p21 is a critical CDK2 regulator essential for proliferation control in Rb-deficient cells

Journal of Cell Biology

Volumn 141, Issue 2, 1998, Pages 503-514

  Brugarolas, James ^a   Bronson, Roderick T ^c   Jacks, Tyler ^a,b,d  

^a Center for Cancer Research   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c TUFTS UNIVERSITY   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE INHIBITOR; PROTEIN P21; UNCLASSIFIED DRUG;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL CYCLE G1 PHASE; CELL PROLIFERATION; CONTACT INHIBITION; EMBRYO; ENZYME REGULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BLOOD; CDC2-CDC28 KINASES; CELL ADHESION; CELL COMMUNICATION; CELL CYCLE; CELL CYCLE PROTEINS; CELL DIVISION; CELL SIZE; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; CYCLIN D1; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASE 4; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASE INHIBITOR P27; CYCLIN-DEPENDENT KINASES; CYCLINS; ENZYME INHIBITORS; FIBROBLASTS; G1 PHASE; MICE; MICE, KNOCKOUT; MICE, NUDE; MICROTUBULE-ASSOCIATED PROTEINS; MUTATION; NEOPLASMS, EXPERIMENTAL; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; RETINOBLASTOMA PROTEIN; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

ANIMALIA; MAMMALIA; MUS MUSCULUS;

EID: 0032550224     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.141.2.503     Document Type: Article

References (83)

1. Assoian, R.K. 1997. Anchorage-dependent cell cycle progression. J. Cell Biol. 136:1-4.
2. Baldin, V., J. Lukas, M.J. Marcote, M. Pagano, and J. Draetta. 1993. Cyclin D1 is a nuclear protein required for progression in G1. Genes Dev. 7:812-821.
3. Bohmer, R., E. Scharf, and R.K. Assoian. 1996. Cytoskeletal integrity is required throughout the mitogen stimulation phase of the cell cycle and mediates anchorage-dependent expression of cyclin D1. Mol. Biol. Cell. 7:101-111.
4. 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.
5. Chellappan, S.P., S. Hiebert, M. Mudryj, J.M. Horowitz, and J.R. Nevins. 1991. The E2F transcription factor is a cellular target for the RB protein. Cell. 65: 1053-1061.
6. Coats, S., W.M. Flanagan, J. Nourse, and J.M. Roberts. 1996. Requirement of p27Kip1 for restriction control of fibroblast cell cycle. Science. 272:877-880.
7. CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell. 82:675-684.
8. Dulbecco, R. 1970. Topoinhibition and serum requirement of transformed and untransformed cells. Nature. 227:802-806.
9. Duronio, R.J., and P.H. O'Farrell. 1995. Developmental control of the G1 to S transition in Drosophila: cyclin E is a limiting downstream target of E2F. Genes Dev. 9:1456-1464.
10. El-Deiry, W.S., T. Tokino, V.E. Velculescu, D.B. Levy, R. Parsons, J.M. Trent, D. Lin, W.E. Mercer, K. Kinzler, and B. Vogelstein. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell. 75:817-825.
11. Fang, F., G. Orend, N. Watanabe, T. Hunter, and E. Ruoslahti. 1996. Dependence of cyclin E-cdk2 kinase activity on cell anchorage. Science. 271:499-502.
12. Freedman, V.H., and S. Shin. 1974. Cellular tumorigenicity in nude mice: correlation with cell growth in semi-solid medium. Cell. 3:355-359.
13. Green, H., and K. Nilausen. 1962. Repression of growth of mammalian cells under agar. Nature. 194:406-407.
14. Gu, Y., W. Turck, and D.O. Morgan. 1993. Inhibition of cdk2 activity in vivo by an associated 20K regulatory subunit. Nature. 366:707-710.
15. Guadagno, T.M., and R.K. Assoian. 1991. G1/S control of anchorage-independent growth in the fibroblast cell cycle. J. Cell Biol. 115:1419-1425.
16. Guadagno, T.M., M. Ohtsubo, J.M. Roberts, and R.K. Assoian. 1993. A link between cyclin A expression and adhesion-dependent cell cycle progression. Science. 262:1572-1575.
17. 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 kinases. Cell. 75:805-816.
18. Harper, J.W., S.J. Elledge, K. Keyomarsi, B. Dynlacht, L. Tsai, P. Zhang, S. Dobrowolski, C. Bai, L. Connell-Crowley, E. Swindell, et al. 1995. Inhibition of cyclin-dependent kinases by p21. Mol. Biol. Cell. 6:387-400.
19. Harvey, M., H. Vogel, E.Y. Lee, A. Bradley, and L.A. Donehauer. 1995. Mice deficient in both p53 and Rb develop tumors primarily of endocrine origin. Cancer Res. 55:1146-1151.
20. Herrera, R.E., V.P. Sah, B.O. Williams, R.A. Weinberg, and T. Jacks. 1996. Altered cell cycle kinetics, gene expression and G1 restriction point regulation in Rb-deficient fibroblasts. Mol. Cell Biol. 16:2402-2407.
21. Hirama, T., and H.P. Koeffler. 1995. Role of the cyclin-dependent kinase inhibitors in the development of cancer. Blood. 86:841-854.
22. Hiyama, H., A. Iavarone, J. LaBaer, and S.A. Reeves. 1997. Regulated ectopic expression of cyclin D1 induces transcriptional activation of the cdk inhibitor p21 gene without altering cell cycle progression. Oncogene. 14:2533-2542.
23. Holley, R.W., and J.A. Kiernan. 1968. "Contact inhibition" of cell division in 3T3 cells. Proc. Natl Acad. Sci. USA. 60:300-304.
24. Jacks, T., A. Fazeli, E. Schmidt, R. Bronson, M. Goodell, and R.A. Weinberg. 1992. Effects of an Rb mutation in the mouse. Nature. 359:295-300.
25. Jainchill, J.L., and G.J. Todaro. 1970. Stimulation of cell growth in vitro by serum and without growth factor. Exp. Cell Res. 59:137-146.
26. Johnson, D.G., J.K. Schwarz, W.D. Cress, and J.R. Nevins. 1993. Expression of transcription factor E2F1 induces quiescent cells to enter S phase. Nature. 365:349-352.
27. Keyomarsi, K., and A.B. Pardee. 1993. Redundant cyclin expression and gene amplification in breast cancer cells. Proc. Natl. Acad. Sci. USA. 90:1112-1116.
28. Kitahara, K., W. Yasui, H. Kuniyasu, H. Yokozaki, Y. Akama, S. Yunotani, T. Hisatsugu, and E. Tahara. 1995. Concurrent amplification of cyclin E and CDK2 genes in colorectal carcinomas. Int. J. Cancer. 62:25-28.
29. 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.
30. Lowe, S.W., T. Jacks, D.E. Housman, and H.E. Ruley. 1994. Abrogation of oncogene-associated apoptosis allows transformation of p53-deficient cells. Proc. Natl. Acad. Sci. USA. 91:2026-2030.
31. Lukas, J.H., H. Muller, J. Bartkova, D. Spitkovsky, A.A. Kjerulff, P. Jansen-Dun, M. Strauss, and J. Bartek. 1994. DNA tumor virus oncoproteins and retinoblastoma gene mutations share the ability to relieve the cell's requirements for cyclin D1 function in G1. J. Cell Biol. 125:625-638.
32. Lukas, J.B., M. Rohde, M. Strauss, and J. Bartek. 1995. Cyclin D1 is dispensable for G1 control in retinoblastoma gene-deficient cells independently of cdk4 activity. Mol. Cell. Biol. 15:2600-2611.
33. Macleod, K.F., N. Sherry, G.J. Hannon, D. Beach, T. Tokino, K. Kinzler, B. Vogelstein, and T. Jacks. 1995. p53 dependent and independent expression of p21 during cell growth, differentiation and DNA damage. Genes Dev. 9:935-944.
34. MacPherson, I., and L. Montagnier. 1964. Agar suspension culture for the selective assay of cells transformed by polyoma virus. Virology. 23:291-294.
35. Matsushime, H., M.F. Roussel, R.A. Ashmun, and C.J. Sherr. 1991. Colony-stimulating factor 1 regulates novel cyclins during the G1 phase of the cell cycle. Cell. 65:701-713.
36. Matsushime, H., D.E. Quelle, S.A. Shurtleff, M. Shibuya, C.J. Sherr, and J.Y. Kato. 1994. D-type cyclin-dependent kinase activity in mammalian cells. Mol. Cell. Biol. 14:2066-2076.
37. Matsushisa, T., and Y. Mori. 1981. An anchorage-dependent locus in the cell cycle for the growth of 3T3 cells. Exp. Cell Res. 135:393-398.
38. Missero, C., F.D. Cunto, H. Kiyokawa, A. Koff, and P. Dotto. 1996. The absence of p21Cip1/Waf1 alters keratinocyte growth and differentiation and promotes ras-tumor progression. Genes Dev. 10:3065-3075.
39. Morgan, D.O. 1995. Principles of cdk regulation. Nature. 374:131-134.
40. Nakayama, K., N. Ishida, M. Shirame, A. Inomata, T. Inoue, N. Shishido, I. Horii, D.Y. Loh, and K. Nakayama. 1996. Mice lacking p27 (Kip1) display an increased body size, multiple organ hyperplasia, retinal dysplasia and pituitary tumors. Cell. 85:707-720.
41. Nilausen, K., and H. Green. 1965. Reversible arrest of growth in G1 of an established cell fibroblast line (3T3). Exp. Cell Res. 40:166-168.
42. Noda, A., Y. Ning, S.F. Venable, O.M. Pereira-Smith, and J.R. Smith. 1994. Cloning of Senescence cell-derived inhibitors of DNA synthesis using an expression screen. Exp. Cell Res. 211:90-98.
43. 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.
44. Ohtsubo, M., and J.M. Roberts. 1993. Cyclin-dependent regulation of G1 in mammalian fibroblasts. Science. 259:1908-1912.
45. 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.
46. Otsuka, H., and M. Moskowitz. 1975. Arrest of 3T3 cells in G1 phase in suspension culture. J. Cell. Phys. 87:213-220.
47. Pagano, M., R. Pepperkok, J. Lukas, V. Baldin, W. Ansorge, J. Bartek, and G. Draetta. 1993. Regulation of the cell cycle by the cdk2 protein kinase in cultured human fibroblasts. J. Cell Biol. 121:101-111.
48. Pardee, A.B. 1989. G1 events and regulation of cell proliferation. Science. 246: 603-608.
49. Peeper, D.S., T.M. Upton, M.H. Ladha, E. Neuman, J. Zalvide, R. Bernards, J.A. DeCaprio, and M.E. Ewen. 1997. Ras signaling linked to the cell-cycle machinery by the retinoblastoma protein. Nature. 386:177-181.
50. Peter, M., and I. Herskowitz. 1994. Joining the complex: cyclin-dependent kinase inhibitory proteins and the cell cycle. Cell. 79:181-184.
51. Polyak, K., M.-H. Lee, H. Erdjument-Bromage, A. Koff, J.M. Roberts, P. Tempst, and J. Massague. 1994a. Cloning of p27 KIP1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell. 78:59-66.
52. Polyak, K., J.Y. Kato, M.J. Solomon, C.J. Sherr, J. Massague, J.M. Roberts, and A. Koff. 1994b. p27Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-beta and contact inhibition to cell cycle arrest. Genes Dev. 8:9-22.
53. Ponten, J. 1976. The relationship between in vitro transformation and tumor formation in vivo. Biochim. Biophys. Acta. 458:397-422.
54. Porter, P.L., K.E. Malone, P.J. Heagerty, G.M. Alexander, L.A Gatti, E.J. Firpo, J.R. Daling, and J.M Roberts. 1997. Expression of cell-cycle regulators p27Kipl and cyclin E, alone and in combination, correlate with survival in young breast cancer patients. Nat. Med. 3:222-225,
55. Quelle, D.E., R.A. Ashmun, S.A. Shurtleff, J. Kato, D. Bar-Sagi, M.F. Roussel, and C.J. Sherr. 1993. Overexpression of mouse D-type cyclins accelerates G1 phase in rodent fibroblasts. Genes Dev. 7:1559-1571.
56. Resnitzky, D., M. Gossen, H. Bujard, and S.I. Reed. 1994. Acceleration of the G1 to S phase transition by expression of cyclin D1 and E with an inducible system. Mol. Cell. Biol. 14:1669-1679.
57. Resnitzky, D., and S. Reed. 1995. Different roles for cyclins D1 and E in regulation of the G1 to S transition. Mol. Cell. Biol. 15:3463-3469.
58. Rivard, N., G. L'Allemain, J. Bartek, and J. Poyssegur. 1996. Abrogation of p27Kip1 by cDNA antisense suppresses quiescence (G0 state) in fibroblasts. J. Biol. Chem. 271:18337-18341.
59. Sanders, F.K., and B.O. Burford. 1964. Ascites tumours from BHK.21 cells transformed in vitro by polyoma virus. Nature. 201:786-789.
60. Serrano, M., H-W. Lee, L. Chin, C. Cordon-Cardo, D. Beach, and R.A. DePinho. 1996. Role of the INK4a locus in tumor suppression and cell mortality. Cell. 85:27-37.
61. Serrano, M., A.W. Lin, M.E. McCurrach, D. Beach and S.W. Lowe. 1997. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16ink4. Cell. 88:593-602.
62. Sherr, C.J. 1994. G1 phase progression: cyclin on cue. Cell. 79:551-555.
63. Sherr, C.J. 1995. D-type cyclins. Trends Biochem. Sci. 20:187-190.
64. Sherr, C.J. 1996. Cancer cell cycles. Science. 274:1672-1677.
65. Sherr, C.J., and Roberts, J.M. 1995. Inhibitors of mammalian cyclin-dependent kinases. Genes Dev. 9:1149-1163.
66. Slebos, R.J.C., M.H. Lee, B.S. Plunkett, T.D. Kessis, B.O. Williams, T. Jacks, L. Hedrick, M.B. Kastan, and K.R. Cho. 1994. p53-dependent G1 arrest involves pRb related proteins and is disrupted by the human papilloma virus 16 E7 oncoprotein. Proc. Natl. Acad. Sci. USA. 91:5320-5324.
67. Smets, L.A. 1979. Cell transformation as a model for tumor induction and neoplastic growth. Biochim. Biophys. Acta. 605:93-111.
68. Stoker, M., C. O'Neill, S. Berryman, and V. Waxman. 1968. Anchorage and growth regulation in normal and virus-transformed cells. Int. J. Cancer. 3:683-693.
69. Temin, H.M., and H. Rubin. 1958. Characteristcs of an assay for Rous sarcoma virus and Rous sarcoma cells in tissue culture. Virology. 6:669-688.
70. Todaro, G., H. Green, and B.D. Goldberg. 1963. Transformation of properties of an established cell line by SV40 and polyoma virus. Proc. Natl. Acad. Sei. USA. 51:66-73.
71. Todaro, G.J., O.K. Lazar, and H. Green. 1965. The initiation of cell division in a contact-inhibited mammalian cell line. J. Cell. Comp. Physiol. 66:325-334.
72. Toyoshima, H., and T. Hunter. 1994. p27, a novel inhibitor of G1 cyclin-cdk protein kinase activity, is related to p21. Cell. 78:67-74.
73. Vogt, M., and R. Dulbecco. 1963. Steps in transformation of hamster embryo cells by Polyoma virus. Proc. Natl. Acad. Sci. USA. 49:171-179.
74. Weinberg, R.A. 1995. The retinoblastoma protein and cell cycle control. Cell. 81:323-330.
75. Williams, B.O., L. Remington, R.T. Bronson, S. Mukai, D.M. Albert, T. Dryja, and T. Jacks. 1994. Cooperative tumorigenic effects of germline mutations in Rb and p53. Nat. Genet. 7:480-484.
76. Williams, B.O., E. Schmitt, L. Remington, R.T. Bronson, D.M. Albert, R.A. Weinberg, and T. Jacks. 1994. Extensive contribution of Rb-deficient cells to adult chimeric mice with limited histopathological consequences. EMBO (Eur. Mol. Biol. Organ.) J. 13:4251-4259.
77. Won, K., Y. Xiong, D. Beach, and M.Z. Gilman. 1992. Growth-regulated expression of D-type cyclin genes in human diploid fibroblasts. Proc. Natl. Acad. Sci. USA. 89:9910-9914.
78. Xiong, Y., H. Zhang, and D. Beach. 1992. D type cyclins associate with multiple protein kinases and the DNA replication factor PCNA. Cell. 71:505-514.
79. Xiong, Y., G.J. Hannon, H. Zhang, D. Casso, R. Kobayashi, and D. Beach. 1993a. p21 is a universal inhibitor of cyclin kinases. Science. 366:701-704.
80. Xiong, Y., H. Zhang, and D. Beach. 1993b. Subunit rearrangement of cyclin-dependent kinases is associated with cellular transformation. Genes Dev. 7:1572-1583.
81. Zhang, H., G.J. Hannon, D. Casso, and D. Beach. 1994. p21 is a component of active cell cycle kinases. Cold Spring Harbor Symp. Quant. Biol. 59:21-29.
82. 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.
83. Zhu, X., M. Ohtsubo, R.M. Bohmer, J.M. Roberts, and R.K. Assoian. 1996. Adhesion-dependent cell cycle progression linked to the expression of cyclin D1, activation of cyclin E-cdk2, and phophorylation of the retinoblastoma protein. J. Cell Biol. 133:391-403.