The proto-oncogene Bcl3, induced by tax, represses tax-mediated transcription via p300 displacement from the human T-cell leukemia virus type 1 promoter

Journal of Virology

Volumn 82, Issue 23, 2008, Pages 11939-11947

  Kim, Young Mi ^a   Sharma, Neelam ^a   Nyborg, Jennifer K ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN BCL 3; PROTEIN P300; TAX PROTEIN;

ARTICLE; BINDING SITE; CELL DIVISION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN T CELL LEUKEMIA VIRUS 1; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION;

HUMAN T-LYMPHOTROPIC VIRUS 1;

ANKYRINS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; E1A-ASSOCIATED P300 PROTEIN; ENHANCER ELEMENTS, GENETIC; GENE PRODUCTS, TAX; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMANS; JURKAT CELLS; NF-KAPPA B; PROMOTER REGIONS, GENETIC; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 56449108537     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01356-08     Document Type: Article

References (61)

1. Akagi, T., H. Ono, and K. Shimotohno. 1995. Characterization of T cells immortalized by Tax1 of human T-cell leukemia virus type 1. Blood 86:4243-4249.
2. Anderson, M. G., K. E. Scoggin, C. M. Simbulan-Rosenthal, and J. A. Steadman. 2000. Identification of poly(ADP-ribose) polymerase as a transcriptional coactivator of the human T-cell leukemia virus type 1 Tax protein. J. Virol. 74:2169-2177.
3. Asquith, B., and C. R. Bangham. 2007. Quantifying HTLV-I dynamics. Immunol. Cell Biol. 85:280-286.
4. Asquith, B., Y. Zhang, A. J. Mosley, C. M. de Lara, D. L. Wallace, A. Worth, L. Kaftantzi, K. Meekings, G. E. Griffin, Y. Tanaka, D. F. Tough, P. C. Beverley, G. P. Taylor, D. C. Macallan, and C. R. Bangham. 2007. In vivo T lymphocyte dynamics in humans and the impact of human T-lymphotropic virus 1 infection. Proc. Natl. Acad. Sci. USA 104:8035-8040.
5. Beraud, C., S. C. Sun, P. Ganchi, D. W. Ballard, and W. C. Greene. 1994. Human T-cell leukemia virus type I Tax associates with and is negatively regulated by the NF-κB2 p100 gene product: implications for viral latency. Mol. Cell. Biol. 14:1374-1382.
6. Bours, V., G. Franzoso, V. Azarenko, S. Park, T. Kanno, K. Brown, and U. Siebenlist. 1993. The oncoprotein Bcl-3 directly transactivates through kappa B motifs via association with DNA-binding p50B homodimers. Cell 72:729-739.
7. Canoz, O., G. Z. Rassidakis, J. H. Admirand, and L. J. Medeiros. 2004. Immunohistochemical detection of BCL-3 in lymphoid neoplasms: a survey of 353 cases. Mod. Pathol. 17:911-917.
8. Carmody, R. J., Q. Ruan, S. Palmer, B. Hilliard, and Y. H. Chen. 2007. Negative regulation of toll-like receptor signaling by NF-kappaB p50 ubiquitination blockade. Science 317:675-678.
9. Courtois, G., and T. D. Gilmore. 2006. Mutations in the NF-kappaB signaling pathway: implications for human disease. Oncogene 25:6831-6843.
10. Dechend, R., F. Hirano, K. Lehmann, V. Heissmeyer, S. Ansieau, F. G. Wulczyn, C. Scheidereit, and A. Leutz. 1999. The Bcl-3 oncoprotein acts as a bridging factor between NF-kappaB/Rel and nuclear co-regulators. Oncogene 18:3316-3323.
11. Dynan, W. S. 1987. DNase I footprinting as an assay for mammalian gene regulatory proteins. Genet. Engineer. 9:75-87.
12. Fujita, T., G. P. Nolan, H. C. Liou, M. L. Scott, and D. Baltimore. 1993. The candidate proto-oncogene bcl-3 encodes a transcriptional coactivator that activates through NF-kappa B p50 homodimers. Genes Dev. 7:1354-1363.
13. Ge, B., O. Li, P. Wilder, A. Rizzino, and T. W. McKeithan. 2003. NF-kappa B regulates BCL3 transcription in T lymphocytes through an intronic enhancer. J. Immunol. 171:4210-4218.
14. Geiger, T. R., N. Sharma, Y. M. Kim, and J. K. Nyborg. 2008. The human T-cell leukemia virus type 1 tax protein confers CBP/p300 recruitment and transcriptional activation properties to phosphorylated CREB. Mol. Cell. Biol. 28:1383-1392.
15. Georges, S. A., H. A. Giebler, P. A. Cole, K. Luger, P. J. Laybourn, and J. K. Nyborg. 2003. Tax recruitment of CBP/p300, via the KIX domain, reveals a potent requirement for acetyltransferase activity that is chromatin dependent and histone tail independent. Mol. Cell. Biol. 23:3392-3404.
16. Giebler, H. A., J. E. Loring, K. van Orden, M. A. Colgin, J. E. Garrus, K. W. Escudero, A. Brauweiler, and J. K. Nyborg. 1997. Anchoring of CREB binding protein to the human T-cell leukemia virus type 1 promoter: a molecular mechanism of Tax transactivation. Mol. Cell. Biol. 17:5156-5164.
17. Hall, W. W., and M. Fujii. 2005. Deregulation of cell-signaling pathways in HTLV-1 infection. Oncogene 24:5965-5975.
18. Hirai, H., J. Fujisawa, T. Suzuki, K. Ueda, M. Muramatsu, A. Tsuboi, N. Arai, and M. Yoshida. 1992. Transcriptional activator Tax of HTLV-1 binds to the NF-kappa B precursor p105. Oncogene 7:1737-1742.
19. Hirai, H., T. Suzuki, J. Fujisawa, J. Inoue, and M. Yoshida. 1994. Tax protein of human T-cell leukemia virus type I binds to the ankyrin motifs of inhibitory factor kappa B and induces nuclear translocation of transcription factor NF-kappa B proteins for transcriptional activation. Proc. Natl. Acad. Sci. USA 91:3584-3588.
20. Hishiki, T., T. Ohshima, T. Ego, and K. Shimotohno. 2007. BCL3 acts as a negative regulator of transcription from the human T-cell leukemia virus type 1 long terminal repeat through interactions with TORC3. J. Biol. Chem. 282:28335-28343.
21. Jamaluddin, M., S. Choudhary, S. Wang, A. Casola, R. Huda, R. P. Garofalo, S. Ray, and A. R. Brasier. 2005. Respiratory syncytial virus-inducible BCL-3 expression antagonizes the STAT/IRF and NF-κB signaling pathways by inducing histone deacetylase 1 recruitment to the interleukin-8 promoter. J. Virol. 79:15302-15313.
22. Kashatus, D., P. Cogswell, and A. S. Baldwin. 2006. Expression of the Bcl-3 proto-oncogene suppresses p53 activation. Genes Dev. 20:225-235.
23. Kerr, L. D., C. S. Duckett, P. Wamsley, Q. Zhang, P. Chiao, G. Nabel, T. W. McKeithan, P. A. Baeuerle, and I. M. Verma. 1992. The proto-oncogene bcl-3 encodes an I kappa B protein. Genes Dev. 6:2352-2363.
24. Kim, Y. M., J. A. Ramirez, J. E. Mick, H. A. Giebler, J. P. Yan, and J. K. Nyborg. 2007. Molecular characterization of the Tax-containing HTLV-1 enhancer complex reveals a prominent role for CREB phosphorylation in Tax transactivation. J. Biol. Chem. 282:18750-18757.
25. Kimzey, A. L., and W. S. Dynan. 1998. Specific regions of contact between human T-cell leukemia virus type I Tax protein and DNA identified by photocross-linking. J. Biol. Chem. 273:13768-13775.
26. Kraus, W. L., E. T. Manning, and J. T. Kadonaga. 1999. Biochemical analysis of distinct activation functions in p300 that enhance transcription initiation with chromatin templates. Mol. Cell. Biol. 19:8123-8135.
27. Kuwata, H., Y. Watanabe, H. Miyoshi, M. Yamamoto, T. Kaisho, K. Takeda, and S. Akira. 2003. IL-10-inducible Bcl-3 negatively regulates LPS-induced TNF-alpha production in macrophages. Blood 102:4123-4129.
28. Kwok, R. P., M. E. Laurance, J. R. Lundblad, P. S. Goldman, H. 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 380:642-646.
29. Lenzmeier, B. A., H. A. Giebler, and J. K. Nyborg. 1998. Human T-cell leukemia virus type 1 Tax requires direct access to DNA for recruitment of CREB binding protein to the viral promoter. Mol. Cell. Biol. 18:721-731.
30. Lopez, D. I., J. E. Mick, and J. K. Nyborg. 2007. Purification of CREB to apparent homogeneity: removal of truncation products and contaminating nucleic acid. Protein Expr. Purif. 55:406-418.
31. Lu, H., C. A. Pise-Masison, T. M. Fletcher, R. L. Schiltz, A. K. Nagaich, M. Radonovich, G. Hager, P. A. Cole, and J. N. Brady. 2002. Acetylation of nucleosomal histones by p300 facilitates transcription from Tax-responsive human T-cell leukemia virus type 1 chromatin template. Mol. Cell. Biol. 22:4450-4462.
32. Lundblad, J. R., R. P. Kwok, M. E. Laurance, M. S. Huang, J. P. Richards, R. G. Brennan, and R. H. Goodman. 1998. The human T-cell leukemia virus-1 transcriptional activator Tax enhances cAMP-responsive element-binding protein (CREB) binding activity through interactions with the DNA minor groove. J. Biol. Chem. 273:19251-19259.
33. Matsuoka, M. 2005. Human T-cell leukemia virus type 1 (HTLV-1) infection and the onset of adult T-cell leukemia (ATL). Retrovirology 2:2-27.
34. Matsuoka, M., and K. T. Jeang. 2007. Human T-cell leukaemia virus type 1 (HTLV-1) infectivity and cellular transformation. Nat. Rev. Cancer 7:270-280.
35. McKeithan, T. W., J. D. Rowley, T. B. Shows, and M. O. Diaz. 1987. Cloning of the chromosome translocation breakpoint junction of the t(14;19) in chronic lymphocytic leukemia. Proc. Natl. Acad. Sci. USA 84:9257-9260.
36. McKeithan, T. W., G. S. Takimoto, H. Ohno, V. S. Bjorling, R. Morgan, B. K. Hecht, I. Dube, A. A. Sandberg, and J. D. Rowley. 1997. BCL3 rearrangements and t(14;19) in chronic lymphocytic leukemia and other B-cell malignancies: a molecular and cytogenetic study. Genes Chromosomes Cancer 20:64-72.
37. Mitchell, T. C., D. Hildeman, R. M. Kedl, T. K. Teague, B. C. Schaefer, J. White, Y. Zhu, J. Kappler, and P. Marrack. 2001. Immunological adjuvants promote activated T cell survival via induction of Bcl-3. Nat. Immunol. 2:397-402.
38. Mori, N., M. Fujii, M. Hinz, K. Nakayama, Y. Yamada, S. Ikeda, Y. Yamasaki, F. Kashanchi, Y. Tanaka, M. Tomonaga, and N. Yamamoto. 2002. Activation of cyclin D1 and D2 promoters by human T-cell leukemia virus type I tax protein is associated with IL-2-independent growth of T cells. Int. J. Cancer 99:378-385.
39. Na, S. Y., H. S. Choi, J. W. Kim, D. S. Na, and J. W. Lee. 1998. Bcl3, an IkappaB protein, as a novel transcription coactivator of the retinoid X receptor. J. Biol. Chem. 273:30933-30938.
40. Ng, P. W., H. Iha, Y. Iwanaga, M. Bittner, Y. Chen, Y. Jiang, G. Gooden, J. M. Trent, P. Meltzer, K. T. Jeang, and S. L. Zeichner. 2001. Genome-wide expression changes induced by HTLV-1 Tax: evidence for MLK-3 mixed lineage kinase involvement in Tax-mediated NF-kappaB activation. Oncogene 20:4484-4496.
41. Nolan, G. P., T. Fujita, K. Bhatia, C. Huppi, H.-C. Liou, M. L. Scott, and D. Baltimore. 1993. The bcl-3 proto-oncogene encodes a nuclear IκB-like molecule that preferentially interacts with NF-κB p50 and p52 in a phosphorylation-dependent manner. Mol. Cell. Biol. 13:3557-3566.
42. Ohno, H., G. Takimoto, and T. W. McKeithan. 1990. The candidate protooncogene bcl-3 is related to genes implicated in cell lineage determination and cell cycle control. Cell 60:991-997.
43. O'Neil, B. H., P. Buzkova, H. Farrah, D. Kashatus, H. Sanoff, R. M. Goldberg, A. S. Baldwin, and W. K. Funkhouser. 2007. Expression of nuclear factor-kappaB family proteins in hepatocellular carcinomas. Oncology 72:97-104.
44. Petropoulos, L., and J. Hiscott. 1998. Association between HTLV-1 Tax and I kappa B alpha is dependent on the I kappa B alpha phosphorylation state. Virology 252:189-199.
45. 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.
46. Ramirez, J. A., and J. K. Nyborg. 2007. Molecular characterization of HTLV-1 tax interaction with the KIX domain of CBP/p300. J. Mol. Biol. 372:958-969.
47. Rousset, R., C. Desbois, F. Bantignies, and P. Jalinot. 1996. Effects on NF-kappa B1/p105 processing of the interaction between the HTLV-1 transactivator Tax and the proteasome. Nature 381:328-331.
48. Scoggin, K. E., A. Ulloa, and J. K. Nyborg. 2001. The oncoprotein Tax binds the SRC-1-interacting domain of CBP/p300 to mediate transcriptional activation. Mol. Cell. Biol. 21:5520-5530.
49. Sharma, N., and J. K. Nyborg. 2008. The coactivators CBP/p300 and the histone chaperone NAP1 promote transcription-independent nucleosome eviction at the HTLV-1 promoter. Proc. Natl. Acad. Sci. USA 105:7959-7963.
50. Siu, Y.-T., K.-T. Chin, K.-L. Siu, E. Yee Wai Choy, K.-T. Jeang, and D.-Y. Jin. 2006. TORC1 and TORC2 coactivators are required for Tax activation of the human T-cell leukemia virus type 1 long terminal repeats. J. Virol. 80:7052-7059.
51. Smith, M. R., and W. C. Greene. 1990. Identification of HTLV-I tax transactivator mutants exhibiting novel transcriptional phenotypes. Genes Dev. 4:1875-1885.
52. Sun, S. C., and D. W. Ballard. 1999. Persistent activation of NF-kappaB by the tax transforming protein of HTLV-1: hijacking cellular IkappaB kinases. Oncogene 18:6948-6958.
53. Sun, S. C., and S. Yamaoka. 2005. Activation of NF-kappaB by HTLV-I and implications for cell transformation. Oncogene 24:5952-5964.
54. Thornburg, N. J., R. Pathmanathan, and N. Raab-Traub. 2003. Activation of nuclear factor-kappaB p50 homodimer/Bcl-3 complexes in nasopharyngeal carcinoma. Cancer Res. 63:8293-8301.
55. Trevisan, R., L. Daprai, L. Acquasaliente, V. Ciminale, L. Chieco-Bianchi, and D. Saggioro. 2004. Relevance of CREB phosphorylation in the antiapoptotic function of human T-lymphotropic virus type 1 tax protein in serum-deprived murine fibroblasts. Exp. Cell Res. 299:57-67.
56. Trevisan, R., L. Daprai, L. Paloschi, N. Vajente, L. Chieco-Bianchi, and D. Saggioro. 2006. Antiapoptotic effect of human T-cell leukemia virus type 1 tax protein correlates with its creb transcriptional activity. Exp. Cell Res. 312:1390-1400.
57. Valenzuela, J. O., C. D. Hammerbeck, and M. F. Mescher. 2005. Cutting edge: Bcl-3 up-regulation by signal 3 cytokine (IL-12) prolongs survival of antigen-activated CD8 T cells. J. Immunol. 174:600-604.
58. Viatour, P., E. Dejardin, M. Warnier, F. Lair, E. Claudio, F. Bureau, J. C. Marine, M. P. Merville, U. Maurer, D. Green, J. Piette, U. Siebenlist, V. Bours, and A. Chariot. 2004. GSK3-mediated BCL-3 phosphorylation modulates its degradation and its oncogenicity. Mol. Cell 16:35-45.
59. Westerheide, S. D., M. W. Mayo, V. Anest, J. L. Hanson, and A. S. Baldwin, Jr. 2001. The putative oncoprotein Bcl-3 induces cyclin D1 to stimulate G1 transition. Mol. Cell. Biol. 21:8428-8436.
60. Wulczyn, F. G., M. Naumann, and C. Scheidereit. 1992. Candidate protooncogene bcl-3 encodes a subunit-specific inhibitor of transcription factor NF-kappa B. Nature 358:597-599.
61. Zhao, L. J., and C. Z. Giam. 1991. Interaction of the human T-cell lymphotrophic virus type I (HTLV-I) transcriptional activator Tax with cellular factors that bind specifically to the 21-base-pair repeats in the HTLV-I enhancer. Proc. Natl. Acad. Sci. USA 88:11445-11449.