Human T-cell leukemia/lymphoma virus type 1 p30, but not p12/p8, counteracts toll-like receptor 3 (TLR3) and TLR4 signaling in human monocytes and dendritic cells

Journal of Virology

Volumn 88, Issue 1, 2014, Pages 393-402

  Fenizia, Claudio ^a   Fiocchi, Martina ^b   Jones, Kathryn ^c   Parks, Robyn Washington ^a   Ceribelli, Michele ^a   Chevalier, Sebastien A ^a   Edwards, Dustin ^a   Ruscetti, Francis ^c   Pise Masison, Cynthia A ^a   Franchini, Genoveffa ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b LITA VIALBA   (Italy)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA1 INTERFERON; BETA INTERFERON; IMIQUIMOD; INTERFERON; LIPOPOLYSACCHARIDE; PROTEIN P30; PROTEIN P8; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8;

ARTICLE; B LYMPHOCYTE; CELL TYPE; CHROMATIN IMMUNOPRECIPITATION; DENDRITIC CELL; EX VIVO STUDY; GENE EXPRESSION; HUMAN T CELL LEUKEMIA VIRUS; IN VITRO STUDY; IN VIVO STUDY; MONOCYTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; VIRUS DETECTION; VIRUS EXPRESSION; VIRUS INFECTIVITY;

BASE SEQUENCE; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; DENDRITIC CELLS; DNA PRIMERS; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMANS; MONOCYTES; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 4; VIRAL PROTEINS;

EID: 84890873535     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01788-13     Document Type: Article

References (55)

1. Poiesz BJ, Ruscetti FW, Gazdar AF, Bunn PA, Minna JD, Gallo RC. 1980. Detection and isolation of type C retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous T-cell lymphoma. Proc. Natl. Acad. Sci. U. S. A. 77:7415-7419. http://dx.doi.org/10.1073/pnas.77 .12.7415.
2. Poiesz BJ, Ruscetti FW, Reitz MS, Kalyanaraman VS, Gallo RC. 1981. Isolation of a new typeCretrovirus (HTLV) in primary uncultured cells of a patient with Sezary T-cell leukaemia. Nature 294:268-271. http://dx.doi .org/10.1038/294268a0.
3. Edwards D, Fenizia C, Gold H, de Castro-Amarante MF, Buchmann C, Pise-Masison CA, Franchini G. 2011. Orf-I and orf-II-encoded proteins in HTLV-1 infection and persistence. Viruses 3:861-885. http://dx.doi .org/10.3390/v3060861.
4. Hinuma Y, Nagata K, Hanaoka M, Nakai M, Matsumoto T, Kinoshita KI, Shirakawa S, Miyoshi I. 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. http://dx.doi.org/10.1073 /pnas.78.10.6476.
5. Kaplan JE, Osame M, Kubota H, Igata A, Nishitani H, Maeda Y, Khabbaz RF, Janssen RS. 1990. The risk of development of HTLV-Iassociated myelopathy/tropical spastic paraparesis among persons infected with HTLV-I. J. Acquir. Immune. Defic. Syndr. 3:1096-1101.
6. Kondo T, Kono H, Nonaka H, Miyamoto N, Yoshida R, Bando F, Inoue H, Miyoshi I, Hinuma Y, Hanaoka M. 1987. Risk of adult T-cell leukaemia/ lymphoma in HTLV-I carriers. Lancet ii:159.
7. Maloney EM, Cleghorn FR, Morgan OS, Rodgers-Johnson P, Cranston B, Jack N, Blattner WA, Bartholomew C, Manns A. 1998. Incidence of HTLVI- associated myelopathy/tropical spastic paraparesis (HAM/TSP) in Jamaica and Trinidad. J. Acquir. Immune. Defic. Syndr. Hum. Retrovirol. 17:167- 170. http://dx.doi.org/10.1097/00042560-199802010-00011.
8. Murphy EL, Hanchard B, Figueroa JP, Gibbs WN, Lofters WS, Campbell M, Goedert JJ, Blattner WA. 1989. Modeling the risk of adult T-cell leukemia/lymphoma in persons infected with human T-lymphotropic virus type I. Int. J. Cancer 43:250-253. http://dx.doi.org/10.1002/ijc .2910430214.
9. Seiki M, Hattori S, Kirayama Y, Yoshida M. 1983. Human T-cell leukemia/ lymphotropic virus: complete nucleotide sequence of the provirus genome integrated in leukemia cell DNA. Proc. Natl. Acad. Sci. U. S. A. 80:3618-3622. http://dx.doi.org/10.1073/pnas.80.12.3618.
10. Yamaguchi K, Watanabe T. 2002. Human T lymphotropic virus type-I and adult T-cell leukemia in Japan. Int. J. Hematol. 76(Suppl 2):240-245. http://dx.doi.org/10.1007/BF03165123.
11. de Revel T, Mabondzo A, Gras G, Delord B, Roques P, Boussin F, Neveux Y, Bahuau M, Fleury HJ, Dormont D. 1993. In vitro infection of human macrophages with human T-cell leukemia virus type 1. Blood 81:1598-1606.
12. Jones KS, Petrow-Sadowski C, Huang YK, Bertolette DC, Ruscetti FW. 2008. Cell-free HTLV-1 infects dendritic cells leading to transmission and transformation of CD4(α) T cells. Nat. Med. 14:429-436. http://dx.doi .org/10.1038/nm1745.
13. Koralnik I, Lemp JF, Jr, Gallo RC, Franchini G. 1992. In vitro infection of human macrophages by human T-cell leukemia/lymphotropic virus type I (HTLV-I). AIDS Res. Hum. Retrovir. 8:1845-1849. http://dx.doi .org/10.1089/aid.1992.8.1845.
14. Koyanagi Y, Itoyama Y, Nakamura N, Takamatsu K, Kira J, Iwamasa T, Goto I, Yamamoto N. 1993. In vivo infection of human T-cell leukemia virus type I in non-T cells. Virology 196:25-33. http://dx.doi.org/10.1006 /viro.1993.1451.
15. Macatonia SE, Cruickshank JK, Rudge P, Knight SC. 1992. Dendritic cells from patients with tropical spastic paraparesis are infected with HTLV-1 and stimulate autologous lymphocyte proliferation. AIDS Res. Hum. Retrovir. 8:1699-1706. http://dx.doi.org/10.1089/aid.1992.8.1699.
16. Hishizawa M, Imada K, Kitawaki T, Ueda M, Kadowaki N, Uchiyama T. 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. http://dx.doi.org/10 .1111/j.1365-2141.2004.04956.x.
17. Makino M, Wakamatsu S, Shimokubo S, Arima N, Baba M. 2000. Production of functionally deficient dendritic cells from HTLV-I-infected monocytes: implications for the dendritic cell defect in adult T cell leukemia. Virology 274:140-148. http://dx.doi.org/10.1006/viro.2000.0445.
18. Nascimento CR, Lima MA, de Andrada Serpa MJ, Espindola O, Leite AC, Echevarria-Lima J. 2011. Monocytes from HTLV-1-infected patients are unable to fully mature into dendritic cells. Blood 117:489-499. http: //dx.doi.org/10.1182/blood-2010-03-272690.
19. Valeri VW, Hryniewicz A, Andresen V, Jones K, Fenizia C, Bialuk I, Chung HK, Fukumoto R, Parks RW, Ferrari MG, Nicot C, Cecchinato V, Ruscetti F, Franchini G. 2010. Requirement of the human T-cell leukemia virus p12 and p30 products for infectivity of human dendritic cells and macaques but not rabbits. Blood 116:3809-3817. http://dx.doi .org/10.1182/blood-2010-05-284141.
20. Datta A, Sinha-Datta U, Dhillon NK, Buch S, Nicot C. 2006. The HTLV-I p30 interferes with TLR4 signaling and modulates the release of pro- and anti-inflammatory cytokines from human macrophages. J. Biol. Chem. 281:23414-23424. http://dx.doi.org/10.1074/jbc.M600684200.
21. Zhang W, Nisbet JW, Bartoe JT, Ding W, Lairmore MD. 2000. Human T-lymphotropic virus type 1 p30(II) functions as a transcription factor and differentially modulates CREB-responsive promoters. J. Virol. 74: 11270-11277. http://dx.doi.org/10.1128/JVI.74.23.11270-11277.2000.
22. Kanno Y, Levi BZ, Tamura T, Ozato K. 2005. Immune cell-specific amplification of interferon signaling by the IRF-4/8-PU. 1 complex. J. Interferon Cytokine Res. 25:770-779. http://dx.doi.org/10.1089/jir.2005 .25.770.
23. Marecki S, Fenton MJ. 2002. The role of IRF-4 in transcriptional regulation. J. Interferon Cytokine Res. 22:121-133. http://dx.doi.org/10.1089 /107999002753452737.
24. Lehtonen A, Ahlfors H, Veckman V, Miettinen M, Lahesmaa R, Julkunen I. 2007. Gene expression profiling during differentiation of human monocytes to macrophages or dendritic cells. J. Leukoc. Biol. 82: 710-720. http://dx.doi.org/10.1189/jlb.0307194.
25. Koralnik IJ, Fullen J, Franchini G. 1993. The p12I, p13II, and p30II proteins encoded by human T-cell leukemia/lymphotropic virus type I open reading frames I and II are localized in three different cellular compartments. J. Virol. 67:2360-2366.
26. Li S, Labrecque S, Gauzzi MC, Cuddihy AR, Wong AH, Pellegrini S, Matlashewski GJ, Koromilas AE. 1999. The human papilloma virus (HPV)-18 E6 oncoprotein physically associates with Tyk2 and impairs Jak-STAT activation by interferon-alpha. Oncogene 18:5727-5737. http: //dx.doi.org/10.1038/sj.onc.1202960.
27. Schmidt M, Bies J, Tamura T, Ozato K, Wolff L. 2004. The interferon regulatory factor ICSBP/IRF-8 in combination with PU.1 up-regulates expression of tumor suppressor p15(Ink4b) in murine myeloid cells. Blood 103:4142-4149. http://dx.doi.org/10.1182/blood-2003-01-0285.
28. Schroder K, Lichtinger M, Irvine KM, Brion K, Trieu A, Ross IL, Ravasi T, Stacey KJ, Rehli M, Hume DA, Sweet MJ. 2007. PU.1 and ICSBP control constitutive and IFN-gamma-regulated Tlr9 gene expression in mouse macrophages. J. Leukoc. Biol. 81:1577-1590. http://dx.doi.org/10 .1189/jlb.0107036.
29. Hengel H, Koszinowski UH, Conzelmann KK. 2005. Viruses know it all: new insights into IFN networks. Trends Immunol. 26:396-401. http://dx .doi.org/10.1016/j.it.2005.05.004.
30. Hughes R, Towers G, Noursadeghi M. 2012. Innate immune interferon responses to human immunodeficiency virus-1 infection. Rev. Med. Virol. 22:257-266. http://dx.doi.org/10.1002/rmv.1708.
31. WangBX, Fish EN. 2012. The yin and yang of viruses and interferons. Trends Immunol. 33:190-197. http://dx.doi.org/10.1016/j.it.2012.01.004.
32. Severa M, Fitzgerald KA. 2007. TLR-mediated activation of type I IFN during antiviral immune responses: fighting the battle to win the war. Curr. Top. Microbiol. Immunol. 316:167-192. http://dx.doi.org/10.1007 /978-3-540-71329-6_9.
33. Van Prooyen N, Gold H, Andresen V, Schwartz O, Jones K, Ruscetti F, Lockett S, Gudla P, Venzon D, Franchini G. 2010. Human T-cell leukemia virus type 1 p8 protein increases cellular conduits and virus transmission. Proc. Natl. Acad. Sci. U. S. A. 107:20738-20743. http://dx.doi .org/10.1073/pnas.1009635107.
34. Kirk PD, Witkover A, Courtney A, Lewin AM, Wait R, Stumpf MP, Richardson S, Taylor GP, Bangham CR. 2011. Plasma proteome analysis in HTLV-1-associated myelopathy/tropical spastic paraparesis. Retrovirology 8:81. http://dx.doi.org/10.1186/1742-4690-8-81.
35. Matsuzaki T, Nakagawa M, Nagai M, Usuku K, Higuchi I, Arimura K, Kubota H, Izumo S, Akiba S, Osame M. 2001. HTLV-I proviral load correlates with progression of motor disability in HAM/TSP: analysis of 239 HAM/TSP patients including 64 patients followed up for 10 years. J. Neurovirol. 7:228-234. http://dx.doi.org/10.1080/13550280152403272.
36. Montanheiro PA, Oliveira AC, Posada-Vergara MP, Milagres AC, Tauil C, Marchiori PE, Duarte AJ, Casseb J. 2005. Human T-cell lymphotropic virus type I (HTLV-I) proviral DNA viral load among asymptomatic patients and patients with HTLV-I-associated myelopathy/tropical spastic paraparesis. Braz. J. Med. Biol. Res. 38:1643-1647. http://dx.doi.org/10 .1590/S0100-879X2005001100011.
37. Yamano Y, Nagai M, Brennan M, Mora CA, Soldan SS, Tomaru U, Takenouchi N, Izumo S, Osame M, Jacobson S. 2002. Correlation of human T-cell lymphotropic virus type 1 (HTLV-1) mRNA with proviral DNA load, virus-specific CD8(α) T cells, and disease severity in HTLV- 1-associated myelopathy (HAM/TSP). Blood 99:88-94. http://dx.doi.org /10.1182/blood.V99.1.88.
38. Wissing S, Galloway NL, Greene WC. 2010. HIV-1 Vif versus the APOBEC3 cytidine deaminases: an intracellular duel between pathogen and host restriction factors. Mol. Aspects Med. 31:383-397. http://dx.doi .org/10.1016/j.mam.2010.06.001.
39. Baydoun H, Duc-Dodon M, Lebrun S, Gazzolo L, Bex F. 2007. Regulation of the human T-cell leukemia virus gene expression depends on the localization of regulatory proteins Tax, Rex and p30II in specific nuclear subdomains. Gene 386:191-201. http://dx.doi.org/10.1016/j.gene.2006 .09.008.
40. Ghorbel S, Sinha-Datta U, Dundr M, Brown M, Franchini G, Nicot C. 2006. Human T-cell leukemia virus type I p30 nuclear/nucleolar retention is mediated through interactions with RNA and a constituent of the 60 S ribosomal subunit. J. Biol. Chem. 281:37150-37158. http://dx.doi.org/10 .1074/jbc.M603981200.
41. Weber F, Kochs G, Haller O. 2004. Inverse interference: how viruses fight the interferon system. Viral Immunol. 17:498-515. http://dx.doi.org/10 .1089/vim.2004.17.498.
42. Journo C, Mahieux R. 2011. HTLV-1 and innate immunity. Viruses 3:1374-1394. http://dx.doi.org/10.3390/v3081374.
43. Wang X, Li M, Zheng H, Muster T, Palese P, Beg AA, Garcia-Sastre A. 2000. InfluenzaAvirus NS1 protein prevents activation of NF-kappaB and induction of alpha/beta interferon. J. Virol. 74:11566-11573. http://dx .doi.org/10.1128/JVI.74.24.11566-11573.2000.
44. Komatsu T, Takeuchi K, Yokoo J, Gotoh B. 2004. C and V proteins of Sendai virus target signaling pathways leading to IRF-3 activation for the negative regulation of interferon-beta production. Virology 325:137-148. http://dx.doi.org/10.1016/j.virol.2004.04.025.
45. Naniche D, Yeh A, Eto D, Manchester M, Friedman RM, Oldstone MB. 2000. Evasion of host defenses by measles virus: wild-type measles virus infection interferes with induction of alpha/beta interferon production. J. Virol. 74:7478-7484. http://dx.doi.org/10.1128/JVI.74.16.7478-7484.2000.
46. Basler CF, Mikulasova A, Martinez-Sobrido L, Paragas J, Muhlberger E, Bray M, Klenk HD, Palese P, Garcia-Sastre A. 2003. The Ebola virus VP35 protein inhibits activation of interferon regulatory factor 3. J. Virol. 77:7945-7956. http://dx.doi.org/10.1128/JVI.77.14.7945-7956.2003.
47. Foy E, Li K, Wang C, Sumpter R, Jr, Ikeda M, Lemon SM, Gale M, Jr. 2003. Regulation of interferon regulatory factor-3 by the hepatitis C virus serine protease. Science 300:1145-1148. http://dx.doi.org/10.1126 /science.1082604.
48. Roy S, Katze MG, Parkin NT, Edery I, Hovanessian AG, Sonenberg N. 1990. Control of the interferon-induced 68-kilodalton protein kinase by the HIV-1 tat gene product. Science 247:1216-1219. http://dx.doi.org/10 .1126/science.2180064.
49. Sheehy AM, Gaddis NC, Choi JD, Malim MH. 2002. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418:646-650. http://dx.doi.org/10.1038/nature00939.
50. Fenner JE, Starr R, Cornish AL, Zhang JG, Metcalf D, Schreiber RD, Sheehan K, Hilton DJ, Alexander WS, Hertzog PJ. 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. http://dx.doi.org/10.1038/ni1287.
51. Oliere S, Hernandez E, Lezin A, Arguello M, Douville R, Nguyen TL, Olindo S, Panelatti G, Kazanji M, Wilkinson P, Sekaly RP, Cesaire R, Hiscott J. 2010. HTLV-1 evades type I interferon antiviral signaling by inducing the suppressor of cytokine signaling 1 (SOCS1). PLoS Pathog. 6:e1001177. http://dx.doi.org/10.1371/journal.ppat.1001177.
52. Smith D, Buckle GJ, Hafler DA, Frank DA, Hollsberg P. 1999. HTLVI- infected T cells evade the antiproliferative action of IFN-beta. Virology 257:314-321. http://dx.doi.org/10.1006/viro.1999.9679.
53. Feng X, Ratner L. 2008. Human T-cell leukemia virus type 1 blunts signaling by interferon alpha. Virology 374:210-216. http://dx.doi.org/10 .1016/j.virol.2007.12.036.
54. Zhang J, Yamada O, Kawagishi K, Araki H, Yamaoka S, Hattori T, Shimotohno K. 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. http://dx.doi.org/10.1016/j .virol.2008.06.035.
55. Kinpara S, Kijiyama M, Takamori A, Hasegawa A, Sasada A, Masuda T, Tanaka Y, Utsunomiya A, Kannagi M. 2013. Interferon-alpha (IFNalpha) suppresses HTLV-1 gene expression and cell cycling, while IFNalpha combined with zidovudine induces p53 signaling and apoptosis in HTLV-1-infected cells. Retrovirology 10:52. http://dx.doi.org/10.1186 /1742-4690-10-52.