Tax protein-induced expression of antiapoptotic Bfl-1 protein contributes to survival of human T-cell leukemia virus type 1 (HTLV-1)-infected T-cells

Journal of Biological Chemistry

Volumn 287, Issue 25, 2012, Pages 21357-21370

  Macaire, Héloïse ^a,b   Riquet, Aurélien ^a,b,c   Moncollin, Vincent ^c,d   Biémont Trescol, Marie Claude ^a,b,c   Dodon, Madeleine Duc ^a,c,d   Hermine, Olivier ^e   Debaud, Anne Laure ^a,b,c   Mahieux, Renaud ^a,c,d   Mesnard, Jean Michel ^f   Pierre, Marlène ^a,b,c   Gazzolo, Louis ^a,c,d   Bonnefoy, Nathalie ^a,b,c,g   Valentin, Hélène ^a,b,c  

^a UNIVERSITÉ DE LYON   (France)

^b INSERM   (France)

^c University Lyon i   (France)

^d UNIVERSITÉ DE LYON   (France)

^e HÔPITAL NECKER ENFANTS MALADES   (France)

^f CNRS   (France)

^g HOSPICES CIVILS DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-APOPTOTIC PROTEIN; ANTIAPOPTOTIC; BCL-2 FAMILY; CELLULAR FUNCTION; ETIOLOGIC AGENTS; ETOPOSIDE; GENE ACTIVATION; HUMAN T CELLS; LEUCINE ZIPPERS; REGULATORY PROTEIN; T CELLS; T-CELL LEUKEMIA; THERAPEUTIC TARGETS;

CELL CULTURE; CELL DEATH; GENES; TRANSCRIPTION; TRANSCRIPTION FACTORS; VIRUSES;

TAXATION;

BCL2 RELATED PROTEIN A1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN P100; PROTEIN P105; PROTEIN P50; PROTEIN P52; TAX PROTEIN; TRANSCRIPTION FACTOR REL; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR RELB;

ARTICLE; BCL 2 FETAL LIVER 1 GENE; BINDING SITE; CELL DEATH; CELL LINE; CELL REGENERATION; GENE; GENE ACTIVATION; GENE SILENCING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN T CELL LEUKEMIA VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; T LYMPHOCYTE; VIRUS SURVIVAL;

ADULT; ANTINEOPLASTIC AGENTS, PHYTOGENIC; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; BCL-X PROTEIN; BIPHENYL COMPOUNDS; CD4-POSITIVE T-LYMPHOCYTES; CELL SURVIVAL; DNA-BINDING PROTEINS; ETOPOSIDE; FEMALE; GENE KNOCKDOWN TECHNIQUES; GENE PRODUCTS, TAX; GENES, JUN; HELA CELLS; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMANS; LEUKEMIA-LYMPHOMA, ADULT T-CELL; LIGASES; MALE; NF-KAPPA B P50 SUBUNIT; NITROPHENOLS; NUCLEAR PROTEINS; PIPERAZINES; PROTO-ONCOGENE PROTEINS C-BCL-2; PROTO-ONCOGENE PROTEINS C-JUN; SULFONAMIDES; TRANSCRIPTION FACTOR RELB; TRANSCRIPTION, GENETIC; VIRAL PROTEINS;

EID: 84862297612     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.340992     Document Type: Article

References (94)

1. Cavrois, M., Wain-Hobson, S., Gessain, A., Plumelle, Y., and Wattel, E. (1996) Adult T-cell leukemia/lymphoma on a background of clonally expanding human T-cell leukemia virus type-1-positive cells. Blood 88, 4646-4650 (Pubitemid 26419148)
2. Etoh, K., Tamiya, S., Yamaguchi, K., Okayama, A., Tsubouchi, H., Ideta, T., Mueller, N., Takatsuki, K., and Matsuoka, M. (1997) Persistent clonal proliferation of human T-lymphotropic virus type I-infected cells in vivo. Cancer Res. 57, 4862-4867 (Pubitemid 27468995)
3. Li, M., and Green, P. L. (2007) Detection and quantitation of HTLV-1 and HTLV-2 mRNA species by real time RT-PCR. J. Virol. Methods 142, 159-168 (Pubitemid 46590416)
4. Franchini, G., Wong-Staal, F., and Gallo, R. C. (1984) Human T-cell leukemia virus (HTLV-I) transcripts in fresh and cultured cells of patients with adult T-cell leukemia. Proc. Natl. Acad. Sci. U.S.A. 81, 6207-6211 (Pubitemid 15220809)
5. Sugamura, K., Fujii, M., Kannagi, M., Sakitani, M., Takeuchi, M., and Hinuma, Y. (1984) Cell surface phenotypes and expression of viral antigens of various human cell lines carrying human T-cell leukemia virus. Int. J. Cancer 34, 221-228 (Pubitemid 14053144)
6. Furukawa, Y., Osame, M., Kubota, R., Tara, M., and Yoshida, M. (1995) Human T-cell leukemia virus type-1 (HTLV-1) Tax is expressed at the same level in infected cells of HTLV-1-associated myelopathy or tropical spastic paraparesis patients as in asymptomatic carriers but at a lower level in adult T-cell leukemia cells. Blood 85, 1865-1870
7. Grassmann, R., Berchtold, S., Radant, I., Alt, M., Fleckenstein, B., Sodroski, J. G., Haseltine, W. A., and Ramstedt, U. (1992) Role of human T-cell leukemia virus type 1 X region proteins in immortalization of primary human lymphocytes in culture. J. Virol. 66, 4570-4575
8. Grossman, W. J., Kimata, J. T., Wong, F. H., Zutter, M., Ley, T. J., and Ratner, L. (1995) Development of leukemia in mice transgenic for the tax gene of human T-cell leukemia virus type I. Proc. Natl. Acad. Sci. U.S.A. 92, 1057-1061
9. Bellon, M., Baydoun, H. H., Yao, Y., and Nicot, C. (2010) HTLV-I Tax-dependent and -independent events associated with immortalization of human primary T lymphocytes. Blood 115, 2441-2448
10. + T lymphocytes by human T-cell leukemia virus type 1 Tax mutants expressed in a functional molecular clone. J. Virol. 73, 4856-4865
11. Pozzatti, R., Vogel, J., and Jay, G. (1990) The human T-lymphotropic virus type I tax gene can cooperate with the ras oncogene to induce neoplastic transformation of cells. Mol. Cell. Biol. 10, 413-417
12. Nerenberg, M., Hinrichs, S. H., Reynolds, R. K., Khoury, G., and Jay, G. (1987) The tat gene of human T-lymphotropic virus type 1 induces mesenchymal tumors in transgenic mice. Science 237, 1324-1329 (Pubitemid 17134616)
13. Hasegawa, H., Sawa, H., Lewis, M. J., Orba, Y., Sheehy, N., Yamamoto, Y., Ichinohe, T., Tsunetsugu-Yokota, Y., Katano, H., Takahashi, H., Matsuda, J., Sata, T., Kurata, T., Nagashima, K., and Hall, W. W. (2006) Thymus-derived leukemia-lymphoma in mice transgenic for the Tax gene of human T-lymphotropic virus type I. Nat. Med. 12, 466-472
14. Journo, C., Douceron, E., and Mahieux, R. (2009) HTLV gene regulation. Because size matters, transcription is not enough. Future Microbiol. 4, 425-440
15. Ishikawa, C., Nakachi, S., Senba, M., Sugai, M., and Mori, N. (2011) Activation of AID by human T-cell leukemia virus Tax oncoprotein and the possible role of its constitutive expression in ATL genesis. Carcinogenesis 32, 110-119
16. Grassmann, R., Aboud, M., and Jeang, K. T. (2005) Molecular mechanisms of cellular transformation by HTLV-1 Tax. Oncogene 24, 5976-5985 (Pubitemid 43086115)
17. + cells relies on cIAP-2 but not on c-FLIP expression. Virology 407, 341-351
18. Taylor, J. M., and Nicot, C. (2008) HTLV-1 and apoptosis. Role in cellular transformation and recent advances in therapeutic approaches. Apoptosis 13, 733-747
19. Silbermann, K., and Grassmann, R. (2007) Human T cell leukemia virus type 1 Tax-induced signals in cell survival, proliferation, and transformation. Signal Transduction 7, 34-52 (Pubitemid 46326742)
20. Hall, W. W., and Fujii, M. (2005) Deregulation of cell-signaling pathways in HTLV-1 infection. Oncogene 24, 5965-5975 (Pubitemid 43086114)
21. Chlichlia, K., and Khazaie, K. (2010) HTLV-1 Tax. Linking transformation, DNA damage, and apoptotic T-cell death. Chem. Biol. Interact. 188, 359-365
22. Fujita, M., and Shiku, H. (1995) Differences in sensitivity to induction of apoptosis among rat fibroblast cells transformed by HTLV-I tax gene or cellular nuclear oncogenes. Oncogene 11, 15-20
23. Satou, Y., Yasunaga, J., Yoshida, M., and Matsuoka, M. (2006) HTLV-I basic leucine zipper factor gene mRNA supports proliferation of adult T-cell leukemia cells. Proc. Natl. Acad. Sci. U.S.A. 103, 720-725 (Pubitemid 43153092)
24. Takeda, S., Maeda, M., Morikawa, S., Taniguchi, Y., Yasunaga, J., Nosaka, K., Tanaka, Y., and Matsuoka, M. (2004) Genetic and epigenetic inactivation of tax gene in adult T-cell leukemia cells. Int. J. Cancer 109, 559-567 (Pubitemid 38339647)
25. Usui, T., Yanagihara, K., Tsukasaki, K., Murata, K., Hasegawa, H., Yamada, Y., and Kamihira, S. (2008) Characteristic expression of HTLV-1 basic zipper factor (HBZ) transcripts in HTLV-1 provirus-positive cells. Retrovirology 5, 34
26. + T-cells and ATL cells expressing Tax. Int. J. Cancer 120, 1591-1597
27. Nakayama, T., Hieshima, K., Arao, T., Jin, Z., Nagakubo, D., Shirakawa, A. K., Yamada, Y., Fujii, M., Oiso, N., Kawada, A., Nishio, K., and Yoshie, O. (2008) Aberrant expression of Fra-2 promotes CCR4 expression and cell proliferation in adult T-cell leukemia. Oncogene 27, 3221-3232 (Pubitemid 351733385)
28. Matsuoka, M. (2010) HTLV-1 bZIP factor gene. Its roles in HTLV-1 pathogenesis. Mol. Aspects Med. 31, 359-366
29. Kuhlmann, A. S., Villaudy, J., Gazzolo, L., Castellazzi, M., Mesnard, J. M., and Duc Dodon, M. (2007) HTLV-1 HBZ cooperates with JunD to enhance transcription of the human telomerase reverse transcriptase gene (hTERT). Retrovirology 4, 92
30. Satou, Y., Yasunaga, J., Zhao, T., Yoshida, M., Miyazato, P., Takai, K., Shimizu, K., Ohshima, K., Green, P. L., Ohkura, N., Yamaguchi, T., Ono, M., Sakaguchi, S., and Matsuoka, M. (2011) HTLV-1 bZIP factor induces T-cell lymphoma and systemic inflammation in vivo. PLoS Pathog. 7, e1001274
31. Hagiya, K., Yasunaga, J., Satou, Y., Ohshima, K., and Matsuoka, M. (2011) ATF3, an HTLV-1 bZIP factor-binding protein, promotes proliferation of adult T-cell leukemia cells. Retrovirology 8, 19
32. Arnold, J., Zimmerman, B., Li, M., Lairmore, M. D., and Green, P. L. (2008) Human T-cell leukemia virus type-1 antisense-encoded gene, Hbz, promotes T-lymphocyte proliferation. Blood 112, 3788-3797
33. White, E. (2006) Mechanisms of apoptosis regulation by viral oncogenes in infection and tumorigenesis. Cell Death Differ. 13, 1371-1377
34. Postigo, A., and Ferrer, P. E. (2009) Viral inhibitors reveal overlapping themes in regulation of cell death and innate immunity. Microbes Infect. 11, 1071-1078
35. Polster, B. M., Pevsner, J., and Hardwick, J. M. (2004) Viral Bcl-2 homologs and their role in virus replication and associated diseases. Biochim. Biophys. Acta 1644, 211-227 (Pubitemid 38292107)
36. Adams, J. M., and Cory, S. (2007) The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 26, 1324-1337 (Pubitemid 46328466)
37. Kirkin, V., Joos, S., and Zörnig, M. (2004) The role of Bcl-2 family members in tumorigenesis. Biochim. Biophys. Acta 1644, 229-249 (Pubitemid 38281277)
38. Zong, W. X., Edelstein, L. C., Chen, C., Bash, J., and Gélinas, C. (1999) The prosurvival Bcl-2 homolog Bfl-1/A1 is a direct transcriptional target of NF-κB that blocks TNFα-induced apoptosis. Genes Dev. 13, 382-387 (Pubitemid 29108753)
39. Wang, C. Y., Guttridge, D. C., Mayo, M. W., and Baldwin, A. S., Jr. (1999) NF-κB induces expression of the Bcl-2 homologue A1/Bfl-1 to preferentially suppress chemotherapy-induced apoptosis. Mol. Cell. Biol. 19, 5923-5929 (Pubitemid 29399297)
40. Simonian, P. L., Grillot, D. A., and Nuñez, G. (1997) Bcl-2 and Bcl-XL can differentially block chemotherapy-induced cell death. Blood 90, 1208-1216 (Pubitemid 27314158)
41. Schneider, T. J., Grillot, D., Foote, L. C., Núñez, G. E., and Rothstein, T. L. (1997) Bcl-x protects primary B-cells against Fas-mediated apoptosis. J. Immunol. 159, 4834-4839 (Pubitemid 127471019)
42. Olsson, A., Norberg, M., Okvist, A., Derkow, K., Choudhury, A., Tobin, G., Celsing, F., Osterborg, A., Rosenquist, R., Jondal, M., and Osorio, L. M. (2007) Up-regulation of bfl-1 is a potential mechanism of chemoresistance in B-cell chronic lymphocytic leukemia. Br. J. Cancer 97, 769-777 (Pubitemid 47396296)
43. Lee, H. H., Dadgostar, H., Cheng, Q., Shu, J., and Cheng, G. (1999) NF-κB-mediated up-regulation of Bcl-x and Bfl-1/A1 is required for CD40 survival signaling in B lymphocytes. Proc. Natl. Acad. Sci. U.S.A. 96, 9136-9141 (Pubitemid 29374720)
44. Lam, L. T., Davis, R. E., Pierce, J., Hepperle, M., Xu, Y., Hottelet, M., Nong, Y., Wen, D., Adams, J., Dang, L., and Staudt, L. M. (2005) Small molecule inhibitors of IκB kinase are selectively toxic for subgroups of diffuse large B-cell lymphoma defined by gene expression profiling. Clin. Cancer Res. 11, 28-40 (Pubitemid 40075775)
45. Grumont, R. J., Rourke, I. J., and Gerondakis, S. (1999) Rel-dependent induction of A1 transcription is required to protect B-cells from antigen receptor ligation-induced apoptosis. Genes Dev. 13, 400-411 (Pubitemid 29108756)
46. Chen, C., Edelstein, L. C., and Gélinas, C. (2000) The Rel/NF-κB family directly activates expression of the apoptosis inhibitor Bcl-xL. Mol. Cell. Biol. 20, 2687-2695 (Pubitemid 30183487)
47. Brien, G., Trescol-Biemont, M. C., and Bonnefoy-Bérard, N. (2007) Down-regulation of Bfl-1 protein expression sensitizes malignant B-cells to apoptosis. Oncogene 26, 5828-5832 (Pubitemid 47312815)
48. de la Fuente, C., Wang, L., Wang, D., Deng, L., Wu, K., Li, H., Stein, L. D., Denny, T., Coffman, F., Kehn, K., Baylor, S., Maddukuri, A., Pumfery, A., and Kashanchi, F. (2003) Paradoxical effects of a stress signal on pro- and anti-apoptotic machinery in HTLV-1 Tax-expressing cells. Mol. Cell Biochem. 245, 99-113 (Pubitemid 36416826)
49. D'Souza, B., Rowe, M., and Walls, D. (2000) The bfl-1 gene is transcriptionally up-regulated by the Epstein-Barr virus LMP1, and its expression promotes the survival of a Burkitt's lymphoma cell line. J. Virol. 74, 6652-6658 (Pubitemid 30429836)
50. D'Souza, B. N., Edelstein, L. C., Pegman, P. M., Smith, S. M., Loughran, S. T., Clarke, A., Mehl, A., Rowe, M., Gélinas, C., and Walls, D. (2004) Nuclear factor κB-dependent activation of the antiapoptotic bfl-1 gene by the Epstein-Barr virus latent membrane protein 1 and activated CD40 receptor. J. Virol. 78, 1800-1816 (Pubitemid 38176712)
51. Portis, T., and Longnecker, R. (2004) Epstein-Barr virus (EBV) LMP2A mediates B-lymphocyte survival through constitutive activation of the Ras/PI3K/Akt pathway. Oncogene 23, 8619-8628 (Pubitemid 39576469)
52. L is up-regulated by HTLV-I and HTLV-II in vitro and in ex vivo ATLL samples. Blood 96, 275-281
53. Mori, N., Fujii, M., Cheng, G., Ikeda, S., Yamasaki, Y., Yamada, Y., Tomonaga, M., and Yamamoto, N. (2001) Human T-cell leukemia virus type I tax protein induces the expression of anti-apoptotic gene Bcl-xL in human T-cells through nuclear factor-κB and c-AMP-responsive elementbinding protein pathways. Virus Genes 22, 279-287 (Pubitemid 32587634)
54. Smith, M. R., and Greene, W. C. (1990) Identification of HTLV-I tax trans-activator mutants exhibiting novel transcriptional phenotypes. Genes Dev. 4, 1875-1885 (Pubitemid 120012589)
55. Meertens, L., Chevalier, S., Weil, R., Gessain, A., and Mahieux, R. (2004) A 10-amino acid domain within human T-cell leukemia virus type 1 and type 2 Tax protein sequences is responsible for their divergent subcellular distribution. J. Biol. Chem. 279, 43307-43320 (Pubitemid 39372226)
56. Lamsoul, I., Lodewick, J., Lebrun, S., Brasseur, R., Burny, A., Gaynor, R. B., and Bex, F. (2005) Exclusive ubiquitination and sumoylation on overlapping lysine residues mediate NF-κB activation by the human T-cell leukemia virus Tax oncoprotein. Mol. Cell. Biol. 25, 10391-10406 (Pubitemid 41681963)
57. Thébault, S., Basbous, J., Hivin, P., Devaux, C., and Mesnard, J. M. (2004) HBZ interacts with JunD and stimulates its transcriptional activity. FEBS Lett. 562, 165-170 (Pubitemid 38388465)
58. Basbous, J., Arpin, C., Gaudray, G., Piechaczyk, M., Devaux, C., and Mesnard, J. M. (2003) TheHBZfactor of human T-cell leukemia virus type I dimerizes with transcription factors JunB and c-Jun and modulates their transcriptional activity. J. Biol. Chem. 278, 43620-43627 (Pubitemid 37345988)
59. Sun, S., Elwood, J., and Greene, W. C. (1996) Both amino- and carboxylterminal sequences within IκBα regulate its inducible degradation. Mol. Cell. Biol. 16, 1058-1065 (Pubitemid 26061677)
60. Meertens, L., Pise-Masison, C., Quere, N., Brady, J., Gessain, A., and Mahieux, R. (2004) Utilization of the CBP but not the p300 co-activator by human T-lymphotropic virus type-2 Tax for p53 inhibition. Oncogene 23, 5447-5458 (Pubitemid 39044055)
61. Hivin, P., Frédéric, M., Arpin-André, C., Basbous, J., Gay, B., Thébault, S., and Mesnard, J. M. (2005) Nuclear localization of HTLV-I bZIP factor (HBZ) is mediated by three distinct motifs. J. Cell Sci. 118, 1355-1362 (Pubitemid 40585116)
62. Nagata, K., Ohtani, K., Nakamura, M., and Sugamura, K. (1989) Activation of endogenous c-fos proto-oncogene expression by human T-cell leukemia virus type I-encoded p40tax protein in the human T-cell line, Jurkat. J. Virol. 63, 3220-3226 (Pubitemid 19181376)
63. Lemasson, I., Robert-Hebmann, V., Hamaia, S., Duc Dodon, M., Gazzolo, L., and Devaux, C. (1997) Transrepression of lck gene expression by human T-cell leukemia virus type 1-encoded p40tax. J. Virol. 71, 1975-1983 (Pubitemid 27078576)
64. Chung, H. K., Young, H. A., Goon, P. K., Heidecker, G., Princler, G. L., Shimozato, O., Taylor, G. P., Bangham, C. R., and Derse, D. (2003) Activation of interleukin-13 expression in T-cells from HTLV-1-infected individuals and in chronically infected cell lines. Blood 102, 4130-4136 (Pubitemid 37486998)
65. Cottalorda, A., Verschelde, C., Marçais, A., Tomkowiak, M., Musette, P., Uematsu, S., Akira, S., Marvel, J., and Bonnefoy-Berard, N. (2006) TLR2 engagement on CD8 T-cells lowers the threshold for optimal antigeninduced T-cell activation. Eur. J. Immunol. 36, 1684-1693 (Pubitemid 44089036)
66. Oltersdorf, T., Elmore, S. W., Shoemaker, A. R., Armstrong, R. C., Augeri, D. J., Belli, B. A., Bruncko, M., Deckwerth, T. L., Dinges, J., Hajduk, P. J., Joseph, M. K., Kitada, S., Korsmeyer, S. J., Kunzer, A. R., Letai, A., Li, C., Mitten, M. J., Nettesheim, D. G., Ng, S., Nimmer, P. M., O'Connor, J. M., Oleksijew, A., Petros, A. M., Reed, J. C., Shen, W., Tahir, S. K., Thompson, C. B., Tomaselli, K. J., Wang, B., Wendt, M. D., Zhang, H., Fesik, S. W., and Rosenberg, S. H. (2005) An inhibitor of Bcl-2 family proteins induces regression of solid tumors. Nature 435, 677-681 (Pubitemid 40825512)
67. Edelstein, L. C., Lagos, L., Simmons, M., Tirumalai, H., and Gélinas, C. (2003) NF-κB-dependent assembly of an enhanceosome-like complex on the promoter region of apoptosis inhibitor Bfl-1/A1. Mol. Cell. Biol. 23, 2749-2761 (Pubitemid 36403075)
68. Peloponese, J. M., Jr., and Jeang, K. T. (2006) Role for Akt/protein kinase B and activator protein-1 in cellular proliferation induced by the human T-cell leukemia virus type 1 tax oncoprotein. J. Biol. Chem. 281, 8927-8938
69. Matsumoto, J., Ohshima, T., Isono, O., and Shimotohno, K. (2005) HTLV-1 HBZ suppresses AP-1 activity by impairing both the DNA-binding ability and the stability of c-Jun protein. Oncogene 24, 1001-1010 (Pubitemid 40313877)
70. Vogler, M., Dinsdale, D., Dyer, M. J., and Cohen, G. M. (2009) Bcl-2 inhibitors. Small molecules with a big impact on cancer therapy. Cell Death Differ. 16, 360-367
71. Tsukasaki, K., Hermine, O., Bazarbachi, A., Ratner, L., Ramos, J. C., Harrington, W., Jr., O'Mahony, D., Janik, J. E., Bittencourt, A. L., Taylor, G. P., Yamaguchi, K., Utsunomiya, A., Tobinai, K., and Watanabe, T. (2009) J. Clin. Oncol. 27, 453-459
72. Vogler, M. (2012) BCL2A1. The underdog in the BCL2 family. Cell Death Differ. 19, 67-74
73. Harhaj, E. W., Good, L., Xiao, G., and Sun, S. C. (1999) Gene expression profiles in HTLV-I-immortalized T-cells: deregulated expression of genes involved in apoptosis regulation. Oncogene 18, 1341-1349 (Pubitemid 29094886)
74. c-/- mice. PLoS Pathog. 7, e1002231
75. Mori, N., Yamada, Y., Ikeda, S., Yamasaki, Y., Tsukasaki, K., Tanaka, Y., Tomonaga, M., Yamamoto, N., and Fujii, M. (2002) Bay 11-7082 inhibits transcription factor NF-κB and induces apoptosis of HTLV-I-infected T-cell lines and primary adult T-cell leukemia cells. Blood 100, 1828-1834 (Pubitemid 34925163)
76. Shaulian, E. (2010) AP-1-The Jun proteins. Oncogenes or tumor suppressors in disguise? Cell. Signal. 22, 894-899
77. Eferl, R., and Wagner, E. F. (2003) AP-1. A double-edged sword in tumorigenesis. Nat. Rev. Cancer 3, 859-868
78. Mori, N., Fujii, M., Iwai, K., Ikeda, S., Yamasaki, Y., Hata, T., Yamada, Y., Tanaka, Y., Tomonaga, M., and Yamamoto, N. (2000) Constitutive activation of transcription factor AP-1 in primary adult T-cell leukemia cells. Blood 95, 3915-3921 (Pubitemid 30412868)
79. Iwai, K., Mori, N., Oie, M., Yamamoto, N., and Fujii, M. (2001) Human T-cell leukemia virus type 1 Tax protein activates transcription through AP-1 site by inducing DNA binding activity in T-cells. Virology 279, 38-46 (Pubitemid 34160997)
80. Fujii, M., Iwai, K., Oie, M., Fukushi, M., Yamamoto, N., Kannagi, M., and Mori, N. (2000) Activation of oncogenic transcription factor AP-1 in T-cells infected with human T-cell leukemia virus type 1. AIDS Res. Hum. Retroviruses 16, 1603-1606
81. Iwanaga, Y., Tsukahara, T., Ohashi, T., Tanaka, Y., Arai, M., Nakamura, M., Ohtani, K., Koya, Y., Kannagi, M., Yamamoto, N., and Fujii, M. (1999) Human T-cell leukemia virus type 1 Tax protein abrogates interleukin-2 dependence in a mouse T-cell line. J. Virol. 73, 1271-1277 (Pubitemid 29036781)
82. Zhi, H., Yang, L., Kuo, Y. L., Ho, Y. K., Shih, H. M., and Giam, C. Z. (2011) NF-κB hyper-activation by HTLV-1 tax induces cellular senescence but can be alleviated by the viral anti-sense protein HBZ. PLoS Pathog. 7, e1002025
83. Zhao, T., Yasunaga, J., Satou, Y., Nakao, M., Takahashi, M., Fujii, M., and Matsuoka, M. (2009) Human T-cell leukemia virus type 1 bZIP factor selectively suppresses the classical pathway of NF-κB. Blood 113, 2755-2764
84. Matsuoka, M., and Jeang, K. T. (2011) Human T-cell leukemia virus type 1 (HTLV-1) and leukemic transformation. Viral infectivity, Tax, HBZ, and therapy. Oncogene 30, 1379-1389
85. Bindhu, M., Nair, A., and Lairmore, M. D. (2004) Role of accessory proteins of HTLV-1 in viral replication, T-cell activation, and cellular gene expression. Front. Biosci. 9, 2556-2576
86. Morales, A. A., Olsson, A., Celsing, F., Osterborg, A., Jondal, M., and Osorio, L. M. (2005) High expression of bfl-1 contributes to the apoptosis resistant phenotype in B-cell chronic lymphocytic leukemia. Int. J. Cancer 113, 730-737 (Pubitemid 40101253)
87. Certo, M., Del Gaizo Moore, V., Nishino, M., Wei, G., Korsmeyer, S., Armstrong, S. A., and Letai, A. (2006) Mitochondria primed by death signals determine cellular addiction to antiapoptotic BCL-2 family members. Cancer Cell 9, 351-365 (Pubitemid 43668734)
88. Mahieux, R., Pise-Masison, C., Gessain, A., Brady, J. N., Olivier, R., Perret, E., Misteli, T., and Nicot, C. (2001) Arsenic trioxide induces apoptosis in human T-cell leukemia virus type 1- and type 2-infected cells by a caspase- 3-dependent mechanism involving Bcl-2 cleavage. Blood 98, 3762-3769
89. Ishitsuka, K., Kunami, N., Katsuya, H., Nogami, R., Ishikawa, C., Yotsumoto, F., Tanji, H., Mori, N., Takeshita, M., Miyamoto, S., and Tamura, K. (2011) Targeting Bcl-2 family proteins in adult T-cell leukemia/lymphoma. In vitro and in vivo effects of the novel Bcl-2 family inhibitor ABT-737. Cancer Lett. 317, 218-225
90. Chen, S., Dai, Y., Harada, H., Dent, P., and Grant, S. (2007) Mcl-1 downregulation potentiates ABT-737 lethality by cooperatively inducing Bak activation and Bax translocation. Cancer Res. 67, 782-791 (Pubitemid 46192219)
91. van Delft, M. F., Wei, A. H., Mason, K. D., Vandenberg, C. J., Chen, L., Czabotar, P. E., Willis, S. N., Scott, C. L., Day, C. L., Cory, S., Adams, J. M., Roberts, A. W., and Huang, D. C. (2006) The BH3 mimetic ABT-737 targets selective Bcl-2 proteins and efficiently induces apoptosis via Bak/ Bax if Mcl-1 is neutralized. Cancer Cell 10, 389-399 (Pubitemid 44711953)
92. Yecies, D., Carlson, N. E., Deng, J., and Letai, A. (2010) Acquired resistance to ABT-737 in lymphoma cells that up-regulate MCL-1 and BFL-1. Blood 115, 3304-3313
93. Vogler, M., Butterworth, M., Majid, A., Walewska, R. J., Sun, X. M., Dyer, M. J., and Cohen, G. M. (2009) Concurrent up-regulation of BCL-XL and BCL2A1 induces approximately 1000-fold resistance to ABT-737 in chronic lymphocytic leukemia. Blood 113, 4403-4413
94. Cheng, Q., Lee, H. H., Li, Y., Parks, T. P., and Cheng, G. (2000) Up-regulation of Bcl-x and Bfl-1 as a potential mechanism of chemoresistance, which can be overcome by NF-κB inhibition. Oncogene 19, 4936-4940