Expression of the pRb-binding regions of E1A enables efficient transformation of primary epithelial cells by v-src

Journal of Virology

Volumn 72, Issue 4, 1998, Pages 2815-2824

  Fischer, Robert S ^a,b   Quinlan, Margaret P ^b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS; ARTICLE; CELL CYCLE; CELL TRANSFORMATION; HUMAN; HUMAN CELL; ONCOGENE SRC; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS CARCINOGENESIS;

EID: 0031949105     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.4.2815-2824.1998     Document Type: Article

References (94)

1. Amini, S., A. J. Lewis, M. A. Israel, J. S. Butel, and J. B. Bolen. 1986. Analysis of pp60c-src protein kinase activity in hamster embryo cells transformed by simian virus 40, human adenoviruses, and bovine papillomavirus 1. J. Virol. 57:357-61.
2. Bayley, S. T., and J. S. Mymryk. 1994. Adenovirus E1A proteins and transformation (review). Int. J. Oncol. 5:325-444.
3. Billon, N., L. van Grunsven, and B. B. Rudkin. 1996. The CDK inhibitor p21WAF1/Cip1 is induced through a P300-dependent mechanism during NGF-mediated neuronal differentiation of PC12 cells. Oncogene 13:2047-2054.
4. Bishop, J. M. 1991. Molecular themes in oncogenesis. Cell 64:235-248.
5. Bolen, J. B., C. J. Thiele, M. A. Israel, W. Yonemoto, L. A. Lipsich, and J. S. Brugge. 1984. Enhancement of cellular src gene product tyrosyl kinase activity following polyoma virus infection and transformation. Cell 38:767-777.
6. Branton, P. E., S. T. Bayley, and F. L. Graham. 1985. Transformation by human adenoviruses. Biochim. Biophys. Acta 780:67-94.
7. Chang, J.-H., S. Gill, J. Settleman, and S. J. Parsons. 1995. c-Src regulates the simultaneous rearrangement of actin cytoskeleton, p190RhoGAP, and p120RasGAP following epidermal growth factor stimulation. J. Cell Biol. 130:355-368.
8. Chinnadurai, G. 1992. Adenovirus E1a as a tumor-suppressor gene. Oncogene 7:1255-1258.
9. Coats, S., W. M. Flanagan, J. Nourse, and J. M. Roberts. 1996. Requirement of p27Kip1 for restriction point control of the fibroblast cell cycle. Science 272:877-880.
10. Courtneidge, S. A., and A. E. Smith. 1983. Polyoma virus transforming protein associates with the product of the c-src gene. Nature 303:435-439.
11. Cuzin, F. 1984. The polyoma virus oncogenes. Coordinated functions of three distinct proteins in the transformation of rodent cells in culture. Biochim. Biophys. Acta 781:193-204.
12. Datto, M. B., P. P. Hu, T. F. Kowalik, J. Yingling, and X. F. Wang. 1997. The viral oncoprotein E1A blocks transforming growth factor β-mediated induction of p21/WAF1/Cip1 and p15/INK4B. Mol. Cell. Biol. 17:2030-2037.
13. Douglas, J. L., S. Gopalakrishnan, and M. P. Quinlan. 1991. Modulation of transformation of primary epithelial cells by the second exon of the Ad5 E1A 12S gene. Oncogene 6:2093-2103.
14. Douglas, J. L., and M. P. Quinlan. 1995. Efficient nuclear localization and immortalizing ability, two functions dependent on the adenovirus type 5 (Ad5) E1A second exon, are necessary for cotransformation with Ad5 E1B but not with T24 ras. J. Virol. 69:8061-8065.
15. Douglas, J. L., and M. P. Quinlan. 1994. Efficient nuclear localization of the Ad5 E1A 12S protein is necessary for immortalization but not cotransformation of primary epithelial cells. Cell Growth Differ. 5:475-483.
16. Egan, C., T. N. Jelsma, J. A. Howe, S. T. Bayley, B. Ferguson, and P. E. Branton. 1988. Mapping of cellular protein-binding sites on the products of early-region 1A of human adenovirus type 5. Mol. Cell. Biol. 8:3955-3959.
17. 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.
18. Fabian, J. R., I. O. Daar, and D. K. Morrison. 1993. Critical tyrosine residues regulate the enzymatic and biological activity of Raf-1 kinase. Mol. Cell. Biol. 13:7170-7179.
19. 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.
20. v-src association with the actin cytoskelton induces actin reorganization without affecting polymerization status. J. Cell Biol. 52:47-59.
21. 20a. Fischer, R. S., Y. Zheng, and M. P. Quinlan. Primary epithelial cell transformation by E1A and ras requires Rac1 and ERK activation, while progression can be modulated by E1A and Rac1. Cell Growth Differ., in press.
22. Franza, B. R., Jr., K. Maruyama, J. I. Garrels, and H. E. Ruley. 1986. In vitro establishment is not a sufficient prerequisite for transformation by activated ras oncogenes. Cell 44:409-418.
23. Frisch, S. M. 1994. E1A induces the expression of epithelial characteristics. J. Cell Biol. 127:1085-1096.
24. Gilmer, T. M., L. A. Annab, M. Oshimura, and J. C. Barret. 1985. Neoplastic transformation of normal and carcinogen-induced preneoplastic Syrian hamster embryo cells by the v-src oncogene. Mol. Cell. Biol. 5:1707-1713.
25. Gopalakrishnan, S., J. L. Douglas, and M. P. Quinlan. 1997. Immortalization of primary epithelial cells by E1A 12S requires late, second exon-encoded functions in addition to complex formation with pRb and p300. Cell Growth Differ. 8:541-551.
26. Gopalakrishnan, S., and M. P. Quinlan. 1995. Modulation of E-cadherin localization in cells expressing wild type E1A 12S or hypertransforming mutants. Cell Growth Differ. 6:985-998.
27. Graham, F. L., J. Smiley, W. C. Russell, and R. Nairn. 1977. Characteristics of a human cell line transformed by DNA from adenovirus type 5. J. Gen. Virol. 36:59-72.
28. Gu, H., and N. Oliver. 1995. Transcriptional repression of fibronectin gene expression in v-src transformation. Exp. Cell Res. 217:428-439.
29. Gu, Z., and G. Matlashewski. 1995. Effect of human papillomavirus type 16 oncogenes on MAP kinase activity. J. Virol. 69:8051-8056.
30. Hamaguchi, M., N. Matsuyoshi, Y. Ohnishi, B. Gotoh, M. Takeichi, and Y. Nagai. 1993. p60v-src causes tyrosine phosphorylation and inactivation of the N-cadherin-catenin cell adhesion system. EMBO J. 12:307-314.
31. CDKN2 expression and its implications for cell immortalization and senescence. Mol. Cell. Biol. 16:859-867.
32. 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.
33. Herzog, M., A. Dreager, E. Ehler, and J. V. Small. 1994. Immunofluorescence microscopy of the cytoskeleton: double and triple immunofluorescence, p. 355-374. In J. E. Celis (ed.), Cell biology: a laboratory handbook, 1st ed., vol. 2. Academic Press, San Diego, Calif.
34. Hildebrand, J. D., J. M. Taylor, and J. T. Parsons. 1996. An SH3 domain-containing GTPase-activating protein for Rho and Cdc42 associates with focal adhesion kinase. Mol. Cell. Biol. 16:3169-3178.
35. Hjelle, B., E. Liu, and J. M. Bishop. 1988. Oncogene v-src transforms and establishes embryonic rodent fibroblasts, but not diploid human fibroblasts. Proc. Natl. Acad. Sci. USA 85:4355-4359.
36. Houweling, A., P. J. van der Elsen, and A. J. Van der Eb. 1980. Partial transformation of primary rat cells by the leftmost 4.5% fragment of adenovirus 5 DNA. Virology 105:537-550.
37. Howe, J. A., J. S. Mymryk, C. Egan, P. E. Branton, and S. T. Bayley. 1990. Retinoblastoma growth suppressor and a 300-kilodalton protein both appear to regulate cellular DNA synthesis. Proc. Natl. Acad. Sci. USA 87:5883-5887.
38. Hunter, T. 1991. Cooperation between oncogenes. Cell 64:249-270.
39. Inoue, H., N. Tavoloni, and H. Hanafusa. 1995. Suppression of v-Src transformation in primary rat embryo fibroblasts. Oncogene 11:231-238.
40. Kaplan, D. R., D. C. Pallas, W. Morgan, B. Schaffhausen, and T. M. Roberts. 1989. Mechanism of transformation by polyoma virus middle T antigen. Biochim. Biophys. Acta 948:345-368.
41. Kaplan, K. B., J. R. Swedlow, D. O. Morgan, and H. E. Varmus. 1995. c-Src enhances the spreading of src-/-fibroblasts on fibronectin by a kinase-independent mechanism. Genes Dev. 9:1505-1517.
42. Kato, J. Y., M. Matsuoka, K. Polyak, J. Massague, and C. J. Sherr. 1994. Cyclic AMP-induced G1 phase arrest mediated by an inhibitor (p27Kip1) of cyclin-dependent kinase 4 activation. Cell 79:487-496.
43. Kellie, S., B. Patel, N. M. Wigglesworth, D. R. Critchley, and J. A. Wyke. 1986. The use of Rous sarcoma virus transformation mutants with differing tyrosine kinase activities to study the relationships between vinculin phosphorylation, pp60v-src location and adhesion plaque integrity. Exp. Cell. Res. 165:216-228.
44. Khosravi-Far, R., P. A. Solski, G. J. Clark, M. S. Kinch, and C. J. Der. 1995. Activation of Rac1, RhoA, and mitogen-activated protein kinases is required for Ras transformation. Mol. Cell. Biol. 15:6443-6453.
45. Kwon, H. J., M. Yoshida, K. Abe, S. Horinouchi, and T. Beppu. 1992. Radicicol, an agent inducing the reversal of transformed phenotypes of src-transformed fibroblasts. Biosci. Biotech. Biochem. 56:6926-6930.
46. Kwon, H. J., M. Yoshida, Y. Fukui, S. Horinouchi, and T. Beppu. 1992. Potent and specific inhibition of p60v-src protein kinase both in vivo and in vitro by radicicol. Cancer Res. 52:6926-6930.
47. Land, H., L. F. Parada, and R. A. Weinberg. 1983. Cellular oncogenes and multistep carcinogenesis. Science 222:771-778.
48. Land, H., L. F. Parada, and R. A. Weinberg. 1983. Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature (London) 304:596-602.
49. MacAuley, A, and T. Pawson. 1988. Cooperative transforming activities of ras, myc, and src viral oncogenes in nonestablished rat adrenocortical cells. J. Virol. 62:4712-4721.
50. Kip1 by the viral E1A oncoprotein in TGFβ-treated cells. Nature (London) 380:262-265.
51. Malladi, A., and M. P. Quintan. 1997. Mutations in CR1 are dominant negative suppressors of E1A functions in immortalization and the lytic cycle. Virology 233:51-62.
52. Marais, R., Y. Light, H. F. Paterson, and C. J. Marshall. 1995. Ras recruits Raf-1 to the plasma membrane for activation by tyrosine phosphorylation. EMBO J. 14:3136-3145.
53. Meijne, A. M., L. Ruuls-Van Stalle, C. A. Feltkamp, J. B. McCarthy, and E. Roos. 1997. v-src-induced cell shape changes in rat fibroblasts require new gene transcription and precede loss of focal adhesions. Exp. Cell. Res. 234:477-485.
54. Missero, C., E. Calautti, R. Eckner, J. Chin, L. H. Tsai, D. M. Liningston, and G. P. Dotto. 1995. Involvement of the cell-cycle inhibitor Cip1/WAF1 and the E1A-associated p300 protein in terminal differentiation. Proc. Natl. Acad. Sci. USA 92:5451-5455.
55. Mymryk, J. S. 1996. Tumour suppressive properties of the adenovirus 5 E1A oncogene. Oncogene 13:1581-1589.
56. Newbold, R. F., and R. W. Overell. 1983. Fibroblast immortality is a prerequisite for transformation by the EJ cHa-ras oncogene. Nature 304:648-651.
57. Nourse, J., E. Firpo, W. M. Flanagan, S. Coats, K. Polyak, M. H. Lee, J. Massague, G. R. Crabtree, and J. M. Roberts. 1994. Interleukin-2-mediated elimination of the p27Kip1 cyclin-dependent kinase inhibitor prevented by rapamycin. Nature (London) 372:570-573.
58. Parsons, J. T., and S. J. Parsons. 1997. Src family protein tyrosine kinases: cooperating with growth factor and adhesion signalling pathways. Curr. Opin. Cell Biol. 9:187-192.
59. Pillay, I., H. Nakano, and S. V. Sharma. 1996. Radicicol inhibits tyrosine phosphorylation of mitotic src substrate Sam68 and retards subsequent exit from mitosis of src-transformed cells. Cell Growth Differ. 7:1487-1499.
60. Pollack, R., M. Osborn, and K. Weber. 1975. Patterns of organization of actin and myosin in normal and transformed cultured cells. Proc. Natl. Acad. Sci. USA 72:994-998.
61. Polyak, K., J. Y. Kato, M. J. Solomon, C. J. Sherr, J. Massague, J. M. Roberts, and A. Koff. 1994. p27Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-beta and contact inhibition to cell cycle arrest. Genes Dev. 8:9-22.
62. Polyak, K., M. H. Lee, B. H. Erdjument, A. Koff, J. M. Roberts, P. Tempst, and J. Massague. 1994. Cloning of p27Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell 78:59-66.
63. Qui, R.-G., J. Chen, D. Kirn, F. McCormick, and M. Symons. 1995. An essential role for rac in ras transformation. Nature 374:457-459.
64. Qainlan, M. P. 1993. E1A 12S in the absence of E1B or other cooperating oncogenes enables cells to overcome apoptosis. Oncogene 8:3289-3296.
65. Quinlan, M. P., and J. L. Douglas. 1992. Immortalization of primary epithelial cells requires first and second-exon functions of adenovirus type 5 12S. J. Virol. 66:2020-2030.
66. Quinlan, M. P., and T. Grodzicker. 1987. Adenovirus E1A 12S protein induces DNA synthesis and proliferation in primary epithelial cells in both the presence and absence of serum. J. Virol. 61:673-682.
67. Quinlan, M. P., N. Sullivan, and T. Grodzicker. 1987. Growth factor(s) produced during infection with an adenovirus variant stimulates proliferation of nonestablished epithelial cells. Proc. Natl. Acad. Sci. USA 84:3283-3287.
68. Quinlan, M. P., P. Whyte, and T. Grodzicker. 1988. Growth factor induction by the adenovirus type 5 E1A 12S protein is required for immortalization of primary epithelial cells. Mol. Cell. Biol. 8:3191-3203.
69. Ridley, A. J. 1995. Rho-related proteins: actin cytoskeleton and cell cycle. Curr. Opin. Genet. Dev. 5:24-30.
70. Ridley, A. J., and A. Hall. 1992. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70:389-399.
71. Roche, S., S. Fumagalli, and S. A. Courtneidge. 1995. Requirement for Src family protein tyrosine kinases in G2 for fibroblast cell division. Science 269:1567-1569.
72. Ruley, H. E. 1983. Adenovirus early region 1A enables viral and cellular transforming genes to transform primary cells in culture. Nature (London) 304:602-606.
73. Sabe, H., M. Hamaguchi, and H. Hanafusa. 1997. Cell to substratum adhesion is involved in v-Src-induced cellular protein tyrosine phosphorylation: implication for the adhesion-regulated protein tyrosine phosphatase activity. Oncogene 14:1779-1788.
74. Schieffer, B., W. G. Paxton, Q. Chai, M. B. Marrero, and K. E. Bernstein. 1996. Angiotensin II controls p21ras activity via pp60c-src. J. Biol. Chem. 271:10329-10333.
75. Schlaepfer, D. D., S. K. Hanks, T. Hunter, and P. Van der Geer. 1994. Integrin-mediated signal transduction linked to ras pathway by GRB2 binding to focal adhesion kinase. Nature (London) 372:786-791.
76. Schlaepfer, D. D., and T. Hunter. 1996. Evidence for in vivo phosphorylation of the Grb2 SH2-domain binding site on focal adhesion kinase by Src-family protein-tyrosine kinases. Mol. Cell. Biol. 16:5623-5633.
77. Scholz, G., C. Martinerie, B. Perbal, and H. Hanafusa. 1996. Transcriptional down regulation of a novel proto-oncogene in fibroblasts transformed by p60v-src. Mol. Cell. Biol. 16:481-6.
78. INK4. Science 267:249-252.
79. Stokoe, D., and F. McCormick. 1997. Activation of c-Raf-1 by ras and src through different mechanisms: activation in vivo and in vitro. EMBO J. 16:2384-2396.
80. Subramanian, T., M. Kuppuswamy, R. J. Nasr, and G. Chinnadurai. 1988. An N-terminal region of adenovirus E1A essential for cell transformation and induction of an epithelial cell growth factor. Oncogene 2:105-112.
81. Subramanian, T., M. La Regina, and G. Chinnadurai. 1989. Enhanced ras oncogene mediated cell transformation and tumorigenesis by adenovirus 2 mutants lacking the c-terminal region of E1a protein. Oncogene 4:415-420.
82. Subramanian, T., S. E. Malstrom, and G. Chinnadurai. 1991. Requirement of the C-terminal region of adenovirus E1a for cell transformation in cooperation with E1b. Oncogene 6:1171-1173.
83. Tavoloni, N., and H. Inoue. 1997. Cellular aging is a critical determinant of primary cell resistance to v-src transformation. J. Virol. 71:237-247.
84. Tavoloni, N., H. Inoue, H. Sabe, and H. Hanafusa. 1994. v-src transformation of rat embryo fibroblasts. Inefficient conversion to anchorage-independent growth involves heterogeneity of primary cultures. J. Cell Biol. 126:475-483.
85. 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.
86. Vogelstein, B., and K. W. Kinzler. 1993. The multistep nature of cancer. Trends Genet. 9:138-141.
87. Vollet, J. J., J. S. Brugge, C. A. Noonan, and J. S. Butel. 1977. The role of SV40 gene A in the alteration of microfilaments in transformed cells. Exp. Cell Res. 105:119-126.
88. Wang, H. G., E. Moran, and P. Yaciuk. 1995. E1A promotes association between p300 and pRB in multimeric complexes required for normal biological activity. J Virol. 69:7917-7924.
89. Whyte, P., H. E. Ruley, and E. Harlow. 1988. Two regions of the adenovirus early region 1A proteins are required for transformation. J. Virol. 62:257-265.
90. Whyte, P., N. M. Williamson, and E. Harlow. 1989. Cellular targets for transformation by the adenovirus E1A proteins. Cell 56:67-75.
91. Wigler, M., A. Pellicer, S. Silverstein, R. Axel, G. Urlaub, and L. Chasin. 1979. DNA-mediated transfer of the adenine phosphoribosyltransferase locus into mammalian cells. Proc. Natl. Acad. Sci. USA 76:1373-1376.
92. Williams, N., T. M. Roberts, and P. Li. 1992. Both p21ras and pp60v-src are required, but neither alone is sufficient, to activate the raf-1 kinase. Proc. Natl. Acad. Sci. USA 89:2922-2926.
93. Zerler, B., R. J. Roberts, M. B. Mathews, and E. Moran. 1987. Different functional domains of the adenovirus E1A gene are involved in regulation of host cell cycle products. Mol. Cell. Biol. 7:821-829.
94. Zhao, J. F., H. Nakano, and S. Sharma. 1995. Suppression of RAS and MOS transformation by radicicol. Oncogene 11:161-173.