Induction of p21(WAF1/CIP1) and inhibition of Cdk2 mediated by the tumor suppressor p16(INK4α)

Molecular and Cellular Biology

Volumn 19, Issue 5, 1999, Pages 3916-3928

  Mitra, Jayashree ^a   Dai, Charlotte Y ^a   Somasundaram, Kumaravel ^a   El Deiry, Wafik S ^a   Satyamoorthy, Kapaettu ^b   Herlyn, Meenhard ^b   Enders, Greg H ^a,c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b WISTAR INSTITUTE   (United States)

^c Penn/GI Division   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A; CYCLIN D1; CYCLIN DEPENDENT KINASE; CYCLIN E; PROTEIN P16; PROTEIN P21; RETINOBLASTOMA PROTEIN;

ARTICLE; CANCER INHIBITION; CELL DIVISION; DNA SYNTHESIS INHIBITION; GENE CONTROL; GENE EXPRESSION; GENE INDUCTION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INHIBITION KINETICS; PRIORITY JOURNAL; PROTEIN BINDING; REGULATORY MECHANISM; TUMOR SUPPRESSOR GENE;

EID: 0032947853     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.19.5.3916     Document Type: Article

References (115)

1. INK4a in replicative senescence of normal human fibroblasts. Proc. Natl. Acad. Sci. USA 93:13742-13747.
2. INK4a and of hypophosphorylated retinoblastoma family proteins. EMBO J. 16:5322-5333.
3. Ali, A. A., J. N. Marcus, J. P. Harvey, R. Roll, C. P. Hodgson, D. M. Wildrick, A. Chakraborty, and B. M. Boman. 1993. RB1 protein in normal and malignant human colorectal tissue and colon cancer cell lines. FASEB J. 7:931-937.
4. Asamoto, M., T. Hori, H. Baba-Toriyama, M. Sano, S. Takahashi, H. Tsuda, and T. Shirai. 1998. p16 gene overexpression in mouse bladder carcinomas. Cancer Lett. 127:9-13.
5. WAF1/CIP1/SDI1 mutant (Arg94-Trp) identified in a human breast carcinoma. J. Biol. Chem. 271:15782-15786.
6. Baylin, S. B., J. G. Herman, J. R. Graff, P. M. Vertino, and J.-P. Issa. 1998. Alterations in DNA methylation: a fundamental aspect of neoplasia. Adv. Cancer Res. 72:141-196.
7. 1 arrest through reduction of cyclin E/CDK2 kinase activity. Oncogene 15:1347-1356.
8. Kip1 with cyclin A-Cdk2 and cyclin D2-Cdk4. J. Biol. Chem. 272:25863-25872.
9. Brugarolas, J., R. T. Bronson, and T. Jacks. 1998. p21 is a critical CDK2 regulator essential for proliferation control in Rb-deficient cells. J. Cell Biol. 141:503-514.
10. Brugarolas, J., C. Chandrasekaran, J. I. Gordon, D. Beach, T. Jacks, and G. J. Hannon. 1995. Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature 377:552-557.
11. Chen, J., P. Jackson, M. W. Kirschner, and A. Dutta. 1995. Separate domains of p21 involved in the inhibition of cdk kinase and PCNA. Nature 374:386-388.
12. CIP1. Mol. Cell. Biol. 16:4673-4682.
13. WAF1. Science 277:1996-2000.
14. Clurman, B. E., and M. Groudine. 1998. The CDKN2A tumor-suppressor locus - a tale of two proteins. N. Engl. J. Med. 338:910-912.
15. 14a. Dai, C. Y., and G. H. Enders. Unpublished data.
16. 1/S-regulatory genes. Mol. Cell. Biol. 15:4215-4224.
17. 1 checkpoint control. Cell 82:675-684.
18. de Nooij, J. C., M. A. Letendre, and I. K. Hariharan. 1996. A cyclin-dependent kinase inhibitor, Dacapo, is necessary for timely exit from the cell cycle during Drosophila embryogenesis. Cell 87:1237-1247.
19. 1-S phase protein kinase. Science 257:1958-1961.
20. INK4/MTS1 gene transcript expressed in B-cell malignancies. Oncogene 11:21-29.
21. Dyson, N. 1994. pRB, p107, and the regulation of the E2F transcription factor. J. Cell Sci. Suppl. 18:81-87.
22. El-Deiry, W. S. 1998. p21/p53, cellular growth control, and genomic integrity. Curr. Top. Microbiol. Immunol. 227:121-137.
23. 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.
24. Enders, G. H., D. Ganem, and H. E. Varmus. 1987. 5′-Terminal sequences influence the segregation of ground squirrel hepatitis virus RNAs into polyribosomes and viral core particles. J. Virol. 61:35-41.
25. Enders, G. H., J. Koh, C. Missero, A. K. Rustgi, and E. Harlow. 1996. p16 inhibition of transformed and primary squamous epithelial cells. Oncogene 12:1239-1245.
26. 1 cell-cycle arrest. Genes Dev. 9:204-217.
27. CDKN2/INK4A. Curr. Biol. 6:84-91.
28. Kip1-deficient mice. Cell 85:733-744.
29. Foster, S. A., D. J. Wong, M. T. Barrett, and D. A. Galloway. 1998. Inactivation of p16 in human mammary epithelial cells by CpG island methylation. Mol. Cell. Biol. 18:1793-1801.
30. Funk, J. O., S. Waga, J. B. Harry, E. Espling, B. Stillman, and D. A. Galloway. 1997. Inhibition of CDK activity and PCNA-dependent DNA replication by p21 is blocked by interaction with the HPV-16 E7 oncoprotein. Genes Dev. 11:2090-2100.
31. INK4A expression in human breast carcinoma. Am. J. Pathol. 149:15-20.
32. Gossen, M., and H. Bujard. 1992. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl. Acad. Sci. USA 89:5547-5551.
33. Graham, F. L., and L. Prevec. 1995. Methods for construction of adenovirus vectors. Mol. Biotechnol. 3:207-220.
34. Gray-Bablin, J., S. Rao, and K. Keyomarsi. 1997. Lovastatin induction of cyclin-dependent kinase inhibitors in human breast cells occurs in a cell cycle-independent fashion. Cancer Res. 57:604-609.
35. CIP1/Waf1 expression in human breast epithelial cells. Oncogene 11:253-261.
36. ARF. Cell 91:555-558.
37. CDKN2 expression and its implications for cell immortalization and senescence. Mol. Cell. Biol. 16:859-867.
38. WAF1/CIP1 in pancreatic cancer. Br. J. Cancer 76:299-305.
39. Harlow, E., and D. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
40. Helin, K., and E. Harlow. 1993. The retinoblastoma protein as a transcriptional repressor. Trends Cell Biol. 3:43-46.
41. KIP1 accumulation during the cell cycle. Science 271:1861-1864.
42. Herman, J. G., A. Merlo, R. G. Lapidus, J.-P. Issa, N. E. Davidson, D. Sidransky, and S. B. Baylin. 1995. Inactivation of the CDKN2/p16/MTS1 gene is frequently associated with aberrant DNA methylation in all common human cancers. Cancer Res. 55:4525-4530.
43. Horowitz, J. M., S. H. Park, E. Bogenmann, J. C. Cheng, D. W. Yandell, F. J. Kaye, J. D. Minna, T. P. Dryja, and R. A. Weinberg. 1990. Frequent inactivation of the retinoblastoma anti-oncogene is restricted to a subset of human tumor cells. Proc. Natl. Acad. Sci. USA 87:2775-2779.
44. INK4a-mediated growth suppression. Mol. Cell. Biol. 18: 5284-5290.
45. Cip1-mediated inhibition of cdk2. Genes Dev. 11:2101-2111.
46. Kamb, A., D. Shattuck-Eidens, R. Eeles, Q. Liu, N. A. Gruis, W. Ding, C. Hussey, T. Tran, Y. Miki, J. Weaver-Feldhaus, M. McClure, J. F. Aitken, D. E. Anderson, W. Bergman, R. Frants, D. E. Goldgar, A. Green, R. MacLennan, N. G. Martin, L. J. Meyer, P. Youl, J. J. Zone, M. H. Scolnick, and L. A. Cannon-Albright. 1994. Analysis of the p16 gene (cdkN2) as a candidate for the chromosome 9p melanoma susceptibility locus. Nat. Genet. 8:22-26.
47. Kamb, A., N. A. Gruis, J. Weaver-Feldhaus, Q. Liu, K. Harshman, S. V. Tavtigian, E. Stockert, R. S. Day, B. E. Johnson, and M. H. Skolnick. 1994. A cell cycle regulator potentially involved in genesis of many tumor types. Science 264:436-440.
48. ARF. Cell 91:649-660.
49. INK4A fusion protein to human diploid fibroblasts. FEBS Lett. 427:203-208.
50. 1 to multiple cell cycles by lovastatin. Cancer Res. 51:3602-3609.
51. Kip1. Cell 85:721-732.
52. Knoblich, J., K. Sauer, L. Jones, H. Richardson, R. Saint, and C. Lehner. 1994. Cyclin E controls S phase progression and its down-regulation during Drosophila embryogenesis is required for the arrest of cell proliferation. Cell 77:107-120.
53. Koh, J., G. H. Enders, B. D. Dynlacht, and E. Harlow. 1995. Tumor-derived p16 alleles encoding proteins defective in cell cycle inhibition. Nature 375: 506-510.
54. LaBaer, J., M. D. Garret, L. F. Stevenson, J. M. Slingerland, C. Sandhu, H. S. Chou, A. Fattaey, and E. Harlow. 1997. New functional activities for the p21 family of cdk inhibitors. Genes Dev. 11:847-862.
55. Lane, M. E., K. Sauer, K. Wallace, Y. N. Jan, C. F. Lehner, and H. Vaessin. 1996. Dacapo, a cyclin-dependent kinase inhibitor, stops cell proliferation during Drosophila development. Cell 87:1225-1235.
56. Lees, E., B. Faha, V. Dulic, S. I. Reed, and E. Harlow. 1992. Cyclin E/cdk2 and cyclin A/cdk2 kinases associate with p107 and E2F in a temporally distinct manner. Genes Dev. 6:1874-1885.
57. Liggett, W. H., Jr., D. A. Sewell, J. Rocco, S. A. Ahrendt, W. Koch, and D. Sidransky. 1996. p16 and p16 beta are potent growth suppressors of head and neck squamous carcinoma cells in vitro. Cancer Res. 56:4119-4123.
58. Lukas, J., T. Herzinger, K. Hansen, M. C. Moroni, D. Resnitzky, K. Helin, S. I. Reed, and J. Bartek. 1997. Cyclin E-induced S phase without activation of the pRB/E2F pathway. Genes Dev. 11:1479-1492.
59. Lukas, J., D. Parry, L. Aagaard, D. J. Mann, J. Bartkova, M. Strauss, G. Peters, and J. Bartek. 1995. Retinoblastoma-protein-dependent inhibition by the tumor-suppressor p16. Nature 375:503-506.
60. Lundberg, A. S., and R. A. Weinberg. 1998. Functional inactivation of the retinoblastoma protein requires sequential modification by at least two distinct cyclin-cdk complexes. Mol. Cell. Biol. 18:753-761.
61. Cip1. Nature 375:159-161.
62. WAF1/CIP1 mutations in superficial and invasive transitional cell carcinomas. Oncogene 13:1831-1837.
63. 1 cell cycle arrest. Curr. Biol. 6:474-483.
64. INK4A transcript. Cancer Res. 55:2995-2997.
65. Mathews, M., N. Sonnenburg, and J. Hershey. 1996. Origins and targets of translational control, p. 1-29. In J. Hershey, M. Mathews, and N. Sonnenburg (ed.), Translational control, 2nd ed., vol. 1. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
66. INK4a inhibits both CDK4- and CDK2-associated kinase activity by reassortment of cyclin-CDK-inhibitor complexes. Mol. Cell. Biol. 19:1981-1989.
67. McConnell, B. B., M. Starborg, S. Brookes, and G. Peters. 1998. Inhibitors of cyclin-dependent kinases induce features of replicative senescence in early passage human diploid fibroblasts. Curr. Biol. 8:351-354.
68. ink4 requires functional retinoblastoma protein. Proc. Natl. Acad. Sci. USA 92:6289-6293.
69. 1 kinase activity for cdk6, a novel cyclin D partner. Mol. Cell. Biol. 14:2077-2086.
70. Kip1 mRNA is a mechanism contributing to accumulation during growth arrest. J. Biol. Chem. 272: 7093-7098.
71. Cip1/WAF1 alters keratinocyte growth and differentiation. Genes Dev. 10:3065-3075.
72. Mitra, J., and G. H. Enders. Unpublished data.
73. ink4A alleles in neoplasia. Cancer Res. 58:591-593.
74. Kip1 display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell 85:707-720.
75. Nobori, T., K. Miura, D. J. Wu, A. Lois, K. Takabayashi, and D. A. Carson. 1994. Deletions of the cyclin-dependent kinase-4 inhibitor gene in multiple human cancers. Nature 368:753-756.
76. Noda, A., Y. Ning, S. F. Venable, O. M. Pereira-Smith, and J. R. Smith. 1994. Cloning of senescent cell-derived inhibitors of DNA synthesis using an expression screen. Exp. Cell Res. 211:90-98.
77. 1-to-S phase transition. Mol. Cell. Biol. 15:2612-2624.
78. Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell 78:59-66.
79. 1 cyclin CLN3 in yeast. Genes Dev. 11:2522-2531.
80. Arf, interacts with MDM2 and neutralizes MDM2's inhibition of p53. Cell 92:713-723.
81. Poon, R. Y. C., and T. Hunter. 1995. Dephosphorylation of Cdk2 Thr-160 by the cyclin-dependent kinase-interacting phosphatase KAP in the absence of cyclin. Science 270:90-93.
82. ARF. Proc. Natl. Acad. Sci. USA 94:669-673.
83. Quelle, D. E., F. Zindy, R. A. Ashmun, and C. J. Sherr. 1995. Alternative reading frames of the INK4a tumor suppressor gene encode two unrelated proteins capable of inducing cell cycle arrest. Cell 83:993-1000.
84. Kip1 coordinate their inhibitory interactions with cdk4 and cdk2. Genes Dev. 11:492-503.
85. Reynisdottir, I., K. Polyak, A. Iavarone, and J. Massague. 1995. Kip/Cip and Ink4 Cdk inhibitors cooperate to induce cell cycle arrest in response to TGF-β. Genes Dev. 9:1831-1845.
86. Reznikoff, C. A., T. R. Yeager, C. D. Belair, E. Savelia, J. A. Puthenveetil, and W. M. Stadler. 1996. Elevated p16 at senescence and loss of p16 at immortalization in human papillomovirus 16 E6, but not E7, transformed human uroepithelial cells. Cancer Res. 56:2886-2890.
87. Robertson, K. D., and P. A. Jones. 1998. The human ARF cell cycle regulatory gene promoter is a CpG island which can be silenced by DNA methylation and down-regulated by wild-type p53. Mol. Cell. Biol. 18:6457-6473.
88. INK4 expression and telomere length during spontaneous immortalization of Li-Fraumeni syndrome fibroblasts. Mol. Cell. Biol. 15:4745-4753.
89. Rogatsky, I., J. M. Trowbridge, and M. J. Garabedian. 1997. Glucocorticoid receptor-mediated cell cycle arrest is achieved through distinct cell-specific transcriptional regulatory mechanisms. Mol. Cell. Biol. 17:3181-3193.
90. 1-S progression from an associated transcriptional program. Genes Dev. 11:1999-2011.
91. INK4a. Nature 395:237-243.
92. Kip1 cyclin dependent kinase inhibitor bound to the cyclin A-Cdk2 complex. Nature 382:325-331.
93. Sambrook, J., E. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed., vol. 1. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
94. INK4/CDKN2 and p53 cooperate to induce apoptotic tumor cell death. Nat. Med. 3:313-319.
95. Satyamoorthy, K., M. Nesbit, M.-Y. Hsu, and M. Hertyn. 1996. Utility of adenoviruses as gene expression modules in melanoma, p. 71-77. In M. Maio (ed.), Immunology of human melanoma. IOS Press, Amsterdam, The Netherlands.
96. Satyamoorthy, K., P. W. Soballe, F. Soans, and M. Hertyn. 1997. Adenovirus infection enhances killing of melanoma cells by a mitotoxin. Cancer Res. 57:1873-1876.
97. INK4. Science 267:249-252.
98. Serrano, M., G. J. Hannon, and D. Beach. 1993. A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature 366:704-707.
99. Cip1. Mol. Cell. Biol. 17:5588-5597.
100. Sherr, C. J. 1996. Cancer cell cycles. Science 274:1672-1677.
101. Soos, T. J., H. Klyokawa, J. S. Yan, M. S. Rubin, A. Giordano, A. DeBlasio, S. Bottega, B. Wong, J. Mendelsohn, and A. Koff. 1996. Formation of p27-CDK complexes during the human mitotic cell cycle. Cell Growth Differ. 7:135-146.
102. Stone, S., P. Jiang, P. Dayananth, S. V. Tavtigian, H. Katcher, D. Parry, G. Peters, and A. Kamb. 1995. Complex structure and regulation of the P16 (MTS1) locus. Cancer Res. 55:2988-2994.
103. 1-to-S transition in mammalian cells. Oncogene 8:1593-1602.
104. INK4A. Oncogene 15:505-514.
105. van den Heuvel, S., and E. Harlow. 1993. Distinct roles for cyclin-dependent kinases in cell cycle control. Science 262:2050-2054.
106. 1 arrest in human cancer cells. Cancer Res. 55:5187-5190.
107. Wang, J., and K. Walsh. 1996. Resistance to apoptosis conferred by Cdk inhibitors during myocyte differentiation. Science 273:359-361.
108. Weinberg, R. A. 1995. The retinoblastoma protein and cell cycle control. Cell 81:323-330.
109. 1. Mol. Cell. Biol. 16:3698-3706.
110. 1 cyclin-associated kinases. Proc. Natl. Acad. Sci. USA 93:4633-4637.
111. Xiong, Y., H. Zhang, and D. Beach. 1993. Subunit rearrangement of the cyclin-dependent kinases is associated with cellular transformation. Genes Dev. 7:1572-1583.
112. Zhang, H., G. J. Hannon, and D. Beach. 1994. p21-containing cyclin kinases exist in both active and inactive states. Genes Dev. 8:1750-1758.
113. Zhang, Y., Y. Xiong, and W. G. Yarbrough. 1998. ARF promotes MDM2 degradation and stabilizes p53: ARF-INK4a locus deletion impairs both the Rb and p53 tumor suppression pathways. Cell 92:725-734.
114. Zindy, F., C. Eischen, D. Randle, T. Kamijo, J. Cleveland, C. Sherr, and M. Roussel. 1998. Myc signalling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev. 12:2424-2433.
115. INK4a tumor suppressor versus other INK4 family members during mouse development and aging. Oncogene 15:203-211.