Regulatory T cells in virus infections

Immunological Reviews

Volumn 212, Issue , 2006, Pages 272-286

  Rouse, Barry T ^a   Sarangi, Pranita P ^a   Suvas, Susmit ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Herpes simplex virus; Human immunodeficiency virus; Regulatory T cells

Indexed keywords

ANTIRETROVIRUS AGENT; INTERLEUKIN 10; MONOCLONAL ANTIBODY CD3; TRANSCRIPTION FACTOR FOXP3; VIRUS VACCINE;

CD4+ CD25+ T LYMPHOCYTE; CELL FUNCTION; DISEASE SEVERITY; EYE INJURY; HEPATITIS B VIRUS; HEPATITIS C; HEPATITIS C VIRUS; HERPES SIMPLEX VIRUS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE DYSREGULATION; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOPATHOLOGY; IMMUNOREACTIVITY; INFECTION CONTROL; INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; RETROVIRUS; RETROVIRUS INFECTION; REVIEW; TISSUE INJURY; VIRUS IMMUNITY; VIRUS INFECTION;

ANIMALS; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; MICE; T-LYMPHOCYTES, REGULATORY; VIRUS DISEASES; VIRUSES;

EID: 33746383248     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.0105-2896.2006.00412.x     Document Type: Review

References (90)

1. Gershon RK, Kondo K. Gell interactions in the induction of tolerance: the role of thymic lymphocytes. Immunology 1970;18:723-737.
2. Horohov DW, Moore RN, Rouse BT. Regulation of herpes simplex virus-specific lymphoproliferation by suppressor cells. J Virol 1985;56:1-6.
3. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 1995;155:1151-1164.
4. Thornton AM, Shevach EM. CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J Exp Med 1998;188:287-296.
5. Maloy KJ, Powrie F. Regulatory T cells in the control of immune pathology. Nat Immunol 2001;2:816-822.
6. Sakaguchi S. Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat Immunol 2005;6:345-352.
7. Sakaguchi S. Naturally arising CD4+ regulatory t cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 2004;22:531-562.
8. Belkaid Y, Piccirillo CA, Mendez S, Shevach EM, Sacks DL. CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 2002;420:502-507.
9. Suvas S, Kumaraguru U, Pack CD, Lee S, Rouse BT. CD4+CD25+ T cells regulate virus-specific primary and memory CD8+ T cell responses. J Exp Med 2003;198:889-901.
10. Groux H, et al. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 1997;389:737-742.
11. McGuirk P, McCann C, Mills KH. Pathogenspecific T regulatory 1 cells induced in the respiratory tract by a bacterial molecule that stimulates interleukin 10 production by dendritic cells: a novel strategy for evasion of protective T helper type 1 responses by Bordetella pertussis. J Exp Med 2002;195:221-231.
12. Lowenthal JW, Corthesy P, Tougne C, Lees R, MacDonald HR, Nabholz M. High and low affinity IL 2 receptors: analysis by IL 2 dissociation rate and reactivity with monoclonal anti-receptor antibody PC61. J Immunol 1985;135:3988-3994.
13. Suvas S, Azkur AK, Kim BS, Kumaraguru U, Rouse BT. CD4+CD25+ regulatory T cells control the severity of viral immunoinflammatory lesions. J Immunol 2004;172:4123-4132.
14. Lim HW, Hillsamer P, Banham AH, Kim CH. Cutting edge: Direct suppression of B cells by CD4+ CD25+ regulatory T cells. J Immunol 2005;175:4180-4183.
15. Lim HW, Hillsamer P, Kim CH. Regulatory T cells can migrate to follicles upon T cell activation and suppress GC-Th cells and GC-Th cell-driven B cell responses. J Clin Invest 2004;114:1640-1649.
16. Toka FN, Suvas S, Rouse BT. CD4+ CD25+ T cells regulate vaccine-generated primary and memory CD8+ T-cell responses against herpes simplex virus type 1. J Virol 2004;78:13082-13089.
17. Rehermann B, et al. Differential cytotoxic T-lymphocyte responsiveness to the hepatitis B and C viruses in chronically infected patients. J Virol 1996;70:7092-7102.
18. Thimme R, Oldach D, Chang KM, Steiger C, Ray SC, Chisari FV. Determinants of viral clearance and persistence during acute hepatitis C virus infection. J Exp Med 2001;194:1395-1406.
19. MacDonald AJ, et al. CD4 T helper type 1 and regulatory T cells induced against the same epitopes on the core protein in hepatitis C virus-infected persons. J Infect Dis 2002;185:720-727.
20. O'Garra A, Vieira P. Regulatory T cells and mechanisms of immune system control. Nat Med 2004;10:801-805.
21. Sugimoto K, Ikeda F, Stadanlick J, Nunes FA, Alter HJ, Chang KM. Suppression of HCV-specific T cells without differential hierarchy demonstrated ex vivo in persistent HCV infection. Hepatology 2003;38:1437-1448.
22. Boettler T, et al. T cells with a CD4+CD25+ regulatory phenotype suppress in vitro proliferation of virus-specific CD8+ T cells during chronic hepatitis C virus infection. J Virol 2005;79:7860-7867.
23. Rushbrook SM, et al. Regulatory T cells suppress in vitro proliferation of virus-specific CD8+ T cells during persistent hepatitis C virus infection. J Virol 2005;79:7852-7859.
24. Accapezzato D, et al. Hepatic expansion of a virus-specific regulatory CD8(+) T cell population in chronic hepatitis C virus infection. J Clin Invest 2004;113:963-972.
25. Bowen DG, Walker CM. Mutational escape from CD8+ T cell immunity: HCV evolution, from chimpanzees to man. J Exp Med 2005;201:1709-1714.
26. Franzese O, et al. Modulation of the CD8+-T-cell response by CD4+ CD25+ regulatory T cells in patients with hepatitis B virus infection. J Virol 2005;79:3322-3328.
27. Thimme R, et al. CD8(+) T cells mediate viral clearance and disease pathogenesis during acute hepatitis B virus infection. J Virol 2003;77:68-76.
28. Miedema F, et al. Immunological abnormalities in human immunodeficiency virus (HIV)-infected asymptomatic homosexual men. HIV affects the immune system before CD4+ T helper cell depletion occurs. J Clin Invest 1988;82:1908-1914.
29. Douek DC, et al. HIV preferentially infects HIV-specific CD4+ T cells. Nature 2002;417:95-98.
30. Weiss L, Donkova-Petrini V, Caecavelli L, Balbo M, Carbonneil C, Levy Y. Human immunodeficiency virus-driven expansion of CD4+CD25+ regulatory T cells, which suppress HIV-specific CD4 T-cell responses in HIV-infected patients. Blood 2004;104:3249-3256.
31. Kinter AL, et al. CD25(+)CD4(+) regulatory T cells from the peripheral blood of asymptomatic HIV-infected individuals regulate CD4(+) and CD8(+) HIV-specific T cell immune responses in vitro and are associated with favorable clinical markers of disease status. J Exp Med 2004;200:331-343.
32. Oswald-Richter K, et al. HIV infection of naturally occurring and genetically reprogrammed human regulatory T-cells. PLoS Biol 2004;2:E198.
33. Sereti I, et al. In vivo expansion of CD4CD45RO-CD25 T cells expressing foxP3 in IL-2-treated HIV-infected patients. J Clin Invest 2005;115:1839-1847.
34. Andersson J, et al. The prevalence of regulatory T cells in lymphoid tissue is correlated with viral load in HIV-infected patients. J Immunol 2005;174:3143-3147.
35. Weiss L, et al. Restoration of normal interleukin-2 production by CD4+ T cells of human immunodeficiency virus-infected patients after 9 months of highly active antiretro viral therapy. J Infect Dis 1999;180:1057-1063.
36. Aandahl EM, Michaelsson J, Moretto WJ, Hecht FM, Nixon DF. Human CD4+ CD25+ regulatory T cells control T-cell responses to human immunodeficiency virus and cytomegalovirus antigens. J Virol 2004;78:2454-2459.
37. Eggena MP, et al. Depletion of regulatory T cells in HIV infection is associated with immune activation. J Immunol 2005;174:4407-4414.
38. Tsunemi S, et al. Relationship of CD4+CD25+ regulatory T cells to immune status in HIV-infected patients. AIDS 2005;19:879-886.
39. Suffia IJ, Reckling SK, Piccirillo CA, Goldszmid RS, Beilkaid Y. Infected site-restricted Foxp3+ natural regulatory T cells are specific for microbial antigens. J Exp Med (InPress)
40. Iwashiro M, Messer RJ, Peterson KE, Stromnes IM, Sugie T, Hasenkrug KJ. Immunosuppression by CD4+ regulatory T cells induced by chronic retroviral infection. Proc Nad Acad Sci USA 2001;98:9226-9230.
41. Dittmer U, et al. Functional impairment of CD8(+) T cells by regulatory T cells during persistent retroviral infection. Immunity 2004;20:293-303.
42. Beilharz MW, et al. Timed ablation of regulatory CD4+ T cells can prevent murine AIDS progression. J Immunol 2004;172:4917-4925.
43. Uchiyama T. Human T cell leukemia virus type I (HTLV-I) and human diseases. Annu Rev Immunol 1997;15:15-37.
44. Nagai M, Brennan MB, Sakai JA, Mora CA, Jacobson S. CD8(+) T cells are an in vivo reservoir for human T-cell lymphotropic virus type I. Blood 2001;98:1858-1861.
45. Yamano Y, et al. Increased expression of human T lymphocyte virus type I (HTLV-I) Taxi 1-19 peptide-human histocompatibility leukocyte antigen A*201 complexes on CD4+ CD25+ T Cells detected by peptide-specific, major histocompatibility complex-restricted antibodies in patients with HTLV-I-associated neurologic disease. J Exp Med 2004;199:1367-1377.
46. Yamano Y, et al. Virus-induced dysfunction of CD4+CD25+ T cells in patients with HTLV-I-associated neuroimmunological disease. J Clin Invest 2005;115: 1361-1368.
47. Haeryfar SM, DiPaolo RJ, Tscharke DC, Bennink JR, Yewdell JW. Regulatory T cells suppress CD8+ T cell responses induced by direct priming and cross-priming and moderate immunodominance disparities. J Immunol 2005;174:3344-3351.
48. Marshall NA, Vickers MA, Barker RN. Regulatory T cells secreting IL-10 dominate the immune response to EBV latent membrane protein 1. J Immunol 2003;170:6183-6189
49. Belkaid Y, Rouse BT. Natural regulatory T cells in infectious disease. Nat Immunol 2005;6:353-360.
50. Kornfeld C, et al. Antiinflammatory profiles during primary SIV infection in African green monkeys are associated with protection against AIDS. J Clin Invest 2005;115:1082-1091.
51. Deshpande S, Banerjee K, Biswas PS, Rouse BT. Herpetic eye disease: immunopathogenesis and therapeutic measures. Expert Rev Mol Med 2004;2004:1-14.
52. Iellem A, et al. Unique chemotactic response profile and specific expression of chemokine receptors CCR4 and CCR8 by CD4(+)CD25(+) regulatory T cells. J Exp Med 2001;194:847-853.
53. Suvas S, Kim B, Rouse BT. Homeostatic expansion of CD4+ T cells upregulates α4β1 and exacerbates HSV induced corneal immunopathology. Submitted.
54. Sarween N, Chodos A, Raykundalia C, Khan M, Abbas AK, Walker LS. CD4+CD25+ cells controlling a pathogenic CD4 response inhibit cytokine differentiation, CXCR-3 expression, and tissue invasion. J Immunol 2004;173:2942-2951.
55. + T cells in the latently infected trigeminal ganglia. J Immunol 2006;176:1703-1711.
56. Fallarino F, et al. Modulation of tryptophan catabolism by regulatory T cells. Nat Immunol 2003;4:1206-1212.
57. Mellor AL, Munn DH. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat Rev Immunol 2004;4:762-774.
58. Khanna KM, Bonneau RH, Kinchington PR, Hendricks RL. Herpes simplex virus-specific memory CD8+ T cells are selectively activated and retained in latently infected sensory ganglia. Immunity 2003;18:593-603.
59. Shevach EM. CD4+ CD25+ suppressor T cells: more questions than answers. Nat Rev Immunol 2002;2:389-400.
60. Rouse BT, Deshpande S. Viruses and autoimmunity: an affair but not a marriage contract. Rev Med Virol 2002;12:107-113.
61. Zhao ZS, Granucci F, Yeh L, Schaffer PA, Cantor H. Molecular mimicry by herpes simplex virus-type 1: autoimmune disease after viral infection. Science 1998;279:1344-1347.
62. Deshpande SP, et al. Herpes simplex virus-induced keratitis: evaluation of the role of molecular mimicry in lesion pathogenesis. J Virol 2001;75:3077-3088.
63. Caramalho I, Lopes-Carvalho T, Ostler D, Zelenay S, Haury M, Demengeot J. Regulatory T cells selectively express toll-like receptors and are activated by lipopolysaccharide. J Exp Med 2003;197:403-411.
64. Peng G, et al. Toll-like receptor 8-mediated reversal of CD4+ regulatory T cell function. Science 2005;309:1380-1384.
65. Kurt-Jones EA, et al. Herpes simplex virus 1 interaction with Toll-like receptor 2 contributes to lethal encephalitis. Proc Natl Acad Sci USA 2004;101:1315-1320.
66. Kurt-Jones EA, et al. Pattern recognition receptors TLR4 and CD 14 mediate response to respiratory syncytial virus. Nat Immunol 2000;1:398-401.
67. Compton T, et al. Human cytomegalovirus activates inflammatory cytokine responses via CD14 and Toll-like receptor 2. J Virol 2003;77:4588-4596.
68. Krug A, Luker GD, Barchet W, Leib DA, Akira S, Colonna M. Herpes simplex virus type 1 activates murine natural interferon-producing cells through toll-like receptor 9. Blood 2004;103:1433-1437.
69. Dolganiuc A, et al. Hepatitis C core and non-structural 3 proteins trigger toll-like receptor 2-mediated pathways and inflammatory activation. Gastroenterology 2004;127:1513-1524.
70. Asea A, et al. Novel signal transduction pathway utilized by extracellular HSP70: role of toll-like receptor (TLR) 2 and TLR4. J Biol Chem 2002;277:15028-15034.
71. Biragyn A, et al. Toll-like receptor 4-dependent activation of dendritic cells by beta-defensin 2. Science 2002;298:1025-1029.
72. Biswas PS, Rouse BT. Early events in HSV keratitis-setting the stage for a blinding disease. Microbes Infect 2005;7:799-810.
73. Chen W, et al. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med 2003;198:1875-1886.
74. Namba K, Kitaichi N, Nishida T, Taylor AW. Induction of regulatory T cells by the immunomodulating cytokines alphamelanocyte-stimulating hormone and transforming growth factor-beta2. J Leukoc Biol 2002;72:946-952.
75. Reed SG. TGF-beta in infections and infectious diseases. Microbes Infect 1999;1:1313-1325.
76. Paradis V, et al. Histological features predictive of liver fibrosis in chronic hepatitis C infection. J Clin Pathol 1996;49:998-1004.
77. Lotz M, Seth P. TGF beta and HIV infection. Ann NY Acad Sci 1993;685:501-511.
78. Baratelli F, et al. Prostaglandin E2 induces FOXP3 gene expression and T regulatory cell function in human CD4+ T cells. J Immunol 2005;175:1483-1490.
79. Apostolou I, von Boehmer H. In vivo instruction of suppressor commitment in naive T cells. J Exp Med 2004;199:1401-1408.
80. Kretschmer K, Apostolou I, Hawiger D, Khazaie K, Nussenzweig MC, von Boehmer H. Inducing and expanding regulatory T cell populations by foreign antigen. Nat Immunol 2005;6:1219-1227.
81. Pasare C, Medzhitov R. Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells. Science 2003; 299:1033-1036.
82. Yang Y, Huang CT, Huang X, Pardoll DM. Persistent Toll-like receptor signals are required for reversal of regulatory T cell-mediated CD8 tolerance. Nat Immunol 2004;5:508-515.
83. King IL, Segal BM. Cutting edge: IL-12 induces CD4+CD25- T cell activation in the presence of T regulatory cells. J Immunol 2005;175:641-645.
84. Belghith M, Bluestone JA, Barriot S, Megret J, Bach JF, Chatenoud L. TGF-beta-dependent mechanisms mediate restoration of self-tolerance induced by antibodies to CD3 in overt autoimmune diabetes. Nat Med 2003;9:1202-1208.
85. Shimizu J, Yamazaki S, Takahashi T, Ishida Y, Sakaguchi S. Stimulation of CD25(+)CD4(+) regulatory T cells through GITR breaks immunological self-tolerance. Nat Immunol 2002;3:135-142.
86. Stephens GL, et al. Engagement of glucocorticoid-induced TNFR family-related receptor on effector T cells by its ligand mediates resistance to suppression by CD4+CD25+ T cells. J Immunol 2004;173:5008-5020.
87. He H, Messer RJ, Sakaguchi S, Yang G, Robertson SJ, Hasenkrug KJ. Reduction of retrovirus-induced immunosuppression by in vivo modulation of T cells during acute infection. J Virol 2004;78:11641-11647.
88. Moore AC, Gallimore A, Draper SJ, Watkins KR, Gilbert SC, Hill AV. Anti-CD25 antibody enhancement of vaccine-induced immunogenicity: increased durable cellular immunity with reduced immunodominance. J Immunol 2005;175:7264-7273.
89. van der Vliet HJ, et al. Selective decrease in circulating V alpha 24+V beta 11+ NKT cells during HIV type 1 infection. J Immunol 2002;168:1490-1495.
90. Garba ML, Pilcher CD, Bingham AL, Eron J, Frelinger JA. HIV antigens can induce TGF-beta(1)-producing immunoregulatory CD8+ T cells. J Immunol 2002;168:2247-2254.