HSP90 protects the human T-cell leukemia virus type 1 (HTLV-1) tax oncoprotein from proteasomal degradation to support NF-κB activation and HTLV-1 replication

Journal of Virology

Volumn 87, Issue 24, 2013, Pages 13640-13654

  Gao, Linlin ^a   Harhaj, Edward William ^b  

^a UNIVERSITY OF MIAMI   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALVESPIMYCIN; HEAT SHOCK PROTEIN 90; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; SHORT HAIRPIN RNA; TAX PROTEIN;

ARTICLE; CELL FRACTIONATION; CELL STRAIN HEK293; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; HUMAN T CELL LEUKEMIA VIRUS 1; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LENTIVIRINAE; LONG TERMINAL REPEAT; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UBIQUITINATION; VIRUS REPLICATION;

CELL NUCLEUS; GENE PRODUCTS, TAX; HSP90 HEAT-SHOCK PROTEINS; HTLV-I INFECTIONS; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMANS; NF-KAPPA B; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEOLYSIS; TERMINAL REPEAT SEQUENCES; VIRUS REPLICATION;

EID: 84888037891     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02006-13     Document Type: Article

References (69)

1. Poiesz BJ, Ruscetti FW, Gazdar AF, Bunn PA, Minna JD, Gallo RC. 1980. Detection and isolation of type C retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous T-cell lymphoma. Proc. Natl. Acad. Sci. U.S.A. 77:7415-7419.
2. Iwanaga M, Watanabe T, Yamaguchi K. 2012. Adult T-cell leukemia:a review of epidemiological evidence. Front. Microbiol. 3:322. doi:10.3389/fmicb.2012.00322.
3. Iwanaga M, Watanabe T, Utsunomiya A, Okayama A, Uchimaru K, Koh KR, Ogata M, Kikuchi H, Sagara Y, Uozumi K, Mochizuki M, Tsukasaki K, Saburi Y, Yamamura M, Tanaka J, Moriuchi Y, Hino S, Kamihira S, Yamaguchi K. 2010. Human T-cell leukemia virus type I (HTLV-1) proviral load and disease progression in asymptomatic HTLV-1 carriers:a nationwide prospective study in Japan. Blood 116:1211-1219.
4. Grassmann R, Aboud M, Jeang KT. 2005. Molecular mechanisms of cellular transformation by HTLV-1 Tax. Oncogene 24:5976-5985.
5. Kashanchi F, Brady JN. 2005. Transcriptional and post-transcriptional gene regulation of HTLV-1. Oncogene 24:5938-5951.
6. Matsuoka M, Jeang KT. 2007. Human T-cell leukaemia virus type 1 (HTLV-1) infectivity and cellular transformation. Nat. Rev. Cancer 7:270-280.
7. Sun SC, Yamaoka S. 2005. Activation of NF-kappaB by HTLV-I and implications for cell transformation. Oncogene 24:5952-5964.
8. Hayden MS, Ghosh S. 2012. NF-kappaB, the first quarter-century:remarkable progress and outstanding questions. Genes Dev. 26:203-234.
9. Sun SC, Ganchi PA, Ballard DW, Greene WC. 1993. NF-kappa B controls expression of inhibitor I kappa B alpha:evidence for an inducible autoregulatory pathway. Science 259:1912-1915.
10. DiDonato JA, Hayakawa M, Rothwarf DM, Zandi E, Karin M. 1997. A cytokine-responsive IkappaB kinase that activates the transcription factor NF-kappaB. Nature 388:548-554.
11. Karin M, Ben-Neriah Y. 2000. Phosphorylation meets ubiquitination:the control of NF-[kappa]B activity. Annu. Rev. Immunol. 18:621-663.
12. Harhaj EW, Sun SC. 1999. IKKgamma serves as a docking subunit of the IkappaB kinase (IKK) and mediates interaction of IKK with the human T-cell leukemia virus Tax protein. J. Biol. Chem. 274:22911-22914.
13. Jin DY, Giordano V, Kibler KV, Nakano H, Jeang KT. 1999. Role of adapter function in oncoprotein-mediated activation of NF-kappaB. Human T-cell leukemia virus type I Tax interacts directly with IkappaB kinase gamma. J. Biol. Chem. 274:17402-17405.
14. Robek MD, Ratner L. 1999. Immortalization of CD4(+) and CD8(+) T lymphocytes by human T-cell leukemia virus type 1 Tax mutants expressed in a functional molecular clone. J. Virol. 73:4856-4865.
15. Mori N, Fujii M, Ikeda S, Yamada Y, Tomonaga M, Ballard DW, Yamamoto N. 1999. Constitutive activation of NF-kappaB in primary adult T-cell leukemia cells. Blood 93:2360-2368.
16. Cann AJ, Rosenblatt JD, Wachsman W, Shah NP, Chen IS. 1985. Identification of the gene responsible for human T-cell leukaemia virus transcriptional regulation. Nature 318:571-574.
17. Tie F, Adya N, Greene WC, Giam CZ. 1996. Interaction of the human T-lymphotropic virus type 1 Tax dimer with CREB and the viral 21-basepair repeat. J. Virol. 70:8368-8374.
18. Currer R, Van Duyne R, Jaworski E, Guendel I, Sampey G, Das R, Narayanan A, Kashanchi F. 2012. HTLV tax:a fascinating multifunctional co-regulator of viral and cellular pathways. Front. Microbiol. 3:406. doi:10.3389/fmicb.2012.00406.
19. Taipale M, Jarosz DF, Lindquist S. 2010. HSP90 at the hub of protein homeostasis:emerging mechanistic insights. Nat. Rev. Mol. Cell Biol. 11:515-528.
20. Zhao R, Davey M, Hsu YC, Kaplanek P, Tong A, Parsons AB, Krogan N, Cagney G, Mai D, Greenblatt J, Boone C, Emili A, Houry WA. 2005. Navigating the chaperone network:an integrative map of physical and genetic interactions mediated by the hsp90 chaperone. Cell 120:715-727.
21. Whitesell L, Lindquist SL. 2005. HSP90 and the chaperoning of cancer. Nat. Rev. Cancer 5:761-772.
22. Ratzke C, Mickler M, Hellenkamp B, Buchner J, Hugel T. 2010. Dynamics of heat shock protein 90 C-terminal dimerization is an important part of its conformational cycle. Proc. Natl. Acad. Sci. U.S.A. 107:16101-16106.
23. Panaretou B, Prodromou C, Roe SM, O'Brien R, Ladbury JE, Piper PW, Pearl LH. 1998. ATP binding and hydrolysis are essential to the function of the Hsp90 molecular chaperone in vivo. EMBO J. 17:4829-4836.
24. Grenert JP, Sullivan WP, Fadden P, Haystead TA, Clark J, Mimnaugh E, Krutzsch H, Ochel HJ, Schulte TW, Sausville E, Neckers LM, Toft DO. 1997. The amino-terminal domain of heat shock protein 90 (hsp90) that binds geldanamycin is an ATP/ADP switch domain that regulates hsp90 conformation. J. Biol. Chem. 272:23843-23850.
25. Neckers L, Workman P. 2012. Hsp90 molecular chaperone inhibitors:are we there yet? Clin. Cancer Res. 18:64-76.
26. Charoenthongtrakul S, Zhou Q, Shembade N, Harhaj NS, Harhaj EW. 2011. Human T cell leukemia virus type 1 Tax inhibits innate antiviral signaling via NF-kappaB-dependent induction of SOCS1. J. Virol. 85:6955-6962.
27. Shembade N, Harhaj NS, Yamamoto M, Akira S, Harhaj EW. 2007. The human T-cell leukemia virus type 1 Tax oncoprotein requires the ubiquitin-conjugating enzyme Ubc13 for NF-kappaB activation. J. Virol. 81:13735-13742.
28. Lavorgna A, Harhaj EW. 2012. An RNA interference screen identifies the Deubiquitinase STAMBPL1 as a critical regulator of human T-cell leukemia virus type 1 tax nuclear export and NF-kappaB activation. J. Virol. 86:3357-3369.
29. Turci M, Lodewick J, Righi P, Polania A, Romanelli MG, Bex F, Bertazzoni U. 2009. HTLV-2B Tax oncoprotein is modified by ubiquitination and sumoylation and displays intracellular localization similar to its homologue HTLV-1 Tax. Virology 386:6-11.
30. Kimata JT, Wong FH, Wang JJ, Ratner L. 1994. Construction and characterization of infectious human T-cell leukemia virus type 1 molecular clones. Virology 204:656-664.
31. Shevchenko A, Wilm M, Vorm O, Mann M. 1996. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68:850-858.
32. Tanaka T, Grusby MJ, Kaisho T. 2007. PDLIM2-mediated termination of transcription factor NF-kappaB activation by intranuclear sequestration and degradation of the p65 subunit. Nat. Immunol. 8:584-591.
33. Yan P, Fu J, Qu Z, Li S, Tanaka T, Grusby MJ, Xiao G. 2009. PDLIM2 suppresses human T-cell leukemia virus type I Tax-mediated tumorigenesis by targeting Tax into the nuclear matrix for proteasomal degradation. Blood 113:4370-4380.
34. Fu DX, Kuo YL, Liu BY, Jeang KT, Giam CZ. 2003. Human Tlymphotropic virus type I tax activates I-kappa B kinase by inhibiting I-kappa B kinase-associated serine/threonine protein phosphatase 2A. J. Biol. Chem. 278:1487-1493.
35. Kang KI, Devin J, Cadepond F, Jibard N, Guiochon-Mantel A, Baulieu EE, Catelli MG. 1994. In vivo functional protein-protein interaction:nuclear targeted hsp90 shifts cytoplasmic steroid receptor mutants into the nucleus. Proc. Natl. Acad. Sci. U.S.A. 91:340-344.
36. Alefantis T, Barmak K, Harhaj EW, Grant C, Wigdahl B. 2003. Characterization of a nuclear export signal within the human T cell leukemia virus type I transactivator protein Tax. J. Biol. Chem. 278:21814-21822.
37. Burton M, Upadhyaya CD, Maier B, Hope TJ, Semmes OJ. 2000. Human T-cell leukemia virus type 1 Tax shuttles between functionally discrete subcellular targets. J. Virol. 74:2351-2364.
38. Akner G, Mossberg K, Sundqvist KG, Gustafsson JA, Wikstrom AC. 1992. Evidence for reversible, non-microtubule and non-microfilamentdependent nuclear translocation of hsp90 after heat shock in human fibroblasts. Eur. J. Cell Biol. 58:356-364.
39. Burch AD, Weller SK. 2005. Herpes simplex virus type 1 DNA polymerase requires the mammalian chaperone hsp90 for proper localization to the nucleus. J. Virol. 79:10740-10749.
40. Chen W, Sin SH, Wen KW, Damania B, Dittmer DP. 2012. Hsp90 inhibitors are efficacious against Kaposi Sarcoma by enhancing the degradation of the essential viral gene LANA, of the viral co-receptor EphA2 as well as other client proteins. PLoS Pathog. 8:e1003048. doi:10.1371/journal.ppat.1003048.
41. Pozo FM, Oda T, Sekimoto T, Murakumo Y, Masutani C, Hanaoka F, Yamashita T. 2011. Molecular chaperone Hsp90 regulates REV1-mediated mutagenesis. Mol. Cell. Biol. 31:3396-3409.
42. Chen G, Cao P, Goeddel DV. 2002. TNF-induced recruitment and activation of the IKK complex require Cdc37 and Hsp90. Mol. Cell 9:401-410.
43. Qing G, Yan P, Xiao G. 2006. Hsp90 inhibition results in autophagymediated proteasome-independent degradation of IkappaB kinase (IKK). Cell Res. 16:895-901.
44. Hertlein E, Wagner AJ, Jones J, Lin TS, Maddocks KJ, Towns WH, III, Goettl VM, Zhang X, Jarjoura D, Raymond CA, West DA, Croce CM, Byrd JC, Johnson AJ. 2010. 17-DMAG targets the nuclear factor-kappaB family of proteins to induce apoptosis in chronic lymphocytic leukemia:clinical implications of HSP90 inhibition. Blood 116:45-53.
45. Kurashina R, Ohyashiki JH, Kobayashi C, Hamamura R, Zhang Y, Hirano T, Ohyashiki K. 2009. Anti-proliferative activity of heat shock protein (Hsp) 90 inhibitors via beta-catenin/TCF7L2 pathway in adult T cell leukemia cells. Cancer Lett. 284:62-70.
46. Yang K, Shi H, Qi R, Sun S, Tang Y, Zhang B, Wang C. 2006. Hsp90 regulates activation of interferon regulatory factor 3 and TBK-1 stabilization in Sendai virus-infected cells. Mol. Biol. Cell 17:1461-1471.
47. Harhaj NS, Sun SC, Harhaj EW. 2007. Activation of NF-kappaB by the human T cell leukemia virus type I Tax oncoprotein is associated with ubiquitin-dependent relocalization of IkappaB kinase. J. Biol. Chem. 282:4185-4192.
48. Semmes OJ, Jeang KT. 1996. Localization of human T-cell leukemia virus type 1 tax to subnuclear compartments that overlap with interchromatin speckles. J. Virol. 70:6347-6357.
49. Smith MR, Greene WC. 1990. Identification of HTLV-I tax transactivator mutants exhibiting novel transcriptional phenotypes. Genes Dev. 4:1875-1885.
50. Glickman MH, Ciechanover A. 2002. The ubiquitin-proteasome proteolytic pathway:destruction for the sake of construction. Physiol. Rev. 82:373-428.
51. Hemelaar J, Bex F, Booth B, Cerundolo V, McMichael A, Daenke S. 2001. Human T-cell leukemia virus type 1 Tax protein binds to assembled nuclear proteasomes and enhances their proteolytic activity. J. Virol. 75:11106-11115.
52. De Conto F, Pilotti E, Razin SV, Ferraglia F, Geraud G, Arcangeletti C, Scherrer K. 2000. In mouse myoblasts nuclear prosomes are associated with the nuclear matrix and accumulate preferentially in the perinucleolar areas. J. Cell Sci. 113(Part 13):2399-2407.
53. Sun SC, Elwood J, Beraud C, Greene WC. 1994. Human T-cell leukemia virus type I Tax activation of NF-kappa B/Rel involves phosphorylation and degradation of I kappa B alpha and RelA (p65)-mediated induction of the c-rel gene. Mol. Cell. Biol. 14:7377-7384.
54. Fryrear KA, Guo X, Kerscher O, Semmes OJ. 2012. The Sumo-targeted ubiquitin ligase RNF4 regulates the localization and function of the HTLV-1 oncoprotein Tax. Blood 119:1173-1181.
55. Huang J, Ren T, Guan H, Jiang Y, Cheng H. 2009. HTLV-1 Tax is a critical lipid raft modulator that hijacks IkappaB kinases to the microdomains for persistent activation of NF-kappaB. J. Biol. Chem. 284:6208-6217.
56. Durkin SS, Guo X, Fryrear KA, Mihaylova VT, Gupta SK, Belgnaoui SM, Haoudi A, Kupfer GM, Semmes OJ. 2008. HTLV-1 Tax oncoprotein subverts the cellular DNA damage response via binding to DNAdependent protein kinase. J. Biol. Chem. 283:36311-36320.
57. Lodewick J, Lamsoul I, Polania A, Lebrun S, Burny A, Ratner L, Bex F. 2009. Acetylation of the human T-cell leukemia virus type 1 Tax oncoprotein by p300 promotes activation of the NF-kappaB pathway. Virology 386:68-78.
58. Lamsoul I, Lodewick J, Lebrun S, Brasseur R, Burny A, Gaynor RB, Bex F. 2005. Exclusive ubiquitination and sumoylation on overlapping lysine residues mediate NF-kappaB activation by the human T-cell leukemia virus tax oncoprotein. Mol. Cell. Biol. 25:10391-10406.
59. Nasr R, Chiari E, El-Sabban M, Mahieux R, Kfoury Y, Abdulhay M, Yazbeck V, Hermine O, de The H, Pique C, Bazarbachi A. 2006. Tax ubiquitylation and sumoylation control critical cytoplasmic and nuclear steps of NF-kappaB activation. Blood 107:4021-4029.
60. Durkin SS, Ward MD, Fryrear KA, Semmes OJ. 2006. Site-specific phosphorylation differentiates active from inactive forms of the human T-cell leukemia virus type 1 Tax oncoprotein. J. Biol. Chem. 281:31705-31712.
61. El-Sabban ME, Nasr R, Dbaibo G, Hermine O, Abboushi N, Quignon F, Ameisen JC, Bex F, de The H, Bazarbachi A. 2000. Arsenicinterferon-alpha-triggered apoptosis in HTLV-I transformed cells is associated with tax down-regulation and reversal of NF-kappa B activation. Blood 96:2849-2855.
62. El Hajj H, El-Sabban M, Hasegawa H, Zaatari G, Ablain J, Saab ST, Janin A, Mahfouz R, Nasr R, Kfoury Y, Nicot C, Hermine O, Hall W, de The H, Bazarbachi A. 2010. Therapy-induced selective loss of leukemia-initiating activity in murine adult T cell leukemia. J. Exp. Med. 207:2785-2792.
63. Chase G, Deng T, Fodor E, Leung BW, Mayer D, Schwemmle M, Brownlee G. 2008. Hsp90 inhibitors reduce influenza virus replication in cell culture. Virology 377:431-439.
64. Nakagawa S, Umehara T, Matsuda C, Kuge S, Sudoh M, Kohara M. 2007. Hsp90 inhibitors suppress HCV replication in replicon cells and humanized liver mice. Biochem. Biophys. Res. Commun. 353:882-888.
65. Sun X, Bristol JA, Iwahori S, Hagemeier SR, Meng Q, Barlow EA, Fingeroth JD, Tarakanova VL, Kalejta RF, Kenney SC. 2013. Hsp90 inhibitor 17-DMAG decreases expression of conserved herpesvirus protein kinases and reduces virus production in Epstein-Barr virus-infected cells. J. Virol. 87:10126-10138.
66. Yan P, Qing G, Qu Z, Wu CC, Rabson A, Xiao G. 2007. Targeting autophagic regulation of NFkappaB in HTLV-I transformed cells by geldanamycin:implications for therapeutic interventions. Autophagy 3:600-603.
67. Trepel J, Mollapour M, Giaccone G, Neckers L. 2010. Targeting the dynamic HSP90 complex in cancer. Nat. Rev. Cancer 10:537-549.
68. Ikebe E, Kawaguchi A, Tezuka K, Taguchi S, Hirose S, Matsumoto T, Mitsui T, Senba K, Nishizono A, Hori M, Hasegawa H, Yamada Y, Ueno T, Tanaka Y, Sawa H, Hall W, Minami Y, Jeang KT, Ogata M, Morishita K, Hasegawa H, Fujisawa J, Iha H. 2013. Oral administration of an HSP90 inhibitor, 17-DMAG, intervenes tumor-cell infiltration into multiple organs and improves survival period for ATL model mice. Blood Cancer J. 3:e132. doi:10.1038/bcj.2013.30.
69. Takeda S, Maeda M, Morikawa S, Taniguchi Y, Yasunaga J, Nosaka K, Tanaka Y, Matsuoka M. 2004. Genetic and epigenetic inactivation of tax gene in adult T-cell leukemia cells. Int. J. Cancer 109:559-567.