ATL response to arsenic/interferon therapy is triggered by SUMO/PML/RNF4-dependent Tax degradation

Blood

Volumn 125, Issue 3, 2015, Pages 474-482

  Dassouki, Zeina ^a,b   Sahin, Umut ^b,c,d   El Hajj, Hiba ^a   Jollivet, Florence ^b,c,d   Kfoury, Youmna ^a   Lallemand Breitenbach, Valérie ^b,c,d   Hermine, Olivier ^e   De Thé, Hugues ^b,c,d,f   Bazarbachi, Ali ^a  

^a AMERICAN UNIVERSITY OF BEIRUT   (Lebanon)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c Institut Universitaire d'Hématologie   (France)

^d SAINT LOUIS HOSPITAL   (France)

^e HÔPITAL NECKER ENFANTS MALADES   (France)

^f Centre de Recherche Interdisciplinaire en Biologie   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENIC; INTERFERON; PROMYELOCYTIC LEUKEMIA PROTEIN; RNF4 PROTEIN; SUMO 1 PROTEIN; SUMO 2 PROTEIN; SUMO 3 PROTEIN; SUMO PROTEIN; TAX PROTEIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; ANTIVIRUS AGENT; NUCLEAR PROTEIN; ORGANOARSENIC DERIVATIVE; PML PROTEIN, HUMAN; RNF4 PROTEIN, HUMAN; THIOL REAGENT; TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; CELL NUCLEUS INCLUSION BODY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEMALE; HELA CELL LINE; HUMAN; HUMAN CELL; HUMAN T CELL LEUKEMIA VIRUS 1; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SUMOYLATION; T CELL LEUKEMIA; UBIQUITINATION; APOPTOSIS; CELL PROLIFERATION; DRUG COMBINATION; DRUG EFFECTS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; PATHOGENICITY; VIROLOGY; VIRUS CELL TRANSFORMATION; WESTERN BLOTTING;

ANTIVIRAL AGENTS; APOPTOSIS; ARSENICALS; BLOTTING, WESTERN; CELL PROLIFERATION; CELL TRANSFORMATION, VIRAL; DRUG THERAPY, COMBINATION; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE PRODUCTS, TAX; HELA CELLS; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMANS; IMMUNOPRECIPITATION; INTERFERONS; LEUKEMIA-LYMPHOMA, ADULT T-CELL; NUCLEAR PROTEINS; PROTEOLYSIS; SULFHYDRYL REAGENTS; SUMO-1 PROTEIN; SUMOYLATION; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS; UBIQUITINATION;

EID: 84922143461     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-04-572750     Document Type: Article

References (44)

1. 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.
2. Tsukasaki K, Hermine O, Bazarbachi A, et al. Definition, prognostic factors, treatment, and response criteria of adult T-cell leukemialymphoma: a proposal from an international consensus meeting. J Clin Oncol. 2009;27(3):453-459.
3. Bazarbachi A, Suarez F, Fields P, Hermine O. How I treat adult T-cell leukemia/lymphoma. Blood. 2011;118(7):1736-1745.
4. Takeda S, Maeda M, Morikawa S, et al. Genetic and epigenetic inactivation of tax gene in adult T-cell leukemia cells. Int J Cancer. 2004;109(4):559-567.
5. El Hajj H, El-Sabban M, Hasegawa H, et al. Therapy-induced selective loss of leukemia-initiating activity in murine adult T cell leukemia. J Exp Med. 2010;207(13):2785-2792.
6. El-Sabban ME, Nasr R, Dbaibo G, et al. Arsenic-interferon-alpha-triggered apoptosis in HTLV-I transformed cells is associated with tax downregulation and reversal of NF-kappa B activation. Blood. 2000;96(8):2849-2855.
7. Kchour G, Tarhini M, Kooshyar MM, et al. Phase 2 study of the efficacy and safety of the combination of arsenic trioxide, interferon alpha, and zidovudine in newly diagnosed chronic adult T-cell leukemia/lymphoma (ATL). Blood. 2009;113(26):6528-6532.
8. Bazarbachi A, El-Sabban ME, Nasr R, et al. Arsenic trioxide and interferon-alpha synergize to induce cell cycle arrest and apoptosis in HTLV-I transformed cells. Blood. 1999;93:278-283.
9. Nasr R, Rosenwald A, El-Sabban ME, et al. Arsenic/interferon specifically reverses 2 distinct gene networks critical for the survival of HTLV-1-infected leukemic cells. Blood. 2003;101(11):4576-4582.
10. de Thé H, Chen Z. Acute promyelocytic leukaemia: novel insights into the mechanisms of cure. Nat Rev Cancer. 2010;10(11):775-783.
11. Lallemand-Breitenbach V, Zhu J, Puvion F, et al. Role of promyelocytic leukemia (PML) sumolation in nuclear body formation, 11S proteasome recruitment, and As2O3-induced PML or PML/retinoic acid receptor alpha degradation. J Exp Med. 2001;193(12):1361-1371.
12. Jeanne M, Lallemand-Breitenbach V, Ferhi O, et al. PML/RARA oxidation and arsenic binding initiate the antileukemia response of As2O3. Cancer Cell. 2010;18(1):88-98.
13. 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.
14. 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.
15. Zhang XW, Yan XJ, Zhou ZR, et al. Arsenic trioxide controls the fate of the PML-RARalpha oncoprotein by directly binding PML. Science. 2010;328(5975):240-243.
16. Stadler M, Chelbi-Alix MK, Koken MHM, et al. Transcriptional induction of the PML growth suppressor gene by interferons is mediated through an ISRE and a GAS element. Oncogene. 1995;11(12):2565-2573.
17. Zhu J, Koken MHM, Quignon F, et al. Arsenic-induced PML targeting onto nuclear bodies: implications for the treatment of acute promyelocytic leukemia. Proc Natl Acad Sci USA. 1997;94(8):3978-3983.
18. Sahin U, Ferhi O, Jeanne M, et al. Oxidative stress-induced assembly of PML nuclear bodies controls sumoylation of partner proteins. J Cell Biol. 2014;204(6):931-945.
19. Sahin U, Ferhi O, Carnec X, et al. Interferon controls SUMO availability via the Lin28 and let-7 axis to impede virus replication. Nat Commun. 2014;5:4187.
20. 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.
21. 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.
22. Katoh T, Harada T, Morikawa S, Wakutani T. IL-2-and IL-2-R-independent proliferation of T-cell lines from adult T-cell leukemia/lymphoma patients. Int J Cancer. 1986;38(2):265-274.
23. Hinuma Y, Nagata K, Hanaoka M, et al. Adult T-cell leukemia: antigen in an ATL cell line and detection of antibodies to the antigen in human sera. Proc Natl Acad Sci USA. 1981;78(10):6476-6480.
24. Mori N, Murakami S, Oda S, Prager D, Eto S. Production of interleukin 8 in adult T-cell leukemia cells: possible transactivation of the interleukin 8 gene by human T-cell leukemia virus type I tax. Cancer Res. 1995;55(16):3592-3597.
25. 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.
26. 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.
27. Fryrear KA, Guo X, Kerscher O, Semmes OJ. The Sumo-targeted ubiquitin ligase RNF4 regulates the localization and function of the HTLV-1 oncoprotein Tax. Blood. 2012;119(5):1173-1181.
28. Romanelli MG, Diani E, Bergamo E, et al. Highlights on distinctive structural and functional properties of HTLV Tax proteins. Front Microbiol. 2013;4:271.
29. Yasunaga J, Matsuoka M. Molecular mechanisms of HTLV-1 infection and pathogenesis. Int J Hematol. 2011;94(5):435-442.
30. Arnold J, Zimmerman B, Li M, Lairmore MD, Green PL. Human T-cell leukemia virus type-1 antisense-encoded gene, Hbz, promotes T-lymphocyte proliferation. Blood. 2008;112(9):3788-3797.
31. Ablain J, Rice K, Soilihi H, de Reynies A, Minucci S, de Thé H. Activation of a promyelocytic leukemia-tumor protein 53 axis underlies acute promyelocytic leukemia cure. Nat Med. 2014;20(2):167-174.
32. Nasr R, Guillemin MC, Ferhi O, et al. Eradication of acute promyelocytic leukemia-initiating cells through PML-RARA degradation. Nat Med. 2008;14(12):1333-1342.
33. Kogan SC. Curing APL: differentiation or destruction? Cancer Cell. 2009;15(1):7-8.
34. Bangham CR. The immune response to HTLV-I. Curr Opin Immunol. 2000;12(4):397-402.
35. Nasr R, El Hajj H, Kfoury Y, de Thé H, Hermine O, Bazarbachi A. Controversies in targeted therapy of adult T cell leukemia/lymphoma: ON target or OFF target effects? Viruses. 2011;3(6):750-769.
36. Hanon E, Hall S, Taylor GP, et al. Abundant tax protein expression in CD4+ T cells infected with human T-cell lymphotropic virus type I (HTLV-I) is prevented by cytotoxic T lymphocytes. Blood. 2000;95(4):1386-1392.
37. Lallemand-Breitenbach V, de Thé H. PML nuclear bodies. Cold Spring Harb Perspect Biol. 2010;2(5):a000661.
38. Quignon F, De Bels F, Koken M, Feunteun J, Ameisen J-C, de Thé H. PML induces a novel caspase-independent death process. Nat Genet. 1998;20(3):259-265.
39. Sahin U, Lallemand-Breitenbach V, de Thé H. PML nuclear bodies: regulation, function and therapeutic perspectives. J Pathol. 2014;234(3):289-291.
40. Sahin U, de The H, Lallemand-Breitenbach V. PML nuclear bodies: assembly and oxidative stress-sensitive sumoylation [published online ahead of print, October 30, 2014]. Nucleus. doi:10.4161/19491034.2014.970104.
41. Guo L, Giasson BI, Glavis-Bloom A, et al. A cellular system that degrades misfolded proteins and protects against neurodegeneration. Mol Cell. 2014;55(1):15-30.
42. Chort A, Alves S, Marinello M, et al. Interferon beta induces clearance of mutant ataxin 7 and improves locomotion in SCA7 knock-in mice. Brain. 2013;136(Pt 6):1732-1745.
43. Janer A, Martin E, Muriel MP, et al. PML clastosomes prevent nuclear accumulation of mutant ataxin-7 and other polyglutamine proteins. J Cell Biol. 2006;174(1):65-76.
44. Datta A, Bellon M, Sinha-Datta U, et al. Persistent inhibition of telomerase reprograms adult T-cell leukemia to p53-dependent senescence. Blood. 2006;108(3):1021-1029.