Sox9 and Sox8 are required for basal lamina integrity of testis cords and for suppression of FOXL2 during embryonic testis development in mice

Biology of Reproduction

Volumn 87, Issue 4, 2012, Pages

  Georg, Ina ^a,b   Barrionuevo, Francisco ^b   Wiech, Thorsten ^a,c   Scherer, Gerd ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF GRANADA   (Spain)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

FOXL2; Sertoli cells; Sox10; Sox8; Sox9; Testis cords

Indexed keywords

COLLAGEN; COLLAGEN IXA3; COLLAGEN TYPE 4; TESTATIN; TRANSCRIPTION FACTOR SOX8; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; CELL DIFFERENTIATION; CELL ISOLATION; CELL TRANSDIFFERENTIATION; CHROMOSOME INACTIVATION; CONTROLLED STUDY; EMBRYO DEVELOPMENT; EXTRACELLULAR MATRIX; GENE; HISTOLOGY; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SERTOLI CELL; SEX TRANSFORMATION; TESTIS; TRANSCRIPTION REGULATION; ULTRASTRUCTURE;

ANIMALS; BASEMENT MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL TRANSDIFFERENTIATION; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE SILENCING; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PREGNANCY; SERTOLI CELLS; SOX9 TRANSCRIPTION FACTOR; SOXE TRANSCRIPTION FACTORS; TESTIS;

MAMMALIA; MUS;

EID: 84869468368     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.101907     Document Type: Article

References (65)

1. Wagner T, Wirth J, Meyer J, Zabel B, Held M, Zimmer J, Pasantes J, Bricarelli FD, Keutel J, Hustert E, Wolf U, Tommerup N, et al. Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 1994; 79:1111-1120.
2. Foster JW, Dominguez-Steglich MA, Guioli S, Kwok C, Weller PA, Stevanovic M, Weissenbach J, Mansour S, Young ID, Goodfellow PN.Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature 1994; 372:525-530.
3. Morais da Silva S, Hacker A, Harley V, Goodfellow P, Swain A, Lovell-Badge R. Sox9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds.Nat Genet 1996; 14:62-68.
4. Kent J, Wheatley SC, Andrews JE, Sinclair AH, Koopman P. A malespecific role for SOX9 in vertebrate sex determination. Development 1996; 122:2813-2822.
5. Sekido R, Bar I, Narvaez V, Penny G, Lovell-Badge R. SOX9 is upregulated by the transient expression of SRY specifically in Sertoli cell precursors. Dev Biol 2004; 274:271-279.
6. Sekido R, Lovell-Badge R. Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 2008; 453:930-934.
7. Hanley NA, Hagan DM, Clement-Jones M, Ball SG, Strachan T, Salas-Cortés L, McElreavey K, Lindsay S, Robson S, Bullen P, Ostrer H, Wilson DI. SRY, SOX9, and DAX1 expression patterns during human sex determination and gonadal development. Mech Dev 2000; 91:403-407.
8. Bishop CE, Whitworth DJ, Qin Y, Agoulnik AI, Agoulnik IU, Harrison WR, Behringer RR, Overbeek PA. A transgenic insertion upstream of sox9 is associated with dominant XX sex reversal in the mouse. Nat Genet 2000; 26:490-494.
9. Vidal VP, Chaboissier MC, de Rooij DG, Schedl A. Sox9 induces testis development in XX transgenic mice. Nat Genet 2001; 28:216-217.
10. Chaboissier M-C, Kobayashi A, Vidal VIP, Lützkendorf S, van de Kant HJG, Wegner M, de Rooij DG, Behringer RR, Schedl A. Functional analysis of Sox8 and Sox9 during sex determination in the mouse.Development 2004; 131:1891-1901.
11. Barrionuevo F, Bagheri-Fam S, Klattig J, Kist R, Taketo MM, Englert C, Scherer G. Homozygous inactivation of Sox9 causes complete XY sex reversal in mice. Biol Reprod 2006; 74:195-201.
12. Sock E, Schmidt K, Hermanns-Borgmeyer I, Bösl MR, Wegner M.Idiopathic weight reduction in mice deficient in the high-mobility-group transcription factor Sox8. Mol Cell Biol 2001; 21:6951-6959.
13. O'Bryan MK, Takada S, Kennedy CL, Scott G, Harada S, Ray MK, Dai Q, Wilhelm D, de Kretser DM, Eddy EM, Koopman P, Mishina Y. Sox8 is a critical regulator of adult Sertoli cell function and male fertility. Dev Biol 2008; 316:359-370.
14. Barrionuevo F, Georg I, Scherthan H, Lécureuil C, Guillou F, Wegner M, Scherer G. Testis cord differentiation after the sex determination stage is independent of Sox9 but fails in the combined absence of Sox9 and Sox8.Dev Biol 2009; 327:301-312.
15. Peirano RI, Wegner M. The glial transcription factor Sox10 binds to DNA both as monomer and dimer with different functional consequences.Nucleic Acids Res 2000; 28:3047-3055.
16. Britsch S, Goerich DE, Riethmacher D, Peirano RI, Rossner M, Nave KA, Birchmeier C, Wegner M. The transcription factor Sox10 is a key regulator of peripheral glial development. Genes Dev 2001; 15:66-78.
17. Polanco JC, Wilhelm D, Davidson T-L, Knight D, Koopman P. Sox10 gain-of-function causes XX sex reversal in mice: implications for human 22q-linked disorders of sex development. Hum Mol Genet 2010; 19:506-516.
18. Maatouk DM, DiNapoli L, Alvers A, Parker KL, Taketo MM, Capel B.Stabilization of beta-catenin in XY gonads causes male-to-female sexreversal.Hum Mol Genet 2008; 17:2949-2955.
19. Vainio S, Heikkilä M, Kispert A, Chin N, McMahon AP. Female development in mammals is regulated by Wnt-4 signalling. Nature 1999;397:405-409.
20. Jeays-Ward K, Hoyle C, Brennan J, Dandonneau M, Alldus G, Capel B, Swain A. Endothelial and steroidogenic cell migration are regulated by WNT4 in the developing mammalian gonad. Development 2003; 130:3663-3670.
21. Chassot A-A, Ranc F, Gregoire EP, Roepers-Gajadien HL, Taketo MM, Camerino G, de Rooij DG, Schedl A, Chaboissier M-C. Activation of beta-catenin signaling by Rspo1 controls differentiation of the mammalian ovary. Hum Mol Genet 2008; 17:1264-1277.
22. Parma P, Radi O, Vidal V, Chaboissier MC, Dellambra E, Valentini S, Guerra L, Schedl A, Camerino G. R-spondin1 is essential in sex determination, skin differentiation and malignancy. Nat Genet 2006; 38:1304-1309.
23. Mandel H, Shemer R, Borochowitz ZU, Okopnik M, Knopf C, Indelman M, Drugan A, Tiosano D, Gershoni-Baruch R, Choder M, Sprecher E.SERKAL syndrome: an autosomal-recessive disorder caused by a loss-offunction mutation in WNT4. Am J Hum Genet 2008; 82:39-47.
24. Crisponi L, Deiana M, Loi A, Chiappe F, Uda M, Amati P, Bisceglia L, Zelante L, Nagaraja R, Porcu S, Ristaldi MS, Marzella R, et al. The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ptosis/epicanthus inversus syndrome. Nat Genet 2001; 27:159-166.
25. De Baere E, Dixon MJ, Small KW, Jabs EW, Leroy BP, Devriendt K, Gillerot Y, Mortier G, Meire F, Van Maldergem L, Courtens W, Hjalgrim H, et al. Spectrum of FOXL2 gene mutations in blepharophimosis-ptosisepicanthus inversus (BPES) families demonstrates a genotype-phenotype correlation. Hum Mol Genet 2001; 10:1591-1600.
26. Uhlenhaut NH, Jakob S, Anlag K, Eisenberger T, Sekido R, Kress J, Treier A-C, Klugmann C, Klasen C, Holter NI, Riethmacher D, Schütz G, et al. Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 2009; 139:1130-1142.
27. Matson CK, Murphy MW, Sarver AL, Griswold MD, Bardwell VJ, Zarkower D. DMRT1 prevents female reprogramming in the postnatal mammalian testis. Nature 2011; 476:101-104.
28. Brennan J, Capel B. One tissue, two fates: molecular genetic events that underlie testis versus ovary development. Nat Rev Genet 2004; 5:509-521.
29. Perera EM, Martin H, Seeherunvong T, Kos L, Hughes IA, Hawkins JR, Berkovitz GD. Tescalcin, a novel gene encoding a putative EF-hand Ca(2p)-binding protein, Col9a3, and renin are expressed in the mouse testis during the early stages of gonadal differentiation. Endocrinology 2001; 142:455-463.
30. McClive PJ, Sinclair AH. Type II and type IX collagen transcript isoforms are expressed during mouse testis development. Biol Reprod 2003; 68:1742-1747.
31. Jeanes A, Wilhelm D, Wilson MJ, Bowles J, McClive PJ, Sinclair AH, Koopman P. Evaluation of candidate markers for the peritubular myoid cell lineage in the developing mouse testis. Reproduction 2005; 130:509-516.
32. McLaren A. Somatic and germ-cell sex in mammals. Philos Trans R Soc Lond B Biol Sci 1988; 322:3-9.
33. Kist R, Schrewe H, Balling R, Scherer G. Conditional inactivation of Sox9: a mouse model for campomelic dysplasia. Genesis 2002; 32:121-123.
34. Lécureuil C, Fontaine I, Crepieux P, Guillou F. Sertoli and granulosa cellspecific Cre recombinase activity in transgenic mice. Genesis 2002; 33:114-118.
35. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, Costantini F. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 2001; 1:4.
36. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001; 25:402-408.
37. Wilkinson DG, Nieto MA. Detection of messenger RNA by in situ hybridization to tissue sections and whole mounts. Meth Enzymol 1993;225:361-373.
38. Kuhlbrodt K, Herbarth B, Sock E, Hermans-Borgmeyer I, Wegner M.Sox10, a novel transcriptional modulator in glial cells. J Neurosci 1998;18:237-250.
39. Mazaud Guittot S, Vérot A, Odet F, Chauvin M-A, le Magueresse-Battistoni B. A comprehensive survey of the laminins and collagens type IV expressed in mouse Leydig cells and their regulation by LH/hCG.Reproduction 2008; 135:479-488.
40. Sumi E, Iehara N, Akiyama H, Matsubara T, Mima A, Kanamori H, Fukatsu A, Salant DJ, Kita T, Arai H, Doi T. SRY-related HMG box 9 regulates the expression of Col4a2 through transactivating its enhancer element in mesangial cells. Am J Pathol 2007; 170:1854-1864.
41. Bagchi RA, Czubryt MP. Scleraxis: a new regulator of extracellular matrix formation In: Ostadal B, Nagano M, Dhalla NS (eds.), Genes and Cardiovascular Function. New York: Springer; 2011:57-65.
42. Muir T, Sadler-Riggleman I, Skinner MK. Role of the basic helix-loophelix transcription factor, scleraxis, in the regulation of Sertoli cell function and differentiation. Mol Endocrinol 2005; 19:2164-2174.
43. Töhönen V, österlund C, Nordqvist K. Testatin: a cystatin-related gene expressed during early testis development. Proc Natl Acad Sci U S A 1998; 95:14208-14213.
44. Virtanen I, Kallajoki M, Närvänen O, Paranko J, Thornell LE, Miettinen M, Lehto VP. Peritubular myoid cells of human and rat testis are smooth muscle cells that contain desmin-type intermediate filaments. Anat Rec 1986; 215:10-20.
45. Raymond CS, Murphy MW, O'Sullivan MG, Bardwell VJ, Zarkower D.Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev 2000; 14:2587-2595.
46. Lei N, Hornbaker KI, Rice DA, Karpova T, Agbor VA, Heckert LL. Sexspecific differences in mouse DMRT1 expression are both cell type- and stage-dependent during gonad development. Biol Reprod 2007; 77:466-475.
47. Tung PS, Skinner MK, Fritz IB. Cooperativity between Sertoli cells and peritubular myoid cells in the formation of the basal lamina in the seminiferous tubule. Ann N Y Acad Sci 1984; 438:435-446.
48. Cool J, Carmona FD, Szucsik JC, Capel B. Peritubular myoid cells are not the migrating population required for testis cord formation in the XY gonad. Sex Dev 2008; 2:128-133.
49. Bi W, Huang W, Whitworth DJ, Deng JM, Zhang Z, Behringer RR, de Crombrugghe B. Haploinsufficiency of Sox9 results in defective cartilage primordia and premature skeletal mineralization. Proc Natl Acad Sci U S A 2001; 98:6698-6703.
50. Bell DM, Leung KK, Wheatley SC, Ng LJ, Zhou S, Ling KW, Sham MH, Koopman P, Tam PP, Cheah KS. SOX9 directly regulates the type-II collagen gene. Nat Genet 1997; 16:174-178.
51. Bridgewater LC, Lefebvre V, de Crombrugghe B. Chondrocyte-specific enhancer elements in the Col11a2 gene resemble the Col2a1 tissuespecific enhancer. J Biol Chem 1998; 273:14998-15006.
52. Sekiya I, Tsuji K, Koopman P, Watanabe H, Yamada Y, Shinomiya K, Nifuji A, Noda M. SOX9 enhances aggrecan gene promoter/enhancer activity and is up-regulated by retinoic acid in a cartilage-derived cell line, TC6. J Biol Chem 2000; 275:10738-10744.
53. Han Y, Lefebvre V. L-Sox5 and Sox6 drive expression of the aggrecan gene in cartilage by securing binding of Sox9 to a far-upstream enhancer.Mol Cell Biol 2008; 28:4999-5013.
54. Lincoln J, Kist R, Scherer G, Yutzey KE. Sox9 is required for precursor cell expansion and extracellular matrix organization during mouse heart valve development. Dev Biol 2007; 305:120-132.
55. Airik R, Trowe M-O, Foik A, Farin HF, Petry M, Schuster-Gossler K, Schweizer M, Scherer G, Kist R, Kispert A. Hydroureternephrosis due to loss of Sox9-regulated smooth muscle cell differentiation of the ureteric mesenchyme. Hum Mol Genet 2010; 19:4918-4929.
56. Barrionuevo F, Naumann A, Bagheri-Fam S, Speth V, Taketo MM, Scherer G, Neubüser A. Sox9 is required for invagination of the otic placode in mice. Dev Biol 2008; 317:213-224.
57. Stolt CC, Lommes P, Friedrich RP, Wegner M. Transcription factors Sox8 and Sox10 perform non-equivalent roles during oligodendrocyte development despite functional redundancy. Development 2004; 131:2349-2358.
58. Kellerer S, Schreiner S, Stolt CC, Scholz S, Bösl MR, Wegner M.Replacement of the Sox10 transcription factor by Sox8 reveals incomplete functional equivalence. Development 2006; 133:2875-2886.
59. Reginensi A, Clarkson M, Neirijnck Y, Lu B, Ohyama T, Groves AK, Sock E, Wegner M, Costantini F, Chaboissier M-C, Schedl A. SOX9 controls epithelial branching by activating RET effector genes during kidney development. Hum Mol Genet 2011; 20:1143-1153.
60. Pingault V, Bondurand N, Kuhlbrodt K, Goerich DE. Préhu M-O, Puliti A, Herbarth B, Hermans-Borgmeyer I, Legius E, Matthijs G, Amiel J, Lyonnet S, et al. SOX10 mutations in patients with Waardenburg-Hirschsprung disease. Nat Genet 1998; 18:171-173.
61. Kim Y, Kobayashi A, Sekido R, DiNapoli L, Brennan J, Chaboissier M-C, Poulat F, Behringer RR, Lovell-Badge R, Capel B. Fgf9 and Wnt4 act as antagonistic signals to regulate mammalian sex determination. PLoS Biol 2006; 4:e187.
62. Gao F, Maiti S, Alam N, Zhang Z, Deng JM, Behringer RR, Lécureuil C, Guillou F, 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 2006; 103:11987-11992.
63. Chang H, Gao F, Guillou F, Taketo MM, Huff V, Behringer RR. Wt1 negatively regulates beta-catenin signaling during testis development.Development 2008; 135:1875-1885.
64. Ottolenghi C, Omari S, Garcia-Ortiz JE, Uda M, Crisponi L, Forabosco A, Pilia G, Schlessinger D. Foxl2 is required for commitment to ovary differentiation. Hum Mol Genet 2005; 14:2053-2062.
65. Ottolenghi C, Pelosi E, Tran J, Colombino M, Douglass E, Nedorezov T, Cao A, Forabosco A, Schlessinger D. Loss of Wnt4 and Foxl2 leads to female-to-male sex reversal extending to germ cells. Hum Mol Genet 2007; 16:2795-2804.