HTLV-1 Tax Induces Formation of the Active Macromolecular IKK Complex by Generating Lys63- and Met1-Linked Hybrid Polyubiquitin Chains

PLoS Pathogens

Volumn 13, Issue 1, 2017, Pages

  Shibata, Yuri ^a   Tokunaga, Fuminori ^b   Goto, Eiji ^b   Komatsu, Ginga ^a   Gohda, Jin ^a   Saeki, Yasushi ^c   Tanaka, Keiji ^c   Takahashi, Hirotaka ^d   Sawasaki, Tatsuya ^d   Inoue, Satoshi ^e   Oshiumi, Hiroyuki ^f,j   Seya, Tsukasa ^f   Nakano, Hiroyasu ^g   Tanaka, Yuetsu ^h   Iwai, Kazuhiro ⁱ   Inoue, Jun Ichiro ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^d EHIME UNIVERSITY   (Japan)

^e UNIVERSITY OF TOKYO   (Japan)

^f HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^g TOHO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^h UNIVERSITY OF THE RYUKYUS   (Japan)

ⁱ KYOTO UNIVERSITY   (Japan)

^j KUMAMOTO UNIVERSITY   (Japan)

more..

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; POLYUBIQUITIN; TAX PROTEIN; I KAPPA B KINASE;

ARTICLE; AUTOPHOSPHORYLATION; CD4+ T LYMPHOCYTE; CELL CULTURE; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN T-LYMPHOTROPIC VIRUS 1; IMMUNOBLOTTING; LENTIVIRUS INFECTION; LUCIFERASE ASSAY; MACROMOLECULE; MASS SPECTROMETRY; NONHUMAN; OLIGOMERIZATION; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; RETROVIRUS INFECTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T CELL LEUKEMIA; ENZYME ACTIVATION; HEK293 CELL LINE; HTLV-1 INFECTION; IMMUNOPRECIPITATION; JURKAT CELL LINE; METABOLISM; PATHOGENICITY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME ACTIVATION; GENE PRODUCTS, TAX; HEK293 CELLS; HTLV-I INFECTIONS; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMANS; I-KAPPA B KINASE; IMMUNOBLOTTING; IMMUNOPRECIPITATION; JURKAT CELLS; NF-KAPPA B; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 85010976202     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1006162     Document Type: Article

References (68)

1. Ishitsuka K, Tamura K, Human T-cell leukaemia virus type I and adult T-cell leukaemia-lymphoma. Lancet Oncol. 2014;15(11):e517–26. Epub 2014/10/05. doi: 10.1016/S1470-2045(14)70202-525281470
2. Gessain A, Mahieux R, Tropical spastic paraparesis and HTLV-1 associated myelopathy: clinical, epidemiological, virological and therapeutic aspects. Rev Neurol (Paris). 2012;168(3):257–69. Epub 2012/03/13.
3. Grossman WJ, Kimata JT, Wong FH, Zutter M, Ley TJ, Ratner L, 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. 1995;92(4):1057–61. Epub 1995/02/14. 7862633
4. Tanaka A, Takahashi C, Yamaoka S, Nosaka T, Maki M, Hatanaka M, Oncogenic transformation by the tax gene of human T-cell leukemia virus type I in vitro. Proc Natl Acad Sci U S A. 1990;87(3):1071–5. Epub 1990/02/01. 2300570
5. Ma G, Yasunaga J, Matsuoka M, Multifaceted functions and roles of HBZ in HTLV-1 pathogenesis. Retrovirology. 2016;13(1):16. Epub 2016/03/17.
6. Yoshida M, Molecular approach to human leukemia: isolation and characterization of the first human retrovirus HTLV-1 and its impact on tumorigenesis in adult T-cell leukemia. Proc Jpn Acad Ser B Phys Biol Sci. 2010;86(2):117–30. Epub 2010/02/16. doi: 10.2183/pjab.86.11720154469
7. Bellon M, Baydoun HH, Yao Y, Nicot C, HTLV-I Tax-dependent and -independent events associated with immortalization of human primary T lymphocytes. Blood. 2010;115(12):2441–8. Epub 2010/01/23. doi: 10.1182/blood-2009-08-24111720093405
8. Robek MD, Ratner L, 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. 1999;73(6):4856–65. Epub 1999/05/11. 10233947
9. Rosin O, Koch C, Schmitt I, Semmes OJ, Jeang KT, Grassmann R, A human T-cell leukemia virus Tax variant incapable of activating NF-κB retains its immortalizing potential for primary T-lymphocytes. J Biol Chem. 1998;273(12):6698–703. Epub 1998/04/18. 9506967
10. Hayden MS, Ghosh S, Shared principles in NF-κB signaling. Cell. 2008;132(3):344–62. Epub 2008/02/13. doi: 10.1016/j.cell.2008.01.02018267068
11. Chen ZJ, Ubiquitination in signaling to and activation of IKK. Immunol Rev. 2012;246(1):95–106. Epub 2012/03/23. doi: 10.1111/j.1600-065X.2012.01108.x22435549
12. Sun SC, The noncanonical NF-κB pathway. Immunol Rev. 2012;246(1):125–40. Epub 2012/03/23. doi: 10.1111/j.1600-065X.2011.01088.x22435551
13. Currer R, Van Duyne R, Jaworski E, Guendel I, Sampey G, Das R, et al. HTLV Tax: a fascinating multifunctional co-regulator of viral and cellular pathways. Front Microbiol. 2012;3:406. Epub 2012/12/12. doi: 10.3389/fmicb.2012.0040623226145
14. Liu S, Chen ZJ, Expanding role of ubiquitination in NF-κB signaling. Cell Res. 2011;21(1):6–21. Epub 2010/12/08. doi: 10.1038/cr.2010.17021135871
15. Hershko A, Ciechanover A, The ubiquitin system. Annu Rev Biochem. 1998;67:425–79. Epub 1998/10/06. doi: 10.1146/annurev.biochem.67.1.4259759494
16. Komander D, Rape M, The ubiquitin code. Annu Rev Biochem. 2012;81:203–29. Epub 2012/04/25. doi: 10.1146/annurev-biochem-060310-17032822524316
17. Iwai K, Fujita H, Sasaki Y, Linear ubiquitin chains: NF-κB signalling, cell death and beyond. Nat Rev Mol Cell Biol. 2014;15(8):503–8. Epub 2014/07/17. doi: 10.1038/nrm383625027653
18. Bertrand MJ, Milutinovic S, Dickson KM, Ho WC, Boudreault A, Durkin J, et al. cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol Cell. 2008;30(6):689–700. Epub 2008/06/24. doi: 10.1016/j.molcel.2008.05.01418570872
19. Dynek JN, Goncharov T, Dueber EC, Fedorova AV, Izrael-Tomasevic A, Phu L, et al. c-IAP1 and UbcH5 promote K11-linked polyubiquitination of RIP1 in TNF signalling. EMBO J. 2010;29(24):4198–209. Epub 2010/11/30. doi: 10.1038/emboj.2010.30021113135
20. Mahoney DJ, Cheung HH, Mrad RL, Plenchette S, Simard C, Enwere E, et al. Both cIAP1 and cIAP2 regulate TNFα-mediated NF-κB activation. Proc Natl Acad Sci U S A. 2008;105(33):11778–83. Epub 2008/08/14. doi: 10.1073/pnas.071112210518697935
21. Haas TL, Emmerich CH, Gerlach B, Schmukle AC, Cordier SM, Rieser E, et al. Recruitment of the linear ubiquitin chain assembly complex stabilizes the TNF-R1 signaling complex and is required for TNF-mediated gene induction. Mol Cell. 2009;36(5):831–44. Epub 2009/12/17. doi: 10.1016/j.molcel.2009.10.01320005846
22. Ikeda F, Deribe YL, Skanland SS, Stieglitz B, Grabbe C, Franz-Wachtel M, et al. SHARPIN forms a linear ubiquitin ligase complex regulating NF-κB activity and apoptosis. Nature. 2011;471(7340):637–41. Epub 2011/04/02. doi: 10.1038/nature0981421455181
23. Tokunaga F, Nakagawa T, Nakahara M, Saeki Y, Taniguchi M, Sakata S, et al. SHARPIN is a component of the NF-κB-activating linear ubiquitin chain assembly complex. Nature. 2011;471(7340):633–6. Epub 2011/04/02. doi: 10.1038/nature0981521455180
24. Tokunaga F, Sakata S, Saeki Y, Satomi Y, Kirisako T, Kamei K, et al. Involvement of linear polyubiquitylation of NEMO in NF-κB activation. Nat Cell Biol. 2009;11(2):123–32. Epub 2009/01/13. doi: 10.1038/ncb182119136968
25. Chu ZL, Shin YA, Yang JM, DiDonato JA, Ballard DW, IKKγ mediates the interaction of cellular IκB kinases with the tax transforming protein of human T cell leukemia virus type 1. J Biol Chem. 1999;274(22):15297–300. Epub 1999/05/21. 10336413
26. Harhaj EW, Sun SC, 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. 1999;274(33):22911–4. Epub 1999/08/07. 10438454
27. Shibata Y, Tanaka Y, Gohda J, Inoue J, Activation of the IκB kinase complex by HTLV-1 Tax requires cytosolic factors involved in Tax-induced polyubiquitination. J Biochem. 2011;150(6):679–86. Epub 2011/08/25. doi: 10.1093/jb/mvr10621862596
28. Ho YK, Zhi H, Bowlin T, Dorjbal B, Philip S, Zahoor MA, et al. HTLV-1 Tax Stimulates Ubiquitin E3 Ligase, Ring Finger Protein 8, to Assemble Lysine 63-Linked Polyubiquitin Chains for TAK1 and IKK Activation. PLoS Pathog. 2015;11(8):e1005102. Epub 2015/08/19. doi: 10.1371/journal.ppat.100510226285145
29. Wang C, Long W, Peng C, Hu L, Zhang Q, Wu A, et al. HTLV-1 Tax Functions as a Ubiquitin E3 Ligase for Direct IKK Activation via Synthesis of Mixed-Linkage Polyubiquitin Chains. PLoS Pathog. 2016;12(4):e1005584. Epub 2016/04/16. doi: 10.1371/journal.ppat.100558427082114
30. Shembade N, Harhaj NS, Yamamoto M, Akira S, Harhaj EW, The human T-cell leukemia virus type 1 Tax oncoprotein requires the ubiquitin-conjugating enzyme Ubc13 for NF-κB activation. J Virol. 2007;81(24):13735–42. Epub 2007/10/19. doi: 10.1128/JVI.01790-0717942533
31. Alvarez SE, Harikumar KB, Hait NC, Allegood J, Strub GM, Kim EY, et al. Sphingosine-1-phosphate is a missing cofactor for the E3 ubiquitin ligase TRAF2. Nature. 2010;465(7301):1084–8. Epub 2010/06/26. doi: 10.1038/nature0912820577214
32. Gack MU, Shin YC, Joo CH, Urano T, Liang C, Sun L, et al. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature. 2007;446(7138):916–20. Epub 2007/03/30. doi: 10.1038/nature0573217392790
33. Oshiumi H, Miyashita M, Inoue N, Okabe M, Matsumoto M, Seya T, The ubiquitin ligase Riplet is essential for RIG-I-dependent innate immune responses to RNA virus infection. Cell Host Microbe. 2010;8(6):496–509. Epub 2010/12/15. doi: 10.1016/j.chom.2010.11.00821147464
34. Tada K, Okazaki T, Sakon S, Kobarai T, Kurosawa K, Yamaoka S, et al. Critical roles of TRAF2 and TRAF5 in tumor necrosis factor-induced NF-κB activation and protection from cell death. J Biol Chem. 2001;276(39):36530–4. Epub 2001/08/02. doi: 10.1074/jbc.M10483720011479302
35. Silke J, Vaux DL, IAP gene deletion and conditional knockout models. Semin Cell Dev Biol. 2015;39:97–105. Epub 2014/12/30. doi: 10.1016/j.semcdb.2014.12.00425545814
36. Urano T, Saito T, Tsukui T, Fujita M, Hosoi T, Muramatsu M, et al. Efp targets 14-3-3 sigma for proteolysis and promotes breast tumour growth. Nature. 2002;417(6891):871–5. Epub 2002/06/21. doi: 10.1038/nature0082612075357
37. Yamazaki K, Gohda J, Kanayama A, Miyamoto Y, Sakurai H, Yamamoto M, et al. Two mechanistically and temporally distinct NF-κB activation pathways in IL-1 signaling. Sci Signal. 2009;2(93):ra66. Epub 2009/10/22. doi: 10.1126/scisignal.200038719843958
38. Semmes OJ, Jeang KT, HTLV-I Tax is a zinc-binding protein: role of zinc in Tax structure and function. Virology. 1992;188(2):754–64. Epub 1992/06/01. 1585646
39. Wertz IE, O'Rourke KM, Zhou H, Eby M, Aravind L, Seshagiri S, et al. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-κB signalling. Nature. 2004;430(7000):694–9. Epub 2004/07/20. doi: 10.1038/nature0279415258597
40. Sasaki Y, Sano S, Nakahara M, Murata S, Kometani K, Aiba Y, et al. Defective immune responses in mice lacking LUBAC-mediated linear ubiquitination in B cells. EMBO J. 2013;32(18):2463–76. Epub 2013/08/15. doi: 10.1038/emboj.2013.18423942237
41. Nagata K, Ohtani K, Nakamura M, Sugamura K, 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. 1989;63(8):3220–6. Epub 1989/08/01. 2501514
42. Emmerich CH, Ordureau A, Strickson S, Arthur JS, Pedrioli PG, Komander D, et al. Activation of the canonical IKK complex by K63/M1-linked hybrid ubiquitin chains. Proc Natl Acad Sci U S A. 2013;110(38):15247–52. Epub 2013/08/30. doi: 10.1073/pnas.131471511023986494
43. Mevissen TE, Hospenthal MK, Geurink PP, Elliott PR, Akutsu M, Arnaudo N, et al. OTU deubiquitinases reveal mechanisms of linkage specificity and enable ubiquitin chain restriction analysis. Cell. 2013;154(1):169–84. Epub 2013/07/06. doi: 10.1016/j.cell.2013.05.04623827681
44. Wang T, Yin L, Cooper EM, Lai MY, Dickey S, Pickart CM, et al. Evidence for bidentate substrate binding as the basis for the K48 linkage specificity of otubain 1. J Mol Biol. 2009;386(4):1011–23. Epub 2009/02/13. doi: 10.1016/j.jmb.2008.12.08519211026
45. Komander D, Reyes-Turcu F, Licchesi JD, Odenwaelder P, Wilkinson KD, Barford D, Molecular discrimination of structurally equivalent Lys 63-linked and linear polyubiquitin chains. EMBO Rep. 2009;10(5):466–73. Epub 2009/04/18. doi: 10.1038/embor.2009.5519373254
46. Keusekotten K, Elliott PR, Glockner L, Fiil BK, Damgaard RB, Kulathu Y, et al. OTULIN antagonizes LUBAC signaling by specifically hydrolyzing Met1-linked polyubiquitin. Cell. 2013;153(6):1312–26. Epub 2013/06/12. doi: 10.1016/j.cell.2013.05.01423746843
47. Ye Y, Akutsu M, Reyes-Turcu F, Enchev RI, Wilkinson KD, Komander D, Polyubiquitin binding and cross-reactivity in the USP domain deubiquitinase USP21. EMBO Rep. 2011;12(4):350–7. Epub 2011/03/15. doi: 10.1038/embor.2011.1721399617
48. Tsuchiya H, Tanaka K, Saeki Y, The parallel reaction monitoring method contributes to a highly sensitive polyubiquitin chain quantification. Biochem Biophys Res Commun. 2013;436(2):223–9. Epub 2013/06/04. doi: 10.1016/j.bbrc.2013.05.08023726910
49. Xia ZP, Sun L, Chen X, Pineda G, Jiang X, Adhikari A, et al. Direct activation of protein kinases by unanchored polyubiquitin chains. Nature. 2009;461(7260):114–9. Epub 2009/08/14. doi: 10.1038/nature0824719675569
50. Nasr R, Chiari E, El-Sabban M, Mahieux R, Kfoury Y, Abdulhay M, et al. Tax ubiquitylation and sumoylation control critical cytoplasmic and nuclear steps of NF-κB activation. Blood. 2006;107(10):4021–9. Epub 2006/01/21. doi: 10.1182/blood-2005-09-357216424386
51. Lamsoul I, Lodewick J, Lebrun S, Brasseur R, Burny A, Gaynor RB, et al. Exclusive ubiquitination and sumoylation on overlapping lysine residues mediate NF-κB activation by the human T-cell leukemia virus tax oncoprotein. Mol Cell Biol. 2005;25(23):10391–406. Epub 2005/11/17. doi: 10.1128/MCB.25.23.10391-10406.200516287853
52. Bonnet A, Randrianarison-Huetz V, Nzounza P, Nedelec M, Chazal M, Waast L, et al. Low nuclear body formation and tax SUMOylation do not prevent NF-κB promoter activation. Retrovirology. 2012;9:77. Epub 2012/09/27. doi: 10.1186/1742-4690-9-7723009398
53. Laplantine E, Fontan E, Chiaravalli J, Lopez T, Lakisic G, Veron M, et al. NEMO specifically recognizes K63-linked poly-ubiquitin chains through a new bipartite ubiquitin-binding domain. EMBO J. 2009;28(19):2885–95. Epub 2009/09/19. doi: 10.1038/emboj.2009.24119763089
54. Rahighi S, Ikeda F, Kawasaki M, Akutsu M, Suzuki N, Kato R, et al. Specific recognition of linear ubiquitin chains by NEMO is important for NF-κB activation. Cell. 2009;136(6):1098–109. Epub 2009/03/24. doi: 10.1016/j.cell.2009.03.00719303852
55. Wittig I, Braun HP, Schagger H, Blue native PAGE. Nat Protoc. 2006;1(1):418–28. Epub 2007/04/05. doi: 10.1038/nprot.2006.6217406264
56. Gazdar AF, Carney DN, Bunn PA, Russell EK, Jaffe ES, Schechter GP, et al. Mitogen requirements for the in vitro propagation of cutaneous T-cell lymphomas. Blood. 1980;55(3):409–17. Epub 1980/03/01. 6244013
57. Miyoshi I, Kubonishi I, Yoshimoto S, Shiraishi Y, A T-cell line derived from normal human cord leukocytes by co-culturing with human leukemic T-cells. Gan. 1981;72(6):978–81. Epub 1981/12/01. 6281119
58. Miyoshi I, Kubonishi I, Yoshimoto S, Akagi T, Ohtsuki Y, Shiraishi Y, et al. Type C virus particles in a cord T-cell line derived by co-cultivating normal human cord leukocytes and human leukaemic T cells. Nature. 1981;294(5843):770–1. Epub 1981/12/24. 6275274
59. Wang C, Deng L, Hong M, Akkaraju GR, Inoue J, Chen ZJ, TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature. 2001;412(6844):346–51. Epub 2001/07/19. doi: 10.1038/3508559711460167
60. Gohda J, Irisawa M, Tanaka Y, Sato S, Ohtani K, Fujisawa J, et al. HTLV-1 Tax-induced NFκB activation is independent of Lys-63-linked-type polyubiquitination. Biochem Biophys Res Commun. 2007;357(1):225–30. Epub 2007/04/10. doi: 10.1016/j.bbrc.2007.03.12517418100
61. Shibata Y, Oyama M, Kozuka-Hata H, Han X, Tanaka Y, Gohda J, et al. p47 negatively regulates IKK activation by inducing the lysosomal degradation of polyubiquitinated NEMO. Nat Commun. 2012;3:1061. Epub 2012/09/20. doi: 10.1038/ncomms206822990857
62. Yin MJ, Christerson LB, Yamamoto Y, Kwak YT, Xu S, Mercurio F, et al. HTLV-I Tax protein binds to MEKK1 to stimulate IκB kinase activity and NF-κB activation. Cell. 1998;93(5):875–84. Epub 1998/06/18. 9630230
63. Wu X, Sun SC, Retroviral oncoprotein Tax deregulates NF-κB by activating Tak1 and mediating the physical association of Tak1-IKK. EMBO Rep. 2007;8(5):510–5. Epub 2007/03/17. doi: 10.1038/sj.embor.740093117363973
64. Pujari R, Hunte R, Thomas R, van der Weyden L, Rauch D, Ratner L, et al. Human T-cell leukemia virus type 1 (HTLV-1) tax requires CADM1/TSLC1 for inactivation of the NF-κB inhibitor A20 and constitutive NF-κB signaling. PLoS Pathog. 2015;11(3):e1004721. Epub 2015/03/17. doi: 10.1371/journal.ppat.100472125774694
65. Ohtake F, Saeki Y, Ishido S, Kanno J, Tanaka K, The K48-K63 Branched Ubiquitin Chain Regulates NF-κB Signaling. Mol Cell. 2016;64(2):251–66. Epub 2016/10/22. doi: 10.1016/j.molcel.2016.09.01427746020
66. Kirisako T, Kamei K, Murata S, Kato M, Fukumoto H, Kanie M, et al. A ubiquitin ligase complex assembles linear polyubiquitin chains. EMBO J. 2006;25(20):4877–87. Epub 2006/09/29. doi: 10.1038/sj.emboj.760136017006537
67. Lee B, Tanaka Y, Tozawa H, Monoclonal antibody defining tax protein of human T-cell leukemia virus type-I. Tohoku J Exp Med. 1989;157(1):1–11. Epub 1989/01/01. 2711372
68. Takai K, Sawasaki T, Endo Y, Practical cell-free protein synthesis system using purified wheat embryos. Nat Protoc. 2010;5(2):227–38. Epub 2010/02/06. doi: 10.1038/nprot.2009.20720134421