CD4 + CD25 + regulatory T cells in tumor immunity

International Immunopharmacology

Volumn 34, Issue , 2016, Pages 244-249

  Chen, Xin ^a   Du, Yong ^a   Lin, XiuQing ^a   Qian, Yan ^a   Zhou, Ting ^a   Huang, ZhiMing ^a  

^a WENZHOU MEDICAL UNIVERSITY   (China)

Author keywords

CD4 + CD25 + regulatory T cell; CTLA 4; Foxp3; GITR; Tumor immunity

Indexed keywords

CASEIN KINASE II; CD4 ANTIGEN; CETUXIMAB; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; DACARBAZINE; GAMMA INTERFERON; GLUCOCORTICOID INDUCED TUMOR NECROSIS FACTOR RECEPTOR; GLYCOPROTEIN GP 100; GRANZYME B; HUMAN MONOCLONAL ANTIBODY; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 35; IPILIMUMAB; MACROPHAGE DERIVED CHEMOKINE; MICRORNA; MICRORNA 146A; MICRORNA 146B; PEPTIDE VACCINE; TICILIMUMAB; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; UNCLASSIFIED DRUG; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; TUMOR ANTIGEN;

AUTOIMMUNE DISEASE; BREAST CARCINOMA; CANCER GROWTH; CANCER IMMUNOTHERAPY; CANCER RADIOTHERAPY; CANCER THERAPY; CASTRATION RESISTANT PROSTATE CANCER; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; COLORECTAL CANCER; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; DENDRITIC CELL; EFFECTOR CELL; ENHANCER REGION; GENE EXPRESSION; HUMAN; IMMUNE DEFICIENCY; IMMUNE EVASION; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; IMMUNOSURVEILLANCE; INFLAMMATORY DISEASE; LUNG CANCER; LYMPHOCYTE PROLIFERATION; MACROPHAGE; METASTATIC MELANOMA; MONOCYTE; NATURAL KILLER CELL; ONCOLOGICAL PARAMETERS; OVERALL SURVIVAL; PANCREAS CARCINOMA; PRIORITY JOURNAL; RADIATION INDUCED NEOPLASM; REGULATORY T LYMPHOCYTE; REVIEW; SIGNAL TRANSDUCTION; STOMACH CARCINOMA; T CELL DEPLETION; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; ANIMAL; CD4+ T LYMPHOCYTE; IMMUNOLOGY; METABOLISM; NEOPLASM;

ANIMALS; ANTIGENS, NEOPLASM; CD4-POSITIVE T-LYMPHOCYTES; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; NEOPLASMS; T-LYMPHOCYTES, REGULATORY;

EID: 84960871162     PISSN: 15675769     EISSN: 18781705     Source Type: Journal    
DOI: 10.1016/j.intimp.2016.03.009     Document Type: Review

References (114)

1. R.K. Gershon, P. Cohen, R. Hencin, and S.A. Liebhaber Suppressor T cells J. Immunol. 108 3 1972 586 590
2. S. Sakaguchi, N. Sakaguchi, M. Asano, M. Itoh, and M. Toda 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. 155 3 1995 1151 1164
3. R.S. McHugh, M.J. Whitters, C.A. Piccirillo, D.A. Young, E.M. Shevach, M. Collins, and M.C. Byrne CD4(+)CD25(+) immunoregulatory T cells: gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor Immunity 16 2 2002 311 323
4. J. Shimizu, S. Yamazaki, T. Takahashi, Y. Ishida, and S. Sakaguchi Stimulation of CD25 + CD4 + regulatory T cells through GITR breaks immunological self-tolerance Nat. Immunol. 3 2 2002 135 142
5. S. Jiang Regulatory T cells: from bench to bedside Int. Immunopharmacol. 9 5 2009 515 517
6. J.A. Bluestone, E. Trotta, and D. Xu The therapeutic potential of regulatory T cells for the treatment of autoimmune disease Expert Opin. Ther. Targets 19 8 2015 1091 1103
7. S. Yang, N. Fujikado, D. Kolodin, C. Benoist, and D. Mathis Immune tolerance. Regulatory T cells generated early in life play a distinct role in maintaining self-tolerance Science 348 6234 2015 589 594
8. A. Caramibia, B. Freund, D. Schwinge, and et al. Nanoparticle-based autoantigen delivery to Treg-inducing liver sinusoidal endothelial cells enables control of autoimmunity in mice J. Hepatol. 62 6 2015 1349 1356
9. M. Schmaler, M.A. Broggi, N. Lagarde, B.F. Stocklin, C.G. King, D. Finke, and S.W. Rossi IL-7R signaling in regulatory T cells maintains peripheral and allograft tolerance in mice Proc. Natl. Acad. Sci. U. S. A. 112 43 2015 13330 13335
10. R. Yang, C. Qu, Y. Zhou, and et al. Hydrogen sulfide promotes Tet1- and Tet2-mediated Foxp3 demethylation to drive regulatory T cell differentiation and maintain immune homeostasis Immunity 43 2 2015 251 263
11. Y. Gao, J. Tang, W. Chen, and et al. Inflammation negatively regulates FOXP3 and regulatory T-cell function via DBC1 Proc. Natl. Acad. Sci. U. S. A. 112 25 2015 3246 3254
12. J.A. Bluestone Regulatory T-cell therapy: is it ready for the clinic? Nat. Rev. Immunol. 5 4 2005 343 349
13. S. Jiang, J. Tsang, and P. Tam Regulatory T cell immunotherapy for transplantation tolerance: step into clinic Int. Immunopharmacol. 10 12 2010 1486 1490
14. A. Ma, S. Qi, Z. Wang, E. Massicotte, M. Dupuis, P. Daloze, and H. Chen Combined therapy of CD4(+)CD25(+) regulatory T cells with low-dose sirolimus, but not calcineurin inhibitors, preserves suppressive function of regulatory T cells and prolongs allograft survival in mice Int. Immunopharmacol. 9 5 2009 553 563
15. D. Golshayan, J.C. Wyss, C.W. Abulker, S.C. Schaefer, R.I. Lechler, H.A. Lehr, and M. Pascual Transplantation tolerance induced by regulatory T cells: in vivo mechanisms and sites of action Int. Immunopharmacol. 9 6 2009 683 688
16. S. Jiang, D. Golshayan, J. Tsang, G. Lombardi, and R.I. Lechler In vitro expanded alloantigen-specific CD4 + CD25 + regulatory T cell treatment for the induction of donor-specific transplantation tolerance Int. Immunopharmacol. 6 2006 1879 1882
17. N. Ohkura, M. Hamaguchi, H. Morikawa, and et al. T cell receptor stimulation-induced epigenetic changes and Foxp3 expression are independent and complementary events required for Treg cell development Immunity 37 2012 785 799
18. S. Sakaguchi Naturally arising CD4 + regulatory t cells for immunologic self-tolerance and negative control of immune responses Annu. Rev. Immunol. 22 2004 531 562
19. S. Zelenay, T. Lopes-Carvalho, I. Caramalho, M.F. Moraes-Fontes, M. Rebelo, and J. Demengeot 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
20. L. Cassis, S. Aiello, and M. Noris Natural versus adaptive regulatory T cells Contrib. Nephrol. 146 2005 121 131
21. M. Miyara, Y. Yoshioka, A. Kitoh, and et al. Functional delineation and differentiation dynamics of human CD4 + T cells expressing the Foxp3 transcription factor Immunity 30 6 2009 899 911
22. K. Wing, and S. Sakaguchi Regulatory T cells exert checks and balances on self tolerance and autoimmunity Nat. Immunol. 11 1 2010 7 13
23. T. Bopp, C. Becker, M. Klein, and et al. Cyclic adenosine monophosphate is a key component of regulatory T cell-mediated suppression J. Exp. Med. 204 2007 1303 1310
24. N. Arpaia, J.A. Green, B. Moltedo, A. Arvey, S. Hemmers, S. Yuan, P.M. Treuting, and A.Y. Rudensky A distinct function of regulatory T cells in tissue protection Cell 162 5 2015 1078 1089
25. K. Kretschmer, I. Apostolou, E. Jaeckel, K. Khazaie, and H. von Boehmer Making regulatory T cells with defined antigen specificity: role in autoimmunity and cancer Immunol. Rev. 212 2006 163 169
26. D.A. Vignali, L.W. Collison, and C.J. Workman How regulatory T cells work Nat. Rev. Immunol. 8 7 2008 523 532
27. S.Z. Josefowicz, L.F. Lu, and A.Y. Rudensky Regulatory T cells: mechanisms of differentiation and function Annu. Rev. Immunol. 30 2012 531 564
28. F. Ghiringhelli, P.E. Puig, S. Roux, A. Parcellier, E. Schmitt, E. Solary, G. Kroemer, F. Martin, B. Chauffert, and L. Zitvogel Tumor cells convert immature myeloid dendritic cells into TGF-beta-secreting cells inducing CD4 + CD25 + regulatory T cell proliferation J Exp Med 202 2005 919 929
29. J.D. Fontenot, J.P. Rasmussen, L.M. Williams, J.L. Dooley, A.G. Farr, and A.Y. Rudensky Regulatory T cell lineage specification by the forkhead transcription factor foxp3 Immunity 22 3 2005 329 341
30. S. Hori, T. Nomura, and S. Sakaguchi Control of regulatory T cell development by the transcription factor Foxp3 Science 299 2003 1057 1061
31. Z. Chen, F. Lin, Y. Gao, Z. Li, J. Zhang, Y. Xing, and et al. FOXP3 and RORγt: transcriptional regulation of Treg and Th17 Int. Immunopharmacol. 11 5 2011 536 542
32. R.M. Samstein, A. Arvey, S.Z. Josefowicz, and et al. Foxp3 exploits a pre-existent enhancer landscape for regulatory T cell lineage specification Cell 151 1 2012 153 166
33. S. Sakaguchi, K. Wing, and M. Miyara Regulatory T cells - a brief history and perspective Eur. J. Immunol. 37 2007 116 123
34. A.Y. Rudensky Regulatory T cells and Foxp3 Immunol. Rev. 241 1 2011 260 268
35. W. Lin, N. Truong, W.J. Grossman, D. Haribhai, C.B. Williams, J. Wang, M.G. Martin, and T.A. Chatila Allergic dysregulation and hyperimmunoglobulinemia E in Foxp3 mutant mice J. Allergy Clin. Immunol. 116 2005 1106 1115
36. S. Read, V. Malmstrom, and F. Powrie Cytotoxic T lymphocyte-associated antigen 4 plays an essential role in the function of CD25(+)CD4(+) regulatory cells that control intestinal inflammation J Exp Med 192 2000 295 302
37. T. Takahashi, T. Tagami, S. Yamazaki, T. Uede, J. Shimizu, N. Sakaguchi, T.W. Mak, and S. Sakaguchi Immunologic self-tolerance maintained by CD25(+)CD4(+) regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4 J. Exp. Med. 192 2000 303 310
38. N. Jain, H. Nguyen, C. Chambers, and J. Kang Dual function of CTLA-4 in regulatory T cells and conventional T cells to prevent multiorgan autoimmunity Proc. Natl. Acad. Sci. U. S. A. 107 2010 1524 1528
39. K. Wing, Y. Onishi, P. Prieto-Martin, T. Yamaguchi, M. Miyara, Z. Fehervari, T. Nomura, and S. Sakaguchi CTLA-4 control over Foxp3 + regulatory T cell function Science 322 5899 2008 271 275
40. K. Wing, T. Yamaguchi, and S. Sakaguchi Cell-autonomous and-non-autonomous roles of CTLA-4 in immune regulation Trends Immunol. 32 9 2011 428 433
41. T. Yamaguchi, A. Kishi, M. Osaki, H. Morikawa, P. Prieto-Martin, K. Wing, T. Saito, and S. Sakaguchi Construction of self-recognizing regulatory T cells from conventional T cells by controlling CTLA-4 and IL-2 expression Proc. Natl. Acad. Sci. U. S. A. 110 23 2013 116 125
42. J.B. Wing, and S. Sakaguchi Multiple treg suppressive modules and their adaptability Front. Immunol. 3 2012 178
43. C. Oderup, L. Cederbom, A. Makowska, C.M. Cilio, and F. Ivars Cytotoxic T lymphocyte antigen-4-dependent down-modulation of costimulatory molecules on dendritic cells in CD4 + CD25 + regulatory T-cell-mediated suppression Immunology 118 2 2006 240 249
44. Y. Onishi, Z. Fehervari, T. Yamaguchi, and S. Sakaguchi Foxp3 + natural regulatory T cells preferentially form aggregates on dendritic cells in vitro and actively inhibit their maturation Proc. Natl. Acad. Sci. U. S. A. 105 29 2008 10113 10118
45. H. von Boehmer Mechanisms of suppression by suppressor T cells Nat. Immunol. 6 2005 338 344
46. A. Izcue, J.L. Coombes, and F. Powrie Regulatory T cells suppress systemic and mucosal immune activation to control intestinal inflammation Immunol. Rev. 212 2006 256 271
47. W. Zou Regulatory T cells, tumor immunity and immunotherapy Nat. Rev. Immunol. 6 2006 295 307
48. O. Palomares, M. Martin-Fontecha, R. Launer, C. Traidl-Hoffmann, O. Cavkaytar, M. Akdis, and C.A. Akdis Regulatory T cells and immune regulation of allergic diseases: roles of IL-10 and TGF-β Genes Immun. 15 8 2014 511 520
49. E.A. Green, L. Gorelik, C.M. McGregor, E.H. Tran, and R.A. Flavell CD4 + CD25 + T regulatory cells control anti-islet CD8 + T cells through TGF-beta-TGF-beta receptor interactions in type 1 diabetes Proc. Natl. Acad. Sci. U. S. A. 100 2003 10878 10883
50. M.L. Chen, M.J. Pittet, L. Gorelik, R.A. Flavell, R. Weissleder, H. von Boehmer, and K. Khazaie Regulatory T cells suppress tumor-specific CD8 T cell cytotoxicity through TGF-beta signals in vivo Proc. Natl. Acad. Sci. U. S. A. 102 2005 419 424
51. L.W. Collison, C.J. Workman, T.T. Kuo, K. Boyd, Y. Wang, K.M. Viqnali, R. Cross, D. Sehy, R.S. Blumberg, and D.A. Viqnali The inhibitory cytokine IL-35 contributes to regulatory T-cell function Nature 450 2007 566 569
52. P. Pandiyan, L. Zheng, S. Ishihara, J. Reed, and Lenardo MJ CD4 + CD25 + Foxp3 + regulatory T cells induce cytokine deprivation-mediated apoptosis of effector CD4 + T cells Nat. Immunol. 8 12 2007 1353 1362
53. O. Akbari, G.J. Freeman, E.H. Meyer, E.A. Greenfield, T.T. Chang, A.H. Sharpe, G. Berry, R.H. DeKruyff, and D.T. Umetsu Antigen-specific regulatory T cells develop via the ICOS-ICOS-ligand pathway and inhibit allergen-induced airway hyperreactivity Nat. Med. 8 2002 1024 1032
54. A. Ulges, M. Klein, S. Reuter, and et al. Protein kinase CK2 enables regulatory T cells to suppress excessive TH2 responses in vivo Nat. Immunol. 16 3 2015 267 275
55. C. Chen, D. Chen, Y. Zhang, Z. Chen, W. Zhu, and et al. Changes of CD4 + CD25 + FOXP3 + and CD8 + CD28-regulatory T cells in non-small cell lung cancer patients undergoing surgery Int. Immunopharmacol. 18 2 2014 255 261
56. S.T. Ward, K.K. Li, and E. Hepburn The effects of CCR5 inhibition on regulatory T-cell recruitment to colorectal cancer Br. J. Cancer 112 2 2015 319 328
57. Y. Mizukami, K. Kono, Y. Kawaguchi, H. Akaike, K. Kamimura, H. Suqai, and H. Fujii Localisation pattern of Foxp3 + regulatory T cells is associated with clinical behaviour in gastric cancer Br. J. Cancer 98 2008 148 153
58. D. Nummer, E. Suri-payer, and H. Schmitz-Winnenthal Role of tumor endothelium in CD4 + CD25 + regulatory T cell infiltration of human pancreatic carcinoma J. Natl. Cancer Inst. 99 2007 1188 1199
59. U.K. Liyanage, T.T. Moore, and H.G. Joo Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma J. Immunol. 169 2002 2756 2761
60. L.A. Ormandy, T. Hillemann, H. Wedemeyer, M.P. Manns, T.F. Greten, and F. Korangy Increased populations of regulatory T cells in peripheral blood of patients with hepatocellular carcinoma Cancer Res. 65 2005 2457 2464
61. S. Hontsu, H. Yoneyama, S. Ueha, Y. Terashima, M. Kitabatake, A. Nakano, T. Ito, H. Kimura, and K. Matsushima Visualization of naturally occurring Foxp3 + regulatory T cells in normal and tumor-bearing mice Int. Immunopharmacol. 4 14 2004 1785 1793
62. M. Haas, A. Dimmler, W. Hohenberger, G.G. Grabenbauer, G. Niedobitek, and L.V. Distel Stromal regulatory T-cells are associated with a favourable prognosis in gastric cancer of the cardia BMC Gastroenterol. 9 2009 65
63. Z.K. Wang, B. Yang, H. Liu, Y. Hu, J.L. Yang, L.L. Wu, Z.H. Zhou, and S.C. Jiao Regulatory T cells increase in breast cancer and in stage IV breast cancer Cancer Immunol. Immunother. 61 6 2012 911 916
64. E.J. Sayour, P. Mclendon, R. Mclendon, G. De Leon, R. Reynolds, J. Kresak, J.H. Sampson, and D.A. Mitchell Increased proportion of FoxP3 + regulatory T cells in tumor infiltrating lymphocytes is associated with tumor recurrence and reduced survival in patients with glioblastoma Cancer Immunol. Immunother. 64 4 2015 419 427
65. X. Shen, N. Li, H. Li, T. Zhang, F. Wang, and Q. Li Increased prevalence of regulatory T cells in the tumor microenvironment and its correlation with TNM stage of hepatocellular carcinoma J. Cancer Res. Clin. Oncol. 136 11 2010 1745 1754
66. J. Fu, D. Xu, Z. Liu, and et al. Increased regulatory T cells correlate with CD8 T-cell impairment and poor survival in hepatocellular carcinoma patients Gastroenterology 132 7 2007 2328 2339
67. E. Pastille, K. Bardini, D. Fleissner, and et al. Transient ablation of regulatory T cells improves antitumor immunity in colitis-associated colon cancer Cancer Res. 74 16 2014 4258 4269
68. P. Yu, Y. Lee, W. Liu, T. Krausz, A. Chong, H. Schreiber, and Y.X. Fu Intratumor depletion of CD4 + cells unmasks tumor immunogenicity leading to the rejection of late-stage tumors J. Exp. Med. 201 2005 779 791
69. V. Farsam, Z.M. Hassan, A. Zavaran-Hosseini, S. Noori, M. Mahdavi, and M. Ranjbar Antitumor and immunomodulatory properties of artemether and its ability to reduce CD4 + CD25 + Foxp3 + Treg cells in vivo Int. Immunopharmacol. 11 11 2011 1802 1808
70. G.P. Dunn, A.T. Bruce, H. Ikeda, L.J. Old, and Schreiber RD Cancer immunoediting: from immunosurveillance to tumor escape Nat. Immunol. 3 11 2002 991 998
71. S. Malchow, D.S. Leventhal, S. Nishi, and et al. Aire-dependent thymic development of tumor-associated regulatory T cells Science 339 2013 1219 1224
72. A.A. Tveita, F. Schjesvold, O.A. Haabeth, M. Fauskanger, and B. Bogen Tumors escape CD4 + T-cell-mediated immunosurveillance by impairing the ability of infiltrating macrophages to indirectly present tumor antigens Cancer Res. 75 16 2015 3268 3278
73. X. Cao, S.F. Cai, T.A. Fehniqer, J. Song, L.I. Collins, D.R. Piwnica-Worms, and T.J. Ley Granzyme B and perforin are important for regulatory T cell-mediated suppression of tumor clearance Immunity 27 2007 635 646
74. W.J. Grossman, J.W. Verbsky, W. Barchet, M. Colonna, J.P. Atkinson, and T.J. Ley Human T regulatory cells can use the perforin pathway to cause autologous target cell death Immunity 21 2004 589 601
75. F. Yan, R. Du, F. Wei, and et al. Expression of TNFR2 by regulatory T cells in peripheral blood is correlated with clinical pathology of lung cancer patients Cancer Immunol. Immunother. 64 11 2015 1475 1485
76. T.J. Curiel, G. Coukos, L. Zou, and et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival Nat. Med. 10 2004 942 949
77. G. Zhou, and H.I. Levitsky Natural regulatory T cells and de novo-induced regulatory T cells contribute independently to tumor-specific tolerance J. Immunol. 178 2007 2155 2162
78. A. Pedroza-Gonzalez, G. Zhou, S.P. Singh, and et al. GITR engagement in combination with CTLA-4 blockade completely abrogates immunosuppression mediated by human liver tumor-derived regulatory T cells ex vivo Oncoimmunology 2015 4(12)
79. A. Pedroza-Gonzalez, C. Verhoef, J.N. Ijzermans, M.P. Peppelenbosch, J. Kwekkeboom, J. Verheij, H.L. Janssen, and D. Sprengers Activated tumor-infiltrating CD4 + regulatory T cells restrain antitumor immunity in patients with primary or metastatic liver cancer Hepatology 57 1 2013 183 194
80. C.H. Li, W.H. Kuo, W.C. Chang, S.C. Huang, K.J. Chang, and B.C. Sheu Activation of regulatory T cells instigates functional down-regulation of cytotoxic T lymphocytes in human breast cancer Immunol. Res. 51 1 2011 71 79
81. P. Akeus, V. Langenes, J. Kristensen, A. von Mentzer, T. Sparwasser, S. Raqhavan, and M. Quiding-Järbrink Treg-cell depletion promotes chemokine production and accumulation of CXCR3(+) conventional T cells in intestinal tumors Eur. J. Immunol. 45 6 2015 1654 1666
82. T.R. Simpson, F. Li, W. Montalvo-Ortiz, and et al. Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma J. Exp. Med. 210 2013 1695 1710
83. N. Redjimi, C. Raffin, I. Raimbaud, P. Pignon, J. Matsuzaki, K. Odunsi, D. Valmori, and M. Ayyoub CXCR3 + T regulatory cells selectively accumulate in human ovarian carcinomas to limit type I immunity Cancer Res. 72 17 2012 4351 4360
84. J. Zhou, T. Ding, W. Pan, L.Y. Zhu, L. Li, and L. Zheng Increased intratumoral regulatory T cells are related to intratumoral macrophages and poor prognosis in hepatocellular carcinoma patients Int. J. Cancer 125 7 2009 1640 1648
85. C.A. Bauer, E.Y. Kim, F. Marangoni, E. Carrizosa, N.M. Claudio, and T.R. Mempel Dynamic Treg interactions with intratumoral APCs promote local CTL dysfunction J. Clin. Invest. 124 6 2014 2425 2440
86. C.H. Yuan, X.M. Sun, C.L. Zhu, S.P. Liu, L. Wu, H. Chen, M.H. Feng, K. Wu, and F.B. Wang Amphiregulin activates regulatory T lymphocytes and suppresses CD8 + T cell-mediated anti-tumor response in hepatocellular carcinoma cells Oncotarget 6 31 2015 32138 32153
87. L.Y. Chang, Y.C. Lin, J.M. Chiang, and et al. Blockade of TNF-α signaling benefits cancer therapy by suppressing effector regulatory T cell expansion Oncoimmunology 2015 4(10)
88. R.B. Holmgaad, D. Zamarin, Y. Li, B. Gasmi, D.H. Munn, J.P. Allison, T. Merghoub, and J.D. Wolchok Tumor-expressed IDO Recruits and activates MDSCs in a Treg-dependent manner Cell Rep. 13 2 2015 412 424
89. Z. Que, F. Zou, A. Zhang, Y. Zheng, L. Bi, J. Zhong, and et al. Ganoderic acid Me induces the apoptosis of competent T cells and increases the proportion of Treg cells through enhancing the expression and activation of indoleamine 2,3-dioxygenase in mouse lewis lung cancer cells Int. Immunopharmacol. 23 1 2014 192 204
90. J.D. Waight, S. Takai, B. Marelli, and et al. Cutting edge: epigenetic regulation of Foxp3 defines a stable population of CD4 + regulatory T cells in tumors from mice and humans J. Immunol. 194 3 2015 878 882
91. R. Liu, C. Liu, D. Chen, and et al. FOXP3 controls an miR-146/NF-κB negative feedback loop that inhibits apoptosis in breast cancer cells Cancer Res. 75 8 2015 1703 1713
92. B. Azzimonti, E. Zavattaro, M. Provasi, M. Vidali, A. Conca, E. Catalano, L. Rimondini, E. Colombo, and G. Valente Intense Foxp3 + CD25 + regulatory T-cell infiltration is associated with high-grade cutaneous squamous cell carcinoma and counterbalanced by CD8 +/Foxp3 + CD25 + ratio Br. J. Dermatol. 172 1 2015 64 73
93. G. Du, Y. Liu, J. Li, W. Liu, Y. Wang, and H. Li Hypothermic microenvironment plays a key role in tumor immune subversion Int. Immunopharmacol. 17 2 2013 245 253
94. D.M. Hossain, A.K. Panda, A. Manna, and et al. FoxP3 acts as a cotranscription factor with STAT3 in tumor-induced regulatory T cells Immunity 39 6 2013 1057 1069
95. Y. Hasegawa, S. Takanashi, Y. Kanehira, T. Tsushima, T. Imai, and K. Okumura Transforming growth factor-beta1 level correlates with angiogenesis, tumor progression, and prognosis in patients with nonsmall cell lung carcinoma Cancer 91 2001 964 971
96. L. Gorelik, and R.A. Flavell Immune-mediated eradication of tumors through the blockade of transforming growth factor-beta signaling in T cells Nat. Med. 7 2001 1118 1122
97. Y. Shen, Y. Wei, Z. Wang, and et al. TGF-β regulates hepatocellular carcinoma progression by inducing Treg cell polarization Cell. Physiol. Biochem. 35 4 2015 1623 1632
98. T.A. Moo-Young, J.W. Larson, B.A. Belt, M.C. Tan, W.G. Hawkins, T.J. Eberlein, P.S. Goedegebuure, and D.C. Linehan Tumor-derived TGF-beta mediates conversion of CD4 + Foxp3 + regulatory T cells in a murine model of pancreas cancer J. Immunother. 32 2009 12 21
99. S. Yamazaki, T. Iyoda, K. Tarbell, K. Olson, K. Velinzon, K. Inaba, and R.M. Steinman Direct expansion of functional CD25 + CD4 + regulatory T cells by antigen-processing dendritic cells J. Exp. Med. 198 2 2003 235 247
100. R.N. Ramos, L.S. Chin, A.P. Dos Santos, P.C. Bergami-Santos, F. Laginha, and J.A. Barbuto Monocyte-derived dendritic cells from breast cancer patients are biased to induce CD4 + CD25 + Foxp3 + regulatory T cells J. Leukoc. Biol. 92 3 2012 673 682
101. N.S. Joshi, E.H. Akama-garren, Y. Lu, and et al. Regulatory T Cells in tumor-associated tertiary lymphoid structures suppress anti-tumor T cell responses Immunity 43 3 2015 579 590
102. M.H. Jeong, K.M. Yang, Y.J. Choi, S.D. Kim, Y.H. Yoo, and et al. Resveratrol analog, HS-1793 enhance anti-tumor immunity by reducing the CD4 + CD25 + regulatory T cells in FM3A tumor bearing mice Int. Immunopharmacol. 14 3 2012 328 333
103. S. Liu, X. Sun, J. Luo, H. Zhu, X. Yang, and et al. Effects of radiation on T regulatory cells in normal states and cancer: mechanisms and clinical implications Am. J. Cancer Res. 5 11 2015 3276 3285
104. C. Twyman-Saint Victor, A.J. Rech, A. Maity, R. Rengan, K.E. Pauken, and et al. Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer Nature 520 7547 2015 373 377
105. J.D. Wolchok, H. Kluger, M.K. Callahan, M.A. Postow, N.A. Rizvi, and et al. Nivolumab plus ipilimumab in advanced melanoma N. Engl. J. Med. 369 2013 122 133
106. L. Wu, Wu Mo, L. De la Maza, Z. Yun, and et al. Targeting the inhibitory receptor CTLA-4 on T cells increased abscopal effects in murine mesothelioma model Oncotarget 6 14 2015 12468 12480
107. E. Cha, and et al. Improved survival with T cell clonotype stability after anti-CTLA-4 treatment in cancer patients Sci. Transl. Med. 6 238 2014 ra70 238ra70
108. C.A. Chambers, M.S. Kuhns, J.G. Egen, and J.P. Allison CTLA-4-mediated inhibition in regulation of T cell responses: mechanisms and manipulation in tumor immunotherapy Annu. Rev. Immunol. 19 2001 565 594
109. I. Mellman, G. Coukos, and G. Dranoff Cancer immunotherapy comes of age Nature 480 7378 2011 480 489
110. F.S. Hodi, S.J. O'Day, D.F. McDermott, R.W. Weber, J.A. Sosman, and et al. Improved survival with ipilimumab in patients with metastatic melanoma N. Engl. J. Med. 363 2010 711 723
111. C. Robert, L. Thomas, I. Bondarenko, S. O'Day, J. Weber, and et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma N. Engl. J. Med. 364 2011 2517 2526
112. E.D. Kwon, C.G. Drake, H.I. Scher, K. Fizazi, A. Bossi, and et al. Ipilimumab versus placebo after radiotherapy in patients with metastatic castration-resistant prostate cancer that had progressed after docetaxel chemotherapy (CA184-043): a multicentre, randomised, double-blind, phase 3 trial Lancet Oncol. 15 7 2014 700 712
113. A.M. Grimaldi, E. Simeone, D. Giannarelli, P. Muto, S. Falivene, and et al. Abscopal effects of radiotherapy on advanced melanoma patients who progressed after ipilimumab immunotherapy Oncoimmunology 3 2014
114. H.B. Jie, P.J. Schuler, S.C. Lee, R.M. Srivastava, A. Argiris, S. Ferrone, and T.L. Whiteside Ferris RL.CTLA-4 regulatory T Cells increased in cetuximab-treated head and neck cancer patients suppress NK Cell cytotoxicity and correlate with poor prognosis Cancer Res. 75 11 2015 2200 2210