Double control systems for human T-cell leukemia virus type 1 by innate and acquired immunity

Cancer Science

Volumn 102, Issue 4, 2011, Pages 670-676

  Kannagi, Mari ^a   Hasegawa, Atsuhiko ^a   Kinpara, Shuichi ^a   Shimizu, Yukiko ^a   Takamori, Ayako ^a   Utsunomiya, Atae ^b  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b IMAMURA BUN IN HOSPITAL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; MESSENGER RNA; MITOMYCIN C;

ACHROMOBACTER DENITRIFICANS; ADAPTIVE IMMUNITY; CELL CULTURE; CELL ISOLATION; FOLLOW UP; HUMAN; HUMAN T CELL LEUKEMIA VIRUS 1; HUMAN T CELL LEUKEMIA VIRUS INFECTION; IMMUNIZATION; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; STROMA CELL; VIRUS LOAD; VIRUS PATHOGENESIS;

ADAPTIVE IMMUNITY; ADULT; HTLV-I INFECTIONS; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMANS; LYMPHOMA, T-CELL;

EID: 79952763125     PISSN: 13479032     EISSN: 13497006     Source Type: Journal    
DOI: 10.1111/j.1349-7006.2011.01862.x     Document Type: Review

References (79)

1. Hinuma Y, Nagata K, Hanaoka M et al. Adult T-cell leukemia: antigen in an ATL cell line and detection of antibodies to the antigen in human sera. Proc Natl Acad Sci USA 1981; 78: 6476-80.
2. Poiesz BJ, Ruscetti FW, Gazdar AF, Bunn PA, Minna JD, Gallo RC. 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 USA 1980; 77: 7415-9.
3. Tajima K. The 4th nation-wide study of adult T-cell leukemia/lymphoma (ATL) in Japan: estimates of risk of ATL and its geographical and clinical features. The T- and B-cell Malignancy Study Group. Int J Cancer 1990; 45: 237-43.
4. Uchiyama T. Human T cell leukemia virus type I (HTLV-I) and human diseases. Annu Rev Immunol 1997; 15: 15-37.
5. Osame M, Usuku K, Izumo S et al. HTLV-I associated myelopathy, a new clinical entity. Lancet 1986; 1: 1031-2.
6. Gessain A, Barin F, Vernant JC et al. Antibodies to human T-lymphotropic virus type-I in patients with tropical spastic paraparesis. Lancet 1985; 2: 407-10.
7. Mochizuki M, Watanabe T, Yamaguchi K et al. Uveitis associated with human T-cell lymphotropic virus type I. Am J Ophthalmol 1992; 114: 123-9.
8. Nishioka K, Maruyama I, Sato K, Kitajima I, Nakajima Y, Osame M. Chronic inflammatory arthropathy associated with HTLV-I. Lancet 1989; 1: 441.
9. Utsunomiya A, Miyazaki Y, Takatsuka Y et al. Improved outcome of adult T cell leukemia/lymphoma with allogeneic hematopoietic stem cell transplantation. Bone Marrow Transplant 2001; 27: 15-20.
10. Okamura J, Utsunomiya A, Tanosaki R et al. Allogeneic stem-cell transplantation with reduced conditioning intensity as a novel immunotherapy and antiviral therapy for adult T-cell leukemia/lymphoma. Blood 2005; 105: 4143-5.
11. Yamamoto K, Utsunomiya A, Tobinai K et al. Phase I study of KW-0761, a defucosylated humanized anti-CCR4 antibody, in relapsed patients with adult T-cell leukemia-lymphoma and peripheral T-cell lymphoma. J Clin Oncol 2010; 28: 1591-8.
12. Hermine O, Allard I, Levy V, Arnulf B, Gessain A, Bazarbachi A. A prospective phase II clinical trial with the use of zidovudine and interferon-alpha in the acute and lymphoma forms of adult T-cell leukemia/lymphoma. Hematol J 2002; 3: 276-82.
13. Yoshida M. Multiple viral strategies of HTLV-1 for dysregulation of cell growth control. Annu Rev Immunol 2001; 19: 475-96.
14. Grassmann R, Aboud M, Jeang KT. Molecular mechanisms of cellular transformation by HTLV-1 Tax. Oncogene 2005; 24: 5976-85.
15. Jeang KT, Giam CZ, Majone F, Aboud M. Life, death, and tax: role of HTLV-I oncoprotein in genetic instability and cellular transformation. J Biol Chem 2004; 279: 31991-4.
16. Matsuoka M, Jeang KT. Human T-cell leukaemia virus type 1 (HTLV-1) infectivity and cellular transformation. Nat Rev Cancer 2007; 7: 270-80.
17. Kannagi M, Sugamura K, Kinoshita K, Uchino H, Hinuma Y. Specific cytolysis of fresh tumor cells by an autologous killer T cell line derived from an adult T cell leukemia/lymphoma patient. J Immunol 1984; 133: 1037-41.
18. Jacobson S, Shida H, McFarlin DE, Fauci AS, Koenig S. Circulating CD8+ cytotoxic T lymphocytes specific for HTLV-I pX in patients with HTLV-I associated neurological disease. Nature 1990; 348: 245-8.
19. Arnulf B, Thorel M, Poirot Y et al. Loss of the ex vivo but not the reinducible CD8+ T-cell response to Tax in human T-cell leukemia virus type 1-infected patients with adult T-cell leukemia/lymphoma. Leukemia 2004; 18: 126-32.
20. Kato H, Koya Y, Ohashi T et al. Oral administration of human T-cell leukemia virus type 1 induces immune unresponsiveness with persistent infection in adult rats. J Virol 1998; 72: 7289-93.
21. Hasegawa A, Ohashi T, Hanabuchi S et al. Expansion of human T-cell leukemia virus type 1 (HTLV-1) reservoir in orally infected rats: inverse correlation with HTLV-1-specific cellular immune response. J Virol 2003; 77: 2956-63.
22. Kannagi M, Harashima N, Kurihara K et al. Tumor immunity against adult T-cell leukemia. Cancer Sci 2005; 96: 249-55.
23. Jacobson S. Human T lymphotropic virus, type-I myelopathy: an immunopathologically mediated chronic progressive disease of the central nervous system. Curr Opin Neurol 1995; 8: 179-83.
24. Osame M. Pathological mechanisms of human T-cell lymphotropic virus type I-associated myelopathy (HAM/TSP). J Neurovirol 2002; 8: 359-64.
25. Jeffery KJ, Usuku K, Hall SE et al. HLA alleles determine human T-lymphotropic virus-I (HTLV-I) proviral load and the risk of HTLV-I-associated myelopathy. Proc Natl Acad Sci USA 1999; 96: 3848-53.
26. Bangham CR, Osame M. Cellular immune response to HTLV-1. Oncogene 2005; 24: 6035-46.
27. Akimoto M, Kozako T, Sawada T et al. Anti-HTLV-1 tax antibody and tax-specific cytotoxic T lymphocyte are associated with a reduction in HTLV-1 proviral load in asymptomatic carriers. J Med Virol 2007; 79: 977-86.
28. Kubota R, Kawanishi T, Matsubara H, Manns A, Jacobson S. HTLV-I specific IFN-gamma+ CD8+ lymphocytes correlate with the proviral load in peripheral blood of infected individuals. J Neuroimmunol 2000; 102: 208-15.
29. Kinoshita T, Shimoyama M, Tobinai K et al. Detection of mRNA for the tax1/rex1 gene of human T-cell leukemia virus type I in fresh peripheral blood mononuclear cells of adult T-cell leukemia patients and viral carriers by using the polymerase chain reaction. Proc Natl Acad Sci USA 1989; 86: 5620-4.
30. Fujisawa J, Seiki M, Kiyokawa T, Yoshida M. Functional activation of the long terminal repeat of human T-cell leukemia virus type I by a trans-acting factor. Proc Natl Acad Sci USA 1985; 82: 2277-81.
31. Newbound GC, O'Rourke JP, Collins ND, Andrews JM, DeWille J, Lairmore MD. Repression of tax-mediated human t-lymphotropic virus type 1 transcription by inducible cAMP early repressor (ICER) protein in peripheral blood mononuclear cells. J Med Virol 2000; 62: 286-92.
32. Jiang S, Inada T, Tanaka M, Furuta RA, Shingu K, Fujisawa J. Involvement of TORC2, a CREB co-activator, in the in vivo-specific transcriptional control of HTLV-1. Retrovirology 2009; 6: 73.
33. 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 USA 2006; 103: 720-5.
34. Kinpara S, Hasegawa A, Utsunomiya A et al. Stromal cell-mediated suppression of human T-cell leukemia virus type 1 expression in vitro and in vivo by type I interferon. J Virol 2009; 83: 5101-8.
35. Kannagi M, Sugamura K, Sato H, Okochi K, Uchino H, Hinuma Y. Establishment of human cytotoxic T cell lines specific for human adult T cell leukemia virus-bearing cells. J Immunol 1983; 130: 2942-6.
36. Parker CE, Daenke S, Nightingale S, Bangham CR. Activated, HTLV-1-specific cytotoxic T-lymphocytes are found in healthy seropositives as well as in patients with tropical spastic paraparesis. Virology 1992; 188: 628-36.
37. Kannagi M, Harada S, Maruyama I et al. 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 1991; 3: 761-7.
38. Goon PK, Igakura T, Hanon E et al. Human T cell lymphotropic virus type I (HTLV-I)-specific CD4+ T cells: immunodominance hierarchy and preferential infection with HTLV-I. J Immunol 2004; 172: 1735-43.
39. Elovaara I, Koenig S, Brewah AY, Woods RM, Lehky T, Jacobson S. High human T cell lymphotropic virus type 1 (HTLV-1)-specific precursor cytotoxic T lymphocyte frequencies in patients with HTLV-1-associated neurological disease. J Exp Med 1993; 177: 1567-73.
40. Pique C, Ureta-Vidal A, Gessain A et al. Evidence for the chronic in vivo production of human T cell leukemia virus type I Rof and Tof proteins from cytotoxic T lymphocytes directed against viral peptides. J Exp Med 2000; 191: 567-72.
41. Macnamara A, Rowan A, Hilburn S et al. HLA class I binding of HBZ determines outcome in HTLV-1 infection. PLoS Pathog 2010; 6: e1001117.
42. Asquith B, Mosley AJ, Barfield A et al. A functional CD8+ cell assay reveals individual variation in CD8+ cell antiviral efficacy and explains differences in human T-lymphotropic virus type 1 proviral load. J Gen Virol 2005; 86: 1515-23.
43. Komori K, Hasegawa A, Kurihara K et al. Reduction of human T-cell leukemia virus type 1 (HTLV-1) proviral loads in rats orally infected with HTLV-1 by reimmunization with HTLV-1-infected cells. J Virol 2006; 80: 7375-81.
44. Ohashi T, Hanabuchi S, Kato H et al. Prevention of adult T-cell leukemia-like lymphoproliferative disease in rats by adoptively transferred T cells from a donor immunized with human T-cell leukemia virus type 1 Tax-coding DNA vaccine. J Virol 2000; 74: 9610-6.
45. Hanabuchi S, Ohashi T, Koya Y et al. Regression of human T-cell leukemia virus type I (HTLV-I)-associated lymphomas in a rat model: peptide-induced T-cell immunity. J Natl Cancer Inst 2001; 93: 1775-83.
46. Kawano N, Shimoda K, Ishikawa F et al. Adult T-cell leukemia development from a human T-cell leukemia virus type I carrier after a living-donor liver transplantation. Transplantation 2006; 82: 840-3.
47. Suzuki S, Uozumi K, Maeda M et al. Adult T-cell leukemia in a liver transplant recipient that did not progress after onset of graft rejection. Int J Hematol 2006; 83: 429-32.
48. Harashima N, Kurihara K, Utsunomiya A et al. Graft-versus-Tax response in adult T-cell leukemia patients after hematopoietic stem cell transplantation. Cancer Res 2004; 64: 391-9.
49. Kaplan JE, Osame M, Kubota H et al. The risk of development of HTLV-I-associated myelopathy/tropical spastic paraparesis among persons infected with HTLV-I. J Acquir Immune Defic Syndr 1990; 3: 1096-101.
50. Hisada M, Okayama A, Shioiri S, Spiegelman DL, Stuver SO, Mueller NE. Risk factors for adult T-cell leukemia among carriers of human T-lymphotropic virus type I. Blood 1998; 92: 3557-61.
51. Iwanaga M, Watanabe T, Utsunomiya A et al. Human T-cell leukemia virus type I (HTLV-1) proviral load and disease progression in asymptomatic HTLV-1 carriers: a nationwide prospective study in Japan. Blood 2010; 116: 1211-9.
52. Nagai M, Usuku K, Matsumoto W et al. Analysis of HTLV-I proviral load in 202 HAM/TSP patients and 243 asymptomatic HTLV-I carriers: high proviral load strongly predisposes to HAM/TSP. J Neurovirol 1998; 4: 586-93.
53. Shimizu Y, Takamori A, Utsunomiya A et al. Impaired Tax-specific T-cell responses with insufficient control of HTLV-1 in a subgroup of individuals at asymptomatic and smoldering stages. Cancer Sci 2009; 100: 481-9.
54. Wodarz D, Nowak MA, Bangham CR. The dynamics of HTLV-I and the CTL response. Immunol Today 1999; 20: 220-7.
55. Toulza F, Heaps A, Tanaka Y, Taylor GP, Bangham CR. High frequency of CD4+FoxP3+ cells in HTLV-1 infection: inverse correlation with HTLV-1-specific CTL response. Blood 2008; 111: 5047-53.
56. Azakami K, Sato T, Araya N et al. Severe loss of invariant NKT cells exhibiting anti-HTLV-1 activity in patients with HTLV-1-associated disorders. Blood 2009; 114: 3208-15.
57. Harashima N, Tanosaki R, Shimizu Y et al. Identification of two new HLA-A*1101-restricted tax epitopes recognized by cytotoxic T lymphocytes in an adult T-cell leukemia patient after hematopoietic stem cell transplantation. J Virol 2005; 79: 10088-92.
58. Yamano Y, Nagai M, Brennan M et al. Correlation of human T-cell lymphotropic virus type 1 (HTLV-1) mRNA with proviral DNA load, virus-specific CD8(+) T cells, and disease severity in HTLV-1-associated myelopathy (HAM/TSP). Blood 2002; 99: 88-94.
59. Hasui K, Utsunomiya A, Izumo S et al. An immunohistochemical analysis of peripheral blood tissue specimens from leukemia cells: Leukemic cells of Adult T-cell leukemia/lymphoma express p40Tax protein of human T-cell lymphotropic virus type 1 when entering reproliferation. Acta Histochem Cytochem 2003; 36: 345-52.
60. Hinuma Y, Gotoh Y, Sugamura K et al. A retrovirus associated with human adult T-cell leukemia: in vitro activation. Gann 1982; 73: 341-4.
61. Umadome H, Uchiyama T, Hori T et al. Close association between interleukin 2 receptor mRNA expression and human T cell leukemia/lymphoma virus type I viral RNA expression in short-term cultured leukemic cells from adult T cell leukemia patients. J Clin Invest 1988; 81: 52-61.
62. Kurihara K, Harashima N, Hanabuchi S et al. Potential immunogenicity of adult T cell leukemia cells in vivo. Int J Cancer 2005; 114: 257-67.
63. Takeda S, Maeda M, Morikawa S et al. Genetic and epigenetic inactivation of tax gene in adult T-cell leukemia cells. Int J Cancer 2004; 109: 559-67.
64. Tamiya S, Matsuoka M, Etoh K et al. Two types of defective human T-lymphotropic virus type I provirus in adult T-cell leukemia. Blood 1996; 88: 3065-73.
65. Koiwa T, Hamano-Usami A, Ishida T et al. 5'-long terminal repeat-selective CpG methylation of latent human T-cell leukemia virus type 1 provirus in vitro and in vivo. J Virol 2002; 76: 9389-97.
66. Hanon E, Hall S, Taylor GP et al. 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 2000; 95: 1386-92.
67. Sodroski J, Rosen C, Goh WC, Haseltine W. A transcriptional activator protein encoded by the x-lor region of the human T-cell leukemia virus. Science 1985; 228: 1430-4.
68. Nagai K, Jinnai I, Hata T et al. Adhesion-dependent growth of primary adult T cell leukemia cells with down-regulation of HTLV-I p40Tax protein: a novel in vitro model of the growth of acute ATL cells. Int J Hematol 2008; 88: 551-64.
69. Hishizawa M, Imada K, Kitawaki T, Ueda M, Kadowaki N, Uchiyama T. 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 2004; 125: 568-75.
70. Jones KS, Petrow-Sadowski C, Huang YK, Bertolette DC, Ruscetti FW. Cell-free HTLV-1 infects dendritic cells leading to transmission and transformation of CD4(+) T cells. Nat Med 2008; 14: 429-36.
71. Colisson R, Barblu L, Gras C et al. Free HTLV-1 induces TLR7-dependent innate immune response and TRAIL relocalization in killer plasmacytoid dendritic cells. Blood 2010; 115: 2177-85.
72. Miyatake Y, Ikeda H, Ishizu A et al. Role of neuronal interferon-gamma in the development of myelopathy in rats infected with human T-cell leukemia virus type 1. Am J Pathol 2006; 169: 189-99.
73. Iwakura Y, Tosu M, Yoshida E et al. Induction of inflammatory arthropathy resembling rheumatoid arthritis in mice transgenic for HTLV-I. Science 1991; 253: 1026-8.
74. Medzhitov R, Janeway CA Jr. Innate immunity: impact on the adaptive immune response. Curr Opin Immunol 1997; 9: 4-9.
75. Boasso A, Shearer GM. Chronic innate immune activation as a cause of HIV-1 immunopathogenesis. Clin Immunol 2008; 126: 235-42.
76. Nomura M, Ohashi T, Nishikawa K et al. Repression of tax expression is associated both with resistance of human T-cell leukemia virus type 1-infected T cells to killing by tax-specific cytotoxic T lymphocytes and with impaired tumorigenicity in a rat model. J Virol 2004; 78: 3827-36.
77. Meekings KN, Leipzig J, Bushman FD, Taylor GP, Bangham CR. HTLV-1 integration into transcriptionally active genomic regions is associated with proviral expression and with HAM/TSP. PLoS Pathog 2008; 4: e1000027.
78. Tomaru U, Ikeda H, Ohya O et al. Human T lymphocyte virus type I-induced myeloneuropathy in rats: implication of local activation of the pX and tumor necrosis factor-alpha genes in pathogenesis. J Infect Dis 1996; 174: 318-23.
79. Oliere S, Hernandez E, Lezin A et al. HTLV-1 Evades Type I Interferon Antiviral Signaling by Inducing the Suppressor of Cytokine Signaling 1 (SOCS1). PLoS Pathog 2010; 6: e1001177.