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p21 Is Necessary for the p53-mediated G₁ Arrest in Human Cancer Cells¹

The Johns Hopkins Oncology Center and the Program in Human Genetics and Molecular Biology, Baltimore, Maryland 21231 [T. W., K. W. K., B. V.], and The Howard Hughes Medical Institute, Baltimore, Maryland 21231 [B. V.]

DNA-damaging agents induce a p53-dependent G₁ arrest that may be critical for p53-mediated tumor suppression. It has been suggested that p21^WAF1/CIP1, a cdk inhibitory protein transcriptionally regulated by p53, is an effector of this arrest. To test this hypothesis, an isogenic set of human colon adenocarcinoma cell lines differing only in their p21 status was created. The parental cell line underwent the expected cell cycle changes upon induction of p53 expression by DNA damage, but the G₁ arrest was completely abrogated in p21-deficient cells. These results unambiguously establish p21 as a critical mediator of one well-documented p53 function and have important implications for understanding cell cycle checkpoints and the mechanism(s) through which p53 inhibits human neoplasia.

¹ This work was supported by NIH Grants CA43460 and GM07184. B. V. is an Investigator of the Howard Hughes Medical Institute.

² To whom requests for reprints should be addressed, at The Johns Hopkins Oncology Center, 424 North Bond Street, Baltimore, MD 21231. Phone: (410) 955-8878; Fax (410) 955-0548.

Received 9/12/95. Accepted 10/ 5/95.

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				G. Nowak, P. M. Price, and R. G. Schnellmann Lack of a functional p21WAF1/CIP1 gene accelerates caspase-independent apoptosis induced by cisplatin in renal cells Am J Physiol Renal Physiol, September 1, 2003; 285(3): F440 - F450. [Abstract] [Full Text] [PDF]

				T. Efferth, A. Sauerbrey, A. Olbrich, E. Gebhart, P. Rauch, H. O. Weber, J. G. Hengstler, M.-E. Halatsch, M. Volm, K. D. Tew, et al. Molecular Modes of Action of Artesunate in Tumor Cell Lines Mol. Pharmacol., August 1, 2003; 64(2): 382 - 394. [Abstract] [Full Text] [PDF]

				L. Zeng, Y. Zhang, S. Chien, X. Liu, and J. Y.-J. Shyy The Role of p53 Deacetylation in p21Waf1 Regulation by Laminar Flow J. Biol. Chem., June 27, 2003; 278(27): 24594 - 24599. [Abstract] [Full Text] [PDF]

				N. T.V. Le and D. R. Richardson Potent iron chelators increase the mRNA levels of the universal cyclin-dependent kinase inhibitor p21CIP1/WAF1, but paradoxically inhibit its translation: a potential mechanism of cell cycle dysregulation Carcinogenesis, June 1, 2003; 24(6): 1045 - 1058. [Abstract] [Full Text] [PDF]

				P. V. Jallepalli, C. Lengauer, B. Vogelstein, and F. Bunz The Chk2 Tumor Suppressor Is Not Required for p53 Responses in Human Cancer Cells J. Biol. Chem., May 30, 2003; 278(23): 20475 - 20479. [Abstract] [Full Text] [PDF]

				J. Ahn, M. Urist, and C. Prives Questioning the Role of Checkpoint Kinase 2 in the p53 DNA Damage Response J. Biol. Chem., May 30, 2003; 278(23): 20480 - 20489. [Abstract] [Full Text] [PDF]

				R. M. Douglas and G. G. Haddad Genetic Models in Applied Physiology: Invited Review: Effect of oxygen deprivation on cell cycle activity: a profile of delay and arrest J Appl Physiol, May 1, 2003; 94(5): 2068 - 2083. [Abstract] [Full Text] [PDF]

				C. D. Braastad, Z. Han, and E. A. Hendrickson Constitutive DNase I Hypersensitivity of p53-Regulated Promoters J. Biol. Chem., February 28, 2003; 278(10): 8261 - 8268. [Abstract] [Full Text] [PDF]

				J. Yu, Z. Wang, K. W. Kinzler, B. Vogelstein, and L. Zhang PUMA mediates the apoptotic response to p53 in colorectal cancer cells PNAS, February 18, 2003; 100(4): 1931 - 1936. [Abstract] [Full Text] [PDF]

				H.-L. Yang, J.-X. Pan, L. Sun, and S.-C. J. Yeung p21 Waf-1 (Cip-1) Enhances Apoptosis Induced by Manumycin and Paclitaxel in Anaplastic Thyroid Cancer Cells J. Clin. Endocrinol. Metab., February 1, 2003; 88(2): 763 - 772. [Abstract] [Full Text] [PDF]

				A. Wang, J. Gu, K. Judson-Kremer, K.L. Powell, H. Mistry, P. Simhambhatla, C. M. Aldaz, S. Gaddis, and M. C. MacLeod Response of human mammary epithelial cells to DNA damage induced by BPDE: involvement of novel regulatory pathways Carcinogenesis, February 1, 2003; 24(2): 225 - 234. [Abstract] [Full Text] [PDF]

				H. S. Yoon, X. Chen, and V. W. Yang Kruppel-like Factor 4 Mediates p53-dependent G1/S Cell Cycle Arrest in Response to DNA Damage J. Biol. Chem., January 17, 2003; 278(4): 2101 - 2105. [Abstract] [Full Text] [PDF]

				S. Polager and D. Ginsberg E2F Mediates Sustained G2 Arrest and Down-regulation of Stathmin and AIM-1 Expression in Response to Genotoxic Stress J. Biol. Chem., January 10, 2003; 278(3): 1443 - 1449. [Abstract] [Full Text] [PDF]

				T. C. Polek, L. V. Stewart, E. J. Ryu, M. B. Cohen, E. A. Allegretto, and N. L. Weigel p53 Is Required for 1,25-Dihydroxyvitamin D3-Induced G0 Arrest But Is Not Required for G1 Accumulation or Apoptosis of LNCaP Prostate Cancer Cells Endocrinology, January 1, 2003; 144(1): 50 - 60. [Abstract] [Full Text] [PDF]

				P. Russo, D. Arzani, S. Trombino, and C. Falugi c-myc Down-Regulation Induces Apoptosis in Human Cancer Cell Lines Exposed to RPR-115135 (C31H29NO4), a Non-Peptidomimetic Farnesyltransferase Inhibitor J. Pharmacol. Exp. Ther., January 1, 2003; 304(1): 37 - 47. [Abstract] [Full Text] [PDF]

				L. A. McPherson, A. V. Loktev, and R. J. Weigel Tumor Suppressor Activity of AP2alpha Mediated through a Direct Interaction with p53 J. Biol. Chem., November 15, 2002; 277(47): 45028 - 45033. [Abstract] [Full Text] [PDF]

				A. Mauser, S.'i. Saito, E. Appella, C. W. Anderson, W. T. Seaman, and S. Kenney The Epstein-Barr Virus Immediate-Early Protein BZLF1 Regulates p53 Function through Multiple Mechanisms J. Virol., November 13, 2002; 76(24): 12503 - 12512. [Abstract] [Full Text] [PDF]

				L. A. Martinez, I. Naguibneva, H. Lehrmann, A. Vervisch, T. Tchenio, G. Lozano, and A. Harel-Bellan Synthetic small inhibiting RNAs: Efficient tools to inactivate oncogenic mutations and restore p53 pathways PNAS, November 12, 2002; 99(23): 14849 - 14854. [Abstract] [Full Text] [PDF]

				H. Zhang, X. Shi, Q.-J. Zhang, M. Hampong, H. Paddon, D. Wahyuningsih, and S. Pelech Nocodazole-induced p53-dependent c-Jun N-terminal Kinase Activation Reduces Apoptosis in Human Colon Carcinoma HCT116 Cells J. Biol. Chem., November 8, 2002; 277(46): 43648 - 43658. [Abstract] [Full Text] [PDF]

				C. Leger and E. A. Drobetsky Modulation of the DNA damage response in UV-exposed human lymphoblastoid cells through genetic-versus functional-inactivation of the p53 tumor suppressor Carcinogenesis, October 1, 2002; 23(10): 1631 - 1640. [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]

				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]

				D. Javelaud and F. Besancon Inactivation of p21WAF1Sensitizes Cells to Apoptosis via an Increase of Both p14ARF and p53 Levels and an Alteration of the Bax/Bcl-2 Ratio J. Biol. Chem., September 27, 2002; 277(40): 37949 - 37954. [Abstract] [Full Text] [PDF]