Cooperative interactions between RB and p53 regulate cell proliferation, cell senescence, and apoptosis in human vascular smooth muscle cells from atherosclerotic plaques

Circulation Research

Volumn 82, Issue 6, 1998, Pages 704-712

  Bennett, Martin R ^a,b   Macdonald, Kirsty ^a   Chan, Shiu Wan ^a   Boyle, Joseph J ^a   Weissberg, Peter L ^a  

^a ADDENBROOKE S HOSPITAL   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Apoptosis; Atherosclerosis; p53; Retinoblastoma

Indexed keywords

GENE PRODUCT; PROTEIN P53; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR E2F;

APOPTOSIS; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CELL AGING; CELL PROLIFERATION; CONTROLLED STUDY; GROWTH REGULATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; TUMOR SUPPRESSOR GENE; VASCULAR SMOOTH MUSCLE;

EID: 0032489850     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.82.6.704     Document Type: Article

References (56)

1. Gordon D, Reidy MA, Benditt EP, Schwartz SM. Cell proliferation in human coronary arteries. Proc Natl Acad Sci U S A. 1990;87:4600-4604.
2. O'Brien ER, Alpers CE, Stewart DK, Ferguson M, Tran N, Gordon D, Benditt EP, Hinohara T, Simpson JB, Schwartz SM. Proliferation in primary and restenotic coronary atherectomy tissue: implications for antiproliferative therapy. Circ Res. 1993;73:223-231.
3. Mosse PR, Campbell GR, Wang ZL, Campbell JH. Smooth muscle phenotypic expression in human carotid arteries, I: comparison of cells from diffuse intimal thickenings adjacent to atheromatous plaques with those of the media. Lab Invest. 1985;53:556-562.
4. Ross R, Wight TN, Strandness E, Thiele B. Human atherosclerosis, I: cell constitution and characteristics of advanced lesions of the superficial femoral artery. Am J Pathol. 1984;114:79-93.
5. Bennett MR, Evan GI, Schwartz SM. Apoptosis of human vascular smooth muscle cells derived from normal vessels and coronary atherosclerotic plaques. J Clin Invest. 1995;95:2266-2274.
6. Geng Y, Libby P. Evidence for apoptosis in advanced human atheroma: colocalization with interleukin-1β converting enzyme. Am J Pathol. 1995;147:251-266.
7. Han D. Haudenschild C, Hong M, Tinkle B, Leon M, Liau G. Evidence for apoptosis in human atherosclerosis and in a rat vascular injury model. Am J Pathol. 1995;147:267-277.
8. lavarone A, Garg P, Lasorella A, Hsu J, Israel MA. The helix-loop-helix protein Id-2 enhances cell proliferation and binds to the retinoblastoma protein. Genes Dev. 1994;8:1270-1284.
9. Muthukkumar S, Sells SF, Crist SA, Rangnekar VM. Interleukin-1 induces growth arrest by hypophosphorylation of the retinoblastoma susceptibility gene product RB. J Biol Chem. 1996;271:5733-5740.
10. Agarwal ML, Agarwal A, Taylor WR, Stark GR. p53 controls both the G2/M and the G l cell cycle checkpoints and mediates reversible growth arrest in human fibroblasts. Proc Natl Acad Sci U S A. 1995;92: 8493-8497.
11. Gonos ES, Burns JS, Mazars GR, Kobrna A, Riley TE, Barnett SC, Zafarana G, Ludwig RL, Ikram Z, Powell AJ, Jat PS. Rat embryo fibroblasts immortalized with simian virus 40 large T antigen undergo senescence upon its inactivation. Mol Cell Biol. 1996;16:5127-5138.
12. Macleod KF, Sherry N, Hannon G, Beach D, Tokino T, Kinzler K, Vogelstein B, Jacks T. p53-dependent and independent expression of p21 during cell growth, differentiation, and DNA damage. Genes Dev. 1995; 9:935-944.
13. Bond JA, Blaydes JP, Rowson J, Haughton MF, Smith JR, Wynford TD, Wyllie FS. Mutant p53 rescues human diploid cells from senescence without inhibiting the induction of SDI1/WAF1. Cancer Res. 1995;55:2404-2409.
14. Missero C, Calautti E, Eckner R, Chin J, Tsai L, Livingston D, Dotto G. Involvement of the cell-cycle inhibitor cip1/waf1 and the E 1a-associated p300 protein in terminal differentiation. Proc Natl Acad Sci U S A. 1995; 92:5451-5455.
15. Jiang H, Lin J, Su ZZ, Collart FR, Huberman E, Fisher PB. Induction of differentiation in human promyelocytic HL-60 leukemia cells activates p21, WAF1/CIP1, expression in the absence of p53. Oncogene. 1994;9:397-3406.
16. Smith ML, Chen IT, Zhan Q, Bae I. Chen CY, Gilmer TM, Kastan MB, O'Connor PM, Fomace AJJ. Interaction of the p53-regulated protein Gadd45 with proliferating cell nuclear antigen. Science. 1994;266:1376-1380.
17. Bandara LR, Adamczewski JP, Hunt T, La Thangue NB. Cyclin A and the retinoblastoma gene product complex with a common transcription factor. Nature. 1991;352:249-251.
18. Chellappan SP, Hiebert S, Mudryj M, Horowitz JM, Nevins JR. The E2F transcription factor is a cellular target for the RB protein. Cell. 1991;65: 1053-1061.
19. Helin K, Harlow E, Fattaey A. Inhibition of F2F-1 transactivation by direct binding of the retinoblastoma protein. Mol Cell Biol. 1993;13:6501-6508.
20. Dynlacht BD, Flores O, Lees JA, Harlow E. Differential regulation of E2F transactivation by cyclin/cdk2 complexes. Genes Dev. 1994;8:1772-1786.
21. Egan C, Bayley S, Branton P. Binding of RB1 protein to E1A products is required for adenovirus transformation. Oncogene. 1989;4:383-388.
22. Raychaudhuri P, Bagchi S, Devoto SH, Kraus VB, Moran E, Nevins JR. Domains of the adenovirus E1A protein required for oneogenic activity are also required for dissociation of E2F transcription factor complexes. Genes Dev. 1991;5:1200-1211.
23. Hiebert S. Regions of the retinoblastoma gene product required for its interaction with the E2F transcription factor are necessary for E2 promoter repression and pRB-mediated growth suppression. Mol Cell Biol 1993;13:3384-3391.
24. Hiebert S, Chellapan S, Horowitz J, Nevins J, The interaction of RB with E2F coincides with an inhibition of the transcriptional activity of E2F. Genes Dev. 1992;6:177-185.
25. el Deiry WS, Harper JW, O'Connor PM, Velculescu VE, Canman CE, Jackman J, Pietenpol JA, Burrell M, Hill DE, Wang Y, et al. WAF1/CIP1 is induced in p53-mediated G1 arrest and apoptosis. Cancer Res. 1994; 54:1169-1174.
26. Parker SB, Eichele G, Zhang P, Rawls A, Sands AT, Bradley A, Olson EN, Harper JW, Elledge SJ. p53-independent expression of p21Cip1 in muscle and other terminally differentiating cells [comments]. Science. 1995;367:1024-1027.
27. Shaw P, Bovey R, Tardy S, Sahli R, Sordat B, Costa J. Induction of apoptosis by wild-type p53 in a human colon tumor-derived cell line. Proc Natl Acad Sci U S A. 1992;89:4495-4499.
28. Yonish-Rouach E, Resnitzky D, Lotem J, Sachs L, Kimchi A, Oren M. Wild-type p53 induces apoptosis of myeloid leukaemic cells that is inhibited by interleukin-6. Nature. 1991;352:345-347.
29. Haupt Y, Rowan S, Oren M. p53-mediated apoptosis in Hela-cells can he overcome by excess pRB. Oncogene. 1995;10:1563-1571.
30. Oren M. Relationship of p53 to the control of apoptotic cell death. Semin Cancer Biol. 1994;5:3051-3057.
31. Qin XQ, Livingston DM, Kaelin WGJ. Adams PD. Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis. Proc Natl Acad Sci U S A. 1994;91:10918-10922.
32. Shan B, Lee WH. Deregulated expression of E2F-1 induces S-phase entry and leads to apoptosis. Mol Cell Biol. 1994;14:8166-8173.
33. Wu X, Levine AJ. p53 and E2F-1 cooperate to mediate apoptosis. Proc Natl Acad Sci U S A. 1994;91:3602-3606.
34. Hiebert S, Packham G, Strom D, Haffner R, Oren M, Zambetti G, Cleveland J. E2F-1/DP-1 induces p53 and overrides survival factors to trigger apoptosis. Mol Cell Biol. 1995;15:6864-6874.
35. Bennett MR, Littlewood TD, Schwartz SM, Weissberg PL. Increased sensitivity of human vascular smooth muscle cells from atherosclerotic plaque to p53-mediated apoptosis. Circ Res. 1997;81:591-599.
36. Shaulian E, Zauberman A, Ginsberg D. Oren M. Identification of a minimal transforming domain of p53: negative dominance through abrogation of sequence-specific DNA binding. Mol Cell Biol. 1992;12:5581-5592.
37. Morgenstern J, Land H. Choice and manipulation of retroviral vectors. In: Murray EJ, ed. Gene Transfer and Expression Protocols. Clifton, NJ: The Humana Press Inc; 1991:181-206.
38. Waters CM, Littlewood TD, Hancock DC, Moore JP, Evan GI. c-myc protein expression in umransformed fibroblasts. Oncogene. 1991;6:797-805.
39. Kern SE, Kinzler KW, Bruskin A, Jarosz D, Friedman P, Prives C. Vogelstein B. Identification of p53 as a sequence-specific DNA-binding protein. Science. 1991;252:1708-1711.
40. Sambrook J, Fritsch E, Maniatis T. Molecular Cloning: A Laboratory Manual. 2nd ed. New York, NY: Cold Spring Harbor Laboratory Press: 1989.
41. Bennett MR, Evan GI, Newhy AC. Deregulated c-myc oncogene expression blocks vascular smooth muscle cell inhibition mediated by heparin, imerferon-γ. mitogen depletion and cyclic nucleotide analogues and induces apoptotic cell death. Circ Res. 1994;74:525-536.
42. 1 cyclin-cdk complexes. EMBO J. 1995;14: 4814-4826.
43. Stein GH, Beeson M, Gordon L. Failure to phosphorylate the retinoblastoma gene product in senescent human fibroblasts. Science. 1990: 249:666-669.
44. Futreal PA, Barren JC. Failure of senescent cells to phosphorylate the RB protein. Oncogene. 1991;6:1109-1113.
45. Templeton D, Park S, Lanier L, Weinberg R. Nonfunctional mutants of the retinoblastoma protein are characterized by defects in phosphorylation, oncoprotein association and nuclear tethering. Proc Natl Acad Sci U S A. 1991;88:3033-3037.
46. Zhu L, van den Heuvel S, Helin K, Fattaey A, Ewen M, Livingston D, Dyson N, Harlow E. Inhibition of cell proliferation by p107, a relative of the retinoblastoma protein. Genes Dev. 1993;7:1111-1125.
47. Qin XQ, Livingston DM, Ewen M, Sellers WR, Arany Z, Kaelin WGJ. The transcription factor E2F-1 is a downstream target of RB action. Mol Cell Biol. 1995;15:742-755.
48. ink4 expression and telomere length during spontaneous immortalization of Li-Fraumeni syndrome fibroblasts. Mol Cell Biol. 1995;15:4745-4753.
49. Hara E, Tsurui H, Shinozaki A, Nakada S, Oda K. Cooperative effect of antisense-Rb and antisense-p53 oligomers on the extension of life span in human diploid fibroblasts, TIG-1. Biochem Biophys Res Commun. 1991; 179:528-534.
50. Morgenbesser SD, Williams BO, Jacks T, DePinho RA. p53-dependent apoptosis produced by Rb-dcficiency in the developing mouse lens. Nature. 1994;371:72-74.
51. Howes KA, Ransom N, Papermaster DS, Lasudry JG, Albert DM, Windle JJ. Apoptosis or retinoblastoma: alternative fates of photoreceptors expressing the HPV-16 E7 gene in the presence or absence of p53. Genes Dev. I994;8:1300-1310.
52. Pan H, Griep AE. Altered cell cycle regulation in the lens of HPV-16 E6 or E7 transgenic mice: implications for tumor suppressor gene function in development. Genes Dev: 1994;8:1285-1299.
53. Symonds H, Krall L, Remington L, Saenz RM, Lowe S, Jacks T, Van DT. p53-dependent apoptosis suppresses tumor growth and progression in vivo. Cell. 1994;78:703-711.
54. Almasan A, Yin Y, Kelly R, Lee H, Bradley A, Li W, Bertino J, Wahl G. Deficiency of retinoblastoma protein leads to inappropriate S-phase entry, activation of E2F-responsive genes, and apoptosis. Proc Natl Acad Sci U S A. 1995;92:5436-5440.
55. Hansen R, Reddel R, Braithwaite A. The transforming oncoproteins determine the mechanism by which p53 suppresses cell-transformation: pRB-mediated growth arrest or apoptosis. Oncogene. 1995;11:2535-2545.
56. Slansky JE, Farnham PJ. Introduction to the E2F family: protein structure and gene regulation. Curr Top Microbiol Immunol. 1996;208:1-30.