Phosphorylation of SOX9 by Cyclic AMP-Dependent Protein Kinase A Enhances SOX9's Ability To Transactivate aCol2a1 Chondrocyte-Specific Enhancer

REFERENCES

• Aronheim, A., Zandi, E., Hennemann, H., Elledge, S. J., and Karin, M.. 1997. Isolation of an AP-1 repressor by a novel method for detecting protein-protein interaction. Mol. Cell. Biol. 17:3094–3102
   PubMed Web of Science ®Google Scholar
• Bell, D. M., Leung, K. K. H., Whearley, S. C., Ng, L. J., Zhou, S., Ling, K. W., Sham, M. H., Koopman, P., Tam, P. P. L., and Cheah, K. S. E.. 1997. Sox9 directly regulates the type-II collagen gene. Nat. Genet. 16:174–178
   PubMed Web of Science ®Google Scholar
• Bi, W., Deng, J., Zhang, Z., Behringer, R. R., and de Crombrugghe, B.. 1999. Sox9 is required for cartilage formation. Nat. Genet. 22:85–89
   PubMed Web of Science ®Google Scholar
• Boulikas, T.. 1995. Phosphorylation of transcription factors and control of the cell cycle. Crit. Rev. Eukaryot. Gene Expression 5:1–77
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Desclozeaux, M., Poulat, F., de Santa Barbara, P., Capony, J. P., Turowski, P., Jay, P., Mejean, C., Moniot, B., Boizet, B., and Berta, P.. 1998. Phosphorylation of an N-terminal motif enhances DNA-binding activity of the human SRY protein. J. Biol. Chem. 273:7988–7995
   PubMedGoogle Scholar
• Fan, C., Porter, J. A., Chiang, C., Chang, D. T., Beachy, P. A., and Tessier-Lavigne, M.. 1995. Long-range sclerotome induction by Sonic hedgehog: direct role of the amino-terminal cleavage product and modulation by the cyclic AMP signaling pathway. Cell 81:457–465
   PubMed Web of Science ®Google Scholar
• 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., Brook, J. D., and Schafer, A. J.. 1994. Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature 372:525–530
   PubMed Web of Science ®Google Scholar
• Hammerschmidt, M., Bitgood, M. J., and McMahon, A. P.. 1996. Protein kinase A is a common negative regulator of hedgehog signaling in the vertebrate embryo. Genes Dev. 15:647–658
   Google Scholar
• Houston, C. S., Opitz, J. M., Spranger, J. W., Macpherson, R. I., Reed, M. H., Gilbert, E. F., Herrman, J., and Schinzel, A.. 1993. 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. 15:2–28
   Google Scholar
• Jüppner, H., Abou-Samra, A., Freeman, M., Kong, X., Schipani, E., Richards, J., Kolakowski, L. F., Hock, J., Potts, J. T., Kronenberg, H. M., and Segre, G. V.. 1991. A G protein-linked receptor for parathyroid hormone and parathyroid hormone-related peptide. Science 254:1024–1026
   PubMed Web of Science ®Google Scholar
• Kapaplis, A. C., Luz, A., Glowacki, J., Bronson, R. T., Tybulewicz, V. L. J., Kronenberg, H. M., and Mulligan, R. C.. 1994. Lethal skeletal dysplasia from targeted disruption of the parathyroid hormone-related peptide gene. Genes Dev. 8:277–289
   PubMedGoogle Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Kosher, R. A., Gay, S. W., Kamanitz, J. R., Kulyk, W. M., Rodger, B. J., Sai, S., Tanaka, T., and Tanzer, M. L.. 1986. Cartilage proteoglycan core protein gene expression during limb cartilage differentiation. Dev. Biol. 118:112–117
   PubMed Web of Science ®Google Scholar
• Kwok, C., Weller, P. A., Guioli, S., Foster, J. W., Mansour, S., Zuffardi, O., Punett, H. H., Dominguez-Steglich, M. A., Brook, J. D., Young, I. D., Goodfellow, P. N., and Schafer, A. J.. 1995. Mutations in SOX9, the gene responsible for campomelic dysplasia and autosomal sex reversal. Am. J. Hum. Genet. 57:1028–1036
   PubMedGoogle Scholar
• Lanske, B., Karaplis, A. C., Lee, K., Luz, A., Vortkamp, A., Pirro, A., Karperien, M., Defice, L. H. K., Ho, C., Mulligan, R. C., Alou-Samra, A., Juppner, H., Segre, G. V., and Kronenberg, H. M.. 1996. PTH/PTHrP receptor in early development and indian-hedgehog-regulated bone growth. Science 273:663–666
   PubMed Web of Science ®Google Scholar
• Lee, K., Lanske, B., Karaplis, A. C., Deeds, J. D., Kohno, H., Nissenson, R. A., Kronenberg, H. M., and Segre, G. V.. 1996. Parathyroid hormone-related peptide delays terminal differentiation of chondrocytes during endochondral bone development. Endocrinology 137:5109–5118
   PubMedGoogle Scholar
• Lee, Y. S., and Chuong, C. M.. 1997. Activation of protein kinase A is involved in both BMP-2- and cyclic AMP-induced chondrogenesis. J. Cell. Physiol. 170:153–165
   PubMed Web of Science ®Google Scholar
• Lefebvre, V., and de Crombrugghe, B.. 1998. Toward understanding SOX9 function in chondrocyte differentiation. Matrix Biol. 16:529–540
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Lefebvre, V., Zhou, G., Mukhopadhyay, K., Smith, C. N., Zhang, Z., Eberspaecher, H., Zhou, X., Sinha, S., Maity, S. N., and de Crombrugghe, B.. 1996. An 18-base-pair sequence in the mouse proα1(II) collagen gene is sufficient for cartilage expression and binds nuclear proteins that are selectively expressed in chondrocytes. Mol. Cell. Biol. 16:4512–4523
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Malemud, C. J., Mills, T. M., Shuckett, R., and Papay, R. S.. 1986. Stimulation of sulfated-proteoglycan synthesis by forskolin in monolayer cultures of rabbit articular chondrocytes. J. Cell. Physiol. 129:51–59
   PubMedGoogle Scholar
• 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
   PubMedGoogle Scholar
• Meyer, J., Südbeck, P., Held, M., Wagner, T., Schmitz, M. L., Bricarelli, F. D., Eggermont, E., Friedrich, U., Haas, O. A., Kobelt, A., Leroy, J. G., Van Maldergem, L., Michel, E., Mitulla, B., Pfeiffer, R. A., Schinzel, A., Schmidt, H., and Scherer, G.. 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
   PubMedGoogle Scholar
• 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. 13:62–68
   Google Scholar
• Ng, L.-J., Wheatley, S., Muscat, G. E. O., Conway-Campbell, J., Bowles, J., Wright, E., Bell, D. M., Tam, P. P. L., Cheah, K. S. E., 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
   PubMed Web of Science ®Google Scholar
• Rodgers, B. J., Kulyk, W. M., and Kosher, R. A.. 1989. Stimulation of limb cartilage differentiation by cyclic AMP is dependent on cell density. Cell Differ. Dev. 28:179–187
   PubMedGoogle Scholar
• Schipani, E., Lanske, B., Hunzelman, J., Luz, A., Koracs, C. S., Lee, K., Pirro, A., Kronenberg, H. M., and Jüppner, H.. 1997. Targeted expression of constitutively active receptors for parathyroid hormone and parathyroid hormone-related peptide delays endochondral bone formation and rescues mice that lack parathyroid hormone-related peptide. Proc. Natl. Acad. Sci. USA 94:13689–13694
   PubMed Web of Science ®Google Scholar
• Sinha, S., Maity, S. N., Lu, J., and de Crombrugghe, B.. 1995. Recombinant rat CBF-C, the third subunit of CBF/NFY, allows formation of a protein-DNA complex with CBF-A and CBF-B and with yeast HAP2 and HAP3. Proc. Natl. Acad. Sci. USA 92:1624–1628
   PubMed Web of Science ®Google Scholar
• Südbeck, P., Schmitz, 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Wagner, T., Wirth, J., Meyer, J., Zabel, B., Held, M., Zimmer, J., Pasantes, J., Dagna Bricarelli, F., Keutel, J., Hustert, E., Wolf, U., Tommerup, N., Schempp, W., and 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
   PubMed Web of Science ®Google Scholar
• Wirth, J., Wagner, T., Meyer, J., Pfeiffer, R. A., Tietze, H.-U., Schempp, W., and Scherer, G.. 1996. Translocation breakpoints in three patients with campomelic dysplasia and autosomal sex reversal map more than 130 kb from SOX9. Hum. Genet. 97:186–193
   PubMedGoogle Scholar
• Wright, E. M., Snopek, B., and Koopman, P.. 1993. Seven new members of the SOX gene family expressed during mouse development. Nucleic Acids Res. 21: 744
   PubMedGoogle Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Zhao, Q., Eberspaecher, H., Lefebvre, V., and de Crombrugghe, B.. 1997. Parallel expression of Sox9 and Col2a1 in cells undergoing chondrogenesis. Dev. Dyn. 209:377–386
   PubMed Web of Science ®Google Scholar