Human T-cell lymphotropic/leukemia virus type 1 tax abrogates p53- induced cell cycle arrest and apoptosis through its CREB/ATF functional domain

Journal of Virology

Volumn 72, Issue 11, 1998, Pages 8852-8860

  Mulloy, J C ^a   Kislyakova, T ^a,c   Cereseto, A ^a   Casareto, L ^a   Lomonico, A ^a   Fullen, J ^a   Lorenzi, M V ^a   Cara, A ^a,d   Nicot, C ^a   Giam, C Z ^b   Franchini, G ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^c INSTITUTE OF CYTOLOGY   (Russian Federation)

^d MOUNT SINAI MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; PROTEIN P53; TAX PROTEIN; VIRUS PROTEIN; VIRUS VECTOR;

APOPTOSIS; ARTICLE; CHLORIDE TRANSPORT; CONTROLLED STUDY; GENE DISRUPTION; HALF LIFE TIME; HUMAN; HUMAN CELL; HUMAN T CELL LEUKEMIA VIRUS 1; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STRUCTURE; TRANSACTIVATION;

EID: 0031661780     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.11.8852-8860.1998     Document Type: Article

References (63)

1. Agarwal, M. L., W. R. Taylor, M. V. Chernov, O. V. Chernova, and G. R. Stark. 1998. The p53 network. J. Biol. Chem. 273:1-4.
2. Akagi, T., H. Ono, N. Tsuchida, and K. Shimotohno. 1997. Aberrant expression and function of p53 in T-cells immortalized by HTLV-I Tax 1. FEBS Lett. 406:263-266.
3. Aldovini, A., A. De Rossi, M. V. Feinberg, F. Wong-Stall, and G. Franchini. 1986. Molecular analysis of a deletion mutant provirus of type I human T-cell lymphotropic virus: evidence for a doubly spliced x-lor mRNA. Proc. Natl. Acad. Sci. USA 83:38-42.
4. Avantaggiati, M. L., V. Ogryzko, K. Gardner, A. Giordano, A. S. Levine, and K. Kelly. 1987. Recruitment of p300/CBP in p53-dependent signal pathways. Cell 89:1175-1184.
5. Berneman, Z. N., R. B. Gartenhaus, M. S. Reitz, Jr., W. A. Blattner, A. Manns, B. O. Hanchard, R. C. Gallo, and M. E. Klotman. 1992. Expression of alternatively spliced human T-lymphotropic virus type 1 pX mRNA in infected cell lines and in primary uncultured cells from patients with adult T-cell leukemia/lymphoma and healthy carriers. Proc. Natl. Acad. Sci. USA 89:3005-3009.
6. Brockmann, D., and H. Esche. 1995. Regulation of viral and cellular gene expression by E1A proteins encoded by the oncogenic adenovirus type 12. Curr. Top. Microbiol. Immunol. 199:81-112.
7. Caron, C., R. Rousset, C. Beraud, V. Moncollin, J. M. Egly, and P. Jalinot. 1993. Functional and biochemical interaction of the HTLV-I Taxi transactivator with TBP. EMBO J. 12:4269-4278.
8. waf1/cip1 expression in human T-cell lymphotropic/leukemia virus type I-transformed T cells. Blood 88:1551-1560.
9. Cesarman, E., A. Chadburn, G. Inghirami, G. Gaidano, and D. M. Knowles. 1992. Structural and functional analysis of oncogenes and tumor suppressor genes in adult T-cell leukemia/lymphoma shows frequent p53 mutations. Blood 80:3205-3216.
10. Cheng, J., and M. Haas. 1990. Frequent mutations in the p53 tumor suppressor gene in human leukemia T-cell lines. Mol. Cell. Biol. 10:5502-5509.
11. Chichlia, K., G. Moldenhauer, P. T. Daniel, M. Busslinger, L. Gazzolo, V. Schirrmacher, and K. Khazaie. 1995. Immediate effects of reversible HTLV-1 Tax function: T-cell activation and apoptosis. Oncogene 10:269-277.
12. Chiou, S. K., and E. White. 1997. p300 binding by E1A cosegregates with p53 induction but is dispensable for apoptosis. J. Virol. 71:3515-3525.
13. Franchini, G. 1995. Molecular mechanisms of human T-cell leukemia/lymphotropic virus type I infection. Blood 86:3619-3639.
14. Gallo, R. C. 1986. The first human retrovirus. Sci. Am. 255:88-98.
15. Gartenhaus, R. B., and P. Wang. 1995. Functional inactivation of wild-type p53 protein correlates with loss of IL-2 dependence in HTLV-I transformed human T lymphocytes. Leukemia 9:2082-2086.
16. Gessain, A., F. Saal, M. L. Giron, J. Lasneret, S. Lagaye, O. Gout, G. De The, F. Sigaux, and J. Peries. 1990. Cell surface phenotype and human T lymphotropic virus type 1 antigen expression in 12 T cell lines derived from peripheral blood and cerebrospinal fluid of West Indian, Guyanese and African patients with tropical spastic paraparesis. J. Gen. Virol. 71:333-341.
17. Graham, F. L., and A. J. van der Eb. 1973. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology 52:456-467.
18. Grassmann, R., C. Dengler, I. Muller-Fleckenstein, B. Fleckenstein, K. McGuire, M.-C. Dokhelar, J. G. Sodroski, and W. A. Haseltine. 1989. Transformation to continuous growth of primary human T lymphocytes by human T-cell leukemia virus type I X-region genes transduced by a Herpesvirus saimiri vector. Proc. Natl. Acad. Sci. USA 86:3351-3355.
19. Gu, W., X.-L. Shi, and R. G. Roeder. 1997. Synergistic activation of transcription by CBP and P53. Nature 387:819-823.
20. Harada, H., T. Fujita, M. Miyamoto, Y. Kimura, M. Maruyama, A. Furia, T. Miyata, and T. Taniguchi. 1989. Structurally similar but functionally distinct factors, IRF-1 and IRF-2, bind to the same regulatory elements of IFN and IFN-inducible genes. Cell 58:729-739.
21. Harada, H., K. Willison, J. Sakakibara, M. Miyamoto, T. Fujita, and T. Taniguchi. 1990. Absence of the type I IFN system in EC cells: transcriptional activator (IRF-1) and repressor (IRF-2) genes are developmentally regulated. Cell 63:303-312.
22. Hatta, Y., T. Hirama, C. W. Miller, Y. Yamada, M. Tomonaga, and H. P. Koeffler. 1995. Homozygous deletions of the p15 (MTS2) and p16 (CDKN2/ MTS1) genes in adult T-cell leukemia. Blood 85:2699-2704.
23. Hickman, E. S., S. Bates, and K. H. Vousden. 1997. Perturbation of the p53 response by human papillomavirus type 16 E7. J. Virol. 71:3710-3718.
24. Kastan, M. B., O. Onyekwere, D. Sidransky, B. Vogelstein, and R. W. Craig. 1991. Participation of p53 protein in the cellular response to DNA damage. Cancer Res. 51:6304-6311.
25. Kern, S. E., J. A. Pietenpol, S. Thiagalingam, A. Seymour, K. W. Kinzler, and B. Vogelstein. 1992. Oncogenic forms of p53 inhibit p53-regulated gene expression. Science 256:827-830.
26. Kwok, R. P. S., M. E. Laurance, J. R. Lundblad, P. S. Goldman, H.-M. Shih, L. M. Connor, S. J. Marriott, and R. H. Goodman. 1996. Control of cAMP-regulated enhancers by the viral transactivator Tax through CREB and the co-activator CBP. Nature 18:642-646.
27. Levine, A. J. 1997. p53, the cellular gatekeeper for growth and division. Cell 88:323-331.
28. Li, W., P. Michieli, M. Alimandi, M. V. Lorenzi, Y. Wu, L.-H. Wang, M. A. Heidaran, and J. H. Pierce, 1996. Expression of an ATP binding mutant of PKC-delta inhibits Sis-induced transformation of NIH3T3 cells. Oncogene 13:731-737.
29. Lill, N. L., S. R. Grossmann, D. Ginsberg, J. DeCaprio, and D. M. Livingston. 1997. Binding and modulation of p53 by p300/CBP coactivators. Nature 387:823-827.
30. Lin, J.-X., T.-S. Migone, M. Tsang, M. Friedmann, J. A. Weatherbee, L. Shou, A. Yadauchi, E. T. Bloom, J. Mietz, S. John, and W. J. Leonard. 1995. The role of shared receptor motifs and common Stat proteins in the generation of cytokine pleiotropy and redundancy by IL-2, IL-4, IL-7, IL-13, and IL-15. Immunity 2:331-339.
31. INK4a. J. Virol. 71:1956-1962.
32. Lowe, S. W., and H. E. Ruley. 1993. Stabilization of the p53 tumor suppressor is induced by adenovirus 5 E1A and accompanies apoptosis. Genes. Dev. 7:535-545.
33. Migone, T.-S., J.-X. Lin, A. Cereseto, J. C. Mulloy, J. J. O'Shea, G. Franchini, and W. J. Leonard. 1995. Constitutively activated Jak-STAT pathway in T cells transformed with HTLV-I. Science 269:79-81.
34. Miyoshi, I., I. Kubonishi, S. Yoshimoto, T. Akagi, Y. Ohtsuki, Y. Shiraishi, K. Nagata, and Y. Hinuma. 1981. Type C virus particles in a cord T-cell line derived by co-cultivating normal human cord leukocytes and leukaemic T cells. Nature 294:770-771.
35. Neil, J. C., E. R. Cameron, and E. W. Baxter. 1997. p53 and tumor viruses: catching the guardian off-guard. Trends Microbiol. 5:115-120.
36. Nishimura, S., N. Asou, H. Suzushima, T. Okubo, T. Fujimoto, M. Osato, H. Yamaski, L. Lisha, and K. Takatsuki. 1995. p53 gene mutation and loss of heterozygosity are associated with increased risk of disease progression in adult T cell leukemia. Leukemia 9:598-604.
37. Kip1 cyclin-dependent kinase inhibitor prevented by rapamycin. Nature 372:570-573.
38. Ogawa, S., N. Hirano, N. Sato, T. Takahashi, A. Hangaishi, K. Tanaka, M. Kurokawa, T. Tanaka, K. Mitani, Y. Yazaki, and H. Hirai. 1994. Homozygous loss of the cyclin-dependent kinase 4-inhibitor (p16) gene in human leukemias. Blood 84:2431-2435.
39. Pise-Masison, C. A., K.-S. Choi, M. Radonovich, J. Dittmer, S.-J. Kim, and J. N. Brady. 1998. Inhibition of p53 transactivation function by the human T-cell lymphotropic virus type 1 Tax protein. J. Virol. 72:1165-1170.
40. Popovic, M., P. S. Sarin, M. Robert-Guroff, V. S. Kalyanaraman, D. Mann, J. Minowada, and R. C. Gallo. 1983. Isolation and transmission of human retrovirus (human T-cell leukemia virus). Science 219:856-859.
41. Querido, E., R. C. Marcellus, A. Lai, R. Charbonneau, J. G. Teodoro, G. Ketner, P. E. Branton. 1997. Regulation of p53 levels by the E1B 55-kilodalton protein and E4orf6 in adenovirus-infected cells. J. Virol. 71:3788-3798.
42. Reid, R. L., P. F. Lindholm, A. Mireskandari, J. Dittmer, and J. N. Brady. 1993. Stabilization of wild-type p53 in human T-lymphocytes transformed by HTLV-I. Oncogene 8:3029-3036.
43. Sakashita, A., T. Hattori, C. W. Miller, H. Suzushima, N. Asou, K. Takatuski, and H. P. Koeffler. 1992. Mutations of the p53 gene in adult T-cell leukemia. Blood 79:477-480.
44. Salahuddin, S. Z., P. D. Markam, F. Wong-Stall, G. Franchini, V. S. Kalyanaraman, and R. C. Gallo. 1983. Restricted expression of human T-cell leukemia-lymphoma virus (HTLV) in transformed human umbilical cord blood lymphocytes. Virology 129:51-64.
45. Scheffner, M., B. A. Werness, J. M. Huibregtse, A. J. Levine, and P. M. Howley. 1990. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63:1129-1136.
46. Seto, E., A. Usheva, G. Zambetti, J. Momand, N. Horikoshi, R. Weinmann, A. Levine, and T. Shenk. 1992. Wild-type p53 binds to the TATA-binding protein and represses transcription. Proc. Natl. Acad. Sci. USA 89:12028-12032.
47. Smith, M. R., and W. C. Greene. 1990. Identification of HTLV-I tax transactivator mutants exhibiting novel transcriptional phenotypes. Genes Dev. 4:1875-1885.
48. Strasser, A., A. W. Harris, T. Jacks, and S. Cory. 1994. DNA damage can induce apoptosis in proliferating lymphoid cells via p53-independent mechanisms inhibitable by Bcl-2. Cell 79:329-339.
49. ink4a and counteracts its inhibitory activity towards CDK4. EMBO J. 15:1607-1614.
50. Takada, S., N. Kaneniwa, N. Tsuchida, and K. Koike. 1997. Cytoplasmic retention of the p53 tumor suppressor gene product is observed in the hepatitis B virus X gene-transfected cells. Oncogene 15:1895-1901.
51. Tamura, T., M. Ishihra, M. S. Lamphler, N. Tanaka, I. Oishi, S. Alzawa, T. Matsuyama, T. W. Mak, S. Taki, and T. Taniguchi. 1995. An IRF-1-dependent pathway of DNA damage-induced apoptosis in mitogen-activated T lymphocytes. Nature 17:596-599.
52. Tanaka, N., M. Ishihara, M. Kitagawa, H. Harada, T. Kimura, T. Matsuyama, M. S. Lamphier, S. Aizawa, T. W. Mak, and T. Taniguchi. 1994. Cellular commitment to oncogene-induced transformation or apoptosis is dependent on the transcription factor IRF-1. Cell 77:829-839.
53. Teodoro, J. G., G. C. Shore, and P. E. Branton. 1995. Adenovirus E1A proteins induce apoptosis by both p53-dependent and p53-independent mechanisms. Oncogene 11:467-474.
54. Trovato, R., A. Cereseto, S. Takemoto, A. Gessain, T. Watanabe, T. Waldmann, and G. Franchini. Unpublished data.
55. Ueda, H., S. J. Ullrich, J. D. Gangemi, C. A. Kappel, L. Ngo, M. A. Feitelson, and G. Jay. 1995. Functional inactivation but not structural mutation of p53 causes liver cancer. Nat. Genet. 9:41-47.
56. Xu, X., S. H. Kang, O. Heidenreich, M. Okerholm, J. J. O'Shea, and M. I. Nerenberg. 1995. Constitutive activation of different Jak tyrosine kinases in human T-cell leukemia virus type I (HTLV-I) Tax protein or virus-transformed cells. J. Clin. Investig. 96:1548-1555.
57. Yamada, T., S. Yamaoka, T. Goto, M. Nakai, Y. Tsujimoto, and M. Hatanaka. 1994. The human T-cell leukemia virus type I Tax protein induces apoptosis which is blocked by the Bcl-2 protein. J. Virol. 68:3374-3379.
58. Yamada, Y., Y. Hatta, K. Murata, K. Sugawara, S. Ikeda, M. Mine, T. Maeda, Y. Hirakata, S. Kamihira, K. Tsukasaki, S. Ogawa, H. Hirai, H. P. Koeffler, and M. Tomonaga. 1997. Deletions of p15 and/or p16 genes as a poor-prognosis factor in adult T-cell leukemia. J. Clin. Oncol. 5:1778-1785.
59. Yamaoka, S., H. Inoue, M. Sakurai, T. Sugiyama, M. Hazama, T. Yamada, and M. Hatanaka. 1996. Constitutive activation of NF-kappa B is essential for transformation of rat fibroblasts by the human T-cell leukemia virus type I Tax protein. EMBO J. 15:873-887.
60. Yamato, K., T. Oka, M. Hiroi, Y. Iwanara, S. Sugito, N. Tsuchida, and I. Miyoshi. 1993. Aberrant expression of the p53 tumor suppressor gene in adult T-cell leukemia and HTLV-I-infected cells. Jpn. J. Cancer. Res. 84:4-8.
61. Yoshida, M., T. Suzuki, J. Fujisawa, and H. Hirai. 1995. HTLV-I oncoprotein Tax and cellular transcription factors. Curr. Top. Microbiol. Immunol. 193:79-89.
62. Zantema, A., J. A. Fransen, A. Davis-Olivier, F. C. Ramaekers, G. P. Voorjs, B. DeLeys, and A. J. Van der Eb. 1985. Localization of the E1B proteins of adenovirus 5 in transformed cells, as revealed by interaction with monoclonal antibodies. Virology 142:44-58.
63. Zantema, A., P. I. Schrier, A. Davis-Olivier, T. van Laar, R. T. Vaessen, and A. J. van der Eb. 1985. Adenovirus serotype determines association and localization of the large E1B tumor antigen with cellular tumor antigen p53 in transformed cells. Mol. Cell. Biol. 5:3084-3091.