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A male-specific role for SOX9 in vertebrate sex determination
Abstract
Mutation analyses of patients with campomelic dysplasia, a bone dysmorphology and XY sex reversal syndrome, indicate that the SRY-related gene SOX9 is involved in both skeletal development and sex determination. To clarify the role SOX9 plays in vertebrate sex determination, we have investigated its expression during gonad development in mouse and chicken embryos. In the mouse, high levels of Sox9 mRNA were found in male (XY) but not female (XX) genital ridges, and were localised to the sex cords of the developing testis. Purified fetal germ cells lacked Sox9 expression, indicating that Sox9 expression is specific to the Sertoli cell lineage. Sex specificity of SOX9 protein expression was confirmed using a polyclonal antiserum. The timing and cell-type specificity of Sox9 expression suggests that Sox9 may be directly regulated by SRY. Male-specific expression of cSOX9 mRNA during the sex determination period was also observed in chicken genital ridges. The conservation of sexually dimorphic expression in two vertebrate classes which have significant differences in their sex determination mechanisms, points to a fundamental role for SOX9 in testis determination in vertebrates. Sox9 expression was maintained in the mouse testis during fetal and adult life, but no expression was seen at any stage by in situ hybridisation in the developing ovary. Male-specific expression was also observed in the cells surrounding the Müllerian ducts and in the epididymis, and expression in both sexes was detected in the developing collecting ducts of the metanephric kidney. These results suggest that SOX9 may have a wider role in the development of the genitourinary system.
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Citations
Cites
Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4
LAEMMLI, U. K. (1970) · Nature · doi:10.1038/227680a0 · Cited by 249,961
Manipulating the mouse embryo: A laboratory manual
Hogan, B. L. M., Costantini, F. D., & Lacy, E. (1986) · Cited by 4,460
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., & Goodfellow, P. N. (1990) · Nature · doi:10.1038/346240a0 · Cited by 3,236
Self-citationManipulating the mouse embryo: A laboratory manual
Johnson, M. (1986) · Trends in Genetics · doi:10.1016/0168-9525(86)90275-1 · Cited by 2,245
Male development of chromosomally female mice transgenic for Sry
Koopman, P., Gubbay, J., Vivian, N., Goodfellow, P., & Lovell-Badge, R. (1991) · Nature · doi:10.1038/351117a0 · Cited by 2,194
Self-citationGubbay, J., Collignon, J., Koopman, P., Capel, B., Economou, A., Münsterberg, A., Vivian, N., Goodfellow, P., & Lovell-Badge, R. (1990) · Nature · doi:10.1038/346245a0 · Cited by 1,676
Self-citationLuo, X., Ikeda, Y., & Parker, K. L. (1994) · Cell · doi:10.1016/0092-8674(94)90211-9 · Cited by 1,631
Wagner, T., Wirth, J., Meyer, J., Zabel, B., Held, M., Zimmer, J., Pasantes, J., Bricarelli, F. D., Keutel, J., Hustert, E., et al. (1994) · Cell · doi:10.1016/0092-8674(94)90041-8 · Cited by 1,618
Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene
Foster, J. W., Dominguez-Steglich, M. A., Guioli, S., Kwok, C., Weller, P. A., Stevanović, M., Weissenbach, J., Mansour, S., Young, I. D., Goodfellow, P. N., et al. (1994) · Nature · doi:10.1038/372525a0 · Cited by 1,612
A SEX-CHROMOSOME ANOMALY IN A CASE OF GONADAL DYSGENESIS (TURNER'S SYNDROME)
FORD, C. (1959) · The Lancet · doi:10.1016/s0140-6736(59)91893-8 · Cited by 1,354
The mouse; its reproduction and development
Rugh, R. (1968) · Medical Entomology and Zoology · Cited by 1,251
A Case of Human Intersexuality Having a Possible XXY Sex-Determining Mechanism
JACOBS, P. A., & STRONG, J. A. (1959) · Nature · doi:10.1038/183302a0 · Cited by 1,130
Cate, R. L., Mattaliano, R. J., Hession, C., Tizard, R., Farber, N. M., Cheung, A., Ninfa, E. G., Frey, A. Z., Gash, D. J., Chow, E. P., et al. (1986) · Cell · doi:10.1016/0092-8674(86)90783-x · Cited by 1,022
Genetic evidence equating SRY and the testis-determining factor
Berta, P., Hawkins, J. B., Sinclair, A. H., Taylor, A., Griffiths, B. L., Goodfellow, P. N., & Fellous, M. (1990) · Nature · doi:10.1038/348448a0 · Cited by 982
Self-citationZanaria, E., Muscatelli, F., Bardoni, B., Strom, T. M., Guioli, S., Guo, W., Lalli, E., Moser, C., Walker, A. P., McCabe, E. R. B., et al. (1994) · Nature · doi:10.1038/372635a0 · Cited by 858
Expression of a candidate sex-determining gene during mouse testis differentiation
Koopman, P., Münsterberg, A., Capel, B., Vivian, N., & Lovell-Badge, R. (1990) · Nature · doi:10.1038/348450a0 · Cited by 848
Self-citationMuscatelli, F., Strom, T. M., Walker, A. P., Zanaria, E., Récan, D., Meindl, A., Bardoni, B., Guioli, S., Zehetner, G., Rabl, W., et al. (1994) · Nature · doi:10.1038/372672a0 · Cited by 767
Oxford reviews of reproductive biology
(1981) · Comparative Biochemistry and Physiology Part A: Physiology · doi:10.1016/0300-9629(81)93042-5 · Cited by 751
Müllerian-inhibiting substance function during mammalian sexual development
Behringer, R. R., Finegold, M. J., & Cate, R. L. (1994) · Cell · doi:10.1016/0092-8674(94)90251-8 · Cited by 679
The Sry-related gene Sox9 is expressed during chondrogenesis in mouse embryos
Wright, E., Hargrave, M. R., Christiansen, J., Cooper, L., Kun, J., Evans, T., Gangadharan, U., Greenfield, A., & Koopman, P. (1995) · Nature Genetics · doi:10.1038/ng0195-15 · Cited by 659
Self-citationA dosage sensitive locus at chromosome Xp21 is involved in male to female sex reversal
Bardoni, B., Zanaria, E., Guioli, S., Floridia, G., Worley, K. C., Tonini, G., Ferrante, E., Chiumello, G., McCabe, E. R. B., Fraccaro, M., et al. (1994) · Nature Genetics · doi:10.1038/ng0894-497 · Cited by 610
Expression of Sry, the mouse sex determining gene
Hacker, A., Capel, B., Goodfellow, P., & Lovell-Badge, R. (1995) · Development · doi:10.1242/dev.121.6.1603 · Cited by 570
Shen, W.-H., Moore, C. C. D., Ikeda, Y., Parker, K. L., & Ingraham, H. A. (1994) · Cell · doi:10.1016/0092-8674(94)90050-7 · Cited by 559
A Dosage Sensitive Locus at Chromosome Xp21 Is Involved in Male to Female Sex Reversal
Bardoni, B., Zanaria, E., Guioli, S., Floridia, G., Worley, K. C., Tonini, G., Ferrante, E., Chiumello, G., McCabe, E. R. B., Fraccaro, M., et al. (1995) · Obstetrical & Gynecological Survey · doi:10.1097/00006254-199502000-00020 · Cited by 539
Münsterberg, A., & Lovell-Badge, R. (1991) · Development · doi:10.1242/dev.113.2.613 · Cited by 480
DNA Binding Activity of Recombinant SRY from Normal Males and XY Females
Harley, V. R., Jackson, D. I., Hextall, P. J., Hawkins, J. R., Berkovitz, G. D., Sockanathan, S., Lovell-Badge, R., & Goodfellow, P. N. (1992) · Science · doi:10.1126/science.1734522 · Cited by 457
Differentiation of mammalian embryonic gonad
Byskov, A. G. (1986) · Physiological Reviews · doi:10.1152/physrev.1986.66.1.71 · Cited by 456
Abnormal sexual development in transgenic mice chronically expressing Müllerian inhibiting substance
Behringer, R. R., Cate, R. L., Froelick, G. J., Palmiter, R. D., & Brinster, R. L. (1990) · Nature · doi:10.1038/345167a0 · Cited by 437
SRY AND SEX DETERMINATION IN MAMMALS
Goodfellow, P. N., & Lovell-Badge, R. (1993) · Annual Review of Genetics · doi:10.1146/annurev.ge.27.120193.000443 · Cited by 426
An amino-terminal c-myc domain required for neoplastic transformation activates transcription.
Kato, G. J., Barrett, J., Villa-Garcia, M., & Dang, C. V. (1990) · Molecular and Cellular Biology · doi:10.1128/mcb.10.11.5914 · Cited by 410
A human XY female with a frame shift mutation in the candidate testis-determining gene SRY
Jäger, R. J., Anvret, M., Hall, K., & Scherer, G. (1990) · Nature · doi:10.1038/348452a0 · Cited by 408
Swain, A., Zanaria, E., Hacker, A., Lovell-Badge, R., & Camerino, G. (1996) · Nature Genetics · doi:10.1038/ng0496-404 · Cited by 401
Uwanogho, D., Rex, M., Cartwright, E. J., Pearl, G., Healy, C., Scotting, P. J., & Sharpe, P. T. (1995) · Mechanisms of Development · doi:10.1016/0925-4773(94)00299-3 · Cited by 391
The origin and function of the mammalian Y chromosome and Y‐borne genes – an evolving understanding
Graves, J. A. M. (1995) · BioEssays · doi:10.1002/bies.950170407 · Cited by 379
Sox-4, an Sry-like HMG box protein, is a transcriptional activator in lymphocytes.
van de Wetering, M., Oosterwegel, M., van Norren, K., & Clevers, H. (1993) · The EMBO Journal · doi:10.1002/j.1460-2075.1993.tb06063.x · Cited by 348
The nucleotide sequence of the chick cytoplasmic β-actin gene
Kost, T. A., Theodorakis, N., & Hughes, S. H. (1983) · Nucleic Acids Research · doi:10.1093/nar/11.23.8287 · Cited by 321
THE Y-CHROMOSOME AS THE BEARER OF MALE DETERMINING FACTORS IN THE MOUSE
Welshons, W. J., & Russell, L. B. (1959) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.45.4.560 · Cited by 308
Houston, C. S., Opitz, J. M., Spranger, J. W., Macpherson, R. I., Reed, M. H., Gilbert, E. F., Herrmann, J., & Schinzel, A. (1983) · American Journal of Medical Genetics · doi:10.1002/ajmg.1320150103 · Cited by 300
Baarends, W. M., Helmond, M. J. L. V., Post, M., Schoot, P. J. C. M. V. D., Hoogerbrugge, J. W., Winter, J. P. D., Uilenbroek, J. T. J., Karels, B., Wilming, L. G., Meijers, J. H. C., et al. (1994) · Development · doi:10.1242/dev.120.1.189 · Cited by 290
SOX3 is an X-linked gene related to SRY
Stevanovlć, M., Lovell-Badge, R., Collignon, J., & Goodfellow, P. N. (1993) · Human Molecular Genetics · doi:10.1093/hmg/2.12.2013 · Cited by 258
Haqq, C., King, C., Ukiyama, E., Falsafi, S., Haqq, T., Donahoe, P., & Weiss, M. (1994) · Science · doi:10.1126/science.7985018 · Cited by 257
Denny, P., Swift, S., Connor, F., & Ashworth, A. (1992) · The EMBO Journal · doi:10.1002/j.1460-2075.1992.tb05455.x · Cited by 256
Male sexual differentiation in mice lacking H–Y antigen
McLaren, A., Simpson, E., Tomonari, K., Chandler, P., & Hogg, H. (1984) · Nature · doi:10.1038/312552a0 · Cited by 225
The Origin and evolution of sex
Monroy, A. (1985) · Cited by 216
Seven new members of the Sox gene family expressed during mouse development
Wright, E. M., Snopek, B., & Koopman, P. (1993) · Nucleic Acids Research · doi:10.1093/nar/21.3.744 · Cited by 214
Self-citationSex reversal by loss of the C–terminal transactivation domain of human SOX9
Südbeck, P., Schmitz, M. L., Baeuerle, P. A., & Scherer, G. (1996) · Nature Genetics · doi:10.1038/ng0696-230 · Cited by 212
DNA-binding properties of the product of the testis-determining gene and a related protein
Nasrin, N., Buggs, C., Kong, X. F., Carnazza, J., Goebl, M., & Alexander-Bridges, M. (1991) · Nature · doi:10.1038/354317a0 · Cited by 201
Tommerup, N., Schempp, W., Meinecke, P., Pedersen, S., Bolund, L., Brandt, C., Goodpasture, C., Guldberg, P., Held, K. R., Reinwein, H., et al. (1993) · Nature Genetics · doi:10.1038/ng0693-170 · Cited by 195
Burgoyne, P. S., Buehr, M., Koopman, P., Rossant, J., & Mclaren, A. (1988) · Development · doi:10.1242/dev.102.2.443 · Cited by 193
Self-citationKanai, Y., Kanai-Azuma, M., Noce, T., Saido, T. C., Shiroishi, T., Hayashi, Y., & Yazaki, K. (1996) · The Journal of cell biology · doi:10.1083/jcb.133.3.667 · Cited by 189
Comparative Anatomy of the Vertebrates
Kent, G. C. (1969) · Cited by 163
A conserved family of genes related to the testis determining gene,SRY
Denny, P., Swift, S., Brand, N. J., Dabhade, N., Barton, P. J. R., & Ashworth, A. (1992) · Nucleic Acids Research · doi:10.1093/nar/20.11.2887 · Cited by 151
SRY recognizes conserved DNA sites in sex-specific promoters.
Haqq, C. M., King, C., Donahoe, P. K., & Weiss, M. A. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.3.1097 · Cited by 147
Connor, F., Wright, E. M., Denny, P., Koopman, P. A., & Ashworth, A. (1995) · Nucleic Acids Research · doi:10.1093/nar/23.17.3365 · Cited by 145
Self-citationChristiansen, J. H., Dennis, C. L., Wicking, C., Monkley, S. J., Wilkinson, D. G., & Wainwright, B. J. (1995) · Mechanisms of Development · doi:10.1016/0925-4773(95)00383-5 · Cited by 134
Palmer, S. J., & Burgoyne, P. S. (1991) · Development · doi:10.1242/dev.113.2.709 · Cited by 112
Kodama, H., Saitoh, H., Tone, M., Kuhara, S., Sakaki, Y., & Mizuno, S. (1987) · Chromosoma · doi:10.1007/bf00285878 · Cited by 109
Rossi, P., Dolci, S., Albanesi, C., Grimaldi, P., & Geremia, R. (1993) · Molecular Reproduction and Development · doi:10.1002/mrd.1080340404 · Cited by 85
Trans-activation and DNA-binding properties of the transcription factor, Sox-18
Hosking, B. M., Muscat, G. E. O., Koopman, P. A., Dowhan, D. H., & Dunn, T. L. (1995) · Nucleic Acids Research · doi:10.1093/nar/23.14.2626 · Cited by 81
Self-citationGriffiths, R. (1991) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1991.0060 · Cited by 78
Coriat, A., Müller, U., Harry, J. L., Uwanogho, D., & Sharpe, P. T. (1993) · Genome Research · doi:10.1101/gr.2.3.218 · Cited by 66
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Lefebvre, V., Li, P., & de Crombrugghe, B. (1998) · The EMBO Journal · doi:10.1093/emboj/17.19.5718 · Cited by 811
The Sox9 transcription factor determines glial fate choice in the developing spinal cord
Stolt, C. C., Lommes, P., Sock, E., Chaboissier, M.-C., Schedl, A., & Wegner, M. (2003) · Genes & Development · doi:10.1101/gad.259003 · Cited by 636
Wilms’ tumor 1 and Dax-1 modulate the orphan nuclear receptor SF-1 in sex-specific gene expression.
Nachtigal, M. W., Hirokawa, Y., Enyeart-VanHouten, D. L., Flanagan, J. N., Hammer, G. D., & Ingraham, H. A. (1998) · Cell · doi:10.1016/s0092-8674(00)81172-1 · Cited by 591
One tissue, two fates: molecular genetic events that underlie testis versus ovary development
Brennan, J., & Capel, B. (2004) · Nature Reviews Genetics · doi:10.1038/nrg1381 · Cited by 549
Bullock, S. L., Fletcher, J. M., Beddington, R. S. P., & Wilson, V. A. (1998) · Genes & Development · doi:10.1101/gad.12.12.1894 · Cited by 455
Metadata
- Authors
- Kent, J., Wheatley, S. C., Andrews, J. E., Sinclair, A. H., & Koopman, P.
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 1996-09-01
- Volume
- 122
- Issue
- 9
- Pages
- 2813-2822
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- OpenAlex
- W2157259126
- Cited by
- 710
- References
- 61
- FWCI
- 17.45
- Type
- journal article
- Language
- en
- Open access
- closed
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