HTLV-1 Tax Stimulates Ubiquitin E3 Ligase, Ring Finger Protein 8, to Assemble Lysine 63-Linked Polyubiquitin Chains for TAK1 and IKK Activation

PLoS Pathogens

Volumn 11, Issue 8, 2015, Pages

  Ho, Yik Khuan ^a   Zhi, Huijun ^a   Bowlin, Tara ^a   Dorjbal, Batsukh ^a   Philip, Subha ^a   Zahoor, Muhammad Atif ^a   Shih, Hsiu Ming ^b   Semmes, Oliver John ^c   Schaefer, Brian ^a   Glover, J N Mark ^d   Giam, Chou Zen ^a  

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

^b INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^c EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE TRANSFERASE; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LYSINE 63 LINKED POLYUBIQUITIN; POLYUBIQUITIN; PROTEIN S 100; RING FINGER PROTEIN; RING FINGER PROTEIN 8; STRESS ACTIVATED PROTEIN KINASE; TAX PROTEIN; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; MAP KINASE KINASE KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; RNF8 PROTEIN, HUMAN; TAX PROTEIN, HUMAN T-LYMPHOTROPHIC VIRUS 1; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA TRANSFECTION; GENE SILENCING; GENOMIC INSTABILITY; HEK293 CELL LINE; HUMAN; HUMAN CELL; HUMAN T-LYMPHOTROPIC VIRUS 1; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; LUCIFERASE ASSAY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION; T CELL LEUKEMIA; UBIQUITINATION; CELL LINE; CELL TRANSFORMATION; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC TRANSFECTION; METABOLISM; PHYSIOLOGY; POLYMERASE CHAIN REACTION;

CELL LINE; CELL TRANSFORMATION, NEOPLASTIC; DNA-BINDING PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; GENE KNOCKDOWN TECHNIQUES; GENE PRODUCTS, TAX; HUMANS; I-KAPPA B KINASE; IMMUNOBLOTTING; MAP KINASE KINASE KINASES; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSFECTION; UBIQUITIN-PROTEIN LIGASES;

EID: 84940767771     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005102     Document Type: Article

References (59)

1. Tanaka A, Takahashi C, Yamaoka S, Nosaka T, Maki M, et al. (1990) Oncogenic transformation by the tax gene of human T-cell leukemia virus type I in vitro. ProcNatlAcadSciUSA 87: 1071–1075.
2. Chu ZL, Shin YA, Yang JM, Di Donato JA, Ballard DW LH, (1999) IKKgamma mediates the interaction of cellular IkappaB kinases with the tax transforming protein of human T cell leukemia virus type 1. JBiolChem 1999 May 28;274: 15297–15300.
3. Jin DY, Giordano V, Kibler KV, Nakano H, Jeang KT LH, (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. JBiolChem 1999 Jun 18;274: 17402–17405.
4. Xiao G, Sun SC, (2000) Activation of IKKalpha and IKKbeta through their fusion with HTLV-I tax protein. Oncogene 2000 Oct 26;19: 5198–5203. 11064457
5. Grossman WJ, Kimata JT, Wong FH, Zutter M, Ley TJ, et al. (1995) Development of leukemia in mice transgenic for the tax gene of human T-cell leukemia virus type I. ProcNatlAcadSciUSA 92: 1057–1061.
6. Matsumoto K, Shibata H, Fujisawa JI, Inoue H, Hakura A, et al. (1997) Human T-cell leukemia virus type 1 Tax protein transforms rat fibroblasts via two distinct pathways. JVirol 71: 4445–4451.
7. Yamaoka S, Inoue H, Sakurai M, Sugiyama T, Hazama M, et al. (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. 8631308
8. Yamaoka S, Courtois G, Bessia C, Whiteside ST, Weil R, et al. (1998) Complementation cloning of NEMO, a component of the IkappaB kinase complex essential for NF-kappaB activation. Cell 1998 Jun 26;93: 1231–1240. 9657155
9. Hasegawa H, Sawa H, Lewis MJ, Orba Y, Sheehy N, et al. (2006) Thymus-derived leukemia-lymphoma in mice transgenic for the Tax gene of human T-lymphotropic virus type I. NatMed 12: 466–472.
10. Uhlik M, Good L, Xiao G, Harhaj EW, Zandi E, et al. (1998) NF-kappaB-inducing kinase and IkappaB kinase participate in human T-cell leukemia virus I Tax-mediated NF-kappaB activation. JBiolChem 1998 Aug 14;273: 21132–21136.
11. Wu X, Sun SC, (2007) Retroviral oncoprotein Tax deregulates NF-kappaB by activating Tak1 and mediating the physical association of Tak1-IKK. EMBO Rep 8: 510–515. 17363973
12. Ho YK, Zhi H, Debiaso D, Philip S, Shih HM, et al. (2012) HTLV-1 Tax-Induced Rapid Senescence Is Driven by the Transcriptional Activity of NF-kappaB and Depends on Chronically Activated IKKalpha and p65/RelA. JVirol 86: 9474–9483.
13. Deng L, Wang C, Spencer E, Yang L, Braun A, et al. (2000) Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103: 351–361. 11057907
14. Ea CK, Deng L, Xia ZP, Pineda G, Chen ZJ, (2006) Activation of IKK by TNFalpha requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. MolCell 22: 245–257.
15. Liu S, Chen ZJ, (2011) Expanding role of ubiquitination in NF-kappaB signaling. Cell Res 21: 6–21. doi: 10.1038/cr.2010.170 21135871
16. 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. JVirol 81: 13735–13742.
17. Shibata Y, Tanaka Y, Gohda J, Inoue J, (2011) Activation of the IkappaB kinase complex by HTLV-1 Tax requires cytosolic factors involved in Tax-induced polyubiquitination. JBiochem 150: 679–686.
18. Andersen PL, Zhou H, Pastushok L, Moraes T, McKenna S, et al. (2005) Distinct regulation of Ubc13 functions by the two ubiquitin-conjugating enzyme variants Mms2 and Uev1A. J Cell Biol 170: 745–755. 16129784
19. Hofmann RM, Pickart CM, (1999) Noncanonical MMS2-encoded ubiquitin-conjugating enzyme functions in assembly of novel polyubiquitin chains for DNA repair. Cell 96: 645–653. 10089880
20. Dignam JD, Lebovitz RM, Roeder RG, (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 11: 1475–1489. 6828386
21. Zhang M, Windheim M, Roe SM, Peggie M, Cohen P, et al. (2005) Chaperoned ubiquitylation—crystal structures of the CHIP U box E3 ubiquitin ligase and a CHIP-Ubc13-Uev1a complex. Mol Cell 20: 525–538. 16307917
22. Bothos J, Summers MK, Venere M, Scolnick DM, Halazonetis TD, (2003) The Chfr mitotic checkpoint protein functions with Ubc13-Mms2 to form Lys63-linked polyubiquitin chains. Oncogene 22: 7101–7107. 14562038
23. Unk I, Hajdu I, Fatyol K, Hurwitz J, Yoon JH, et al. (2008) Human HLTF functions as a ubiquitin ligase for proliferating cell nuclear antigen polyubiquitination. Proc Natl Acad Sci U S A 105: 3768–3773. doi: 10.1073/pnas.0800563105 18316726
24. Wang B, Elledge SJ, (2007) Ubc13/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Brca1/Brcc36 complex in response to DNA damage. ProcNatlAcadSciUSA 104: 20759–20763.
25. Adhikari A, Xu M, Chen ZJ, (2007) Ubiquitin-mediated activation of TAK1 and IKK. Oncogene 26: 3214–3226. 17496917
26. Takano Y, Adachi S, Okuno M, Muto Y, Yoshioka T, et al. (2004) The RING finger protein, RNF8, interacts with retinoid X receptor alpha and enhances its transcription-stimulating activity. JBiolChem 279: 18926–18934.
27. Campbell SJ, Edwards RA, Leung CC, Neculai D, Hodge CD, et al. (2012) Molecular insights into the function of RING finger (RNF)-containing proteins hRNF8 and hRNF168 in Ubc13/Mms2-dependent ubiquitylation. JBiolChem 287: 23900–23910.
28. Mattiroli F, Vissers JH, van Dijk WJ, Ikpa P, Citterio E, et al. (2012) RNF168 ubiquitinates K13-15 on H2A/H2AX to drive DNA damage signaling. Cell 150: 1182–1195. doi: 10.1016/j.cell.2012.08.005 22980979
29. Huen MS, Grant R, Manke I, Minn K, Yu X, et al. (2007) RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 131: 901–914. 18001825
30. Kolas NK, Chapman JR, Nakada S, Ylanko J, Chahwan R, et al. (2007) Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 318: 1637–1640. 18006705
31. Chahwan R, Gravel S, Matsusaka T, Jackson SP, (2013) Dma/RNF8 proteins are evolutionarily conserved E3 ubiquitin ligases that target septins. Cell Cycle 12: 1000–1008. doi: 10.4161/cc.23947 23442799
32. Plans V, Guerra-Rebollo M, Thomson TM, (2008) Regulation of mitotic exit by the RNF8 ubiquitin ligase. Oncogene 27: 1355–1365. 17724460
33. Nitta T, Kanai M, Sugihara E, Tanaka M, Sun B, et al. (2006) Centrosome amplification in adult T-cell leukemia and human T-cell leukemia virus type 1 Tax-induced human T cells. Cancer Sci 97: 836–841. 16805820
34. Zhao LJ, Giam CZ, (1992) Human T-cell lymphotropic virus type I (HTLV-I) transcriptional activator, Tax, enhances CREB binding to HTLV-I 21-base-pair repeats by protein-protein interaction. ProcNatlAcadSciUSA 89: 7070–7074.
35. Adya N, Zhao LJ, Huang W, Boros I, Giam CZ, (1994) Expansion of CREB's DNA recognition specificity by Tax results from interaction with Ala-Ala-Arg at positions 282–284 near the conserved DNA-binding domain of CREB. ProcNatlAcadSciUSA 91: 5642–5646.
36. Xu X, Heidenreich O, Kitajima I, McGuire K, Li Q, et al. (1996) Constitutively activated JNK is associated with HTLV-1 mediated tumorigenesis. Oncogene 13: 135–142. 8700539
37. Tournier C, Dong C, Turner TK, Jones SN, Flavell RA, et al. (2001) MKK7 is an essential component of the JNK signal transduction pathway activated by proinflammatory cytokines. Genes Dev 15: 1419–1426. 11390361
38. Guerra-Rebollo M, Mateo F, Franke K, Huen MS, Lopitz-Otsoa F, et al. (2012) Nucleolar exit of RNF8 and BRCA1 in response to DNA damage. Exp Cell Res 318: 2365–2376. doi: 10.1016/j.yexcr.2012.07.003 22814251
39. 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. JVirol 2000 Mar;74: 2351–2364.
40. Zhang L, Liu M, Merling R, Giam CZ, (2006) Versatile reporter systems show that transactivation by human T-cell leukemia virus type 1 Tax occurs independently of chromatin remodeling factor BRG1. JVirol 80: 7459–7468.
41. Xia ZP, Sun L, Chen X, Pineda G, Jiang X, et al. (2009) Direct activation of protein kinases by unanchored polyubiquitin chains. Nature 461: 114–119. doi: 10.1038/nature08247 19675569
42. Vallabhapurapu S, Karin M, (2009) Regulation and function of NF-kappaB transcription factors in the immune system. AnnuRevImmunol 27: 693–733.
43. Habelhah H, (2010) Emerging complexity of protein ubiquitination in the NF-kappaB pathway. Genes Cancer 1: 735–747. 21113390
44. Harhaj EW, Dixit VM, (2011) Deubiquitinases in the regulation of NF-kappaB signaling. Cell Res 21: 22–39. doi: 10.1038/cr.2010.166 21119682
45. Emmerich CH, Ordureau A, Strickson S, Arthur JS, Pedrioli PG, et al. (2013) Activation of the canonical IKK complex by K63/M1-linked hybrid ubiquitin chains. Proc Natl Acad Sci U S A 110: 15247–15252. doi: 10.1073/pnas.1314715110 23986494
46. Peloponese JM, Jr.Iha H, Yedavalli VR, Miyazato A, Li Y, et al. (2004) Ubiquitination of human T-cell leukemia virus type 1 tax modulates its activity. JVirol 78: 11686–11695.
47. Lamsoul I, Lodewick J, Lebrun S, Brasseur R, Burny A, et al. (2005) Exclusive ubiquitination and sumoylation on overlapping lysine residues mediate NF-kappaB activation by the human T-cell leukemia virus tax oncoprotein. MolCell Biol 25: 10391–10406.
48. Journo C, Filipe J, About F, Chevalier SA, Afonso PV, et al. (2009) NRP/Optineurin Cooperates with TAX1BP1 to potentiate the activation of NF-kappaB by human T-lymphotropic virus type 1 tax protein. PLoS Pathog 5: e1000521. doi: 10.1371/journal.ppat.1000521 19609363
49. 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. doi: 10.1182/blood-2011-06-358564 22106342
50. Dassouki Z, Sahin U, El Hajj H, Jollivet F, Kfoury Y, et al. (2015) ATL response to arsenic/interferon therapy is triggered by SUMO/PML/RNF4-dependent Tax degradation. Blood 125: 474–482. doi: 10.1182/blood-2014-04-572750 25395419
51. Mailand N, Bekker-Jensen S, Faustrup H, Melander F, Bartek J, et al. (2007) RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131: 887–900. 18001824
52. Marriott SJ, Semmes OJ, (2005) Impact of HTLV-I Tax on cell cycle progression and the cellular DNA damage repair response. Oncogene 24: 5986–5995. 16155605
53. Kuo YL, Giam CZ, (2006) Activation of the anaphase promoting complex by HTLV-1 tax leads to senescence. EMBO J 25: 1741–1752. 16601696
54. Zhi H, Yang L, Kuo YL, Ho YK, Shih HM, et al. (2011) NF-kappaB Hyper-Activation by HTLV-1 Tax Induces Cellular Senescence, but Can Be Alleviated by the Viral Anti-Sense Protein HBZ. PLoSPathog 7: e1002025.
55. Liu M, Yang L, Zhang L, Liu B, Merling R, et al. (2008) Human T-cell leukemia virus type 1 infection leads to arrest in the G1 phase of the cell cycle. JVirol 82: 8442–8455.
56. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, et al. (2013) Genome engineering using the CRISPR-Cas9 system. Nat Protoc 8: 2281–2308. doi: 10.1038/nprot.2013.143 24157548
57. Wang W, Lin C, Lu D, Ning Z, Cox T, et al. (2008) Chromosomal transposition of PiggyBac in mouse embryonic stem cells. ProcNatlAcadSciUSA 105: 9290–9295.
58. Zhao LJ, Giam CZ, (1991) Interaction of the human T-cell lymphotropic 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. ProcNatlAcadSciUSA 88: 11445–11449.
59. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402–408. 11846609