Human CD4 and CD8 regulatory T cells in infectious diseases and vaccination

Human Immunology

Volumn 69, Issue 11, 2008, Pages 760-770

  Joosten, Simone A ^a   Ottenhoff, Tom H M ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

BCG; CD8; Infectious diseases; Mycobacaterium tuberculosis; Regulatory T cells; Vaccination

Indexed keywords

BCG VACCINE; CHEMOKINE RECEPTOR CCR5 ANTAGONIST; CYTOKINE; MACROPHAGE INFLAMMATORY PROTEIN 1BETA;

ADOPTIVE TRANSFER; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; ARTICLE; AUTOIMMUNE DISEASE; BACTERIAL INFECTION; BCG VACCINATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; HELICOBACTER INFECTION; HEPATITIS B; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INFECTION; INFLAMMATION; INFLAMMATORY DISEASE; LEISHMANIASIS; LEPROSY; LUNG TUBERCULOSIS; MALARIA; NONHUMAN; ORGAN TRANSPLANTATION; PERSISTENT INFECTION; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TRANSPLANTATION TOLERANCE; TUMOR IMMUNOLOGY; VACCINATION; VIRUS INFECTION;

ANTIGENS, BACTERIAL; ANTIGENS, VIRAL; BACTERIAL VACCINES; CD8-POSITIVE T-LYMPHOCYTES; HUMANS; MYCOBACTERIUM; MYCOBACTERIUM INFECTIONS; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY; VACCINATION; VIRAL VACCINES; VIRUS DISEASES; VIRUSES;

EID: 57649090701     PISSN: 01988859     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.humimm.2008.07.017     Document Type: Article

References (76)

1. Mills K.H. Regulatory T cells: Friend or foe in immunity to infection?. Nat Rev Immunol 4 (2004) 841-855
2. Tang Q., and Bluestone J.A. The Foxp3+ regulatory T cell: A jack of all trades, master of regulation. Nat Immunol 9 (2008) 239-244
3. Belkaid Y. Regulatory T cells and infection: A dangerous necessity. Nat Rev Immunol 7 (2007) 875-888
4. Joosten S.A., van Meijgaarden K.E., Savage N.D., de Boer T., Triebel F., van der Wal A., et al. Identification of a human CD8+ regulatory T cell subset that mediates suppression through the chemokine CC chemokine ligand 4. Proc Natl Acad Sci U S A 104 (2007) 8029-8034
5. Elrefaei M., Ventura F.L., Baker C.A., Clark R., Bangsberg D.R., and Cao H. HIV-specific IL-10-positive CD8+ T cells suppress cytolysis and IL-2 production by CD8+ T cells. J Immunol 178 (2007) 3265-3271
6. Bacchetta R., Passerini L., Gambineri E., Dai M., Allan S.E., Perroni L., et al. Defective regulatory and effector T cell functions in patients with FOXP3 mutations. J Clin Invest 116 (2006) 1713-1722
7. Fontenot J.D., Gavin M.A., and Rudensky A.Y. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 4 (2003) 330-336
8. Morgan M.E., van Bilsen J.H., Bakker A.M., Heemskerk B., Schilham M.W., Hartgers F.C., et al. Expression of FOXP3 mRNA is not confined to CD4+CD25+ T regulatory cells in humans. Hum Immunol 66 (2005) 13-20
9. Wang J., Ioan-Facsinay A., van der Voort E.I., Huizinga T.W., and Toes R.E. Transient expression of FOXP3 in human activated nonregulatory CD4+ T cells. Eur J Immunol 37 (2007) 129-138
10. Zelenay S., Lopes-Carvalho T., Caramalho I., Moraes-Fontes M.F., Rebelo M., and Demengeot J. Foxp3+ CD25- CD4 T cells constitute a reservoir of committed regulatory cells that regain CD25 expression upon homeostatic expansion. Proc Natl Acad Sci U S A 102 (2005) 4091-4096
11. Ottenhoff T.H., Elferink D.G., Klatser P.R., and de Vries R.R. Cloned suppressor T cells from a lepromatous leprosy patient suppress Mycobacterium leprae reactive helper T cells. Nature 322 (1986) 462-464
12. Modlin R.L., Kato H., Mehra V., Nelson E.E., Fan X.D., Rea T.H., et al. Genetically restricted suppressor T-cell clones derived from lepromatous leprosy lesions. Nature 322 (1986) 459-461
13. Cosmi L., Liotta F., Lazzeri E., Francalanci M., Angeli R., Mazzinghi B., et al. Human CD8+CD25+ thymocytes share phenotypic and functional features with CD4+CD25+ regulatory thymocytes. Blood 102 (2003) 4107-4114
14. Uss E., Rowshani A.T., Hooibrink B., Lardy N.M., van Lier R.A., and ten Berge I.J. CD103 is a marker for alloantigen-induced regulatory CD8+ T cells. J Immunol 177 (2006) 2775-2783
15. Colovai A.I., Mirza M., Vlad G., Wang S., Ho E., Cortesini R., and Suciu-Foca N. Regulatory CD8+CD28- T cells in heart transplant recipients. Hum Immunol 64 (2003) 31-37
16. Brimnes J., Allez M., Dotan I., Shao L., Nakazawa A., and Mayer L. Defects in CD8+ regulatory T cells in the lamina propria of patients with inflammatory bowel disease. J Immunol 174 (2005) 5814-5822
17. Jarvis L.B., Matyszak M.K., Duggleby R.C., Goodall J.C., Hall F.C., and Gaston J.S. Autoreactive human peripheral blood CD8+ T cells with a regulatory phenotype and function. Eur J Immunol 35 (2005) 2896-2908
18. Bisikirska B., Colgan J., Luban J., Bluestone J.A., and Herold K.C. TCR stimulation with modified anti-CD3 mAb expands CD8+ T cell population and induces CD8+CD25+ Tregs. J Clin Invest 115 (2005) 2904-2913
19. Tennakoon D.K., Mehta R.S., Ortega S.B., Bhoj V., Racke M.K., and Karandikar N.J. Therapeutic induction of regulatory, cytotoxic CD8+ T cells in multiple sclerosis. J Immunol 176 (2006) 7119-7129
20. Chang C.C., Ciubotariu R., Manavalan J.S., Yuan J., Colovai A.I., Piazza F., et al. Tolerization of dendritic cells by T(S) cells: The crucial role of inhibitory receptors ILT3 and ILT4. Nat Immunol 3 (2002) 237-243
21. Cai J., Lee J., Jankowska-Gan E., Derks R., Pool J., Mutis T., Goulmy E., and Burlingham W.J. Minor H antigen HA-1-specific regulator and effector CD8+ T cells, and HA-1 microchimerism, in allograft tolerance. J Exp Med 199 (2004) 1017-1023
22. Tilburgs T., Roelen D.L., van der Mast B.J., van Schip J.J., Kleijburg C., de Groot-Swings G.M., et al. Differential distribution of CD4(+)CD25(bright) and CD8(+)CD28(-) T-cells in decidua and maternal blood during human pregnancy. Placenta 27 Suppl A (2006) S47-S53
23. Shao L., Jacobs A.R., Johnson V.V., and Mayer L. Activation of CD8+ regulatory T cells by human placental trophoblasts. J Immunol 174 (2005) 7539-7547
24. Filaci G., Fenoglio D., Fravega M., Ansaldo G., Borgonovo G., Traverso P., et al. CD8+ CD28- T regulatory lymphocytes inhibiting T cell proliferative and cytotoxic functions infiltrate human cancers. J Immunol 179 (2007) 4323-4334
25. Garba M.L., Pilcher C.D., Bingham A.L., Eron J., and Frelinger J.A. HIV antigens can induce TGF-beta(1)-producing immunoregulatory CD8+ T cells. J Immunol 168 (2002) 2247-2254
26. Popescu I., Macedo C., Abu-Elmagd K., Shapiro R., Hua Y., Thomson A.W., et al. EBV-specific CD8+ T cell reactivation in transplant patients results in expansion of CD8+ type-1 regulatory T cells. Am J Transplant 7 (2007) 1215-1223
27. Billerbeck E., Blum H.E., and Thimme R. Parallel expansion of human virus-specific FoxP3- effector memory and de novo-generated FoxP3+ regulatory CD8+ T cells upon antigen recognition in vitro. J Immunol 179 (2007) 1039-1048
28. O'Garra A., and Vieira P. T(H)1 cells control themselves by producing interleukin-10. Nat Rev Immunol 7 (2007) 425-428
29. Suciu-Foca N., and Cortesini R. Central role of ILT3 in the T suppressor cell cascade. Cell Immunol 248 (2007) 59-67
30. Moller G. Do suppressor T cells exist?. Scand J Immunol 27 (1988) 247-250
31. Kinter A.L., Horak R., Sion M., Riggin L., McNally J., Lin Y., et al. CD25+ regulatory T cells isolated from HIV-infected individuals suppress the cytolytic and nonlytic antiviral activity of HIV-specific CD8+ T cells in vitro. AIDS Res Hum Retroviruses 23 (2007) 438-450
32. Mempel T.R., Pittet M.J., Khazaie K., Weninger W., Weissleder R., von B.H., and von Andrian U.H. Regulatory T cells reversibly suppress cytotoxic T cell function independent of effector differentiation. Immunity 25 (2006) 129-141
33. Tiemessen M.M., Jagger A.L., Evans H.G., van Herwijnen M.J., John S., and Taams L.S. CD4+CD25+Foxp3+ regulatory T cells induce alternative activation of human monocytes/macrophages. Proc Natl Acad Sci U S A 104 (2007) 19446-19451
34. Jamieson S.E., Miller E.N., Black G.F., Peacock C.S., Cordell H.J., Howson J.M., et al. Evidence for a cluster of genes on chromosome 17q11-q21 controlling susceptibility to tuberculosis and leprosy in Brazilians. Genes Immun 5 (2004) 46-57
35. Algood H.M., and Flynn J.L. CCR5-deficient mice control Mycobacterium tuberculosis infection despite increased pulmonary lymphocytic infiltration. J Immunol 173 (2004) 3287-3296
36. Ashton L.J., Stewart G.J., Biti R., Law M., Cooper D.A., and Kaldor J.M. Heterozygosity for CCR5-Delta32 but not CCR2b-64I protects against certain intracellular pathogens. HIV Med 3 (2002) 91-96
37. Ahlenstiel G., Woitas R.P., Rockstroh J., and Spengler U. CC-chemokine receptor 5 (CCR5) in hepatitis C-at the crossroads of the antiviral immune response?. J Antimicrob Chemother 53 (2004) 895-898
38. Lim J.K., Louie C.Y., Glaser C., Jean C., Johnson B., Johnson H., et al. Genetic deficiency of chemokine receptor CCR5 is a strong risk factor for symptomatic West Nile virus infection: A meta-analysis of 4 cohorts in the US epidemic. J Infect Dis 197 (2008) 262-265
39. Ha T.Y., Waksman B.H., and Treffers H.P. The thymic suppressor cell. I. Separation of subpopulations with suppressor activity. J Exp Med 139 (1974) 13-23
40. Mutis T., Cornelisse Y.E., Datema G., van den Elsen P.J., Ottenhoff T.H., and de Vries R.R. Definition of a human suppressor T-cell epitope. Proc Natl Acad Sci U S A 91 (1994) 9456-9460
41. Boussiotis V.A., Tsai E.Y., Yunis E.J., Thim S., Delgado J.C., Dascher C.C., Berezovskaya A., et al. IL-10-producing T cells suppress immune responses in anergic tuberculosis patients. J Clin Invest 105 (2000) 1317-1325
42. Delgado J.C., Tsai E.Y., Thim S., Baena A., Boussiotis V.A., Reynes J.M., Sath S., et al. Antigen-specific and persistent tuberculin anergy in a cohort of pulmonary tuberculosis patients from rural Cambodia. Proc Natl Acad Sci U S A 99 (2002) 7576-7581
43. Chen X., Zhou B., Li M., Deng Q., Wu X., Le X., et al. CD4(+)CD25(+)FoxP3(+) regulatory T cells suppress Mycobacterium tuberculosis immunity in patients with active disease. Clin Immunol 123 (2007) 50-59
44. Guyot-Revol V., Innes J.A., Hackforth S., Hinks T., and Lalvani A. Regulatory T cells are expanded in blood and disease sites in tuberculosis patients. Am J Respir Crit Care Med 173 (2005) 803-810
45. Ribeiro-Rodrigues R., Resende C.T., Rojas R., Toossi Z., Dietze R., Boom W.H., et al. A role for CD4+CD25+ T cells in regulation of the immune response during human tuberculosis. Clin Exp Immunol 144 (2006) 25-34
46. Scott-Browne J.P., Shafiani S., Tucker-Heard G., Ishida-Tsubota K., Fontenot J.D., Rudensky A.Y., et al. Expansion and function of Foxp3-expressing T regulatory cells during tuberculosis. J Exp Med 204 (2007) 2159-2169
47. Burl S., Hill P.C., Jeffries D.J., Holland M.J., Fox A., Lugos M.D., et al. FOXP3 gene expression in a tuberculosis case contact study. Clin Exp Immunol 149 (2007) 117-122
48. Roberts T., Beyers N., Aguirre A., and Walzl G. Immunosuppression during active tuberculosis is characterized by decreased interferon-gamma production and CD25 expression with elevated forkhead box P3, transforming growth factor-beta, and interleukin-4 mRNA levels. J Infect Dis 195 (2007) 870-878
49. Wu B., Huang C., Kato-Maeda M., Hopewell P.C., Daley C.L., Krensky A.M., and Clayberger C. Messenger RNA expression of IL-8, FOXP3, and IL-12beta differentiates latent tuberculosis infection from disease. J Immunol 178 (2007) 3688-3694
50. Kursar M., Koch M., Mittrucker H.W., Nouailles G., Bonhagen K., Kamradt T., and Kaufmann S.H. Cutting edge. Regulatory T cells prevent efficient clearance of Mycobacterium tuberculosis. J Immunol 178 (2007) 2661-2665
51. Suffia I.J., Reckling S.K., Piccirillo C.A., Goldszmid R.S., and Belkaid Y. Infected site-restricted Foxp3+ natural regulatory T cells are specific for microbial antigens. J Exp Med 203 (2006) 777-788
52. Belkaid Y., Piccirillo C.A., Mendez S., Shevach E.M., and Sacks D.L. CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 420 (2002) 502-507
53. Campanelli A.P., Roselino A.M., Cavassani K.A., Pereira M.S., Mortara R.A., Brodskyn C.I., et al. CD4+CD25+ T cells in skin lesions of patients with cutaneous leishmaniasis exhibit phenotypic and functional characteristics of natural regulatory T cells. J Infect Dis 193 (2006) 1313-1322
54. Walther M., Tongren J.E., Andrews L., Korbel D., King E., Fletcher H., et al. Upregulation of TGF-beta, FOXP3, and CD4+CD25+ regulatory T cells correlates with more rapid parasite growth in human malaria infection. Immunity 23 (2005) 287-296
55. Watanabe K., Mwinzi P.N., Black C.L., Muok E.M., Karanja D.M., Secor W.E., and Colley D.G. T regulatory cell levels decrease in people infected with Schistosoma mansoni on effective treatment. Am J Trop Med Hyg 77 (2007) 676-682
56. Cavassani K.A., Campanelli A.P., Moreira A.P., Vancim J.O., Vitali L.H., Mamede R.C., et al. Systemic and local characterization of regulatory T cells in a chronic fungal infection in humans. J Immunol 177 (2006) 5811-5818
57. Harris P.R., Wright S.W., Serrano C., Riera F., Duarte I., Torres J., et al. Helicobacter pylori gastritis in children is associated with a regulatory T-cell response. Gastroenterology 134 (2008) 491-499
58. Enarsson K., Lundgren A., Kindlund B., Hermansson M., Roncador G., Banham A.H., et al. Function and recruitment of mucosal regulatory T cells in human chronic Helicobacter pylori infection and gastric adenocarcinoma. Clin Immunol 121 (2006) 358-368
59. Peng G., Li S., Wu W., Sun Z., Chen Y., and Chen Z. Circulating CD4+ CD25+ regulatory T cells correlate with chronic hepatitis B infection. Immunology 123 (2008) 57-65
60. Lin C.Y., Tsai M.C., Huang C.T., Hsu C.W., Tseng S.C., Tsai I.F., et al. Liver injury is associated with enhanced regulatory T-cell activity in patients with chronic hepatitis B. J Viral Hepat 14 (2007) 503-511
61. Visser J., Nijman H.W., Hoogenboom B.N., Jager P., van Baarle D., Schuuring E., et al. Frequencies and role of regulatory T cells in patients with (pre)malignant cervical neoplasia. Clin Exp Immunol 150 (2007) 199-209
62. Molling J.W., de Gruijl T.D., Glim J., Moreno M., Rozendaal L., Meijer C.J., et al. CD4(+)CD25hi regulatory T-cell frequency correlates with persistence of human papillomavirus type 16 and T helper cell responses in patients with cervical intraepithelial neoplasia. Int J Cancer 121 (2007) 1749-1755
63. van der Burg S.H., Piersma S.J., de Jong A., van der Hulst J.M., Kwappenberg K.M., van den H.M., et al. Association of cervical cancer with the presence of CD4+ regulatory T cells specific for human papillomavirus antigens. Proc Natl Acad Sci U S A 104 (2007) 12087-12092
64. Luhn K., Simmons C.P., Moran E., Dung N.T., Chau T.N., Quyen N.T., et al. Increased frequencies of CD4+ CD25(high) regulatory T cells in acute dengue infection. J Exp Med 204 (2007) 979-985
65. Sprengers D., Stoop J.N., Binda R.S., Kusters J.G., Haagmans B.L., Carotenuto P., et al. Induction of regulatory T-cells and interleukin-10-producing cells in non-responders to pegylated interferon-alpha therapy for chronic hepatitis B. Antivir Ther 12 (2007) 1087-1096
66. Karlsson I., Malleret B., Brochard P., Delache B., Calvo J., Le G.R., and Vaslin B. FoxP3+ CD25+ CD8+ T-cell induction during primary simian immunodeficiency virus infection in cynomolgus macaques correlates with low CD4+ T-cell activation and high viral load. J Virol 81 (2007) 13444-13455
67. de Jong E.C., Smits H.H., and Kapsenberg M.L. Dendritic cell-mediated T cell polarization. Springer Semin Immunopathol 26 (2005) 289-307
68. Abel M., Sene D., Pol S., Bourliere M., Poynard T., Charlotte F., et al. Intrahepatic virus-specific IL-10-producing CD8 T cells prevent liver damage during chronic hepatitis C virus infection. Hepatology 44 (2006) 1607-1616
69. Alatrakchi N., Graham C.S., van der Vliet H.J., Sherman K.E., Exley M.A., and Koziel M.J. Hepatitis C virus (HCV)-specific CD8+ cells produce transforming growth factor beta that can suppress HCV-specific T-cell responses. J Virol 81 (2007) 5882-5892
70. Smyk-Pearson S., Golden-Mason L., Klarquist J., Burton Jr. J.R., Tester I.A., Wang C.C., et al. Functional suppression by FoxP3+CD4+CD25(high) regulatory T cells during acute hepatitis C virus infection. J Infect Dis 197 (2008) 46-57
71. Ward S.M., Fox B.C., Brown P.J., Worthington J., Fox S.B., Chapman R.W., et al. Quantification and localisation of FOXP3+ T lymphocytes and relation to hepatic inflammation during chronic HCV infection. J Hepatol 47 (2007) 316-324
72. Hougardy J.M., Place S., Hildebrand M., Drowart A., Debrie A.S., Locht C., and Mascart F. Regulatory T cells depress immune responses to protective antigens in active tuberculosis. Am J Respir Crit Care Med 176 (2007) 409-416
73. Andersen P., and Doherty T.M. The success and failure of BCG-implications for a novel tuberculosis vaccine. Nat Rev Microbiol 3 (2005) 656-662
74. Hanekom W.A. The immune response to BCG vaccination of newborns. Ann N Y Acad Sci 1062 (2005) 69-78
75. Kaufmann S.H. Envisioning future strategies for vaccination against tuberculosis. Nat Rev Immunol 6 (2006) 699-704
76. Rodrigues L.C., Pereira S.M., Cunha S.S., Genser B., Ichihara M.Y., de Brito S.C., et al. Effect of BCG revaccination on incidence of tuberculosis in school-aged children in Brazil: The BCG-REVAC cluster-randomised trial. Lancet 366 (2005) 129-195