The transcription profile of Tax-3 is more similar to Tax-1 than Tax-2: Insights into HTLV-3 potential leukemogenic properties

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Chevalier, Sébastien A ^a,b   Durand, Stéphanie ^b   Dasgupta, Arindam ^a   Radonovich, Michael ^a   Cimarelli, Andrea ^b   Brady, John N ^a   Mahieux, Renaud ^b   Pise Masison, Cynthia A ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 15; LENTIVIRUS VECTOR; TAX PROTEIN; TAX1 PROTEIN; TAX2 PROTEIN; TAX3 PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BIRC 3 GENE; CONTROLLED STUDY; DNA MICROARRAY; ENZYME ACTIVATION; GADD45B GENE; GENE; GENE CLUSTER; GENE DEREGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENETIC PARAMETERS; GENETIC TRANSDUCTION; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN T CELL LEUKEMIA VIRUS 1; HUMAN T CELL LEUKEMIA VIRUS INFECTION; ICAM 1 GENE; IL 15 GENE; IMMUNE RESPONSE; LEUKEMOGENESIS; LEUKOCYTE ACTIVATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; T LYMPHOCYTE ACTIVATION; TRANSACTIVATION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; VIRUS CARCINOGENESIS; VIRUS TYPING;

CELL LINE, TUMOR; CELL TRANSFORMATION, VIRAL; CLUSTER ANALYSIS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE ORDER; GENE PRODUCTS, TAX; GENE REGULATORY NETWORKS; GENETIC VECTORS; HEK293 CELLS; HUMAN T-LYMPHOTROPIC VIRUS 3; HUMANS; REPRODUCIBILITY OF RESULTS; TRANSCRIPTIONAL ACTIVATION; TRANSDUCTION, GENETIC;

HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMAN T-LYMPHOTROPIC VIRUS 2;

EID: 84864097251     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041003     Document Type: Article

References (87)

1. Verdonck K, Gonzalez E, Van Dooren S, Vandamme AM, Vanham G, et al. (2007) Human T-lymphotropic virus 1: recent knowledge about an ancient infection. Lancet Infect Dis 7: 266-281.
2. Anonymous (1988) The third nation-wide study on adult T-cell leukemia/lymphoma (ATL) in Japan: characteristic patterns of HLA antigen and HTLV-I infection in ATL patients and their relatives. The T- and B-cell Malignancy Study Group. Int J Cancer 41: 505-512.
3. Takatsuki T, (1977) Adult T-cell leukemia in Japan. In: Seno S TS, Irino S, editors. pp. 73-77 editor. Topics in Hematology. Amsterdam: Excerpta Medica.
4. Feuer G, Green PL, (2005) Comparative biology of human T-cell lymphotropic virus type 1 (HTLV-1) and HTLV-2. Oncogene 24: 5996-6004.
5. Gessain A, Barin F, Vernant JC, Gout O, Maurs L, et al. (1985) Antibodies to human T-lymphotropic virus type-I in patients with tropical spastic paraparesis. Lancet 2: 407-410.
6. Osame M, Usuku K, Izumo S, Ijichi N, Amitani H, et al. (1986) HTLV-I associated myelopathy, a new clinical entity. Lancet 1: 1031-1032.
7. Mauclere P, Afonso PV, Meertens L, Plancoulaine S, Calattini S, et al. (2011) HTLV-2B strains, similar to those found in several Amerindian tribes, are endemic in central African Bakola Pygmies. J Infect Dis 203: 1316-1323.
8. Bartman MT, Kaidarova Z, Hirschkorn D, Sacher RA, Fridey J, et al. (2008) Long-term increases in lymphocytes and platelets in human T-lymphotropic virus type II infection. Blood 112: 3995-4002.
9. Jacobson S, Lehky T, Nishimura M, Robinson S, McFarlin DE, et al. (1993) Isolation of HTLV-II from a patient with chronic, progressive neurological disease clinically indistinguishable from HTLV-I-associated myelopathy/tropical spastic paraparesis. Ann Neurol 33: 392-396.
10. Araujo A, Hall WW, (2004) Human T-lymphotropic virus type II and neurological disease. Ann Neurol 56: 10-19.
11. Calattini S, Chevalier SA, Duprez R, Bassot S, Froment A, et al. (2005) Discovery of a new human T-cell lymphotropic virus (HTLV-3) in Central Africa. Retrovirology 2: 30.
12. Wolfe ND, Heneine W, Carr JK, Garcia AD, Shanmugam V, et al. (2005) Emergence of unique primate T-lymphotropic viruses among central African bushmeat hunters. Proc Natl Acad Sci U S A 102: 7994-7999.
13. Calattini S, Betsem E, Bassot S, Chevalier SA, Mahieux R, et al. (2009) New strain of human T lymphotropic virus (HTLV) type 3 in a Pygmy from Cameroon with peculiar HTLV serologic results. J Infect Dis 199: 561-564.
14. Zheng H, Wolfe ND, Sintasath DM, Tamoufe U, Lebreton M, et al. (2010) Emergence of a novel and highly divergent HTLV-3 in a primate hunter in Cameroon. Virology 401: 137-145.
15. Mahieux R, Gessain A, (2011) HTLV-3/STLV-3 and HTLV-4 viruses: discovery, epidemiology, serology and molecular aspects. Viruses 3: 1074-1090.
16. Calattini S, Chevalier SA, Duprez R, Afonso P, Froment A, et al. (2006) Human T-cell lymphotropic virus type 3: complete nucleotide sequence and characterization of the human tax3 protein. J Virol 80: 9876-9888.
17. Chevalier SA, Meertens L, Pise-Masison C, Calattini S, Park H, et al. (2006) The tax protein from the primate T-cell lymphotropic virus type 3 is expressed in vivo and is functionally related to HTLV-1 Tax rather than HTLV-2 Tax. Oncogene 25: 4470-4482.
18. Wycuff DR, Marriott SJ, (2005) The HTLV-I Tax oncoprotein: hyper-tasking at the molecular level. Front Biosci 10: 620-642.
19. Matsuoka M, Jeang KT, (2011) Human T-cell leukemia virus type 1 (HTLV-1) and leukemic transformation: viral infectivity, Tax, HBZ and therapy. Oncogene 30: 1379-1389.
20. Matsuoka M, Jeang KT, (2007) Human T-cell leukaemia virus type 1 (HTLV-1) infectivity and cellular transformation. Nat Rev Cancer 7: 270-280.
21. Douceron E, Kaidarova Z, Miyazato P, Matsuoka M, Murphy EL, et al. (2012) HTLV-2 APH-2 expression is correlated with proviral load but APH-2 does not promote lymphocytosis. J Infect Dis 205: 82-86.
22. Halin M, Douceron E, Clerc I, Journo C, Ko NL, et al. (2009) Human T-cell leukemia virus type 2 produces a spliced antisense transcript encoding a protein that lacks a classic bZIP domain but still inhibits Tax2-mediated transcription. Blood 114: 2427-2438.
23. Bellon M, Baydoun HH, Yao Y, Nicot C, (2010) HTLV-I Tax-dependent and-independent events associated with immortalization of human primary T lymphocytes. Blood 115: 2441-2448.
24. Yamaoka S, Tobe T, Hatanaka M, (1992) Tax protein of human T-cell leukemia virus type I is required for maintenance of the transformed phenotype. Oncogene 7: 433-437.
25. 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. Nat Med 12: 466-472.
26. Endo K, Hirata A, Iwai K, Sakurai M, Fukushi M, et al. (2002) Human T-cell leukemia virus type 2 (HTLV-2) Tax protein transforms a rat fibroblast cell line but less efficiently than HTLV-1 Tax. J Virol 76: 2648-2653.
27. Alefantis T, Barmak K, Harhaj EW, Grant C, Wigdahl B, (2003) Characterization of a nuclear export signal within the human T cell leukemia virus type I transactivator protein Tax. J Biol Chem 278: 21814-21822.
28. Chevalier SA, Meertens L, Calattini S, Gessain A, Kiemer L, et al. (2005) Presence of a functional but dispensable nuclear export signal in the HTLV-2 Tax protein. Retrovirology 2: 70.
29. Meertens L, Chevalier S, Weil R, Gessain A, Mahieux R, (2004) A 10-amino acid domain within human T-cell leukemia virus type 1 and type 2 tax protein sequences is responsible for their divergent subcellular distribution. J Biol Chem 279: 43307-43320.
30. Turci M, Romanelli MG, Lorenzi P, Righi P, Bertazzoni U, (2006) Localization of human T-cell lymphotropic virus type II Tax protein is dependent upon a nuclear localization determinant in the N-terminal region. Gene 365: 119-124.
31. Semmes OJ, Majone F, Cantemir C, Turchetto L, Hjelle B, et al. (1996) HTLV-I and HTLV-II Tax: differences in induction of micronuclei in cells and transcriptional activation of viral LTRs. Virology 217: 373-379.
32. Tripp A, Liu Y, Sieburg M, Montalbano J, Wrzesinski S, et al. (2003) Human T-cell leukemia virus type 1 tax oncoprotein suppression of multilineage hematopoiesis of CD34+ cells in vitro. J Virol 77: 12152-12164.
33. Mahieux R, Pise-Masison CA, Lambert PF, Nicot C, De Marchis L, et al. (2000) Differences in the ability of human T-cell lymphotropic virus type 1 (HTLV-1) and HTLV-2 tax to inhibit p53 function. J Virol 74: 6866-6874.
34. Rousset R, Fabre S, Desbois C, Bantignies F, Jalinot P, (1998) The C-terminus of the HTLV-1 Tax oncoprotein mediates interaction with the PDZ domain of cellular proteins. Oncogene 16: 643-654.
35. Shoji T, Higuchi M, Kondo R, Takahashi M, Oie M, et al. (2009) Identification of a novel motif responsible for the distinctive transforming activity of human T-cell leukemia virus (HTLV) type 1 Tax1 protein from HTLV-2 Tax2. Retrovirology 6: 83.
36. Hirata A, Higuchi M, Niinuma A, Ohashi M, Fukushi M, et al. (2004) PDZ domain-binding motif of human T-cell leukemia virus type 1 Tax oncoprotein augments the transforming activity in a rat fibroblast cell line. Virology 318: 327-336.
37. Xie L, Yamamoto B, Haoudi A, Semmes OJ, Green PL, (2006) PDZ binding motif of HTLV-1 Tax promotes virus-mediated T-cell proliferation in vitro and persistence in vivo. Blood 107: 1980-1988.
38. Higuchi M, Tsubata C, Kondo R, Yoshida S, Takahashi M, et al. (2007) Cooperation of NF-kappaB2/p100 activation and the PDZ domain binding motif signal in human T-cell leukemia virus type 1 (HTLV-1) Tax1 but not HTLV-2 Tax2 is crucial for interleukin-2-independent growth transformation of a T-cell line. J Virol 81: 11900-11907.
39. Nicot C, Mahieux R, Opavsky R, Cereseto A, Wolff L, et al. (2000) HTLV-I Tax transrepresses the human c-Myb promoter independently of its interaction with CBP or p300. Oncogene 19: 2155-2164.
40. Pise-Masison CA, Radonovich M, Dohoney K, Morris JC, O'Mahony D, et al. (2009) Gene expression profiling of ATL patients: compilation of disease-related genes and evidence for TCF4 involvement in BIRC5 gene expression and cell viability. Blood 113: 4016-4026.
41. Pise-Masison CA, Radonovich M, Mahieux R, Chatterjee P, Whiteford C, et al. (2002) Transcription profile of cells infected with human T-cell leukemia virus type I compared with activated lymphocytes. Cancer Res 62: 3562-3571.
42. Ruckes T, Saul D, Van Snick J, Hermine O, Grassmann R, (2001) Autocrine antiapoptotic stimulation of cultured adult T-cell leukemia cells by overexpression of the chemokine I-309. Blood 98: 1150-1159.
43. Sasaki H, Nishikata I, Shiraga T, Akamatsu E, Fukami T, et al. (2005) Overexpression of a cell adhesion molecule, TSLC1, as a possible molecular marker for acute-type adult T-cell leukemia. Blood 105: 1204-1213.
44. Iqbal J, Weisenburger DD, Greiner TC, Vose JM, McKeithan T, et al. (2010) Molecular signatures to improve diagnosis in peripheral T-cell lymphoma and prognostication in angioimmunoblastic T-cell lymphoma. Blood 115: 1026-1036.
45. Harhaj EW, Good L, Xiao G, Sun SC, (1999) Gene expression profiles in HTLV-I-immortalized T cells: deregulated expression of genes involved in apoptosis regulation. Oncogene 18: 1341-1349.
46. de La Fuente C, Deng L, Santiago F, Arce L, Wang L, et al. (2000) Gene expression array of HTLV type 1-infected T cells: Up-regulation of transcription factors and cell cycle genes. AIDS Res Hum Retroviruses 16: 1695-1700.
47. Oliere S, Hernandez E, Lezin A, Arguello M, Douville R, et al. (2010) HTLV-1 evades type I interferon antiviral signaling by inducing the suppressor of cytokine signaling 1 (SOCS1). PLoS Pathog 6: e1001177.
48. Ng PW, Iha H, Iwanaga Y, Bittner M, Chen Y, et al. (2001) Genome-wide expression changes induced by HTLV-1 Tax: evidence for MLK-3 mixed lineage kinase involvement in Tax-mediated NF-kappaB activation. Oncogene 20: 4484-4496.
49. Tattermusch S, Skinner JA, Chaussabel D, Banchereau J, Berry MP, et al. (2012) Systems biology approaches reveal a specific interferon-inducible signature in HTLV-1 associated myelopathy. PLoS Pathog 8: e1002480.
50. Baydoun HH, Pancewicz J, Bai X, Nicot C, (2010) HTLV-I p30 inhibits multiple S phase entry checkpoints, decreases cyclin E-CDK2 interactions and delays cell cycle progression. Mol Cancer 9: 302.
51. Nejmeddine M, Barnard AL, Tanaka Y, Taylor GP, Bangham CR, (2005) Human T-lymphotropic virus, type 1, tax protein triggers microtubule reorientation in the virological synapse. J Biol Chem 280: 29653-29660.
52. 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. Mol Cell Biol 25: 10391-10406.
53. Kfoury Y, Nasr R, Favre-Bonvin A, El-Sabban M, Renault N, et al. (2008) Ubiquitylated Tax targets and binds the IKK signalosome at the centrosome. Oncogene 27: 1665-1676.
54. Harhaj NS, Sun SC, Harhaj EW, (2007) 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 282: 4185-4192.
55. Bertazzoni U, Turci M, Avesani F, Di Gennaro G, Bidoia C, et al. (2011) Intracellular Localization and Cellular Factors Interaction of HTLV-1 and HTLV-2 Tax Proteins: Similarities and Functional Differences. Viruses 3: 541-560.
56. Niyogi K, Hildreth JE, (2001) Characterization of new syncytium-inhibiting monoclonal antibodies implicates lipid rafts in human T-cell leukemia virus type 1 syncytium formation. J Virol 75: 7351-7361.
57. Zane L, Sibon D, Legras C, Lachuer J, Wierinckx A, et al. (2010) Clonal expansion of HTLV-1 positive CD8+ cells relies on cIAP-2 but not on c-FLIP expression. Virology 407: 341-351.
58. Wu X, Zhang M, Sun SC, (2011) Mutual regulation between deubiquitinase CYLD and retroviral oncoprotein Tax. Cell Biosci 1: 27.
59. Harhaj EW, Dixit VM, (2011) Deubiquitinases in the regulation of NF-kappaB signaling. Cell Res 21: 22-39.
60. Aldana-Masangkay GI, Sakamoto KM, (2011) The role of HDAC6 in cancer. J Biomed Biotechnol 2011: 875824.
61. Afonso PV, Mekaouche M, Mortreux F, Toulza F, Moriceau A, et al. (2010) Highly active antiretroviral treatment against STLV-1 infection combining reverse transcriptase and HDAC inhibitors. Blood 116: 3802-3808.
62. Tanaka Y, Hayashi M, Takagi S, Yoshie O, (1996) Differential transactivation of the intercellular adhesion molecule 1 gene promoter by Tax1 and Tax2 of human T-cell leukemia viruses. J Virol 70: 8508-8517.
63. Kadiu I, Gendelman HE, (2011) Macrophage bridging conduit trafficking of HIV-1 through the endoplasmic reticulum and Golgi network. J Proteome Res 10: 3225-3238.
64. Van Prooyen N, Andresen V, Gold H, Bialuk I, Pise-Masison C, et al. (2010) Hijacking the T-cell communication network by the human T-cell leukemia/lymphoma virus type 1 (HTLV-1) p12 and p8 proteins. Mol Aspects Med 31: 333-343.
65. Kannian P, Green PL, (2011) Human T Lymphotropic Virus Type 1 (HTLV-1): Molecular Biology and Oncogenesis. Viruses 2: 2037-2077.
66. Turci M, Lodewick J, Righi P, Polania A, Romanelli MG, et al. (2009) HTLV-2B Tax oncoprotein is modified by ubiquitination and sumoylation and displays intracellular localization similar to its homologue HTLV-1 Tax. Virology.
67. Ross TM, Narayan M, Fang ZY, Minella AC, Green PL, (2000) Human T-cell leukemia virus type 2 tax mutants that selectively abrogate NFkappaB or CREB/ATF activation fail to transform primary human T cells. J Virol 74: 2655-2662.
68. Ross TM, Minella AC, Fang ZY, Pettiford SM, Green PL, (1997) Mutational analysis of human T-cell leukemia virus type 2 Tax. J Virol 71: 8912-8917.
69. Arlt A, Schafer H, (2011) Role of the immediate early response 3 (IER3) gene in cellular stress response, inflammation and tumorigenesis. Eur J Cell Biol 90: 545-552.
70. Yan P, Fu J, Qu Z, Li S, Tanaka T, et al. (2009) PDLIM2 suppresses human T-cell leukemia virus type I Tax-mediated tumorigenesis by targeting Tax into the nuclear matrix for proteasomal degradation. Blood 113: 4370-4380.
71. Boumber YA, Kondo Y, Chen X, Shen L, Gharibyan V, et al. (2007) RIL, a LIM gene on 5q31, is silenced by methylation in cancer and sensitizes cancer cells to apoptosis. Cancer Res 67: 1997-2005.
72. Journo C, Douceron E, Mahieux R, (2009) HTLV gene regulation: because size matters, transcription is not enough. Future Microbiol 4: 425-440.
73. Satou Y, Yasunaga J, Zhao T, Yoshida M, Miyazato P, et al. (2011) HTLV-1 bZIP factor induces T-cell lymphoma and systemic inflammation in vivo. PLoS Pathog 7: e1001274.
74. Larocque E, Halin M, Landry S, Marriott SJ, Switzer WM, et al. (2011) Human T-cell lymphotropic virus type 3 (HTLV-3)- and HTLV-4-derived antisense transcripts encode proteins with similar Tax-inhibiting functions but distinct subcellular localization. J Virol 85: 12673-12685.
75. Huang da W, Sherman BT, Tan Q, Kir J, Liu D, et al. (2007) DAVID Bioinformatics Resources: expanded annotation database and novel algorithms to better extract biology from large gene lists. Nucleic Acids Res 35: W169-175.
76. Huang da W, Sherman BT, Tan Q, Collins JR, Alvord WG, et al. (2007) The DAVID Gene Functional Classification Tool: a novel biological module-centric algorithm to functionally analyze large gene lists. Genome Biol 8: R183.
77. Huang da W, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
78. Sherman BT, Huang da W, Tan Q, Guo Y, Bour S, et al. (2007) DAVID Knowledgebase: a gene-centered database integrating heterogeneous gene annotation resources to facilitate high-throughput gene functional analysis. BMC Bioinformatics 8: 426.
79. Eisen MB, Spellman PT, Brown PO, Botstein D, (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95: 14863-14868.
80. Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T, (2011) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27: 431-432.
81. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, et al. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13: 2498-2504.
82. Cline MS, Smoot M, Cerami E, Kuchinsky A, Landys N, et al. (2007) Integration of biological networks and gene expression data using Cytoscape. Nat Protoc 2: 2366-2382.
83. von Mering C, Jensen LJ, Snel B, Hooper SD, Krupp M, et al. (2005) STRING: known and predicted protein-protein associations, integrated and transferred across organisms. Nucleic Acids Res 33: D433-437.
84. Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, et al. (2011) The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res 39: D561-568.
85. Bader GD, Hogue CW, (2003) An automated method for finding molecular complexes in large protein interaction networks. BMC Bioinformatics 4: 2.
86. Maere S, Heymans K, Kuiper M, (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21: 3448-3449.
87. Garcia O, Saveanu C, Cline M, Fromont-Racine M, Jacquier A, et al. (2007) GOlorize: a Cytoscape plug-in for network visualization with Gene Ontology-based layout and coloring. Bioinformatics 23: 394-396.