The Sumo-targeted ubiquitin ligase RNF4 regulates the localization and function of the HTLV-1 oncoprotein Tax

Blood

Volumn 119, Issue 5, 2012, Pages 1173-1181

  Fryrear, Kimberly A ^a,b   Guo, Xin ^a   Kerscher, Oliver ^b   Semmes, O John ^a  

^a EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

^b The College of William and Mary   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; ONCOPROTEIN; REALLY INTERESTING NEW GENE FINGER PROTEIN 4; SUMO PROTEIN; TAX PROTEIN; UBIQUITIN; UBIQUITIN LIGASE RNF4; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYCLIC AMP RESPONSIVE ELEMENT; DNA DAMAGE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HUMAN T CELL LEUKEMIA VIRUS 1; INTRACELLULAR TRANSPORT; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN TRANSPORT; REGULATORY MECHANISM; RNA INTERFERENCE; VIRUS ONCOGENE;

EID: 84856621090     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-06-358564     Document Type: Article

References (50)

1. Proietti FA, Carneiro-Proietti AB, Catalan-Soares BC, Murphy EL. Global epidemiology of HTLV-I infection and associated diseases. Oncogene. 2005;24(39):6058-6068. (Pubitemid 43086123)
2. Matsuoka M, Jeang KT. Human T-cell leukaemia virus type 1 (HTLV-1) infectivity and cellular transformation. Nat Rev Cancer. 2007;7(4):270-280. (Pubitemid 46480972)
3. Marriott SJ, Semmes OJ. Impact of HTLV-I Tax on cell cycle progression and the cellular DNA damage repair response. Oncogene. 2005;24(39):5986-5995. (Pubitemid 43086116)
4. 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):2441-2448.
5. Burton M, Upadhyaya CD, Maier B, Hope TJ, Semmes OJ. Human T-cell leukemia virus type 1 Tax shuttles between functionally discrete subcellular targets. J Virol. 2000;74(5):2351-2364. (Pubitemid 30091490)
6. Smith MR, Greene WC. Characterization of a novel nuclear localization signal in the HTLV-I tax transactivator protein. Virology. 1992;187(1):316-320.
7. Fryrear KA, Durkin SS, Gupta SK, Tiedebohl JB, Semmes OJ. Dimerization and a novel Tax speckled structure localization signal are required for Tax nuclear localization. J Virol. 2009;83(11):5339-5352.
8. Alefantis T, Barmak K, Harhaj EW, Grant C, Wigdahl B. Characterization of a nuclear export signal within the human T cell leukemia virus type I transactivator protein Tax. J Biol Chem. 2003;278(24):21814-21822. (Pubitemid 36792586)
9. Lamsoul I, Lodewick J, Lebrun S, et al. Exclusive ubiquitination and sumoylation on overlapping lysine residues mediate NF-kappaB activation by the human T-cell leukemia virus tax oncoprotein. Mol Cell Biol. 2005;25(23):10391- 10406. (Pubitemid 41681963)
10. Ulrich HD. Mutual interactions between the SUMO and ubiquitin systems: a plea of no contest. Trends Cell Biol. 2005;15(10):525-532. (Pubitemid 41396434)
11. Perry JJ, Tainer JA, Boddy MN. A SIM-ultaneous role for SUMO and ubiquitin. Trends Biochem Sci. 2008;33(5):201-208.
12. Prudden J, Pebernard S, Raffa G, et al. SUMO-targeted ubiquitin ligases in genome stability. EMBO J. 2007;26(18):4089-4101. (Pubitemid 47462097)
13. Sun H, Leverson JD, Hunter T. Conserved function of RNF4 family proteins in eukaryotes: targeting a ubiquitin ligase to SUMOylated proteins. EMBO J. 2007;26(18):4102-4112. (Pubitemid 47462098)
14. Xie Y, Kerscher O, Kroetz MB, McConchie HF, Sung P, Hochstrasser M. The yeast Hex3.Slx8 heterodimer is a ubiquitin ligase stimulated by substrate sumoylation. J Biol Chem. 2007;282(47):34176-34184. (Pubitemid 350159438)
15. Cook CE, Hochstrasser M, Kerscher O. The SUMO-targeted ubiquitin ligase subunit Slx5 resides in nuclear foci and at sites of DNA breaks. Cell Cycle. 2009;8(7):1080-1089.
16. Wang Z, Prelich G. Quality control of a transcriptional regulator by SUMO-targeted degradation. Mol Cell Biol. 2009;29(7):1694-1706.
17. Xie Y, Rubenstein EM, Matt T, Hochstrasser M. SUMO-independent in vivo activity of a SUMO-targeted ubiquitin ligase toward a short-lived transcription factor. Genes Dev. 2010;24(9):893-903.
18. Lallemand-Breitenbach V, Jeanne M, Benhenda S, et al. Arsenic degrades PML or PML-RARalpha through a SUMO-triggered RNF4/ubiquitin-mediated pathway. Nat Cell Biol. 2008;10(5):547-555. (Pubitemid 351627374)
19. Tatham MH, Geoffroy MC, Shen L, et al. RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat Cell Biol. 2008;10(5):538-546. (Pubitemid 351627373)
20. Durkin SS, Ward MD, Fryrear KA, Semmes OJ. Site-specific phosphorylation differentiates active from inactive forms of the human T-cell leukemia virus type 1 Tax oncoprotein. J Biol Chem. 2006;281(42):31705-31712. (Pubitemid 46041435)
21. Semmes OJ, Jeang KT. Localization of human T-cell leukemia virus type 1 tax to subnuclear compartments that overlap with interchromatin speckles. J Virol. 1996;70(9):6347-6357. (Pubitemid 26266855)
22. Gatza ML, Dayaram T, Marriott SJ. Ubiquitination of HTLV-I Tax in response to DNA damage regulates nuclear complex formation and nuclear export. Retrovirology. 2007;4:95.
23. Moilanen AM, Poukka H, Karvonen U, Hakli M, Janne OA, Palvimo JJ. Identification of a novel RING finger protein as a coregulator in steroid receptor-mediated gene transcription. Mol Cell Biol. 1998;18(9):5128-5139. (Pubitemid 28388096)
24. Chu ZL, DiDonato JA, Hawiger J, Ballard DW. The tax oncoprotein of human T-cell leukemia virus type 1 associates with and persistently activates IkappaB kinases containing IKKalpha and IKKbeta. J Biol Chem. 1998;273(26):15891-15894. (Pubitemid 28311350)
25. Harhaj NS, Sun SC, Harhaj EW. Activation of NF-kappa B by the human T cell leukemia virus type I Tax oncoprotein is associated with ubiquitin-dependent relocalization of I kappa B kinase. J Biol Chem. 2007;282(6):4185-4192. (Pubitemid 47084492)
26. Jin DY, Giordano V, Kibler KV, Nakano H, Jeang KT. 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. 1999;274(25):17402-17405.
27. Sun SC, Yamaoka S. Activation of NF-kappaB by HTLV-I and implications for cell transformation. Oncogene. 2005;24(39):5952-5964. (Pubitemid 43086113)
28. Nasr R, Chiari E, El-Sabban M, et al. Tax ubiquitylation and sumoylation control critical cytoplasmic and nuclear steps of NF-kappaB activation. Blood. 2006;107(10):4021-4029. (Pubitemid 43726810)
29. Kfoury Y, Nasr R, Favre-Bonvin A, et al. Ubiquitylated Tax targets and binds the IKK signalosome at the centrosome. Oncogene. 2008;27(12):1665-1676. (Pubitemid 351380258)
30. Kfoury Y, Setterblad N, El-Sabban M, et al. Tax ubiquitylation and SUMOylation control the dynamic shuttling of Tax and NEMO between Ubc9 nuclear bodies and the centrosome. Blood. 2011;117(1):190-199.
31. Mukhopadhyay D, Arnaoutov A, Dasso M. The SUMO protease SENP6 is essential for inner kinetochore assembly. J Cell Biol. 2010;188(5):681-692.
32. Martin N, Schwamborn K, Schreiber V, et al. PARP-1 transcriptional activity is regulated by sumoylation upon heat shock. EMBO J. 2009;28(22):3534-3548.
33. van Hagen M, Overmeer RM, Abolvardi SS, Vertegaal AC. RNF4 and VHL regulate the proteasomal degradation of SUMO-conjugated Hypoxia-Inducible Factor-2alpha. Nucleic Acids Res. 2010;38(6):1922-1931.
34. Belgnaoui SM, Fryrear KA, Nyalwidhe JO, Guo X, Semmes OJ. The viral oncoprotein tax sequesters DNA-damage response factors by tethering MDC1 to chromatin. J Biol Chem. 2010;285(43):32897-32905.
35. Bex F, McDowall A, Burny A, Gaynor R. The human T-cell leukemia virus type 1 transactivator protein Tax colocalizes in unique nuclear structures with NF-kappaB proteins. J Virol. 1997;71(5):3484-3497. (Pubitemid 27172359)
36. Durkin SS, Guo X, Fryrear KA, et al. HTLV-1 Tax oncoprotein subverts the cellular DNA damage response via binding to DNA-dependent protein kinase. J Biol Chem. 2008;283(52):36311-36320.
37. Gupta SK, Guo X, Durkin SS, Fryrear KF, Ward MD, Semmes OJ. Human T-cell leukemia virus type 1 Tax oncoprotein prevents DNA damage-induced chromatin egress of hyperphosphorylated Chk2. J Biol Chem. 2007;282(40):29431-29440. (Pubitemid 350043332)
38. Carter RS, Geyer BC, Xie M, Acevedo-Suarez CA, Ballard DW. Persistent activation of NF-kappa B by the tax transforming protein involves chronic phosphorylation of IkappaB kinase subunits IKKbeta and IKKgamma. J Biol Chem. 2001;276(27):24445-24448.
39. 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):22911-22914.
40. Yin MJ, Christerson LB, Yamamoto Y, et al. HTLV-I Tax protein binds to MEKK1 to stimulate IkappaB kinase activity and NF-kappaB activation. Cell. 1998;93(5):875-884. (Pubitemid 28257592)
41. Neumann M, Naumann M. Beyond IkappaBs: alternative regulation of NF-kappaB activity. FASEB J. 2007;21(11):2642-2654. (Pubitemid 47372732)
42. Jain P, Mostoller K, Flaig KE, et al. Identification of human T cell leukemia virus type 1 tax amino acid signals and cellular factors involved in secretion of the viral oncoprotein. J Biol Chem. 2007;282(47):34581-34593. (Pubitemid 350159468)
43. Chiari E, Lamsoul I, Lodewick J, Chopin C, Bex F, Pique C. Stable ubiquitination of human T-cell leukemia virus type 1 tax is required for proteasome binding. J Virol. 2004;78(21):11823-11832. (Pubitemid 39390769)
44. Peloponese JM Jr, Iha H, Yedavalli VR, et al. Ubiquitination of human T-cell leukemia virus type 1 tax modulates its activity. J Virol. 2004;78(21):11686-11695. (Pubitemid 39390755)
45. Yan P, Fu J, Qu Z, et al. PDLIM2 suppresses human T-cell leukemia virus type I Tax-mediated tumorigenesis by targeting Tax into the nuclear matrix for proteasomal degradation. Blood. 2009;113(18):4370-4380.
46. Hecker CM, Rabiller M, Haglund K, Bayer P, Dikic I. Specification of SUMO1- and SUMO2-interacting motifs. J Biol Chem. 2006;281(23):16117-16127. (Pubitemid 43848507)
47. Sibon D, Gabet AS, Zandecki M, et al. HTLV-1 propels untransformed CD4 lymphocytes into the cell cycle while protecting CD8 cells from death. J Clin Invest. 2006;116(4):974-983.
48. Haoudi A, Daniels RC, Wong E, Kupfer G, Semmes OJ. Human T-cell leukemia virus-I tax oncoprotein functionally targets a subnuclear complex involved in cellular DNA damage-response. J Biol Chem. 2003;278(39):37736-37744. (Pubitemid 37175299)
49. Yasunaga J, Lin FC, Lu X, Jeang KT. Ubiquitin-specific peptidase 20 (USP20) targets TRAF6 and HTLV-1 Tax to negatively regulate NF-kappa B signaling. J Virol. 2011;85(13):6212-6219.
50. Hwang CY, Kim IY, Kwon KS. Cytoplasmic localization and ubiquitination of p21(Cip1) by reactive oxygen species. Biochem Biophys Res Commun. 2007;358(1):219-225. (Pubitemid 46719106)