Foxp3+ T cells inhibit antitumor immune memory modulated by mTOR inhibition

Cancer Research

Volumn 74, Issue 8, 2014, Pages 2217-2228

  Wang, Yanping ^a   Sparwasser, Tim ^b   Figlin, Robert ^a   Kim, Hyung L ^a  

^a CEDARS SINAI MEDICAL CENTER   (United States)

^b INSTITUTE OF INFECTION IMMUNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIBODY; DENDRITIC CELL VACCINE; MAMMALIAN TARGET OF RAPAMYCIN; TEMSIROLIMUS; TRANSCRIPTION FACTOR FOXP3;

ADOPTIVE IMMUNOTHERAPY; ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; FEMALE; IMMUNOLOGICAL MEMORY; KIDNEY CARCINOMA; LUNG METASTASIS; LYMPHOCYTE DEPLETION; MELANOMA B16; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE;

ANIMALS; CANCER VACCINES; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNOLOGIC MEMORY; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; SIROLIMUS; T-LYMPHOCYTES, CYTOTOXIC; T-LYMPHOCYTES, REGULATORY; TOR SERINE-THREONINE KINASES;

EID: 84899561523     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-2928     Document Type: Article

References (48)

1. Araki K, Turner AP, Shaffer VO, Gangappa S, Keller SA, Bachmann MF, et al. mTOR regulates memory CD8 T-cell differentiation. Nature 2009;460:108-12.
2. Wang Y, Wang XY, Subjeck JR, Shrikant PA, Kim HL. Temsirolimus, an mTOR inhibitor, enhances anti-tumour effects of heat shock protein cancer vaccines. Br J Cancer 2011;104:643-52.
3. Rao RR, Li Q, Odunsi K, Shrikant PA. The mTOR kinase determines effector versus memory CD8+ T cell fate by regulating the expression of transcription factors T-bet and Eomesodermin. Immunity 2010;32: 67-78.
4. Jagannath C, Lindsey DR, Dhandayuthapani S, Xu Y, Hunter RL Jr., Eissa NT. Autophagy enhances the efficacy of BCG vaccine by increasing peptide presentation in mouse dendritic cells. Nat Med 2009;15:267-76.
5. Scotta C, Esposito M, Fazekasova H, Fanelli G, Edozie FC, Ali N, et al. Differential effects of rapamycin and retinoic acid on expansion, stability and suppressive qualities of human CD4+ CD25+FOXP3+ T regulatory cell subpopulations. Haematologica 2013;98:1291-9.
6. Gavin MA, Rasmussen JP, Fontenot JD, Vasta V, Manganiello VC, Beavo JA, et al. Foxp3-dependent programme of regulatory T-cell differentiation. Nature 2007;445:771-5.
7. Quezada SA, Peggs KS, Simpson TR, Shen Y, Littman DR, Allison JP. Limited tumor infiltration by activated T effector cells restricts the therapeutic activity of regulatory T cell depletion against established melanoma. J Exp Med 2008;205:2125-38.
8. Elpek KG, Lacelle C, Singh NP, Yolcu ES, Shirwan H. CD4+CD25+ T regulatory cells dominate multiple immune evasion mechanisms in early but not late phases of tumor development in a B cell lymphoma model. J Immunol 2007;178:6840-8.
9. Onizuka S, Tawara I, Shimizu J, Sakaguchi S, Fujita T, Nakayama E. Tumor rejection by in vivo administration of anti-CD25 (interleukin-2 receptor a) monoclonal antibody. Cancer Res 1999;59:3128-33.
10. Curtin JF, Candolfi M, Fakhouri TM, Liu C, Alden A, Edwards M, et al. Treg depletion inhibits efficacy of cancer immunotherapy: implications for clinical trials. PLoS ONE 2008;3:e1983.
11. Cote AL, Byrne KT, Steinberg SM, Zhang P, Turk MJ. Protective CD8 memory T cell responses to mouse melanoma are generated in the absence of CD4 T cell help. PLoS ONE 2011;6:e26491.
12. 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.
13. Mahnke K, Schonfeld K, Fondel S, Ring S, Karakhanova S, Wiedemeyer K, et al. Depletion of CD4+CD25+ human regulatory T cells in vivo: kinetics of Treg depletion and alterations in immune functions in vivo and in vitro. Int J Cancer 2007;120:2723-33.
14. Kim YH, Duvic M, Obitz E, Gniadecki R, Iversen L, Osterborg A, et al. Clinical efficacy of zanolimumab (HuMax-CD4): two phase 2 studies in refractory cutaneous T-cell lymphoma. Blood 2007;109:4655-62.
15. d'Amore F, Radford J, Relander T, Jerkeman M, Tilly H, Osterborg A, et al. Phase II trial of zanolimumab (HuMax-CD4) in relapsed or refractory non-cutaneous peripheral T cell lymphoma. Br J Haematol 2010;150:565-73.
16. Stronkhorst A, Radema S, Yong SL, Bijl H, ten Berge IJ, Tytgat GN, et al. CD4 antibody treatment in patients with active Crohn's disease: a phase 1 dose finding study. Gut 1997;40:320-7.
17. Llewellyn-Smith N, Lai M, Miller DH, Rudge P, Thompson AJ, Cuzner ML. Effects of anti-CD4 antibody treatment on lymphocyte subsets and stimulated tumor necrosis factor a production: a study of 29 multiple sclerosis patients entered into a clinical trial of cM-T412. Neurology 1997;48:810-6.
18. van Oosten BW, Lai M, Hodgkinson S, Barkhof F, Miller DH, Moseley IF, et al. Treatment of multiple sclerosis with the monoclonal anti-CD4 antibody cM-T412: results of a randomized, double-blind, placebocontrolled, MR-monitored phase II trial. Neurology 1997;49:351-7.
19. Lahl K, Loddenkemper C, Drouin C, Freyer J, Arnason J, Eberl G, et al. Selective depletion of Foxp3+ regulatory T cells induces a scurfy-like disease. J Exp Med 2007;204:57-63.
20. Vissers JL, De Vries IJ, Engelen LP, Scharenborg NM, Molkenboer J, Figdor CG, et al. Renal cell carcinoma-Associated antigen G250 encodes a naturally processed epitope presented by human leukocyte antigen-DR molecules to CD4(+) T lymphocytes. Int J Cancer 2002;100:441-4.
21. Intlekofer AM, Takemoto N, Wherry EJ, Longworth SA, Northrup JT, Palanivel VR, et al. Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nat Immunol 2005;6:1236-44.
22. Roque S, Nobrega C, Appelberg R, Correia-Neves M. IL-10 underlies distinct susceptibility of BALB/c and C57BL/6 mice to Mycobacterium avium infection and influences efficacy of antibiotic therapy. J Immunol 2007;178:8028-35.
23. Pace L, Tempez A, Arnold-Schrauf C, Lemaitre F, Bousso P, Fetler L, et al. Regulatory T cells increase the avidity of primary CD8+ T cell responses and promote memory. Science 2012;338:532-6.
24. de Goer de Herve MG, Jaafoura S, Vallee M, Taoufik Y. FoxP3(+) regulatory CD4 T cells control the generation of functional CD8 memory. Nat Commun 2012;3:986.
25. Rethinking therapeutic cancer vaccines. Nat Rev Drug Discov 2009; 8:685-6.
26. Kaufman HL, Kirkwood JM, Hodi FS, Agarwala S, Amatruda T, Bines SD, et al. The Society for Immunotherapy of Cancer consensus statement on tumour immunotherapy for the treatment of cutaneous melanoma. Nat Rev Clin Oncol 2013.
27. McDermott DF, Regan MM, Clark JI, Flaherty LE, Weiss GR, Logan TF, et al. Randomized phase III trial of high-dose interleukin-2 versus subcutaneous interleukin-2 and interferon in patients with metastatic renal cell carcinoma. J Clin Oncol 2005;23:133-41.
28. Grupp SA, Kalos M, Barrett D, Aplenc R, Porter DL, Rheingold SR, et al. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med 2013;368:1509-18.
29. Battaglia M, Stabilini A, Roncarolo MG. Rapamycin selectively expands CD4+CD25+FoxP3+ regulatory T cells. Blood 2005;105: 4743-8.
30. Liu G, Yang K, Burns S, Shrestha S, Chi H. The S1P(1)-mTOR axis directs the reciprocal differentiation of T(H)1 and T(reg) cells. Nat Immunol 2010;11:1047-56.
31. Cote AL, Usherwood EJ, Turk MJ. Tumor-specific T-cell memory: clearing the regulatory T-cell hurdle. Cancer Res 2008;68:1614-7.
32. Fuse S, Tsai CY, Molloy MJ, Allie SR, Zhang W, Yagita H, et al. Recall responses by helpless memory CD8+ T cells are restricted by the upregulation of PD-1. J Immunol 2009;182:4244-54.
33. Jing W, Gershan JA, Johnson BD. Depletion of CD4 T cells enhances immunotherapy for neuroblastoma after syngeneic HSCT but compromises development of antitumor immune memory. Blood 2009;113:4449-57.
34. Jing W, Yan X, Hallett WH, Gershan JA, Johnson BD. Depletion of CD25(+) T cells from hematopoietic stem cell grafts increases posttransplantation vaccine-induced immunity to neuroblastoma. Blood 2011;117:6952-62.
35. Zhang P, Cote AL, de Vries VC, Usherwood EJ, Turk MJ. Induction of postsurgical tumor immunity and T-cell memory by a poorly immunogenic tumor. Cancer Res 2007;67:6468-76.
36. Yu P, Lee Y, Liu W, Krausz T, Chong A, Schreiber H, et al. Intratumor depletion of CD4+ cells unmasks tumor immunogenicity leading to the rejection of late-stage tumors. J Exp Med 2005;201:779-91.
37. Simpson TR, Li F, Montalvo-Ortiz W, Sepulveda MA, Bergerhoff K, Arce F, 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 2013;210:1695-710.
38. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010;363:711-23.
39. Meiser BM, Reiter C, Reichenspurner H, Uberfuhr P, Kreuzer E, Rieber EP, et al. Chimeric monoclonal CD4 antibody - a novel immunosuppressant for clinical heart transplantation. Transplantation 1994; 58:419-23.
40. Moreland LW, Pratt PW, Bucy RP, Jackson BS, Feldman JW, Koopman WJ. Treatment of refractory rheumatoid arthritis with a chimeric anti-CD4 monoclonal antibody. Long-term followup of CD4+ T cell counts. Arthritis Rheum 1994;37:834-8.
41. Moreland LW, Pratt PW, Mayes MD, Postlethwaite A, Weisman MH, Schnitzer T, et al. Double-blind, placebo-controlled multicenter trial using chimeric monoclonal anti-CD4 antibody, cM-T412, in rheumatoid arthritis patients receiving concomitant methotrexate. Arthritis Rheum 1995;38:1581-8.
42. Prinz JC, Meurer M, Reiter C, Rieber EP, Plewig G, Riethmuller G. Treatment of severe cutaneous lupus erythematosus with a chimeric CD4 monoclonal antibody, cM-T412. J Am Acad Dermatol 1996; 34:244-52.
43. van der Lubbe PA, Dijkmans BA, Markusse HM, Nassander U, Breedveld FC. A randomized, double-blind, placebo-controlled study ofCD4 monoclonal antibody therapy in early rheumatoid arthritis. Arthritis Rheum 1995;38:1097-106.
44. Knox S, Hoppe RT, Maloney D, Gibbs I, Fowler S, Marquez C, et al. Treatment of cutaneous T-cell lymphoma with chimeric anti-CD4 monoclonal antibody. Blood 1996;87:893-9.
45. Rep MH, van Oosten BW, RoosMT, Ader HJ, Polman CH, van Lier RA. Treatment with depleting CD4 monoclonal antibody results in a preferential loss of circulating naive T cells but does not affect IFN-g secreting TH1 cells in humans. J Clin Invest 1997;99: 2225-31.
46. van der Lubbe PA, Breedveld FC, Tak PP, Schantz A, Woody J, Miltenburg AM. Treatment with a chimeric CD4 monoclonal antibody is associated with a relative loss of CD4+/CD45RA+ cells in patients with rheumatoid arthritis. J Autoimmun 1997;10:87-97.
47. LaCelle MG, Jensen SM, Fox BA. Partial CD4 depletion reduces regulatory T cells induced by multiple vaccinations and restores therapeutic efficacy. Clin Cancer Res 2009;15:6881-90.
48. Bonertz A, Weitz J, Pietsch DH, 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;119:3311-21.