Steroidogenic gene expression during sex determination in the frog Rana rugosa

General and Comparative Endocrinology

Volumn 158, Issue 1, 2008, Pages 87-94

  Maruo, Koichi ^a   Suda, Mari ^a   Yokoyama, Satoshi ^a   Oshima, Yuki ^a   Nakamura, Masahisa ^a  

^a WASEDA UNIVERSITY   (Japan)

Author keywords

Frog; Gonad; Molecular cloning; Real time RT PCR; Sex differentiation; Steroidogenic genes

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; AROMATASE; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); COMPLEMENTARY DNA; CYTOCHROME P450 17; MESSENGER RNA; STEROID 5ALPHA REDUCTASE; STEROID 5ALPHA REDUCTASE 1; STEROIDOGENIC ACUTE REGULATORY PROTEIN; TESTOSTERONE 17BETA DEHYDROGENASE; TESTOSTERONE 17BETA DEHYDROGENASE 12; TESTOSTERONE 17BETA DEHYDROGENASE 7; TESTOSTERONE 17BETA DEHYDROGENASE 8;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; FROG; GENE EXPRESSION; GENETIC TRANSCRIPTION; GONAD DEVELOPMENT; MALE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RANA RUGOSA; REAL TIME POLYMERASE CHAIN REACTION; SEX DETERMINATION; SEX DIFFERENCE; SEX DIFFERENTIATION; STEROIDOGENESIS;

EID: 47749087004     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2008.04.019     Document Type: Article

References (59)

1. Andersson S.A., Berman D.M., Jenkins E.P., and Russell D.W. Deletion of steroid 5α-reductase II gene on male pseudohermaphroditism. Nature 354 (1991) 159-161
2. Andersson S.A., and Russell D.W. Structure and biochemical properties of cloned and expressed human and rat steroid 5α-reductase. Proc. Natl. Acad. Sci. USA 87 (1990) 3640-3644
3. Aziz N., Anderson E., Lee G.Y., and Woo D.D. Arrested testis development in the cpk mouse may be the result of abnormal steroid metabolism. Mol. Cell. Endocrinol. 171 (2001) 83-88
4. Bull J.J., Gutzke W.H., and Crews D. Sex reversal by estradiol in three reptilian orders. Gen. Comp. Endocrinol. 70 (1988) 425-428
5. Burns R.K. Role of hormones in the differentiation of sex. In: Young W.C. (Ed). Sex and Internal Secretions 1 (1961), Waverly Press, MD 86-95
6. Canosa L.F., Pozzi A.G., Rosemblit C., and Ceballos N.R. Steroid production in toads. J. Steroid Biochem. Mol. Biol. 85 (2003) 227-233
7. Capel B. The battle of the sexes. Mech. Dev. 92 (2000) 89-103
8. Chardard D., Kuntz S., Chesnel A., and Flament S. Effects of androgens on sex differentiation of the urodele Pleurodeles waltl. J. Exp. Zoolog. A Comp. Exp. Biol. 296 (2003) 46-55
9. Clark B., and Stocco D. Steroidogenic acute regulatory protein: the StAR still shines brightly. Mol. Cell. Endoc. 134 (1997) 1-8
10. Desvages G., and Pieau C. Aromatase activity in gonads of turtle embryos as a function of the incubation temperature of eggs. J. Steroid Biochem. Mol. Biol. 41 (1992) 851-853
11. Endo D., Kanaho Y., and Park M.K. Expression of sex steroid hormone-related genes in the embryo of the leopard gecko. Gen. Comp. Endocrinol. 155 (2008) 70-78
12. Fomitcheva J., Baker M.E., Anderson E., Lee G.Y., and Aziz N. Characterization of Ke 6, a new 17βhydroxysteroid dehydrogenase, and its expression in gonadal tissues. J. Biol. Chem. 273 (1998) 22664-22671
13. Freking F., Nazairians T., and Schlinger B.A. The expression of the sex steroid-synthesizing enzymes CYP11A1, 3β-HSD, CYP17, and CYP19 in gonads and adrenals of adult and developing zebra finches. Gen. Comp. Endocrinol. 119 (2000) 140-151
14. Greco T.L., and Payne A.H. Ontogeny of expression of the genes for steroidogenic enzymes P450 side-chain cleavage, 3β-hydroxysteroid dehydrogenase, P450 17α-hydroxylase/C17-20 lyase, and P450 aromatase in fetal mouse gonads. Endocrinology 135 (1994) 262-268
15. Ijiri S., Kaneko H., Kobayashi T., Wang D.S., Sakai F., Paul-Prasanth B., Nakamura M., and Nagahama Y. Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia Oreochromis niloticus. Biol. Reprod. 78 (2008) 333-341
16. Iwade R., Maruo K., Okada G., and Nakamura M. Elevated expression of P450c17 (CYP17) during testicular formation in the frog. Gen. Comp. Endocrinol. 155 (2008) 79-87 (published on line Mar 13, 2007)
17. Kato T., Matsui K., Takase M., Kobayashi M., and Nakamura M. Expression of P450 aromatase protein in developing and in sex-reversed gonads of the XX/XY type of the frog Rana rugosa. Gen. Comp. Endocrinol. 137 (2004) 227-236
18. Kreidberg J.A., Sariola H., Loring J.M., Maeda M., Pelletler J., Housman D., and Jaenisch R. WT-1 is required for early kidney development. Cell 74 (1993) 679-691
19. Kuntz S., Chardard D., Chesnel A., Grillier-Vuissoz I., and Flament S. Steroids, aromatase and sex differentiation of the newt Pleurodeles waltl. Cytogenet. Genome Res. 101 (2003) 283-288
20. Kuntz S., Chesnel A., Duterque-Coquillaud M., Grillier-Vuissoz I., Callier M., Dournon C., Flament S., and Chardard D. Differential expression of P450 aromatase during gonadal sex differentiation and sex reversal of the newt Pleurodeles waltl. J. Steroid Biochem. Mol. Biol. 84 (2003) 89-100
21. Lee S.T., Lam T.J., and Tan C.H. Increased 21-hydroxylase and shutdown of C17, 20 lyase activities in testicular tissues of the grouper (Epinephelus coioides) during 17-methyltestosterone-induced sex inversion. Gen. Comp. Endocrinol. 126 (2002) 298-309
22. Li D., Urs A.N., Allegood J., Leon A., Merrill Jr. A.H., and Sewer M.B. Cyclic AMP-stimulated interaction between steroidogenic factor 1 and diacylglycerol kinase theta facilitates induction of CYP17. Mol. Cell. Biol. 27 (2007) 6669-6685
23. Luu-The V., Tremblay P., and Labrie F. Characterization of type 12 17β-hydroxysteroid dehydrogenase, an isoform of type 3 17β-hydroxysteroid dehydrogenase responsible for estradiol formation in women. Mol. Endocrinol. 20 (2006) 437-443
24. Matsuda M., Nagahama Y., Shinomiya A., Sato T., Matsuda C., Kobayashi T., Morrey C.E., Shibata N., Asakawa S., Shimizu N., Hori H., Hamaguchi S., and Sakaizumi M. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417 (2002) 559-563
25. Miller W.L. Molecular biology of steroid hormone synthesis. Endocr. Rev. 9 (1988) 295-318
26. Miura I., Ohtani H., Nakamura M., Ichikawa Y., and Saitoh K. The origin and differentiation of the heteromorphic sex chromosomes Z, W, X, and Y in the frog Rana rugosa, inferred from the sequences of a sex-linked gene, ADP/ATP translocase. Mol. Biol. Evol. 15 (1998) 1612-1619
27. Nishioka M., Miura I., and Saitoh K. Sex chromosomes of Rana rugosa with special reference to local differences in sex-determining mechanism. Sci. Rep. Lab. Amphibian Biol. Horoshima Univ. 12 (1993) 55-81
28. Oshima Y., Hayashi T., Tokunaga S., and Nakamura M. Wnt4 expression in the differentiating gonad of the frog Rana rugosa. Zool. Sci. 22 (2005) 689-693
29. Oshima Y., Kato T., Wang D., Murakami T., Matsuda M., Nagahama Y., and Nakamura M. Promoter activity and chromosomal location of the Rana rugosa P450 aromatase (P450arom) gene. Zool. Sci. 23 (2006) 79-85
30. Oshima Y., Noguchi K., and Nakamura M. Expression of Lhx9 isoforms in the developing gonads of Rana rugosa. Zool. Sci. 24 (2007) 798-802
31. Ramsey M., Shoemaker C., and Crews D. Gonadal expression of Sf1 and aromatase during sex determination in the red-eared slider turtle (Trachemys scripta), a reptile with temperature-dependent sex determination. Differentiation 75 (2007) 978-991
32. Raymond C.S., Murphy M.W., O'Sullivan M.G., Bardwell V.J., and Zarkower D. Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev. 14 (2000) 2587-2595
33. Sakurai N., Miki Y., Suzuki T., Watanabe K., Narita T., Ando K., Yung T.M., Aoki D., Sasano H., and Handa H. Systemic distribution and tissue localizations of human17β-hydroxysteroid dehydrogenase type 12. J. Steroid Biochem. Mol. Biol. 99 (2006) 174-181
34. Schmid M., Nada I., Steinlein C., Kausch K., Haaf T., and Epplen J.T. Sex-determining mechanisms and sex chromosomes in amphibia. In: Green D.M., and Sessions S.K. (Eds). Amphibian Cytogenetics and Evolution (1991), Academic Press, New York 393-428
35. Shibata K., Takase M., and Nakamura M. The Dmrt1 expression in sex-reversed gonads of amphibians. Gen. Comp. Endocrinol. 127 (2002) 232-241
36. Shimada K. Gene expression of steroidogenic enzymes in chicken embryonic gonads. J. Exp. Zool. 281 (1998) 450-456
37. Shumway W. Stages in the normal development of Rana pipiens. I. External form. Anat. Rec. 78 (1940) 139-147
38. Sinclair A.H., Berta P., Palmer M.S., Hawkins J.R., Griffiths B.L., Smith M.J., Foster J.W., Frischauf A.M., Lövell-Badge R., and Goodfellow P.N. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346 (1990) 240-244
39. Smith C.A., Roeszler K.N., Hudson Q.J., and Sinclair A.H. Avian sex determination: what, when and where?. Cytogenet. Genome Res. 117 (2007) 165-173
40. Specker J.L., and Moore F.L. Annual cycle of plasma androgens and testicular composition in the rough-skinned newt, Taricha granulosa. Gen. Comp. Endocrinol. 42 (1980) 297-303
41. Stocco D.M. The role of the StAR protein in steroidogenesis: challenges for the future. J. Endocrinol. 164 (2000) 247-253
42. Sugita J., Takase M., and Nakamura M. Expression of Dax-1 during gonadal development of the frog. Gene 280 (2001) 67-74
43. Swain A., and Lövell-Badge R. Mammalian sex determination: a molecular drama. Genes Dev. 13 (1999) 755-767
44. Takase M., Noguchi S., and Nakamura M. Two Sox9 messenger RNA isoforms: isolation of cDNAs and their expression during gonadal development in the frog Rana rugosa. FEBS Lett. 466 (2000) 249-254
45. Taylor A.C., and Kollros J.J. Stages in the normal development of Rana pipiens larvae. Anat. Rec. 94 (1946) 7-23
46. Urbatzka R., Lutz I., and Kloas W. Aromatase, steroid-5-alpha-reductase type 1 and type 2 mRNA expression in gonads and in brain of Xenopus laevis during ontogeny. Gen. Comp. Endocrinol. 153 (2007) 280-288
47. Urs A.N., Dammer E., and Sewer M.B. Sphingosine regulates the transcription of CYP17 by binding to steroidogenic factor-1. Endocrinology 147 (2006) 5249-5258
48. Vaillant S., Dorizzi M., Pieau C., and Richard-Mercier N. Sex reversal and aromatase in chicken. J. Exp. Zool. 290 (2001) 727-740
49. Vainio S., Heikkila M., Kispert A., Chinn N., and McMahon A.P. Female development in mammals is regulated by Wnt-4 signalling. Nature 397 (1999) 405-409
50. Villar J., Celay J., Alonso M.M., Rotinen M., de Miguel C., Migliaccio M., and Encío I. Transcriptional regulation of the human type 8 17β-hydroxysteroid dehydrogenase gene by C/EBPβ. J. Steroid Biochem. Mol. Biol. 105 (2007) 131-139
51. Wallace H., Badawy G.M.I., and Wallace B.M.N. Amphibian sex determination and sex reversal. Cell. Mol. Life Sci. 55 (1999) 901-909
52. Wagner T., Wirth I., Meyer I., Zabel B., Held M., Zimmer J., Pananyes J., Bricaelli F.D., Husteri E., Wolf U., Tommerup N., Schempp W., and Scherer G. Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 79 (1994) 1111-1120
53. Wilhelm D., Palmer S., and Koopman P. Sex determination and gonadal development in mammals. Physiol. Rev. 87 (2007) 1-28
54. Woo D., Lee G.Y., Anderson E., and Aziz N. Immature ovaries and polycystic kidneys in the congenital polycystic kidney mouse may be due to abnormal sex steroid metabolism. Mol. Cell. Endocrinol. 176 (2001) 155-162
55. Yamamoto T., and Kajishima T. Sex hormone induction of sex reversal in the goldfish and evidence for male heterogamity. J. Exp. Zool. 168 (1968) 215-221
56. Yamamura Y., Aoyama S., Oshima Y., Kato T., Osawa N., and Nakamura M. Molecular cloning and expression in gonad of Rana rugosa WT1 and Fgf9. Zool. Sci. 22 (2005) 1045-1050
57. Yu H., Cheng H., Guo Y., Xia L., and Zhou R. Alternative splicing and differential expression of P450c17 (CYP17) in gonads during sex transformation in the rice field eel. Biochem. Biophys. Res. Commun. 307 (2003) 165-171
58. Yu R.N., Ito M., Saunders T.L., Camper S.A., and Jameson J.L. Role of Ahch in gonadal development and gametogenesis. Nat. Genet. 20 (1998) 353-357
59. Zhou L.Y., Wang D.S., Shibata Y., Paul-Prasanth B., Suzuki A., and Nagahama Y. Characterization, expression and transcriptional regulation of P450c17-I and -II in the medaka, Oryzias latipes. Biochem. Biophys. Res. Commun. 26 (2007) 619-625