HTLV-1 evades type I interferon antiviral signaling by inducing the suppressor of cytokine signaling 1 (SOCS1)

PLoS Pathogens

Volumn 6, Issue 11, 2010, Pages

  Olière, Stéphanie ^a,b   Hernandez, Eduardo ^a   Lézin, Agnès ^c   Arguello, Meztli ^a   Douville, Renée ^a,b   Nguyen, Thi Lien Anh ^a,b   Olindo, Stéphane ^c   Panelatti, Gérard ^c   Kazanji, Mirdad ^d   Wilkinson, Peter ^e,f   Sékaly, Rafick Pierre ^e,f   Césaire, Raymond ^c   Hiscott, John ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITÉ DES ANTILLES ET DE LA GUYANE   (France)

^d CENTRE INTERNATIONAL DE RECHERCHES MÉDICALES DE FRANCEVILLE   (Gabon)

^e CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^f Vaccine and Gene Therapy Institute of Florida   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; INTERFERON; INTERFERON RECEPTOR; MESSENGER RNA; SMALL INTERFERING RNA; SUPPRESSOR OF CYTOKINE SIGNALING 1; VIRUS RNA; ANTIVIRUS AGENT; SOCS1 PROTEIN, HUMAN; SUPPRESSOR OF CYTOKINE SIGNALING; TUMOR MARKER;

ADULT; ARTICLE; BIOINFORMATICS; BLOOD SAMPLING; CD4+ T LYMPHOCYTE; CELL ISOLATION; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE CARRIER; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC TRANSFECTION; HTLV 1 ASSOCIATED MYELOPATHY; HUMAN; HUMAN CELL; HUMAN T CELL LEUKEMIA VIRUS 1; MESSENGER RNA SYNTHESIS; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; SIGNAL TRANSDUCTION; T CELL LEUKEMIA; TROPICAL SPASTIC PARAPARESIS; UBIQUITINATION; UPREGULATION; VIRUS REPLICATION; CASE CONTROL STUDY; CELL CULTURE; COMPARATIVE STUDY; DNA MICROARRAY; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; HUMAN T CELL LEUKEMIA VIRUS INFECTION; IMMUNOBLOTTING; IMMUNOPRECIPITATION; METABOLISM; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIROLOGY; VIRUS LOAD; WESTERN BLOTTING;

HUMAN T-LYMPHOTROPIC VIRUS 1;

ADULT; ANTIVIRAL AGENTS; BLOTTING, WESTERN; CASE-CONTROL STUDIES; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; GENE EXPRESSION PROFILING; HTLV-I INFECTIONS; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; INTERFERON TYPE I; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PARAPARESIS, TROPICAL SPASTIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; RNA, VIRAL; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TUMOR MARKERS, BIOLOGICAL; VIRAL LOAD;

EID: 79251516712     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001177     Document Type: Article

References (72)

1. Grant C, Barmak K, Alefantis T, Yao J, Jacobson S, et al. (2002) Human T cell leukemia virus type I and neurologic disease: events in bone marrow, peripheral blood, and central nervous system during normal immune surveillance and neuroinflammation. J Cell Physiol 190: 133-159.
2. Bangham CR, Meekings K, Toulza F, Nejmeddine M, Majorovits E, et al. (2009) The immune control of HTLV 1 infection: selection forces and dynamics. Front Biosci 14: 2889-2903.
3. Ohshima K (2007) Pathological features of diseases associated with human Tcell leukemia virus type I. Cancer Sci 98: 772-778.
4. Proietti FA, Carneiro-Proietti AB, Catalan-Soares BC, Murphy EL (2005) Global epidemiology of HTLV-I infection and associated diseases. Oncogene 24: 6058-6068.
5. Sabouri AH, Usuku K, Hayashi D, Izumo S, Ohara Y, et al. (2008) Impaired function of human T-lymphotropic virus type 1 (HTLV-1)-specific CD8+ T cells in HTLV-1-associated neurologic disease. Blood 112: 2411-2420.
6. Azran I, Schavinsky-Khrapunsky Y, Priel E, Huleihel M, Aboud M (2004) Implications of the evolution pattern of human T-cell leukemia retroviruses on their pathogenic virulence (Review). Int J Mol Med 14: 909-915.
7. Tsukasaki K, Hermine O, Bazarbachi A, Ratner L, Ramos JC, et al. (2009) Definition, prognostic factors, treatment, and response criteria of adult T-cell leukemia-lymphoma: a proposal from an international consensus meeting. J Clin Oncol 27: 453-459.
8. Grassmann R, Aboud M, Jeang KT (2005) Molecular mechanisms of cellular transformation by HTLV-1 Tax. Oncogene 24: 5976-5985.
9. Matsuoka M, Jeang KT (2007) Human T-cell leukaemia virus type 1 (HTLV-1) infectivity and cellular transformation. Nat Rev Cancer 7: 270-280.
10. Jeang KT, Giam CZ, Majone F, Aboud M (2004) Life, death, and tax: role of HTLV-I oncoprotein in genetic instability and cellular transformation. J Biol Chem 279: 31991-31994.
11. Boxus M, Twizere JC, Legros S, Dewulf JF, Kettmann R, et al. (2008) The HTLV-1 Tax interactome. Retrovirology 5: 76.
12. Peloponese JM, Jr., Kinjo T, Jeang KT (2007) Human T cell leukemia virus type 1 Tax and cellular transformation. Int J Hematol 86: 101-106.
13. Nagai M, Osame M (2003) Human T-cell lymphotropic virus type I and neurological diseases. J Neurovirol 9: 228-235.
14. Puccioni-Sohler M, Chimelli L, Mercon M, Goncalves RR, Pimenta G, et al. (2003) Pathological and virological assessment of acute HTLV-I-associated myelopathy complicated with encephalopathy and systemic inflammation. J Neurol Sci 207: 87-93.
15. Afonso PV, Ozden S, Prevost MC, Schmitt C, Seilhean D, et al. (2007) Human blood-brain barrier disruption by retroviral-infected lymphocytes: role of myosin light chain kinase in endothelial tight-junction disorganization. J Immunol 179: 2576-2583.
16. Nagai M, Brennan MB, Sakai JA, Mora CA, Jacobson S (2001) CD8(+) T cells are an in vivo reservoir for human T-cell lymphotropic virus type I. Blood 98: 1858-1861.
17. Yamano Y, Nagai M, Brennan M, Mora CA, Soldan SS, et al. (2002) Correlation of human T-cell lymphotropic virus type 1 (HTLV-1) mRNA withproviral DNA load, virus-specific CD8(+) T cells, and disease severity in HTLV-1-associated myelopathy (HAM/TSP). Blood 99: 88-94.
18. Lepoutre V, Jain P, Quann K, Wigdahl B, Khan ZK (2009) Role of resident CNS cell populations in HTLV-1-associated neuroinflammatory disease. Front Biosci 14: 1152-1168.
19. Grant C, Oh U, Yao K, Yamano Y, Jacobson S (2008) Dysregulation of TGFbeta signaling and regulatory and effector T-cell function in virus-induced neuroinflammatory disease. Blood 111: 5601-5609.
20. Vendrame D, Sourisseau M, Perrin V, Schwartz O, Mammano F (2009) Partial Inhibition of HIV Replication by Type-I Interferons: Impact of Cell-to-Cell Viral Transfer. J Virol.
21. Hong S, Cao J, Tu YT (2009) Evolution of HIV-1 in a patient population failing multiple-drug therapy. Microbiol Immunol 53: 535-539.
22. Kinpara S, Hasegawa A, Utsunomiya A, Nishitsuji H, Furukawa H, et al. (2009) Stromal cell-mediated suppression of human T-cell leukemia virus type 1 expression in vitro and in vivo by type I interferon. J Virol 83: 5101-5108.
23. Mahieux R, Hermine O (2005) In vivo and in vitro treatment of HTLV-1 and HTLV-2 infected cells with arsenic trioxide and interferon-alpha. Leuk Lymphoma 46: 347-355.
24. Hishizawa M, Imada K, Kitawaki T, Ueda M, Kadowaki N, et al. (2004) Depletion and impaired interferon-alpha-producing capacity of blood plasmacytoid dendritic cells in human T-cell leukaemia virus type I-infected individuals. Br J Haematol 125: 568-575.
25. Randall RE, Goodbourn S (2008) Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 89: 1-47.
26. Hiscott J (2007) Triggering the innate antiviral response through IRF-3 activation. J Biol Chem 282: 15325-15329.
27. Sharma S, tenOever BR, Grandvaux N, Zhou GP, Lin R, et al. (2003) Triggering the interferon antiviral response through an IKK-related pathway. Science 300: 1148-1151.
28. Fitzgerald KA, McWhirter SM, Faia KL, Rowe DC, Latz E, et al. (2003) IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol 4: 491-496.
29. Genin P, Lin R, Hiscott J, Civas A (2009) Differential regulation of human interferon A gene expression by interferon regulatory factors 3 and 7. Mol Cell Biol 29: 3435-3450.
30. Honda K, Takaoka A, Taniguchi T (2006) Type I interferon gene induction by the interferon regulatory factor family of transcription factors. Immunity 25: 349-360.
31. Levy DE, Marie I, Smith E, Prakash A (2002) Enhancement and diversification of IFN induction by IRF-7-mediated positive feedback. J Interferon Cytokine Res 22: 87-93.
32. O'Shea JJ, Gadina M, Schreiber RD (2002) Cytokine signaling in 2002: new surprises in the Jak/Stat pathway. Cell 109 Suppl: S121-131.
33. Yasukawa H, Sasaki A, Yoshimura A (2000) Negative regulation of cytokine signaling pathways. Annu Rev Immunol 18: 143-164.
34. Kubo M, Hanada T, Yoshimura A (2003) Suppressors of cytokine signaling and immunity. Nat Immunol 4: 1169-1176.
35. Fenner JE, Starr R, Cornish AL, Zhang JG, Metcalf D, et al. (2006) Suppressor of cytokine signaling 1 regulates the immune response to infection by a unique inhibition of type I interferon activity. Nat Immunol 7: 33-39.
36. Mansell A, Smith R, Doyle SL, Gray P, Fenner JE, et al. (2006) Suppressor of cytokine signaling 1 negatively regulates Toll-like receptor signaling by mediating Mal degradation. Nat Immunol 7: 148-155.
37. De Sepulveda P, Ilangumaran S, Rottapel R (2000) Suppressor of cytokine signaling-1 inhibits VAV function through protein degradation. J Biol Chem 275: 14005-14008.
38. Ryo A, Suizu F, Yoshida Y, Perrem K, Liou YC, et al. (2003) Regulation of NFkappaB signaling by Pin1-dependent prolyl isomerization and ubiquitinmediated proteolysis of p65/RelA. Mol Cell 12: 1413-1426.
39. Babon JJ, Sabo JK, Zhang JG, Nicola NA, Norton RS (2009) The SOCS box encodes a hierarchy of affinities for Cullin5: implications for ubiquitin ligase formation and cytokine signalling suppression. J Mol Biol 387: 162-174.
40. Piessevaux J, Lavens D, Peelman F, Tavernier J (2008) The many faces of the SOCS box. Cytokine Growth Factor Rev 19: 371-381.
41. Dalpke A, Heeg K, Bartz H, Baetz A (2008) Regulation of innate immunity by suppressor of cytokine signaling (SOCS) proteins. Immunobiology 213: 225-235.
42. Mbow ML, Sarisky RT (2004) What is disrupting IFN-alpha's antiviral activity? Trends Biotechnol 22: 395-399.
43. Pothlichet J, Chignard M, Si-Tahar M (2008) Cutting edge: innate immune response triggered by influenza A virus is negatively regulated by SOCS1 and SOCS3 through a RIG-I/IFNAR1-dependent pathway. J Immunol 180: 2034-2038.
44. Nishiura Y, Nakamura T, Fukushima N, Moriuchi R, Katamine S, et al. (2004) Increased mRNA expression of Th1-cytokine signaling molecules in patients with HTLV-I-associated myelopathy/tropical spastic paraparesis. Tohoku J Exp Med 204: 289-298.
45. Hiscott J, Nguyen TL, Arguello M, Nakhaei P, Paz S (2006) Manipulation of the nuclear factor-kappaB pathway and the innate immune response by viruses. Oncogene 25: 6844-6867.
46. Nagai M, Yamano Y, Brennan MB, Mora CA, Jacobson S (2001) Increased HTLV-I proviral load and preferential expansion of HTLV-I Tax-specific CD8+ T cells in cerebrospinal fluid from patients with HAM/TSP. Ann Neurol 50: 807-812.
47. 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.
48. Baba M, Okamoto M, Hamasaki T, Horai S, Wang X, et al. (2008) Highly enhanced expression of CD70 on human T-lymphotropic virus type 1-carrying T-cell lines and adult T-cell leukemia cells. J Virol 82: 3843-3852.
49. Wu K, Bottazzi ME, de la Fuente C, Deng L, Gitlin SD, et al. (2004) Protein profile of tax-associated complexes. J Biol Chem 279: 495-508.
50. Solis M, Wilkinson P, Romieu R, Hernandez E, Wainberg MA, et al. (2006) Gene expression profiling of the host response to HIV-1 B, C, or A/E infection in monocyte-derived dendritic cells. Virology 352: 86-99.
51. Oh U, Jacobson S (2008) Treatment of HTLV-I-associated myelopathy/tropical spastic paraparesis: toward rational targeted therapy. Neurol Clin 26: 781-797, ix-x.
52. Feng X, Ratner L (2008) Human T-cell leukemia virus type 1 blunts signaling by interferon alpha. Virology 374: 210-216.
53. Zhang J, Yamada O, Kawagishi K, Araki H, Yamaoka S, et al. (2008) Human T-cell leukemia virus type 1 Tax modulates interferon-alpha signal transduction through competitive usage of the coactivator CBP/p300. Virology 379: 306-313.
54. Kile BT, Alexander WS (2001) The suppressors of cytokine signalling (SOCS). Cell Mol Life Sci 58: 1627-1635.
55. Mahller YY, Sakthivel B, Baird WH, Aronow BJ, Hsu YH, et al. (2008) Molecular analysis of human cancer cells infected by an oncolytic HSV-1 reveals multiple upregulated cellular genes and a role for SOCS1 in virus replication. Cancer Gene Ther 15: 733-741.
56. Kamio M, Yoshida T, Ogata H, Douchi T, Nagata Y, et al. (2004) SOCS1 [corrected] inhibits HPV-E7-mediated transformation by inducing degradation of E7 protein. Oncogene 23: 3107-3115.
57. Ryo A, Tsurutani N, Ohba K, Kimura R, Komano J, et al. (2008) SOCS1 is an inducible host factor during HIV-1 infection and regulates the intracellular trafficking and stability of HIV-1 Gag. Proc Natl Acad Sci U S A 105: 294-299.
58. Kamizono S, Hanada T, Yasukawa H, Minoguchi S, Kato R, et al. (2001) The SOCS box of SOCS-1 accelerates ubiquitin-dependent proteolysis of TELJAK2. J Biol Chem 276: 12530-12538.
59. Ali S, Nouhi Z, Chughtai N, Ali S (2003) SHP-2 regulates SOCS-1-mediated Janus kinase-2 ubiquitination/degradation downstream of the prolactin receptor. J Biol Chem 278: 52021-52031.
60. Weber F, Kochs G, Haller O (2004) Inverse interference: how viruses fight the interferon system. Viral Immunol 17: 498-515.
61. Saira K, Zhou Y, Jones C (2007) The infected cell protein 0 encoded by bovine herpesvirus 1 (bICP0) induces degradation of interferon response factor 3 and, consequently, inhibits beta interferon promoter activity. J Virol 81: 3077-3086.
62. Alexander WS (2002) Suppressors of cytokine signalling (SOCS) in the immune system. Nat Rev Immunol 2: 410-416.
63. Palmer DC, Restifo NP (2009) Suppressors of cytokine signaling (SOCS) in T cell differentiation, maturation, and function. Trends Immunol 30: 592-602.
64. Baker BJ, Akhtar LN, Benveniste EN (2009) SOCS1 and SOCS3 in the control of CNS immunity. Trends Immunol 30: 392-400.
65. Kobayashi T, Yoshimura A (2005) Keeping DCs awake by putting SOCS1 to sleep. Trends Immunol 26: 177-179.
66. Osame M, Janssen R, Kubota H, Nishitani H, Igata A, et al. (1990) Nationwide survey of HTLV-I-associated myelopathy in Japan: association with blood transfusion. Ann Neurol 28: 50-56.
67. Hinuma Y, Nagata K, Hanaoka M, Nakai M, Matsumoto T, et al. (1981) Adult T-cell leukemia: antigen in an ATL cell line and detection of antibodies to the antigen in human sera. Proc Natl Acad Sci U S A 78: 6476-6480.
68. Kobayashi N, Yamamoto N, Koyanagi Y, Schneider J, Hunsmann G, et al. (1984) Translation of HTLV (human T-cell leukemia virus) RNA in a nucleasetreated rabbit reticulocyte system. EMBO J 3: 321-325.
69. Adaui V, Verdonck K, Best I, Gonzalez E, Tipismana M, et al. (2006) SYBR Green-based quantitation of human T-lymphotropic virus type 1 proviral load in Peruvian patients with neurological disease and asymptomatic carriers: influence of clinical status, sex, and familial relatedness. J Neurovirol 12: 456-465.
70. Iwamura T, Yoneyama M, Yamaguchi K, Suhara W, Mori W, et al. (2001) Induction of IRF-3/-7 kinase and NF-kappaB in response to double-stranded RNA and virus infection: common and unique pathways. Genes Cells 6: 375-388.
71. Huang FJ, Steeg PS, Price JE, Chiu WT, Chou PC, et al. (2008) Molecular basis for the critical role of suppressor of cytokine signaling-1 in melanoma brain metastasis. Cancer Res 68: 9634-9642.
72. Zitzmann K, Brand S, De Toni EN, Baehs S, Goke B, et al. (2007) SOCS1 silencing enhances antitumor activity of type I IFNs by regulating apoptosis in neuroendocrine tumor cells. Cancer Res 67: 5025-5032.