Direct inhibition of RNAse T2 expression by the HTLV-1 viral protein Tax

Viruses

Volumn 3, Issue 8, 2011, Pages 1485-1500

  Polakowski, Nicholas ^a   Han, Hongjin ^a   Lemasson, Isabelle ^a  

^a EAST CAROLINA UNIVERSITY   (United States)

Author keywords

HTLV 1; Repression; RNase T2; Tax; Transcription

Indexed keywords

BRM PROTEIN; HISTONE DEACETYLASE 1; MESSENGER RNA; RIBONUCLEASE; RIBONUCLEASE T2; TAX PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING ASSAY; BINDING SITE; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CPG ISLAND; DNA PROTEIN COMPLEX; ENZYME INHIBITION; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; HUMAN T CELL LEUKEMIA VIRUS 1; MICROARRAY ANALYSIS; MOLECULAR PROBE; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN ISOLATION; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; RIBONUCLEASE T2 GENE; T LYMPHOCYTE; TRANSIENT EXPRESSION; VIRUS GENE;

BINDING SITES; CELL TRANSFORMATION, VIRAL; CHROMATIN IMMUNOPRECIPITATION; CPG ISLANDS; ENDORIBONUCLEASES; GENE EXPRESSION REGULATION, LEUKEMIC; GENE EXPRESSION REGULATION, VIRAL; GENE PRODUCTS, TAX; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMANS; LEUKEMIA-LYMPHOMA, ADULT T-CELL; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; REPRESSOR PROTEINS; RIBONUCLEASES; TUMOR SUPPRESSOR PROTEINS;

HUMAN T-LYMPHOTROPIC VIRUS 1;

EID: 80052138515     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v3081485     Document Type: Article

References (59)

1. Mahieux, R.; Gessain, A. Adult T-cell leukemia/lymphoma and HTLV-1. Curr. Hematol. Malig. Rep. 2007, 2, 257-264.
2. Azran, I.; Schavinsky-Khrapunsky, Y.; Aboud, M. Role of Tax protein in human T-cell leukemia virus type-I leukemogenicity. Retrovirology 2004, 1, 20.
3. Hasegawa, H.; Sawa, H.; Lewis, M.J.; Orba, Y.; Sheehy, N.; Yamamoto, Y.; Ichinohe, T.; Tsunetsugu-Yokota, Y.; Katano, H.; Takahashi, H.; et al. Thymus-derived leukemia-lymphoma in mice transgenic for the Tax gene of human T-lymphotropic virus type I. Nat. Med. 2006, 12, 466-472.
4. Marriott, S.J.; Semmes, O.J. Impact of HTLV-I Tax on cell cycle progression and the cellular DNA damage repair response. Oncogene 2005, 24, 5986-5995.
5. Polakowski, N.; Lemasson, I. Regulation of HTLV-1 transcription by viral and cellular proteins. In Recent Advances in Human Retroviruses: Principles of Replication and Pathogenesis. Advances in Retroviral Research; Lever, A.M.L., Jeang, K.T., Berkhout, B., Eds.; World Scientific Publishing Co.: Singapore, 2010; pp. 129-169.
6. Wang, D.; Guo, M.X.; Hu, H.M.; Zhao, Z.Z.; Qiu, H.L.; Shao, H.J.; Zhu, C.G.; Xue, L.; Shi, Y.B.; Li, W.X. Human T-cell leukemia virus type 1 oncoprotein tax represses ZNF268 expression through the cAMP-responsive element-binding protein/activating transcription factor pathway. J. Biol. Chem. 2008, 283, 16299-16308.
7. Kibler, K.V.; Jeang, K.T. CREB/ATF-dependent repression of cyclin a by human T-cell leukemia virus type 1 Tax protein. J. Virol. 2001, 75, 2161-2173.
8. Van Orden, K.; Nyborg, J.K. Insight into the tumor suppressor function of CBP through the viral oncoprotein Tax. Gene Expr. 2000, 9, 29-36.
9. Riou, P.; Bex, F.; Gazzolo, L. The human T cell leukemia/lymphotropic virus type 1 Tax protein represses MyoD-dependent transcription by inhibiting MyoD-binding to the KIX domain of p300. A potential mechanism for Tax-mediated repression of the transcriptional activity of basic helix-loop-helix factors. J. Biol. Chem. 2000, 275, 10551-10560.
10. Colgin, M.A.; Nyborg, J.K. The human T-cell leukemia virus type 1 oncoprotein Tax inhibits the transcriptional activity of c-Myb through competition for the CREB binding protein. J. Virol. 1998, 72, 9396-9399.
11. Nicot, C.; Opavsky, R.; Mahieux, R.; Johnson, J.M.; Brady, J.N.; Wolff, L.; Franchini, G. Tax oncoprotein trans-represses endogenous B-myb promoter activity in human T cells. AIDS Res. Hum. Retroviruses 2000, 16, 1629-1632.
12. Boxus, M.; Twizere, J.C.; Legros, S.; Dewulf, J.F.; Kettmann, R.; Willems, L. The HTLV-1 Tax interactome. Retrovirology 2008, 5, 76.
13. Chlichlia, K.; Khazaie, K. HTLV-1 Tax: Linking transformation, DNA damage and apoptotic T-cell death. Chem. Biol. Interact. 2010, 188, 359-365.
14. Kuo, Y.L.; Giam, C.Z. Activation of the anaphase promoting complex by HTLV-1 tax leads to senescence. EMBO J. 2006, 25, 1741-1752.
15. Tripp, A.; Banerjee, P.; Sieburg, M.; Planelles, V.; Li, F.; Feuer, G. Induction of cell cycle arrest by human T-cell lymphotropic virus type 1 Tax in hematopoietic progenitor (CD34+) cells: Modulation of p21cip1/waf1 and p27kip1 expression. J. Virol. 2005, 79, 14069-14078.
16. Yang, L.; Kotomura, N.; Ho, Y.K.; Zhi, H.; Bixler, S.; Schell, M.J.; Giam, C.Z. Complex cell cycle abnormalities caused by human T-lymphotropic virus type 1 Tax. J. Virol. 2011, 85, 3001-3009.
17. Acquati, F.; Morelli, C.; Cinquetti, R.; Bianchi, M.G.; Porrini, D.; Varesco, L.; Gismondi, V.; Rocchetti, R.; Talevi, S.; Possati, L.; et al. Cloning and characterization of a senescence inducing and class II tumor suppressor gene in ovarian carcinoma at chromosome region 6q27. Oncogene 2001, 20, 980-988.
18. Luhtala, N.; Parker, R. T2 Family ribonucleases: Ancient enzymes with diverse roles. Trends Biochem. Sci. 2010, 35, 253-259.
19. Trubia, M.; Sessa, L.; Taramelli, R. Mammalian Rh/T2/S-glycoprotein ribonuclease family genes: Cloning of a human member located in a region of chromosome 6 (6q27) frequently deleted in human malignancies. Genomics 1997, 42, 342-344.
20. Tsukasaki, K.; Krebs, J.; Nagai, K.; Tomonaga, M.; Koeffler, H.P.; Bartram, C.R.; Jauch, A. Comparative genomic hybridization analysis in adult T-cell leukemia/lymphoma: Correlation with clinical course. Blood 2001, 97, 3875-3881.
21. Liu, Y.; Emilion, G.; Mungall, A.J.; Dunham, I.; Beck, S.; Le Meuth-Metzinger, V.G.; Shelling, A.N.; Charnock, F.M.; Ganesan, T.S. Physical and transcript map of the region between D6S264 and D6S149 on chromosome 6q27, the minimal region of allele loss in sporadic epithelial ovarian cancer. Oncogene 2002, 21, 387-399.
22. Lin, H.; Morin, P.J. A novel homozygous deletion at chromosomal band 6q27 in an ovarian cancer cell line delineates the position of a putative tumor suppressor gene. Cancer Lett. 2001, 173, 63-70.
23. Monti, L.; Rodolfo, M.; Lo Russo, G.; Noonan, D.; Acquati, F.; Taramelli, R. RNASET2 as a tumor antagonizing gene in a melanoma cancer model. Oncol. Res. 2008, 17, 69-74.
24. Acquati, F.; Possati, L.; Ferrante, L.; Campomenosi, P.; Talevi, S.; Bardelli, S.; Margiotta, C.; Russo, A.; Bortoletto, E.; Rocchetti, R.; et al. Tumor and metastasis suppression by the human RNASET2 gene. Int. J. Oncol. 2005, 26, 1159-1168.
25. Liu, J.; Zhawar, V.K.; Kaur, G.; Kaur, G.P.; Deriel, J.K.; Kandpal, R.P.; Athwal, R.S. Chromosome 6 encoded RNaseT2 protein is a cell growth regulator. J. Cell Mol. Med. 2010, 14,
26. Acquati, F.; Bertilaccio, S.; Grimaldi, A.; Monti, L.; Cinquetti, R.; Bonetti, P.; Lualdi, M.; Vidalino, L.; Fabbri, M.; Sacco, M.G.; et al. Microenvironmental control of malignancy exerted by RNASET2, a widely conserved extracellular RNase. Proc. Natl. Acad. Sci. U. S. A. 2010, 108, 1104-1109.
27. Smirnoff, P.; Roiz, L.; Angelkovitch, B.; Schwartz, B.; Shoseyov, O. A recombinant human RNASET2 glycoprotein with antitumorigenic and antiangiogenic characteristics: Expression, purification, and characterization. Cancer 2006, 107, 2760-2769.
28. Polakowski, N.; Gregory, H.; Mesnard, J.M.; Lemasson, I. Expression of a protein involved in bone resorption, Dkk1, is activated by HTLV-1 bZIP factor through its activation domain. Retrovirology 2010, 7, 61.
29. Cartharius, K.; Frech, K.; Grote, K.; Klocke, B.; Haltmeier, M.; Klingenhoff, A.; Frisch, M.; Bayerlein, M.; Werner, T. MatInspector and beyond: Promoter analysis based on transcription factor binding sites. Bioinformatics 2005, 21, 2933-2942.
30. Mori, N.; Fujii, M.; Ikeda, S.; Yamada, Y.; Tomonaga, M.; Ballard, D.W.; Yamamoto, N. Constitutive activation of NF-kappaB in primary adult T-cell leukemia cells. Blood 1999, 93, 2360-2368.
31. Hironaka, N.; Mochida, K.; Mori, N.; Maeda, M.; Yamamoto, N.; Yamaoka, S. Tax-independent constitutive IkappaB kinase activation in adult T-cell leukemia cells. Neoplasia 2004, 6, 266-278.
32. Narlikar, G.J.; Fan, H.Y.; Kingston, R.E. Cooperation between complexes that regulate chromatin structure and transcription. Cell 2002, 108, 475-487.
33. Wu, K.; Bottazzi, M.E.; de la Fuente, C.; Deng, L.; Gitlin, S.D.; Maddukuri, A.; Dadgar, S.; Li, H.; Vertes, A.; Pumfery, A.; et al. Protein profile of tax-associated complexes. J. Biol. Chem. 2004, 279, 495-508.
34. Ego, T.; Ariumi, Y.; Shimotohno, K. The interaction of HTLV-1 Tax with HDAC1 negatively regulates the viral gene expression. Oncogene 2002, 21, 7241-7246.
35. Villanueva, R.; Iglesias, A.H.; Camelo, S.; Sanin, L.C.; Gray, S.G.; Dangond, F. Histone deacetylase 3 represses HTLV-1 tax transcription. Oncol. Rep. 2006, 16, 581-585.
36. Riccio, A. New endogenous regulators of class I histone deacetylases. Sci. Signal 2010, 3, pe1.
37. Clerc, I.; Polakowski, N.; Andre-Arpin, C.; Cook, P.; Barbeau, B.; Mesnard, J.M.; Lemasson, I. An interaction between the human T cell leukemia virus type 1 basic leucine zipper factor (HBZ) and the KIX domain of p300/CBP contributes to the down-regulation of tax-dependent viral transcription by HBZ. J. Biol. Chem. 2008, 283, 23903-23913.
38. Lemasson, I.; Polakowski, N.J.; Laybourn, P.J.; Nyborg, J.K. Tax-dependent displacement of nucleosomes during transcriptional activation of human T-cell leukemia virus type 1. J. Biol. Chem. 2006, 281, 13075-13082.
39. Rousset, R.; Desbois, C.; Bantignies, F.; Jalinot, P. Effects on NF-kappa B1/p105 processing of the interaction between the HTLV-1 transactivator Tax and the proteasome. Nature 1996, 381, 328-331.
40. Lemasson, I.; Nyborg, J.K. Human T-cell leukemia virus type I Tax repression of p73beta is mediated through competition for the C/H1 domain of CBP. J. Biol. Chem. 2001, 276, 15720-15727.
41. Lemasson, I.; Polakowski, N.; Laybourn, P.J.; Nyborg, J.K. Transcription factor binding and histone modifications on the integrated proviral promoter in HTLV-I-infected T-cells. J. Biol. Chem. 2002, 277, 49459-49465.
42. Oberley, M.J.; Tsao, J.; Yau, P.; Farnham, P.J. High-throughput screening of chromatin immunoprecipitates using CpG-island microarrays. Methods Enzymol. 2004, 376, 315-334.
43. Cross, S.H.; Charlton, J.A.; Nan, X.; Bird, A.P. Purification of CpG islands using a methylated DNA binding column. Nat. Genet. 1994, 6, 236-244.
44. Ren, B.; Dynlacht, B.D. Use of chromatin immunoprecipitation assays in genome-wide location analysis of mammalian transcription factors. Methods Enzymol. 2004, 376, 304-315.
45. Yie, J.; Senger, K.; Thanos, D. Mechanism by which the IFN-beta enhanceosome activates transcription. Proc. Natl. Acad. Sci. U. S. A. 1999, 96, 13108-13113.
46. Dignam, J.D.; Lebovitz, R.M.; Roeder, R.G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983, 11, 1475-1489.
47. Zhao, L.J.; Giam, C.Z. 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. U. S. A. 1991, 88, 11445-11449.
48. Kim, Y.M.; Geiger, T.R.; Egan, D.I.; Sharma, N.; Nyborg, J.K. The HTLV-1 tax protein cooperates with phosphorylated CREB, TORC2 and p300 to activate CRE-dependent cyclin D1 transcription. Oncogene 2010, 29, 2142-2152.
49. Cheng, J.; Kydd, A.R.; Nakase, K.; Noonan, K.M.; Murakami, A.; Tao, H.; Dwyer, M.; Xu, C.; Zhu, Q.; Marasco, W.A. Negative regulation of the SH2-homology containing protein-tyrosine phosphatase-1 (SHP-1) P2 promoter by the HTLV-1 Tax oncoprotein. Blood 2007, 110, 2110-2120.
50. de la Fuente, C.; Gupta, M.V.; Klase, Z.; Strouss, K.; Cahan, P.; McCaffery, T.; Galante, A.; Soteropoulos, P.; Pumfery, A.; Fujii, M.; et al. Involvement of HTLV-I Tax and CREB in aneuploidy: A bioinformatics approach. Retrovirology 2006, 3, 43.
51. Jeang, K.T.; Widen, S.G.; Semmes, O.J.; Wilson, S.H. HTLV-I trans-activator protein, Tax, is a trans-repressor of the human b-polymerase gene. Science 1990, 247, 1082-1084.
52. Lemasson, I.; Robert-Hebmann, V.; Hamaia, S.; Duc Dodon, M.; Gazzolo, L.; Devaux, C. Transrepression of lck gene expression by human T-cell leukemia virus type 1-encoded p40Tax. J. Virol. 1997, 71, 1975-1983.
53. Uittenbogaard, M.N.; Giebler, H.A.; Reisman, D.; Nyborg, J.K. Transcriptional repression of p53 by human T-cell leukemia virus type I Tax protein. J. Biol. Chem. 1995, 270, 28503-28506.
54. Suzuki, T.; Narita, T.; Uchida-Toita, M.; Yoshida, M. Down-regulation of the INK4 family of cyclin-dependent kinase inhibitors by tax protein of HTLV-1 through two distinct mechanisms. Virology 1999, 259, 384-391.
55. Chin, K.T.; Chun, A.C.; Ching, Y.P.; Jeang, K.T.; Jin, D.Y. Human T-cell leukemia virus oncoprotein tax represses nuclear receptor-dependent transcription by targeting coactivator TAX1BP1. Cancer Res. 2007, 67, 1072-1081.
56. Kinjo, T.; Ham-Terhune, J.; Peloponese, J.M., Jr.; Jeang, K.T. Induction of reactive oxygen species by human T-cell leukemia virus type 1 tax correlates with DNA damage and expression of cellular senescence marker. J. Virol. 2010, 84, 5431-5437.
57. Los, M.; Khazaie, K.; Schulze-Osthoff, K.; Baeuerle, P.A.; Schirrmacher, V.; Chlichlia, K. Human T cell leukemia virus-I (HTLV-I) Tax-mediated apoptosis in activated T cells requires an enhanced intracellular prooxidant state. J. Immunol. 1998, 161, 3050-3055.
58. Thompson, D.M.; Parker, R. The RNase Rny1p cleaves tRNAs and promotes cell death during oxidative stress in Saccharomyces cerevisiae. J. Cell Biol. 2009, 185, 43-50.
59. Masutani, H.; Hirota, K.; Sasada, T.; Ueda-Taniguchi, Y.; Taniguchi, Y.; Sono, H.; Yodoi, J. Transactivation of an inducible anti-oxidative stress protein, human thioredoxin by HTLV-I Tax. Immunol. Lett. 1996, 54, 67-71.