Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16(INK4a)

Cell

Volumn 88, Issue 5, 1997, Pages 593-602

  Serrano, Manuel ^a,b,c   Lin, Athena W ^a   McCurrach, Mila E ^a   Beach, David ^a,b   Lowe, Scott W ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN KINASE; PROTEIN P16; PROTEIN P53;

ANIMAL CELL; ARTICLE; CELL AGING; CELL TRANSFORMATION; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN CELL; MITOSIS INHIBITION; NONHUMAN; ONCOGENE RAS; PRIORITY JOURNAL;

ANIMALIA; RODENTIA;

EID: 0030944985     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81902-9     Document Type: Article

References (73)

1. Afshari, C.A., Vojta, P.J., Annab, L.A., Futreal, P.A., Willard, T.B., and Barrett, J.C. (1993). Investigation of the role of G1/S cell cycle mediators in cellular senescence. Exp. Cell Res. 209, 231-237
2. . Alcorta, D.A., Xiong, Y., Phelps, D., Hannon, G., Beach, D., and Barrett, J.C. (1996). Involvement of the cyclin-dependent kinase inhibitor p16 (INK4a) in replicative senescence of normal human fibroblasts. Proc. Natl. Acad. Sci. USA 93, 13742-13747.
3. Atadja, P., Wong, H., Garkavtsev, I., Veillette, C., and Riabowol, K. (1995). Increased activity of p53 in senescing fibroblasts. Proc. Natl. Acad. Sci. USA 92, 8348-8352.
4. Bar-Sagi, D., and Feramisco, J.R. (1985). Microinjection of the ras oncogene protein into PC12 cells induces morphological differentiation. Cell 42, 841-848.
5. Barbacid, M. (1987). ras genes. Annu. Rev. Biochem. 56, 779-827.
6. Bartkova, J., Lukas, J., Guldberg, G., Alsner, J., Kirkin, A.F., Zuethen, J., and Bartek, J. (1996). The p16-cyclin D/Cdk4-pRb pathway as a functional unit frequently altered in melanoma pathogenesis. Cancer Res. 56, 5475-5483.
7. Benito, M., Porras, A., Nebreda, A.R., and Santos, E. (1991). Differentiation of 3T3-L1 fibroblasts to adipocytes induced by transfection of ras oncogenes. Science 253, 565-568.
8. Bos, J.L. (1988). The ras gene family and human carcinogenesis. Mutat. Res. 195, 255-271.
9. Brugarolas, J., Chandrasekaran, C., Gordon, J.I., Beach, D., Jacks, T., and Hannon, G. (1995). Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature 377, 552-557.
10. Cahill, M.A., Janknecht, R., and Nordheim, A. (1996). Signalling pathways: jack of all cascades. Curr. Biol. 6, 16-19.
11. Caldas, C., Hahn, S., da Costa, L.T., Redston, M.S., Schutte, M., Seymour, A.B., Weinstein, C.L., Hruban, R.H., Yeo, C.J., and Kern, S.E. (1994). Frequent somatic mutations and homozygous deletions of the p16 (MTS1) gene in pancreatic adenocarcinoma. Nature Genet. 8, 27-32.
12. Dimri, G.P., Lee. X., Basile, G., Acosta, M., Scott, G., Roskelley, C., Medrano, E.E., Linskens, M., Rubelj, I., Pereira-Smith, O., Peacocke, M., and Campisi, J. (1995). A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. USA 92, 9363-9367.
13. Donehower, L.A., Harvey, M., Slagle, B.L., McArthur, M.J., Montgomery, C.A., Jr., Butel, J.S., and Bradley, A. (1992). Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356, 215-221.
14. Dulic, V., Drullinger, L.F., Lees, E., Reed, S.I., and Stein, G.H. (1993). Altered regulation of G1 in senescent human diploid fibroblasts: accumulation of inactive cyclin E-Cdk2 and cyclin D1-Cdk2 complexes. Proc. Natl. Acad. Sci. USA 90, 11034-11038.
15. Fairweather, D.S., Fox, M., and Margison, G.P. (1987). The in vitro lifespan of MRC-5 cells is shortened by 5-azacytidine-induced demethylation. Exp. Cell Res. 168, 153-159.
16. Franza, B.R., Jr., Maruyama, K., Garrels, J.I., and Ruley, H.E. (1986). In vitro establishment is not a sufficient prerequisite for transformation by activated Ras oncogenes. Cell 44, 409-418.
17. Galaktionov, K., Lee, A.K., Eckstein, E., Draetta, G., Mecklet, J., Loda, M., and Beach, D. (1995). CDC25 phosphatases as potential human oncogenes. Science 269, 1575-1577.
18. Galaktionov, K., Chen, X., and Beach, D. (1996). Cdc25 cell-cycle phosphatase as a target of c-myc. Nature 382, 511-517.
19. Goldstein, S., Moerman, E.J., Fujii, S., and Sobel, B.E. (1994). Over-expression of plasminogen activator inhibitor type-1 in senescent fibroblasts from normal subjects and those with Werner syndrome. J. Cell Physiol. 161, 571-579.
20. CDKN2 expression and its implications for cell immortalization and senescence. Mol. Cell Biol. 16, 859-867.
21. Harvey, D.M., and Levine, A.J. (1991). p53 alteration is a common event in the spontaneous immortalization of primary BALB/c murine embryo fibroblasts. Genes Dev. 5, 2357-2385.
22. Harvey, M., Sands, A.T., Weiss, R.S., Hegi, M.E., Wiseman, R.W., Pantazis, P., Giovanella, B.C., Tainsky, M.A., Bradley, A., and Donehower, L.A. (1993). In vitro growth characteristics of embryo fibroblasts isolated from p53-deficient mice. Oncogene 8, 2457-2467.
23. Hayflick, L., and Moorhead, P.S. (1961). The serial cultivation of human diploid cell strains. Exp. Cell Res. 25, 585-621.
24. Hicks, G.G., Egan, S.E., Greenberg, A.H., and Mowat, M. (1991). Mutant p53 tumor suppressor alleles release ras-induced cell cycle growth arrest. Mol. Cell Biol. 11, 1344-1352.
25. Hinds, P.W., Dowdy, S.F., Eaton, E.N., Arnold, A., and Weinberg, R.A. (1994). Function of a human cyclin gene as an oncogene. Proc. Natl. Acad. Sci. USA 91, 709-713.
26. Hirakawa, T., and Ruley, H.E. (1988). Rescue of cells from ras oncogene-induced growth arrest by a second complementing oncogene. Proc. Natl. Acad. Sci. USA 85, 1519-1523.
27. Hirama, T., and Koeffler, H.P. (1995). Role of the cyclin-dependent kinase inhibitors in the development of cancer. Blood 86, 841-854.
28. Holliday, R. (1986). Strong effects of 5-azacytidine on the in vitro lifespan of human diploid fibroblasts. Exp. Cell Res. 166, 543-552.
29. Hollstein, M., Shomer, B., Greenblatt, M., Soussi, T., Hovig, E., Montesano, R., and Harris, C.C. (1996). Somatic point mutations in the p53 gene of human tumors and cell lines: updated compilation. Nucleic Acids Res. 24, 141-146.
30. Hunter, T. (1991). Cooperation between oncogenes. Cell 64, 249-270.
31. Jacks, T., Remington, L., Williams, B.O., Schmitt, E.M., Halachmi, S., Bronson, R.T., and Weinberg, R.A. (1994). Tumor spectrum analysis in p53-mutant mice. Curr. Biol. 4, 1-7.
32. Kemp, C.J., Donehower, L.A., Bradley, A., and Balmain, A. (1993). Reduction of p53 gene dosage does not increase initiation or promotion but enhances malignant progression of chemically induced skin tumors. Cell 74, 813-822.
33. Kinzler, K.W., and Vogelstein, B. (1996). Lessons from hereditary colorectal cancer. Cell 87, 159-170.
34. Ko, L.J., and Prives, C. (1996). p53: puzzle and paradigm. Genes Dev. 10, 1054-1072.
35. Land, H., Parada, L.F., and Weinberg, R.A. (1983). Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature 304, 596-602.
36. INK4b in undifferentiated mouse skin tumors. Cancer Res. 55, 5168-5172.
37. Liu, J.J., Chao, J.R., Jiang, M.C., Ng, S.Y., Yen, J.J., and Yang-Yen, H.F. (1995). Ras transformation results in an elevated level of cyclin D1 and acceleration of G1 progression in NIH 3T3 cells. Mol. Cell Biol. 15, 3654-3663.
38. Lovec, H., Sewing, A., Lucibello, F.C., Müller, R., and Möröy, T. (1994). Oncogenic activity of cyclin D1 revealed through cooperation with Ha-ras: link between cell cycle control and malignant transformation. Oncogene 9, 323-326.
39. Lowe, S.W., and Ruley, H.E. (1993). Stabilization of the p53 tumor suppressor is induced by adenovirus 5 E1A and accompanies apoptosis. Genes Dev. 7, 535-545.
40. Lowe, S.W., Ruley, H.E., Jacks, T., and Housman, D.E. (1993). p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell 74, 957-967.
41. Lowe, S.W., Jacks, T., Housman, D.E., and Ruley, H.E. (1994). Abrogation of oncogene-associated apoptosis allows transformation of p53-deficient cells. Proc. Natl. Acad. Sci. USA 91, 2026-2030.
42. Lumpkin, C.K., Knepper, J.E., Butel, J.S., Smith, J.R., and Pereira-Smith, O.M. (1986). Mitogenic effects of the proto-oncogene and oncogene forms of c-Ha-ras DNA in human diploid fibroblasts. Mol. Cell Biol. 6, 2990-2993.
43. Marshall, C.J. (1995). Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80, 179-185.
44. McCurrach, M.E., Connor, T.M.F., Knudson, C.M., Korsmeyer, S.J., and Lowe, S.W. (1997). bax-deficiency promotes drug resistance and oncogenic transformation by attenuating p53-dependent apoptosis. Proc. Natl. Acad. Sci. USA, in press.
45. Metz, T., Harris, A.W., and Adams, J.M. (1995). Absence of p53 allows direct immortalization of hematopoietic cells by the myc and raf oncogenes. Cell 82, 29-36.
46. Morgenstern, J.P., and Land, H. (1990). Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18, 3587-3596.
47. Mu, X.-C., and Higgins, P.J. (1995). Differential growth state-dependent regulation of plasminogen activator inhibitor type-1 expression in senescent IMR-90 human diploid fibroblasts. J. Cell. Physiol. 165, 647-657.
48. Newbold, R.F., and Overell, R.W. (1983). Fibroblast immortality is a prerequisite for transformation by EJ c-H-ras oncogene. Nature 304, 648-651.
49. Noda, A., Ning, Y., Venable, S.F., Pereira-Smith, O.M., and Smith, J.R. (1994). Cloning of senescent cell-derived inhibitors of DNA synthesis using an expression screen. Exp. Cell Res. 211, 90-98.
50. Ogryzko, V.V., Hirai, T.H., Russanova, V.R., Barbie, D.A., and Howard, B.H. (1996). Human fibroblast commitment to a senescence-like state in response to histone deacetylase inhibitors is cell cycle dependent. Mol. Cell Biol. 16, 5210-5218.
51. INK4b genes. Oncogene 11, 635-645.
52. Reznikoff, C.A., Yeager, T.R., Belair, C.D., Savelieva, E., Puthenveettil, J.A., and Stadler, W.M. (1996). Elevated p16 at senescence and loss of p16 at immortalization in human papillomavirus 16 E6, but not E7, transformed human uroepithelial cells. Cancer Res. 56, 2886-2890.
53. Ridley, A.J., Paterson, H.F., Noble, M., and Land, H. (1988). ras-mediated cell cycle arrest is altered by nuclear oncogenes to induce Schwann cell transformation. EMBO J. 7, 1635-1645.
54. INK4 expression and telomere length during spontaneous immortalization of Li-Fraumeni syndrome fibroblasts. Mol. Cell Biol. 15, 4745-4753.
55. Röhme, D. (1981). Evidence for a relationship between longevity of mammalian species and life spans of normal fibroblasts in vitro and erythrocytes in vivo. Proc. Natl. Acad. Sci. USA 78, 5009-5013.
56. Ruley, H.E. (1983). Adenovirus early region 1A enables viral and cellular transforming genes to transform primary cells in culture. Nature 304, 602-606.
57. Ruley, H.E. (1990). Transforming collaborations between ras and nuclear oncogenes. Cancer Cells 2, 258-268.
58. Serrano, M., Hannon, G.J., and Beach, D. (1993). A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature 366, 704-707.
59. INK4. Science 267, 249-252.
60. Serrano, M., Lee, H.-W., Chin, L., Cordon-Cardo, C., Beach, D., and DePinho, R.A. (1996). Role of the INK4a locus in tumor suppression and cell mortality. Cell 85, 27-37.
61. Seshadri, T., and Campisi, J. (1990). Repression of c-fos transcription and an altered genetic program in senescent human fibroblasts. Science 247, 205-209.
62. Sherr, C.J., and Roberts, J.M. (1995). Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev. 9, 1149-1163.
63. Stein, G.H., and Dulic, V. (1995). Originis of G1 arrest in senescent human fibroblasts. Bioessays 17, 537-543.
64. Sullivan, N.F., Sweet, R.W., Rosenberg, M., and Feramisco, J.R. (1986). Microinjection of the ras oncogene protein into nonestablished rat embryo fibroblasts. Cancer Res. 46, 6427-6432.
65. INK4A and counteracts its inhibitory activity towards CDK4. EMBO J. 15, 1607-1614.
66. Tanaka, N., Ishihara, M., Kitagawa, M., Harada, H., Kimura, T., Matsuyama, T., Lamphier, M.S., Aizawa, S., Mak, T.W., and Taniguchi, T. (1994). Cellular commitment to oncogene-induced transformation or apoptosis is dependent on the transcription factor IRF-1. Cell 77, 829-839.
67. Venable, M.E., Lee, J.Y., Smyth, M.J., Bielawska, A., and Obeid, L.M. (1995). Role of ceramide in cellular senescence. J. Biol. Chem. 270, 30701-30708.
68. Vogelstein, B., and Kinzler, K.W. (1993). The multistep nature of cancer. Trends Genet. 9, 138-141.
69. Votja, P.J., and Barrett, J.C. (1995). Genetic analysis of cellular senescence. Biochim. Biophys. Acta 1242, 29-41.
70. Weinberg, R.A. (1989). Oncogenes, antioncogenes, and the molecular bases of multistep carcinogenesis. Cancer Res. 49, 3713-3721.
71. Weinberg, R.A. (1995). The retinoblastoma protein and cell cycle control. Cell 81, 323-330.
72. INK4a-insensitive CDK4 mutant targeted by cytolytic T lymphocytes in a human melanoma. Science 269, 1281-1284.
73. Xiong, Y., Zhang, H., and Beach, D. (1993). Subunit rearrangement of the cyclin-dependent kinases is associated with cellular transformation. Genes Dev. 7, 1572-1583.