The opposing roles of CD4+ T cells in anti-tumour immunity

Immunology

Volumn 154, Issue 4, 2018, Pages 582-592

  Ahrends, Tomasz ^a   Borst, Jannie ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

cancer; CD4 cell; regulatory T cell; T cell; tumour immunology

Indexed keywords

CXCL9 CHEMOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10;

ADOPTIVE TRANSFER; CANCER IMMUNOTHERAPY; CANCER PATIENT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL KILLING; CELL TRANSFER; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; HUMAN; IMMUNOMODULATION; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; T CELL DEPLETION; TUMOR IMMUNITY;

EID: 85050112025     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12941     Document Type: Review

References (133)

1. Danke NA, Koelle DM, Yee C, Beheray S, Kwok WW. Autoreactive T cells in healthy individuals. J Immunol 2004; 172:5967–72
2. + regulatory T cells: their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance. Immunol Rev 2001; 182:18–32
3. + T cell deletion induced by cross-presentation of self-antigens and favors autoimmunity. J Exp Med 1997; 186:2057–62
4. + T cells in anti-tumor immune responses. Immunol Rev 2008; 222:129–44
5. Josefowicz SZ, Lu L-F, Rudensky AY. Regulatory T cells: mechanisms of differentiation and function. Annu Rev Immunol 2012; 30:531–64
6. + T-cell response. Nat Rev Immunol 2004; 4:595–602
7. + T-helper and a T-killer cell. Nature 1998; 393:474–8
8. Wiesel M, Kratky W, Oxenius A. Type I IFN substitutes for T cell help during viral infections. J Immunol 2011; 186:754–63
9. + T lymphocytes from cancer patients are required for optimal induction of cytotoxic T cells against the autologous tumor. J Immunol 2000; 164:3902–12
10. Marzo AL, Lake RA, Robinson BW, Scott B. T-cell receptor transgenic analysis of tumor-specific CD8 and CD4 responses in the eradication of solid tumors. Cancer Res 1999; 59:1071–9
11. Knocke S, Fleischmann-Mundt B, Saborowski M, Manns MP, Kühnel F, Wirth TC et al. Tailored tumor immunogenicity reveals regulation of CD4 and CD8 T cell responses against cancer. Cell Rep 2016; 17:2234–46
12. Ott PA, Hu Z, Keskin DB, Shukla SA, Sun J, Bozym DJ et al. An immunogenic personal neoantigen vaccine for patients with melanoma. Nature 2017; 547:217–21
13. Sahin U, Derhovanessian E, Miller M, Kloke BP, Simon P, Löwer M et al. Personalized RNA mutanome vaccines mobilize poly-specific therapeutic immunity against cancer. Nature 2017; 547:222–6
14. Scurr M, Pembroke T, Bloom A, Roberts D, Thomson A, Smart K et al. Effect of modified vaccinia Ankara–5T4 and low-dose cyclophosphamide on antitumor immunity in metastatic colorectal cancer: a randomized clinical trial. JAMA Oncol 2017; 3:1–9
15. Bennett SRM, Carbone FR, Karamalis F, Flavell RA, Miller JFAP, Heath WR. Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature 1998; 393:478–80
16. Eickhoff S, Brewitz A, Gerner MY, Klauschen F, Komander K, Hemmi H et al. Robust anti-viral immunity requires multiple distinct T cell-dendritic cell interactions. Cell 2015; 162:1322–37
17. + T cell activation to localized viral infection. Immunity 2015; 43:554–65
18. + T cell priming. Cell Rep 2016; 14:586–97
19. Filatenkov AA, Jacovetty EL, Fischer UB, Curtsinger JM, Mescher MF, Ingulli E. CD4 T cell-dependent conditioning of dendritic cells to produce IL-12 results in CD8-mediated graft rejection and avoidance of tolerance. J Immunol 2005; 174:6909–17
20. + T cells. J Immunol 2005; 174:710–7
21. + T cell help confers a cytotoxic T cell effector program including coinhibitory receptor downregulation and increased tissue invasiveness. Immunity 2017; 47:848–61.e5
22. + T-cells via CD27–CD70 interactions. Nat Commun 2012; 3:1948
23. Prilliman KR, Lemmens EE, Palioungas G, Wolfe TG, Allison JP, Sharpe AH et al. Cutting edge: a crucial role for B7-CD28 in transmitting T help from APC to CTL. J Immunol 2002; 169:4094–7
24. Peperzak V, Xiao Y, Veraar EAM, Borst J. CD27 sustains survival of CTLs in virus-infected nonlymphoid tissue in mice by inducing autocrine IL-2 production. J Clin Invest 2010; 120:168–78
25. + T cell–dendritic cell interaction. Nature 2006; 440:890–5
26. + T cells elicit host immune responses to MHC class II-negative ovarian cancer through CCL5 secretion and CD40-mediated licensing of dendritic cells. J Immunol 2010; 184:5654–62
27. + T cells support cytotoxic T lymphocyte priming by controlling lymph node input. Proc Natl Acad Sci USA 2011; 108:8749–54
28. + T cells involving acquired MHC class II:peptide complexes: another mechanism to limit clonal expansion? Blood 2003; 101:2704–10
29. + T cell responses. Nat Commun 2017; 8:1591
30. + T cell responses of low antigen affinity to protect against viral variants. Immunity 2011; 35:97–108
31. + T cell reactivity to a model tumor antigen. J Immunol 2000; 164:562–5
32. + T cells. J Immunol 2008; 180:3122–31
33. + T cells. J Immunol 2016; 197:1809–22
34. + T cells. Eur J Immunol 2014; 44:69–79
35. + T-cell help in therapeutic anticancer vaccination. Cancer Res 2016; 76:2921–31
36. Jiang Y, Li Y, Zhu B. T-cell exhaustion in the tumor microenvironment. Cell Death Dis 2015; 6:1–9
37. + cytotoxic T-cell responses during chronic viral infection. J Virol 1994; 68:8056–63
38. + T cell help over the course of persistent infection. J Immunol 2007; 179:1113–21
39. Aubert RD, Kamphorst AO, Sarkar S, Vezys V, Ha S-J, Barber DL et al. Antigen-specific CD4 T-cell help rescues exhausted CD8 T cells during chronic viral infection. Proc Natl Acad Sci 2011; 108:21182–7
40. Elsaesser H, Sauer K, Brooks DG. IL-21 is required to control chronic viral infection. Science 2009; 324:1569–72
41. Frohlich A, Kisielow J, Schmitz I, Freigang S, Shamshiev AT, Weber J et al. IL-21R on T cells is critical for sustained functionality and control of chronic viral infection. Science 2009; 324:1576–80
42. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003; 299:1057–61
43. Vignali DAA, Collison LW, Workman CJ. How regulatory T cells work. Nat Rev Immunol 2008; 8:523–32
44. Frydrychowicz M, Boruczkowski M, Kolecka-Bednarczyk A, Dworacki G. The dual role of Treg in cancer. Scand J Immunol 2017; 86:436–43
45. + natural regulatory T cells preferentially form aggregates on dendritic cells in vitro and actively inhibit their maturation. Proc Natl Acad Sci 2008; 105:10113–8
46. + T cells and dendritic cells in vivo. J Exp Med 2006; 203:505–11
47. Tang Q, Adams JY, Tooley AJ, Bi M, Fife BT, Serra P et al. Visualizing regulatory T cell control of autoimmune responses in nonobese diabetic mice. Nat Immunol 2006; 7:83–92
48. Walker LSK. Treg and CTLA-4: two intertwining pathways to immune tolerance. J Autoimmun 2013; 45:49–57
49. Liang B, Workman C, Lee J, Chew C, Dale BM, Colonna L et al. Regulatory T cells inhibit dendritic cells by lymphocyte activation Gene-3 engagement of MHC class II. J Immunol 2008; 180:5916–26
50. Dhainaut M, Coquerelle C, Uzureau S, Denoeud J, Acolty V, Oldenhove G et al. Thymus-derived regulatory T cells restrain pro-inflammatory Th1 responses by downregulating CD70 on dendritic cells. EMBO J 2015; 34:1336–48
51. Jang JE, Hajdu CH, Liot C, Miller G, Dustin ML, Bar-Sagi D. Crosstalk between regulatory T cells and tumor-associated dendritic cells negates anti-tumor immunity in pancreatic cancer. Cell Rep 2017; 20:558–71
52. + regulatory T cell proliferation. J Exp Med 2005; 202:919–29
53. + regulatory T cell suppression of dendritic cell function involves TGF-β and IL-10. Cancer Immunol Immunother 2007; 56:48–59
54. Chinen T, Kannan AK, Levine AG, Fan X, Klein U, Zheng Y et al. An essential role for the IL-2 receptor in T reg cell function. Nat Immunol 2016; 17:1322–33
55. Morlacchi S, Dal Secco V, Soldani C, Glaichenhaus N, Viola A, Sarukhan A. Regulatory T cells target chemokine secretion by dendritic cells independently of their capacity to regulate T cell proliferation. J Immunol 2011; 186:6807–14
56. + T cell responses and promote memory. Science 2012; 338:532–6
57. Fontaine M, Vogel I, Van Eycke Y, Galuppo A, Ajouaou Y, Decaestecker C et al. Regulatory T cells constrain the TCR repertoire of antigen-stimulated conventional CD4 T cells. EMBO J 2017; 37:e96881
58. Cabrera T, Ruiz-Cabello F, Garrido F. Biological implications of HLA-DR expression in tumours. Scand J Immunol 1995; 41:398–406
59. Sconocchia G, Eppenberger-Castori S, Zlobec I, Karamitopoulou E, Arriga R, Coppola A et al. HLA class II antigen expression in colorectal carcinoma tumors as a favorable prognostic marker. Neoplasia 2014; 16:31–W15
60. Zanetti M. Tapping CD4 T cells for cancer immunotherapy: the choice of personalized genomics. J Immunol 2015; 194:2049–56
61. + T cells, their differentiation and function. Front Immunol 2017; 8:1–7
62. + T cell-mediated tumor rejection involves inhibition of angiogenesis that is dependent on IFNγ receptor expression by nonhematopoietic cells. Immunity 2000; 12:677–86
63. Shklovskaya E, Terry AM, Guy TV, Buckley A, Bolton HA, Zhu E et al. Tumour-specific CD4 T cells eradicate melanoma via indirect recognition of tumour-derived antigen. Immunol Cell Biol 2016; 94:593–603
64. Perez-diez A, Joncker NT, Choi K, Chan WFN, Anderson CC, Lantz O et al. CD4 cells can be more efficient at tumor rejection than CD8 cells. Blood 2016; 109:5346–55
65. + T cells during the effector phase. J Exp Med 2010; 207:2469–77
66. Braumüller H, Wieder T, Brenner E, Aßmann S, Hahn M, Alkhaled M et al. T-helper-1-cell cytokines drive cancer into senescence. Nature 2013; 494:361–5
67. + T lymphocytes. Cancer Res 2010; 70:8368–77
68. + T-cell subset potently mediates tumor growth inhibition and orchestrates anti-tumor immune responses. Sci Rep 2015; 5:1–14
69. + T-cell help. Nature 2009; 462:510–3
70. + T-cell antitumor reactivity. Cancer Res 2015; 75:3747–59
71. + T cells. Immunity 2005; 22:371–83
72. Lorvik KB, Hammarström C, Fauskanger M, Haabeth OAW, Zangani M, Haraldsen G et al. Adoptive transfer of tumor-specific Th2 cells eradicates tumors by triggering an in situ inflammatory immune response. Cancer Res 2016; 76:6864–76
73. + T cells in the antitumor immune response. J Exp Med 1998; 188:2357–68
74. + T cells enter the scene. Cell Mol Life Sci 2011; 68:3457–67
75. – lymphocytes is thymus and proliferation independent. Cancer Res 2006; 66:4488–95
76. + T regulatory cells: role of tumor-derived TGF-β. J Immunol 2007; 178:2883–92
77. + regulatory T cells in search of origin, distinction, and function. Front Immunol 2013; 4:1–11
78. Fourcade J, Sun Z, Kudela P, Janjic B, Kirkwood JM, El-Hafnawy T et al. Human tumor antigen-specific helper and regulatory T cells share common epitope specificity but exhibit distinct T cell repertoire. J Immunol 2010; 184:6709–18
79. Hindley JP, Ferreira C, Jones E, Lauder SN, Ladell K, Wynn KK et al. Analysis of the T-cell receptor repertoires of tumor-infiltrating conventional and regulatory T cells reveals no evidence for conversion in carcinogen-induced tumors. Cancer Res 2011; 71:736–46
80. Malchow S, Leventhal DS, Nishi S, Fischer BI, Shen L, Paner GP et al. Aire-dependent thymic development of tumor-associated regulatory T cells. Science 2013; 339:1219–24
81. Overacre-Delgoffe AE, Chikina M, Dadey RE, Yano H, Brunazzi EA, Shayan G et al. Interferon-γ drives Treg fragility to promote anti-tumor immunity. Cell 2017; 169:1130–41.e11
82. +) T-cell tumor infiltration is a favorable prognostic factor in advanced colon cancer patients undergoing chemo or chemoimmunotherapy. J Immunother 2010; 33:435–41
83. Bonertz A, Weitz J, Pietsch DK, Rahbari NN, Schlude C, Ge Y et al. Antigen-specific Tregs control T cell responses against a limited repertoire of tumor antigens in patients with colorectal carcinoma. J Clin Invest 2009; 119:3211–21
84. + ratio are associated with adverse prognosis in resectable gastric cancer. J Cancer Res Clin Oncol 2010; 136:1585–95
85. +/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci 2005; 102:18538–43
86. Joshi NS, Akama-Garren EH, Lu Y, Lee DY, Chang GP, Li A et al. Regulatory T cells in tumor-associated tertiary lymphoid structures suppress anti-tumor T cell responses. Immunity 2015; 43:579–90
87. Cao X, Cai SF, Fehniger TA, Song J, Collins LI, Piwnica-Worms DR et al. Granzyme B and perforin are important for regulatory T cell-mediated suppression of tumor clearance. Immunity 2007; 27:635–46
88. + T cells. Nat Immunol 2007; 8:1353–62
89. Deaglio S, Dwyer KM, Gao W, Friedman D, Usheva A, Erat A et al. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med 2007; 204:1257–65
90. Mandapathil M, Szczepanski MJ, Szajnik M, Ren J, Jackson EK, Johnson JT et al. Adenosine and prostaglandin e2 cooperate in the suppression of immune responses mediated by adaptive regulatory T cells. J Biol Chem 2010; 285:27571–80
91. + regulatory T cells. J Immunol 2006; 177:896–904
92. + cells unmasks tumor immunogenicity leading to the rejection of late-stage tumors. J Exp Med 2005; 201:779–91
93. + regulatory T cells induce alternative activation of human monocytes/macrophages. PNAS 2007; 104:19446–51
94. Turnis ME, Sawant DV, Szymczak-Workman AL, Andrews LP, Delgoffe GM, Yano H et al. Interleukin-35 limits anti-tumor immunity. Immunity 2016; 44:316–29
95. Bauer CA, Kim EY, Marangoni F, Carrizosa E, Claudio NM, Mempel TR. Dynamic Treg interactions with intratumoral APCs promote local CTL dysfunction. J Clin Invest 2014; 124:2425–40
96. Penaloza-MacMaster P, Kamphorst AO, Wieland A, Araki K, Iyer SS, West EE et al. Interplay between regulatory T cells and PD-1 in modulating T cell exhaustion and viral control during chronic LCMV infection. J Exp Med 2014; 211:1905–18
97. Facciabene A, Peng X, Hagemann IS, Balint K, Barchetti A, Wang LP et al. Tumour hypoxia promotes tolerance and angiogenesis via CCL28 and Treg cells. Nature 2011; 475:226–30
98. + regulatory CD4 T cells control the generation of functional CD8 memory. Nat Commun 2012; 3:986
99. + T cells is mediated by regulatory T cells through inhibitory receptor CTLA-4. Immunity 2015; 42:1116–29
100. + T cells. Nat Immunol 2015; 16:871–9
101. Chen DS, Mellman I. Oncology meets immunology: the cancer-immunity cycle. Immunity 2013; 39:1–10
102. Diehl L, Den Boer AT, Schoenberger SP, Van Der Voort EIH, Schumacher TNM, Melief CJM et al. CD40 activation in vivo overcomes peptide-induced peripheral cytotoxic T-lymphocyte tolerance and augments anti-tumor vaccine efficacy. Nat Med 1999; 5:774–9
103. Van Der Burg SH, Arens R, Ossendorp F, Van Hall T, Melief CJM. Vaccines for established cancer: overcoming the challenges posed by immune evasion. Nat Rev Cancer 2016; 16:219–33
104. Kenter GG, Welters MJP, Valentijn ARPM, Lowik MJG, der Berends-van Meer DMA, Vloon APG et al. Vaccination against HPV-16 oncoproteins for vulvar intraepithelial neoplasia. N Engl J Med 2009; 361:1838–47
105. Reed CM, Cresce ND, Mauldin IS, Slingluff CL, Olson WC. Vaccination with melanoma helper peptides induces antibody responses associated with improved overall survival. Clin Cancer Res 2015; 21:3879–87
106. + T-helper cells improves the induction of antitumor responses in dendritic cell-based vaccination. Cancer Res 2013; 73:19–29
107. Kreiter S, Vormehr M, Van De Roemer N, Diken M, Löwer M, Diekmann J et al. Mutant MHC class II epitopes drive therapeutic immune responses to cancer. Nature 2015; 520:692–6
108. Dannull J, Su Z, Rizzieri D, Yang BK, Coleman D, Yancey D et al. Enhancement of vaccine-mediated antitumor immunity in cancer patients after depletion of regulatory T cells. J Clin Invest 2005; 115:3623–33
109. Morse MA, Hobeika AC, Osada T, Serra D, Niedzwiecki D, Lyerl HK et al. Depletion of human regulatory T cells specifically enhances antigen specific immune responses to cancer vaccines. Blood 2008; 112:2–4
110. + T cells following peptide vaccination. J Immunol 2006; 176:6340–6
111. Intlekofer AM, Thompson CB. At the bench: preclinical rationale for CTLA-4 and PD-1 blockade as cancer immunotherapy. J Leukoc Biol 2013; 94:25–39
112. + T cell response. Sci Transl Med 2014; 6:254ra128
113. Peggs KS, Quezada SA, Chambers CA, Korman AJ, Allison JP. Blockade of CTLA-4 on both effector and regulatory T cell compartments contributes to the antitumor activity of anti-CTLA-4 antibodies. J Exp Med 2009; 206:1717–25
114. + regulatory T cells in antitumor therapy reveals alternative pathways for suppression of autoreactive cytotoxic T lymphocyte responses. J Exp Med 2001; 98231000:823–32
115. Selby MJ, Engelhardt JJ, Quigley M, Henning KA, Chen T, Srinivasan M et al. Anti-CTLA-4 antibodies of IgG2a isotype enhance antitumor activity through reduction of intratumoral regulatory T cells. Cancer Immunol Res 2013; 1:32–42
116. Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJM, Robert L et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 2014; 515:568–71
117. Homet Moreno B, Zaretsky JM, Garcia-Diaz A, Tsoi J, Parisi G, Robert L et al. Response to programmed cell death-1 blockade in a murine melanoma syngeneic model requires costimulation, CD4, and CD8 T cells. Cancer Immunol Res 2016; 4:845–57
118. Hui E, Cheung J, Zhu J, Su X, Taylor MJ, Wallweber HA et al. T cell costimulatory receptor CD28 is a primary target for PD-1-mediated inhibition. Science 2017; 355:1428–33
119. + T cells during recurrence of melanoma. J Immunol 2013; 190:4899–909
120. Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 2013; 369:122–33
121. Wei SC, Levine JH, Cogdill AP, Zhao Y, Anang NAAS, Andrews MC et al. Distinct cellular mechanisms underlie anti-CTLA-4 and anti-PD-1 checkpoint blockade. Cell 2017; 170:1120–33.e17
122. + T helper cells and hindered by naturally occurring T regulatory cells. J Immunol 2005; 174:2591–601
123. + T cells against NY-ESO-1. N Engl J Med 2008; 358:2698–703
124. + T cell precursors. J Immunol 2004; 172:4215–24
125. + T cell function in the pancreas. Front Immunol 2018; 8:2001
126. + T cell responses to influenza. J Exp Med 2013; 210:1591–601
127. + helper T cell responses in cancer patients. Blood 2005; 106:1008–11
128. Gros A, Parkhurst MR, Tran E, Pasetto A, Robbins PF, Ilyas S et al. Prospective identification of neoantigen-specific lymphocytes in the peripheral blood of melanoma patients. Nat Med 2016; 22:433–8
129. Klatzmann D, Abbas AK. The promise of low-dose interleukin-2 therapy for autoimmune and inflammatory diseases. Nat Rev Immunol 2015; 15:283–94
130. Wang H, Franco F, Ho PC. Metabolic regulation of Tregs in cancer: opportunities for immunotherapy. Trends Cancer 2017; 3:583–92
131. Srivastava S, Koch MA, Pepper M, Campbell DJ. Type I interferons directly inhibit regulatory T cells to allow optimal antiviral T cell responses during acute LCMV infection. J Exp Med 2014; 211:961–74
132. Wasiuk A, Testa J, Weidlick J, Sisson C, Vitale L, Widger J et al. CD27-mediated regulatory T cell depletion and effector T cell costimulation both contribute to antitumor efficacy. J Immunol 2017; 199:4110–23
133. Burris HA, Infante JR, Ansell SM, Nemunaitis JJ, Weiss GR, Villalobos VM et al. Safety and activity of varlilumab, a novel and first-in-class agonist anti-CD27 antibody, in patients with advanced solid tumors. J Clin Oncol 2017; 35:2028–36