The role of regulatory T cells in the control of natural killer cells: Relevance during tumor progression

Immunological Reviews

Volumn 214, Issue 1, 2006, Pages 229-238

  Ghiringhelli, Francois ^a,b   Ménard, Cédric ^a   Martin, Francois ^b   Zitvogel, Laurence ^a  

^a INSERM   (France)

^b UNIVERSITÉ DE BOURGOGNE   (France)

Author keywords

CD4+CD25+ regulatory T cells; NK cells; Tumor immunity

Indexed keywords

BASILIXIMAB; FAS LIGAND; GAMMA INTERFERON; GENE PRODUCT; IMATINIB; INTERLEUKIN 12; NATURAL KILLER CELL RECEPTOR NKG2D; PLATELET DERIVED GROWTH FACTOR RECEPTOR; TRANSFORMING GROWTH FACTOR BETA;

CANCER GROWTH; CANCER IMMUNOTHERAPY; CANCER RISK; CARCINOGENESIS; CELL PROLIFERATION; CHEDIAK HIGASHI SYNDROME; CHRONIC MYELOID LEUKEMIA; COLON CANCER; CYTOKINE PRODUCTION; CYTOTOXICITY; DISEASE FREE SURVIVAL; EPSTEIN BARR VIRUS; GENE MUTATION; HODGKIN DISEASE; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOSURVEILLANCE; LEUKEMIA; LIVER CARCINOGENESIS; LIVER CARCINOMA; LIVER CIRRHOSIS; LUNG CANCER; MOUSE STRAIN; NATURAL KILLER CELL; NONHODGKIN LYMPHOMA; NONHUMAN; PRIORITY JOURNAL; PROSTATE CARCINOMA; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; REVIEW; TUMOR IMMUNITY;

ANIMALS; DISEASE PROGRESSION; HUMANS; KILLER CELLS, NATURAL; NEOPLASMS; T-LYMPHOCYTES, REGULATORY;

EID: 33750691006     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2006.00445.x     Document Type: Review

References (87)

1. Shankaran V, et al. IFN-γ lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 2001;410:1107-1111.
2. Kaplan DH, et al. Demonstration of an interferon gamma-dependent tumor surveillance system in immunocompetent mice. Proc Natl Acad Sci USA 1998;95:7556-7561.
3. Willimsky G, Blankenstein T. Sporadic immunogenic tumours avoid destruction by inducing T-cell tolerance. Nature 2005;437:141-146.
4. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD. Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 2002;3:991-998.
5. Dunn GP, Old LJ, Schreiber RD. The immunobiology of cancer immunosurveillance and immunoediting. Immunity 2004;21:137-148.
6. Takeda K, et al. Critical role for tumor necrosis factor-related apoptosis-inducing ligand in immune surveillance against tumor development. J Exp Med 2002;195:161-169.
7. Ortaldo JR, Bere EW, Hodge D, Young HA. Activating Ly-49 NK receptors: central role in cytokine and chemokine production. J Immunol 2001;166:4994-4999.
8. Raulet DH. Interplay of natural killer cells and their receptors with the adaptive immune response. Nat Immunol 2004;5:996-1002.
9. Crowe NY, et al. Differential antitumor immunity mediated by NKT cell subsets in vivo. J Exp Med 2005;202:1279-1288.
10. Taieb J, et al. A novel dendritic cell subset involved in tumor immunosurveillance. Nat Med 2006;12:214-219.
11. Trinchieri G. Natural killer cells wear different hats: effector cells of innate resistance and regulatory cells of adaptive immunity and of hematopoiesis. Semin Immunol 1995;7:83-88.
12. Screpanti V, Wallin RP, Grandien A, Ljunggren HG. Impact of FASL-induced apoptosis in the elimination of tumor cells by NK cells. Mol Immunol 2005;42:495-499.
13. Moretta L, Moretta A. Unravelling natural killer cell function: triggering and inhibitory human NK receptors. EMBO J 2004;23:255-259.
14. Vivier E, Biron CA. A pathogen receptor on natural killer cells. Science 2002;296:1248-1249.
15. Vely F, Vivier E. Natural killer cell receptor signaling pathway in mammals. Sci STKE 2005;12:cm7.
16. Biassoni R, et al. Human natural killer cell receptors: insights into their molecular function and structure. J Cell Mol Med 2003;7:376-387.
17. Lanier LL. Natural killer cell receptor signaling. Curr Opin Immunol 2003;15:308-314.
18. Smyth MJ, Crowe NY, Godfrey DI. NK cells and NKT cells collaborate in host protection from methylcholanthrene induced fibrosarcoma. Int Immunol 2001;13:459-463.
19. Roder JC, Lohmann-Matthes ML, Domzig W, Wigzell H. The beige mutation in the mouse. II. Selectivity of the natural killer (NK) cell defect. J Immunol 1979;123:2174-2180.
20. Haliotis T, Ball JK, Dexter D, Roder JC. Spontaneous and induced primary oncogenesis in natural killer (NK)-cell-deficient beige mutant mice. Int J Cancer 1985;35:505-513.
21. Kim S, Iizuka K, Aguila HL, Weissman IL, Yokoyama WM. In vivo natural killer cell activities revealed by natural killer cell-deficient mice. Proc Natl Acad Sci USA 2000;97:2731-2736.
22. Diefenbach A, Jensen ER, Jamieson AM, Raulet DH. Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature 2001;413:165-171.
23. Cerwenka A, Baron JL, Lanier LL. Ectopic expression of retinoic acid early inducible-1 gene (RAE-1) permits natural killer cell-mediated rejection of a MHC class I-bearing tumor in vivo. Proc Natl Acad Sci USA 2001;98:11521-11526.
24. Kobayashi H, et al. Role of trans-cellular IL-15 presentation in the activation of NK cell-mediated killing, which leads to enhanced tumor immunosurveillance. Blood 2005;105:721-727.
25. Eidenschenk C, et al. A novel primary immunodeficiency with specific natural-killer cell deficiency maps to the centromeric region of chromosome 8. Am J Hum Genet 2006;78:721-727.
26. Brittenden J, Heys SD, Ross J, Eremin O. Natural killer cells and cancer. Cancer 1996;77:1226-1243.
27. Kobayashi N. Malignant neoplasms in registered cases of primary immunodeficiency syndrome. Jpn J Clin Oncol 1985;15:307-312.
28. Clementi R, et al. A proportion of patients with lymphoma may harbor mutations of the perforin gene. Blood 2005;105:4424-4428.
29. Sun T, et al. FASL-844C polymorphism is associated with increased activation-induced T cell death and risk of cervical cancer. J Exp Med 2005;202:967-974.
30. Carrington M. Hierarchy of resistance to cervical neoplasia mediated by combinations of killer immunoglobulin-like receptor and human leukocyte antigen loci. J Exp Med 2005;201:1069-1075.
31. Nakachi K, Hayashi T, Imai K, Kusunoki Y. Perspectives on cancer immuno-epidemiology. Cancer Sci 2004;95:921-929.
32. Imai K, Matsuyama S, Miyake S, Suga K, Nakachi K. Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general population. Lancet 2000;356:1795-1799.
33. Hayashi T, Imai K, Morishita Y, Hayashi I, Kusunoki Y, Nakachi K. Identification of the NKG2D haplotypes associated with natural cytotoxic activity of peripheral blood lymphocytes and cancer immunosurveillance. Cancer Res 2006;66:563-570.
34. Nakajima T, Mizushima N, Kanai K. Relationship between natural killer activity and development of hepatocellular carcinoma in patients with cirrhosis of the liver. Jpn J Clin Oncol 1987;17:327-332.
35. Schantz SP, Campbell BH, Guillamondegui OM. Pharyngeal carcinoma and natural killer cell activity. Am J Surg 1986;152:467-474.
36. Sakaguchi S. Regulatory T cells: key controllers of immunologic self-tolerance. Cell 2000;101:455-458.
37. Shevach EM. CD4+ CD25+ suppressor T cells: more questions than answers. Nat Rev Immunol 2002;2:389-400.
38. 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.
39. 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.
40. Takahashi T, et al. Immunologic self-tolerance maintained by CD25+CD4+ naturally anergic and suppressive T cells: induction of autoimmune disease by breaking their anergic/suppressive state. Int Immunol 1998;10:1969-1980.
41. 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.
42. Thornton CA, et al. Functional maturation of CD4+CD25+CTLA4+CD45RA+ T regulatory cells in human neonatal T cell responses to environmental antigens/allergens. J Immunol 2004;173:3084-3092.
43. Takahashi T, et al. Immunologic self-tolerance maintained by CD25+CD4+ regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4. J Exp Med 2000;192:303-310.
44. Yamazaki S, et al. Direct expansion of functional CD25+CD4+ regulatory T cells by antigen-processing dendritic cells. J Exp Med 2003;198:235-247.
45. Pasare C, Medzhitov R. Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells. Science 2003;299:1033-1036.
46. Almeida AR, Legrand N, Papiernik M, Freitas AA. Homeostasis of peripheral CD4+ T cells: IL-2R alpha and IL-2 shape a population of regulatory cells that controls CD4+ T cell numbers. J Immunol 2002;169:4850-4860.
47. Gavin MA, Clarke SR, Negrou E, Gallegos A, Rudensky A. Homeostasis and anergy of CD4(+)CD25(+) suppressor T cells in vivo. Nat Immunol 2001;3:33-41.
48. Liyanage UK, et al. Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma. J Immunol 2002;169:2756-2761.
49. Sato E, et al. Intraepithelial CD8+ tumorin-filtrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci USA 2005;102:18538-18543.
50. Sasada T, Kimura M, Yoshida Y, Kanai M, Takabayashi A. CD4+CD25+ regulatory T cells in patients with gastrointestinal malignancies: possible involvement of regulatory T cells in disease progression. Cancer 2003;98:1089-1099.
51. Woo EY, et al. Regulatory CD4(+)CD25(+) T cells in tumors from patients with early-stage non-small cell lung cancer and late-stage ovarian cancer. Cancer Res 2001;61: 4766-4772.
52. Curiel TJ, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004;10:942-949.
53. Ghiringhelli F, et al. CD4+CD25+ regulatory T cells suppress tumor immunity but are sensitive to cyclophosphamide which allows immunotherapy of establish tumors. Eur J Immunol 2004;34:336-344.
54. Ghiringhelli F, et al. Tumor cells convert immature myeloid dendritic cells into TGF-beta-secreting cells inducing CD4+CD25+ regulatory T cell proliferation. J Exp Med 2005;202:919-929.
55. Onizuka S, Tawara I, Shimizu J, Sakaguchi S, Fujita T, Nakayama E. Tumor rejection by in vivo administration of anti-CD25 (interleukin-2 receptor alpha) monoclonal antibody. Cancer Res 1999;59:3128-3133.
56. Shimizu J, Yamazaki S, Sakaguchi S. Induction of tumor immunity by removing CD25+CD4+ T cells: a common basis between tumor immunity and autoimmunity. J Immunol 1999;163:5211-5218.
57. Sutmuller RP, et al. Synergism of cytotoxic T lymphocyte-associated antigen 4 blockade and depletion of CD25+ regulatory T cells in antitumor therapy reveals alternative pathways for suppression of autoreactive cytotoxic T lymphocyte responses. J Exp Med 2001;194:823-832.
58. Lutsiak ME, Semnani RT, De Pascalis R, Kashmiri SV, Schlom J, Sabzevari H. Inhibition of CD4+ CD25+ T regulatory cell function implicated in enhanced immune response by low-dose cyclophosphamide. Blood 2005;105:2862-2868.
59. Danke NA, Koelle DM, Yee C, Beheray S, Kwok WW. Autoreactive T cells in healthy individuals. J Immunol 2004;172:5967-5972.
60. Nishikawa H, et al. Accelerated chemically induced tumor development mediated by CD4+CD25+ regulatory T cells in wild-type hosts. Proc Natl Acad Sci USA 2005;102:9253-9257.
61. Wolf AM, Wolf D, Steurer M, Gastl G, Gunsilius E, Grubeck-Loebenstein B. Increase of regulatory T cells in the peripheral blood of cancer patients. Clin Cancer Res 2003;9:606-612.
62. Trzonkowski P, Szmit E, Mysliwska J, Dobyszuk A, Mysliwski A. CD4+CD25+ T regulatory cells inhibit cytotoxic activity of T CD8+ and NK lymphocytes in the direct cell-to-cell interaction. Clin Immunol 2004;112:258-267.
63. Rubin BP, et al. KIT activation is a ubiquitous feature of gastrointestinal stromal tumors. Cancer Res 2001;61:8118-8121.
64. Heinrich MC, et al. PDGFRA activating mutations in gastrointestinal stromal tumors. Science 2003;31:708-710.
65. Borg C, et al. Novel mode of action of c-kit tyrosine kinase inhibitors leading to NK cell-dependent antitumor effects. J Clin Invest 2004;114:379-388.
66. Terme M, et al. BCR/ABL promotes dendritic cell-mediated natural killer cell activation. Cancer Res 2005;65:6409-6417.
67. Cebo C, et al. The decreased susceptibility of Bcr/Abl targets to NK cell-mediated lysis in response to imatinib mesylate involves modulation of NKG2D ligands, GM1 expression, and synapse formation. J Immunol 2006;176:864-872.
68. Apperley JF, et al. Response to imatinib mesylate in patients with chronic myeloproliferative diseases with rearrangements of the platelet-derived growth factor receptor beta. N Engl J Med 2002;347:481-487.
69. Buchdunger E, O'Reilly T, Wood J. Pharmacology of imatinib (STI571). Eur J Cancer 2002;38:S28-S36.
70. Heinrich MC, Blanke CD, Druker BJ, Corless CL. Inhibition of KIT tyrosine kinase activity: a novel molecular approach to the treatment of KIT-positive malignancies. J Clin Oncol 2002;20:1692-1703.
71. Demetri GD, et al. Efficacy and safety of imatinib mesylate in advanced gastrointestinal stromal tumors. N Engl J Med 2002;347:472-480.
72. Ghiringhelli F, et al. CD4+CD25+ regulatory T cells inhibit natural killer cell functions in a transforming growth factor-beta-dependent manner. J Exp Med 2005;202:1075-1085.
73. Morse MA, et al. A phase I study of dexosome immunotherapy in patients with advanced non-small cell lung cancer. J Transl Med 2005;3:9.
74. Escudier B, et al. Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of the first phase I clinical trial. J Transl Med 2005;3:10.
75. Dasgupta S, Bhattacharya-Chatterjee M, O'Malley BW Jr, Chatterjee SK. Inhibition of NK cell activity through TGF-beta 1 by down-regulation of NKG2D in a murine model of head and neck cancer. J Immunol 2005;175:5541-5550.
76. Nakamura K, et al. TGF-beta 1 plays an important role in the mechanism of CD4+CD25+ regulatory T cell activity in both humans and mice. J Immunol 2004;172:834-842.
77. Uhl M, et al. SD-208, a novel transforming growth factor beta receptor I kinase inhibitor, inhibits growth and invasiveness and enhances immunogenicity of murine and human glioma cells in vitro and in vivo. Cancer Res 2004;64:7954-7961.
78. Friese MA, et al. RNA interference targeting transforming growth factor-beta enhances NKG2D-mediated antiglioma immune response, inhibits glioma cell migration and invasiveness, and abrogates tumorigenicity in vivo. Cancer Res 2004;64:7596-7603.
79. Lee JC, Lee KM, Kim DW, Heo DS. Elevated TGF-beta 1 secretion and down-modulation of NKG2D underlies impaired NK cytotoxicity in cancer patients. J Immunol 2004;172:7335-7340.
80. Smyth MJ, Teng MW, Swann J, Kyparissoudis K, Godfrey DI, Hayakawa Y. CD4+CD25+ T regulatory cells suppress NK cell-mediated immunotherapy of cancer. J Immunol 2006;176:1582-1587.
81. Doubrovina ES, et al. Evasion from NK cell immunity by MHC class I chain-related molecules expressing colon adenocarcinoma. J Immunol 2003;171:6891-6899.
82. Wu JD, Higgins LM, Steinle A, Cosman D, Haugk K, Plymate SR. Prevalent expression of the immunostimulatory MHC class I chain-related molecule is counteracted by shedding in prostate cancer. J Clin Invest 2004;114:560-568.
83. Nakamura K, Kitani A, Strober W. Cell contact-dependent immunosuppression by CD4(+)CD25(+) regulatory T cells is mediated by cell surface-bound transforming growth factor beta. J Exp Med 2001;194:629-644.
84. Chen Y, Ali T, Todorovic V, O'leary JM, Kristina Downing A, Rifkin DB. Amino acid requirements for formation of the TGF-beta-latent TGF-beta binding protein complexes. J Mol Biol 2005;345:175-186.
85. Annes JP, Munger JS, Rifkin DB. Making sense of latent TGF-beta activation. J Cell Sci 2003;116:217-224.
86. Crawford SE, et al. Thrombospondin-1 is a major activator of TGF-beta 1 in vivo. Cell 1998;3:1159-1170.
87. Oida T, et al. CD4+CD25- T cells that express latency-associated peptide on the surface suppress CD4+CD45RBhigh-induced colitis by a TGF-beta-dependent mechanism. J Immunol 2003;170:2516-2522.