Antagonistic regulation of Cyp26b1 by transcription factors SOX9/SF1 and FOXL2 during gonadal development in mice

FASEB Journal

Volumn 25, Issue 10, 2011, Pages 3561-3569

  Kashimada, Kenichi ^a   Svingen, Terje ^a   Feng, Chun Wei ^a   Pelosi, Emanuele ^b   Bagheri Fam, Stefan ^c   Harley, Vincent R ^c   Schlessinger, David ^b   Bowles, Josephine ^a   Koopman, Peter ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b NATIONAL INSTITUTE ON AGING   (United States)

^c HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

Forkhead box protein L2; Germ cells; Meiosis; Retinoic acid; Sex determination

Indexed keywords

CYTOCHROME P450 26B1; STEROIDOGENIC FACTOR 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXL2; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME REGULATION; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSFECTION; GERM CELL; GONAD DEVELOPMENT; HIGH MOBILITY GROUP BOX DOMAIN; HYPOTHESIS; IN SITU HYBRIDIZATION; LEYDIG CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; SERTOLI CELL; SOMATIC CELL; TESTIS; UPREGULATION; WILD TYPE;

ANIMALS; CYTOCHROME P-450 ENZYME SYSTEM; DNA-BINDING PROTEINS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MICE; SEX DETERMINATION PROCESSES; SOX9 TRANSCRIPTION FACTOR; TESTIS; TRANSCRIPTION FACTORS; UP-REGULATION;

MUS;

EID: 80053896420     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-184333     Document Type: Article

References (57)

1. Koopman, P., Gubbay, J., Vivian, N., Goodfellow, P., and Lovell-Badge, R. (1991) Male development of chromosomally female mice transgenic for Sry. Nature 351, 117-121
2. Sekido, R., and Lovell-Badge, R. (2008) Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453, 930-934
3. De Santa Barbara, P., Moniot, B., Poulat, F., Boizet, B., and Berta, P. (1998) Steroidogenic factor-1 regulates transcription of the human anti-Müllerian hormone receptor. J. Biol. Chem. 273, 29654-29660
4. Wilson, M. J., Jeyasuria, P., Parker, K. L., and Koopman, P. (2005) The transcription factors steroidogenic factor-1 and SOX9 regulate expression of Vanin-1 during mouse testis development. J. Biol. Chem. 280, 5917-5923
5. Wilhelm, D., Hiramatsu, R., Mizusaki, H., Widjaja, L., Combes, A. N., Kanai, Y., and Koopman, P. (2007) SOX9 regulates prostaglandin D synthase gene transcription in vivo to ensure testis development. J. Biol. Chem. 282, 10553-10560
6. Wilhelm, D., Palmer, S., and Koopman, P. (2007) Sex determination and gonadal development in mammals. Physiol. Rev. 87, 1-28
7. Nef, S., and Vassalli, J. D. (2009) Complementary pathways in mammalian female sex determination. J. Biol. 8, 74
8. Hilscher, B., Hilscher, W., Bulthoff-Ohnolz, B., Kramer, U., Birke, A., Pelzer, H., and Gauss, G. (1974) Kinetics of gametogenesis. I. Comparative histological and autoradiographic studies of oocytes and transitional prospermatogonia during oogenesis and prespermatogenesis. Cell Tissue Res. 154, 443-470
9. McLaren, A. (1984) Meiosis and differentiation of mouse germ cells. Symp. Soc. Exp. Biol. 38, 7-23
10. Palmer, S. J., and Burgoyne, P. S. (1991) In situ analysis of fetal, prepuberal and adult XX-XY chimaeric mouse testes: Sertoli cells are predominantly, but not exclusively, XY. Development 112, 265-268
11. McLaren, A. (1995) Germ cells and germ cell sex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 350, 229-233
12. McLaren, A. (2003) Primordial germ cells in the mouse. Dev. Biol. 262, 1-15
13. Bowles, J., Knight, D., Smith, C., Wilhelm, D., Richman, J., Mamiya, S., Yashiro, K., Chawengsaksophak, K., Wilson, M. J., Rossant, J., Hamada, H., and Koopman, P. (2006) Retinoid signaling determines germ cell fate in mice. Science 312, 596-600
14. Koubova, J., Menke, D. B., Zhou, Q., Capel, B., Griswold, M. D., and Page, D. C. (2006) Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc. Natl. Acad. Sci. U. S. A. 103, 2474-2479
15. Chambon, P. (1996) A decade of molecular biology of retinoic acid receptors. FASEB J. 10, 940-954
16. Duester, G. (2008) Retinoic acid synthesis and signaling during early organogenesis. Cell 134, 921-931
17. MacLean, G., Abu-Abed, S., Dolle, P., Tahayato, A., Chambon, P., and Petkovich, M. (2001) Cloning of a novel retinoic-acid metabolizing cytochrome P450, Cyp26B1, and comparative expression analysis with Cyp26A1 during early murine development. Mech. Dev. 107, 195-201
18. MacLean, G., Li, H., Metzger, D., Chambon, P., and Petkovich, M. (2007) Apoptotic extinction of germ cells in testes of Cyp26b1 knockout mice. Endocrinology 148, 4560-4567
19. Barrionuevo, F., Georg, I., Scherthan, H., Lecureuil, C., Guillou, F., Wegner, M., and Scherer, G. (2009) Testis cord differentiation after the sex determination stage is independent of Sox9 but fails in the combined absence of Sox9 and Sox8. Dev. Biol. 327, 301-312
20. Val, P., Martinez-Barbera, J. P., and Swain, A. (2007) Adrenal development is initiated by Cited2 and Wt1 through modulation of Sf-1 dosage. Development 134, 2349-2358
21. Buaas, F. W., Val, P., and Swain, A. (2009) The transcription co-factor CITED2 functions during sex determination and early gonad development. Hum. Mol. Genet. 18, 2989-3001
22. Combes, A. N., Spiller, C. M., Harley, V. R., Sinclair, A. H., Dunwoodie, S. L., Wilhelm, D., and Koopman, P. (2010) Gonadal defects in Cited2-mutant mice indicate a role for SF1 in both testis and ovary differentiation. Int. J. Dev. Biol. 54, 683-689
23. Hadjantonakis, A. K., Gertsenstein, M., Ikawa, M., Okabe, M., and Nagy, A. (1998) Non-invasive sexing of preimplantation stage mammalian embryos. Nat. Genet. 19, 220-222
24. Barbera, J. P., Rodriguez, T. A., Greene, N. D., Weninger, W. J., Simeone, A., Copp, A. J., Beddington, R. S., and Dunwoodie, S. (2002) Folic acid prevents exencephaly in Cited2 deficient mice. Hum. Mol. Genet. 11, 283-293
25. Chuma, S., and Nakatsuji, N. (2001) Autonomous transition into meiosis of mouse fetal germ cells in vitro and its inhibition by gp130-mediated signaling. Dev. Biol. 229, 468-479
26. Uda, M., Ottolenghi, C., Crisponi, L., Garcia, J. E., Deiana, M., Kimber, W., Forabosco, A., Cao, A., Schlessinger, D., and Pilia, G. (2004) Foxl2 disruption causes mouse ovarian failure by pervasive blockage of follicle development. Hum. Mol. Genet. 13, 1171-1181
27. Kent, J., Wheatley, S. C., Andrews, J. E., Sinclair, A. H., and Koopman, P. (1996) A male-specific role for SOX9 in vertebrate sex determination. Development 122, 2813-2822
28. Schepers, G., Wilson, M., Wilhelm, D., and Koopman, P. (2003) SOX8 is expressed during testis differentiation in mice and synergizes with SF1 to activate the Amh promoter in vitro. J. Biol. Chem. 278, 28101-28108
29. Beverdam, A., Wilhelm, D., and Koopman, P. (2003) Molecular characterization of three gonad cell lines. Cytogenet. Genome Res. 101, 242-249
30. Kashimada, K., Pelosi, E., Chen, H., Schlessinger, D., Wilhelm, D., and Koopman, P. (2011) FOXL2 and BMP2 act cooperatively to regulate follistatin gene expression during ovarian development. Endocrinology 152, 272-280
31. Svingen, T., Spiller, C. M., Kashimada, K., Harley, V. R., and Koopman, P. (2009) Identification of suitable normalizing genes for quantitative real-time RT-PCR analysis of gene expression in fetal mouse gonads. Sex. Dev. 3, 194-204
32. Ottolenghi, C., Pelosi, E., Tran, J., Colombino, M., Douglass, E., Nedorezov, T., Cao, A., Forabosco, A., and Schlessinger, D. (2007) Loss of Wnt4 and Foxl2 leads to female-to-male sex reversal extending to germ cells. Hum. Mol. Genet. 16, 2795-2804
33. Wilhelm, D., Martinson, F., Bradford, S., Wilson, M. J., Combes, A. N., Beverdam, A., Bowles, J., Mizusaki, H., and Koopman, P. (2005) Sertoli cell differentiation is induced both cell-autonomously and through prostaglandin signaling during mammalian sex determination. Dev. Biol. 287, 111-124
34. Morais da Silva, S., Hacker, A., Harley, V., Goodfellow, P., Swain, A., and Lovell-Badge, R. (1996) Sox9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds. Nat. Genet. 14, 62-68
35. Morohashi, K. I., and Omura, T. (1996) Ad4BP/SF-1, a transcription factor essential for the transcription of steroidogenic cytochrome P450 genes and for the establishment of the reproductive function. FASEB J. 10, 1569-1577
36. Sadovsky, Y., and Crawford, P. A. (1998) Developmental and physiologic roles of the nuclear receptor steroidogenic factor-1 in the reproductive system. J. Soc. Gyn. Invest. 5, 6-12
37. Mather, J. P. (1980) Establishment and characterization of two distinct mouse testicular epithelial cell lines. Biol. Reprod. 23, 243-252
38. Bowles, J., Feng, C. W., Knight, D., Smith, C. A., Roeszler, K. N., Bagheri-Fam, S., Harley, V. R., Sinclair, A. H., and Koopman, P. (2009) Male-specific expression of Aldh1a1 in mouse and chicken fetal testes: implications for retinoid balance in gonad development. Dev. Dyn. 238, 2073-2080
39. Haselbeck, R. J., Hoffmann, I., and Duester, G. (1999) Distinct functions for Aldh1 and Raldh2 in the control of ligand production for embryonic retinoid signaling pathways. Dev. Genet. 25, 353-364
40. Ray, W. J., Bain, G., Yao, M., and Gottlieb, D. I. (1997) CYP26, a novel mammalian cytochrome P450, is induced by retinoic acid and defines a new family. J. Biol. Chem. 272, 18702-18708
41. Reijntjes, S., Blentic, A., Gale, E., and Maden, M. (2005) The control of morphogen signalling: regulation of the synthesis and catabolism of retinoic acid in the developing embryo. Dev. Biol. 285, 224-237
42. Agarwal, C., Chandraratna, R. A., Johnson, A. T., Rorke, E. A., and Eckert, R. L. (1996) AGN193109 is a highly effective antagonist of retinoid action in human ectocervical epithelial cells. J. Biol. Chem. 271, 12209-12212
43. Barrionuevo, F., Bagheri-Fam, S., Klattig, J., Kist, R., Taketo, M. M., Englert, C., and Scherer, G. (2006) Homozygous inactivation of Sox9 causes complete XY sex reversal in mice. Biol. Reprod. 74, 195-201
44. Luo, X., Ikeda, Y., and Parker, K. L. (1994) A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. Cell 77, 481-490
45. Sadovsky, Y., Crawford, P. A., Woodson, K. G., Polish, J. A., Clements, M. A., Tourtellotte, L. M., Simburger, K., and Milbrandt, J. (1995) Mice deficient in the orphan receptor steroidogenic factor 1 lack adrenal glands and gonads but express P450 side-chain-cleavage enzyme in the placenta and have normal embryonic serum levels of corticosteroids. Proc. Natl. Acad. Sci. U. S. A. 92, 10939-10943
46. Kim, Y., and Capel, B. (2006) Balancing the bipotential gonad between alternative organ fates: a new perspective on an old problem. Dev. Dyn. 235, 2292-2300
47. Ottolenghi, C., Uda, M., Crisponi, L., Omari, S., Cao, A., Forabosco, A., and Schlessinger, D. (2007) Determination and stability of sex. Bioessays 29, 15-25
48. Crisponi, L., Deiana, M., Loi, A., Chiappe, F., Uda, M., Amati, P., Bisceglia, L., Zelante, L., Nagaraja, R., Porcu, S., Ristaldi, M. S., Marzella, R., Rocchi, M., Nicolino, M., Lienhardt-Roussie, A., Nivelon, A., Verloes, A., Schlessinger, D., Gasparini, P., Bonneau, D., Cao, A., and Pilia, G. (2001) The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ ptosis/epicanthus inversus syndrome. Nat. Genet. 27, 159-166
49. Schmidt, D., Ovitt, C. E., Anlag, K., Fehsenfeld, S., Gredsted, L., Treier, A. C., and Treier, M. (2004) The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development 131, 933-942
50. Wilhelm, D., Washburn, L. L., Truong, V., Fellous, M., Eicher, E. M., and Koopman, P. (2009) Antagonism of the testis- and ovary-determining pathways during ovotestis development in mice. Mech. Dev. 126, 324-336
51. Park, M., Shin, E., Won, M., Kim, J. H., Go, H., Kim, H. L., Ko, J. J., Lee, K., and Bae, J. (2010) FOXL2 interacts with steroidogenic factor-1 (SF-1) and represses SF-1-induced CYP17 transcription in granulosa cells. Mol. Endocrinol. 24, 1024-1036
52. Ikeda, Y., Shen, W. H., Ingraham, H. A., and Parker, K. L. (1994) Developmental expression of mouse steroidogenic factor- 1, an essential regulator of the steroid hydroxylases. Mol. Endocrinol. 8, 654-662
53. Yashiro, K., Zhao, X., Uehara, M., Yamashita, K., Nishijima, M., Nishino, J., Saijoh, Y., Sakai, Y., and Hamada, H. (2004) Regulation of retinoic acid distribution is required for proximodistal patterning and outgrowth of the developing mouse limb. Dev. Cell. 6, 411-422
54. Pailhoux, E., Vigier, B., Chaffaux, S., Servel, N., Taourit, S., Furet, J. P., Fellous, M., Grosclaude, F., Cribiu, E. P., Cotinot, C., and Vaiman, D. (2001) A 11.7-kb deletion triggers intersexuality and polledness in goats. Nat. Genet. 29, 453-458
55. Wang, D. S., Kobayashi, T., Zhou, L. Y., Paul-Prasanth, B., Ijiri, S., Sakai, F., Okubo, K., Morohashi, K., and Nagahama, Y. (2007) Foxl2 up-regulates aromatase gene transcription in a female-specific manner by binding to the promoter as well as interacting with ad4 binding protein/steroidogenic factor 1. Mol. Endocrinol. 21, 712-725
56. Garcia-Ortiz, J. E., Pelosi, E., Omari, S., Nedorezov, T., Piao, Y., Karmazin, J., Uda, M., Cao, A., Cole, S. W., Forabosco, A., Schlessinger, D., and Ottolenghi, C. (2009) Foxl2 functions in sex determination and histogenesis throughout mouse ovary development. BMC Dev. Biol. 9, 36
57. Bowles, J., Feng, C. W., Spiller, C., Davidson, T. L., Jackson, A., and Koopman, P. (2010) FGF9 suppresses meiosis and promotes male germ cell fate in mice. Dev. Cell 19, 440-449