Phosphorylation of SOX9 by cyclic AMP-dependent protein kinase A enhances SOX9's ability to transactivate a Col2a1 chondrocyte-specific enhancer

Molecular and Cellular Biology

Volumn 20, Issue 11, 2000, Pages 4149-4158

  Huang, Wendong ^a   Zhou, Xin ^a   Lefebvre, Véronique ^a   De Crombrugghe, Benoit ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; PARATHYROID HORMONE RELATED PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CARTILAGE CELL; CELL DIFFERENTIATION; CELL STRAIN COS1; DNA LIBRARY; ENHANCER REGION; GENETIC TRANSFECTION; IMMUNOHISTOCHEMISTRY; MUTAGENESIS; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; TRANSACTIVATION; WESTERN BLOTTING; YEAST;

8-BROMO CYCLIC ADENOSINE MONOPHOSPHATE; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CHONDROCYTES; CHONDROSARCOMA; COLLAGEN; CONSENSUS SEQUENCE; COS CELLS; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DNA; ENHANCER ELEMENTS (GENETICS); ENZYME ACTIVATION; HIGH MOBILITY GROUP PROTEINS; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PHOSPHORYLATION; RATS; SACCHAROMYCES CEREVISIAE; SERINE; SUBCELLULAR FRACTIONS; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS; TUMOR CELLS, CULTURED; TWO-HYBRID SYSTEM TECHNIQUES;

ANIMALIA;

EID: 0034067651     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.11.4149-4158.2000     Document Type: Article

References (37)

1. Aronheim, A., E. Zandi, H. Hennemann, S. J. Elledge, and M. Karin. 1997. Isolation of an AP-1 repressor by a novel method for detecting protein-protein interaction. Mol. Cell. Biol. 17:3094-3102.
2. Bell, D. M., K. K. H. Leung, S. C. Whearley, L. J. Ng, S. Zhou, K. W. Ling, M. H. Sham, P. Koopman, P. P. L. Tam, and K. S. E. Cheah. 1997. Sox9 directly regulates the type-II collagen gene. Nat. Genet. 16:174-178.
3. Bi, W., J. Deng, Z. Zhang, R. R. Behringer, and B. de Crombrugghe. 1999. Sox9 is required for cartilage formation. Nat. Genet. 22:85-89.
4. Boulikas, T. 1995. Phosphorylation of transcription factors and control of the cell cycle. Crit. Rev. Eukaryot. Gene Expression 5:1-77.
5. Bridgewater, L. C., V. Lefebvre, and B. de Crombrugghe. 1998. Chondrocyte-specific enhancer elements in the Col11a2 gene resemble the Col2a1 tissue-specific enhancer. J. Biol. Chem. 273:14998-15006.
6. Desclozeaux, M., F. Poulat, P. de Santa Barbara, J. P. Capony, P. Turowski, P. Jay, C. Mejean, B. Moniot, B. Boizet, and P. Berta. 1998. Phosphorylation of an N-terminal motif enhances DNA-binding activity of the human SRY protein. J. Biol. Chem. 273:7988-7995.
7. Fan, C., J. A. Porter, C. Chiang, D. T. Chang, P. A. Beachy, and M. Tessier-Lavigne. 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.
8. Foster, J. W., M. A. Dominguez-Steglich, S. Guioli, C. Kwok, P. A. Weller, M. Stevanovic, J. Weissenbach, S. Mansour, I. D. Young, P. N. Goodfellow, J. D. Brook, and A. J. Schafer. 1994. Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature 372:525-530.
9. Hammerschmidt, M., M. J. Bitgood, and A. P. McMahon. 1996. Protein kinase A is a common negative regulator of hedgehog signaling in the vertebrate embryo. Genes Dev. 15:647-658.
10. Houston, C. S., J. M. Opitz, J. W. Spranger, R. I. Macpherson, M. H. Reed, E. F. Gilbert, J. Herrman, and A. Schinzel. 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.
11. Jüppner, H., A. Abou-Samra, M. Freeman, X. Kong, E. Schipani, J. Richards, L. F. Kolakowski, J. Hock, J. T. Potts, H. M. Kronenberg, and G. V. Segre. 1991. A G protein-linked receptor for parathyroid hormone and parathyroid hormone-related peptide. Science 254:1024-1026.
12. Kapaplis, A. C., A. Luz, J. Glowacki, R. T. Bronson, V. L. J. Tybulewicz, H. M. Kronenberg, and R. C. Mulligan. 1994. Lethal skeletal dysplasia from targeted disruption of the parathyroid hormone-related peptide gene. Genes Dev. 8:277-289.
13. Kent, J., S. C. Wheatley, J. E. Andrews, A. H. Sinclair, and P. Koopman. 1996. A male-specific role for SOX9 in vertebrate sex determination. Development 122:2813-2822.
14. Kosher, R. A., S. W. Gay, J. R. Kamanitz, W. M. Kulyk, B. J. Rodger, S. Sai, T. Tanaka, and M. L. Tanzer. 1986. Cartilage proteoglycan core protein gene expression during limb cartilage differentiation. Dev. Biol. 118:112-117.
15. Kwok, C., P. A. Weller, S. Guioli, J. W. Foster, S. Mansour, O. Zuffardi, H. H. Punett, M. A. Dominguez-Steglich, J. D. Brook, I. D. Young, P. N. Goodfellow, and A. J. Schafer. 1995. Mutations in SOX9, the gene responsible for campomelic dysplasia and autosomal sex reversal. Am. J. Hum. Genet. 57:1028-1036.
16. Lanske, B., A. C. Karaplis, K. Lee, A. Luz, A. Vortkamp, A. Pirro, M. Karperien, L. H. K. Defice, C. Ho, R. C. Mulligan, A. Alou-Samra, H. Juppner, G. V. Segre, and H. M. Kronenberg. 1996. PTH/PTHrP receptor in early development and indian-hedgehog-regulated bone growth. Science 273:663-666.
17. Lee, K., B. Lanske, A. C. Karaplis, J. D. Deeds, H. Kohno, R. A. Nissenson, H. M. Kronenberg, and G. V. Segre. 1996. Parathyroid hormone-related peptide delays terminal differentiation of chondrocytes during endochondral bone development. Endocrinology 137:5109-5118.
18. Lee, Y. S., and C. M. Chuong. 1997. Activation of protein kinase A is involved in both BMP-2- and cyclic AMP-induced chondrogenesis. J. Cell. Physiol. 170:153-165.
19. Lefebvre, V., and B. de Crombrugghe. 1998. Toward understanding SOX9 function in chondrocyte differentiation. Matrix Biol. 16:529-540.
20. Lefebvre, V., W. Huang, V. R. Harley, P. N. Goodfellow, and B. de Crombrugghe. 1997. SOX9 is a potent activator of the chondrocyte-specific enhancer of the proα1(II) collagen gene. Mol. Cell. Biol. 17:2336-2346.
21. Lefebvre, V., G. Zhou, K. Mukhopadhyay, C. N. Smith, Z. Zhang, H. Eberspaecher. X. Zhou, S. Sinha, S. N. Maity, and B. de Crombrugghe. 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.
22. Lefebvre, V., P. Li, and B. de Crombrugghe. 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.
23. Malemud, C. J., T. M. Mills, R. Shuckelt, and R. S. Papay. 1986. Stimulation of sulfated-proteoglycan synthesis by forskolin in monolayer cultures of rabbit articular chondrocytes. J. Cell. Physiol. 129:51-59.
24. Mansour, S., C. M. Hall, M. E. Pembrey, and I. D. Young. 1995. A clinical and genetic study of campomelic dysplasia. J. Med. Genet. 32:415-420.
25. Meyer, J., P. Südbeck, M. Held, T. Wagner, M. L. Schmitz, F. D. Bricarelli, E. Eggermont, U. Friedrich, O. A. Haas, A. Kobelt, J. G. Leroy, L. Van Maldergem, E. Michel, B. Mitulla, R. A. Pfeiffer, A. Schinzel, H. Schmidt, and G. Scherer. 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.
26. Morals da Silva, S., A. Hacker, V. Harley, P. Goodfellow, A. Swain, and R. Lovell-Badge. 1996. Sox9 expression during gonadal development implies a conserved role fur the gene in testis differentiation in mammals and birds. Nat. Genet. 13:62-68.
27. Ng, L.-J., S. Wheatley, G. E. O. Muscat, J. Conway-Campbell, J. Bowles, E. Wright, D. M. Bell, P. P. L. Tam, K. S. E. Cheah, and P. Koopman. 1997. Sox9 binds DNA, activates transcription, and coexpresses with type II collagen during chondrogenesis in the mouse. Dev. Biol. 183:108-121.
28. Rodgers, B. J., W. M. Kulyk, and R. A. Kosher. 1989. Stimulation of limb cartilage differentiation by cyclic AMP is dependent on cell density. Cell Differ. Dev. 28:179-187.
29. Schipani, E., B. Lanske, J. Hunzelman, A. Luz, C. S. Koracs, K. Lee, A. Pirro, H. M. Kronenberg, and H. Juppner. 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.
30. Sinha, S., S. N. Maity, J. Lu, and B. de Crombrugghe. 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.
31. Südbeck, P., L. Schmitz, P. A. Baeuerle, and G. Scherer. 1996. Sex reversal by loss of the C-terminal transactivation domain of human SOX9. Nat. Genet. 13:230-232.
32. Südbeck, P., and G. Scherer. 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.
33. Wagner, T., J. Wirth, J. Meyer, B. Zabel, M. Held, J. Zimmer, J. Pasantes, F. Dagna Bricarelli, J. Keutel, E. Mustert, U. Wolf, N. Tommerup, W. Schempp, and G. Scherer. 1994. Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 79:1111-1120.
34. Wirth, J., T. Wagner, J. Meyer, R. A. Pfeiffer, H.-U. Tietze, W. Schempp, and G. Scherer. 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.
35. Wright, E. M., B. Snopek, and P. Koopman. 1993. Seven new members of the SOX gene family expressed during mouse development. Nucleic Acids Res. 21:744.
36. Wright, E., M. R. Hargrave, J. Christiansen, L. Cooper, J. Kun, T. Evans, U. Gangadharan, A. Greenfield, and P. Koopman. 1995. The Sry-related gene Sox9 is expressed during chondrogenesis in mouse embryos. Nat. Genet. 9:15-20.
37. Zhao, Q., H. Eberspaecher, V. Lefebvre, and B. de Crombrugghe. 1997. Parallel expression of Sox9 and Col2a1 in cells undergoing chondrogenesis. Dev. Dyn. 209:377-386.