Establishment of testis-specific SOX9 activation requires high-glucose metabolism in mouse sex differentiation

Developmental Biology

Volumn 324, Issue 1, 2008, Pages 76-87

  Matoba, Shogo ^a   Hiramatsu, Ryuji ^a   Kanai Azuma, Masami ^b   Tsunekawa, Naoki ^a   Harikae, Kyoko ^a   Kawakami, Hayato ^b   Kurohmaru, Masamichi ^a   Kanai, Yoshiakira ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b KYORIN UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Energy metabolism; Glycogen; Gonad; Mouse; pre Sertoli cell; Sex differentiation; SOX9

Indexed keywords

TRANSCRIPTION FACTOR SOX9;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EXTRACELLULAR MATRIX; GLUCOSE METABOLISM; MOUSE; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN EXPRESSION; SERTOLI CELL; SEX DIFFERENTIATION; SOMATIC CELL; TRANSGENIC MOUSE;

EID: 55749096051     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2008.09.004     Document Type: Article

References (49)

1. Barrionuevo F., Bagheri-Fam S., Klattig J., Kist R., Taketo M.M., Englert C., and Scherer G. Homozygous inactivation of Sox9 causes complete XY sex reversal in mice. Biol. Reprod. 74 (2006) 195-201
2. Bell D.M., Leung K.K., Wheatley S.C., Ng L.J., Zhou S., Ling K.W., Sham M.H., Koopman P., Tam P.P., and Cheah K.S. SOX9 directly regulates the type-II collagen gene. Nat. Genet. 16 (1997) 174-178
3. Bi W., Huang W., Whitworth D.J., Deng J.M., Zhang Z., Behringer R.R., and de Crombrugghe B. Haploinsufficiency of Sox9 results in defective cartilage primordia and premature skeletal mineralization. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 6698-6703
4. Bishop C.E., Whitworth D.J., Qin Y., Agoulnik A.I., Agoulnik I.U., Harrison W.R., Behringer R.R., and Overbeek P.A. A transgenic insertion upstream of Sox9 is associated with dominant XX sex reversal in the mouse. Nat. Genet. 26 (2000) 490-494
5. Brennan J., Karl J., and Capel B. Divergent vascular mechanisms downstream of Sry establish the arterial system in the XY gonad. Dev. Biol. 244 (2002) 418-428
6. Buehr M., Gu S., and McLaren A. Mesonephric contribution to testis differentiation in the fetal mouse. Development 117 (1993) 273-281
7. Burgoyne P.S., Buehr M., and McLaren A. XY follicle cells in ovaries of XX-XY female mouse chimaeras. Development 104 (1988) 683-688
8. Capel B. The battle of the sexes. Mech. Dev. 92 (2000) 89-103
9. Capel B., Albrecht K.H., Washburn L.L., and Eicher E.M. Migration of mesonephric cells into the mammalian gonad depends on Sry. Mech. Dev. 84 (1999) 127-131
10. Chaboissier M.C., Kobayashi A., Vidal V.I., Lutzkendorf S., van de Kant H.J., Wegner M., de Rooij D.G., Behringer R.R., and Schedl A. Functional analysis of Sox8 and Sox9 during sex determination in the mouse. Development 131 (2004) 1891-1901
11. Colvin J.S., Green R.P., Schmahl J., Capel B., and Ornitz D.M. Male-to-female sex reversal in mice lacking fibroblast growth factor 9. Cell 104 (2001) 875-889
12. Dzeja P.P., and Terzic A. Phosphotransfer networks and cellular energetics. J. Exp. Biol. 206 (2003) 2039-2047
13. Gao F., Maiti S., Alam N., Zhang Z., Deng J.M., Behringer R.R., Lécureuil C., Guillou F., and Huff V. The Wilms tumor gene, Wt1, is required for Sox9 expression and maintenance of tubular architecture in the developing testis. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 11987-11992
14. Hacker A., Capel B., Goodfellow P., and Lovell-Badge R. Expression of Sry, the mouse sex determining gene. Development 121 (1995) 1603-1614
15. Hanley K.P., Oakley F., Sugden S., Wilson D.I., Mann D.A., and Hanley N.A. Ectopic SOX9 mediates extracellular matrix deposition characteristic of organ fibrosis. J. Biol. Chem. 283 (2008) 14063-14071
16. Hiramatsu R., Kanai Y., Mizukami T., Ishii M., Matoba S., Kanai-Azuma M., Kurohmaru M., Kawakami H., and Hayashi Y. Regionally distinct potencies of mouse XY genital ridge to initiate testis differentiation dependent on anteroposterior axis. Dev. Dyn. 228 (2003) 247-253
17. Ikeda Y., Takeda Y., Shikayama T., Mukai T., Hisano S., and Morohashi K.I. Comparative localization of Dax-1 and Ad4BP/SF-1 during development of the hypothalamic-pituitary-gonadal axis suggests their closely related and distinct functions. Dev. Dyn. 220 (2001) 363-376
18. Kanai Y., Hiramatsu R., Matoba S., and Kidokoro T. From SRY to SOX9: mammalian testis differentiation. J. Biochem. (Tokyo) 138 (2005) 13-19
19. Karl J., and Capel B. Sertoli cells of the mouse testis originate from the coelomic epithelium. Dev. Biol. 203 (1998) 323-333
20. Kent J., Wheatley S.C., Andrews J.E., Sinclair A.H., and Koopman P. A male-specific role for SOX9 in vertebrate sex determination. Development 122 (1996) 2813-2822
21. Kidokoro T., Matoba S., Hiramatsu R., Fujisawa M., Kanai-Azuma M., Taya C., Kurohmaru M., Kawakami H., Hayashi Y., Kanai Y., and Yonekawa H. Influence on spatiotemporal patterns of a male-specific Sox9 activation by ectopic Sry expression during early phases of testis differentiation in mice. Dev. Biol. 278 (2005) 511-525
22. Kim Y., Kobayashi A., Sekido R., DiNapoli L., Brennan J., Chaboissier M.C., Poulat F., Behringer R.R., Lovell-Badge R., and Capel B. Fgf9 and Wnt4 act as antagonistic signals to regulate mammalian sex determination. PLoS Biol. 4 (2006) e187
23. 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
24. Lee A.S. The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem. Sci. 26 (2001) 504-510
25. Lee J.M., Grabb M.C., Zipfel G.J., and Choi D.W. Brain tissue responses to ischemia. J. Clin. Invest. 106 (2000) 723-731
26. Li X., Chen Y., Schéele S., Arman E., Haffner-Krausz R., Ekblom P., and Lonai P. Fibroblast growth factor signaling and basement membrane assembly are connected during epithelial morphogenesis of the embryoid body. J. Cell Biol. 153 (2001) 811-822
27. Liu C.J., Zhang Y., Xu K., Parsons D., Alfonso D., and Di Cesare P.E. Transcriptional activation of cartilage oligomeric matrix protein by Sox9, Sox5, and Sox6 transcription factors and CBP/p300 coactivators. Front. Biosci. 12 (2007) 3899-3910
28. Ma Y., and Hendershot L.M. The mammalian endoplasmic reticulum as a sensor for cellular stress. Cell Stress Chaperones 7 (2002) 222-229
29. Malki S., Nef S., Notarnicola C., Thevenet L., Gasca S., Méjean C., Berta P., Poulat F., and Boizet-Bonhoure B. Prostaglandin D2 induces nuclear import of the sex-determining factor SOX9 via its cAMP-PKA phosphorylation. EMBO J. 24 (2005) 1798-1809
30. Martineau J., Nordqvist K., Tilmann C., Lovell-Badge R., and Capel B. Male-specific cell migration into the developing gonad. Curr. Biol. 7 (1997) 958-968
31. Matoba S., Kanai Y., Kidokoro T., Kanai-Azuma M., Kawakami H., Hayashi Y., and Kurohmaru M. A novel Sry-downstream cellular event which preserves the readily available energy source of glycogen in mouse sex differentiation. J. Cell Sci. 118 (2005) 1449-1459
32. Matsuyama M., Mizusaki H., Shimono A., Mukai T., Okumura K., Abe K., Shimada K., and Morohashi K. A novel isoform of Vinexin, Vinexin gamma, regulates Sox9 gene expression through activation of MAPK cascade in mouse fetal gonad. Genes Cells 10 (2005) 421-434
33. McClive P.J., and Sinclair A.H. Type II and type IX collagen transcript isoforms are expressed during mouse testis development. Biol. Reprod. 68 (2003) 1742-1747
34. Mittwoch U. Genetics of sex differentiation: an unsettled relationship between gene and chromosome. In: Mayo O., and Leach C. (Eds). Fifty Years of Human Genetics (2007), Wakefield Press, South Australia 260-265
35. Mizusaki H., Kawabe K., Mukai T., Ariyoshi E., Kasahara M., Yoshioka H., Swain A., and Morohashi K. Dax-1 (dosage-sensitive sex reversal-adrenal hypoplasia congenita critical region on the X chromosome, gene 1) gene transcription is regulated by wnt4 in the female developing gonad. Mol. Endocrinol. 17 (2003) 507-519
36. Morais da Silva S., Hacker A., Harley V., Goodfellow P., Swain A., and Lovell-Badge R. Sox9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds. Nat. Genet. 14 (1996) 62-68
37. Nef S., Verma-Kurvari S., Merenmies J., Vassalli J.D., Efstratiadis A., Accili D., and Parada L.F. Testis determination requires insulin receptor family function in mice. Nature 426 (2003) 291-295
38. Qin Y., and Bishop C.E. Sox9 is sufficient for functional testis development producing fertile male mice in the absence of Sry. Hum. Mol. Genet. 14 (2005) 1221-1229
39. Schepers G., Wilson M., Wilhelm D., and Koopman P. SOX8 is expressed during testis differentiation in mice and synergizes with SF1 to activate the Amh promoter in vitro. J. Biol. Chem. 278 (2003) 28101-28108
40. Schmahl J., and Capel B. Cell proliferation is necessary for the determination of male fate in the gonad. Dev. Biol. 258 (2003) 264-276
41. Schmahl J., Eicher E.M., Washburn L.L., and Capel B. Sry induces cell proliferation in the mouse gonad. Development 127 (2000) 65-73
42. Schmahl J., Kim Y., Colvin J.S., Ornitz D.M., and Capel B. Fgf9 induces proliferation and nuclear localization of FGFR2 in Sertoli precursors during male sex determination. Development 131 (2004) 3627-3636
43. Sekido R., and Lovell-Badge R. Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453 (2008) 930-934
44. Sekido R., Bar I., Narváez V., Penny G., and Lovell-Badge R. SOX9 is up-regulated by the transient expression of SRY specifically in Sertoli cell precursors. Dev. Biol. 274 (2004) 271-279
45. Sinclair A.H., Berta P., Palmer M.S., Hawkins J.R., Griffiths B.L., Smith M.J., Foster J.W., Frischauf A.M., Lovell-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
46. Tilmann C., and Capel B. Mesonephric cell migration induces testis cord formation and Sertoli cell differentiation in the mammalian gonad. Development 126 (1999) 2883-2890
47. Vidal V.P., Chaboissier M.C., de Rooij D.G., and Schedl A. Sox9 induces testis development in XX transgenic mice. Nat. Genet. 28 (2001) 216-217
48. Wilhelm D., Martinson F., Bradford S., Wilson M.J., Combes A.N., Beverdam A., Bowles J., Mizusaki H., and Koopman P. Sertoli cell differentiation is induced both cell-autonomously and through prostaglandin signaling during mammalian sex determination. Dev. Biol. 287 (2005) 111-124
49. Wilhelm D., Hiramatsu R., Mizusaki H., Widjaja L., Combes A.N., Kanai Y., and Koopman P. SOX9 regulates prostaglandin D synthase gene transcription in vivo to ensure testis development. J. Biol. Chem. 282 (2007) 10553-10560