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WAF1/CIP1 Is Induced in p53-mediated G₁ Arrest and Apoptosis¹

The Oncology Center and Program in Human Genetics and Molecular Biology, The Johns Hopkins University School of Medicine, Baltimore, Maryland 21231 [W. S. E-D., V. E. V., C. E. C., J. A. P., M. B. K., K. W. Ki., B. V.] The Laboratory of Molecular Pharmacology, Division of Cancer Treatment, Developmental Therapeutics Program, National Cancer Institute, NIH, Bethesda, Maryland 20892 [P. M. O., J. J., K. W. Ko.] Oncogene Science, Inc., Cambridge, Massachussetts 02142 [M. B., D. E. H.] Department of Tumor Biology, Karolinska Institutet, Box 60400, S-104 01, Stockholm, Sweden [K. G. W., Y. W.]; Howard Hughes Medical Institute [S. J. E.] and Verna and Marrs McLean Department of Biochemistry and Institute of Molecular Genetics [J. W. H., S. J. E.], Baylor College of Medicine, Houston, Texas 77030; and Department of Microbiology and Immunology, Jefferson Cancer Institute, Thomas Jefferson University, Philadelphia, Pennsylvania 19107 [W. E. M.]

The tumor growth suppressor WAF1/CIP1 was recently shown to be induced by p53 and to be a potent inhibitor of cyclin-dependent kinases. In the present studies, we sought to determine the relationship between the expression of WAF1/CIP1 and endogenous regulation of p53 function. WAF1/CIP1 protein was first localized to the nucleus of cells containing wild-type p53 and undergoing G₁ arrest. WAF1/CIP1 was induced in wild-type p53-containing cells by exposure to DNA damaging agents, but not in mutant p53-containing cells. The induction of WAF1/CIP1 protein occurred in cells undergoing either p53-associated G₁ arrest or apoptosis but not in cells induced to arrest in G₁ or to undergo apoptosis through p53-independent mechanisms. DNA damage led to increased levels of WAF1/CIP1 in cyclin E-containing complexes and to an associated decrease in cyclin-dependent kinase activity. These results support the idea that WAF1/CIP1 is a critical downstream effector in the p53-specific pathway of growth control in mammalian cells.

¹ This work was supported by the Preuss Foundation, the Clayton Fund, the National Foundation for Cancer Research, the Glaxo Research Institute, Inc. (M. B. K. and C. E. C.), the Council for Tobacco Research (M. B. K. and C. E. C.), and NIH Grants GM07309, GM07184, ES05777 (M. B. K.), CA-09071, CA-55541 (W. E. M.), AG-11085 (S. J. E., and J. W. H.), and CA-43460. B. V. is an American Cancer Society research professor.

Received 12/28/93. Accepted 1/20/94.

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				S. Dey, P. M. Spring, S. Arnold, J. Valentino, D. Chendil, W. F. Regine, M. Mohiuddin, and M. M. Ahmed Low-Dose Fractionated Radiation Potentiates the Effects of Paclitaxel in Wild-type and Mutant p53 Head and Neck Tumor Cell Lines Clin. Cancer Res., April 1, 2003; 9(4): 1557 - 1565. [Abstract] [Full Text] [PDF]

				A. Krones-Herzig, E. Adamson, and D. Mercola Early growth response 1 protein, an upstream gatekeeper of the p53 tumor suppressor, controls replicative senescence PNAS, March 18, 2003; 100(6): 3233 - 3238. [Abstract] [Full Text] [PDF]

				M J Pellikainen, T T Pekola, K M Ropponen, V V Kataja, J K Kellokoski, M J Eskelinen, and V-M Kosma p21WAF1 expression in invasive breast cancer and its association with p53, AP-2, cell proliferation, and prognosis J. Clin. Pathol., March 1, 2003; 56(3): 214 - 220. [Abstract] [Full Text] [PDF]

				N. Denko, K. Wernke-Dollries, A. B. Johnson, E. Hammond, C.-M. Chiang, and M. C. Barton Hypoxia Actively Represses Transcription by Inducing Negative Cofactor 2 (Dr1/DrAP1) and Blocking Preinitiation Complex Assembly J. Biol. Chem., February 14, 2003; 278(8): 5744 - 5749. [Abstract] [Full Text] [PDF]

				M. A. O'Reilly, R. J. Staversky, J. N. Finkelstein, and P. C. Keng Activation of the G2 cell cycle checkpoint enhances survival of epithelial cells exposed to hyperoxia Am J Physiol Lung Cell Mol Physiol, February 1, 2003; 284(2): L368 - L375. [Abstract] [Full Text] [PDF]

				F. M. D'Souza, R. L. Sparks, H. Chen, P. J. Kadowitz, and J. R. Jeter Jr. Mechanism of eNOS gene transfer inhibition of vascular smooth muscle cell proliferation Am J Physiol Cell Physiol, January 1, 2003; 284(1): C191 - C199. [Abstract] [Full Text] [PDF]

				N. S Fearnhead, J. L Wilding, and W. F Bodmer Genetics of colorectal cancer: hereditary aspects and overview of colorectal tumorigenesis Br. Med. Bull., December 1, 2002; 64(1): 27 - 43. [Abstract] [Full Text] [PDF]

				W. C. Weinberg and M. F. Denning P21WAF1 CONTROL OF EPITHELIAL CELL CYCLE AND CELL FATE Critical Reviews in Oral Biology & Medicine, November 1, 2002; 13(6): 453 - 464. [Abstract] [Full Text] [PDF]

				J. Y. Ahn, E. Y. Jung, H. J. Kwun, C.-W. Lee, Y.-C. Sung, and K. L. Jang Dual effects of hepatitis B virus X protein on the regulation of cell-cycle control depending on the status of cellular p53 J. Gen. Virol., November 1, 2002; 83(11): 2765 - 2772. [Abstract] [Full Text] [PDF]

				M.-H. Pan, W.-J. Chen, S.-Y. Lin-Shiau, C.-T. Ho, and J.-K. Lin Tangeretin induces cell-cycle G1 arrest through inhibiting cyclin-dependent kinases 2 and 4 activities as well as elevating Cdk inhibitors p21 and p27 in human colorectal carcinoma cells Carcinogenesis, October 1, 2002; 23(10): 1677 - 1684. [Abstract] [Full Text] [PDF]

				S R McBride, N Leonard, and N J Reynolds Loss of p21WAF1 compartmentalisation in sebaceous carcinoma compared with sebaceous hyperplasia and sebaceous adenoma J. Clin. Pathol., October 1, 2002; 55(10): 763 - 766. [Abstract] [Full Text] [PDF]

				P. P. McKenzie, C. R. McPake, A. A. Ashford, E. F. Vanin, and L. C. Harris MDM2 Does Not Influence p53-mediated Sensitivity to DNA-damaging Drugs Mol. Cancer Ther., October 1, 2002; 1(12): 1097 - 1104. [Abstract] [Full Text] [PDF]

				J. Megyesi, L. Andrade, J. M. Vieira Jr., R. L. Safirstein, and P. M. Price Coordination of the cell cycle is an important determinant of the syndrome of acute renal failure Am J Physiol Renal Physiol, October 1, 2002; 283(4): F810 - F816. [Abstract] [Full Text] [PDF]

				T. Shoji, F. Tanaka, T. Takata, K. Yanagihara, Y. Otake, N. Hanaoka, R. Miyahara, T. Nakagawa, Y. Kawano, S. Ishikawa, et al. Clinical Significance of p21 Expression in Non-Small-Cell Lung Cancer J. Clin. Oncol., September 15, 2002; 20(18): 3865 - 3871. [Abstract] [Full Text] [PDF]

				A.-M. Helt, J. O. Funk, and D. A. Galloway Inactivation of both the Retinoblastoma Tumor Suppressor and p21 by the Human Papillomavirus Type 16 E7 Oncoprotein Is Necessary To Inhibit Cell Cycle Arrest in Human Epithelial Cells J. Virol., September 11, 2002; 76(20): 10559 - 10568. [Abstract] [Full Text] [PDF]

				L Leoncini, S Lazzi, C Bellan, and P Tosi Cell kinetics and cell cycle regulation in lymphomas J. Clin. Pathol., September 1, 2002; 55(9): 648 - 655. [Abstract] [Full Text] [PDF]

				X. Tang, T. Yano, Y. Osuga, H. Matsumi, N. Yano, J. Xu, O. Wada, K. Koga, K. Kugu, O. Tsutsumi, et al. Cellular Mechanisms of Growth Inhibition of Human Epithelial Ovarian Cancer Cell Line by LH-Releasing Hormone Antagonist Cetrorelix J. Clin. Endocrinol. Metab., August 1, 2002; 87(8): 3721 - 3727. [Abstract] [Full Text] [PDF]

				P. J. Smith, M. Wiltshire, S. Davies, S.-F. Chin, A. K. Campbell, and R. J. Errington DNA damage-induced [Zn2+]i transients: correlation with cell cycle arrest and apoptosis in lymphoma cells Am J Physiol Cell Physiol, August 1, 2002; 283(2): C609 - C622. [Abstract] [Full Text] [PDF]

				T. W. Perkins, B. Faha, M. Ni, J. A. Kiland, G. L. Poulsen, D. Antelman, I. Atencio, J. Shinoda, D. Sinha, L. Brumback, et al. Adenovirus-Mediated Gene Therapy Using Human p21WAF-1/Cip-1 to Prevent Wound Healing in a Rabbit Model of Glaucoma Filtration Surgery Arch Ophthalmol, July 1, 2002; 120(7): 941 - 949. [Abstract] [Full Text] [PDF]

				H. Jankala, C. J. P. Eriksson, K. K. Eklund, M. Harkonen, and T. Maki COMBINED CALCIUM CARBIMIDE AND ETHANOL TREATMENT INDUCES HIGH BLOOD ACETALDEHYDE LEVELS, MYOCARDIAL APOPTOSIS AND ALTERED EXPRESSION OF APOPTOSIS-REGULATING GENES IN RAT Alcohol Alcohol., May 1, 2002; 37(3): 222 - 228. [Abstract] [Full Text] [PDF]

				H.-J. Im, M. R. Pittelkow, and R. Kumar Divergent Regulation of the Growth-promoting Gene IEX-1 by the p53 Tumor Suppressor and Sp1 J. Biol. Chem., April 19, 2002; 277(17): 14612 - 14621. [Abstract] [Full Text] [PDF]

				S. Stromblad, A. Fotedar, H. Brickner, C. Theesfeld, E. Aguilar de Diaz, M. Friedlander, and D. A. Cheresh Loss of p53 Compensates for alpha v-Integrin Function in Retinal Neovascularization J. Biol. Chem., April 12, 2002; 277(16): 13371 - 13374. [Abstract] [Full Text] [PDF]

				D. J. Bearss, R. J. Lee, D. A. Troyer, R. G. Pestell, and J. J. Windle Differential Effects of p21WAF1/CIP1 Deficiency on MMTV-ras and MMTV-myc Mammary Tumor Properties Cancer Res., April 1, 2002; 62(7): 2077 - 2084. [Abstract] [Full Text] [PDF]

				S. T. C. Neuteboom, P. L. Karjian, C. R. Boyer, M. Beryt, M. Pegram, G. M. Wahl, and H. M. Shepard Inhibition of Cell Growth by NB1011 Requires High Thymidylate Synthase Levels and Correlates with p53, p21, Bax, and GADD45 Induction Mol. Cancer Ther., April 1, 2002; 1(6): 377 - 384. [Abstract] [Full Text] [PDF]