA;

EID: 54549098139     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21700     Document Type: Article

References (70)

1. Arnold AP, Breedlove SM. 1985. Organizational and activational effects of sex steroids on brain and behavior: a reanalysis. Horm Behav 19:469-498.
2. Asadi FK, Dimaculangan DD, Berger FG. 1994. Androgen regulation of gene expression in primary epithelial cells of the mouse kidney. Endocrinology 134:1179-1187.
3. Bazer GT, Ebbesson SOE, Reynolds JB, Bailey RP. 1987. A cobalt-lysine study of primary olfactory projections in king salmon fry (Oncorhynchus tshawytscha Walbaum). Cell Tissue Res 248:499-503.
4. Becerra M, Manso MJ, Rodriguez-Moldes I, Anadon R. 1994. Primary olfactory fibres project to the ventral telencephalon and preoptic region in trout (Salmo trutta): a developmental immunocytochemical study. J Comp Neurol 342:131-143.
5. Berger FG, Watson G. 1989. Androgen-regulated gene expression. Annu Rev Physiol 51:51-65.
6. Borg B. 1994. Androgens in teleost fishes. Comp Biochem Physiol C 109:219-245.
7. Brantley RK, Marchaterre MA, Bass AH. 1993. Androgen effects on vocal muscle structure in a teleost fish with inter- and intra-sexual dimorphism. J Morphol 216:305-318.
8. Capel B. 2000. The battle of the sexes. Mech Dev 92:89-103.
9. Cardwell JR, Stacey NE, Lang SLC, Tan ESP, McAdam DSO. 1995. Androgen increases olfactory receptor response to a vertebrate sex pheromone. J Comp Physiol [A] 176:55-61.
10. Chai C, Liu YW, Chan WK. 2003. Ff1b is required for the development of steroidogenic component of the zebrafish interrenal organ. Dev Biol 260:226-244.
11. Cooke B, Hegstrom CD, Villeneuve LS, Breedlove SM. 1998. Sexual differentiation of the vertebrate brain: principles and mechanisms. Front Neuroendocrinol 19:323-362.
12. Crews D, Silver R. 1985. Reproductive physiology and behavior interactions in nonmammalian vertebrates. In: Adler NT, Pfaff DW, Goy RW, editors. Handbook of behavioral neurobiology. Vol. 7. New York: Plenum Press. p xxi, 797.
13. Cupp AS, Skinner MK. 2001. Actions of the endocrine disruptor methoxychlor and its estrogenic metabolite on in vitro embryonic rat seminiferous cord formation and perinatal testis growth. Reprod Toxicol 15:317-326.
14. de Waal P, Wang D, Nijenhuis W, Schulz R, Bogerd J. 2008. Functional characterization and expression analysis of the androgen receptor in zebrafish (Danio rerio) testis. Reproduction.
15. Drummond I. 2003. Making a zebrafish kidney: a tale of two tubes. Trends Cell Biol 13:357-365.
16. Fenske M, Segner H. 2004. Aromatase modulation alters gonadal differentiation in developing zebrafish (Danio rerio). Aquat Toxicol 67:105-126.
17. Folgueira M, Anadon R, Yanez J. 2004. An experimental study of the connections of the telencephalon in the rainbow trout (Oncorhynchus mykiss). I. Olfactory bulb and ventral area. J Comp Neurol 480:180-203.
18. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J. 1999. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531-1545.
19. Gamse JT, Shen Y-C, Thisse C, Thisse B, Raymond PA, Halpern ME, Liang JO. 2002. Otx5 regulates genes that show circadian expression in the zebrafish pineal complex. Nat Genet 30:117-121.
20. Gao W, Bohl CE, Dalton JT. 2005. Chemistry and structural biology of androgen receptor. Chem Rev 105:3352-3370.
21. Gelinas D, Callard GV. 1997. Immunolocalization of aromatase- and androgen receptor-positive neurons in the goldfish brain. Gen Comp Endocrinol 106:155-168.
22. Harbott LK, Burmeister SS, White RB, Vagell M, Fernald RD. 2007. Androgen receptors in a cichlid fish, Astatotilapia burtoni: structure, localization, and expression levels. J Comp Neurol 504:57-73.
23. Hart BL, Leedy MG. 1985. Neurological basis of male sexual behavior: a comparative analysis. In: Adler NT, Pfaff DW, Goy RW, editors. Handbook of behavioral neurobiology. Vol. 7. New York: Plenum Press. p xxi, 797.
24. Holbech H, Kinnberg K, Petersen GI, Jackson P, Hylland K, Norrgren L, Bjerregaard P. 2006. Detection of endocrine disrupters: evaluation of a Fish Sexual Development Test (FSDT). Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 144:57-66.
25. Honkanen T, Ekstrom P. 1990. An immunocytochemical study of the olfactory projections in the three-spined stickleback, Gasterosteus aculeatus, L. J Comp Neurol 292:65-72.
26. Honkanen T, Ekstrom P. 1991. An immunocytochemical study of the development of the olfactory system in the three-spined stickleback (Gasterosteus aculeatus L., Teleostei). Anat Embryol (Berl) 184:469-477.
27. Hossain MS, Larsson A, Scherbak N, Olsson PE, Orban L. 2007. Zebrafish androgen receptor: isolation, molecular, and biochemical characterization. Biol Reprod 78:361-369.
28. Hsu H-J, Hsiao P, Kuo M-W, Chung B-C. 2002. Expression of zebrafish cyp11a1 as a maternal transcript and in yolk syncytial layer. Gene Expr Patterns 2:219-222.
29. Hsu HJ, Lin G, Chung BC. 2003. Parallel early development of zebrafish interrenal glands and pronephros: differential control by wt1 and ff1b. Development 130:2107-2116.
30. Ikeuchi T, Todo T, Kobayashi T, Nagahama Y. 2001. Two subtypes of androgen and progestogen receptors in fish testes. Comp Biochem Physiol B Biochem Mol Biol 129:449-455.
31. Jaillon O, Aury J-M, Brunet F, Petit J-L, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A, Nicaud S, Jaffe D, Fisher S, Lutfalla G, Dossat C, Segurens B, Dasilva C, Salanoubat M, Levy M, Boudet N, Castellano S, Anthouard V, Jubin C, Castelli V, Katinka M, Vacherie B, Biemont C, Skalli Z, Cattolico L, Poulain J, de Berardinis V, Cruaud C, Duprat S, Brottier P, Coutanceau J-P, Gouzy J, Parra G, Lardier G, Chapple C, McKernan KJ, McEwan P, Bosak S, Kellis M, Volff J-N, Guigo R, Zody MC, Mesirov J, Lindblad-Toh K, Birren B, Nusbaum C, Kahn D, Robinson-Rechavi M, Laudet V, Schachter V, Quetier F, Saurin W, Scarpelli C, Wincker P, Lander ES, Weissenbach J, Roest Crollius H. 2004. Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate protokaryotype. Nature 431:946-957.
32. Jorgensen A, Andersen O, Bjerregaard P, Rasmussen LJ. 2007. Identification and characterisation of an androgen receptor from zebrafish Danio rerio. Comp Biochem Physiol C Toxicol Pharmacol 146:561-568.
33. Kaslin J, Panula P. 2001. Comparative anatomy of the histaminergic and other aminergic systems in zebrafish (Danio rerio). J Comp Neurol 440:342-377.
34. Koyama Y, Satou M, Oka Y, Ueda K. 1984. Involvement of the telencephalic hemispheres and the preoptic area in sexual behavior of the male goldfish, Carassius auratus: a brain-lesion study. Behav Neural Biol 40:70-86.
35. Liang JO, Etheridge A, Hantsoo L, Rubinstein AL, Nowak SJ, Izpisua Belmonte JC, Halpern ME. 2000. Asymmetric nodal signaling in the zebrafish diencephalon positions the pineal organ. Development 127:5101-5112.
36. Martineau J, Nordqvist K, Tilmann C, Lovell-Badge R, Capel B. 1997. Male-specific cell migration into the developing gonad. Curr Biol 7:958-968.
37. McAbee MD, DonCarlos LL. 1998. Ontogeny of region-specific sex differences in androgen receptor messenger ribonucleic acid expression in the rat forebrain. Endocrinology 139:1738-1745.
38. Merlet J, Moreau E, Habert R, Racine C. 2007a. Development of fetal testicular cells in androgen receptor deficient mice. Cell Cycle 6:2258-2262.
39. Merlet J, Racine C, Moreau E, Moreno SG, Habert R. 2007b. Male fetal germ cells are targets for androgens that physiologically inhibit their proliferation. Proc Natl Acad Sci U S A 104:3615-3620.
40. Morris JA, Jordan CL, Breedlove SM. 2004. Sexual differentiation of the vertebrate nervous system. Nat Neurosci 7:1034-1039.
41. Murphy CA, Stacey NE. 2002. Methyl-testosterone induces male-typical ventilatory behavior in response to putative steroidal pheromones in female round gobies (Neogobius melanostomus). Horm Behav 42:109-115.
42. Nunez JL, Huppenbauer CB, McAbee MD, Juraska JM, DonCarlos LL. 2003. Androgen receptor expression in the developing male and female rat visual and prefrontal cortex. J Neurobiol 56:293-302.
43. Orn S, Holbech H, Madsen TH, Norrgren L, Petersen GI. 2003. Gonad development and vitellogenin production in zebrafish (Danio rerio) exposed to ethinylestradiol and methyltestosterone. Aquat Toxicol 65:397-411.
44. Orn S, Yamani S, Norrgren L. 2006. Comparison of vitellogenin induction, sex ratio, and gonad morphology between zebrafish and Japanese medaka after exposure to 17alpha-ethinylestradiol and 17beta-trenbolone. Arch Environ Contam Toxicol 51:237-243.
45. Pandian TJ, Sheela SG. 1995. Hormonal induction of sex reversal in fish. Aquaculture 138:1-22.
46. Parikh VN, Clement TS, Fernald RD. 2006. Androgen level and male social status in the African cichlid, Astatotilapia burtoni. Behav Brain Res 166:291-295.
47. Pauls S, Geldmacher-Voss B, Campos-Ortega JA. 2001. A zebrafish histone variant H2A.F/Z and a transgenic H2A.F/Z: GFP fusion protein for in vivo studies of embryonic development. Dev Genes Evol 211:603-610.
48. Pelegri F, Knaut H, Maischein H-M, Schulte-Merker S, Nusslein-Volhard C. 1999. A mutation in the zebrafish maternal-effect gene nebel affects furrow formation and vasa RNA localization. Curr Biol 9:1431-1440.
49. Pfaff D, Modianos D. 1985. Neural mechanisms of female reproductive behavior. In: Adler NT, Pfaff DW, Goy RW, editors. Handbook of behavioral neurobiology. Vol. 7. New York: Plenum Press. p xxi, 797.
50. Postlethwait J, Amores A, Cresko W, Singer A, Yan Y-L. 2004. Subfunction partitioning, the teleost radiation and the annotation of the human genome. Trends Genet 20:481-490.
51. Quinkler M, Bujalska IJ, Kaur K, Onyimba CU, Buhner S, Allolio B, Hughes SV, Hewison M, Stewart PM. 2005. Androgen receptor-mediated regulation of the alpha-subunit of the epithelial sodium channel in human kidney. Hypertension 46:787-798.
52. Rink E, Wullimann MF. 2001. The teleostean (zebrafish) dopaminergic system ascending to the subpallium (striatum) is located in the basal diencephalon (posterior tuberculum). Brain Res 889:316-330.
53. Rodriguez-Mari A, Yan YL, Bremiller RA, Wilson C, Canestro C, Postlethwait JH. 2005. Characterization and expression pattern of zebrafish Anti-Mullerian hormone (Amh) relative to sox9a, sox9b, and cyp19a1a, during gonad development. Gene Expr Patterns 5:655-667.
54. Serluca FC, Fishman MC. 2001. Pre-pattern in the pronephric kidney field of zebrafish. Development 128:2233-2241.
55. Shah NM, Pisapia DJ, Maniatis S, Mendelsohn MM, Nemes A, Axel R. 2004. Visualizing sexual dimorphism in the brain. Neuron 43:313-319.
56. Simerly RB. 2002. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci 25:507-536.
57. Simerly RB, Chang C, Muramatsu M, Swanson LW. 1990. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J Comp Neurol 294:76-95.
58. Soma KK, Francis RC, Wingfield JC, Fernald RD. 1996. Androgen regulation of hypothalamic neurons containing gonadotropin-releasing hormone in a cichlid fish: integration with social cues. Horm Behav 30:216-226.
59. Takahashi T. 1977. Juvenile hermaphroditism in the zebrafish, Brachydanio rerio. Bull Fac Fish Hokkaido Univ 28:57-65.
60. Thisse C, Thisse B. 2008. High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat Protoc 3:59-69.
61. To TT, Hahner S, Nica G, Rohr KB, Hammerschmidt M, Winkler C, Allolio B. 2007. Pituitary-interrenal interaction in Zebrafish interrenal organ development. Mol Endocrinol 21:472-485.
62. Walker C. 1999. Haploid screens and gamma-ray mutagenesis. Methods Cell Biol 60:43-70.
63. Weidinger G, Wolke U, Koprunner M, Klinger M, Raz E. 1999. Identification of tissues and patterning events required for distinct steps in early migration of zebrafish primordial germ cells. Development 126:5295-5307.
64. Weidinger G, Stebler J, Slanchev K, Dumstrei K, Wise C, Lovell-Badge R, Thisse C, Thisse B, Raz E. 2003. dead end, a novel vertebrate germ plasm component, is required for zebrafish primordial germ cell migration and survival. Curr Biol 13:1429-1434.
65. Werner MH, Huth JR, Gronenborn AM, Clore GM. 1996. Molecular determinants of mammmalian sex. Trends Biochem Sci 21:302-308.
66. Westerfield M. 1993. The Zebrafish book: a guide for the laboratory use of zebrafish (Brachydanio rerio). Eugene, OR: University of Oregon Press. 1 v. (various pagings) p.
67. Wingert RA, Selleck R, Yu J, Song HD, Chen Z, Song A, Zhou Y, Thisse B, Thisse C, McMahon AP, Davidson AJ. 2007. The cdx genes and retinoic acid control the positioning and segmentation of the zebrafish pronephros. PLoS Genet 3:1922-1938.
68. Wullimann MF, Mueller T. 2004. Teleostean and mammalian forebrains contrasted: evidence from genes to behavior. J Comp Neurol 475:143-162.
69. Wullimann MF, Rupp B, Reichert H. 1996. Neuroanatomy of the zebrafish brain. Amsterdam: Birkhauser.
70. Zhou X, Kudo A, Kawakami H, Hirano H. 1996. Immunohistochemical localization of androgen receptor in mouse testicular germ cells during fetal and postnatal development. Anat Rec 245:509-518.