Sexual dimorphic expression of DMRT1 and Sox9a during gonadal differentiation and hormone-induced sex reversal in the teleost fish nile tilapia (Oreochromis niloticus)

Developmental Dynamics

Volumn 237, Issue 1, 2008, Pages 297-306

  Kobayashi, Tohru ^a,b,c   Kajiura Kobayashi, Hiroko ^a,b   Guan, Guijun ^b   Nagahama, Yoshitaka ^a,b  

^a NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c FISHERIES RESEARCH AGENCY   (Japan)

Author keywords

DMRT1; Germ cell supporting cell; Gonial proliferation; Sertoli cell; Sex reversal; Sox9; Teleost; Testicular differentiation; Testis; Tilapia

Indexed keywords

ANDROGEN;

ANIMAL EXPERIMENT; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DMRT1 GENE; FEMALE; GENE; GENE EXPRESSION; GERM CELL; GONAD DEVELOPMENT; IN SITU HYBRIDIZATION; MALE; NONHUMAN; OREOCHROMIS NILOTICUS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEX DIFFERENCE; SEX DIFFERENTIATION; SEXUAL DEVELOPMENT; SOX9A GENE; TELEOST; TESTIS;

ANDROGENS; ANIMALS; CELL DIFFERENTIATION; CICHLIDS; FEMALE; FISH PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GONADS; HIGH MOBILITY GROUP PROTEINS; HORMONES; IN SITU HYBRIDIZATION; MALE; OVARY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEX DIFFERENTIATION; SEX REVERSAL, GONADAL; TESTIS; TIME FACTORS; TRANSCRIPTION FACTORS;

OREOCHROMIS NILOTICUS; TELEOSTEI; TILAPIA;

EID: 38149067419     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21409     Document Type: Article

References (52)

1. Baroiller JF, Guiguen Y, Fostier A. 1999. Endocrine and environmental aspects of sex differentiation in fish. Cell Mol Life Sci 55:910-931.
2. Bennett CP, Docherty Z, Robb SA, Ramani P, Hawkins JR, Grant D. 1993. Deletion 9p and sex reversal. J Med Genet 30:518-520.
3. Bhandari RK, Nakamura M, Kobayashi T, Nagahama Y. 2006. Suppression of steroidogenic enzyme expression during androgen-induced sex reversal in Nile tilapia (Oreochromis niloticus). Gen Comp Endocrinol 145:20-24.
4. Capel B. 2000. The battle of the sexes. Mech Dev 92:89-103.
5. Carrasco LAP, Penman DJ, Villalos SA, Bromage N. 1999. The effects of oral administration with 17a-methyltestosterone on chromosomal synapsis in Oreochromis niloticus (Pisces, Cichlidae). Mutat Res 430:87-98.
6. Chen JK, Heckert LL. 2001. Dmrt1 expression is regulated by follicle-stimulating hormone and phorbol esters in postnatal Sertoli cells. Endocrinology 142:1167-1178.
7. Chiang EF, Pai CI, Wyatt M, Yan YL, Postlethwait J, Chung B. 2001. Two sox9 genes on duplicated zebrafish chromosomes: expression of similar transcription activities in distinct sites. Dev Biol 231:149-163.
8. Coschigano KT, Wensink PC. 1993. Sex specific transcriptional regulation by male and female doublesex proteins of Drosophila. Genes Dev 7:42-54.
9. De Grandi A, Calvari V, Bertini V, Bulfone A, Peverali G, Camerino G, Borsani G, Guioli S. 2000. The expression pattern of a mouse doublesex-related gene is consistent with a role in gonadal differentiation. Mech Dev 90:323-326.
10. Erdman SE, Burtis KC. 1993. The Drosophila doublesex proteins share a novel zinc finger related DNA binding domain. EMBO J 12:527-535.
11. Flejter WL, Fergestad J, Gorski J, Varvill T, Chandrasekharappa S. 1998. A gene involved in XY sex reversal is located on chromosome 9, distal to marker D9S1779. Am J Hum Genet 63:794-802.
12. Guan G, Kobayashi T, Nagahama Y. 2000. Sexually dimorphic expression of two types of DM (Doublesex/mab-3)-domain genes in a teleost fish, the tilapia (Oreochromis niloticus). Biochem Biophys Res Commun 272:662-666.
13. Guo Y, Cheng H, Huang X, Gao S, Yu H, Zhou R. 2005. Gene structure, multiple alternative splicing, and expression in gonads of zebrafish Dmrt1. Biochem Biophys Res Commun 330:950-957.
14. He CL, Du JL, Lee YH, Sun LT, Chang CF. 2003. Differential Dmrt1 transcripts in gonads of the protandrous black porgy, Acanthopagrus schlegeli. Cytogenet Genome Res 101:309-313.
15. Jameson RV, Zhou SX, Tan SS, Tam PPL. 1997. X-chromosome inactivation during the development of the male urogenital ridge of the mouse. Int J Dev Biol 41:49-55.
16. a mouse embryos. Dev Biol 199:235-244.
17. Kettlewell JR, Raymond CS, Zarkower D. 2000. Temperature-dependent expression of turtle Dmrt1 prior to sexual differentiation. Genesis 26:174-178.
18. Kobayashi T, Sakai N, Adachi S, Asahina K, Iwasawa H, Nagahama Y. 1993. 17α,20α-dihydroxy-4-pregnen-3-one is naturally occurring spermiation-inducing hormone in a frog, Rana nigromaculata. Endocrinology 133:321-327.
19. Kobayashi T, Kajiura-Kobayashi H, Nagahama Y. 2000. Differential expression of vasa homologue gene in the germ cells during oogenesis and spermatogenesis in a teleost fish, tilapia, Oreochromis niloticus. Mech Dev 99:139-142.
20. Kobayashi T, Kajiura-Kobayashi H, Nagahama Y. 2002. Two isoforms of vasa homologs in a teleost fish: their differential expression during germ cell differentiation. Mech Dev 111:167-171.
21. Kobayashi T, Kajiura-Kobayashi H, Nagahama Y. 2003. Induction of XY sex reversal by estrogen involves altered gene expression in a teleost, tilapia. Cytogenet Genome Res 101:289-294.
22. Kobayashi T, Matsuda M, Kajiura-Kobayashi H, Suzuki A, Saito N, Nakamoto M, Shibata N, Nagahama Y. 2004. Two DM domain genes, DMY and DMRT1, involved in testicular differentiation and development in the medaka, Oryzias latipes. Dev Dyn 231:518-526.
23. Marchand O, Govoroun M, D'Cotta H, McMeel O, Lareyre J-J, Bernot A, Laudet V, Guiguen Y. 2000. DMRT1 expression during gonadal differentiation and spermatogenesis in the rainbow trout, Oncorhynchus mykiss. Biochim Biophys Acta 1493:180-187.
24. Marin I, Baker BS. 1998. The evolutionary dynamics of sex determination. Science 281:1990-1994.
25. Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Asakawa S, Shimizu N, Hori H, Hamaguchi S, Sakaizumi M. 2002. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417:559-563.
26. Matsuda M, Sato T, Toyazaki Y, Nagahama Y, Hamaguchi S, Sakaizumi M. 2003. Oryzias curvinotus has DMY, a gene that is required for male development in the medaka, O. latipes. Zool. Sci 20:159-161.
27. McLaren A. 1983. Sex reversal in the mouse. Differentiation 23(Suppl):93-98.
28. McLaren A. 1991. Development of the mammalian gonad: the fate of the supporting cell lineage. Bioessays 13:151-156.
29. McLaren A. 1997. Entry of mouse embryonic germ cells into meiosis. Dev Biol 187:107-113.
30. Moniot B, Berta P, Scherer G, Sudbeck P, Poulat F. 2000. Male specific expression suggests a role of DMRT1 in human sex determination. Mech Dev 91:323-325.
31. Moreno-Mendoza N, Harley VR, Merchant-Larios H. 1999. Differential expression of SOX9 in gonads of the sea turtle Lepidochelys olivacea at male- or female-promoting temperatures. J Exp Zool 284:705-710.
32. Nakamoto M, Suzuki A, Matsuda M, Nagahama Y, Shibata N. 2005. Testicular type Sox9 is not involved in sex determination but might be in the development of testicular structures in the medaka, Oryzias latipes. Biochem Biophys Res Commun 333:729-736.
33. Nakamura M, Kobayashi T, Chang X-T, Nagahama Y. 1998. Gonadal sex differentiation in teleost fish. J Exp Zool 281:362-372.
34. Nakamura M, Kobayashi T, Yoshiura Y, Nagahama Y. 1999. Role of endogenous steroid hormones on gonadal sex differentiation in fish. In: Norberg B, Kjesbu OS, Taranger GL, Andersson E, Stefansson SO, editors. Proceedings of the 6th International Symposium on the Reproductive Physiology of Fish. Bergen. p 247-249.
35. Raymond CS, Shamu CE, Shen MM, Seifert KJ, Hirsch B, Hodgkin J, Zarkower D. 1998. Evidence for evolutionary conservation of sex-determining genes. Nature 391:691-695.
36. Raymond CS, Kettlewell JR, Hirsch B, Bardwell VJ, Zarkower D. 1999. Expression of Dmrt1 in the genital ridge of mouse and chicken embryos suggests a role in vertebrate sexual development. Dev Biol 215:208-220.
37. Reinboth R. 1983. The peculiarities of gonad transformation in teleosts. In: Muller U, Franke WW, editors. Mechanisms of gonadal differentiation in vertebrates. Berlin: Springer-Verlag. p 82-86.
38. Rodriguez-Mari A, Yan Y-L, BreMiller RA, Wilson C, Canestro C, Postlewait 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.
39. Satoh N, Egami N. 1972. Sex differentiation of germ cells in the teleost, Oryzias latipes, during normal embryonic development. J Embryol Exp Morphol 28:385-395.
40. Scheib D. 1983. Effects and role of estrogens in avian gonadal differentiation. In: Muller U, Franke WW, editors. Mechanisms of gonadal differentiation in vertebrates. Berlin: Springer-Verlag. p 87-92.
41. Shen MM, Hodgkin J. 1988. mab-3, a gene required for sex-specific yolk protein expression and a male-specific lineage in C. elegans. Cell 54:1019-1031.
42. Shibata K, Takase M, Nakamura M. 2002. The Dmrt1 expression in sex-reversed gonads of amphibians. Gen Comp Endocrinol 127:232-241.
43. Smith CA, McClive PJ, Western PS, Reed KJ, Sinclair AH. 1999. Conservation of sex-determining gene. Nature 402:601-602.
44. Smith CA, Katz M, Sinclair AH. 2003. DMRT1 is upregulated in the gonads during female-to-male sex reversal in ZW chicken embryos. Biol Reprod 68:560-570.
45. Valleley EM, Cartwright EJ, Croft NJ, Markham AF, Coletta PL. 2001. Characterization and expression of Sox9 in the Leopard gecho, Eublepharis macularius. J Exp Zool 291:85-91.
46. Veitia RA, Salas-Cortes L, Ottolenghi C, Pailhoux E, Cotinot C, Fellous M. 2001. Testis determination in mammals: more questions than answers. Mol Cell Endocrinol 179:3-16.
47. Vidal VP, Chaboissier MC, de Rooij DG, Schedl A. 2001. Sox9 induces testis development in XX transgenic mice. Nat Genet 28:216-217.
48. Western PS, Harry JL, Graves JA, Sinclair AH. 1999. Temperature-dependent sex determination: upregulation of SOX9 expression after commitment to male development. Dev Dyn 214:171-177.
49. Yamamoto T. 1953. Artificially induced sex-reversal in genotypic males of the medaka (Oryzias latipes). J Exp Zool 123:571-594.
50. Yamamoto T. 1958. Artificial induction of functional sex-reversal in genotypic females of the medaka (Oryzias latipes). J Exp Zool 137:227-264.
51. Yamamoto T. 1969. Sex differentiation. In: Hoar WS, Randall DJ, editors. Fish physiology. Vol. III. New York: Academic Press. p 117-175.
52. Yi W, Ross JM, Zarkower D. 2000. Mab-3 is a direct tra-1 target gene regulating diverse aspects of C. elegans male sexual development and behavior. Development 127:4469-4480.