Loss of DNA-dependent dimerization of the transcription factor SOX9 as a cause for campomelic dysplasia

Human Molecular Genetics

Volumn 12, Issue 12, 2003, Pages 1439-1447

  Sock, Elisabeth ^a   Pagon, Roberta A ^b   Keymolen, Kathelijn ^c   Lissens, Willy ^c   Wegner, Michael ^a   Scherer, Gerd ^d  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^c UNIVERSITY HOSPITAL BRUSSELS   (Belgium)

^d UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; COLLAGEN; DNA; DNA BINDING PROTEIN; HIGH MOBILITY GROUP PROTEIN; MUTANT PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BINDING SITE; BONE BOWING; CAMPOMELIC DYSPLASIA; CARBOXY TERMINAL SEQUENCE; CARTILAGE; CHONDRODYSPLASIA; CHONDROGENESIS; CONTROLLED STUDY; DIMERIZATION; FEMALE; GENE DELETION; GENE MUTATION; HUMAN; KARYOTYPE 46,XY; LETHALITY; LONG BONE; MALE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRESCHOOL CHILD; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; SEX TRANSFORMATION; SKELETON MALFORMATION; TESTIS DEVELOPMENT; TISSUE DIFFERENTIATION; TRANSACTIVATION;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; BASE SEQUENCE; CERCOPITHECUS AETHIOPS; CHONDROGENESIS; COLLAGEN TYPE XI; COS CELLS; DIMERIZATION; DNA; DNA-BINDING PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EXTRACELLULAR MATRIX PROTEINS; FEMALE; GENE EXPRESSION REGULATION; HIGH MOBILITY GROUP PROTEINS; HUMANS; INFANT, NEWBORN; MALE; MOLECULAR SEQUENCE DATA; MUTATION; NEOPLASM PROTEINS; OSTEOCHONDRODYSPLASIAS; PROTEINS; RESPONSE ELEMENTS; SEQUENCE DELETION; SEQUENCE HOMOLOGY, AMINO ACID; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS; TRANSFECTION;

ANIMALIA;

EID: 0038039240     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (40)

1. Houston, C.S., Opitz, J.M., Spranger, J.W., Macpherson, R.I., Reed, M.H., Gilbert, E.F., Herrmann, J. and Schinzel, A. (1983) The campomelic syndrome: review, report of 17 cases, and follow-up on the currently 17-year-old boy first reported by Maroteaux et al. in 1971. Am. J. Med. Genet., 15, 3-28.
2. Mansour, S., Hall, C.M., Pembrey, M.E. and Young, I.D. (1995) A clinical and genetic study of campomelic dysplasia. J. Med. Genet., 32, 415-420.
3. Foster, J.W., Dominguez-Steglich, M.A., Guioli, S., Kwok, C., Weller, P.A., Stevanovic, M., Weissenbach, J., Mansour, S., Young, I.D., Goodfellow, P.N. et al. (1994) Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature, 372, 525-530.
4. Wagner, T., Wirth, J., Meyer, J., Zabel, B., Held, M., Zimmer, J., Pasantes, J., Bricarelli, F.D., Keutel, J., Hustert, E. et al. (1994) Amosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell, 79, 1111-1120.
5. Wright, E., Hargrave, M.R., Christiansen, J., Cooper, L., Kun, J., Evans, T., Gangadharan, U., Greenfield, A. and Koopman, P. (1995) The Sry-related gene Sox9 is expressed during chondrogenesis in mouse embryos. Nat. Genet., 9, 15-20.
6. Ng, L.J., Wheatley, S., Muscat, G.E.O., Conway-Campbell, J., Bowles, J., Wright, E., Bell, D.M., Tam, P.P., Cheah, K.S. and Koopman, P. (1997) SOX9 binds DNA, activates transcription, and coexpresses with type II collagen during chondrogenesis in the mouse. Dev. Biol., 183, 108-121.
7. Kent, J., Wheatley, S.C., Andrews, J.E., Sinclair, A.H. and Koopman, P. (1996) A male-specific role for SOX9 in vertebrate sex determination. Development, 122, 2813-2822.
8. Morais da Silva, S., Hacker, A., Harley, V., Goodfellow, P., Swain, A. and 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.
9. Bi, W., Huang, W., Whitworth, D.J., Deng, J.M., Zhang, Z., Behringer, R.R. and de Crombrugghe, B. (2001) Haploinsufficiency of Sox9 results in defective cartilage primordia and premature skeletal mineralization. Proc. Natl Acad. Sci. USA, 98, 6698-6703.
10. Kist, R., Schrewe, H., Balling, R. and Scherer, G. (2002) Conditional inactivation of Sox9: a mouse model for campomelic dysplasia. Genesis, 32, 121-123.
11. Akiyama, H., Chaboissier, M.-C., Martin, J.F., Schedl, A. and de Crombrugghe, B. (2002) The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev., 16, 2813-2829.
12. Lefebvre, V., Huang, W., Harley, V.R., Goodfellow, P.N. and de Crombrugghe, B. (1997) Sox9 is a potent activator of the chondrocyte-specific enhancer of the proα1(II) collagen gene. Mol. Cell. Biol., 17, 2336-2346.
13. Bridgewater, L.C., Lefebvre, V. and de Crombrugghe, B. (1998) Chondrocyte-specific enhancer elements in the Col11a2 gene resemble the Col2a1 tissue-specific enhancer. J. Biol. Chem., 273, 14998-15006.
14. Xie, W.F., Zhang, X., Sakano, S., Lefebvre, V. and Sandell, L.J. (1999) Trans-activation of the mouse cartilage-derived retinoic acid-sensitive protein gene by Sox9. J. Bone Miner Res., 14, 757-763.
15. Sekiya, I., Tsuji, K., Koopman, P., Watanabe, H., Yamada, Y., Shinomiya, K., Nifuji, A. and Noda, M. (2000) SOX9 enhances aggrecan gene promoter/enhancer activity and is up-regulated by retinoic acid in a cartilage-derived cell line, TC6. J. Biol. Chem., 275, 10738-10744.
16. de Santa Barbara, P., Bonneaud, N., Boizet, B., Desclozeaux, M., Moniot, B., Südbeck, P., Scherer, G., Poulat, F. and Berta, P. (1998) Direct interaction of SRY-related protein SOX9 and steroidogenic factor 1 regulates transcription of the human anti-Müllerian hormone gene. Mol. Cell. Biol., 18, 6653-6665.
17. Arango, N.A., Lovell-Badge, R. and Behringer, R.R. (1999) Targeted mutagenesis of the endogenous mouse Mis gene promoter: in vivo definition of genetic pathways of vertebrate sexual development. Cell, 99, 409-419.
18. Wegner, M. (1999) From head to toes: the multiple facets of Sox proteins. Nucl. Acids Res., 27, 1409-1420.
19. Bowles, J., Schepers, G. and Koopman, P. (2000) Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev. Biol., 227, 239-255.
20. McDowall, S., Argentaro, A., Ranganathan, S., Weller, P., Mertin, S., Mansour, S., Tolmie, J. and Harley, V. (1999) Functional and structural studies of wild type SOX9 and mutations causing campomelic dysplasia. J. Biol. Chem., 274, 24023-24030.
21. Südbeck, P., Schmitz, M.L., Baeuerle, P.A. and Scherer, G. (1996) Sex reversal by loss of the C-terminal transactivation domain of human SOX9. Nat. Genet., 13, 230-232.
22. Peirano, R.I. and Wegner, M. (2000) The glial transcription factor Sox10 binds to DNA both as monomer and dimer with different functional consequences. Nucl. Acids Res., 28, 3047-3055.
23. Südbeck, P. and Scherer, G. (1997) Two independent nuclear localization signals are present in the DNA-binding high-mobility group domains of SRY and SOX9. J. Biol. Chem., 272, 27848-27852.
24. Gasca, S., Canizares, J., de Santa Barbara, P., Mejean, C., Poulat, F., Berta, P. and 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. USA, 99, 11199-11204.
25. Rehberg, S., Lischka, P., Glaser, G., Stamminger, T., Wegner, M. and Rosorius, O. (2002) Sox10 is an active nucleocytoplasmic shuttle protein, and shuttling is crucial for Sox10-mediated transactivation. Mol. Cell. Biol., 22, 5826-5834.
26. Peirano, R.I., Goerich, D.E., Riethmacher, D. and Wegner, M. (2000) Protein zero expression is regulated by the glial transcription factor Sox10. Mol. Cell. Biol., 20, 3198-3209.
27. Lefebvre, V., Li, P. and de Crombrugghe, B. (1998) A new long form of Sox5 (L-Sox5), Sox6 and Sox9 are coexpressed in chondrogenesis and cooperatively activate the type II collagen gene. EMBO J, 17, 5718-5733.
28. Zhou, G., Lefebvre, V., Zhang, Z., Eberspaecher, H. and de Crombrugghe, B. (1998) Three high mobility group-like sequences within a 48-base pair enhancer of the Col2a1 gene are required for cartilage-specific expression in vivo. J. Biol. Chem., 273, 14989-14997.
29. Bridgewater, L.C., Walker, M.D., Miller, G.C., Ellison, T.A., Holsinger, L.D., Potter, J.L., Jackson, T.L., Chen, R.K., Winkel, V.L., Zhang, Z. et al. (2003) Adjacent DNA sequences modulate Sox9 transcriptional activation at paired Sox sites in three chondrocyte-specific enhancer elements. Nucl. Acids Res., 31, 1541-1553.
30. Koopman, P. (2001) Sry, Sox9 and mammalian sex determination. In Scherer, G. and Schmidt, M. (eds), Genes and Mechanisms in Vertebrate Sex Determination. Birkhäuser, Basel, pp. 25-56.
31. Cooper, D.N. and Krawczak, M. (1993) Human Gene Mutation. BIOS Scientific Publishers, Oxford.
32. Meyer, J., Südbeck, P., Held, M., Wagner, T., Schmitz, M.L., Bricarelli, F.D., Eggermont, E., Friedrich, U., Haas, O.A., Kobelt, A. et al. (1997) Mutational analysis of the SOX9 gene in campomelic dysplasia and autosomal sex reversal: lack of genotype/phenotype correlations. Hum. Mol. Genet., 6, 91-98.
33. Pfeifer, D., Kist, R., Dewar, K., Devon, K., Lander, E.S., Birren, B., Korniszewski, L., Back, E. and Scherer, G. (1999) Campomelic dysplasia translocation breakpoints are scattered over 1 Mb proximal to SOX9: evidence for an extended control region. Am. J. Hum. Genet., 65, 111-124.
34. Bondurand, N., Girard, M., Pingault, V., Lemort, N., Dubourg, O. and Goossens, M. (2001) Human Connexin 32, a gap junction protein altered in the X-linked form of Charcot-Marie-Tooth disease, is directly regulated by the transcription factor SOX10. Hum. Mol. Genet., 10, 2783-2795.
35. Stolt, C.C., Rehberg, S., Ader, M., Lommes, P., Riethmacher, D., Schachner, M., Bartsch, U. and Wegner, M. (2002) Terminal differentiation of myelin-forming oligodendrocytes depends on the transcription factor Sox10. Genes Dev., 16, 165-170.
36. Schlierf, B., Ludwig, A., Klenovsek, K. and Wegner, M. (2002) Cooperative binding of Sox10 to DNA: requirements and consequences. Nucl. Acids Res., 30, 5509-5516.
37. Kwok, C., Weller, P.A., Guioli, S., Foster, J.W., Mansour, S., Zuffardi, O., Punnett, H.H., Dominguez-Steglich, M.A., Brook, J.D., Young, I.D. et al. (1995) Mutations in SOX9, the gene responsible for campomelic dysplasia and autosomal sex reversal. Am. J. Hum. Genet., 57, 1028-1036.
38. Hageman, R.M., Cameron, F.J. and Sinclair, A.H. (1998) Mutation analysis of the SOX9 gene in a patient with campomelic dysplasia. Hum. Mutat., Suppl. 1, S112-S113.
39. Kuhlbrodt, K., Herbarth, B., Sock, E., Hermans-Borgmeyer, I. and Wegner, M. (1998) Sox10, a novel transcriptional modulator in glial cells. J Neurosci., 18, 237-250.
40. Tuerk, E.E., Schreiber, J. and Wegner, M. (2000) Protein stability and domain topology determine the transcriptional activity of the mammalian glial cells missing homolog, GCMb. J. Biol. Chem., 275, 4774-4782.