CD4+CD25+ regulatory T cells inhibit natural killer cell functions in a transforming growth factor-β-dependent manner

Journal of Experimental Medicine

Volumn 202, Issue 8, 2005, Pages 1075-1085

  Ghiringhelli, François ^a,c   Ménard, Cédric ^a   Terme, Magali ^a   Flament, Caroline ^a   Taieb, Julien ^a   Chaput, Nathalie ^a   Puig, Pierre E ^c   Novault, Sophie ^a   Escudier, Bernard ^b   Vivier, Eric ^d   Lecesne, Axel ^b   Robert, Caroline ^b   Blay, Jean Yves ^e   Bernard, Jacky ^f   Caillat Zucman, Sophie ^g   Freitas, Antonio ^d   Tursz, Thomas ^a   Wagner Ballon, Orianne ^b   Capron, Claude ^b   Vainchencker, William ^b   Martin, François ^c   Zitvogel, Laurence ^a   more..

^a INSERM   (France)

^b INSTITUT GUSTAVE ROUSSY   (France)

^c UNIVERSITÉ DE BOURGOGNE   (France)

^d CNRS   (France)

^e EDOUARD HERRIOT HOSPITAL   (France)

^f ETABLISSEMENT FRANÇAIS DU SANG   (France)

^g HÔPITAL SAINT VINCENT DE PAUL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; IMATINIB; INTERLEUKIN 2 RECEPTOR ALPHA; NATURAL KILLER CELL RECEPTOR NKG2D; TRANSFORMING GROWTH FACTOR BETA;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER IMMUNOLOGY; CELL FUNCTION; CELLULAR IMMUNITY; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DOWN REGULATION; EFFECTOR CELL; GASTROINTESTINAL STROMAL TUMOR; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOREGULATION; INNATE IMMUNITY; LYMPHOCYTE DEPLETION; LYMPHOCYTIC INFILTRATION; MOLECULAR RECOGNITION; MOUSE; NATURAL KILLER CELL; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; NONHUMAN; NUDE MOUSE; PHASE 2 CLINICAL TRIAL; PRIORITY JOURNAL; RECEPTOR SENSITIVITY; TUMOR GROWTH; WILD TYPE;

ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; CYTOKINES; CYTOTOXICITY TESTS, IMMUNOLOGIC; FLOW CYTOMETRY; FRANCE; HUMANS; IMMUNITY, NATURAL; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; NEOPLASMS; RECEPTORS, IMMUNOLOGIC; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA;

EID: 26844464792     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20051511     Document Type: Article

References (47)

1. Sakaguchi, S. 2000. Regulatory T cells: key controllers of immunologic self-tolerance. Cell. 101:455-458.
2. Shevach, E.M. 2002. CD4+ CD25+ suppressor T cells: more questions than answers. Nat. Rev. Immunol. 2:389-400.
3. Sakaguchi, S. 2004. Naturally arising CD4+ regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu. Rev. Immunol. 22:531-562.
4. + T regulatory cells suppress Helicobacter hepaticus-induced colitis. J. Exp. Med. 196:505-515.
5. Belkaid, Y., C.A. Piccirillo, S. Mendez, E.M. Shevach, and D.L. Sacks. 2002. CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature. 420:502-507.
6. van Maurik, A., M. Herber, K.J. Wood, and N.D. Jones. 2002. Cutting edge: CD4+CD25+ alloantigen-specific immunoregulatory cells that can prevent CD8+ T cell-mediated graft rejection: implications for anti-CD154 immunotherapy. J. Immunol. 169:5401-5404.
7. Trenado, A., F. Charlotte, S. Fisson, M. Yagello, D. Klatzmann, B.L. Salomon, and J.L. Cohen. 2003. Recipient-type specific CD4+ CD25+ regulatory T cells favour immune reconstitution and control graft-versus-host disease while maintaining graft-versus-leukemia. J. Clin. Invest. 112:1688-1696.
8. Sasada, T., M. Kimura, Y. Yoshida, M. Kanai, and A. Takabayashi. 2003. CD4+CD25+ regulatory T cells in patients with gastrointestinal malignancies: possible involvement of regulatory T cells in disease progression. Cancer. 98:1089-1099.
9. Onizuka, S., I. Tawara, J. Shimizu, S. Sakaguchi, T. Fujita, and E. Nakayama. 1999. Tumor rejection by in vivo administration of anti-CD25 (interleukin-2 receptor alpha) monoclonal antibody. Cancer Res. 59:3128-3133.
10. + regulatory T cells in antitumor therapy reveals alternative pathways for suppression of autoreactive cytotoxic T lymphocyte responses. J. Exp. Med. 194:823-832.
11. Steitz, J., J. Bruck, J. Lenz, J. Knop, and T. Tuting. 2001. Depletion of CD25(+) CD4(+) T cells and treatment with tyrosinase-related protein 2-transduced dendritic cells enhance the interferon alpha-induced, CD8(+) T-cell-dependent immune defense of B16 melanoma. Cancer Res. 61:8643-8646.
12. Ghiringhelli, F., N. Larmonier, E. Schmitt, A. Parcellier, D. Cathelin, C. Garrido, B. Chauffert, E. Solary, B. Bonnotte, and F. Martin. 2004. CD4+CD25+ regulatory T cells suppress tumor immunity but are sensitive to cyclophosphamide which allows immunotherapy of established tumors to be curative. Eur. J. Immunol. 34:336-344.
13. Turk, M.J., J.A. Guevara-Patino, G.A. Rizzuto, M.E. Engelhorn, and A.N. Houghton. 2004. Concomitant tumor immunity to a poorly immunogenic melanoma is prevented by regulatory T cells. J. Exp. Med. 200:771-782.
14. Woo, E.Y., H. Yeh, C.S. Chu, K. Schlienger, R.G. Carroll, J.L. Riley, L.R. Kaiser, and C.H. June. 2002. Cutting edge: regulatory T cells from lung cancer patients directly inhibit autologous T cell proliferation. J. Immunol. 168:4272-4276.
15. Woo, E.Y., C.S. Chu, T.J. Goletz, K. Schlienger, H. Yeh, G. Coukos, S.C. Rubin, L.R. Kaiser, and C.H. June. 2001. Regulatory CD4(+)CD25(+) T cells in tumors from patients with early-stage non-small cell lung cancer and late-stage ovarian cancer. Cancer Res. 61:4766-4772.
16. Liyanage, U.K., T.T. Moore, H.G. Joo, Y. Tanaka, V. Herrmann, G. Doherty, J.A. Drebin, S.M. Strasberg, T.J. Eberlein, P.S. Goedegebuure, and D.C. Linehan. 2002. Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma. J. Immunol. 169:2756-2761.
17. Curiel, T.J., G. Coukos, L. Zou, X. Alvarez, P. Cheng, M. Mottram, J.R. Evdemon-Hogan, L. Conejo-Garcia, M. Zhang, Y. Burow, et al. 2004. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med. 10:942-949.
18. Ruggeri, L., M. Capanni, E. Urbani, K. Perruccio, W.D. Shlomchik, A. Tosti, S. Posati, D. Rogaia, F. Frassoni, F. Aversa, et al. 2002. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science. 295:2097-2100.
19. Castriconi, R., A. Dondero, R. Augugliaro, C. Cantoni, B. Carnemolla, A.R. Sementa, F. Negri, R. Conte, M.V. Corrias, L. Moretta, and C. Bottino. 2004. Identification of 4Ig-B7-H3 as a neuroblastoma-associated molecule that exerts a protective role from an NK cell-mediated lysis. Proc. Natl. Acad. Sci. USA. 101:12640-12645.
20. Borg, C., M. Terme, J. Taieb, C. Menard, C. Flament, C. Robert, K. Maruyama, H. Wakasugi, E. Angevin, K. Thielemans, et al. 2004. Novel mode of action of c-kit tyrosine kinase inhibitors leading to NK cell-dependent antitumor effects. J. Clin. Invest. 114:379-388.
21. Moretta, A., C. Bottino, M.C. Mingari, R. Biassoni, and L. Moretta. 2002. What is a natural killer cell? Nat. Immunol. 3:6-8.
22. Lanier, L.L. 2001. On guard-activating NK cell receptors. Nat. Immunol. 2:23-27.
23. Vivier, E., J.A. Nunes, and F. Vely. 2004. Natural killer cell signaling pathways. Science. 306:1517-1519.
24. Bauer, S., V. Groh, J. Wu, A. Steinle, J.H. Phillips, L.L. Lanier, and T. Spies. 1999. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science. 285:727-729.
25. Wu, J.D., L.M. Higgins, A. Steinle, D. Cosman, K. Haugk, and S.R. Plymate. 2004. Prevalent expression of the immunostimulatory MHC class I chain-related molecule is counteracted by shedding in prostate cancer. J. Clin. Invest. 114:560-568.
26. Rosenberg, S.A., M.T. Lotze, J.C. Yang, P.M. Aebersold, W.M. Linehan, C.A. Seipp, and D.E. White. 1989. Experience with the use of high dose of interleukin-2 in the treatment of 652 cancer patients. Ann. Surg. 210:474-485.
27. Baecher-Allan, C., V. Viglietta, and D.A. Hafler. 2004. Human CD4+CD25+ regulatory T cells. Semin. Immunol. 16:89-98.
28. + regulatory T cells is mediated by cell surface-bound transforming growth factor-β. J. Exp. Med. 194:629-644.
29. + human thymocytes. J. Exp. Med. 196:379-387.
30. + T suppressor cell clones produce transforming growth factor-β, but not interleukin 10, and are distinct from type 1 T regulatory cells. J. Exp. Med. 196:1335-1346.
31. Castriconi, R., C. Cantoni, M. Della Chiesa, M. Vitale, E. Marcenaro, R. Conte, R. Biassoni, C. Bottino, L. Moretta, and A. Moretta. 2003. Transforming growth factor beta 1 inhibits expression of NKp30 and NKG2D receptors: consequences for the NK-mediated killing of dendritic cells. Proc. Natl. Acad. Sci. USA. 100:4120-4125.
32. Fontenot, J.D., M.A. Gavin, and A.Y. Rudensky. 2003. Foxp3 programs the development and function of CD4 CD25 regulatory T cells. Nat. Immunol. 4:330-336.
33. Glas, R., L. Franksson, C. Une, M.L. Eloranta, C. Ohlen, A. Orn, and K. Karre. 2000. Recruitment and activation of natural killer (NK) cells in vivo determined by the target cell phenotype. An adaptive component of NK cell-mediated responses. J. Exp. Med. 191:129-138.
34. Viguier, M., F. Lemaitre, O. Verola, M.S. Cho, G. Gorochov, L. Dubertret, H. Bachelez, P. Kourilsky, and L. Ferradini. 2004. Foxp3 expressing CD4+CD25(high) regulatory T cells are overrepresented in human metastatic melanoma lymph nodes and inhibit the function of infiltrating T cells. J. Immunol. 173:1444-1453.
35. Shimizu, J., S. Yamazaki, and S. Sakaguchi. 1999. Induction of tumor immunity by removing CD25+CD4+ T cells: a common basis between tumor immunity and autoimmunity. J. Immunol. 163:5211-5218.
36. Wolf, A.M., D. Wolf, M. Steurer, G. Gastl, E. Gunsilius, and B. Grubeck-Loebenstein. 2003. Increase of regulatory T cells in the peripheral blood of cancer patients. Clin. Cancer Res. 9:606-612.
37. Trzonkowski, P., E. Szmit, J. Mysliwska, A. Dobyszuk, and A. Mysliwski. 2004. CD4+CD25+ T regulatory cells inhibit cytotoxic activity of T CD8+ and NK lymphocytes in the direct cell-to-cell interaction. Clin. Immunol. 112:258-267.
38. Ostroukhova, M., C. Seguin-Devaux, T.B. Oriss, B. Dixon-McCarthy, L. Yang, B.T. Ameredes, T.E. Corcoran, and A. Ray. 2004. Tolerance induced by inhaled antigen involves CD4+ T cells expressing membrane-bound TGF-β and FOXP3. J. Clin. Invest. 114:28-38.
39. Doubrovina, E.S., M.M. Doubrovin, E. Vider, R.B. Sisson, R.J. O'Reilly, B. Dupont, and Y.M. Vyas. 2003. Evasion from NK cell immunity by MHC class I chain-related molecules expressing colon adenocarcinoma. J. Immunol. 171:6891-6899.
40. + immunoregulatory T cells suppress polyclonal T cell activation by inhibiting interleukin 2 production. J. Exp. Med. 188:287-296.
41. Thornton, A.M., and E.M. Shevach. 2000. Suppressor effector function of CD4+ CD25+ immunoregulatory T cells is antigen non-specific. J. Immunol. 164:183-190.
42. Piccirillo, C.A., and E.M. Shevach. 2001. Cutting edge: control of CD8+ T cell activation by CD4+ CD25+ immunoregulatory T cells. J. Immunol. 167:1137-1142.
43. Brunkow, M.E., E.W. Jeffery, K.A. Hjerrild, B. Paeper, L.B. Clark, S.A. Yasayko, J.E. Wilkinson, D. Galas, S.F. Ziegler, and F. Ramsdell. 2001. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat. Genet. 27:68-73.
44. Smyth, M.J., J. Swann, J.M. Kelly, E. Cretney, W.M. Yokoyama, A. Diefenbach, T.J. Sayers, and Y. Hayakawa. 2004. NKG2D recognition and perforin effector function mediate effective cytokine immunotherapy of cancer. J. Exp. Med. 200:1325-1335.
45. Diefenbach, A., A.M. Jamieson, S.D. Liu, N. Shastri, and D.H. Raulet. 2000. Ligands for the murine NKG2D receptor: expression by tumor cells and activation of NK cells and macrophages. Nat. Immunol. 1:119-126.
46. Hue, S., J.J. Mention, R.C. Monteiro, S. Zhang, C. Cellier, J. Schmitz, V. Verkarre, N. Fodil, S. Bahram, N. Cerf-Bensussan, and S. Caillat-Zucman. 2004. A direct role for NKG2D/MICA interaction in villous atrophy during celiac disease. Immunity. 21:367-377.
47. Terme, M., E. Tomasello, K. Maruyama, F. Crepineau, N. Chaput, C. Flament, J.P. Marolleau, E. Angevin, E.F. Wagner, B. Salomon, et al. 2004. IL-4 confers NK stimulatory capacity to murine dendritic cells: a signaling pathway involving KARAP/DAP12-triggering receptor expressed on myeloid cell 2 molecules. J. Immunol. 172:5957-5966.