Regulatory T cells and treatment of cancer

Current Opinion in Immunology

Volumn 20, Issue 2, 2008, Pages 241-246

  Curiel, Tyler J ^a  

^a University of Texas Health Science Center at San Antonio   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; CANCER VACCINE; CD4 ANTIGEN; CYCLOPHOSPHAMIDE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; DENDRITIC CELL VACCINE; DENILEUKIN DIFTITOX; FLT3 LIGAND; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 12; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; PROTEIN TYROSINE KINASE INHIBITOR; TRANSCRIPTION FACTOR FOXP3;

BONE MARROW CELL; CANCER GENE THERAPY; CANCER IMMUNOTHERAPY; CANCER PREVENTION; CANCER SURVIVAL; CD4+ CD25+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; COLON CARCINOMA; DRUG MECHANISM; HELPER CELL; HUMAN; IMMUNOSURVEILLANCE; LIVER CELL CARCINOMA; LYMPHOCYTE COUNT; LYMPHOCYTE DEPLETION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE FUNCTION; LYMPHOCYTE MIGRATION; MELANOMA; MICROENVIRONMENT; NATURAL KILLER T CELL; NONHUMAN; PROGNOSIS; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; REVIEW; SARCOMA; T CELL LYMPHOMA; TUMOR CELL; TUMOR IMMUNITY;

ANIMALS; HUMANS; LYMPHOCYTE DEPLETION; MICE; NEOPLASMS; T-LYMPHOCYTES, REGULATORY;

EID: 44749092510     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.coi.2008.04.008     Document Type: Review

References (68)

1. Zou W. Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol 6 (2006) 295-307. This is a comprehensive review of the subject.
2. Curiel T.J. Tregs and rethinking cancer immunotherapy. J Clin Invest 117 (2007) 1167-1174. This paper examines how infectious disease models shaped tumor immunotherapy, perhaps not always for the better.
3. Zou W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 5 (2005) 263-274
4. Rüter J., Barnett B.G., Kryczek I., Brumlik M.J., Daniel B.J., Coukos G., Zou W., and Curiel T.J. Manipulating T Regulatory Cells in Cancer Immunotherapy. Exp Rev Derm 1 (2006) 589-597
5. Curiel T.J. Regulatory T-cell development: is Foxp3 the decider?. Nat Med 13 (2007) 250-253
6. Larmonier N., Marron M., Zeng Y., Cantrell J., Romanoski A., Sepassi M., Thompson S., Chen X., Andreansky S., and Katsanis E. Tumor-derived CD4(+)CD25(+) regulatory T cell suppression of dendritic cell function involves TGF-beta and IL-10. Cancer Immunol Immunother 56 (2007) 48-59
7. Strauss L., Bergmann C., Szczepanski M., Gooding W., Johnson J.T., and Whiteside T.L. A unique subset of CD4+CD25highFoxp3+ T cells secreting interleukin-10 and transforming growth factor-beta1 mediates suppression in the tumor microenvironment. Clin Cancer Res 13 (2007) 4345-4354
8. Zhou G., and Levitsky H.I. Natural regulatory T cells and de novo-induced regulatory T cells contribute independently to tumor-specific tolerance. J Immunol 178 (2007) 2155-2162
9. Battaglia A., Buzzonetti A., Monego G., Peri L., Ferrandina G., Fanfani F., Scambia G., and Fattorossi A. Neuropilin-1 expression identifies a subset of regulatory T cells in human lymph nodes that is modulated by preoperative chemoradiation therapy in cervical cancer. Immunology 123 (2008) 129-138
10. Liu W., Putnam A.L., Xu-Yu Z., Szot G.L., Lee M.R., Zhu S., Gottlieb P.A., Kapranov P., Gingeras T.R., Fazekas de St Groth B., et al. CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ Treg cells. J Exp Med 203 (2006) 1701-1711
11. Yokokawa J., Cereda V., Remondo C., Gulley J.L., Arlen P.M., Schlom J., and Tsang K.Y. Enhanced functionality of CD4+CD25highFoxP3+ regulatory T cells in the peripheral blood of patients with prostate cancer. Clin Cancer Res 14 (2008) 1032-1040
12. Bergmann C., Strauss L., Zeidler R., Lang S., and Whiteside T.L. Expansion of human T regulatory type 1 cells in the microenvironment of cyclooxygenase 2 overexpressing head and neck squamous cell carcinoma. Cancer Res 67 (2007) 8865-8873
13. Yang Z.Z., Novak A.J., Ziesmer S.C., Witzig T.E., and Ansell S.M. CD70+ non-Hodgkin lymphoma B cells induce Foxp3 expression and regulatory function in intratumoral CD4+CD25 T cells. Blood 110 (2007) 2537-2544
14. Juszczynski P., Ouyang J., Monti S., Rodig S.J., Takeyama K., Abramson J., Chen W., Kutok J.L., Rabinovich G.A., and Shipp M.A. The AP1-dependent secretion of galectin-1 by Reed Sternberg cells fosters immune privilege in classical Hodgkin lymphoma. Proc Natl Acad Sci U S A 104 (2007) 13134-13139
15. Liu V.C., Wong L.Y., Jang T., Shah A.H., Park I., Yang X., Zhang Q., Lonning S., Teicher B.A., and Lee C. Tumor evasion of the immune system by converting CD4+CD25- T cells into CD4+CD25+ T regulatory cells: role of tumor-derived TGF-beta. J Immunol 178 (2007) 2883-2892
16. Li X., Ye F., Chen H., Lu W., Wan X., and Xie X. Human ovarian carcinoma cells generate CD4(+)CD25(+) regulatory T cells from peripheral CD4(+)CD25(-) T cells through secreting TGF-beta. Cancer Lett 253 (2007) 144-153
17. Curti A., Pandolfi S., Valzasina B., Aluigi M., Isidori A., Ferri E., Salvestrini V., Bonanno G., Rutella S., Durelli I., et al. Modulation of tryptophan catabolism by human leukemic cells results in the conversion of CD25- into CD25+ T regulatory cells. Blood 109 (2007) 2871-2877
18. Mittal S., Marshall N.A., Duncan L., Culligan D.J., Barker R.N., and Vickers M.A. Local and systemic induction of CD4+CD25+ regulatory T cell population by non-Hodgkin's lymphoma. Blood (2008) 10.1182/blood-2007-08-105395 published online Feb 27, 2008
19. Baumgartner J., Wilson C., Palmer B., Richter D., Banerjee A., and McCarter M. Melanoma induces immunosuppression by up-regulating FOXP3(+) regulatory T cells. J Surg Res 141 (2007) 72-77
20. Sharma M.D., Baban B., Chandler P., Hou D.Y., Singh N., Yagita H., Azuma M., Blazar B.R., Mellor A.L., and Munn D.H. Plasmacytoid dendritic cells from mouse tumor-draining lymph nodes directly activate mature Tregs via indoleamine 2,3-dioxygenase. J Clin Invest 117 (2007) 2570-2582
21. Kryczek I., Zou L., Rodriguez P., Zhu G., Wei S., Mottram P., Brumlik M., Cheng P., Curiel T., Myers L., et al. B7-H4 expression identifies a novel suppressive macrophage population in human ovarian carcinoma. J Exp Med 203 (2006) 871-881
22. Siddiqui S.A., Frigola X., Bonne-Annee S., Mercader M., Kuntz S.M., Krambeck A.E., Sengupta S., Dong H., Cheville J.C., Lohse C.M., et al. Tumor-infiltrating Foxp3-CD4+CD25+ T cells predict poor survival in renal cell carcinoma. Clin Cancer Res 13 (2007) 2075-2081
23. Tzankov A., Meier C., Hirschmann P., Went P., Pileri S.A., and Dirnhofer S. Correlation of high numbers of intratumoral FOXP3+ regulatory T cells with improved survival in germinal center-like diffuse large B-cell lymphoma, follicular lymphoma and classical Hodgkin's lymphoma. Haematologica 93 (2008) 193-200
24. Kakinuma T., Nadiminti H., Lonsdorf A.S., Murakami T., Perez B.A., Kobayashi H., Finkelstein S.E., Pothiawala G., Belkaid Y., and Hwang S.T. Small numbers of residual tumor cells at the site of primary inoculation are critical for anti-tumor immunity following challenge at a secondary location. Cancer Immunol Immunother 56 (2007) 1119-1131
25. Mizukami Y., Kono K., Kawaguchi Y., Akaike H., Kamimura K., Sugai H., and Fujii H. Localisation pattern of Foxp3(+) regulatory T cells is associated with clinical behaviour in gastric cancer. Br J Cancer 98 (2008) 148-153
26. Kelley T.W., Pohlman B., Elson P., and Hsi E.D. The ratio of FOXP3+ regulatory T cells to granzyme B+ cytotoxic T/NK cells predicts prognosis in classical Hodgkin lymphoma and is independent of bcl-2 and MAL expression. Am J Clin Pathol 128 (2007) 958-965
27. Poutahidis T., Haigis K.M., Rao V.P., Nambiar P.R., Taylor C.L., Ge Z., Watanabe K., Davidson A., Horwitz B.H., Fox J.G., et al. Rapid reversal of interleukin-6-dependent epithelial invasion in a mouse model of microbially induced colon carcinoma. Carcinogenesis 28 (2007) 2614-2623
28. Betts G., Twohig J., Van den Broek M., Sierro S., Godkin A., and Gallimore A. The impact of regulatory T cells on carcinogen-induced sarcogenesis. Br J Cancer 96 (2007) 1849-1854
29. Beissert S., and Loser K. Molecular and cellular mechanisms of photocarcinogenesis. Photochem Photobiol 84 (2008) 29-34
30. Molling J.W., de Gruijl T.D., Glim J., Moreno M., Rozendaal L., Meijer C.J., van den Eertwegh A.J., Scheper R.J., von Blomberg M.E., and Bontkes H.J. 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
31. Zhou G., Drake C.G., and Levitsky H.I. Amplification of tumor-specific regulatory T cells following therapeutic cancer vaccines. Blood 107 (2006) 628-636. The first report of a cancer vaccine inducing antigen-specific Tregs.
32. Welters M.J., Kenter G.G., Piersma S.J., Vloon A.P., Lowik M.J., Berends-van der Meer D.M., Drijfhout J.W., Valentijn A.R., Wafelman A.R., Oostendorp J., et al. Induction of tumor-specific CD4+ and CD8+ T-cell immunity in cervical cancer patients by a human papillomavirus type 16 E6 and E7 long peptides vaccine. Clin Cancer Res 14 (2008) 178-187
33. Ahonen C.L., Wasiuk A., Fuse S., Turk M.J., Ernstoff M.S., Suriawinata A.A., Gorham J.D., Kedl R.M., Usherwood E.J., and Noelle R.J. Enhanced efficacy and reduced toxicity of multifactorial adjuvants compared with unitary adjuvants as cancer vaccines. Blood 111 (2008) 3116-3125
34. Chen W., Yan W., and Huang L. A simple but effective cancer vaccine consisting of an antigen and a cationic lipid. Cancer Immunol Immunother 57 (2008) 517-530
35. Yang Y., Yang S., Ye Z., Jaffar J., Zhou Y., Cutter E., Lieber A., Hellstrom I., and Hellstrom K.E. Tumor cells expressing anti-CD137 scFv induce a tumor-destructive environment. Cancer Res 67 (2007) 2339-2344
36. Palucka A.K., Ueno H., Fay J.W., and Banchereau J. Taming cancer by inducing immunity via dendritic cells. Immunol Rev 220 (2007) 129-150
37. Berhanu A., Huang J., Watkins S.C., Okada H., and Storkus W.J. Treatment-enhanced CD4+Foxp3+ glucocorticoid-induced TNF receptor family related high regulatory tumor-infiltrating T cells limit the effectiveness of cytokine-based immunotherapy. J Immunol 178 (2007) 3400-3408
38. Zabala M., Lasarte J.J., Perret C., Sola J., Berraondo P., Alfaro M., Larrea E., Prieto J., and Kramer M.G. Induction of immunosuppressive molecules and regulatory T cells counteracts the antitumor effect of interleukin-12-based gene therapy in a transgenic mouse model of liver cancer. J Hepatol 47 (2007) 807-815
39. Wei S., Kryczek I., Edwards R.P., Zou L., Szeliga W., Banerjee M., Cost M., Cheng P., Chang A., Redman B., et al. Interleukin-2 administration alters the CD4+FOXP3+ T-cell pool and tumor trafficking in patients with ovarian carcinoma. Cancer Res 67 (2007) 7487-7494
40. Tao R., de Zoeten E.F., Ozkaynak E., Chen C., Wang L., Porrett P.M., Li B., Turka L.A., Olson E.N., Greene M.I., et al. Deacetylase inhibition promotes the generation and function of regulatory T cells. Nat Med 13 (2007) 1299-1307
41. Kato Y., Yoshimura K., Shin T., Verheul H., Hammers H., Sanni T.B., Salumbides B.C., Van Erp K., Schulick R., and Pili R. Synergistic in vivo antitumor effect of the histone deacetylase inhibitor MS-275 in combination with interleukin 2 in a murine model of renal cell carcinoma. Clin Cancer Res 13 (2007) 4538-4546
42. Kang S.G., Lim H.W., Andrisani O.M., Broxmeyer H.E., and Kim C.H. Vitamin A metabolites induce gut-homing FoxP3+ regulatory T cells. J Immunol 179 (2007) 3724-3733
43. Colombo M.P., and Piconese S. Regulatory-T-cell inhibition versus depletion: the right choice in cancer immunotherapy. Nat Rev Cancer 7 (2007) 880-887
44. Piconese S., Valzasina B., and Colombo M.P. OX40 triggering blocks suppression by regulatory T cells and facilitates tumor rejection. J Exp Med 205 (2008) 825-839. The first demonstration that Treg inhibition versus depletion may be useful clinically.
45. Litzinger M.T., Fernando R., Curiel T.J., Grosenbach D.W., Schlom J., and Palena C. IL-2 immunotoxin denileukin diftitox reduces regulatory T cells and enhances vaccine-mediated T-cell immunity. Blood 110 (2007) 3192-3201
46. Liu J.Y., Wu Y., Zhang X.S., Yang J.L., Li H.L., Mao Y.Q., Wang Y., Cheng X., Li Y.Q., Xia J.C., et al. Single administration of low dose cyclophosphamide augments the antitumor effect of dendritic cell vaccine. Cancer Immunol Immunother 56 (2007) 1597-1604
47. Nair S., Boczkowski D., Fassnacht M., Pisetsky D., and Gilboa E. Vaccination against the forkhead family transcription factor Foxp3 enhances tumor immunity. Cancer Res 67 (2007) 371-380
48. Barnett B., Kryczek I., Cheng P., Zou W., and Curiel T.J. Regulatory T cells in ovarian cancer: biology and therapeutic potential. Am J Reprod Immunol 54 (2005) 369-377
49. Powell Jr. D.J., Felipe-Silva A., Merino M.J., Ahmadzadeh M., Allen T., Levy C., White D.E., Mavroukakis S., Kreitman R.J., Rosenberg S.A., et al. Administration of a CD25-directed immunotoxin, LMB-2, to patients with metastatic melanoma induces a selective partial reduction in regulatory T cells in vivo. J Immunol 179 (2007) 4919-4928
50. Powell Jr. D.J., de Vries C.R., Allen T., Ahmadzadeh M., and Rosenberg S.A. Inability to mediate prolonged reduction of regulatory T Cells after transfer of autologous CD25-depleted PBMC and interleukin-2 after lymphodepleting chemotherapy. J Immunother 30 (2007) 438-447
51. Molenkamp B.G., van Leeuwen P.A., Meijer S., Sluijter B.J., Wijnands P.G., Baars A., van den Eertwegh A.J., Scheper R.J., and de Gruijl T.D. Intradermal CpG-B activates both plasmacytoid and myeloid dendritic cells in the sentinel lymph node of melanoma patients. Clin Cancer Res 13 (2007) 2961-2969
52. Wang H.Y., Lee D.A., Peng G., Guo Z., Li Y., Kiniwa Y., Shevach E.M., and Wang R.F. Tumor-specific human CD4+ regulatory T cells and their ligands: implications for immunotherapy. Immunity 20 (2004) 107-118
53. Vence L., Palucka A.K., Fay J.W., Ito T., Liu Y.J., Banchereau J., and Ueno H. Circulating tumor antigen-specific regulatory T cells in patients with metastatic melanoma. Proc Natl Acad Sci U S A 104 (2007) 20884-20889
54. Yamaguchi T., Hirota K., Nagahama K., Ohkawa K., Takahashi T., Nomura T., and Sakaguchi S. Control of immune responses by antigen-specific regulatory T cells expressing the folate receptor. Immunity 27 (2007) 145-159
55. O'Mahony D., Morris J.C., Quinn C., Gao W., Wilson W.H., Gause B., Pittaluga S., Neelapu S., Brown M., Fleisher T.A., et al. A pilot study of CTLA-4 blockade after cancer vaccine failure in patients with advanced malignancy. Clin Cancer Res 13 (2007) 958-964
56. Song X.T., Kabler K.E., Shen L., Rollins L., Huang X.F., and Chen S.Y. A20 is an antigen presentation attenuator, and its inhibition overcomes regulatory T cell-mediated suppression. Nat Med 14 (2008) 258-265. A novel means to raise effector cell threshold to Treg suppression.
57. van der Vliet H.J., Koon H.B., Yue S.C., Uzunparmak B., Seery V., Gavin M.A., Rudensky A.Y., Atkins M.B., Balk S.P., and Exley M.A. Effects of the administration of high-dose interleukin-2 on immunoregulatory cell subsets in patients with advanced melanoma and renal cell cancer. Clin Cancer Res 13 (2007) 2100-2108
58. Curiel T.J., Coukos G., Zou L., Alvarez X., Cheng P., Mottram P., Evdemon-Hogan M., Conejo-Garcia J.R., Zhang L., Burow M., et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 10 (2004) 942-949. The first demonstration of functional Tregs in the solid human tumor mass, and first demonstration that increasing Tregs predict reduced survival in human cancer.
59. Nitcheu-Tefit J., Dai M.S., Critchley-Thorne R.J., Ramirez-Jimenez F., Xu M., Conchon S., Ferry N., Stauss H.J., and Vassaux G. Listeriolysin O expressed in a bacterial vaccine suppresses CD4+CD25high regulatory T cell function in vivo. J Immunol 179 (2007) 1532-1541
60. Pallandre J.R., Brillard E., Crehange G., Radlovic A., Remy-Martin J.P., Saas P., Rohrlich P.S., Pivot X., Ling X., Tiberghien P., et al. Role of STAT3 in CD4+CD25+FOXP3+ regulatory lymphocyte generation: implications in graft-versus-host disease and antitumor immunity. J Immunol 179 (2007) 7593-7604
61. Kurooka M., and Kaneda Y. Inactivated Sendai virus particles eradicate tumors by inducing immune responses through blocking regulatory T cells. Cancer Res 67 (2007) 227-236
62. Li B., Saouaf S.J., Samanta A., Shen Y., Hancock W.W., and Greene M.I. Biochemistry and therapeutic implications of mechanisms involved in FOXP3 activity in immune suppression. Curr Opin Immunol 19 (2007) 583-588
63. Mantel P.Y., Kuipers H., Boyman O., Rhyner C., Ouaked N., Ruckert B., Karagiannidis C., Lambrecht B.N., Hendriks R.W., Crameri R., et al. GATA3-driven Th2 responses inhibit TGF-beta1-induced FOXP3 expression and the formation of regulatory T cells. PLoS Biol 5 (2007) e329
64. Quintana FJ, Basso AS, Iglesias AH, Korn T, Farez MF, Bettelli E, Caccamo M, Oukka M, Weiner HL: Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor. Nature, 2008, 453:65-71. A novel mechanism to subvert Treg differentiation, which could turn Tregs into effector cells.
65. Kiniwa Y., Miyahara Y., Wang H.Y., Peng W., Peng G., Wheeler T.M., Thompson T.C., Old L.J., and Wang R.F. CD8+ Foxp3+ regulatory T cells mediate immunosuppression in prostate cancer. Clin Cancer Res 13 (2007) 6947-6958
66. Obeid M., Tesniere A., Ghiringhelli F., Fimia G.M., Apetoh L., Perfettini J.L., Castedo M., Mignot G., Panaretakis T., Casares N., et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 13 (2007) 54-61
67. Yano H., Ishida T., Inagaki A., Ishii T., Kusumoto S., Komatsu H., Iida S., Utsunomiya A., and Ueda R. Regulatory T-cell function of adult T-cell leukemia/lymphoma cells. Int J Cancer 120 (2007) 2052-2057
68. Hallermann C., Niermann C., and Schulze H.J. Regulatory T-cell phenotype in association with large cell transformation of mycosis fungoides. Eur J Haematol 78 (2007) 260-263