1932

Abstract

The human T cell leukemia virus persists in vivo in 103 to 106 clones of T lymphocytes that appear to survive for the lifetime of the host. The plus strand of the provirus is typically transcriptionally silent in freshly isolated lymphocytes, but the strong, persistently activated cytotoxic T lymphocyte (CTL) response to the viral antigens indicates that the virus is not constantly latent in vivo. There is now evidence that the plus strand is transcribed in intense intermittent bursts that are triggered by cellular stress, modulated by hypoxia and glycolysis, and inhibited by polycomb repressive complex 1 (PRC1). The minus-strand gene is transcribed at a lower, more constant level but is silent in a proportion of infected cells at a given time. Viral genes in the sense and antisense strands of the provirus play different respective roles in latency and de novo infection: Expression of the plus-strand gene is essential for de novo infection, whereas appears to facilitate survival of the infected T cell clone in vivo.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-092818-015501
2019-09-29
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/virology/6/1/annurev-virology-092818-015501.html?itemId=/content/journals/10.1146/annurev-virology-092818-015501&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Gessain A, Cassar O. 2012. Epidemiological aspects and world distribution of HTLV-1 infection. Front. Microbiol. 3:388
    [Google Scholar]
  2. 2. 
    Bangham CRM. 2018. Human T cell leukemia virus type 1: persistence and pathogenesis. Annu. Rev. Immunol. 36:43–71
    [Google Scholar]
  3. 3. 
    Bangham CRM, Matsuoka M. 2017. Human T-cell leukemia virus type 1: parasitism and pathogenesis. Philos. Trans. R. Soc. B 372:20160272
    [Google Scholar]
  4. 4. 
    Bangham CR, Araujo A, Yamano Y, Taylor GP 2015. HTLV-1-associated myelopathy/tropical spastic paraparesis. Nat. Rev. Dis. Primers 1:15012
    [Google Scholar]
  5. 5. 
    Iwanaga M, Watanabe T, Yamaguchi K 2012. Adult T-cell leukemia: a review of epidemiological evidence. Front. Microbiol. 3:322
    [Google Scholar]
  6. 6. 
    Matsuura E, Nozuma S, Tashiro Y, Kubota R, Izumo S, Takashima H 2016. HTLV-1 associated myelopathy/tropical spastic paraparesis (HAM/TSP): a comparative study to identify factors that influence disease progression. J. Neurol. Sci. 371:112–16
    [Google Scholar]
  7. 7. 
    Overbaugh J, Bangham CR. 2001. Selection forces and constraints on retroviral sequence variation. Science 292:1106–9
    [Google Scholar]
  8. 8. 
    Mbonye U, Karn J. 2017. The molecular basis for human immunodeficiency virus latency. Annu. Rev. Virol. 4:261–85
    [Google Scholar]
  9. 9. 
    Asquith B, Hanon E, Taylor GP, Bangham CR 2000. Is human T-cell lymphotropic virus type I really silent?. Philos. Trans. R. Soc. B Biol. Sci. 355:1013–19
    [Google Scholar]
  10. 10. 
    Cavrois M, Gessain A, Wain-Hobson S, Wattel E 1996. Proliferation of HTLV-1 infected circulating cells in vivo in all asymptomatic carriers and patients with TSP/HAM. Oncogene 12:2419–23
    [Google Scholar]
  11. 11. 
    Wattel E, Cavrois M, Gessain A, Wain-Hobson S 1996. Clonal expansion of infected cells: a way of life for HTLV-I. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 13:Suppl. 1S92–99
    [Google Scholar]
  12. 12. 
    Furukawa Y, Fujisawa J, Osame M, Toita M, Sonoda S et al. 1992. Frequent clonal proliferation of human T-cell leukemia virus type 1 (HTLV-1)-infected T cells in HTLV-1-associated myelopathy (HAM-TSP). Blood 80:1012–16
    [Google Scholar]
  13. 13. 
    Maldarelli F, Wu X, Su L, Simonetti FR, Shao W et al. 2014. Specific HIV integration sites are linked to clonal expansion and persistence of infected cells. Science 345:179–83
    [Google Scholar]
  14. 14. 
    Wagner TA, McLaughlin S, Garg K, Cheung CY, Larsen BB et al. 2014. Proliferation of cells with HIV integrated into cancer genes contributes to persistent infection. Science 345:570–73
    [Google Scholar]
  15. 15. 
    Murray AJ, Kwon KJ, Farber DL, Siliciano RF 2016. The latent reservoir for HIV-1: how immunologic memory and clonal expansion contribute to HIV-1 persistence. J. Immunol. 197:407–17
    [Google Scholar]
  16. 16. 
    Bangham CR, Cook LB, Melamed A 2014. HTLV-1 clonality in adult T-cell leukaemia and non-malignant HTLV-1 infection. Semin. Cancer Biol. 26C:89–98
    [Google Scholar]
  17. 17. 
    Gillet NA, Malani N, Melamed A, Gormley N, Carter R et al. 2011. The host genomic environment of the provirus determines the abundance of HTLV-1-infected T-cell clones. Blood 117:3113–22
    [Google Scholar]
  18. 18. 
    Melamed A, Laydon DJ, Gillet NA, Tanaka Y, Taylor GP, Bangham CR 2013. Genome-wide determinants of proviral targeting, clonal abundance and expression in natural HTLV-1 infection. PLOS Pathog 9:e1003271
    [Google Scholar]
  19. 19. 
    Bangham CR, Osame M. 2005. Cellular immune response to HTLV-1. Oncogene 24:6035–46
    [Google Scholar]
  20. 20. 
    Derse D, Hill SA, Princler G, Lloyd P, Heidecker G 2007. Resistance of human T cell leukemia virus type 1 to APOBEC3G restriction is mediated by elements in nucleocapsid. PNAS 104:2915–20
    [Google Scholar]
  21. 21. 
    Journo C, Mahieux R. 2011. HTLV-1 and innate immunity. Viruses 3:1374–94
    [Google Scholar]
  22. 22. 
    Satou Y, Yasunaga J, Yoshida M, Matsuoka M 2006. HTLV-I basic leucine zipper factor gene mRNA supports proliferation of adult T cell leukemia cells. PNAS 103:720–25
    [Google Scholar]
  23. 23. 
    Billman MR, Rueda D, Bangham CRM 2017. Single-cell heterogeneity and cell-cycle-related viral gene bursts in the human leukaemia virus HTLV-1. Wellcome Open Res 2:87
    [Google Scholar]
  24. 24. 
    Hilburn S, Rowan A, Demontis MA, MacNamara A, Asquith B et al. 2011. In vivo expression of human T-lymphotropic virus type 1 basic leucine-zipper protein generates specific CD8+ and CD4+ T-lymphocyte responses that correlate with clinical outcome. J. Infect. Dis. 203:529–36
    [Google Scholar]
  25. 25. 
    MacNamara A, Rowan A, Hilburn S, Kadolsky U, Fujiwara H et al. 2010. HLA class I binding of HBZ determines outcome in HTLV-1 infection. PLOS Pathog 6:e1001117
    [Google Scholar]
  26. 26. 
    Seich al Basatena NK, MacNamara A, Vine AM, Thio CL, Astemborski J et al. 2011. KIR2DL2 enhances protective and detrimental HLA class I-mediated immunity in chronic viral infection. PLOS Pathog 7:e1002270
    [Google Scholar]
  27. 27. 
    Rende F, Cavallari I, Corradin A, Silic-Benussi M, Toulza F et al. 2011. Kinetics and intracellular compartmentalization of HTLV-1 gene expression: nuclear retention of HBZ mRNAs. Blood 117:4855–59
    [Google Scholar]
  28. 28. 
    Rowan AG, Suemori K, Fujiwara H, Yasukawa M, Tanaka Y et al. 2014. Cytotoxic T lymphocyte lysis of HTLV-1 infected cells is limited by weak HBZ protein expression, but non-specifically enhanced on induction of Tax expression. Retrovirology 11:116
    [Google Scholar]
  29. 29. 
    Tchasovnikarova IA, Timms RT, Matheson NJ, Wals K, Antrobus R et al. 2015. Epigenetic silencing by the HUSH complex mediates position-effect variegation in human cells. Science 348:1481–85
    [Google Scholar]
  30. 30. 
    Zhu Y, Wang GZ, Cingoz O, Goff SP 2018. NP220 mediates silencing of unintegrated retroviral DNA. Nature 564:278–82
    [Google Scholar]
  31. 31. 
    Matsuoka M, Jeang KT. 2007. Human T-cell leukaemia virus type 1 (HTLV-1) infectivity and cellular transformation. Nat. Rev. Cancer 7:270–80
    [Google Scholar]
  32. 32. 
    Nyborg JK, Egan D, Sharma N 2010. The HTLV-1 Tax protein: revealing mechanisms of transcriptional activation through histone acetylation and nucleosome disassembly. Biochim. Biophys. Acta Gene Regul. Mech. 1799:266–74
    [Google Scholar]
  33. 33. 
    Inoue J, Yoshida M, Seiki M 1987. Transcriptional (p40x) and post-transcriptional (p27x-III) regulators are required for the expression and replication of human T-cell leukemia virus type I genes. PNAS 84:3653–57
    [Google Scholar]
  34. 34. 
    Philip S, Zahoor MA, Zhi HJ, Ho YK, Giam CZ 2014. Regulation of human T-lymphotropic virus type I latency and reactivation by HBZ and Rex. PLOS Pathog 10:e1004040
    [Google Scholar]
  35. 35. 
    Clerc I, Polakowski N, Andre-Arpin C, Cook P, Barbeau B et al. 2008. 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. 283:23903–13
    [Google Scholar]
  36. 36. 
    Fauquenoy S, Robette G, Kula A, Vanhulle C, Bouchat S et al. 2017. Repression of human T-lymphotropic virus type 1 long terminal repeat sense transcription by Sp1 recruitment to novel Sp1 binding sites. Sci. Rep. 7:43221
    [Google Scholar]
  37. 37. 
    Huang H, Santoso N, Power D, Simpson S, Dieringer M et al. 2015. FACT proteins, SUPT16H and SSRP1, are transcriptional suppressors of HIV-1 and HTLV-1 that facilitate viral latency. J. Biol. Chem. 290:27297–310
    [Google Scholar]
  38. 38. 
    Ma G, Yasunaga J, Matsuoka M 2016. Multifaceted functions and roles of HBZ in HTLV-1 pathogenesis. Retrovirology 13:16
    [Google Scholar]
  39. 39. 
    Zhao T, Satou Y, Sugata K, Miyazato P, Green PL et al. 2011. HTLV-1 bZIP factor enhances TGF-β signaling through p300 coactivator. Blood 118:71865–76
    [Google Scholar]
  40. 40. 
    Zhao T, Yasunaga J, Satou Y, Nakao M, Takahashi M et al. 2009. Human T-cell leukemia virus type 1 bZIP factor selectively suppresses the classical pathway of NF-κB. Blood 113:122755–64
    [Google Scholar]
  41. 41. 
    Zhi H, Yang L, Kuo YL, Ho YK, Shih HM, Giam CZ 2011. NF-κB hyper-activation by HTLV-1 tax induces cellular senescence, but can be alleviated by the viral anti-sense protein HBZ. PLOS Pathog 7:4e1002025
    [Google Scholar]
  42. 42. 
    Matsuoka M, Yasunaga J. 2013. Human T-cell leukemia virus type 1: replication, proliferation and propagation by Tax and HTLV-1 bZIP factor. Curr. Opin. Virol. 3:684–91
    [Google Scholar]
  43. 43. 
    Yoshida M, Satou Y, Yasunaga J, Fujisawa J, Matsuoka M 2008. Transcriptional control of spliced and unspliced human T-cell leukemia virus type 1 bZIP factor (HBZ) gene. J. Virol. 82:9359–68
    [Google Scholar]
  44. 44. 
    Taniguchi Y, Nosaka K, Yasunaga J, Maeda M, Mueller N et al. 2005. Silencing of human T-cell leukemia virus type I gene transcription by epigenetic mechanisms. Retrovirology 2:64
    [Google Scholar]
  45. 45. 
    Miura M, Miyazato P, Satou Y, Tanaka Y, Bangham CRM 2018. Epigenetic changes around the pX region and spontaneous HTLV-1 transcription are CTCF-independent. Wellcome Open Res 3:105
    [Google Scholar]
  46. 46. 
    Satou Y, Miyazato P, Ishihara K, Yaguchi H, Melamed A et al. 2016. The retrovirus HTLV-1 inserts an ectopic CTCF-binding site into the human genome. PNAS 113:3054–59
    [Google Scholar]
  47. 47. 
    Takeda S, Maeda M, Morikawa S, Taniguchi Y, Yasunaga J et al. 2004. Genetic and epigenetic inactivation of tax gene in adult T-cell leukemia cells. Int. J. Cancer 109:559–67
    [Google Scholar]
  48. 48. 
    Belrose G, Gross A, Olindo S, Lezin A, Dueymes M et al. 2011. Effects of valproate on Tax and HBZ expression in HTLV-1 and HAM/TSP T lymphocytes. Blood 118:2483–91
    [Google Scholar]
  49. 49. 
    Ma G, Yasunaga J, Akari H, Matsuoka M 2015. TCF1 and LEF1 act as T-cell intrinsic HTLV-1 antagonists by targeting Tax. PNAS 112:2216–21
    [Google Scholar]
  50. 50. 
    Kulkarni A, Mateus M, Thinnes CC, McCullagh JS, Schofield CJ et al. 2017. Glucose metabolism and oxygen availability govern reactivation of the latent human retrovirus HTLV-1. Cell Chem. Biol. 24:1377–87.e3
    [Google Scholar]
  51. 51. 
    Kulkarni A, Taylor GP, Klose RJ, Schofield CJ, Bangham CR 2018. Histone H2A monoubiquitylation and p38-MAPKs regulate immediate-early gene-like reactivation of latent retrovirus HTLV-1. JCI Insight 3:e123196
    [Google Scholar]
  52. 52. 
    Mahgoub M, Yasunaga JI, Iwami S, Nakaoka S, Koizumi Y et al. 2018. Sporadic on/off switching of HTLV-1 Tax expression is crucial to maintain the whole population of virus-induced leukemic cells. PNAS 115:E1269–78
    [Google Scholar]
  53. 53. 
    Basbous J, Arpin C, Gaudray G, Piechaczyk M, Devaux C, Mesnard JM 2003. The HBZ factor of human T-cell leukemia virus type I dimerizes with transcription factors JunB and c-Jun and modulates their transcriptional activity. J. Biol. Chem. 278:43620–27
    [Google Scholar]
  54. 54. 
    Arpin-Andre C, Laverdure S, Barbeau B, Gross A, Mesnard JM 2014. Construction of a reporter vector for analysis of bidirectional transcriptional activity of retrovirus LTR. Plasmid 74:45–51
    [Google Scholar]
  55. 55. 
    Wattel E, Vartanian JP, Pannetier C, Wain-Hobson S 1995. Clonal expansion of human T-cell leukemia virus type I-infected cells in asymptomatic and symptomatic carriers without malignancy. J. Virol. 69:2863–68
    [Google Scholar]
  56. 56. 
    Daenke S, Nightingale S, Cruickshank JK, Bangham CR 1990. Sequence variants of human T-cell lymphotropic virus type I from patients with tropical spastic paraparesis and adult T-cell leukemia do not distinguish neurological from leukemic isolates. J. Virol. 64:1278–82
    [Google Scholar]
  57. 57. 
    Ina Y, Gojobori T. 1990. Molecular evolution of human T-cell leukemia virus. J. Mol. Evol. 31:493–99
    [Google Scholar]
  58. 58. 
    Furuta R, Yasunaga JI, Miura M, Sugata K, Saito A et al. 2017. Human T-cell leukemia virus type 1 infects multiple lineage hematopoietic cells in vivo. PLOS Pathog 13:11e1006722
    [Google Scholar]
  59. 59. 
    Farber DL, Yudanin NA, Restifo NP 2014. Human memory T cells: generation, compartmentalization and homeostasis. Nat. Rev. Immunol. 14:24–35
    [Google Scholar]
  60. 60. 
    Bangham CR. 2009. CTL quality and the control of human retroviral infections. Eur. J. Immunol. 39:1700–12
    [Google Scholar]
  61. 61. 
    Goon PK, Biancardi A, Fast N, Igakura T, Hanon E et al. 2004. Human T cell lymphotropic virus (HTLV) type-1-specific CD8+ T cells: frequency and immunodominance hierarchy. J. Infect. Dis. 189:2294–98
    [Google Scholar]
  62. 62. 
    Jacobson S, Shida H, McFarlin DE, Fauci AS, Koenig S 1990. Circulating CD8+ cytotoxic T lymphocytes specific for HTLV-I pX in patients with HTLV-I associated neurological disease. Nature 348:245–48
    [Google Scholar]
  63. 63. 
    Kannagi M, Harada S, Maruyama I, Inoko H, Igarashi H et al. 1991. Predominant recognition of human T cell leukemia virus type I (HTLV-I) pX gene products by human CD8+ cytotoxic T cells directed against HTLV-I-infected cells. Int. Immunol. 3:761–67
    [Google Scholar]
  64. 64. 
    Hanon E, Hall S, Taylor GP, Saito M, Davis R et al. 2000. 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 95:1386–92
    [Google Scholar]
  65. 65. 
    Minato S, Itoyama Y, Goto I, Yamamoto N 1988. Expression of HTLV-I antigen in cultured peripheral blood mononuclear cells from patients with HTLV-I associated myelopathy. J. Neurol. Sci. 87:233–44
    [Google Scholar]
  66. 66. 
    Tochikura T, Iwahashi M, Matsumoto T, Koyanagi Y, Hinuma Y, Yamamoto N 1985. Effect of human serum anti-HTLV antibodies on viral antigen induction in vitro cultured peripheral lymphocytes from adult T-cell leukemia patients and healthy virus carriers. Int. J. Cancer 36:1–7
    [Google Scholar]
  67. 67. 
    Fukushima N, Nishiura Y, Nakamura T, Yamada Y, Kohno S, Eguchi K 2005. Involvement of p38 MAPK signaling pathway in IFN-gamma and HTLV-1 expression in patients with HTLV-I-associated myelopathy/tropical spastic paraparesis. J. Neuroimmunol. 159:196–202
    [Google Scholar]
  68. 68. 
    Washiyama M, Nishigaki K, Ahmed N, Kinpara S, Ishii Y et al. 2007. IL-2 withdrawal induces HTLV-1 expression through p38 activation in ATL cell lines. FEBS Lett 581:5207–12
    [Google Scholar]
  69. 69. 
    Silic-Benussi M, Cavallari I, Vajente N, Vidali S, Chieco-Bianchi L et al. 2010. Redox regulation of T-cell turnover by the p13 protein of human T-cell leukemia virus type 1: distinct effects in primary versus transformed cells. Blood 116:54–62
    [Google Scholar]
  70. 70. 
    Bahrami S, Drablos F. 2016. Gene regulation in the immediate-early response process. Adv. Biol. Regul. 62:37–49
    [Google Scholar]
  71. 71. 
    Herschman HR. 1991. Primary response genes induced by growth-factors and tumor promoters. Annu. Rev. Biochem. 60:281–319
    [Google Scholar]
  72. 72. 
    Kulkarni A, Bangham CRM. 2018. HTLV-1: regulating the balance between proviral latency and reactivation. Front. Microbiol. 9:449
    [Google Scholar]
  73. 73. 
    Francis NJ, Kingston RE, Woodcock CL 2004. Chromatin compaction by a polycomb group protein complex. Science 306:1574–77
    [Google Scholar]
  74. 74. 
    Zhou W, Zhu P, Wang J, Pascual G, Ohgi KA et al. 2008. Histone H2A monoubiquitination represses transcription by inhibiting RNA polymerase II transcriptional elongation. Mol. Cell 29:69–80
    [Google Scholar]
  75. 75. 
    Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ et al. 2006. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125:315–26
    [Google Scholar]
  76. 76. 
    Vidal M, Starowicz K. 2017. Polycomb complexes PRC1 and their function in hematopoiesis. Exp. Hematol. 48:12–31
    [Google Scholar]
  77. 77. 
    Farcas AM, Blackledge NP, Sudbery I, Long HK, McGouran JF et al. 2012. KDM2B links the polycomb repressive complex 1 (PRC1) to recognition of CpG islands. eLife 1:e00205
    [Google Scholar]
  78. 78. 
    van den Boom V, Maat H, Geugien M, Rodriguez Lopez A, Sotoca AM et al. 2016. Non-canonical PRC1.1 targets active genes independent of H3K27me3 and is essential for leukemogenesis. Cell Rep 14:332–46
    [Google Scholar]
  79. 79. 
    Stanton BZ, Hodges C, Calarco JP, Braun SM, Ku WL et al. 2017. Smarca4 ATPase mutations disrupt direct eviction of PRC1 from chromatin. Nat. Genet. 49:282–88
    [Google Scholar]
  80. 80. 
    Cotto-Rios XM, Bekes M, Chapman J, Ueberheide B, Huang TT 2012. Deubiquitinases as a signaling target of oxidative stress. Cell Rep 2:1475–84
    [Google Scholar]
  81. 81. 
    Silic-Benussi M, Marin O, Biasiotto R, D'Agostino DM, Ciminale V 2010. Effects of human T-cell leukemia virus type 1 (HTLV-1) p13 on mitochondrial K+ permeability: a new member of the viroporin family?. FEBS Lett 584:2070–75
    [Google Scholar]
  82. 82. 
    Schoenfelder S, Sugar R, Dimond A, Javierre BM, Armstrong H et al. 2015. Polycomb repressive complex PRC1 spatially constrains the mouse embryonic stem cell genome. Nat. Genet. 47:1179–86
    [Google Scholar]
  83. 83. 
    Bickmore WA. 2013. The spatial organization of the human genome. Annu. Rev. Genom. Hum. Genet. 14:67–84
    [Google Scholar]
  84. 84. 
    Eagen KP, Aiden EL, Kornberg RD 2017. Polycomb-mediated chromatin loops revealed by a subkilobase-resolution chromatin interaction map. PNAS 114:8764–69
    [Google Scholar]
  85. 85. 
    Melamed A, Yaguchi H, Miura M, Witkover A, Fitzgerald TW et al. 2018. The human leukemia virus HTLV-1 alters the structure and transcription of host chromatin in cis. eLife 7:e36245
    [Google Scholar]
  86. 86. 
    Nguyen K, Das B, Dobrowolski C, Karn J 2017. Multiple histone lysine methyltransferases are required for the establishment and maintenance of HIV-1 latency. mBio 8:e00133–17
    [Google Scholar]
  87. 87. 
    Fujikawa D, Nakagawa S, Hori M, Kurokawa N, Soejima A et al. 2016. Polycomb-dependent epigenetic landscape in adult T-cell leukemia. Blood 127:1790–802
    [Google Scholar]
  88. 88. 
    Kar G, Kim JK, Kolodziejczyk AA, Natarajan KN, Torlai Triglia E et al. 2017. Flipping between Polycomb repressed and active transcriptional states introduces noise in gene expression. Nat. Commun. 8:36
    [Google Scholar]
  89. 89. 
    Melamed A, Laydon DJ, Al Khatib H, Rowan AG, Taylor GP, Bangham CR 2015. HTLV-1 drives vigorous clonal expansion of infected CD8+ T cells in natural infection. Retrovirology 12:91
    [Google Scholar]
  90. 90. 
    Satou Y, Utsunomiya A, Tanabe J, Nakagawa M, Nosaka K, Matsuoka M 2012. HTLV-1 modulates the frequency and phenotype of FoxP3+CD4+ T cells in virus-infected individuals. Retrovirology 9:46
    [Google Scholar]
  91. 91. 
    Toulza F, Heaps A, Tanaka Y, Taylor GP, Bangham CR 2008. High frequency of CD4+FoxP3+ cells in HTLV-1 infection: inverse correlation with HTLV-1-specific CTL response. Blood 111:5047–53
    [Google Scholar]
  92. 92. 
    Toulza F, Nosaka K, Tanaka Y, Schioppa T, Balkwill F et al. 2010. Human T-lymphotropic virus type 1-induced CC chemokine ligand 22 maintains a high frequency of functional FoxP3+ regulatory T cells. J. Immunol. 185:183–89
    [Google Scholar]
  93. 93. 
    O'Neill LA, Kishton RJ, Rathmell J 2016. A guide to immunometabolism for immunologists. Nat. Rev. Immunol. 16:553–65
    [Google Scholar]
  94. 94. 
    Procaccini C, Carbone F, Di Silvestre D, Brambilla F, De Rosa V et al. 2016. The proteomic landscape of human ex vivo regulatory and conventional T cells reveals specific metabolic requirements. Immunity 44:2406–21
    [Google Scholar]
  95. 95. 
    Manel N, Kim FJ, Kinet S, Taylor N, Sitbon M, Battini JL 2003. The ubiquitous glucose transporter GLUT-1 is a receptor for HTLV. Cell 115:449–59
    [Google Scholar]
  96. 96. 
    Sanchez EL, Lagunoff M. 2015. Viral activation of cellular metabolism. Virology 479–480:609–18
    [Google Scholar]
  97. 97. 
    Taylor N. 2017. Just a spoonful of sugar, HTLV-1 style. Cell Chem. Biol. 24:1319–20
    [Google Scholar]
  98. 98. 
    Eales KL, Hollinshead KE, Tennant DA 2016. Hypoxia and metabolic adaptation of cancer cells. Oncogenesis 5:e190
    [Google Scholar]
  99. 99. 
    Mohyeldin A, Garzon-Muvdi T, Quinones-Hinojosa A 2010. Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell 7:150–61
    [Google Scholar]
  100. 100. 
    Islam MS, Leissing TM, Chowdhury R, Hopkinson RJ, Schofield CJ 2018. 2-Oxoglutarate-dependent oxygenases. Annu. Rev. Biochem. 87:585–620
    [Google Scholar]
  101. 101. 
    Femino AM, Fay FS, Fogarty K, Singer RH 1998. Visualization of single RNA transcripts in situ. Science 280:585–90
    [Google Scholar]
  102. 102. 
    Raj A, Peskin CS, Tranchina D, Vargas DY, Tyagi S 2006. Stochastic mRNA synthesis in mammalian cells. PLOS Biol 4:e309
    [Google Scholar]
  103. 103. 
    Phillips JE, Corces VG. 2009. CTCF: master weaver of the genome. Cell 137:1194–211
    [Google Scholar]
  104. 104. 
    Ganji M, Shaltiel IA, Bisht S, Kim E, Kalichava A et al. 2018. Real-time imaging of DNA loop extrusion by condensin. Science 360:102–5
    [Google Scholar]
  105. 105. 
    Corces MR, Corces VG. 2016. The three-dimensional cancer genome. Curr. Opin. Genet. Dev. 36:1–7
    [Google Scholar]
  106. 106. 
    Flavahan WA, Drier Y, Liau BB, Gillespie SM, Venteicher AS et al. 2016. Insulator dysfunction and oncogene activation in IDH mutant gliomas. Nature 529:110–14
    [Google Scholar]
  107. 107. 
    Hnisz D, Weintraub AS, Day DS, Valton AL, Bak RO et al. 2016. Activation of proto-oncogenes by disruption of chromosome neighborhoods. Science 351:1454–58
    [Google Scholar]
  108. 108. 
    Ong CT, Corces VG. 2014. CTCF: an architectural protein bridging genome topology and function. Nat. Rev. Genet. 15:234–46
    [Google Scholar]
  109. 109. 
    Bartman CR, Hsu SC, Hsiung CC, Raj A, Blobel GA 2016. Enhancer regulation of transcriptional bursting parameters revealed by forced chromatin looping. Mol. Cell 62:237–47
    [Google Scholar]
  110. 110. 
    Gibcus JH, Dekker J. 2013. The hierarchy of the 3D genome. Mol. Cell 49:773–82
    [Google Scholar]
  111. 111. 
    Schwarzer W, Spitz F. 2014. The architecture of gene expression: integrating dispersed cis-regulatory modules into coherent regulatory domains. Curr. Opin. Genet. Dev. 27:74–82
    [Google Scholar]
  112. 112. 
    Laydon DJ, Melamed A, Sim A, Gillet NA, Sim K et al. 2014. Quantification of HTLV-1 clonality and TCR diversity. PLOS Comput. Biol. 10:e1003646
    [Google Scholar]
  113. 113. 
    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. 12:466–72
    [Google Scholar]
  114. 114. 
    Nerenberg M, Hinrichs SH, Reynolds RK, Khoury G, Jay G 1987. The tat gene of human T-lymphotropic virus type 1 induces mesenchymal tumors in transgenic mice. Science 237:1324–29
    [Google Scholar]
  115. 115. 
    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
    [Google Scholar]
  116. 116. 
    Grossman WJ, Kimata JT, Wong FH, Zutter M, Ley TJ, Ratner L 1995. Development of leukemia in mice transgenic for the tax gene of human T-cell leukemia virus type I. PNAS 92:1057–61
    [Google Scholar]
  117. 117. 
    Furukawa Y, Kubota R, Tara M, Izumo S, Osame M 2001. Existence of escape mutant in HTLV-I tax during the development of adult T-cell leukemia. Blood 97:987–93
    [Google Scholar]
  118. 118. 
    Koiwa T, Hamano-Usami A, Ishida T, Okayama A, Yamaguchi K et al. 2002. 5′-long terminal repeat-selective CpG methylation of latent human T-cell leukemia virus type 1 provirus in vitro and in vivo. J. Virol. 76:9389–97
    [Google Scholar]
  119. 119. 
    Tamiya S, Matsuoka M, Etoh K, Watanabe T, Kamihira S et al. 1996. Two types of defective human T-lymphotropic virus type I provirus in adult T-cell leukemia. Blood 88:3065–73
    [Google Scholar]
  120. 120. 
    Fan J, Ma G, Nosaka K, Tanabe J, Satou Y et al. 2010. APOBEC3G generates nonsense mutations in human T-cell leukemia virus type 1 proviral genomes in vivo. J. Virol 84:7278–87
    [Google Scholar]
  121. 121. 
    Miyazaki M, Yasunaga J, Taniguchi Y, Tamiya S, Nakahata T, Matsuoka M 2007. Preferential selection of human T-cell leukemia virus type 1 provirus lacking the 5′ long terminal repeat during oncogenesis. J. Virol. 81:5714–23
    [Google Scholar]
  122. 122. 
    Suter DM, Molina N, Gatfield D, Schneider K, Schibler U, Naef F 2011. Mammalian genes are transcribed with widely different bursting kinetics. Science 332:472–74
    [Google Scholar]
  123. 123. 
    Raj A, van Oudenaarden A 2008. Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135:216–26
    [Google Scholar]
  124. 124. 
    Nicolas D, Zoller B, Suter DM, Naef F 2018. Modulation of transcriptional burst frequency by histone acetylation. PNAS 115:7153–58
    [Google Scholar]
  125. 125. 
    Skinner SO, Xu H, Nagarkar-Jaiswal S, Freire PR, Zwaka TP, Golding I 2016. Single-cell analysis of transcription kinetics across the cell cycle. eLife 5:e12175
    [Google Scholar]
  126. 126. 
    Ho YC, Shan L, Hosmane NN, Wang J, Laskey SB et al. 2013. Replication-competent noninduced proviruses in the latent reservoir increase barrier to HIV-1 cure. Cell 155:540–51
    [Google Scholar]
  127. 127. 
    Tamaki H, Matsuoka M. 2006. Donor-derived T-cell leukemia after bone marrow transplantation. N. Engl. J. Med. 354:1758–59
    [Google Scholar]
  128. 128. 
    Tamaki H, Taniguchi Y, Kikuchi A, Yamagami T, Soma T, Matsuoka M 2007. Development of adult T-cell leukemia in donor-derived human T-cell leukemia virus type I-infected T cells after allogeneic bone marrow transplantation. Leukemia 21:1594–96
    [Google Scholar]
  129. 129. 
    Kataoka K, Nagata Y, Kitanaka A, Shiraishi Y, Shimamura T et al. 2015. Integrated molecular analysis of adult T cell leukemia/lymphoma. Nat. Genet. 47:1304–15
    [Google Scholar]
  130. 130. 
    Bangham CR, Ratner L. 2015. How does HTLV-1 cause adult T-cell leukaemia/lymphoma (ATL)?. Curr. Opin. Virol. 14:93–100
    [Google Scholar]
  131. 131. 
    Tomasetti C, Vogelstein B. 2015. Variation in cancer risk among tissues can be explained by the number of stem cell divisions. Science 347:78–81
    [Google Scholar]
  132. 132. 
    Oyama T, Yamamoto K, Asano N, Oshiro A, Suzuki R et al. 2007. Age-related EBV-associated B-cell lymphoproliferative disorders constitute a distinct clinicopathologic group: a study of 96 patients. Clin. Cancer Res. 13:5124–32
    [Google Scholar]
  133. 133. 
    Yasunaga J, Sakai T, Nosaka K, Etoh K, Tamiya S et al. 2001. Impaired production of naive T lymphocytes in human T-cell leukemia virus type I-infected individuals: its implications in the immunodeficient state. Blood 97:3177–83
    [Google Scholar]
/content/journals/10.1146/annurev-virology-092818-015501
Loading
/content/journals/10.1146/annurev-virology-092818-015501
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error