HTLV-1 bZIP Factor Impairs Anti-viral Immunity by Inducing Co-inhibitory Molecule, T Cell Immunoglobulin and ITIM Domain (TIGIT)

PLoS Pathogens

Volumn 12, Issue 1, 2016, Pages

  Yasuma, Keiko ^a   Yasunaga, Jun Ichirou ^a   Takemoto, Keiko ^a   Sugata, Kenji ^a   Mitobe, Yuichi ^a   Takenouchi, Norihiro ^b   Nakagawa, Masanori ^c   Suzuki, Yutaka ^d   Matsuoka, Masao ^a  

^a KYOTO UNIVERSITY   (Japan)

^b KANSAI MEDICAL UNIVERSITY   (Japan)

^c KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; CD226 PROTEIN; CHEMOKINE RECEPTOR CCR4; FIBRINOGEN LIKE 2 PROTEIN; INTERLEUKIN 10; INTERLEUKIN 4; PROTEIN; T CELL IMMUNOGLOBULIN AND ITIM DOMAIN; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; VIRUS PROTEIN; IMMUNOGLOBULIN RECEPTOR; T CELL IG AND ITIM DOMAIN PROTEIN, MOUSE; TIGIT PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; EPIGENETICS; FLOW CYTOMETRY; GENE SILENCING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN T CELL LEUKEMIA VIRUS INFECTION; HUMAN T-LYMPHOTROPIC VIRUS 1; IMMUNE RESPONSE; LUCIFERASE ASSAY; MOUSE; NONHUMAN; PROTEIN ACETYLATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA SEQUENCE; TROPICAL SPASTIC PARAPARESIS; VIRAL GENE DELIVERY SYSTEM; VIRUS IMMUNITY; ANIMAL; C57BL MOUSE; DNA MICROARRAY; GENE EXPRESSION REGULATION; IMMUNE EVASION; IMMUNOLOGY; T CELL LEUKEMIA; TRANSGENIC MOUSE; VIROLOGY;

ANIMALS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CD4-POSITIVE T-LYMPHOCYTES; CHROMATIN IMMUNOPRECIPITATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, VIRAL; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMANS; IMMUNE EVASION; LEUKEMIA-LYMPHOMA, ADULT T-CELL; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, IMMUNOLOGIC;

EID: 84956781376     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005372     Document Type: Article

References (57)

1. Mesri EA, Feitelson MA, Munger K, Human viral oncogenesis: a cancer hallmarks analysis. Cell Host Microbe. 2014;15(3):266–82. doi: 10.1016/j.chom.2014.02.011 24629334; PubMed Central PMCID: PMC3992243.
2. Matsuoka M, Jeang KT, Human T-cell leukaemia virus type 1 (HTLV-1) infectivity and cellular transformation. Nature reviews. 2007;7(4):270–80. 17384582.
3. Bangham CR, Cook LB, Melamed A, HTLV-1 clonality in adult T-cell leukaemia and non-malignant HTLV-1 infection. Seminars in cancer biology. 2014;26:89–98. doi: 10.1016/j.semcancer.2013.11.003 24316494; PubMed Central PMCID: PMC4062949.
4. Matsuoka M, Green PL, The HBZ gene, a key player in HTLV-1 pathogenesis. Retrovirology. 2009;6:71. Epub 2009/08/05. doi: 1742-4690-6-71 [pii] doi: 10.1186/1742-4690-6-71 19650892; PubMed Central PMCID: PMC2731725.
5. Satou Y, Yasunaga J, Zhao T, Yoshida M, Miyazato P, Takai K, et al. HTLV-1 bZIP Factor Induces T-Cell Lymphoma and Systemic Inflammation In Vivo. PLoS Pathog. 2011;7(2):e1001274. Epub 2011/02/25. doi: 10.1371/journal.ppat.1001274 21347344.
6. Philip S, Zahoor MA, Zhi H, Ho YK, Giam CZ, Regulation of human T-lymphotropic virus type I latency and reactivation by HBZ and Rex. PLoS Pathog. 2014;10(4):e1004040. doi: 10.1371/journal.ppat.1004040 24699669; PubMed Central PMCID: PMC3974842.
7. Yamano Y, Araya N, Sato T, Utsunomiya A, Azakami K, Hasegawa D, et al. Abnormally high levels of virus-infected IFN-gamma+ CCR4+ CD4+ CD25+ T cells in a retrovirus-associated neuroinflammatory disorder. PLoS One. 2009;4(8):e6517. doi: 10.1371/journal.pone.0006517 19654865; PubMed Central PMCID: PMC2715877.
8. Nakahata S, Saito Y, Marutsuka K, Hidaka T, Maeda K, Hatakeyama K, et al. Clinical significance of CADM1/TSLC1/IgSF4 expression in adult T-cell leukemia/lymphoma. Leukemia. 2012;26(6):1238–46. doi: 10.1038/leu.2011.379 22289924.
9. Satou Y, Utsunomiya A, Tanabe J, Nakagawa M, Nosaka K, Matsuoka M, HTLV-1 modulates the frequency and phenotype of FoxP3+CD4+ T cells in virus-infected individuals. Retrovirology. 2012;9(1):46. Epub 2012/06/01. doi: 10.1186/1742-4690-9-46 22647666.
10. Zhao T, Satou Y, Sugata K, Miyazato P, Green PL, Imamura T, et al. HTLV-1 bZIP factor enhances TGF-{beta} signaling through p300 coactivator. Blood. 2011;118(7):1865–76. Epub 2011/06/28. doi: 10.1182/blood-2010-12-326199 21705495.
11. Schneider H, Downey J, Smith A, Zinselmeyer BH, Rush C, Brewer JM, et al. Reversal of the TCR stop signal by CTLA-4. Science. 2006;313(5795):1972–5. doi: 10.1126/science.1131078 16931720.
12. Chen L, Flies DB, Molecular mechanisms of T cell co-stimulation and co-inhibition. Nat Rev Immunol. 2013;13(4):227–42. doi: 10.1038/nri3405 23470321; PubMed Central PMCID: PMC3786574.
13. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 2012;366(26):2443–54. doi: 10.1056/NEJMoa1200690 22658127; PubMed Central PMCID: PMC3544539.
14. Ansell SM, Lesokhin AM, Borrello I, Halwani A, Scott EC, Gutierrez M, et al. PD-1 blockade with nivolumab in relapsed or refractory Hodgkin's lymphoma. N Engl J Med. 2015;372(4):311–9. doi: 10.1056/NEJMoa1411087 25482239; PubMed Central PMCID: PMC4348009.
15. Topalian SL, Drake CG, Pardoll DM, Immune Checkpoint Blockade: A Common Denominator Approach to Cancer Therapy. Cancer Cell. 2015;27(4):450–61. doi: 10.1016/j.ccell.2015.03.001 25858804; PubMed Central PMCID: PMC4400238.
16. Yu X, Harden K, Gonzalez LC, Francesco M, Chiang E, Irving B, et al. The surface protein TIGIT suppresses T cell activation by promoting the generation of mature immunoregulatory dendritic cells. Nat Immunol. 2009;10(1):48–57. doi: 10.1038/ni.1674 19011627.
17. Joller N, Hafler JP, Brynedal B, Kassam N, Spoerl S, Levin SD, et al. Cutting edge: TIGIT has T cell-intrinsic inhibitory functions. Journal of immunology. 2011;186(3):1338–42. doi: 10.4049/jimmunol.1003081 21199897; PubMed Central PMCID: PMC3128994.
18. Levin SD, Taft DW, Brandt CS, Bucher C, Howard ED, Chadwick EM, et al. Vstm3 is a member of the CD28 family and an important modulator of T-cell function. Eur J Immunol. 2011;41(4):902–15. doi: 10.1002/eji.201041136 21416464; PubMed Central PMCID: PMC3733993.
19. Johnston RJ, Comps-Agrar L, Hackney J, Yu X, Huseni M, Yang Y, et al. The immunoreceptor TIGIT regulates antitumor and antiviral CD8(+) T cell effector function. Cancer Cell. 2014;26(6):923–37. doi: 10.1016/j.ccell.2014.10.018 25465800.
20. Kobayashi S, Nakano K, Watanabe E, Ishigaki T, Ohno N, Yuji K, et al. CADM1 expression and stepwise downregulation of CD7 are closely associated with clonal expansion of HTLV-I-infected cells in adult T-cell leukemia/lymphoma. Clin Cancer Res. 2014;20(11):2851–61. doi: 10.1158/1078-0432.CCR-13-3169 24727323.
21. Matsuoka M, Hattori T, Chosa T, Tsuda H, Kuwata S, Yoshida M, et al. T3 surface molecules on adult T cell leukemia cells are modulated in vivo. Blood. 1986;67(4):1070–6. 2869803.
22. Zhang Y, Maksimovic J, Naselli G, Qian J, Chopin M, Blewitt ME, et al. Genome-wide DNA methylation analysis identifies hypomethylated genes regulated by FOXP3 in human regulatory T cells. Blood. 2013;122(16):2823–36. doi: 10.1182/blood-2013-02-481788 23974203; PubMed Central PMCID: PMC3798997.
23. Satou Y, Yasunaga J, Yoshida M, Matsuoka M, HTLV-I basic leucine zipper factor gene mRNA supports proliferation of adult T cell leukemia cells. Proc Natl Acad Sci U S A. 2006;103(3):720–5. 16407133.
24. Mitobe Y, Yasunaga J, Furuta R, Matsuoka M, HTLV-1 bZIP Factor RNA and Protein Impart Distinct Functions on T-cell Proliferation and Survival. Cancer Res. 2015;75(19):4143–52. doi: 10.1158/0008-5472.CAN-15-0942 26383166.
25. Joller N, Lozano E, Burkett PR, Patel B, Xiao S, Zhu C, et al. Treg cells expressing the coinhibitory molecule TIGIT selectively inhibit proinflammatory Th1 and Th17 cell responses. Immunity. 2014;40(4):569–81. doi: 10.1016/j.immuni.2014.02.012 24745333; PubMed Central PMCID: PMC4070748.
26. Cretney E, Xin A, Shi W, Minnich M, Masson F, Miasari M, et al. The transcription factors Blimp-1 and IRF4 jointly control the differentiation and function of effector regulatory T cells. Nat Immunol. 2011;12(4):304–11. doi: 10.1038/ni.2006 21378976.
27. Lozano E, Dominguez-Villar M, Kuchroo V, Hafler DA, The TIGIT/CD226 axis regulates human T cell function. Journal of immunology. 2012;188(8):3869–75. doi: 10.4049/jimmunol.1103627 22427644; PubMed Central PMCID: PMC3324669.
28. Kim R, Emi M, Tanabe K, Arihiro K, Tumor-driven evolution of immunosuppressive networks during malignant progression. Cancer Res. 2006;66(11):5527–36. doi: 10.1158/0008-5472.CAN-05-4128 16740684.
29. Zhao T, Coutts A, Xu L, Yu J, Ohshima K, Matsuoka M, HTLV-1 bZIP factor supports proliferation of adult T cell leukemia cells through suppression of C/EBPalpha signaling. Retrovirology. 2013;10:159. doi: 10.1186/1742-4690-10-159 24359396; PubMed Central PMCID: PMC3880043.
30. Kozako T, Yoshimitsu M, Fujiwara H, Masamoto I, Horai S, White Y, et al. PD-1/PD-L1 expression in human T-cell leukemia virus type 1 carriers and adult T-cell leukemia/lymphoma patients. Leukemia. 2009;23(2):375–82. doi: 10.1038/leu.2008.272 18830259.
31. Chauvin JM, Pagliano O, Fourcade J, Sun Z, Wang H, Sander C, et al. TIGIT and PD-1 impair tumor antigen-specific CD8+ T cells in melanoma patients. J Clin Invest. 2015;125(5):2046–58. doi: 10.1172/JCI80445 25866972.
32. Kleffel S, Posch C, Barthel SR, Mueller H, Schlapbach C, Guenova E, et al. Melanoma Cell-Intrinsic PD-1 Receptor Functions Promote Tumor Growth. Cell. 2015;162(6):1242–56. doi: 10.1016/j.cell.2015.08.052 26359984.
33. Kuipers H, Muskens F, Willart M, Hijdra D, van Assema FB, Coyle AJ, et al. Contribution of the PD-1 ligands/PD-1 signaling pathway to dendritic cell-mediated CD4+ T cell activation. Eur J Immunol. 2006;36(9):2472–82. doi: 10.1002/eji.200635978 16917960.
34. Foy E, Li K, Sumpter R, Jr.Loo YM, Johnson CL, Wang C, et al. Control of antiviral defenses through hepatitis C virus disruption of retinoic acid-inducible gene-I signaling. Proc Natl Acad Sci U S A. 2005;102(8):2986–91. doi: 10.1073/pnas.0408707102 15710892; PubMed Central PMCID: PMC549461.
35. Verweij MC, Horst D, Griffin BD, Luteijn RD, Davison AJ, Ressing ME, et al. Viral inhibition of the transporter associated with antigen processing (TAP): a striking example of functional convergent evolution. PLoS Pathog. 2015;11(4):e1004743. doi: 10.1371/journal.ppat.1004743 25880312; PubMed Central PMCID: PMC4399834.
36. Johnson JM, Nicot C, Fullen J, Ciminale V, Casareto L, Mulloy JC, et al. Free major histocompatibility complex class I heavy chain is preferentially targeted for degradation by human T-cell leukemia/lymphotropic virus type 1 p12(I) protein. J Virol. 2001;75(13):6086–94. Epub 2001/06/08. doi: 10.1128/JVI.75.13.6086–6094.2001 11390610; PubMed Central PMCID: PMC114324.
37. Qin Z, Kearney P, Plaisance K, Parsons CH, Pivotal advance: Kaposi's sarcoma-associated herpesvirus (KSHV)-encoded microRNA specifically induce IL-6 and IL-10 secretion by macrophages and monocytes. J Leukoc Biol. 2010;87(1):25–34. 20052801; PubMed Central PMCID: PMC2801620.
38. Slobedman B, Barry PA, Spencer JV, Avdic S, Abendroth A, Virus-encoded homologs of cellular interleukin-10 and their control of host immune function. J Virol. 2009;83(19):9618–29. doi: 10.1128/JVI.01098-09 19640997; PubMed Central PMCID: PMC2747999.
39. de Waal Malefyt R, Haanen J, Spits H, Roncarolo MG, te Velde A, Figdor C, et al. Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression. J Exp Med. 1991;174(4):915–24. 1655948; PubMed Central PMCID: PMC2118975.
40. Said EA, Dupuy FP, Trautmann L, Zhang Y, Shi Y, El-Far M, et al. Programmed death-1-induced interleukin-10 production by monocytes impairs CD4+ T cell activation during HIV infection. Nat Med. 2010;16(4):452–9. doi: 10.1038/nm.2106 20208540; PubMed Central PMCID: PMC4229134.
41. Takenouchi N, Yao K, Jacobson S, Immunopathogensis of HTLV-I associated neurologic disease: molecular, histopathologic, and immunologic approaches. Front Biosci. 2004;9:2527–39. 15353305.
42. Yamamoto-Taguchi N, Satou Y, Miyazato P, Ohshima K, Nakagawa M, Katagiri K, et al. HTLV-1 bZIP factor induces inflammation through labile Foxp3 expression. PLoS Pathog. 2013;9(9):e1003630. doi: 10.1371/journal.ppat.1003630 24068936; PubMed Central PMCID: PMC3777874.
43. Araya N, Sato T, Ando H, Tomaru U, Yoshida M, Coler-Reilly A, et al. HTLV-1 induces a Th1-like state in CD4+CCR4+ T cells. J Clin Invest. 2014;124(8):3431–42. doi: 10.1172/JCI75250 24960164; PubMed Central PMCID: PMC4109535.
44. Clerc I, Polakowski N, Andre-Arpin C, Cook P, Barbeau B, Mesnard JM, et al. 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(35):23903–13. Epub 2008/07/05. doi: M803116200 [pii] doi: 10.1074/jbc.M803116200 18599479.
45. Ferrari R, Gou D, Jawdekar G, Johnson SA, Nava M, Su T, et al. Adenovirus small E1A employs the lysine acetylases p300/CBP and tumor suppressor Rb to repress select host genes and promote productive virus infection. Cell Host Microbe. 2014;16(5):663–76. doi: 10.1016/j.chom.2014.10.004 25525796; PubMed Central PMCID: PMC4418520.
46. Feuerer M, Hill JA, Kretschmer K, von Boehmer H, Mathis D, Benoist C, Genomic definition of multiple ex vivo regulatory T cell subphenotypes. Proc Natl Acad Sci U S A. 2010;107(13):5919–24. doi: 10.1073/pnas.1002006107 20231436; PubMed Central PMCID: PMC2851866.
47. Zhao T, Yasunaga J, Satou Y, Nakao M, Takahashi M, Fujii M, et al. Human T-cell leukemia virus type 1 bZIP factor selectively suppresses the classical pathway of NF-kappaB. Blood. 2009;113(12):2755–64. 19064727. doi: 10.1182/blood-2008-06-161729
48. Suzuki A, Makinoshima H, Wakaguri H, Esumi H, Sugano S, Kohno T, et al. Aberrant transcriptional regulations in cancers: genome, transcriptome and epigenome analysis of lung adenocarcinoma cell lines. Nucleic Acids Res. 2014;42(22):13557–72. doi: 10.1093/nar/gku885 25378332; PubMed Central PMCID: PMC4267666.
49. Langmead B, Trapnell C, Pop M, Salzberg SL, Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10(3):R25. doi: 10.1186/gb-2009-10-3-r25 19261174; PubMed Central PMCID: PMC2690996.
50. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative genomics viewer. Nat Biotechnol. 2011;29(1):24–6. doi: 10.1038/nbt.1754 21221095; PubMed Central PMCID: PMC3346182.
51. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012;7(3):562–78. doi: 10.1038/nprot.2012.016 22383036; PubMed Central PMCID: PMC3334321.
52. Thorvaldsdottir H, Robinson JT, Mesirov JP, ntegrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform. 2013;14(2):178–92. doi: 10.1093/bib/bbs017 22517427; PubMed Central PMCID: PMC3603213.
53. Gomez-del Arco P, Kashiwagi M, Jackson AF, Naito T, Zhang J, Liu F, et al. Alternative promoter usage at the Notch1 locus supports ligand-independent signaling in T cell development and leukemogenesis. Immunity. 2010;33(5):685–98. doi: 10.1016/j.immuni.2010.11.008 21093322; PubMed Central PMCID: PMCPMC3072037.
54. Papait R, Cattaneo P, Kunderfranco P, Greco C, Carullo P, Guffanti A, et al. Genome-wide analysis of histone marks identifying an epigenetic signature of promoters and enhancers underlying cardiac hypertrophy. Proc Natl Acad Sci U S A. 2013;110(50):20164–9. doi: 10.1073/pnas.1315155110 24284169; PubMed Central PMCID: PMCPMC3864351.
55. Kobayashi S, Watanabe E, Ishigaki T, Ohno N, Yuji K, Nakano K, et al. Advanced human T-cell leukemia virus type 1 carriers and early-stage indolent adult T-cell leukemia-lymphoma are indistinguishable based on CADM1 positivity in flow cytometry. Cancer Sci. 2015;106(5):598–603. doi: 10.1111/cas.12639 25703103.
56. Sugata K, Yasunaga JI, Mitobe Y, Miura M, Miyazato P, Kohara M, et al. Protective effect of cytotoxic T lymphocytes targeting HTLV-1 bZIP factor. Blood. 2015. doi: 10.1182/blood-2015-04-641118 26063164.
57. Lee N, Moss WN, Yario TA, Steitz JA, EBV noncoding RNA binds nascent RNA to drive host PAX5 to viral DNA. Cell. 2015;160(4):607–18. doi: 10.1016/j.cell.2015.01.015 25662012; PubMed Central PMCID: PMCPMC4329084.