Analysis of medaka sox9 orthologue reveals a conserved role in germ cell maintenance

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Nakamura, Shuhei ^a   Watakabe, Ikuko ^a   Nishimura, Toshiya ^a,b   Toyoda, Atsushi ^c   Taniguchi, Yoshihito ^d   Tanaka, Minoru ^a,b  

^a NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^c NATIONAL INSTITUTE OF GENETICS   (Japan)

^d KEIO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR SOX9;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; EXTRACELLULAR MATRIX; FEMALE; GENE DOSAGE; GENE EXPRESSION; GERM CELL; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; ORYZIAS; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEX DETERMINATION; ALLELE; ANIMAL; APOPTOSIS; CELL COUNT; CHEMISTRY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HETEROZYGOTE; METABOLISM; MOLECULAR GENETICS; MUTATION; SEQUENCE HOMOLOGY; SEX DETERMINATION PROCESS; SEX DIFFERENTIATION; SYNTENY; TESTIS;

ANIMALIA; MAMMALIA; ORYZIAS LATIPES; ORYZIINAE; VERTEBRATA;

ALLELES; ANIMALS; APOPTOSIS; BASE SEQUENCE; CELL COUNT; CELL PROLIFERATION; CELL SURVIVAL; CONSERVED SEQUENCE; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION REGULATION; GERM CELLS; HETEROZYGOTE; MALE; MOLECULAR SEQUENCE DATA; MUTATION; ORYZIAS; PHENOTYPE; SEQUENCE HOMOLOGY, AMINO ACID; SEX DETERMINATION PROCESSES; SEX DIFFERENTIATION; SOX9 TRANSCRIPTION FACTOR; SYNTENY; TESTIS;

EID: 84855789623     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029982     Document Type: Article

References (40)

1. Lincoln J, Kist R, Scherer G, Yutzey KE, (2007) Sox9 is required for precursor cell expansion and extracellular matrix organization during mouse heart valve development. Dev Biol 305: 120-132.
2. Hong CS, Saint-Jeannet JP, (2005) Sox proteins and neural crest development. Semin Cell Dev Biol 16: 694-703.
3. Jakob S, Lovell-Badge R, (2011) Sex determination and the control of Sox9 expression in mammals. FEBS J 278: 1002-1009.
4. Akiyama H, Lefebvre V, (2011) Unraveling the transcriptional regulatory machinery in chondrogenesis. J Bone Miner Metab 29: 390-395.
5. Vidal VPI, Chaboissier MC, de Rooij DG, Schedl A, (2001) Sox9 induces testis development in XX transgenic mice. Nat Genet 28: 216-217.
6. Wagner T, Wirth J, Meyer J, Zabel B, Held M, et al. (1994) Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the Sry-related gene Sox9. Cell 79: 1111-1120.
7. Sekido R, Lovell-Badge R, (2008) Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453: 930-934.
8. Huang B, Wang SB, Ning Y, Lamb AN, Bartley J, (1999) Autosomal XX sex reversal caused by duplication of SOX9. Am J Med Genet 87: 349-353.
9. Foster JW, Dominguezsteglich M, Guioli S, Kwok C, Weller P, et al. (1994) Campomelic dysplasia and autosomal sex reversal caused by mutations in an Sry-related gene. Nature 372: 525-530.
10. Morais da Silva S, Hacker A, Harley V, Goodfellow P, Swain A, et al. (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.
11. Western PS, Harry JL, Graves JAM, Sinclair AH, (1999) Temperature-dependent sex determination: Upregulation of SOX9 expression after commitment to male development. Dev Dyn 214: 171-177.
12. Barske LA, Capel B, (2010) Estrogen represses SOX9 during sex determination in the red-eared slider turtle Trachemys scripta. Dev Biol 341: 305-314.
13. Tanaka M, (2011) Interaction of Germ Cells and Gonadal Somatic Cells During Gonadal Formation. In: Naruse K, Tanaka M, Takeda H, editors. Medaka: A model for Organogenesis, Human Disease, and Evolution Heidelberg Springer pp. 219-227.
14. Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, et al. (2002) DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417: 559-563.
15. Nanda I, Kondo M, Hornung U, Asakawa S, Winkler C, et al. (2002) A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proc Natl Acad Sci USA 99: 11778-11783.
16. Kohara Y, Kasahara M, Naruse K, Sasaki S, Nakatani Y, et al. (2007) The medaka draft genome and insights into vertebrate genome evolution. Nature 447: 714-719.
17. 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.
18. 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 333: 729-736.
19. Yokoi H, Kobayashi T, Tanaka M, Nagahama Y, Wakamatsu Y, et al. (2002) Sox9 in a teleost fish, medaka (Oryzias latipes): evidence for diversified function of Sox9 in gonad differentiation. Mol Reprod Dev 63: 5-16.
20. Nakamura S, Aoki Y, Saito D, Kuroki Y, Fujiyama A, et al. (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.
21. Nakamura S, Kobayashi K, Nishimura T, Higashijima S, Tanaka M, (2010) Identification of germline stem cells in the ovary of the teleost medaka. Science 328: 1561-1563.
22. Chiang EF, Pai CI, Wyatt M, Yan YL, Postlethwait J, et al. (2001) Two sox9 genes on duplicated zebrafish chromosomes: expression of similar transcription activators in distinct sites. Dev Biol 231: 149-163.
23. Rodriguez-Mari A, Yan YL, Bremiller RA, Wilson C, Canestro C, et al. (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.
24. Taniguchi Y, Takeda S, Furutani-Seiki M, Kamei Y, Todo T, et al. (2006) Generation of medaka gene knockout models by target-selected mutagenesis. Genome Biol 7: R116.
25. Shibata Y, Paul-Prasanth B, Suzuki A, Usami T, Nakamoto M, et al. (2010) Expression of gonadal soma derived factor (GSDF) is spatially and temporally correlated with early testicular differentiation in medaka. Gene Expr Patterns 10: 283-289.
26. Nakamura S, Kurokawa H, Asakawa S, Shimizu N, Tanaka M, (2009) Two distinct types of theca cells in the medaka gonad: germ cell-dependent maintenance of cyp19a1-expressing theca cells. Dev Dyn 238: 2652-2657.
27. Barrionuevo F, Georg I, Scherthan H, Lecureuil C, Guillou F, et al. (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.
28. Kanamori A, Nagahama Y, Egami N, (1985) Development of the tissue architecture in the gonads of the medaka Oryzias latipes. Zool Sci 2: 695-706.
29. Saito D, Morinaga C, Aoki Y, Nakamura S, Mitani H, et al. (2007) Proliferation of germ cells during gonadal sex differentiation in medaka: Insights from germ cell-depleted mutant zenzai. Dev Biol 310: 280-290.
30. Matoba S, Hiramatsu R, Kanai-Azuma M, Tsunekawa N, Harikae K, et al. (2008) Establishment of testis-specific SOX9 activation requires high-glucose metabolism in mouse sex differentiation. Dev Biol 324: 76-87.
31. Kurokawa H, Saito D, Nakamura S, Katoh-Fukui Y, Ohta K, et al. (2007) Germ cells are essential for sexual dimorphism in the medaka gonad. Proc Natl Acad Sci USA 104: 16958-16963.
32. Tanaka M, Saito D, Morinaga C, Kurokawa H, (2008) Cross talk between germ cells and gonadal somatic cells is critical for sex differentiation of the gonads in the teleost fish, medaka (Oryzias latipes). Dev Growth Differ 50: 273-278.
33. Morinaga C, Saito D, Nakamura S, Sasaki T, Asakawa S, et al. (2007) The hotei mutation of medaka in the anti-Müllerian hormone receptor causes the dysregulation of germ cell and sexual development. Proc Natl Acad Sci USA 104: 9691-9696.
34. Bell DM, Leung KK, Wheatley SC, Ng LJ, Zhou S, et al. (1997) SOX9 directly regulates the type-II collagen gene. Nat Genet 16: 174-178.
35. Bi W, Deng JM, Zhang Z, Behringer RR, de Crombrugghe B, (1999) Sox9 is required for cartilage formation. Nat Genet 22: 85-89.
36. Bagheri-Fam S, Sinclair AH, Koopman P, Harley VR, (2010) Conserved regulatory modules in the Sox9 testis-specific enhancer predict roles for SOX, TCF/LEF, Forkhead, DMRT, and GATA proteins in vertebrate sex determination. Int J Biochem Cell Biol 42: 472-477.
37. Nakamura S, Saito D, Tanaka M, (2008) Generation of transgenic medaka using modified bacterial artificial chromosome. Dev Growth Differ 50: 415-419.
38. Aoki Y, Nagao I, Saito D, Ebe Y, Kinjo M, et al. (2008) Temporal and spatial localization of three germline-specific proteins in medaka. Dev Dyn 237: 800-807.
39. Nakamura S, Kobayashi D, Aoki Y, Yokoi H, Ebe Y, et al. (2006) Identification and lineage tracing of two populations of somatic gonadal precursors in medaka embryos. Dev Biol 295: 678-688.
40. Nojima H, Rothhamel S, Shimizu T, Kim CH, Yonemura S, et al. (2010) Syntabulin, a motor protein linker, controls dorsal determination. Development 137: 923-933.