Role of c-fos and E2F in the induction of cyclin A transcription and vascular smooth muscle cell proliferation

Journal of Clinical Investigation

Volumn 101, Issue 5, 1998, Pages 940-948

  Sylvester, Amy M ^a   Chen, Dongfen ^a   Krasinski, Kevin ^a   Andrés, Vicente ^a,b,c  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUTO DE BIOMEDICINA DE VALENCIA   (Spain)

^c ST ELIZABETH'S MEDICAL CENTER   (United States)

Author keywords

C fos; Cyclin A; E2F; Ras; Vascular smooth muscle cell proliferation

Indexed keywords

CYCLIN A; PROTEIN C FOS; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR E2F;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYCLIC AMP RESPONSIVE ELEMENT; DNA REPLICATION; MALE; NONHUMAN; PERCUTANEOUS TRANSLUMINAL ANGIOPLASTY; PRIORITY JOURNAL; PROMOTER REGION; RAT; TRANSCRIPTION REGULATION; VASCULAR SMOOTH MUSCLE;

EID: 0032031659     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI1630     Document Type: Article

References (76)

1. Owens, G.K. 1995. Regulation of differentiation of vascular smooth muscle cells. Physiol. Rev. 75:487-517.
2. Ross, R. 1993. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 362:801-809.
3. Fuster, V., L. Badimón, J.J. Badimón, and J.H. Chesebro. 1992. The pathogenesis of coronary artery disease and the acute coronary syndromes. N. Engl. J. Med. 236:242-250.
4. Hegele, R.A. 1996. The pathogenesis of atherosclerosis, Clin. Chim. Acta. 246:21-38.
5. Libby, P., D. Schwartz, E. Brogi, H. Tanaka, and S.K. Clinton. 1992. A cascade model for restenosis: a special case of atherosclerosis progression. Circulation. 86(6 Suppl.):III47-III52.
6. Leimgruber, P.P., G.S. Roubin, J. Hollman, G.A. Cotsonis, B. Meier, J.S. Douglas, S.B. King, and A.R. Gruentzig. 1986. Restenosis after successful coronary angioplasty in patients with single-vessel disease. Circulation. 73:710-717.
7. Nobuyoshi, M., T. Kimura, H. Nosaka, S. Mioka, K. Ueno, H. Yokoi, N. Hamasaki, H. Horiuchi, and H. Ohishi. 1988. Restenosis after successful percutaneous transluminal coronary angioplasty: serial angiographie follow-up of 229 patients. J. Am. Coll. Cardiol. 12:616-623.
8. 1993. Coronary angioplasty versus coronary artery bypass surgery: the Randomized Intervention Treatment of Angina (RITA) trial. Lancet. 341:573-580.
9. Kip1. an inhibitor of neointima formation in the rat carotid artery. J. Clin. Invest. 99:2334-2341.
10. CIP1-mediated inhibition of cell proliferation by overexpression of the Gax homeodomain gene. Genes Dev. 11:1674-1689.
11. Chang, M.W., E. Barr, J. Seltzer, Y. Jiang, G.J. Nabel, E.G. Nabel, M.S. Parmacek, and J.M. Leiden. 1995. Cytostatic gene therapy for vascular proliferative disorders with a constitutively active form of the retinoblastoma gene product. Science. 267:518-522.
12. Chang, M.W., E. Barr, M.M. Lu, K. Barton, and J.M. Leiden. 1995. Adenovirus-mediated over-expression of the cyclin/cyclin-dependent kinase inhibitor, p21 inhibits vascular smooth muscle cell proliferation and neointima formation in the rat carotid artery model of balloon angioplasty. J. Clin. Invest. 96: 2260-2268.
13. Lindner, V., and M.A. Reidy. 1991. Proliferation of smooth muscle cells after vascular injury is inhibited by an antibody against basic fibroblast growth factor. Proc. Natl. Acad. Sci. USA. 88:3739-3743.
14. Abe, J., W. Zhou, J. Taguchi, N. Takuwa,. K. Miki, H. Okazaki, K. Kurokawa, M. Kumada, and Y. Takuwa. 1994. Suppression of neointimal smooth muscle cell accumulation in vivo by antisense cdc2 and cdk2 oligonucleotides in rat carotid artery. Biochem. Biophys. Res. Commun. 198:16-24.
15. Bennett, M.R., S. Anglin, J.R. McEwan, R. Jagoe, A.C. Newby, and G.I. Evan. 1994. Inhibition of vascular smooth muscle cell proliferation in vitro and in vivo by c-myc antisense oligodeoxynucleotides. J. Clin. Invest. 93:820-828.
16. Morishita, R., G.H. Gibbons, K.E. Ellison, M. Nakajima, L. Zhang, Y. Kaneda, T. Ogihara, and V.J. Dzau. 1993. Single intraluminal delivery of antisense cdc2 kinase and proliferating-cell nuclear antigen oligonucleotides results in chronic inhibition of neointimal hyperplasia. Proc. Natl. Acad. Sci. USA. 90: 8474-8478.
17. Morishita, R., G.H. Gibbons, K.E. Ellison, M. Nakajima, H. von der Leyen, L. Zhang, Y. Kaneda, T. Ogihara, and V.J. Dzau. 1994. Intimal hyperplasia after vascular injury is inhibited by antisense cdk 2 kinase oligonucleotides. J. Clin. Invest. 93:1458-1464.
18. Morishita, R., G.H. Gibbons, Y. Kaneda, T. Ogihara, and V.J. Dzau. 1994. Pharmacokinetics of antisense oligodeoxyribonucleotides (cyclin B1 and CDC 2 kinase) in the vessel wall in vivo: enhanced therapeutic utility for restenosis by HVJ-liposome delivery. Gene (Amst.). 149:13-19.
19. Nabel, E.G., Z. Yang, S. Liptay, H. San, D. Gordon, C.C. Haudenschild, and G.J. Nabel. 1993. Recombinant platelet-derived growth factor B gene expression in porcine arteries induces intimal hyperplasia in vivo. J. Clin. Invest. 91:1822-1829.
20. Nabel, E.G., Z. Yang, G. Plautz, R. Forough, X. Zhan, C.C. Haudenschild, T. Maciag, and G.J. Nabel. 1993. Recombinant fibroblast growth factor-1 promotes intimal hyperplasia and angiogenesis in arteries in vivo. Nature. 362: 844-846.
21. Shi, Y., A. Fard, A. Galeo, H.G. Hutchinson, P. Vermani, G.R. Dodge, D.J. Hall, F. Shaheen, and A. Zalewski. 1994. Transcatheter delivery of c-myc antisense oligomers reduces neointimal formation in a porcine model of coronary artery ballooon injury. Circulation. 90:944-951.
22. Simons, M., E.R. Edelman, J.-L. DeKeyser, R. Langer, and R.D. Rosenberg. 1992. Anlisense c-myb oligonucleotides inhibit intimal arterial smooth muscle cell accumulation in vivo. Nature. 359:67-70.
23. Yang, Z.-Y., R.D. Simari, N.D. Perkins, H. San, D. Gordon, G.J. Nabel, and E.G. Nabel. 1996. Role of p21 cydin-dependent kinase inhibitor in limiting intimal cell proliferation in response to arterial injury. Proc. Natl. Acad. Sci. USA. 93:7905-7910.
24. Zhu, N.L., L. Wu, P.X. Liu, E.M. Gordon, W.F. Anderson, V.A. Starnes, and F.L. Hall. 1997. Downregulation of cyclin G1 expression by retrovirus-mediated antisense gene transfer inhibits vascular smooth muscle cell proliferation and neointima formation. Circulation. 96:628-635.
25. Ueno, H., S. Masuda, S. Nishio, J.J. Li, H. Yamamoto, and A. Takeshita. , 1997. Adenovirus-mediated transfer of cyclin-dependent kinase inhibitor-p21 suppresses neointimal formation in the balloon-injured rat carotid arteries in vivo. Ann. NY Acad. Sci. 811:401-411.
26. Morishita, R., G.H. Gibbons, M. Horiuchi, K.E. Ellison, M. Nakajima, L. Zhang, Y. Kaneda, T. Ogihara, and V.J. Dzau. 1995. A gene therapy strategy using a transcription factor decoy of the E2F binding site inhibits smooth muscle cell proliferation in vivo. Proc. Natl. Acad. Sci. USA. 92:5855-5859.
27. Smith, R.C., K.N. Wills, D. Antelman, H. Perlman, L.N. Truong, K. Krasinski, and K. Walsh. 1997. Adenoviral constructs encoding phosphorylation-competent full-length and truncated forms of the human retinoblastoma protein inhibit myocyte proliferation and neointima formation. Circulation. 96: 1899-1905.
28. Pardee, A.B. 1989. G1 events and regulation of cell proliferation. Science: 246:603-608.
29. Zhu, L., G.H. Enders, C.L. Wu, M. A. Starz, K.H. Moberg, J.A. Lees, N. Dyson, and E. Harlow. 1994. Growth suppression by members of the retinoblastoma protein family. Cold Spring Harbor Symp. Quant. Biol. 59:75-84.
30. Sherr, C.J. 1996. Cancer cell cycles. Science. 274:1672-1677.
31. Weinberg, R.A. 1995. The retinoblastoma protein and cell cycle control. Cell. 81:323-330.
32. Hunter, T., and J. Pines. 1994. Cyclins and cancer. II: Cyclin D and CDK inhibitors come of age. Cell. 79:573-582.
33. Morgan, D.O. 1995. Principles of CDK regulation. Nature. 374:131-134.
34. Winston, J.T., S.R, Coats, Y.-Z. Wang, and W.J. Pledger. 1996. Regulation of the cell cycle machinery by oncogenic ras. Oncogene: 12:127-134.
35. KIP1. Mol. Cell. Biol. 17:3850-3857.
36. Leone, G., J. DeGregori, R. Sears, L. Jakoi, and J.R, Nevins. 1997. Myc and Ras collaborate in inducing accumulation of active cyclin E/cdk2 and E2F. Nature. 387:422-426.
37. Lloyd, A.C., F. Obermüller, S. Staddon, C.F. Barth, M. McMahon, and H. Land. 1997. Cooperating oncogenes converge to regulate cyclin/cdk complexes. Genes Dev. 11:663-677.
38. Peeper, D.S., T.M. Upton, M.H. Ladha, E. Neuman, J. Zalvide, R. Bernards, J.A. DeCaprio, and M.E. Ewen. 1997. Ras signalling linked to the cellcycle machinery by the retinoblastoma protein. Nature. 386:177-181.
39. Zou, X., S. Rudchenko, K. Wong, and K. Calame. 1997. Induction of c-myc transcription by the v-Abl tyrosine kinase requires Ras. Raf1. and cyclin-dependent kinases. Genes Dev. 11:654-662.
40. Kerkhoff, E., and U.R. Rapp. 1997. Induction of cell proliferation in quiescent NIH 3T3 cells by oncogenic c-Raf-1. Mol. Cell. Biol. 17:2576-2586.
41. Indolfi, C., E.V. Avvedimento, A. Rapacciuolo, E. Di Lorenzo, G. Esposito, E. Stabile, A. Feliciello, E. Mele, P. Giuliano, G. Condorelli, and M. Chiariello. 1995. Inhibition of cellular ras prevents smooth muscle cell proliferation after vascular injury in vivo. Nat. Med. 1:541-545.
42. Ueno, H., H. Yamamoto, S. Ito, J.-J. Li, and A. Takeshita. 1997. Adenovirus-mediated transfer of a dominant-negative H-ras suppresses neointimal formation in balloon-injured arteries in vivo. Arterioscler. Thromb. Vasc. Biol. 17:898-904.
43. Wei, G.L., K. Krasinski, M. Kearney, J.M. Isner, K. Walsh, and V. Andrés. 1997. Temporally and spatially coordinated expression of cell cycle regulatory factors after angioplasty. Circ. Res. 80:418-426.
44. Rothman, A., T.J. Kulik, M.B. Taubman, B.C. Berk, C.W.J. Smith, and B. Nadal-Ginard. 1992. Development and characterization of a cloned pulpul-monary arterial smooth muscle cell line that maintains differentiated properties through multiple subcultures. Circulation. 86:1977-1986.
45. Henglein, B., X. Chenivesse, J. Wang, D. Eick, and C. Bréchot. 1994. Structure and cell cycle-regulated transcription of the human cyclin A gene. Proc. Natl. Acad. Sci. USA. 91:5490-5494.
46. Desdouets, C., G. Matesic, C.A. Molina, N.S. Foulkes, P. Sassone-Corsi, C. Bréchot, and J. Sobczak-Thépot. 1995. Cell cycle regulation of cyclin A gene expression by the cyclic AMP-responsive transcription factors CREB and CREM. Mol. Cell. Biol. 15:3301-3309.
47. Schulze, A., K. Zerfass, D. Spitkovsky, S. Middendorp, J. Berges, K. Helin, P. Jansen-Dürr, and B. Henglein. 1995. Cell cycle regulation of the cyclin A gene promoter is mediated by a variant E2F site. Proc. Natl. Acad. Sci. USA. 92:11264-11268.
48. Simonson, M., Y. Wang, and W.H. Herman. 1996. Nuclear signaling by endothelin-1 requires Src protein-tyrosine kinases. J. Biol. Chem. 271:77-82.
49. Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell. 78:59-66.
50. Henthorn, P., P. Zervos, M. Raducha, H. Harris, and T. Kadesch. 1988. Expression of a human placental alkaline phosphatase gene in transfected cells: use as a reporter for studies of gene expression. Proc. Natl. Acad. Sci. USA. 85: 6342-6346.
51. Andrés, V., S. Fisher, P. Wearsch, and K. Walsh. 1995. Regulation of Gax homeobox gene transcription by a combination of positive factors including MEF2. Mol. Cell. Biol. 15:4272-4281.
52. Szeberényi, J., H. Cai, and G.M. Cooper. 1990. Effect of a dominant inhibitory HA-ras mutation on neuronal differentiation of PC12 cells. Mol. Cell. Biol. 10:5324-5332.
53. Andrés, V., and K. Walsh. 1996. Myogenin expression, cell cycle withdrawal and phenotypic differentiation are temporally separable events that precede cell fusion upon myogenesis. J. Cell Biol. 132:657-666.
54. Clowes, A., M. Reidy, and M. Clowes. 1983. Kinetics of cellular proliferation after arterial injury. I. Smooth muscle cell growth in the absence of endothelium. Lab. Invest. 49:327-333.
55. Karin, M., Z. Liu, and E. Zandi. 1997. AP-1 function and regulation. Curr. Opin. Cell Biol. 9:240-246.
56. Miano, J.M., N. Vlasic, R.R. Tota, and M.B. Stemerman. 1993. Localization of fos and jun proteins in rat aortic smooth muscle cells after vascular injury. Am. J. Pathol. 142:715-724.
57. Miano, J.M., R.R. Tota, N. Vlasic, K.J. Danishefsky, and M.B. Stemerman. 1990. Early proto-oncogene expression in rat aortic smooth muscle cells following endothelial removal. Am. J. Pathol. 137:761-765.
58. Zwicker, J., N. Liu, K. Engeland, F.C. Lucibello, and R. Müller. 1996. Cell cycle regulation of E2F site occupation in vivo. Science. 271:1595-1597.
59. Huet, X., J. Rech, A. Plet, A. Vié, and J.M. Blanchard. 1996. Cyclin A expression is under negative transcriptional control during the cell cycle. Mol. Cell. Biol. 16:3789-3798.
60. Desdouets, C., C. Ory, G. Matesic, T. Soussi, C. Bréchot, and J. Sobczak-Thépot. 1996. ATF/CREB site mediated transcriptional activation and p53 dependent repression of the cyclin A promoter. FEBS (Fed. Eur. Biochem. Soc.) Lett. 385:34-38.
61. Fattaey, A., K. Helin, and E. Harlow. 1993. Transcriptional inhibition by the retinoblastoma protein. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 340: 333-336.
62. Adams, P.D., and W.G. Kaelin, Jr. 1995. Transcriptional control by E2F. Cancer Biol. 6:99-108.
63. Weinberg, R.A. 1996. E2F and cell proliferation: a world turned upside down. Cell. 85:457-459.
64. Nevins, J.R. 1992. E2F: a link between the Rb tumor suppressor protein and viral oncoproteins. Science. 258:424-429.
65. La Thangue, N.B. 1994. DRTF1/E2F: an expanding family of heterodimeric transcription factors implicated in cell-cycle control. Trends Biochem. Sci. 19:108-114.
66. Koyama, H., E.W. Raines, K.E. Bornfeldt, J.M. Roberts, and R. Ross. 1996. Fibrillar collagen inhibits arterial smooth muscle proliferation through regulation of cdk2 inhibitors. Cell. 87:1069-1078.
67. Schulze, A., K. Zerfass-Thome, J. Bergès, S. Middendorp, P. Jansen-Dürr, and B. Henglein. 1996. Anchorage-dependent transcription of the cyclin A gene. Mol. Cell. Biol. 16:4632-4638.
68. Majesky, M.W., S.M. Schwartz, M.M. Clowes, and A.W. Clowes. 1987. Heparin regulates smooth muscle S phase entry in the injured rat carotid artery. Circ. Res. 61:296-300.
69. Dobrowolski, S., M. Harter, and D.W. Stacey. 1994. Cellular ras activity is required for passage through multiple points of the G0/G1 phase in BALB/c 3T3 cells. Mul. Cell. Biol. 14:5441-5449.
70. Feramisco, J.R., M. Gross, T. Kamata, M. Rosenberg, and R.W. Sweet. , 1984. Microinjection of the oncogen form of the human H-ras (T-24) protein results in rapid proliferation of quiescent cells. Cell. 38:109-117.
71. Stacey, D.W., and H.F. Kung. 1984. Transformation of NIH 3T3 cells by microinjection of Ha-ras protein. Nature. 310:508-511.
72. Mulcahy, L.S., M.R. Smith, and D.W. Stacey. 1985. Requirement for ras proto-oncogen function during serum-stimulated growth of NIH 3T3 cells. Nature. 313:241-243.
73. Feig, L.A., and G.M. Cooper. 1988. Inhibition of NIH 3T3 proliferation by a mutant ras protein with preferential affinity for GDP. Mol. Cell. Biol. 8:3235-3243.
74. Herber, S., M. Truss, M. Beato, and R. Müller. 1994. Inducible regulatory elements in the human cyclin D1 promoter. Oncogene. 9:1295-1304.
75. ras mutants and c-Ets-2 activate the cyclin D1 promoter through distinguishable regions. J. Biol. Chem. 270:23589-23597.
76. MAPK pathway. J. Biol. Chem. 271:20608-20615.