E1A oncogene-induced cellular sensitization to immune-mediated apoptosis is independent of p53 and resistant to blockade by E1B 19 kDa protein

Experimental Cell Research

Volumn 252, Issue 1, 1999, Pages 199-210

  Cook, James L ^a   Routes, Barbara A ^b   Leu, Cheryl Y ^b   Walker, Thomas A ^b   Colvin, Kelley L ^b  

^a UNIVERSITY OF ILLINOIS   (United States)

^b NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

Author keywords

Adenovirus; Apoptosis; Cytolytic lymphocyte; E1A; E1B 19 kDa; p53; Tumor necrosis factor alpha

Indexed keywords

GENE PRODUCT; PROTEIN BCL 2; PROTEIN P53; TUMOR NECROSIS FACTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL ONCOGENE; CONTROLLED STUDY; GENE EXPRESSION; GENE FUNCTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOCOMPETENCE; IMMUNOMODULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SENSITIZATION; TUMOR CELL;

EID: 0033543987     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1006/excr.1999.4617     Document Type: Article

References (95)

1. Ames R. S., Holskin B., Mitcho M., Shalloway D., Chen M. J. Induction of sensitivity to the cytotoxic action of tumor necrosis factor alpha by adenovirus E1A is independent of transformation and transcriptional activation. J. Virol. 64:1990;4115-4122.
2. Ashkenazi A., Dixit M. Death receptors: Signaling and modulation. Science. 281:1998;1305-1308.
3. Bernards R., Houweling A., Schrier P. I., Bos J. L., van der Eb A. J. Characterization of cells transformed by Ad5/Ad12 hybrid early region I plasmids. Virology. 120:1982;422-432.
4. Boulakia C. A., Chen G., Ng F. W., Teodoro J. G., Branton P. E., Nicholson D. W., Poirier G. G., Shore G. C. Bcl-2 and adenovirus E1B 19 kDa protein prevent E1A-induced processing of CPP32 and cleavage of poly(ADP-ribose) polymerase. Oncogene. 12:1996;529-535.
5. Chen C. H., Zhang J., Ling C. C. Transfected c-myc and c-Ha-ras modulate radiation-induced apoptosis in rat embryo cells. Radiat. Res. 139:1994;307-315.
6. Chen C. Y., Faller D. V. Direction of p21ras-generated signals towards cell growth or apoptosis is determined by protein kinase C and Bcl-2. Oncogene. 11:1995;1487-1498.
7. Chen C. Y., Faller D. V. Phosphorylation of Bcl-2 protein and association with p21Ras in Ras-induced apoptosis. J. Biol. Chem. 271:1996;2376-2379.
8. Chen M.-J., Holskin B., Strickler J., Gorniak J., Clark M. A., Johnson P. J., Mitcho M., Shalloway D. Induction by E1A oncogene expression of cellular susceptibility to lysis by TNF. Nature. 330:1987;581-583.
9. Chiou S. K., Rao L., White E. Bcl-2 blocks p53-dependent apoptosis. Mol. Cell Biol. 14:1994;2556-2563.
10. Chiou S. K., Tseng C. C., Rao L., White E. Functional complementation of the adenovirus E1B 19-kilodalton protein with Bcl-2 in the inhibition of apoptosis in infected cells. J. Virol. 68:1994;6553-6566.
11. Chiou S. K., White E. p300 binding by E1A cosegregates with p53 induction but is dispensable for apoptosis. J. Virol. 71:1997;3515-3525.
12. Chiu V. K., Walsh C. M., Liu C. C., Reed J. C., Clark W. R. Bcl-2 blocks degranulation but not fas-based cell-mediated cytotoxicity. J. Immunol. 154:1995;2023-2032.
13. Clarke A. R., Purdie C. A., Harrison D. J., Morris R. G., Bird C. C., Hooper M. L., Wyllie A. H. Thymocyte apoptosis induced by p53-dependent and independent pathways [see comments]. Nature. 362:1993;849-852.
14. Cook J., Iklé D., Routes B. Natural killer cell ontogeny in the athymic rat: Relationship between functional maturation and acquired resistance to E1A oncogene-expressing cells. J. Immunol. 155:1995;5512-5518.
15. Cook J., Krantz C., Routes B. Role of p300-family proteins in E1A oncogene induction of cytolytic susceptibility and tumor rejection. Proc. Natl. Acad. Sci. USA. 93:1996;13985-13990.
16. Cook J., Routes B., Walker T., Colvin K., Routes J. E1A oncogene induction of cellular susceptibility to killing by cytolytic lymphocytes through target cell sensitization to apoptotic injury. Exp. Cell Res. 251:1999;414-423.
17. Cook J. L., Hauser J., Patch C. T., Lewis A. M. Jr., Levine A. S. Adenovirus 2 early gene expression promotes susceptibility to effector cell lysis of hybrids formed between hamster cells transformed by adenovirus 2 and simian virus 40. Proc. Natl. Acad. Sci. USA. 80:1983;5995-5999.
18. Cook J. L., Hibbs J. B. Jr., Lewis A. M. Jr. DNA virus-transformed hamster cell-host effector cell interactions: Level of resistance to cytolysis correlated with tumorigenicity. Int. J. Cancer. 30:1982;795-803.
19. Cook J. L., Lewis A. M. Jr. Differential NK cell and macrophage killing of hamster cells infected with nononcogenic or oncogenic adenovirus. Science. 224:1984;612-615.
20. Cook J. L., Lewis A. M. Jr. Immunological surveillance against DNA virus-transformed cells: Correlations between natural killer cell cytolytic competence and tumor susceptibility of athymic rodents. J. Virol. 61:1987;2155-2161.
21. Cook J. L., Lewis A. M. Jr., Klimkait T., Knust B., Doerfler W., Walker T. A. In vivo evolution of adenovirus 2-transformed cell virulence associated with altered E1A gene function. Virology. 163:1988;374-390.
22. Cook J. L., May D. L., Lewis A. M. Jr., Walker T. A. Adenovirus E1A gene induction of susceptibility to lysis by natural killer cells and activated macrophages in infected rodent cells. J. Virol. 61:1987;3510-3520.
23. Cook J. L., May D. L., Wilson B. A., Holskin B., Chen M.-J., Shalloway D., Walker T. A. Role of tumor necrosis factor-alpha in E1A oncogene-induced susceptibility of neoplastic cells to lysis by natural killer cells and activated macrophages. J. Immunol. 142:1989;4527-4534.
24. Cook J. L., Potter T. A., Bellgrau D., Routes B. A. E1A oncogene expression in target cells induces cytolytic susceptibility at a post-recognition stage in the interaction with killer lymphocytes. Oncogene. 13:1996;833-842.
25. Cook J. L., Walker T. A., Lewis A. M. Jr., Ruley H. E., Graham F. L., Pilder S. H. Expression of the adenovirus E1A oncogene during cell transformation is sufficient to induce susceptibility to lysis by host inflammatory cells. Proc. Natl. Acad. Sci. USA. 83:1986;6965-6969.
26. Cook J. L., Wilson B. A., Wolf L. A., Walker T. A. E1A oncogene expression level in sarcoma cells: An independent determinant of cytolytic susceptibility and tumor rejection. Oncogene. 8:1993;625-635.
27. Curnow S. J., Glennie M. J., Stevenson G. T. The role of apoptosis in antibody-dependent cellular cytotoxicity. Cancer Immunol. Immunother. 36:1993;149-155.
28. Darmon A., Nicholson D., Bleackley R. Activation of the apoptotic protease CPP32 by cytotoxic T-cell-derived granzyme B. Nature. 377:1995;446-448.
29. Debbas M., White E. Wild-type p53 mediates apoptosis by E1A, which is inhibited by E1B. Genes Dev. 7:1993;546-554.
30. Deng J., Xia W., Hung M. C. Adenovirus 5 E1A-mediated tumor suppression associated with E1A-mediated apoptosis in vivo. Oncogene. 17:1998;2167-2175.
31. Diller L., Kassel J., Nelson C., Gryka M., Litwak G., Gebhardt M., Bressac B., Ozturk M., Baker S., Vogelstein B., Friend S. p53 functions as a cell cycle control protein in osteosarcomas. Mol. Cell. Biol. 10:1990;5772-5781.
32. Duerksen-Hughes P., Wold W. S. M., Gooding L. R. Adenovirus E1A renders infected cells sensitive to cytolysis by tumor necrosis factor. J. Immunol. 143:1989;4193-4200.
33. Duke R., Cohen J. Morphological and biochemical assays of apoptosis. Curr. Prot. Immunol. 3:1992;3.17.11-13.17.16.
34. Fernandes R. S., McGowan A. J., Cotter T. G. Mutant H-ras overexpression inhibits drug and U.V. induced apoptosis. Anticancer Res. 16:1996;1691-1705.
35. Fernandez A., Marin M. C., McDonnell T., Ananthaswamy H. N. Differential sensitivity of normal and Ha-ras-transformed C3H mouse embryo fibroblasts to tumor necrosis factor: Induction of bcl-2, c-myc, and manganese superoxide dismutase in resistant cells. Oncogene. 9:1994;2009-2017.
36. Fuchs E. J., McKenna K. A., Bedi A. p53-dependent DNA damage-induced apoptosis requires Fas/APO-1-independent activation of CPP32beta. Cancer Res. 57:1997;2550-2554.
37. Gooding L. R., Aquino L., Duerksen-Hughes P. J., Day D., Horton T. M., Yei S., Wold W. S. M. The E1B 19,000-molecular-weight protein of group C adenoviruses prevents tumor necrosis factor cytolysis of human cells but not of mouse cells. J. Virol. 65:1991;3083-3094.
38. Gottlieb E., Oren M. p53 facilitates pRb cleavage in IL-3-deprived cells: Novel pro-apoptotic activity of p53. EMBO J. 17:1998;3587-3596.
39. Graham F. L., Smiley J., Russell W. C., Nairn R. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J. Gen. Virol. 36:1977;59-72.
40. Harlow E., Franza R. Jr., Schley C. Monoclonal antibodies specific for adenovirus early region 1A proteins: Extensive heterogeneity in early region 1A products. J. Virol. 55:1985;533-546.
41. Harvey D., Levine A. p53 alteration is a common event in the spontaneous immortalization of primary BALB/c murine embryo fibroblasts. Genes Dev. 5:1991;2375-2385.
42. Hashimoto S., Ishii A., Yonehara S. The E1B oncogene of adenovirus confers cellular resistance to cytotoxicity of tumor necrosis factor and monoclonal anti-Fas antibody. Int. Immunol. 3:1991;343-351.
43. Jeoung D. I., Tang B., Sonenberg M. Effects of tumor necrosis factor-alpha on antimitogenicity and cell cycle-related proteins in MCF-7 cells. J. Biol. Chem. 270:1995;18367-18373.
44. Kenyon D. J., Dougherty J., Raska J. K. Tumorigenicity of adenovirus-transformed cells and their sensitivity to tumor necrosis factor alpha and NK/LAK cell cytolysis. Virology. 180:1991;818-821.
45. Kinoshita T., Yokota T., Arai K., Miyajima A. Regulation of Bcl-2 expression by oncogenic Ras protein in hematopoietic cells. Oncogene. 10:1995;2207-2212.
46. Knall C., Smith P. A., Potter T. A. CD8-dependent CTL require co-engagement of CD8 and the TCR for phosphatidylinositol hydrolysis, but CD8-independent CTL do not and can kill in the absence of phosphatidylinositol hydrolysis. Int. Immunol. 7:1995;995-1004.
47. Lanni J. S., Lowe S. W., Licitra E. J., Liu J. O., Jacks T. p53-independent apoptosis induced by paclitaxel through an indirect mechanism. Proc. Natl. Acad. Sci. USA. 94:1997;9679-9683.
48. Laster S. M., Wood J. G., Gooding L. R. Tumor necrosis factor can induce both apoptic and necrotic forms of cell lysis. J. Immunol. 141:1988;2629-2634.
49. Lavoie J. N., Nguyen M., Marcellus R. C., Branton P. E., Shore G. C. E4orf4, a novel adenovirus death factor that induces p53-independent apoptosis by a pathway that is not inhibited by zVAD-fmk. J. Cell. Biol. 140:1998;637-645.
50. Lewis A. Jr., Cook J. A new role for DNA virus early proteins in viral carcinogenesis. Science. 227:1985;15-20.
51. Lewis A. M. Jr., Cook J. L. The interface between adenovirus-transformed cells and cellular immune response in the challenged host. Curr. Topics Microbiol. Immunol. 110:1984;1-22.
52. Lill N. L., Tevethia M. J., Eckner R., Livingston D. M., Modjtahedi N. p300 family members associate with the carboxyl terminus of simian virus 40 large tumor antigen. J. Virol. 71:1997;129-137.
53. Lin H. J., Eviner V., Prendergast G. C., White E. Activated H-ras rescues E1A-induced apoptosis and cooperates with E1A to overcome p53-dependent growth arrest. Mol. Cell Biol. 15:1995;4536-4544.
54. Lowe S. W., Ruley H. E. Stabilization of the p53 tumor suppressor is induced by adenovirus 5 E1A and accompanies apoptosis. Genes Dev. 7:1993;535-545.
55. Lowe S. W., Ruley H. E., Jacks T., Housman D. E. p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell. 74:1993;957-967.
56. Lowe S. W., Schmitt E. M., Smith S. W., Osborne B. A., Jacks T. p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature. 362:1993;847-849.
57. Marcellus R. C., Teodoro J. G., Wu T., Brough D. E., Ketner G., Shore G. C., Branton P. E. Adenovirus type 5 early region 4 is responsible for E1A-induced p53-independent apoptosis. J. Virol. 70:1996;6207-6215.
58. Mayo M. W., Wang C. Y., Cogswell P. C., Rogers-Graham K. S., Lowe S. W., Der C. J., Baldwin A. S. Jr. Requirement of NF-kappaB activation to suppress p53-independent apoptosis induced by oncogenic Ras. Science. 278:1997;1812-1815.
59. Medema J. P., Toes R. E., Scaffidi C., Zheng T. S., Flavell R. A., Melief C. J., Peter M. E., Offringa R., Krammer P. H. Cleavage of FLICE (caspase-8) by granzyme B during cytotoxic T lymphocyte-induced apoptosis. Eur. J. Immunol. 27:1997;3492-3498.
60. Memon S. A., Moreno M. B., Petrak D., Zacharchuk C. M. Bcl-2 blocks glucocorticoid- but not Fas- or activation-induced apoptosis in a T cell hybridoma. J. Immunol. 155:1995;4644-4652.
61. Moore J., Boswell S., Hoffman R., Burgess G., Hromas R. Mutant H-ras over-expression inhibits a random apoptotic nuclease in myeloid leukemia cells. Leukocyte Res. 17:1993;703-709.
62. Mymryk J. S., Shire K., Bayley S. T. Induction of apoptosis by adenovirus type 5 E1A in rat cells requires a proliferation block. Oncogene. 9:1994;1187-1193.
63. Ng F. W., Nguyen M., Kwan T., Branton P. E., Nicholson D. W., Cromlish J. A., Shore G. C. p28 Bap31, a Bcl-2/Bcl-XL- and procaspase-8-associated protein in the endoplasmic reticulum. J. Cell Biol. 139:1997;327-338.
64. Orth K., Chinnaiyan A. M., Garg M., Froelich C. J., Dixit V. M. The CED-3/ICE-like protease Mch2 is activated during apoptosis and cleaves the death substrate lamin A. J. Biol. Chem. 271:1996;16443-16446.
65. Perez D., White E. E1B 19K inhibits Fas-mediated apoptosis through FADD-dependent sequestration of FLICE. J. Cell Biol. 141:1998;1255-1266.
66. Querido E., Teodoro J. G., Branton P. E. Accumulation of p53 induced by the adenovirus E1A protein requires regions involved in the stimulation of DNA synthesis. J. Virol. 71:1997;3526-3533.
67. Rao L., Debbas M., Sabbatini P., Hockenbery D., Korsmeyer S., White E. The adenovirus E1A proteins induce apoptosis, which is inhibited by the E1B 19-kDa and Bcl-2 proteins. Proc. Natl. Acad. Sci. USA. 89:1992;7742-7746.
68. Raska K. Jr., Gallimore P. H. An inverse relation of the oncogenic potential of adenovirus-transformed cells and their sensitivity to killing by syngeneic natural killer cells. Virology. 123:1982;8-18.
69. Reed J. C. Bcl-2 and the regulation of programmed cell death. J. Cell Biol. 124:1994;1-6.
70. Renvoize C., Roger R., Moulian N., Bertoglio J., Breard J. Bcl-2 expression in target cells leads to functional inhibition of caspase-3 protease family in human NK and lymphokine-activated killer cell granule-mediated apoptosis. J. Immunol. 159:1997;126-134.
71. Routes J. M., Cook J. L. E1A gene expression induces susceptibility to killing by NK cells following immortalization but not adenovirus infection of human cells. Virology. 210:1995;421-428.
72. Sabbatini P., Han J., Chiou S. K., Nicholson D. W., White E. Interleukin 1 beta converting enzyme-like proteases are essential for p53-mediated transcriptionally dependent apoptosis. Cell Growth Differ. 8:1997;643-653.
73. Sabbatini P., Lin J., Levine A. J., White E. Essential role for p53-mediated transcription in E1A-induced apoptosis. Genes Dev. 9:1995;2184-2192.
74. Sarin A., Haddad E. K., Henkart P. A. Caspase dependence of target cell damage induced by cytotoxic lymphocytes. J. Immunol. 161:1998;2810-2816.
75. Sawada Y., Fohring B., Shenk T. E., Raska K. Jr. Tumorigenicity of adenovirus-transformed cells; Region E1A of adenovirus 12 confers resistance to natural killer cells. Virology. 147:1985;413-421.
76. Scaffidi C., Fulda S., Srinivasan A., Friesen C., Li F., Tomaselli K. J., Debatin K. M., Krammer P. H., Peter M. E. Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 17:1998;1675-1687.
77. Schroter M., Lowin B., Borner C., Tschopp J. Regulation of Fas(Apo-1/CD95)- and perforin-mediated lytic pathways of primary cytotoxic T lymphocytes by the protooncogene bcl-2. Eur. J. Immunol. 25:1995;3509-3513.
78. Scolnick D. M., Chehab N. H., Stavridi E. S., Lien M. C., Caruso L., Moran E., Berger S. L., Halazonetis T. D. CREB-binding protein and p300/CBP-associated factor are transcriptional coactivators of the p53 tumor suppressor protein. Cancer Res. 57:1997;3693-3696.
79. Sheil J. M., Gallimore P. H., Zimmer S. G., Sopori M. L. Susceptibility of adenovirus 2-transformed rat cell lines to natural killer (NK) cells: Direct correlation between NK resistance and in vivo tumorigenesis. J. Immunol. 132:1984;1578-1582.
80. Shisler J., Duerksen-Hughes P., Hermiston T. M., Wold W. S., Gooding L. R. Induction of susceptibility to tumor necrosis factor by E1A is dependent on binding to either p300 or p105-Rb and induction of DNA synthesis. J. Virol. 70:1996;68-77.
81. Shtrichman R., Kleinberger T. Adenovirus type 5 E4 open reading frame 4 protein induces apoptosis in transformed cells. J. Virol. 72:1998;2975-2982.
82. Smyth M. J., Trapani J. A. The relative role of lymphocyte granule exocytosis versus death receptor-mediated cytotoxicity in viral pathophysiology. J. Virol. 72:1998;1-9.
83. Somasundaram K., El-Deiry W. S. Inhibition of p53-mediated transactivation and cell cycle arrest by E1A through its p300/CBP-interacting region. Oncogene. 14:1997;1047-1057.
84. Strasser A., Harris A. W., Huang D. C., Krammer P. H., Cory S. Bcl-2 and Fas/APO-1 regulate distinct pathways to lymphocyte apoptosis. EMBO J. 14:1995;6136-6147.
85. Teodoro J. G., Shore G. C., Branton P. E. Adenovirus E1A proteins induce apoptosis by both p53-dependent and p53-independent mechanisms. Oncogene. 11:1995;467-474.
86. Trapani J. A., Jans D. A., Jans P. J., Smyth M. J., Browne K. A., Sutton V. R. Efficient nuclear targeting of granzyme B and the nuclear consequences of apoptosis induced by granzyme B and perforin are caspase-dependent, but cell death is caspase-independent. J. Biol. Chem. 273:1998;27934-27938.
87. Vanhaesebroeck B., Timmers H. T., Pronk G. J., van Roy F., Van der Eb A. J., Fiers W. Modulation of cellular susceptibility to the cytotoxic/cytostatic action of tumor necrosis factor by adenovirus E1 gene expression is cell type-dependent. Virology. 176:1990;362-368.
88. Vater C. A., Bartle L. M., Dionne C. A., Littlewood T. D., Goldmacher V. S. Induction of apoptosis by tamoxifen-activation of a p53-estrogen receptor fusion protein expressed in E1A and T24 H-ras transformed p53-/- mouse embryo fibroblasts. Oncogene. 13:1996;739-748.
89. Vujanovic N. L., Nagashima S., Herberman R. B., Whiteside T. L. Nonsecretory apoptotic killing by human NK cells. J. Immunol. 157:1996;1117-1126.
90. Walker T. A., Wilson B. A., Lewis A. M. Jr., Cook J. L. E1A oncogene induction of cytolytic susceptibility eliminates sarcoma cell tumorigenicity. Proc. Natl. Acad. Sci. USA. 88:1991;6491-6495.
91. Wang H. G., Millan J. A., Cox A. D., Der C. J., Rapp U. R., Beck T., Zha H., Reed J. C. R-Ras promotes apoptosis caused by growth factor deprivation via a Bcl-2 suppressible mechanism. J. Cell Biol. 129:1995;1103-1114.
92. White E. Life, death, and the pursuit of apoptosis. Genes Dev. 10:1996;1-15.
93. White E., Sabbatini P., Debbas M., Wold W. S., Kusher D. I., Gooding L. R. The 19-kilodalton adenovirus E1B transforming protein inhibits programmed cell death and prevents cytolysis by tumor necrosis factor alpha. Mol. Cell Biol. 12:1992;2570-2580.
94. Yin D., Kondo S., Barnett G. H., Morimura T., Takeuchi J. Tumor necrosis factor-alpha induces p53-dependent apoptosis in rat glioma cells. Neurosurgery. 37:1995;758-762.
95. Yoshida K., Murohashi I., Hirashima K. p53-independent induction of p21 (WAF1/CIP1) during differentiation of HL-60 cells by tumor necrosis factor alpha. Int. J. Hematol. 65:1996;41-48.