Molecular characterization of cyp11a1 and cyp11b1 and their gene expression profile in pejerrey (Odontesthes bonariensis) during early gonadal development

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 156, Issue 1, 2010, Pages 110-118

  Blasco, Martín ^a   Fernandino, Juan I ^a   Guilgur, Leonardo G ^a   Strüssmann, Carlos A ^b   Somoza, Gustavo M ^a   Vizziano Cantonnet, Denise ^c  

^a INSTITUTO DE INVESTIGACIONES BIOTECNOLÓGICAS   (Argentina)

^b TOKYO UNIVERSITY OF MARINE SCIENCE AND TECHNOLOGY   (Japan)

^c Facultad de Ciencias   (Uruguay)

Author keywords

cyp11a1; cyp11b1; Gonadal development; Pejerrey; Sex differentiation markers; Steroidogenic enzymes; Teleost fish

Indexed keywords

ALDOSTERONE SYNTHASE; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING);

ANDROGEN SYNTHESIS; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GONAD DEVELOPMENT; LEYDIG CELL; MALE; NONHUMAN; PROTEIN EXPRESSION; SERTOLI CELL; SEX DIFFERENTIATION; TEMPERATURE; TESTIS;

ODONTESTHES BONARIENSIS; TELEOSTEI;

EID: 77649191407     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2010.01.006     Document Type: Article

References (60)

1. Baroiller J., Guiguen Y., and Fostier A. Endocrine and environmental aspects of sex differentiation in fish. Cell. Mol. Life Sci. 55 (1999) 910-931
2. Baron D., Houlgatte R., Fostier A., and Guiguen Y. Large-scale temporal gene expression profiling during gonadal differentiation and early gametogenesis in rainbow trout. Biol. Reprod. 73 (2005) 959-966
3. Blasco M., Somoza G., and Vizziano D. Androgens in pejerrey (Odontesthes bonariensis). Cybium 32 (2008) 86
4. Borg B. Androgens in teleost fishes. Comp. Biochem. Physiol. C 109 (1994) 219-245
5. Bowles J., and Koopman P. New clues to the puzzle of mammalian sex determination. Genome Biol. 2 (2001) 1025.1-1025.4
6. Brennan J., and Capel B. One tissue, two fates: molecular genetic events that underlie testis versus ovary development. Nat. Rev. Genet. 5 (2004) 509-521
7. Chardard D., Kuntz S., Chesnel A., and Flament S. Effects of androgens on sex differentiation of the urodele Pleurodeles waltl. J. Exp. Zool. 296A (2003) 46-55
8. Chen H.L., Guo Q.L., and Ortí G. Optimal data partitioning and a test case for ray-finned fishes (Actinopterygii) based on ten nuclear loci. Syst. Biol. 57 (2008) 519-539
9. Chiang E.F., Pai C.I., Wyatt M., Yan Y.L., Postlethwait J., and Chung B. Two sox9 genes on duplicated zebrafish chromosomes: expression of similar transcription activators in distinct sites. Dev. Biol. 231 (2001) 149-163
10. Cresko W.A., Yan Y.L., Baltrus D.A., Amores A., Singer A., Rodriguez-Mari A., and Postlethwait J.H. Genome duplication, subfunction partitioning, and lineage divergence: Sox9 in stickleback and zebrafish. Dev. Dyn. 228 (2003) 480-489
11. Desprez D., Géraz E., Hoareau M., Mélard C., Bosc P., and Baroiller J. Production of a high percentage of male offspring with a natural androgen, 11β-hydroxyandrostenedione (11βOHA4) in Florida red tilapia. Aquaculture 216 (2003) 55-65
12. Fernandino J.I., Guilgur L.G., Strobl-Mazzulla P.H., and Somoza G.M. Molecular cloning of SOX9 and DMRT-1 cDNA partial sequences in the pejerrey fish Odontesthes bonariensis (Atheriniformes). Fish Physiol. Biochem. 28 (2003) 145-146
13. Fernandino J.I., Hattori R.S., Shinoda T., Kimura H., Strobl-Mazzulla P.H., Strüssmann C.A., and Somoza G.M. Dimorphic expression of dmrt1 and cyp19a1 (ovarian aromatase) during early gonadal development in pejerrey, Odontesthes bonariensis. Sex. Dev. 2 (2008) 316-324
14. Fernandino J.I., Hattori R.S., Kimura H., Strüssmann C.A., and Somoza G.M. Expression profile and estrogenic regulation of anti-Müllerian hormone during gonadal development in pejerrey Odontesthes bonariensis, a teleost fish with strong temperature-dependent sex determination. Dev. Dyn. 237 (2008) 3192-3199
15. Fostier A., Jalabert B., Billard R., Breton B., and Zohar Y. The gonadal steroids. Fish Physiol 9A (1983) 277-372
16. Guiguen Y. Implications of steroids in fish gonadal sex differentiation and sex inversion. Curr. Top. Steroid Res. 3 (2000) 127-143
17. Guiguen Y., Fostier A., Piferrer F., and Chang Ch.-F. Ovarian aromatase and estrogens: a pivotal role for gonadal sex differentiation and sex change in fish. Gen. Comp. Endocrinol. 165 (2010) 352-366
18. Govoroun M., Mcmeel O., D'Cotta H., Ricordel M., Smith T., Fostier A., and Guiguen Y. Steroid enzyme gene expressions during natural and androgen-induced gonadal differentiation in the rainbow trout, Oncorhynchus mykiss. J. Exp. Zool. 290 (2001) 558-566
19. Hattori R.S., Fernandino J.I., Kishii A., Kimura H., Kinno T., Oura M., Somoza G.M., Yokota M., Strüssmann C.A., and Watanabe S. Cortisol-induced masculinization: does thermal stress affect gonadal fate in pejerrey, a teleost fish with temperature-dependent sex determination?. PLoS ONE 4 (2009) e6548 10.1371/journal.pone.0006548
20. Hayes T. Sex determination and primary sex differentiation in amphibians: genetic and developmental mechanisms. J. Exp. Zool. 281 (1998) 373-399
21. Hsu H., Hsiao P., Kuo M., and Chung B. Expression of zebrafish cyp11a1 as a maternal transcript and in yolk syncytial layer. Gene Expr. Patterns 2 (2002) 219-222
22. Hsu H., Lin G., and Chung B. Parallel early development of zebrafish interrenal glands and pronephros: differential control by wt1 and ff1b. Development 130 (2003) 2107-2116
23. Hu M., Hsu H., Guo I., and Chung B. Function of cyp11a1 in animal models. Mol. Cell. Endocrinol. 215 (2004) 95-100
24. Hunter G.A., and Donaldson E.M. Hormonal sex control and its application to fish culture. Fish Physiol. 9A (1983) 223-303
25. Ijiri S., Kaneko H., Kobayashi T., Wang D., 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
26. Ito L., Yamashita M., Takashima F., and Strüssmann C.A. Dynamics and histological characteristics of gonadal sex differentiation in pejerrey (Odontesthes bonariensis) at feminizing and masculinizing temperatures. J. Exp. Zool. 303A (2005) 504-514
27. Jiang J.Q., Kobayashi T., Ge W., Kobayashi H., Tanaka M., Okamoto M., Nonaka Y., and Nagahama Y. Fish testicular 11β-hydroxylase: cDNA cloning and mRNA expression during spermatogenesis. FEBS Lett. 397 (1996) 250-252
28. Karube M., Fernandino J.I., Strobl-Mazzulla P.H., Strüssmann C.A., Yoshizaki G., Somoza G.M., and Patiño R. Characterization and expression profile of the ovarian cytochrome p-450 aromatase (cyp19a1) gene during the thermolabile sex determination period in pejerrey, Odontesthes bonariensis. J. Exp. Zool. 307A (2007) 625-636
29. Klüver N., Kondo M., Herpin A., Mitani H., and Schartl M. Divergent expression patterns of Sox9 duplicates in teleosts indicate a lineage specific subfunctionalization. Dev. Genes. Evol. 215 (2005) 297-305
30. Kobayashi T., Matsuda M., Kajiura-Kobayashi H., Suzuki A., Saito N., Nakamoto M., Shibata N., and Nagahama Y. Two DM domain genes, DMY and DMRT1, involved in testicular differentiation and development in the medaka, Oryzias latipes. Dev. Dyn. 231 (2004) 518-526
31. Koopman P., Gubbay J., Vivian N., Goodfellow P., and Lovell-Badge R. Male development of chromosomally female mice transgenic for Sry. Nature 351 (1991) 117-121
32. Koopman P., Schepers G., Brenner S., and Venkatesh B. Origin and diversity of the SOX transcription factor gene family: genomewide analysis in Fugu rubripes. Gene 328 (2004) 177-186
33. Kusakabe M., Kobayashu T., Todo T., Lokman P., Nagahama Y., and Young G. Molecular cloning and expression during spermatogenesis of a cDNA encoding testicular 11β-hydroxylase (P45011β) in rainbow trout (Oncorhynchus mykiss). Mol. Reprod. Develop. 62 (2002) 456-469
34. Miller W. Molecular biology of steroid hormone synthesis. Endocr. Rev. 9 (1988) 295-318
35. Miura T., and Miura C.I. Molecular control mechanisms of fish spermatogenesis. Fish Physiol. Biochem. 28 (2003) 181-186
36. Miura S., Horiguchi R., and Nakamura M. Immunohistochemical evidence for 11β-hydroxylase (P45011β) and androgen production in the gonad during sex differentiation and in adults in the protandrous anemonefish Amphiprion clarkia. Zool. Sci. 25 (2008) 212-219
37. Nakamura M., Kobayashi T., Chang X., and Nagahama Y. Gonadal sex differentiation in teleost fish. J. Exp. Zool. 281 (1998) 362-372
38. Nakamura M., Bhandari R.K., and Higa M. The role estrogens play in sex differentiation and sex changes of fish. Fish Physiol. Biochem. 28 (2003) 113-117
39. Nakamoto M., Suzuki A., Matsuda M., Nagahama Y., and Shibata N. 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 (2005) 729-736
40. Nelson J.S. Fishes of the World. Fourth Edition (2006), John Wiley & Sons, Inc., New Jersey pp. 622
41. Omura T. Forty years of cytochrome P450. Biochem. Biophys. Res. Commun. 266 (1999) 690-698
42. Parker K.L., and Schimmer B.P. Steroidogenic factor 1: a key determinant of endocrine development and function. Endocr. Rev. 18 (1997) 361-377
43. Pieau C., and Dorizzi M. Oestrogens and temperature-dependent sex determination in reptiles: all is in the gonads. J. Endocrinol. 181 (2004) 367-377
44. Piferrer F., Baker I., and Donaldson E. Effects of natural, synthetic, aromatizable, and nonaromatizable androgens in inducing male sex differentiation in genotypic female chinook salmon (Oncorhynchus tshawytscha). Gen. Comp. Endocrinol. 91 (1993) 59-65
45. Piferrer F., and Guiguen Y. Fish gonadogenesis part II: molecular biology and genomics of sex differentiation. Rev. Fish. Sci. 16 (2008) 35-55
46. Schulz R.W., de Franca L.R., Lareyre J.J., Le Gac F., Chiarini-García H., Nobrega R.H., and Miura T. Spermatogenesis in fish. Gen. Comp. Endocrinol. 165 (2010) 390-411
47. Smith C., and Sinclair A. Sex determination: insights from the chicken. BioEssays 26 (2004) 120-132
48. Socorro S., Martins R., Deloffre L., Mylonas C., and Canario A. A cDNA for European sea bass (Dicentrachus labrax) 11beta-hydroxylase: gene expression during the thermosensitive period and gonadogenesis. Gen. Comp. Endocrinol. 150 (2007) 164-173
49. Strüssmann C., Moriyama S., Hanke E., Calsina Cota J., and Takashima F. Evidence of thermolabile sex determination in pejerrey. J. Fish. Biol. 48 (1996) 643-651
50. Strüssmann C., Saito T., Usui M., Yamada H., and Takashima F. Thermal thresholds and critical period of thermolabile sex determination in two atherinid fishes, Odontesthes bonariensis and Patagonina hatcheri. J. Exp. Zool. 278 (1997) 167-177
51. Strüssmann C., Takashima F., and Toda K. Sex differentiation and hormonal feminisation in pejerrey Odontesthes bonariensis. Aquaculture 139 (1996) 31-45
52. Subramaniam S. The biology workbench-a seamless database and analysis environment for the biologist. Proteins 32 (1998) 1-2
53. van den Hurk R., and van Oordt P. Effects of natural androgens and corticosteroids on gonad differentiation in the rainbow trout, Salmo gairdneri. Gen. Comp. Endocrinol. 57 (1985) 216-222
54. van den Hurk R., Lambert J.G., and Peute J. Steroidogenesis in the gonads of rainbow trout fry (Salmo gairdneri) before and after the onset of gonadal sex differentiation. Reprod. Nutr. Dev. 22 (1982) 413-425
55. Vizziano D., Randuineau G., Baron D., Cauty C., and Guiguen Y. Characterization of early molecular sex differentiation in rainbow trout, Oncorhynchus mykiss. Dev. Dyn. 236 (2007) 2198-2206
56. Vizziano D., Baron D., Randuineau G., Mahé S., Cauty C., and Guiguen Y. Rainbow trout gonadal masculinization induced by inhibition of estrogen synthesis is more physiological than masculinization induced by androgen supplementation. Biol. Reprod. 78 (2008) 939-946
57. Vizziano-Cantonnet D., Baron D., Mahè S., Cauty C., Fostier A., and Guiguen Y. Estrogen treatment up-regulates female genes but does not suppress all early testicular markers during rainbow trout male-to-female gonadal transdifferentiation. J. Mol. Endocrinol. 41 (2008) 277-288
58. Wu G.C., Tomy S., and Chang C.F. The expression of nr0b1 and nr5a4 during gonad development and sex change in protandrous black porgy fish, Acanthopagrus schlegeli. Biol. Reprod. 78 (2008) 200-210
59. Yamamoto T. Sex differentiation. Fish Physiol. 9A (1969) 117-372
60. Zhou R., Liu L., Guo Y., Yu H., Cheng H., Huang X., Tiersch T.R., and Berta P. Similar gene structure of two Sox9a genes and their expression patterns during gonadal differentiation in a teleost fish, rice field eel (Monopterus albus). Mol. Reprod. Dev. 66 (2003) 211-217