p21 (cip1)-mediated inhibition of cell proliferation by overexpression of the gax homeodomain gene

Genes and Development

Volumn 11, Issue 13, 1997, Pages 1674-1689

  Smith, Roy C ^a   Branellec, Didier ^b   Gorski, David H ^c   Guo, Kun ^a   Perlman, Harris ^a,d   Dedieu, Jean François ^b   Pastore, Christopher ^a   Mahfoudi, Abderrahim ^b   Denèfle, Patrice ^b   Isner, Jeffrey M ^a   Walsh, Kenneth ^a,d  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SANOFI   (France)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d TUFTS UNIVERSITY   (United States)

Author keywords

Angioplasty; Cell cycle; Gax; Homeobox gone; p21; Smooth muscle

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR; MESSENGER RNA; PROTEIN P21; RECOMBINANT PROTEIN; CDK2 PROTEIN, HUMAN; CDK2 PROTEIN, RAT; CDKN1A PROTEIN, HUMAN; CDKN1A PROTEIN, RAT; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLINE; HOMEODOMAIN PROTEIN; HYBRID PROTEIN; MEOX2 PROTEIN, RAT; MUSCLE PROTEIN; PROTEIN P53; PROTEIN SERINE THREONINE KINASE;

ADENOVIRUS; ANGIOPLASTY; ANIMAL CELL; ARTERY INJURY; ARTICLE; CAROTID ARTERY; CELL CYCLE; CELL PROLIFERATION; DOWN REGULATION; FIBROBLAST CULTURE; GENE EXPRESSION REGULATION; GROWTH INHIBITION; HOMEOBOX; HUMAN; HUMAN CELL; MITOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; VASCULAR SMOOTH MUSCLE; VIRUS INFECTION; ANIMAL; CAROTID ARTERY INJURY; CELL DIVISION; CELL LINE; CYTOLOGY; DEFECTIVE VIRUS; DRUG ANTAGONISM; GENE VECTOR; GENETICS; METABOLISM; PERCUTANEOUS TRANSLUMINAL ANGIOPLASTY; PHYSIOLOGY; RAT;

ADENOVIRIDAE; ANIMALIA;

ADENOVIRIDAE; ANGIOPLASTY, BALLOON; ANIMALS; CAROTID ARTERY INJURIES; CDC2-CDC28 KINASES; CELL DIVISION; CELL LINE; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASES; CYCLINS; DEFECTIVE VIRUSES; GENE EXPRESSION REGULATION; GENETIC VECTORS; HOMEODOMAIN PROTEINS; HUMANS; MUSCLE PROTEINS; MUSCLE, SMOOTH, VASCULAR; PROTEIN-SERINE-THREONINE KINASES; RATS; RECOMBINANT FUSION PROTEINS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0030610836     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.11.13.1674     Document Type: Article

References (81)

1. Aberdam, D., V. Negreanu, L. Sachs, and C. Blatt. 1991. The oncogenic potential of an activated Hox-2.4 homeobox gene in mouse fibroblasts. Mol. Cell Biol. 11: 554-557.
2. 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.
3. 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.
4. Ansorge, W. and R. Pepperkok. 1988. Performance of an automated system for capillary microinjection into living cells. J. Biochem. Biophys. Methods 16: 283-292.
5. 1/S arrest. Genes & Dev. 8: 453-464.
6. Campbell, G.R., J.H. Campbell, J.A. Manderson, S. Horrigan, and R.E. Rennick. 1988. Arterial smooth muscle: A multifunctional mesenchymal cell. Arch. Pathol. Lab. Med. 112: 977-986.
7. Castellot, J.J., D.L. Cochran, and M.J. Karnovsky. 1985. Effect of heparin on vascular smooth muscle cells. I. Cell metabolism. J. Cell. Physiol. 124: 21-28.
8. Castrillo, J.L., L.E. Theill, and M. Karin. 1991. Function of the homeodomain protein GHF1 in pituitary cell proliferation. Science 253: 197-199.
9. Chang, M.W., E. Barr, M.M. Lu, K. Barton, and J.M. Leiden. 1995a. 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.
10. Chang, M.W., E. Barr, J. Seltzer, Y. Jiang, G.J. Nabel, E.G. Nabel, M.S. Parmacek, and J.M. Leiden. 1995b. Cytostatic gene therapy for vascular proliferative disorders with a constitutively active form of the retinoblastoma gene product. Science 267: 518-522.
11. Chomczynski, P. and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenolchloroform extraction. Anal. Biochem. 162: 156-159.
12. Clesham, G.J., H. Browne, S. Efstathiou, and P.L. Weissberg. 1996. Enhancer stimulation unmasks latent gene transfer after adenovirus-mediated gene delivery into human vascular smooth muscle cells. Circ. Res. 79: 1188-1195.
13. Clowes, A.W., M.A. Reidy, and M.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.
14. Crescenzi, M., T.P. Fleming, A.B. Lassar, H. Weintraub, and S.A. Aaronson. 1990. MyoD induces growth arrest independent of differentiation in normal and transformed cell lines. Proc. Natl. Acad. Sci. 87: 8442-8446.
15. Cserjesi, P., B. Lilly, L. Bryson, Y. Wang, D. Sassoon, and E.N. Olson. 1992. MHox: A mesodermally restricted homeodomain protein that binds an essential site in the muscle creatine kinase enhancer. Development 15: 1087-1101.
16. Davis, R.L., H. Weintraub, and A.B. Lassar. 1987. Expression of a single transfected cDNA converts fihroblasts to myoblasts. Cell 51: 987-1000.
17. Deguchi, Y., and J.H. Kehrl. 1993. High level expression of the homeobox gene HB24 in a human T-cell line confers the ability to form tumors in nude mice. Cancer Res. 53: 373-377.
18. Del Sal, G., M.E. Ruaro, L. Philipson, and C. Schneider. 1992. The growth arrest-specific gene, gas1, is involved in growth suppression. Cell 70: 595-607.
19. Deng, C., P. Zhang, J.W. Harper, S.J. Elledge, and P. Leder. 1995. Mice lacking p21CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell 82: 675-684.
20. Edelman, G.M. and F.S. Jones. 1993. Outside and downstream of the homeobox. J. Biol. Chem. 268: 20683-20686.
21. El-Deiry, W.S., T. Tokino, V.E. Velculescu, D.B. Levy, R. Parsons, J.M. Trent, D. Lin, W.E. Mercer, K.W. Kinzler, and B. Vogelstein. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75: 817-825.
22. Field, J., J. Nikawa, D. Broek, B. MacDonald, L. Rodgers, I.A. Wilson, R.A. Lerner, and M. Wigler. 1988. Purification of a RAS-responsive adenylyl cyclase complex from Saccharomyces cerevisiae by use of an epitope addition method. Mol. Cell. Biol. 8: 2159-2165.
23. Fornace, A.J., D.W. Nebert, M.C. Hollander, J.D. Luethy, M. Papathanasiou, J. Fargnoli, and N.J. Holbrook. 1989. Mammalian genes coordinately regulated by growth arrest signals and DNA-damaging agents. Mol. Cell. Biol. 9: 4196-4203.
24. Fornace, A.J., J. Jackman, M.C. Hollander, B. Hoffman-Liebermann, and D.A. Liebermann. 1992. Genotoxic-stress-response genes and growth arrest genes: gadd, MyD, and other genes induced by treatments eliciting growth arrest. Ann. N.Y. Acad. Sci. 663: 139-153.
25. French, B.A., W. Mazur, N.M. Ali, R.S. Geske, J.P. Finnigan, G.P. Rodgers, R. Roberts, and A.E. Raizner. 1994. Percutaneous transluminal in vivo gene transfer by recombinant adcnovirus in normal porcine coronary arteries, atherosclerotic arteries, and two models of coronary restenosis. Circulation 90: 2402-2413.
26. Goodrich, D.W., N.P. Wang, Y.-W. Qian, E.Y.-H. Lee, and W.-H. Lee. 1991. The retinoblastoma gene product regulates progression through the G1 phase of the cell cycle. Cell 67: 293-302.
27. 1 transition in vascular smooth muscle cells. Mol. Cell. Biol. 13: 3722-3733.
28. Graham, F.L. and A.J. van der Eb. 1973. A new technique for assay of infectivity of human adenovirus 5 DNA. Virology 52: 456-463.
29. Gualberto, A. D.F. LePage, G. Pons, S.L. Mader, K. Park, M.L. Atchinson, and K. Walsh. 1992. Functional antagonism between YY1 and the serum response factor. Mol. Cell. Biol. 12: 4209-4214.
30. Guo, K., J. Wang, V. Andrés, R.C. Smith, and K. Walsh. 1995. MyoD-induced expression of p21 inhibits cyclin-dependent kinuse activity upon myocyte terminal differentiation. Mol. Cell. Biol. 15: 3823-3829.
31. Guzman, R.J., E.A. Hirschowitz, S.L. Brody, R.G. Crystal, S.E. Epstein, and T. Finkel. 1994. In vivo suppression of injury-induced vascular smooth muscle cell accumulation using adenovirus-mediated transfer of the herpes simplex virus thymidine kinase gene. Proc. Natl. Acad. Sci. 91: 10732-10736.
32. Halevy, O., B.G. Novitch, D.B. Spicer, S.X. Skapek, J. Rhee, G.J. Hannon, D. Beach, and A.B. Lassar. 1995. Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science 267: 1018-1021.
33. Harper, J.W., G.R. Adami, N. Wei, K. Keyomarsi, and S.J. Elledge. 1993. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinascs. Cell 75: 805-816.
34. Harvey, D.M. and A.J. Levine. 1991. p53 alteration is a common event in the spontaneous immortalization of primary BALB/c murine embryo fibroblasts. Genes & Dev. 5: 2375-2385.
35. Henthorn, P., P. Zervos, M. Raducha, H. Harris, and T. Kadesch. 1988. Expression of human placental alkaline phosphatase gene in transfected cells: use as a reporter for studies of gene expression. Proc. Natl. Acad. Sci. 87: 6922-6926.
36. Hochuli, E., W. Bannwarth, H. Döbeli, R. Gentz, and D. Stüber. 1988. Genetic approach to facilitate purification of recombinant proteins with a novel metal chelate adsorbent. BioTechnology 6: 1321-1325.
37. Hockenberry, D. 1995. Defining apoptosis. Am. J. Pathol. 146: 16-19.
38. 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.
39. Krek, W., G. Xu, and D.M. Livingston. 1995. Cyclin A-kinase Regulation of E2F-1 DNA binding function underlies suppression of an S phase checkpoint. Cell 83: 1149-1158.
40. Lassar, A.B., J.N. Buskin, D. Lockshon, R.L. Davis, S. Apone, S.D. Hauschka, and H. Weintraub. 1989. MyoD is a sequence-specific DNA binding protein requiring a region of myc homology to bind to the muscle creatine kinase enhancer. Cell 58: 823-831.
41. Lee, S.W., B.C. Trapnell, J.J. Rade, R. Virmani, and D.A. Dichek. 1993. In vivo vector-mediated gene transfer into balloon-injured rat carotid arteries. Circ. Res. 73: 797-807.
42. Li, X., P. Tsai, E.D. Wieder, A. Kribben, V.V. Putten, R.W. Schrier, and R.A. Nemenoff. 1994. Vascular smooth muscle cells grown on matrigel: A model of the contractile phenotype with decreased activation of mitogen-activated protein kinase. J. Biol. Chem. 30: 19653-19658.
43. Liu, M., M.-H. Lee, M. Cohen, M. Bommakanti, and L.P. Freedman. 1996. Transcriptional activation of the Cdk inhibitor p21 by vitamin D3 leads to the induced differentiation of the myelomonocytic cell line U937. Genes & Dev. 10: 142-153.
44. Mader, S. L. 1992. Influence of animal age on the β-adrenergic system in cultured rat aortic and mesenteric artery smooth muscle cells. J. Gerontol. Biol. Sci. 47: B32-36.
45. Majno, G. and I. Joris. 1995. Apoptosis, oncosis, and necrosis: an overview of cell death. Am. J. Pathol. 146: 3-15.
46. March, K.L., J.E. Madison, and B.C. Trapnell. 1995. Pharmacokinetics of adenoviral vector-mediated gene delivery to vascular smooth muscle cells: Modulation by poloxamer 407 and implications for cardiovascular gene therapy. Hum. Gene Ther. 6: 41-53.
47. Mulcahy, L.S., M.R. Smith, and D.W. Stacey. 1985. Requirement for ras proto-oncogene function during serum-stimulated growth of NIH3T3 cells. Nature 313: 241-243.
48. Niehrs, C., R. Keller, K.W.Y. Cho, and E.M. De Robertis. 1993. The homeobox gene goosecoid controls cell migration in embryos. Cell 72: 491-503.
49. Nilsson, J. 1986. Growth factors and the pathogenesis of atherosclerosis. Atherosclerosis 62: 185-189.
50. Ohno, T., D. Gordon, H. San, V.J. Pompili, M.J. Imperiale, G.J. Nabel, and E.G. Nabel. 1994. Gene therapy for vascular smooth muscle cell proliferation after arterial injury. Science 265: 781-784.
51. Ohtsubo, M., A.M. Theodoras, J. Schumacher, J.M. Roberts, and M. Pagano. 1995. Human cyclin E, a nuclear protein essential for the G1-to-S phase transition. Mol. Cell. Biol. 15: 2612-2624.
52. Park, K. and M.L. Atchison. 1991. Isolation of a candidate repressor/activator, NF-E1 (YY-1, Δ), that hinds to the immunoglobulin κ 3′ enhancer and the immunoglobulin heavy-chain μE1 site. Proc. Natl. Acad. Sci. 88: 9804-9808.
53. cip1 in muscle and other terminally differentiating cells. Science 267: 1024-1027.
54. Pastore, C.J., J.M. Isner, P.A. Bacha, M. Kearney, and J.G. Pickering. 1995. Ipidermal growth factor receptor-targeted cytotoxin inhibits neointimal hyperplasia in vivo. Circ. Res 77: 519-529.
55. Pauly, R.R., A. Passaniti, M. Crow, J.L. Kinsella, N. Papadopoulos, R. Monticone, E.G. Lakatta, and G.R. Martin. 1992. Experimental models that mimic the differentiation and dedifferentiation of vascular cells. Circulation 86: III68-III73.
56. Pepperkok, R., C. Schneider, L. Philipson, and W. Ansorge. 1988. Single cell assay with an automated microinjection system. Exp. Cell Res. 178: 369-376.
57. Pickering, J.G., L. Weir, K. Rosenfield, J. Stetz, J. Jekanowski, and J.M. Isner. 1992. Smooth muscle cell outgrowth from human atherosclerotic plaque: Implications for the assessment of lesion biology. J. Am. Coll. Cardiol. 20: 1430-1439.
58. Rade, J.J., A.H. Schulick, R. Virmani, and D.A. Dichek. 1996. Local adenoviral-mediated expression of recombinant hirudin reduces neointima formation after arterial injury. Nature Med. 2: 293-298.
59. Ross, R. 1993. The pathogenesis of atherosclerosis: A perspective for the 1990s. Nature 362: 801-809.
60. Ross, R., D.F. Bowen-Pope, and E.W. Raines. 1990. Platelet-derived growth factor in health and disease. Trans. R. Soc. Lond. B 327: 155-169.
61. Salser, S.J. and C. Kenyon. 1992. Activation of a C. elegans Antennapedia homologue in migrating cells controls their direction of migration. Nature 355: 255-258.
62. Schneider, C., R.M. King, and L. Philipson. 1988. Genes specifically expressed at growth arrest of mammalian cells. Cell 54: 787-793.
63. Shi, Y., E. Seto, L.-S. Chang, and T. Shenk. 1991. Transcriptional repression by YY1, a human GLI-Krüppel-related protein, and relief of repression by adenovirus E1A protein. Cell 67: 377-388.
64. Simari, R.D., H. San, M. Rekhter, T. Ohno, D. Gordon, J. Nabel, and E.G. Nabel. 1996. Regulation of cellular proliferation and intimal formation following balloon injury in atherosclerotic rabbit arteries. J. Clin. Invest. 98: 225-235.
65. Skopicki, H.A., G.E. Lyons, G. Schatteman, R.C. Smith, V. Andrés, S. Schirm, J.M. Isner, and K. Walsh. 1997. Embryonic expression of the gax homeodomain protein in cardiac, smooth and skeletal muscle. Circ. Res. 80: 452-462.
66. Smith, D.B. and K.S. Johnson. 1988. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67: 31-40.
67. Song, K., Y. Wang, and D. Sassoon. 1992. Expression of Hox-7.1 in myoblasts inhibits terminal differentiation and induces cell transformation. Nature 360: 477-481.
68. Sorrentino, V., R. Pepperkok, R. Davis, W. Ansorge, and L. Philipson. 1990. Cell proliferation inhibited by MyoD1 independently of myogenic differentiation. Nature 345: 813-815.
69. Stratford-Perricaudet, L.D., I. Makeh, M. Perricaudet, and P. Briand. 1992. Widespread long-term gene transfer to mouse skeletal muscles and heart. J. Clin. Invest. 90: 626-630.
70. Tanaka, M. and W. Herr. 1990. Differential transcriptional activation by Oct-1 and Oct-2: interdependent activation domains induce Oct-2 phosphorylation. Cell 60: 375-386.
71. Taub, M., Y. Wang, T.M. Szczesny, and H.K. Kleinman. 1990. Epidermal growth factor or transforming growth factor alpha is required for kidney tubulogenesis in matrigel cultures in serum-free medium. Proc. Natl. Acad. Sci. 87: 4002-4006.
72. Timchenko, N.A., M. Wilde, M. Nakanishi, J.R. Smith, and G.J. Darlington. 1996. CCAAT/enhancer-binding protein alpha (C/EBPα) inhibits cell proliferation through the p21 (WAF-1/CIP-1/SDI-1) protein. Genes & Dev. 10: 804-815.
73. van den Heuvel, S. and E. Harlow. 1993. Distinct roles for cyclin-dependent kinases in cell cycle control. Science 262: 2050-2054.
74. Waga, S., G.J. Hannon, D. Beach, and B. Stillman. 1994. The p21 inhibitor of cyclin-dependent kinases controls DNA replication by interacting with PCNA. Nature 369: 574-577.
75. Walsh, K. and H. Perlman. 1996. Molecular strategies to inhibit restenosis: Modulation of the vascular myocyte phenotype. Semin. Intervent. Cardiol. 1: 173-179.
76. Wang, J. and K. Walsh. 1996. Resistance to apoptosis conferred by Cdk inhibitors during myocyte differentiation. Science 273: 359-361.
77. Weinberg, R.A. 1995. The retinoblastoma protein and cell cycle control. Cell 81: 323-330.
78. Weir, L., D. Chen, C. Pastore, J.M. Isner, and K. Walsh. 1995. Expression of GAX, a growth-arrest homeobox gene, is rapidly down-regulated in the rat carotid artery during the proliferative response to balloon injury. J. Biol. Chem. 270: 5457-5461.
79. Willard, J.E., C. Landau, D.B. Glamann, D. Burns, M.E. Jessen, M.J. Pirwitz, R. D. Gerard, and M.S. Meidell. 1994. Genetic modification of the vessel wall: comparison of surgical and catheter-based techniques for delivery of recombinant adenovirus. Circulation 89: 2190-2197.
80. Yang, Z.-Y., R.D. Simari, N.D. Perkins, H. San, D. Gordon, G.J. Nabel, and E.G. Nabel. 1996. Role of the p21 cyclin-dependent kinase inhibitor in limiting intimal cell proliferation in response to arterial injury. Proc. Natl. Acad. Sci. 93: 7905-7910.
81. Zhan, Q., K.A. Lord, I.J. Alamo, M.C. Hollander, F. Carrier, D. Ron, K.W. Kohn, B. Hoffman, D.A. Liebermann, and A.J.J. Fornace. 1994. The gadd and MyD genes define a novel set of mammalian genes encoding acidic proteins that synergistically suppress cell growth. Mol. Cell. Biol. 14: 2361-2371.