Runx2 Represses Myocardin-Mediated Differentiation and Facilitates Osteogenic Conversion of Vascular Smooth Muscle Cells

REFERENCES

• Aronson, B. D., A. L. Fisher, K. Blechman, M. Caudy, and J. P. Gergen. 1997. Groucho-dependent and -independent repression activities of Runt domain proteins. Mol. Cell. Biol. 17:5581–5587.
   PubMed Web of Science ®Google Scholar
• Brunelli, S., E. Tagliafico, F. G. De Angelis, R. Tonlorenzi, S. Baesso, S. Ferrari, M. Niinobe, K. Yoshikawa, R. J. Schwartz, I. Bozzoni, S. Ferrari, and G. Cossu. 2004. Msx2 and necdin combined activities are required for smooth muscle differentiation in mesoangioblast stem cells. Circ. Res. 94:1571–1578.
   PubMedGoogle Scholar
• Cao, D., Z. Wang, C. L. Zhang, J. Oh, W. Xing, S. Li, J. A. Richardson, D. Z. Wang, and E. N. Olson. 2005. Modulation of smooth muscle gene expression by association of histone acetyltransferases and deacetylases with myocardin. Mol. Cell. Biol. 25:364–376.
   PubMedGoogle Scholar
• Cheng, S. L., J. S. Shao, N. Charlton-Kachigian, A. P. Loewy, and D. A. Towler. 2003. MSX2 promotes osteogenesis and suppresses adipogenic differentiation of multipotent mesenchymal progenitors. J. Biol. Chem. 278:45969–45977.
   PubMed Web of Science ®Google Scholar
• Diamond, M. I., J. N. Miner, S. K. Yoshinaga, and K. R. Yamamoto. 1990. Transcription factor interactions: selectors of positive or negative regulation from a single DNA element. Science 249:1266–1272.
   PubMed Web of Science ®Google Scholar
• Doi, H., T. Iso, H. Sato, M. Yamazaki, H. Matsui, T. Tanaka, I. Manabe, M. Arai, R. Nagai, and M. Kurabayashi. 2006. Jagged1-selective Notch signaling induces smooth muscle differentiation via a RBP-Jκ-dependent pathway. J. Biol. Chem. 281:28555–28564.
   PubMedGoogle Scholar
• Doi, H., T. Iso, M. Yamazaki, H. Akiyama, H. Kanai, H. Sato, K. Kawai-Kowase, T. Tanaka, T. Maeno, E. Okamoto, M. Arai, L. Kedes, and M. Kurabayashi. 2005. HERP1 inhibits myocardin-induced vascular smooth muscle cell differentiation by interfering with SRF binding to CArG box. Arterioscler. Thromb. Vasc. Biol. 25:2328–2334.
   PubMedGoogle Scholar
• Ducy, P., R. Zhang, V. Geoffroy, A. L. Ridall, and G. Karsenty. 1997. Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 89:747–754.
   PubMed Web of Science ®Google Scholar
• Enomoto, H., T. Furuichi, A. Zanma, K. Yamana, C. Yoshida, S. Sumitani, H. Yamamoto, M. Enomoto-Iwamoto, M. Iwamoto, and T. Komori. 2004. Runx2 deficiency in chondrocytes causes adipogenic changes in vitro. J. Cell Sci. 117:417–425.
   PubMed Web of Science ®Google Scholar
• Garg, V., A. N. Muth, J. F. Ransom, M. K. Schluterman, R. Barnes, I. N. King, P. D. Grossfeld, and D. Srivastava. 2005. Mutations in NOTCH1 cause aortic valve disease. Nature 437:270–274.
   PubMed Web of Science ®Google Scholar
• Gersbach, C. A., B. A. Byers, G. K. Pavlath, and A. J. Garcia. 2004. Runx2/Cbfa1 stimulates transdifferentiation of primary skeletal myoblasts into a mineralizing osteoblastic phenotype. Exp. Cell Res. 300:406–417.
   PubMedGoogle Scholar
• Giachelli, C. M. 2004. Vascular calcification mechanisms. J. Am. Soc. Nephrol. 15:2959–2964.
   PubMed Web of Science ®Google Scholar
• Gori, F., T. Thomas, K. C. Hicok, T. C. Spelsberg, and B. L. Riggs. 1999. Differentiation of human marrow stromal precursor cells: bone morphogenetic protein-2 increases OSF2/CBFA1, enhances osteoblast commitment, and inhibits late adipocyte maturation. J. Bone Miner. Res. 14:1522–1535.
   PubMed Web of Science ®Google Scholar
• Gunther, T., C. Poli, J. M. Muller, P. Catala-Lehnen, T. Schinke, N. Yin, S. Vomstein, M. Amling, and R. Schule. 2005. Fhl2 deficiency results in osteopenia due to decreased activity of osteoblasts. EMBO J. 24:3049–3056.
   PubMedGoogle Scholar
• Hata, K., R. Nishimura, M. Ueda, F. Ikeda, T. Matsubara, F. Ichida, K. Hisada, T. Nokubi, A. Yamaguchi, and T. Yoneda. 2005. A CCAAT/enhancer binding protein beta isoform, liver-enriched inhibitory protein, regulates commitment of osteoblasts and adipocytes. Mol. Cell. Biol. 25:1971–1979.
   PubMedGoogle Scholar
• Hayashi, K., S. Nakamura, W. Nishida, and K. Sobue. 2006. Bone morphogenetic protein-induced Msx1 and Msx2 inhibit myocardin-dependent smooth muscle gene transcription. Mol. Cell. Biol. 26:9456–9470.
   PubMed Web of Science ®Google Scholar
• Hong, J. H., E. S. Hwang, M. T. McManus, A. Amsterdam, Y. Tian, R. Kalmukova, E. Mueller, T. Benjamin, B. M. Spiegelman, P. A. Sharp, N. Hopkins, and M. B. Yaffe. 2005. TAZ, a transcriptional modulator of mesenchymal stem cell differentiation. Science 309:1074–1078.
   PubMed Web of Science ®Google Scholar
• Hruska, K. A., S. Mathew, and G. Saab. 2005. Bone morphogenetic proteins in vascular calcification. Circ. Res. 97:105–114.
   PubMed Web of Science ®Google Scholar
• Jiang, H., F. Zhang, T. Kurosu, and B. M. Peterlin. 2005. Runx1 binds positive transcription elongation factor b and represses transcriptional elongation by RNA polymerase II: possible mechanism of CD4 silencing. Mol. Cell. Biol. 25:10675–10683.
   PubMedGoogle Scholar
• Kim, B. G., H. J. Kim, H. J. Park, Y. J. Kim, W. J. Yoon, S. J. Lee, H. M. Ryoo, and J. Y. Cho. 2006. Runx2 phosphorylation induced by fibroblast growth factor-2/protein kinase C pathways. Proteomics 6:1166–1174.
   PubMed Web of Science ®Google Scholar
• Komori, T., H. Yagi, S. Nomura, A. Yamaguchi, K. Sasaki, K. Deguchi, Y. Shimizu, R. T. Bronson, Y. H. Gao, M. Inada, M. Sato, R. Okamoto, Y. Kitamura, S. Yoshiki, and T. Kishimoto. 1997. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89:755–764.
   PubMed Web of Science ®Google Scholar
• Lee, B., K. Thirunavukkarasu, L. Zhou, L. Pastore, A. Baldini, J. Hecht, V. Geoffroy, P. Ducy, and G. Karsenty. 1997. Missense mutations abolishing DNA binding of the osteoblast-specific transcription factor OSF2/CBFA1 in cleidocranial dysplasia. Nat. Genet. 16:307–310.
   PubMed Web of Science ®Google Scholar
• Lee, K. S., H. J. Kim, Q. L. Li, X. Z. Chi, C. Ueta, T. Komori, J. M. Wozney, E. G. Kim, J. Y. Choi, H. M. Ryoo, and S. C. Bae. 2000. Runx2 is a common target of transforming growth factor beta1 and bone morphogenetic protein 2, and cooperation between Runx2 and Smad5 induces osteoblast-specific gene expression in the pluripotent mesenchymal precursor cell line C2C12. Mol. Cell. Biol. 20:8783–8792.
   PubMed Web of Science ®Google Scholar
• Levanon, D., V. Negreanu, Y. Bernstein, I. Bar-Am., L. Avivi, and Y. Groner. 1994. AML1, AML2, and AML3, the human members of the runt domain gene-family: cDNA structure, expression, and chromosomal localization. Genomics 23:425–432.
   PubMed Web of Science ®Google Scholar
• Liu, Y., S. Sinha, O. G. McDonald, Y. Shang, M. H. Hoofnagle, and G. K. Owens. 2005. Kruppel-like factor 4 abrogates myocardin-induced activation of smooth muscle gene expression. J. Biol. Chem. 280:9719–9727.
   PubMedGoogle Scholar
• Liu, Z. P., Z. Wang, H. Yanagisawa, and E. N. Olson. 2005. Phenotypic modulation of smooth muscle cells through interaction of Foxo4 and myocardin. Dev. Cell 9:261–270.
   PubMed Web of Science ®Google Scholar
• Miano, J. M. 2003. Serum response factor: toggling between disparate programs of gene expression. J. Mol. Cell Cardiol. 35:577–593.
   PubMed Web of Science ®Google Scholar
• Mundlos, S., F. Otto, C. Mundlos, J. B. Mulliken, A. S. Aylsworth, S. Albright, D. Lindhout, W. G. Cole, W. Henn, J. H. Knoll, M. J. Owen, R. Mertelsmann, B. U. Zabel, and B. R. Olsen. 1997. Mutations involving the transcription factor CBFA1 cause cleidocranial dysplasia. Cell 89:773–779.
   PubMed Web of Science ®Google Scholar
• Otto, F., A. P. Thornell, T. Crompton, A. Denzel, K. C. Gilmour, I. R. Rosewell, G. W. Stamp, R. S. Beddington, S. Mundlos, B. R. Olsen, P. B. Selby, and M. J. Owen. 1997. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 89:765–771.
   PubMed Web of Science ®Google Scholar
• Owens, G. K., M. S. Kumar, and B. R. Wamhoff. 2004. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev. 84:767–801.
   PubMed Web of Science ®Google Scholar
• Philippar, U., G. Schratt, C. Dieterich, J. M. Muller, P. Galgoczy, F. B. Engel, M. T. Keating, F. Gertler, R. Schule, M. Vingron, and A. Nordheim. 2004. The SRF target gene Fhl2 antagonizes RhoA/MAL-dependent activation of SRF. Mol. Cell 16:867–880.
   PubMedGoogle Scholar
• Pipes, G. C., E. E. Creemers, and E. N. Olson. 2006. The myocardin family of transcriptional coactivators: versatile regulators of cell growth, migration, and myogenesis. Genes Dev. 20:1545–1556.
   PubMed Web of Science ®Google Scholar
• Sakata, Y., F. Xiang, Z. Chen, Y. Kiriyama, C. N. Kamei, D. I. Simon, and M. T. Chin. 2004. Transcription factor CHF1/Hey2 regulates neointimal formation in vivo and vascular smooth muscle proliferation and migration in vitro. Arterioscler. Thromb. Vasc. Biol. 24:2069–2074.
   PubMedGoogle Scholar
• Schroeder, T. M., R. A. Kahler, X. Li, and J. J. Westendorf. 2004. Histone deacetylase 3 interacts with runx2 to repress the osteocalcin promoter and regulate osteoblast differentiation. J. Biol. Chem. 279:41998–42007.
   PubMed Web of Science ®Google Scholar
• Shao, J. S., J. Cai, and D. A. Towler. 2006. Molecular mechanisms of vascular calcification: lessons learned from the aorta. Arterioscler. Thromb. Vasc. Biol. 26:1423–1430.
   PubMed Web of Science ®Google Scholar
• Steitz, S. A., M. Y. Speer, G. Curinga, H. Y. Yang, P. Haynes, R. Aebersold, T. Schinke, G. Karsenty, and C. M. Giachelli. 2001. Smooth muscle cell phenotypic transition associated with calcification: upregulation of Cbfa1 and downregulation of smooth muscle lineage markers. Circ. Res. 89:1147–1154.
   PubMed Web of Science ®Google Scholar
• Tanaka, T., H. Kanai, K. Sekiguchi, Y. Aihara, T. Yokoyama, M. Arai, T. Kanda, R. Nagai, and M. Kurabayashi. 2000. Induction of VEGF gene transcription by IL-1 beta is mediated through stress-activated MAP kinases and Sp1 sites in cardiac myocytes. J. Mol. Cell Cardiol. 32:1955–1967.
   PubMedGoogle Scholar
• Tanaka, T., D. Nishimura, R. C. Wu, M. Amano, T. Iso, L. Kedes, H. Nishida, K. Kaibuchi, and Y. Hamamori. 2006. Nuclear Rho kinase, ROCK2, targets p300 acetyltransferase. J. Biol. Chem. 281:15320–15329.
   PubMed Web of Science ®Google Scholar
• Thirunavukkarasu, K., D. L. Halladay, R. R. Miles, X. Yang, R. J. Galvin, S. Chandrasekhar, T. J. Martin, and J. E. Onyia. 2000. The osteoblast-specific transcription factor Cbfa1 contributes to the expression of osteoprotegerin, a potent inhibitor of osteoclast differentiation and function. J. Biol. Chem. 275:25163–25172.
   PubMed Web of Science ®Google Scholar
• Tyson, K. L., J. L. Reynolds, R. McNair, Q. Zhang, P. L. Weissberg, and C. M. Shanahan. 2003. Osteo/chondrocytic transcription factors and their target genes exhibit distinct patterns of expression in human arterial calcification. Arterioscler. Thromb. Vasc. Biol. 23:489–494.
   PubMed Web of Science ®Google Scholar
• Vega, R. B., K. Matsuda, J. Oh, A. C. Barbosa, X. Yang, E. Meadows, J. McAnally, C. Pomajzl, J. M. Shelton, J. A. Richardson, G. Karsenty, and E. N. Olson. 2004. Histone deacetylase 4 controls chondrocyte hypertrophy during skeletogenesis. Cell 119:555–566.
   PubMed Web of Science ®Google Scholar
• Wang, D., P. S. Chang, Z. Wang, L. Sutherland, J. A. Richardson, E. Small, P. A. Krieg, and E. N. Olson. 2001. Activation of cardiac gene expression by myocardin, a transcriptional cofactor for serum response factor. Cell 105:851–862.
   PubMed Web of Science ®Google Scholar
• Westendorf, J. J. 2006. Transcriptional co-repressors of Runx2. J. Cell Biochem. 98:54–64.
   PubMedGoogle Scholar
• Westendorf, J. J., S. K. Zaidi, J. E. Cascino, R. Kahler, A. J. van Wijnen, J. B. Lian, M. Yoshida, G. S. Stein, and X. Li. 2002. Runx2 (Cbfa1, AML-3) interacts with histone deacetylase 6 and represses the p21(CIP1/WAF1) promoter. Mol. Cell. Biol. 22:7982–7992.
   PubMed Web of Science ®Google Scholar
• Xiao, G., D. Jiang, R. Gopalakrishnan, and R. T. Franceschi. 2002. Fibroblast growth factor 2 induction of the osteocalcin gene requires MAPK activity and phosphorylation of the osteoblast transcription factor, Cbfa1/Runx2. J. Biol. Chem. 277:36181–36187.
   PubMed Web of Science ®Google Scholar
• Zhou, Y. X., X. Xu, L. Chen, C. Li, S. G. Brodie, and C. X. Deng. 2000. A Pro250Arg substitution in mouse Fgfr1 causes increased expression of Cbfa1 and premature fusion of calvarial sutures. Hum. Mol. Genet. 9:2001–2008.
   PubMed Web of Science ®Google Scholar