Evolutionarily Conserved, Growth Plate Zone-Specific Regulation of the Matrilin-1 Promoter: L-Sox5/Sox6 and Nfi Factors Bound near TATA Finely Tune Activation by Sox9

REFERENCES

• Akiyama, H. 2008. Control of chondrogenesis by the transcription factor Sox9. Mod. Rheumatol. 18:213–219.
   PubMed Web of Science ®Google Scholar
• Akiyama, H., M.-C. Chaboissier, J. F. Martin, A. Schedl, and B. de Crombrugghe. 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. 16:2813–2828.
   PubMed Web of Science ®Google Scholar
• Alevizopoulos, A., et al. 1995. A proline-rich TGF-β-responsive transcriptional activator interacts with histone H3. Genes Dev. 9:3051–3066.
   PubMedGoogle Scholar
• Aszódi, A., et al. 1996. Cloning, sequencing and expression analysis of mouse cartilage matrix protein cDNA. Eur. J. Biochem. 236:970–977.
   PubMedGoogle Scholar
• Aszódi, A., et al. 1994. The zonal expression of chicken cartilage matrix protein gene in the developing skeleton of transgenic mice. Matrix Biol. 14:181–190.
   PubMed Web of Science ®Google Scholar
• Barta, E., et al. 2005. DoOP: databases of orthologous promoters, collections of clusters of orthologous upstream sequences from chordates and plants. Nucleic Acids Res. 33:D86–D90.
   PubMedGoogle Scholar
• Bi, W., J. M. Deng, Z. Zhang, R. R. Behringer, and B. de Crombrugghe. 1999. Sox9 is required for cartilage formation. Nat. Genet. 22:85–89.
   PubMed Web of Science ®Google Scholar
• Cancedda, R., F. D. Cancedda, and P. Castagnola. 1995. Chondrocyte differentiation. Int. Rev. Cytol. 159:265–359.
   PubMed Web of Science ®Google Scholar
• Chaudhry, A. Z., A. D. Vitullo, and R. M. Gronostajski. 1998. Nuclear factor I (NFI) isoforms differentially activate simple versus complex NFI-responsive promoters. J. Biol. Chem. 273:18538–18546.
   PubMedGoogle Scholar
• Deák, F., R. Wagener, I. Kiss, and M. Paulsson. 1999. The matrilins: a novel family of oligomeric extracellular matrix proteins. Matrix Biol. 18:55–64.
   PubMedGoogle Scholar
• Goldring, M. B., K. Tsuchimochi, and K. Ijiri. 2006. The control of chondrogenesis. J. Cell. Biochem. 97:33–44.
   PubMed Web of Science ®Google Scholar
• Gronostajski, R. M. 2000. Roles of the NFI/CTF gene family in transcription and development. Gene 249:31–45.
   PubMed Web of Science ®Google Scholar
• Han, Y., and V. Lefebvre. 2008. L-Sox5 and Sox6 drive expression of the aggrecan gene in cartilage by securing binding of Sox9 to a far-upstream enhancer. Mol. Cell. Biol. 28:4999–5013.
   PubMed Web of Science ®Google Scholar
• Ikeda, T., et al. 2004. The combination of SOX5, SOX6, and SOX9 (the SOX trio) provides signals sufficient for induction of permanent cartilage. Arthritis Rheum. 50:3561–3573.
   PubMed Web of Science ®Google Scholar
• Imamura, T., C. Imamura, Y. Iwamoto, and L. J. Sandell. 2005. Transcriptional co-activators CREB-binding protein/p300 increase chondrocyte Cd-rap gene expression by multiple mechanisms including sequestration of the repressor CCAAT/enhancer-binding protein. J. Biol. Chem. 280:16625–16634.
   PubMed Web of Science ®Google Scholar
• Kálmán, J., et al. 2005. Gene expression profile analysis of lymphocytes from Alzheimer's patients. Psychiatr. Genet. 15:1–6.
   PubMed Web of Science ®Google Scholar
• Kamachi, Y., et al. 2009. Evolution of non-coding regulatory sequences involved in the developmental process: reflection of differential employment of paralogous genes as highlighted by Sox2 and group B1 Sox genes. Proc. Jpn. Acad. 85:55–68.
   Google Scholar
• Kamachi, Y., M. Uchikawa, and H. Kondoh. 2000. Pairing Sox off with partners in the regulation of embryonic development. Trends Genet. 16:182–187.
   PubMed Web of Science ®Google Scholar
• Karcagi, I., et al. 2004. Functional analysis of the regulatory regions of the matrilin-1 gene in transgenic mice reveals modular arrangement of tissue-specific control elements. Matrix Biol. 22:605–618.
   PubMedGoogle Scholar
• Karsenty, G., H. M. Kronenberg, and C. Settembre. 2009. Genetic control of bone formation. Annu. Rev. Cell Dev. Biol. 25:629–648.
   PubMed Web of Science ®Google Scholar
• Kiefer, J. C. 2007. Back to basics: Sox genes. Dev. Dyn. 236:2356–2366.
   PubMed Web of Science ®Google Scholar
• Kiss, I., et al. 1989. Structure of the gene for cartilage matrix protein, a modular protein of the extracellular matrix. J. Biol. Chem. 264:8126–8134.
   PubMed Web of Science ®Google Scholar
• Kou, I., and S. Ikegawa. 2004. SOX9-dependent and -independent transcriptional regulation of human cartilage link protein. J. Biol. Chem. 279:50942–50948.
   PubMed Web of Science ®Google Scholar
• Lefebvre, V., and P. Smits. 2005. Transcriptional control of chondrocyte fate and differentiation. Birth Defects Res. C Embryo Today 75:200–212.
   PubMedGoogle Scholar
• Lefebvre, V., B. Dumitriu, A. Penzo-Méndez, Y. Han, and B. Pallavi. 2007. Control of cell fate and differentiation by Sry-related high-mobility-group box (Sox) transcription factors. Int. J. Biochem. Cell Biol. 39:2195–2214.
   PubMed Web of Science ®Google Scholar
• Lefebvre, V., P. Li, and B. de Crombrugghe. 1998. A long new 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
• Liu, C., et al. 2007. Transcriptional activation of cartilage oligomeric matrix protein by Sox9, Sox5, and Sox6 transcription factors and CBP/p300 coactivators. Front. Biosci. 12:3899–3910.
   PubMedGoogle Scholar
• Liu, Y., H. Li, K. Tanaka, N. Tsumaki, and Y. Yamada. 2000. Identification of an enhancer sequence within the first intron required for cartilage-specific transcription of the α2(XI) collagen gene. J. Biol. Chem. 275:12712–12718.
   PubMedGoogle Scholar
• Mertin, S., S. G. McDowall, and V. R. Harley. 1999. The DNA-binding specificity of SOX9 and other SOX proteins. Nucleic Acids Res. 27:1359–1364.
   PubMed Web of Science ®Google Scholar
• Mundlos, S., and B. Zabel. 1994. Developmental expression of human cartilage matrix protein. Dev. Dyn. 199:241–252.
   PubMed Web of Science ®Google Scholar
• Muratoglu, S., et al. 1995. Expression of the cartilage matrix protein gene at different chondrocyte developmental stages. Eur. J. Cell Biol. 68:411–418.
   PubMedGoogle Scholar
• Pfeifer, G. P., H. H. Chen, J. Komura, and A. D. Riggs. 1999. Chromatin structure analysis by ligation-mediated and terminal transferase-mediated polymerase chain reaction. Methods Enzymol. 304:548–571.
   PubMed Web of Science ®Google Scholar
• Provot, S., and E. Schipani. 2005. Molecular mechanisms of endochondral bone development. Biochem. Biophys. Res. Commun. 328:658–665.
   PubMed Web of Science ®Google Scholar
• Rentsendorj, O., et al. 2005. Highly conserved proximal promoter element harbouring paired Sox9-binding sites contributes to the tissue- and developmental stage-specific activity of the matrilin-1 gene. Biochem. J. 389:705–716.
   PubMedGoogle Scholar
• Roulet, E., et al. 2000. Experimental analysis and computer prediction of CTF/NFI transcription factor DNA binding sites. J. Mol. Biol. 297:833–848.
   PubMed Web of Science ®Google Scholar
• Santoro, C., N. Mermod, P. C. Andrews, and R. Tjian. 1988. A family of human CAAT-box-binding proteins active in transcription and DNA replication: cloning and expression of multiple cDNAs. Nature 334:218–224.
   PubMedGoogle Scholar
• Shimizu, H., S. Yokoyama, and H. Asahara. 2007. Growth and differentiation of developing limb bud from perspective of chondrogenesis. Dev. Growth Differ. 49:449–454.
   PubMed Web of Science ®Google Scholar
• Smits, P., et al. 2001. The transcription factors L-Sox5 and Sox6 are essential for cartilage formation. Dev. Cell 1:277–290.
   PubMed Web of Science ®Google Scholar
• Stirpe, N. S., and P. F. Goetinck. 1989. Gene regulation during cartilage differentiation: temporal and spatial expression of link protein and cartilage matrix protein in developing limb. Development 107:23–33.
   PubMedGoogle Scholar
• Stolt, C. C., et al. 2006. SoxD proteins influence multiple stages of oligodendrocyte development and modulate SoxE protein function. Dev. Cell 11:697–709.
   PubMed Web of Science ®Google Scholar
• Szabó, P., et al. 1995. Identification of a nuclear factor-I family protein-binding site in the silencer region of the cartilage matrix protein gene. J. Biol. Chem. 270:10212–10221.
   PubMedGoogle Scholar
• Szüts, V., et al. 1998. Terminal differentiation of chondrocytes is arrested at distinct stages identified by their expression repertoire of marker genes. Matrix Biol. 17:435–448.
   PubMed Web of Science ®Google Scholar
• Uchihashi, T., et al. 2007. Involvement of nuclear factor I transcription/replication factor in the early stage of chondrogenic differentiation. Bone 41:1025–1035.
   PubMedGoogle Scholar
• Wagener, R., et al. 2005. The matrilins—adaptor proteins in the extracellular matrix. FEBS Lett. 579:3323–3329.
   PubMed Web of Science ®Google Scholar
• Wiberg, C., et al. 2003. Complexes of matrilin-1 and biglycan or decorin connect collagen VI mircofibrils to both collagen II and aggrecan. J. Biol. Chem. 278:37698–37704.
   PubMed Web of Science ®Google Scholar
• Zhang, P., S. A. Jimenez, and D. G. Stokes. 2003. Regulation of human COL9A1 gene expression. J. Biol. Chem. 278:117–123.
   PubMed Web of Science ®Google Scholar
• Zhou, G., et al. 1995. A 182 bp fragment of the mouse proα1(II) collagen gene is sufficient to direct chondrocyte expression in transgenic mice. J. Cell Sci. 108:3677–3684.
   PubMedGoogle Scholar
• Zhou, G., V. Lefebvre, Z. Zhang, H. Eberspaecher, and B. de Crombrugghe. 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.
   PubMed Web of Science ®Google Scholar