Regulation of Collagen Type I in Vascular Smooth Muscle Cells by Competition between Nkx2.5 and δEF1/ZEB1

REFERENCES

• Antoniv, T., De Val S., Wells D., Denton C. P., Rabe C., de Crombrugghe B., Ramirez F., and Bou-Gharios G.. 2001. Characterization of an evolutionarily conserved far-upstream enhancer in the human alpha 2(I) collagen (COL1A2) gene. J. Biol. Chem. 276:21754–21764.
   PubMedGoogle Scholar
• Bogdanovic, Z., Bedalov A., Krebsbach P. H., Pavlin D., Woody C. O., Clark S. H., Thomas H. F., Rowe D. W., Kream B. E., and Lichtler A. C.. 1994. Upstream regulatory elements necessary for expression of the rat COL1A1 promoter in transgenic mice. J. Bone Miner. Res. 9:285–292.
   PubMed Web of Science ®Google Scholar
• Bou-Gharios, G., Garrett L. A., Rossert J., Niederreither K., Eberspaecher H., Smith C., Black C., and Crombrugghe B.. 1996. A potent far-upstream enhancer in the mouse pro alpha 2(I) collagen gene regulates expression of reporter genes in transgenic mice. J. Cell Biol. 134:1333–1344.
   PubMedGoogle Scholar
• Brenner, D. A., Rippe R. A., and Veloz L.. 1989. Analysis of the collagen alpha 1(I) promoter. Nucleic Acids Res. 17:6055–6064.
   PubMed Web of Science ®Google Scholar
• Carson, J. A., Fillmore R. A., Schwartz R. J., and Zimmer W. E.. 2000. The smooth muscle gamma-actin gene promoter is a molecular target for the mouse bagpipe homologue, mNkx3-1, and serum response factor. J. Biol. Chem. 275:39061–39072.
   PubMedGoogle Scholar
• Chang, D. F., Belaguli N. S., Iyer D., Roberts W. B., Wu S. P., Dong X. R., Marx J. G., Moore M. S., Beckerle M. C., Majesky M. W., and Schwartz R. J.. 2003. Cysteine-rich LIM-only proteins CRP1 and CRP2 are potent smooth muscle differentiation cofactors. Dev. Cell 4:107–118.
   PubMed Web of Science ®Google Scholar
• Chen, C. Y., and Schwartz R. J.. 1995. Identification of novel DNA binding targets and regulatory domains of a murine tinman homeodomain factor, nkx-2.5. J. Biol. Chem. 270:15628–15633.
   PubMedGoogle Scholar
• Chomczynski, P., and Sacchi N.. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156–159.
   PubMed Web of Science ®Google Scholar
• Davis, D. L., Wessels A., and Burch J. B.. 2000. An Nkx-dependent enhancer regulates cGATA-6 gene expression during early stages of heart development. Dev. Biol. 217:310–322.
   PubMedGoogle Scholar
• De Val, S., Ponticos M., Antoniv T., Wells D., Abraham D., Partridge T., and Bou-Gharios G.. 2002. Identification of the key regions within the mouse pro a2(I) collagen gene far-upstream enhancer. J. Biol. Chem. 277:9286–9292.
   PubMedGoogle Scholar
• Durocher, D., Charron F., Warren R., Schwartz R. J., and Nemer M.. 1997. The cardiac transcription factors Nkx2-5 and GATA-4 are mutual cofactors. EMBO J. 16:5687–5696.
   PubMed Web of Science ®Google Scholar
• Geary, R. L., Wong J. M., Rossini A., Schwartz S. M., and Adams L. D.. 2002. Expression profiling identifies 147 genes contributing to a unique primate neointimal smooth muscle cell phenotype. Arterioscler. Thromb. Vasc. Biol. 22:2010–2016.
   PubMed Web of Science ®Google Scholar
• Hafizi, S. A. S. P., Goodwin A. T., Chester A. H., and Yacoub M. H.. 1999. Endothelin-1 stimulates proliferation of human coronary smooth muscle cells via the ETA receptor and is co-mitogenic with growth factors. Atherosclerosis 146:351–359.
   PubMedGoogle Scholar
• Harvey, R. P. 1996. NK-2 homeobox genes and heart development. Dev. Biol. 178:203–216.
   PubMed Web of Science ®Google Scholar
• Kim, S., Brown P. H., and Birrer M. J.. 1996. The inhibitory activity of a transdominant c-jun mutant fused to the ligand binding domain of the estrogen receptor. Oncogene 12:1043–1053.
   PubMedGoogle 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 pro alpha1(II) collagen gene. Mol. Cell. Biol. 17:2336–2346.
   PubMed Web of Science ®Google Scholar
• Libby, P., Ridker P. M., and Maseri A.. 2002. Inflammation and atherosclerosis. Circulation 105:1135–1143.
   PubMed Web of Science ®Google Scholar
• Liska, D. J., Reed M. J., Sage E. H., and Bornstein P.. 1994. Cell-specific expression of alpha 1(I) collagen-hGH minigenes in transgenic mice. J. Cell Biol. 125:695–704.
   PubMed Web of Science ®Google Scholar
• Murray, D., Precht P., Balakir R., and Horton W. E., Jr. 2000. The transcription factor δEF1 is inversely expressed with type II collagen mRNA and can repress Col2a1 promoter activity in transfected chondrocytes. J. Biol. Chem. 275:3610–3618.
   PubMed Web of Science ®Google Scholar
• Myllyharju, J., and Kivirikko K. I.. 2001. Collagens and collagen-related diseases. Ann. Med. 33:7–21.
   PubMed Web of Science ®Google Scholar
• Niederreither, K., D'Souza R., Metsaranta M., Eberspaecher H., Toman P. D., Vuorio E., and de Crombrugghe B.. 1995. Coordinate patterns of expression of type I and III collagens during mouse development. Matrix Biol. 14:705–713.
   PubMedGoogle Scholar
• Nishida, W., Nakamura M., Mori S., Takahashi M., Ohkawa Y., Tadokoro S., Yoshida K., Hiwada K., Hayashi K., and Sobue K.. 2002. A triad of serum response factor and the GATA and NK families governs the transcription of smooth and cardiac muscle genes. J. Biol. Chem. 277:7308–7317.
   PubMed Web of Science ®Google Scholar
• Pavlin, D., Lichtler A. C., Bedalov A., Kream B. E., Harrison J. R., Thomas H. F., Gronowicz G. A., Clark S. H., Woody C. O., and Rowe D. W.. 1992. Differential utilization of regulatory domains within the alpha 1(I) collagen promoter in osseous and fibroblastic cells. J. Cell Biol. 116:227–236.
   PubMed Web of Science ®Google Scholar
• Plenz, G. A., Deng M. C., Robenek H., and Volker W.. 2003. Vascular collagens: spotlight on the role of type VIII collagen in atherogenesis. Atherosclerosis 166:1–11.
   PubMedGoogle Scholar
• Postigo, A. A. 2003. Opposing functions of ZEB proteins in the regulation of the TGFβ/BMP signaling pathway. EMBO J. 22:2443–2452.
   PubMedGoogle Scholar
• Postigo, A. A., and Dean D. C.. 1999. ZEB represses transcription through interaction with the corepressor CtBP. Proc. Natl. Acad. Sci. USA 96:6683–6688.
   PubMedGoogle Scholar
• Quandt, K., Frech K., Karas H., Wingender E., and Werner T.. 1995. MatInd and MatInspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucleic Acids Res. 23:4878–4884.
   PubMed Web of Science ®Google Scholar
• Remacle, J. E., Kraft H., Lerchner W., Wuytens G., Collart C., Verschueren K., Smith J. C., and Huylebroeck D.. 1999. New mode of DNA binding of multi-zinc finger transcription factors: δEF1 family members bind with two hands to two target sites. EMBO J. 18:5073–5084.
   PubMedGoogle Scholar
• Ross, R. 1999. Atherosclerosis—an inflammatory disease. N. Engl. J. Med. 340:115–126.
   PubMed Web of Science ®Google Scholar
• Rossert, J., Eberspaecher H., and de Crombrugghe B.. 1995. Separate cis-acting DNA elements of the mouse pro-alpha 1(I) collagen promoter direct expression of reporter genes to different type I collagen-producing cells in transgenic mice. J. Cell Biol. 129:1421–1432.
   PubMed Web of Science ®Google Scholar
• Rossert, J. A., Chen S. S., Eberspaecher H., Smith C. N., and de Crombrugghe B.. 1996. Identification of a minimal sequence of the mouse pro-alpha 1(I) collagen promoter that confers high-level osteoblast expression in transgenic mice and that binds a protein selectively present in osteoblasts. Proc. Natl. Acad. Sci. USA 93:1027–1031.
   PubMed Web of Science ®Google Scholar
• Schwartz, R. J., and Olson E. N.. 1999. Building the heart piece by piece: modularity of cis-elements regulating Nkx2-5 transcription. Development 126:4187–4192.
   PubMedGoogle Scholar
• Sekido, R., Murai K., Kamachi Y., and Kondoh H.. 1997. Two mechanisms in the action of repressor δEF1: binding site competition with an activator and active repression. Genes Cells 2:771–783.
   PubMedGoogle Scholar
• Sekido, R., Takagi T., Okanami M., Moribe H., Yamamura M., Higashi Y., and Kondoh H.. 1996. Organization of the gene encoding transcriptional repressor δEF1 and cross-species conservation of its domains. Gene 173:227–232.
   PubMedGoogle Scholar
• Slack, J. L., Liska D. J., and Bornstein P.. 1991. An upstream regulatory region mediates high-level, tissue-specific expression of the human alpha 1(I) collagen gene in transgenic mice. Mol. Cell. Biol. 11:2066–2074.
   PubMed Web of Science ®Google Scholar
• Sooy, K., and Demay M. B.. 2002. Transcriptional repression of the rat osteocalcin gene by δEF1. Endocrinology 143:3370–3375.
   PubMedGoogle Scholar
• Stary, H. C., Blankenhorn D. H., Chandler A. B., Glagov S., Insull W., Jr., Richardson M., Rosenfeld M. E., Schaffer S. A., Schwartz C. J., Wagner W. D., et al. 1992. A definition of the intima of human arteries and of its atherosclerosis-prone regions. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Arterioscler. Thromb. 12:120–134.
   PubMed Web of Science ®Google Scholar
• Suzuki, E., Evans T., Lowry J., Truong L., Bell D. W., Testa J. R., and Walsh K.. 1996. The human GATA-6 gene: structure, chromosomal location, and regulation of expression by tissue-specific and mitogen-responsive signals. Genomics 38:283–290.
   PubMed Web of Science ®Google Scholar
• Suzuki, Y. J., Day R. M., Tan C. C., Sandven T. H., Liang Q., Molkentin J. D., and Fanburg B. L.. 2003. Activation of GATA-4 by serotonin in pulmonary artery smooth muscle cells. J. Biol. Chem. 278:17525–17531.
   PubMedGoogle Scholar
• Tanaka, K., Tsumaki N., Kozak C. A., Matsumoto Y., Nakatani F., Iwamoto Y., and Yamada Y.. 2002. A Kruppel-associated box-zinc finger protein, NT2, represses cell-type-specific promoter activity of the α2(XI) collagen gene. Mol. Cell. Biol. 22:4256–4267.
   PubMedGoogle Scholar
• Tanaka, M., Chen Z., Bartunkova S., Yamasaki N., and Izumo S.. 1999. The cardiac homeobox gene Csx/Nkx2.5 lies genetically upstream of multiple genes essential for heart development. Development 126:1269–1280.
   PubMed Web of Science ®Google Scholar
• Tanaka, M., Lyons G. E., and Izumo S.. 1999. Expression of the Nkx3.1 homeobox gene during pre- and postnatal development. Mech. Dev. 85:179–182.
   PubMedGoogle Scholar
• Terraz, C., Brideau G., Ronco P., and Rossert J.. 2002. A combination of cis-acting elements is required to activate the pro-alpha 1(I) collagen promoter in tendon fibroblasts of transgenic mice. J. Biol. Chem. 277:19019–19026.
   PubMedGoogle Scholar
• Terraz, C., Toman D., Delauche M., Ronco P., and Rossert J.. 2001. δEf1 binds to a far upstream sequence of the mouse pro-alpha 1(I) collagen gene and represses its expression in osteoblasts. J. Biol. Chem. 276:37011–37019.
   PubMedGoogle Scholar
• Virmani, R., Kolodgie F. D., Burke A. P., Farb A., and Schwartz S. M.. 2000. Lessons from sudden coronary death: a comprehensive morphological classification scheme for atherosclerotic lesions. Arterioscler. Thromb. Vasc. Biol. 20:1262–1275.
   PubMed Web of Science ®Google Scholar
• Vuust, J., Sobel M. E., and Martin G. R.. 1985. Regulation of type I collagen synthesis. Total pro alpha 1(I) and pro alpha 2(I) mRNAs are maintained in a 2:1 ratio under varying rates of collagen synthesis. Eur. J. Biochem. 151:449–453.
   PubMedGoogle Scholar
• Yang, G. H., and Pestka J. J.. 2002. Vomitoxin (deoxynivalenol)-mediated inhibition of nuclear protein binding to NRE-A, an IL-2 promoter negative regulatory element, in EL-4 cells. Toxicology 172:169–179.
   PubMedGoogle Scholar
• Zilberman, A., Dave V., Miano J., Olson E. N., and Periasamy M.. 1998. Evolutionarily conserved promoter region containing CArG*-like elements is crucial for smooth muscle myosin heavy chain gene expression. Circ. Res. 82:566–575.
   PubMedGoogle Scholar