Sex-specific expression of SOX9 during gonadogenesis in the amphibian Xenopus tropicalis

Developmental Dynamics

Volumn 237, Issue 10, 2008, Pages 2996-3005

  El Jamil, Anwar ^a   Kanhoush, Rasha ^a   Magre, Solange ^b   Boizet Bonhoure, Brigitte ^c   Penrad Mobayed, May ^a  

^a INSTITUT JACQUES MONOD   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c INSTITUTE OF HUMAN GENETICS   (France)

Author keywords

Gonad; Oocyte; Sertoli cell; SOX9 immunodetection; SOX9 in situ hybridization; Xenopus tropicalis

Indexed keywords

MESSENGER RNA; TRANSCRIPTION FACTOR SOX9;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOPLASM; FEMALE; GONAD DEVELOPMENT; MALE; METAMORPHOSIS; NONHUMAN; OOCYTE; OOCYTE DEVELOPMENT; OVARY DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SERTOLI CELL; TESTIS DEVELOPMENT; XENOPUS;

AMINO ACID SEQUENCE; ANIMALS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GONADS; HUMANS; MALE; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, MESSENGER; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SEX CHARACTERISTICS; SOX9 TRANSCRIPTION FACTOR; XENOPUS;

AMPHIBIA; VERTEBRATA; XENOPUS TROPICALIS;

EID: 54549114387     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21692     Document Type: Article

References (56)

1. Bell DM, Leung KK, Wheatley SC, Ng LJ, Zhou S, Ling KW, Sham MH, Koopman P, Tam PPL, Chah KSE. 1997. SOX9 directly regulates the type-II collagen gene. Nat Genet 16:174-178.
2. Bergstrom D, Young M, Albrecht K, Eicher E. 2000. Related function of mouse SOX3, SOX9 and SRY HMG domains assayed by male sex determination. Genesis 28:111-124.
3. Bishop CE, Whitworth DJ, Qin Y, Agoulnik AI, Agoulnik IU, Harrison WR, Behringer RR, Overbeek PA. 2000. A transgenic insertion upstream of sox9 is associated with dominant XX sex reversal in the mouse. Nat Genet 26:490-494.
4. Burgos MH, Fawcett DW. 1956. An electron microscope study of spermatid differentiation in the toad, Bufo arenarum Hensel. J Biophys Biochem Cytol 3:223-240.
5. Chaboissier MC, Kobayashi A, Vidal VI, Lützkendorf S, van de Kant HJ, Wegner M, de Rooij DG, Behringer RR, Schedl A. 2004. Functional analysis of Sox8 and Sox9 during sex determination in the mouse. Development 131:1891-1901.
6. Chavadej J, Jerareungrattana A, Sretarugsa P, Sobhon P. 2000. Structure and development of the testis of bullfrog, Rana catesbeiana, and their changes during seasonal variation. Science Asia 26:69-80.
7. Chiang EF, Pai CI, Wyatt M, Yan YL, Postlethwait J, Chung B. 2001, Two sox9 genes on duplicated zebrafish chromosomes: expression of similar transcription activators in distinct sites. Dev Biol 231:149-163.
8. Coggins LW. 1973. An ultrastructural and radioautographic study of early oogenesis in the toad Xenopus laevis. J Cell Sci 12:71-93.
9. Collenot G, Collenot A. 1977. L'activité 3βhydroxysté roide déshydrogénasique dans les gonads en différenciation de Pleurodeles waltlii(Amphibien, urodèle); visualization sur coupes sériées à l'aide d'une nouvelle technique histochimique. J Embryol Exp Morphol 42:29-42.
10. de Santa Barbara P, Moniot B, Poulat F, Berta P. 2000. Expression and subcellular localizationof SF-1, SOX9, WT1, and AMH proteins during early human testicular development. Dev Dyn 217:293-298.
11. DeFalco TJ, Verney G, Jenkins AB, McCaffery JM, Russell S, Van Doren M. 2003. Sex-specific apoptosis regulates sexual dimorphism in the Drosophila embryonic gonad. Dev Cell 5:205-216.
12. Dumont JN. 1972. Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J Morphol 136:153-179.
13. El Jamil A, Magre S, Mazabraud A, Penrad-Mobayed M. 2008. Early aspects of gonadal sex differentiation in Xenopus tropicalis with reference to an anteroposterior gradient. J Exp Zool Part A Ecol Genet Physiol 309:127-137.
14. Felsenstein J. 1989. PHYLIP- Phylogeny Inference Package (Version 3.2). Cladistics 5:164-166.
15. Fierro AC, Thuret R, Coen L, Perron M, Demeneix BA, Wegnez M, Gyapay G, Weissenbach J, Wincker P, Mazabraud A, Pollet N. 2007. Exploring nervous system transcriptomes during embryogenesis and metamorphosis in Xenopus tropicalis using EST analysis. BMC Genomics 8:118.
16. Fort DJ, Thomas JH, Rogers RL, Noll A, Spaulding CD, Guiney PD, Weeks JA. 2004. Evaluation of the developmental and reproductive toxicity of methoxychlor using an anuran (Xenopus tropicalis) chronic exposure model. Toxicol Sci 81:443-453.
17. Foster JW, Dominguez-Steglich MA, Guioli S, Kwok C, Weller PA, Stevanovic M, Weisenbach J, Mansour S, Young ID, Goodfellow PN, Brook JD, Schafer AJ. 1994. Campomelic dysplasia and autosomal sex reversal caused by mutations in a SRY-related gene. Nature 372:525-530.
18. Gasca S, Canizares J, De Santa Barbara P, Mejean C, Poulat F, Berta P, Boizet-Bonhoure B. 2002. A nuclear export signal within the high mobility group domain regulates the nucleocytoplasmic translocation of SOX9 during sexual determination. Proc Natl Acad Sci U S A 99:11199-11204.
19. Grammer TC, Khokha MK, Lane MA, Lam K, Harland RM. 2005. Identification of mutants in inbred Xenopus tropicalis. Mech Dev 22:263-272.
20. Hirsch N, Zimmerman LB, Grainger RM. 2002. Xenopus, the next generation: X. tropicalis genetics and genomics. Dev Dyn 225:422-433.
21. Huang B, Wang S, Ning Y, Lamb AN, Bartley J. 1999. Autosomal XX sex reversal caused by duplication of SOX9. Am J Med Genet 87:349-353.
22. Kalt MR. 1975. Mitochondrial pleiomorphism in sustentacular cells of Xenopus laevis. Anat Rec 1:53-60.
23. Kent J, Wheatley SC, Andrews JE, Sinclair AH, Koopman P. 1996. A male-specific role for SOX9 in vertebrate sex determination. Development 122:2813-2822.
24. Kiefer JC. 2007. Back to basics: Sox genes. Dev Dyn 236:2356-2366.
25. Klüver N, Kondo M, Herpin A, Mitani H, Schartl M. 2005. Divergent expression patterns of Sox9 duplicates in teleosts indicate a lineage specific subfunctionalization. Dev Genes Evol 215:297-305.
26. Larkin AM, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
27. Lefebvre V, Dumitriu B, Penzo-Méndez A, Han Y, Pallavi B. 2007. Control of cell fate and differentiation by Sry-related high-mobility-group box (Sox) transcription factors. Int J Biochem Cell Biol 39:2195-2214.
28. Lofts B. 1974. Reproduction. In: Lofts B , editor. Physiology of the amphibia. New York: Academic Press. p 107-218.
29. Malki S, Nef S, Notarnicola C, Thevenet L, Gasca S, Mejean C, Berta P, Poulat F, Boizet-Bonhoure B. 2005. Prostaglandin D2 induces nuclear import of the sex-determining factor SOX9 via its cAMP-PKA phosphorylation. EMBO J 24:1798-1809.
30. Meyer R, Posalky Z, McGinley D. 1977. Intercellular junction development in maturing rat seminiferous tubules. J Ultrastruct Res 61:271-283.
31. Morais da Silva S, Hacker A, Harley V. Goodfellow P, Swain A, 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.
32. Moreno-Mendoza N, Harley VR, Merchant-Larios H. 2001. Temperature regulates SOX9 expression in cultured gonads of Lepidochelys olivacea, a species with temperature sex determination. Dev Biol 229:319-326.
33. Morrish BC, Sinclair AH. 2002. Vertebrate sex determination: many means to an end. Reproduction. 124:447-457.
34. Nakamoto M, Suzuki A, Matsuda M, Nagahama Y, Shibata N. 2005. 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 300:729-736.
35. Nakamura S, Aoki Y, Saito D, Kuroki Y, Fujiyama A, Naruse K, Tanaka M. 2008. Sox9b/sox9a2-EGFP transgenic medaka reveals the morphological reorganization of the gonads and a common precursor of both the female and male supporting cells. Mol Reprod Dev 75:472-476.
36. Nieuwkoop PD, Faber J. 1967. Normal table of Xenopus laevis (Daudin): a systematical and chronological survey of the development from the fertilized egg till the end of metamorphosis, 2nd ed. Amsterdam: North-Holland.
37. Notarnicola C, Malki S, Berta P, Poulat F, Boizet-Bonhoure B. 2006. Transient expression of SOX9 protein during follicular development in the adult mouse ovary. Gene Expr Patterns 6:695-702.
38. Oréal E, Mazaud S, Picard JY, Magre S, Carré-Eusèbe D. 2002. Different patterns of anti-Müllerian hormone expression, as related to DMRT1, SF-1, WT1, GATA-4, Wnt-4, and Lhx9 expression, in the chick differentiating gonads. Dev Dyn 225:221-232.
39. Osawa N, Oshima Y, Nakamura M. 2005. Molecular cloning of Dmrt1 and its expression in the gonad of Xenopus. Zoolog Sci 6:681-687.
40. Penrad-Mobayed MM. 1983. Behavior of testicular and ovarian fragments of the newt pleurodele cultured in serum-free medium. In Vitro 19:435-442.
41. Risley MS. 1990. Support of Xenopus laevis spermatogenesis in vitro by different energy substrates. Biol Reprod 3:511-522.
42. Risley MS, Morse-Gaudio M. 1992. comparative aspects of spermatogenic cell metabolism and Sertoli cell function in Xenopus laevis and mammals. J Exp Zool 2:185-193.
43. Rodriguez-Mari A, Yan YL, Bremiller RA, Wilson C, Cañestro C, Postlethwait JH. 2005. Characterization and expression pattern of zebrafish Anti-Müllerian hormone (Amh) relative to sox9a, sox9b, and cyp19a1a, during gonad development. Gene Expr Patterns 5:655-667.
44. Sáez FJ, Madrid JF, Leis O, Aparicio R, Oporto B. 1999. Lectin histochemical localization of N- and O-linked oligosaccharides during the spermiogenesis o the urodele amphibian Pleurodeles waltl. Glycoconj J 16:639-648.
45. Sáez FJ, Madrid JF, Cardoso S, Goacute; mez L, Hernández F. 2004. Glycoconjugates of the urodele amphibian testis shown by lectin cytochemical methods. J Electron Microsc Tech 64:63-76.
46. Sekido R, Lovell-Badge R. 2008. Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 7197:930-934.
47. Sekido R, Bar I, Narváez V, Penny G, Lovell-Badge R. 2004. SOX9 is up-regulated by the transient expression of SRY specifically in Sertoli cell precursors. Dev Biol 274:271-279.
48. Smith JM, Koopman PA. 2004. The ins and outs of transcriptional control: nucleocytoplasmic shuttling in development and disease. Trends Genet 20:4-8.
49. Smyk M, Obersztyn E, Nowakowska B, Bocian E, Cheung SW, Mazurczak T, Stankiewicz P. 2007. Recurrent SOX9 deletion campomelic dysplasia due to somatic mosaicism in the father. Am J Med Genet A 143:866-870.
50. Song MO, Fort DJ, McLaughlin DL, Rogers RL, Thomas JH, Buzzard BO, Noll AM, Myers NK. 2003. Evaluation of Xenopus tropicalis as an alternative test organism for frog embryoteratogenesis assay-Xenopus (FETAX). Drug Chem Toxicol 26:177-189.
51. Takase M, Noguchi S, Nakamura M. 2000. Two Sox9 messenger RNA isoforms: isolation of cDNAs and their expression during gonadal development in the frog Rana rugosa. FEBS Lett 466:249-254.
52. Vaillant S, Magre S, Dorizzi M, Pieau C, Richard-Mercier N. 2001. Expression of AMH, SF1, and SOX9 in gonads of genetic female chickens during sex reversal induced by an aromatase inhibitor. Dev Dyn 222:228-237.
53. Vidal VP, Chaboissier MC, de Rooij DG, Schedl A. 2001. Sox9 induces testis development in XX transgenic mice. Nat Genet 28:216-217.
54. Wagner T, Wirth J, Meyer J, Zabel B, Heid M, Zimmer J, Pasantes J, Bricarelli FD, Keutel J, Huster E, Wolf U, Tommerup N, Schempp W, Scherer G. 1994. Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 79:1111-1120.
55. Western PS, Harry JL, Graves JA, Sinclair AH. 1999. Temperature dependent sex determination: upregulation of SOX9 expression after commitment to male development. Dev Dyn 216:171-177.
56. Yokoi H, Kobayashi T, Tanaka M, Nagahama Y, Wakamatsu Y, Takeda H, Araki K, Morohashi K, Ozato K. 2002. sox9 in a teleost fish, medaka (Oryzias latipes): evidence for diversified function of Sox9 in gonad differentiation, Mol Reprod Dev 63:5-16.