Immortalization of human cells and its mechanisms

Critical Reviews in Oncogenesis

Volumn 7, Issue 1-2, 1996, Pages 19-31

  Namba, Masayoshi ^a   Mihara, Koichiro ^a   Fushimi, Kazuo ^a  

^a OKAYAMA UNIVERSITY MEDICAL SCHOOL   (Japan)

Author keywords

cellular senescence; human cells; immortalization; neoplastic transformation; p53

Indexed keywords

PROTEIN P53;

CELL IMMORTALIZATION; HUMAN; HUMAN CELL; MALIGNANT TRANSFORMATION; REVIEW;

EID: 0030440667     PISSN: 08939675     EISSN: None     Source Type: Journal    
DOI: 10.1615/critrevoncog.v7.i1-2.20     Document Type: Review

References (95)

1. Atadja, P., H. Wong, I. Garkavtsev, C. Veillette, and K. Riabowol:Increased activity of p53 in senescing fibroblasts. Proc. Natl. Acad. Sci. U.SA., 92:3348-8352 (1995).
2. Baden, H. P., J. Kubilus, J. C. Kvedar, M. L. Steinberg, and S. R. Wolman:Isolation and characterization of a spontaneously arising long-lived line of human keratinocytes (NM 1). In vitro Cell. Dev. Biol., 23:205-213 (1987).
3. Bai, L., K. Mihara, T. Kondo, M. Honma, and M. Namba:Immortalization of normal human fibroblasts by treatment with 4-nitroquinoline 1-oxide. Int. J. Cancer, 53:451-456 (1993).
4. Band, V., S. Dalal, L. Delmolino, and E. J. Androphy:Enhanced degradation of p53 protein in HPV-6 and BPV-1 E6-immortalized human mammary epithelial cells. EMBO J., 12:1847-1852 (1993).
5. Bischoff, F. Z., S. O. Yim, S. Pathak, G. Grant, M. J. Siciliano, B. C. Giovanella, L. C. Strong, and M. A. Tainsky:Spontaneous abnormalities in normal fibroblasts from patients with Li-Fraumeni cancer syndrome: aneuploidy and immortalization. Cancer Res., 50:7979-7984 (1990).
6. Bookland, E. A., S. Swaminathan, R. Oyasu, K. W. Gilchrist, M. Lindstrom, and C. A. Reznikoff:Tumorigenic transformation and neoplastic progression of human uroepithelial cells after exposure in vitro to 4-aminobiphenyl or its metabolites. Cancer Res., 52:1606-1614 (1992).
7. Boukamp, P., R. T. Petrussevska, D. Breitkreutz, J. Hornung, A. Markham, and N. E. Fusenig:Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol., 106:761-771 (1988).
8. Bryan, T. M. and R. R. Reddel:SV40-indueed immortalization of human cells. Crit. Rev. Oncogen., 5:331-357 (1994).
9. Byrd, P., K. W. Brown, and P. H. Gallimore:Malignant transformation of human embryo retinoblasts by cloned adenovirus 12 DNA. Nature, 298:69-71 (1982).
10. Calaf, G. and J. Russo:Transformation of human breast epithelial cells by chemical carcinogens. Carcinogenesis, 14:483-492 (1993).
11. Chang, S. E.:In vitro transformation of human epithelial cells. Biochim. Biophys. Acta., 823:161-194 (1986).
12. Chopra, D. P., I. C. Xue-Hu, and L. V. Reddy:Growth and gene expression in diploid epithelial cell lines derived from normal human parotid gland. Differentiation, 58:241-251 (1995).
13. DeCaprio, J. A., J. W. Ludlow, J. Figge, J.-Y. Shew, C.-M. Huang, W.-H. Lee, E. Marsilio, E. Paucha, and D. M. Livingston:SV40 large tumor antigen forms a specific complex with the product of the retinoblastoma susceptibility gene. Cell, 54:275-283 (1988).
14. De Silva, R., N. J. Whitaker, E. M. Rogan, and R. R. Reddel:HPV-16 E6 and E7 genes, like SV40 early region genes, are insufficient for immortalization of human mesothelial and bronchial epithelial cells. Exp. Cell Res., 213:418-427(1994).
15. Dorman, B. H., J. M. Siegfried, and D. G. Kaufman:Alterations of human endometrial stromal cells produced by N-methyl-N'-nitro-N-nitrosoguanidine. Cancer Res., 43:3348-3357 (1983).
16. Dürst, M., L. Gissmann, H. Ikenberg, and H. zur Hausen:A papillomavirus DNA from a cervical carcinoma and its prevalence in cancer biopsy samples from different geographic regions. Proc. Natl. Acad. Sci. U.S.A., 80:3812-3815 (1983).
17. Dyson, N., P. M. Howley, K. Münger, and E. Harlow:The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science, 243:934-937 (1989).
18. 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:WAF1, a potential mediator of p53 tumor suppression. Cell, 75:817-825 (1993).
19. Faller, D. V., S. Kourembanas, D. Ginsberg, R. Hannan, T. Collins, B. M. Ewenstein, J. S. Pober, and R. Tantravahi:Immortalization of human endothelial cells by murine sarcoma viruses, without morphologic transformation. J. Cell. Physiol, 134:47-56 (1988).
20. Farmer, G., J. Bargonetti, H. Zhu, P. Friedman, R. Prywes, and C. Prives:Wild-type p53 activates transcription in vitro. Nature, 358:83-86 (1992).
21. Fukasawa, K., T. Choi, R. Kuriyama, S. Rulong, and G. F. Vande Woude:Abnormal centrosome amplification in the absence of p53. Science, 271:1744-1747 (1996).
22. 1. Proc. Natl. Acad. Sci. U.SA., 89:2759-2763 (1992)
23. Graham, F. L., J. Smiley, W. C. Russell, and R. Nairn:Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J. Gen. Virol., 36:59-74 (1977).
24. Harley, C. B., A. B. Futcher, and C. W. Greider:Telomeres shorten during ageing of human fibroblasts. Nature, 345:458-460 (1990).
25. Harper, J. W., G. R. Adarni, N. Wei, K. Keyomarsi, and S. J. Elledge:The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell, 75:805-816 (1993).
26. Hayflick, L. and P. S. Moorhead:The serial cultivation of human diploid cell strains. Exp. Cell Res., 25:585-621 (1961).
27. Hei, T. K., C. Q. Piao, J. C. Willey, S. Thomas, and E. J. Hall:Malignant transformation of human bronchial epithelial cells by radon-simulated a particles. Carcinogenesis, 1.5:431-437 (1994).
28. Hensler, P. J., L. A. Annab, J. C. Barrett, and O. M. Pereira-Smith:A gene involved in control of human cellular senescence on human chromosome 1q. Mol. Cell. Biol., 14:2291-2297 (1994).
29. Hurlin, P. J., V. M. Maher, and J. J. McCormick:Malignant transformation of human fibroblasts caused by expression of a transfected T24 HRAS oncogene. Proc. Natl. Acad. Sci. U.S.A., 86:187-191 (1989).
30. 60Co gamma rays. Int. J. Cancer, 66:698-702 (1996).
31. Karlsson, C., G. Stenman, P. J. Vojta, E. Bongcam-Rudloff, J. C. Barrett, B. Westermark, and Y. Paulsson:Escape from senescence, in hybrid cell clones involves deletions of two regions located on human chromosome 1q. Cancer Res., 56:241-245 (1996).
32. Kim, N. W., M. A. Piatyszek, K. R. Prowse, C. B. Harley, M. D. West, P. L. C. Ho, G. M. Coviello, W. E. Wright, S. L. Weinrich, and J. W. Shay:Specific association of human telomerase activity with immortal cells and cancer. Science, 266:2011-2015 (1994).
33. Kinsella, A. R., L. Fiszer-Maliszewska, E. L. D. Mitchell, Y. Guo, M. Fox, and D. Scott:Introduction of the activated N-ras oncogene into human fibroblasts by retroviral vector induces morphological transformation and tumorigenicity. Carcinogenesis, 11:1803-1809 (1990).
34. Kono, Y., S. Yang, M. Letarte, and E. A. Roberts:Establishment of a human hepatocyte line derived from primary culture in a collagen gel sandwich culture system. Exp. Cell Res., 221:478-485 (1995).
35. Kuettel, M. R., P. J. Thraves, M. Jung, S. P. Varghese, S. C. Prasad, J. S. Rhim, and A. Dritschilo:Radiation-induced neoplastic transformation of human prostate epithelial cells. Cancer Res., 56:5-10 (1996).
36. Kulju, K. S. and J. M. Lehman:Increased p53 protein associated with aging in human diploid fibroblasts. Exp. Cell Res., 217:336-345 (1995).
37. Lane, D. P. and L. V. Crawford:T antigen is bound to a host protein in SV40-transformed cells. Nature (London), 278:261-263 (1979).
38. Lecka-Czernik, B., E. J. Moennan, R. A. Jones, and S. Goldstein:Identification of gene sequences overexpressed in senescent and Werner syndrome human fibroblasts. Exp. Gerontol., 31:159-174 (1996).
39. Lehman, T. A., R. Modali, P. Boukamp, J. Stanek, W. P. Bennett, J. A. Welsh, R. A. Metcalf, M. Stampfer, N. Fusenig, E. M. Rogan, and C. C. Harris: p53 Mutations in human immortalized epithelial cell lines. Carcinogenesis, 14:833-839 (1993).
40. Linder, S. and H. Marshall:Immortalization of primary cells by DNA tumor viruses. Exp. Cell Res., 191:1-7 (1990).
41. Linzer, D. I. and A. J. Levine:Characterization of a 54 kDa cellular SV40 tumor antigen present in SV40-transformed cells and uninfected embryonal carcinoma cells. Cell, 17:43-52 (1979).
42. Livingstone, L. R., A. White, J. Sprouse, E. Livanos, T. Jacks, and T. D. Tisty:Altered cell cycle arrest and gene amplification potential accompany loss of wild-type p53. Cell, 70:923-935 (1992).
43. Maclean, K., E. M. Rogan, N. J. Whitaker, A. C. M. Chang, P. B. Rowe, L. Dalla-Pozza, G. Symonds, and R. R. Reddel:In vitro transformation of Li-Fraumeni syndrome fibroblasts by SV40 large T antigen mutants. Oncogene, 9:719-725 (1994).
44. McCormick, J. J. and V. M. Maher:Towards an understanding of the malignant transformation of diploid human fibroblasts. Mutat. Res., 199:273-291 (1988).
45. Metz, T., A. W. Harris, and J. M. Adams:Absence of p53 allows direct immortalization of hematopoietic cells by the myc and raf oncogenes. Cell, 82:29-36 (1995).
46. 60Co gamma rays. Int. J. Cancer, 50:639-643 (1992).
47. Milner, J. and E. A. Medcalf:Cotranslation of activated mutant p53 with wild-type drives the wild-type p53 protein into the mutant conformation. Cell, 65:765-774 (1991).
48. Momand, J., G. P. Zambetti, D. C. Olson, D. George, and A. J. Levine:The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell, 69:1237-4245 (1992).
49. Morgan, T. L., D. Yang, D. G. Fry, P. J. Hurlin, S. K. Kohler, V. M. Maher, and J. J. McCormick:Characteristics of an infinite life span diploid human fibroblast cell strain and a near-diploid strain arising from a clone of cells expressing a transfected v-myc oncogene. Exp. Cell Res., 197:125-136 (1991).
50. Namba, M., K. Mihara, T. Kondo, Y. Inoue, T. Tsuji, K. Fushimi, T. Shima, and M. Iijima:Immortalization of cultured human fibroblasts treated with the mutant p53 gene and X-rays. Radiat. Oncol. Invest., 3:294-298 (1996).
51. Namba, M., K. Nishitani, F. Fukushima, T. Kimoto, J. Utsunomiya, and L. Hayflick:Neoplastic transformation of human diploid fibroblasts with chemical carcinogens and Co-60 gamma rays. Gann Monogr. Cancer Res., 27:221-230 (1981).
52. 60Co gamma rays. Int. J. Cancer., 35:275-280 (1985).
53. 60Co gamma rays and Harvey sarcoma viruses. Int. J. Cancer, 37:419-423 (1986).
54. Namba, M., K. Nishitani, F. Fukushima, T. Kimoto, and Y. Yuasa:Multi-step neoplastic transformation of normal human fibroblasts by Co 60 gamma rays and Ha-ras oncogenes. Mutat. Res., 199:415-423 (1988).
55. Ning, Y., J. L. Weber, A. M. Killary, D. H. Ledbetter, J. R. Smith, and O. M. Pereira-Smith:Genetic analysis of indefinite division in human cells: evidence for a cell senescence-related gene(s) on human chromosome 4. Proc. Natl. Acad. Sci. U.S.A., 88:5635-5639 (1991).
56. Noda, A., Y. Ning, S. F. Venable, O. M. Pereira-Smith, and J. R. Smith:Cloning of senescent cell-derived inhibitors of DNA synthesis using an expression screen. Exp. Cell Res., 211:90-98 (1994).
57. Ogata, T., D. Ayusawa, M. Namba, E. Takahashi, M. Oshimura, and M. Oishi:Chromosome 7 suppresses indefinite division of nontumorigenic immortalized human fibroblast cell lines KMST-6 and SUSM-1. Mol. Cell. Biol., 13:6036-6043 (1993).
58. Okamoto, A., D. J. Demetrick, E. A. Spillare, K. Hagiwara, S. P. Hussain, W. P. Bennett, K. Forrester, B. Gerwin, M. Serrano, D. H. Beach, and C. C. Harris:Mutations and altered expression of p161NK4 in human cancer. Proc. Natl. Acad. Sci. USA., 91:11045-11049 (1994).
59. Olson, D. C., V. Marrchal, J. Momand, J. Chen, C. Romocki, and A. J. Levine:Identification and characterization of multiple mdm-2 proteins and mdm-2-p53 protein complexes. Oncogene, 8:2353-2360 (1993).
60. Otterson, G. A., R. A. Kratzke, A. Coxon, Y. W. Kim, and F. J. Kaye:Absence of p161NK4 protein is restricted to the subset of lung cancer lines that retains wild-type RB. Oncogene, 9:3375-3378 (1994).
61. Paine, T. M., H. D. Soule, R. J. Pauley, and P. J. Dawson:Characterization of epithelial phenotyes in mortal and immortal human breast cells. Int. J. Cancer, 50:463-473 (1992).
62. Parda, D. S., P. J. Thraves, M. R. Kuettel, M. S. Lee, P. Amstein, M. E. Kaighn, J. S. Rhim, and A. Dritschilo:Neoplastic transformation of human prostate epithelial cell line by the v-Ki-ras oncogene. Prostate, 23:91-98 (1993).
63. Pereira-Smith, O. M. and J. R. Smith:Genetic analysis of indefinite division in human cells: Identification of four complementation groups. Proc. Natl. Acad. Sci. U.S.A., 85:6042-6046 (1988).
64. Pfeifer, A. M. A., R. T. Jones, P. E. Bowden, D. Mann, E. Spillare, A. J. P. Klein-Szanto, B. F. Trump, and C. C. Harris:Human bronchial epithelial cells transformed by the c-raf-1 and c-myc protooncogenes induce multidifferentiated carcinomas in nude mice: a model for lung carcinogenesis. Cancer Res., 51:3793-3801 (1991).
65. Reddel, R. R., R. de Silva, E. L. Duncan, E. M. Rogan, N. J. Whitaker, D. G. Zahra, Y. Ke, M. G. McMenamin, B. I. Gerwin, and C. C. Harris: SV40-induced immortalization and ras-transformation of human bronchial epithelial cells. Int. J. Cancer, 61:199-205 (1995).
66. Rhim, J. S., J. H. Yoo, J. H. Park, P. Thraves, Z. Salchi, and A. Dritschilo:Evidence for the multistep nature of in vitro human epithelial cell carcinogenesis. Cancer Res. (Suppl.), 50:5653s-5657s (1990).
67. INK4 expression and telomere length during spontaneous immortalization of Li-Fraumeni syndrome fibroblasts. Mol. Cell. Biol., 15:4745-4753 (1995).
68. Sager, R., K. Tanaka, C. C. Lau, Y. Ebina, and A. Anisowicz:Resistance of human cells to tumorigenesis induced by cloned transforming genes. Proc. Natl. Acad. Sci. U.S.A., 80:7601-7605 (1983).
69. Sandhu, A. K., K. Hubbard, G. P. Kaur, K. K. Jha, H. L. Ozer, and R. S. Athwal:Senescence of immortal human fibroblasts by the introduction of normal human chromosome 6. Proc. Natl. Acad. Sci. U.S.A., 91:5498-5502 (1994).
70. Sarnow, P., Y. S. Ho, J. Williams, and A. J. Levine:Adenovirus E1b-58 Kd tumor antigen and SV40 large tumor antigen are physically associated with the same 54 Kd cellular protein in transformed cells. Cell, 28:387-394 (1982).
71. Shay, J. W., W. E. Wright, and H. Werbin:Defining the molecular mechanisms of human cell immortalization. Biochim. Biophys. Acta, 1072:1-7 (1991).
72. Shay, J. W., G. Tomlinson, M. A. Piatyszek, and L. S. Gollahon:Spontaneous in vitro immortalization of breast epithelial cells from a patient with Li-Fraumeni syndrome. Mol. Cell. Biol., 15:425-432 (1995).
73. Soule, H. D., T. M. Maloney, S. R. Wolman, W. D. Peterson, Jr., R. Brenz, C. M. McGrath, J. Russo, R. J. Pauley, R. F. Jones, and S. C. Brooks:Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Res., 50:6075-6086 (1990).
74. Stampfer, M. R. and J. C. Bartley:Induction of transformation and continuous cell lines from normal human mammary epithelial cells after exposure to benzo[α]pyrene. Proc. Natl. Acad. Sci. U.S.A., 82:2394-2398 (1985).
75. Stein, G. H., M. Namba, and C. M. Corsaro:Relationship of finite proliferative lifespan, senescence, and quiescence in human cells. J. Cell. Physiol., 122:343-349 (1985).
76. 60Co gamma rays or4-nitroquinoline 1-oxide.Hum. Genet., 97:1-6 (1996).
77. Takahashi, K., Y. Sawasaki, J. Hata, K. Mukai, and T. Goto:Spontaneous transformation and immortalization of human endothelial cells. In Vitro Cell. Dev. Biol., 25:265-274 (1990).
78. Takemoto, K. K., H. Linke, T. Miyamura, and G. C. Farced:Persistent BK papovavirus infection of transformed human fetal brain cells. I. Episomal viral DNA in cloned lines deficient in T-antigen expression. J. Virol., 29:1177-1185 (1979).
79. Thraves, P., Z. Salehi, A. Dritschilo, and J. S. Rhim:Neoplastic transformation of immortalized human epidermal keratinocytes by ionizing radiation. Proc. Natl. Acad. Sci. U.S.A., 87:1174-1177 (1990).
80. 1-induced immoitalization of cultured skin fibroblasts from a patient with Li-Fiaumeni syndrome. Carcinogenesis, 16:25-34 (1995).
81. Tuynder, M., S. Godfrine, J. J. Cornelis, and J. Rommelaere:Dose-dependent induction of resistance to terminal differentiation in x-irradiated cultures of normal human keratinocytes. Proc. Natl. Acad. Sci. U.S.A., 88:2638-2642 (1991).
82. Tveito, G., I.-L. Hansteen, H. Dalen, and A. Haugen:Immortalization of normal human kidney epithelial cells by nickel(II). Cancer Res., 49:1829-1835 (1989).
83. Vojta, P. J. and J. C. Barrett:Genetic analysis of cellular senescence. Biochim. Biophys. Acta, 1242:29-41 (1995).
84. Wazer, D. E., Q. Chu, X. L. Liu, Q. Gao, H. Safaii, and V. Band:Loss of p53 protein during radiation transformation of primary human mammary epithelial cells. Mol. Cell. Biol., 14:2468-2478 (1994).
85. Weaver, J. D., G. Stellen, and J. W. Littlefield:Partial trisomies in two spontaneously arising long-lived human keratinocyte lines. In Vitro Cell. Dev. Biol., 27A:670-675 (1991).
86. Werness, B. A., A. J. Levine, and P. M. Howley:Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science, 248: 76-79 (1990).
87. Whittaker, J. L., P. J. Byrd, R. J. A. Grand, and P. H. Gallimore:Isolation and characterization of four adenovirus type 12-transformed human embryo kidney cell lines. Mol. Cell. Biol., 4:110-116 (1984).
88. INK4, and telomerase in immortalization of human cells. Oncogene, 11:971-976 (1995).
89. Whyte, P., K. J. Buchkovich, J. M. Horowitz, S. H. Friend, M. Raybuck, R. A. Weinberg, and E. Harlow:Association between an oncogene and an anti-oncogene: the adenovirus E1A proteins bind to the retinoblastoma gene product. Nature, 334:124-129 (1988).
90. Wilson, D. M., D. Yang, J. E. Dillberger, S. E. Dietrich, V. M. Maher, and J. J. McCormick:Malignant transformation of human fibroblasts by a transfected N-ras oncogene. Cancer Res., 50:5587-5593 (1990).
91. Yang, D., C. Louden, D. S. Reinhold, S. K. Kohler, V. M. Maher, and J. J. McCormick:Malignant transformation of human fibroblast cell strain MSU-1.1 by (±)-7β, 8α-dihydroxy-9α, 10α-epoxy-7, 8, 9, 10-tetrahydrobenzo [α]pyrene. Proc. Natl. Acad. Sci. U.S.A., 89:2237-2241 (1992).
92. Yang, D., S. K. Kohler, V. M. Maher, and J. J. McCormick: v-sis oncogene-induced transformation of human fibroblasts into cells capable of forming benign tumors. Carcinogenesis, 15:2167-2175 (1994).
93. Yin, Y., M. A. Tainsky, F. Z. Bischoff, L. C. Strong, and G. M. Wahl:Wild-type p53 restores cell cycle control and inhibits gene amplification in cells with mutant p53 alleles. Cell, 70:937-948 (1992).
94. Yoakum, G. H., J. F. Lechner, E. W. Gabrielson, B. E. Korba, L. Malan-Shibley, J. C. Willey, M. G. Valerio, A. M. Shainsuddin, B. F. Trump, and C. C. Harris:Transforma-tion of human bronchial epithelial cells transfected by Harvey ras oncogene. Science, 227:1174-4179 (1985).
95. Zimmerman, R. J. and P. A. Cerutti:A comparison of markers of human fibroblast transformation induced by chemical carcinogen treatment or by transfection of an origin-defective SV40-containing plasmid. Mutat. Res., 199:449-459 (1988).