Selective depletion of Foxp3+ regulatory T cells improves effective therapeutic vaccination against established melanoma

Cancer Research

Volumn 70, Issue 20, 2010, Pages 7788-7799

  Klages, Katjana ^a   Mayer, Christian T ^b   Lahl, Katharina ^c   Loddenkemper, Christoph ^d   Teng, Michele W L ^e   Ngiow, Shin Foong ^e   Smyth, Mark J ^e   Hamann, Alf ^f   Huehn, Jochen ^a   Sparwasser, Tim ^b  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^b INSTITUTE OF INFECTION IMMUNOLOGY   (Germany)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^f PETER MACCALLUM CANCER CENTRE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CPG OLIGODEOXYNUCLEOTIDE; INSULIN; OVALBUMIN; TRANSCRIPTION FACTOR FOXP3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNIZATION; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; IMMUNOLOGICAL TOLERANCE; MELANOMA; MELANOMA B16; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY T LYMPHOCYTE; T CELL DEPLETION; TRANSGENIC MOUSE; TUMOR REGRESSION;

ANIMALS; AUTOANTIGENS; CANCER VACCINES; CROSSES, GENETIC; DISEASE MODELS, ANIMAL; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LYMPHOCYTE DEPLETION; LYMPHOCYTES, TUMOR-INFILTRATING; MELANOMA; MELANOMA, EXPERIMENTAL; MICE; MICE, MUTANT STRAINS; OVALBUMIN; PROGNOSIS; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY;

EID: 78049276260     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-1736     Document Type: Article

References (50)

1. Shevach EM. From vanilla to 28 flavors: multiple varieties of T regulatory cells. Immunity 2006;25:195-201. (Pubitemid 44224153)
2. Yamaguchi T, Sakaguchi S. Regulatory T cells in immune surveillance and treatment of cancer. Semin Cancer Biol 2006;16:115-23. (Pubitemid 43172060)
3. Sakaguchi S, Wing K, Yamaguchi T. Dynamics of peripheral tolerance and immune regulation mediated by Treg. Eur J Immunol 2009;39:2331-6.
4. Fontenot JD, Rudensky AY. A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat Immunol 2005;6:331-7.
5. Gavin MA, Rasmussen JP, Fontenot JD, et al. Foxp3-dependent programme of regulatory T-cell differentiation. Nature 2007;445:771-5.
6. Huehn J, Polansky JK, Hamann A. Epigenetic control of FOXP3 expression: the key to a stable regulatory T-cell lineage? Nat Rev Immunol 2009;9:83-9.
7. Kim J, Lahl K, Hori S, et al. Cutting edge: depletion of Foxp3+ cells leads to induction of autoimmunity by specific ablation of regulatory T cells in genetically targeted mice. J Immunol 2009;183:7631-4.
8. Lahl K, Mayer CT, Bopp T, et al. Nonfunctional regulatory T cells and defective control of Th2 cytokine production in natural scurfy mutant mice. J Immunol 2009;183:5662-72.
9. Zou W. Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol 2006;6:295-307.
10. Yu P, Lee Y, Liu W, 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. (Pubitemid 40395122)
11. Terabe M, Berzofsky JA. Immunoregulatory T cells in tumor immunity. Curr Opin Immunol 2004;16:157-62.
12. Beyer M, Schultze JL. Regulatory T cells: major players in the tumor microenvironment. Curr Pharm Des 2009;15:1879-92.
13. Onizuka S, Tawara I, Shimizu J, Sakaguchi S, Fujita T, Nakayama E. Tumor rejection by in vivo administration of anti-CD25 (interleukin-2 receptor α) monoclonal antibody. Cancer Res 1999;59:3128-33. (Pubitemid 29316012)
14. Shimizu J, Yamazaki S, Sakaguchi S. Induction of tumor immunity by removing CD25+CD4+ T cells: a common basis between tumor immunity and autoimmunity. J Immunol 1999;163:5211-8.
15. Sutmuller RP, van Duivenvoorde LM, van Elsas A, et al. Synergism of cytotoxic T lymphocyte-associated antigen 4 blockade and depletion of CD25+ regulatory T cells in antitumor therapy reveals alternative pathways for suppression of autoreactive cytotoxic T lymphocyte responses. J Exp Med 2001;194:823-32.
16. Jones E, Dahm-Vicker M, Simon AK, et al. Depletion of CD25+ regulatory cells results in suppression of melanoma growth and induction of autoreactivity in mice. Cancer Immun 2002;2:1.
17. Li J, Hu P, Khawli LA, Epstein AL. Complete regression of experimental solid tumors by combination LEC/chTNT-3 immunotherapy and CD25+ T-cell depletion. Cancer Res 2003;63:8384-92. (Pubitemid 37549493)
18. Teng MW, Swann JB, von Scheidt B, et al. Multiple antitumor mechanisms downstream of prophylactic regulatory T-cell depletion. Cancer Res 2010;70:2665-74.
19. Ko K, Yamazaki S, Nakamura K, et al. Treatment of advanced tumors with agonistic anti-GITR mAb and its effects on tumor-infiltrating Foxp3+CD25+CD4+ regulatory T cells. J Exp Med 2005;202:885-91. (Pubitemid 41396888)
20. 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.
21. Dannull J, Su Z, Rizzieri 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. (Pubitemid 43121851)
22. Mahnke K, Schonfeld K, Fondel S, 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. (Pubitemid 46651297)
23. Morse MA, Hobeika AC, Osada T, et al. Depletion of human regulatory T cells specifically enhances antigen-specific immune responses to cancer vaccines. Blood 2008;112:610-8.
24. Barnett B, Kryczek I, Cheng P, Zou W, Curiel TJ. Regulatory T cells in ovarian cancer: biology and therapeutic potential. Am J Reprod Immunol 2005;54:369-77. (Pubitemid 41748714)
25. Lahl K, Loddenkemper C, Drouin C, et al. Selective depletion of Foxp3+ regulatory T cells induces a scurfy-like disease. J Exp Med 2007;204:57-63. (Pubitemid 46148756)
26. Blanas E, Carbone FR, Allison J, Miller JF, Heath WR. Induction of autoimmune diabetes by oral administration of autoantigen. Science 1996;274:1707-9. (Pubitemid 26414901)
27. Falo LD, Jr., Kovacsovics-Bankowski M, Thompson K, Rock KL. Targeting antigen into the phagocytic pathway in vivo induces protective tumour immunity. Nat Med 1995;1:649-53.
28. Knutson KL, Dang Y, Lu H, et al. IL-2 immunotoxin therapy modulates tumor-associated regulatory T cells and leads to lasting immune-mediated rejection of breast cancers in neu-transgenic mice. J Immunol 2006;177:84-91. (Pubitemid 43939119)
29. Turk MJ, Guevara-Patino JA, Rizzuto GA, Engelhorn ME, Sakaguchi S, Houghton AN. Concomitant tumor immunity to a poorly immunogenic melanoma is prevented by regulatory T cells. J Exp Med 2004;200:771-82.
30. Piconese S, Valzasina B, Colombo MP. OX40 triggering blocks suppression by regulatory T cells and facilitates tumor rejection. J Exp Med 2008;205:825-39. (Pubitemid 351549881)
31. Steeg C, Adler G, Sparwasser T, Fleischer B, Jacobs T. Limited role of CD4+Foxp3+ regulatory T cells in the control of experimental cerebral malaria. J Immunol 2009;183:7014-22.
32. Zelinskyy G, Dietze K, Sparwasser T, Dittmer U. Regulatory T cells suppress antiviral immune responses and increase viral loads during acute infection with a lymphotropic retrovirus. PLoS Pathog 2009;5:e1000406.
33. Schildknecht A, Brauer S, Brenner C, et al. FoxP3+ regulatory T cells essentially contribute to peripheral CD8+ T-cell tolerance induced by steady-state dendritic cells.ProcNatlAcad SciUSA 2010;107:199-203.
34. Chen GY, Chen C, Wang L, Chang X, Zheng P, Liu Y. Cutting edge: Broad expression of the FoxP3 locus in epithelial cells: a caution against early interpretation of fatal inflammatory diseases following in vivo depletion of FoxP3-expressing cells. J Immunol 2008;180:5163-6.
35. Zuo T, Wang L, Morrison C, et al. FOXP3 is an X-linked breast cancer suppressor gene and an important repressor of the HER-2/ErbB2 oncogene. Cell 2007;129:1275-86. (Pubitemid 46970708)
36. Wolf D, Wolf AM, Tzankov A. Comment on "Cutting edge: depletion of Foxp3+ cells leads to induction of autoimmunity by specific ablation of regulatory T cells in genetically targeted mice". J Immunol 2010;184:4051.
37. Heit A, Gebhardt F, Lahl K, et al. Circumvention of regulatory CD4+ T cell activity during cross-priming strongly enhances T cell-mediated immunity. Eur J Immunol 2008;38:1585-97.
38. Pellegrini M, Calzascia T, Elford AR, et al. Adjuvant IL-7 antagonizes multiple cellular and molecular inhibitory networks to enhance immunotherapies. Nat Med 2009;15:528-36.
39. Sparwasser T, Koch ES, Vabulas RM, et al. Bacterial DNA and immunostimulatory CpG oligonucleotides trigger maturation and activation of murine dendritic cells. Eur J Immunol 1998;28:2045-54. (Pubitemid 28271721)
40. Sparwasser T, Vabulas RM, Villmow B, Lipford GB, Wagner H. Bacterial CpG-DNA activates dendritic cells in vivo: T helper cellindependent cytotoxic T cell responses to soluble proteins. Eur J Immunol 2000;30:3591-7.
41. Bellone M, Cantarella D, Castiglioni P, et al. Relevance of the tumor antigen in the validation of three vaccination strategies for melanoma. J Immunol 2000;165:2651-6. (Pubitemid 30660713)
42. Schreiber TH, Deyev VV, Rosenblatt JD, Podack ER. Tumor-induced suppression of CTL expansion and subjugation by gp96-Ig vaccination. Cancer Res 2009;69:2026-33.
43. Meyer Zu Horste G, Zozulya AL, El-Haddad H, et al. Active immunization induces toxicity of diphtheria toxin in diphtheria resistant mice-implications for neuroinflammatory models. J Immunol Methods 2010;354:80-4.
44. Attia P, Maker AV, Haworth LR, Rogers-Freezer L, Rosenberg SA. Inability of a fusion protein of IL-2 and diphtheria toxin (Denileukin Diftitox, DAB389IL-2, ONTAK) to eliminate regulatory T lymphocytes in patients with melanoma. J Immunother 2005;28:582-92. (Pubitemid 41533092)
45. 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. (Pubitemid 46847409)
46. Parish IA, Waithman J, Davey GM, et al. Tissue destruction caused by cytotoxic T lymphocytes induces deletional tolerance. Proc Natl Acad Sci U S A 2009;106:3901-6.
47. Gogas H, Ioannovich J, Dafni U, et al. Prognostic significance of autoimmunity during treatment of melanoma with interferon. N Engl J Med 2006;354:709-18. (Pubitemid 43247141)
48. Maker AV, Yang JC, Sherry RM, et al. Intrapatient dose escalation of anti-CTLA-4 antibody in patients with metastatic melanoma. J Immunother 2006;29:455-63.
49. Phan GQ, Yang JC, Sherry RM, et al. Cancer regression and autoimmunity induced by cytotoxic T lymphocyte-associated antigen 4 blockade in patients with metastatic melanoma. Proc Natl Acad Sci U S A 2003;100:8372-7.
50. Weinhold M, Sommermeyer D, Uckert W, Blankenstein T. Dual T cell receptor expressing CD8+ T cells with tumor- and self-specificity can inhibit tumor growth without causing severe autoimmunity. J Immunol 2007;179:5534-42.