Role of Regulatory T-Cells in Immunization Strategies Involving a Recombinant Alphavirus Vector System

Dannull J. , Su Z. , Rizzieri D. Enhancement of vaccine-mediated antitumor immunity in cancer patients after depletion of regulatory T cells. J Clin Invest 2005; 115: 3623–3633.

Delluc S. , Hachem P. , Rusakiewicz S. Dramatic efficacy improvement of a DC-based vaccine against AML by CD25 T cell depletion allowing the induction of a long-lasting T cell response. Cancer Immunol Immunother 2009; 58: 1669–1677.

Imai H. , Saio M. , Nonaka K. Depletion of CD4⁺CD25⁺ regulatory T cells enhances interleukin-2-induced antitumor immunity in a mouse model of colon adenocarcinoma. Cancer Sci 2007; 98: 416–423.

Jacob J.B. , Kong Y.C. , Nalbantoglu I. , Snower D.P. , Wei W.Z. Tumor regression following DNA vaccination and regulatory T cell depletion in neu transgenic mice leads to an increased risk for autoimmunity. J Immunol 2009; 182: 5873–5881.

Kottke T. , Pulido J. , Thompson J. Antitumor immunity can be uncoupled from autoimmunity following heat shock protein 70-mediated inflammatory killing of normal pancreas. Cancer Res 2009; 69: 7767–7774.

Kudo-Saito C. , Schlom J. , Camphausen K. , Coleman C.N. , Hodge J.W. The requirement of multimodal therapy (vaccine, local tumor radiation, and reduction of suppressor cells) to eliminate established tumors. Clin Cancer Res 2005; 11: 4533–4544.

Lutsiak M.E. , Semnani R.T. , De P.R. , Kashmiri S.V. , Schlom J. , Sabzevari H. Inhibition of CD4⁺25⁺ T regulatory cell function implicated in enhanced immune response by low-dose cyclophosphamide. Blood 2005; 105: 2862–2868.

Wada S. , Yoshimura K. , Hipkiss E.L. Cyclophosphamide augments antitumor immunity: studies in an autochthonous prostate cancer model. Cancer Res 2009; 69: 4309–4318.

Apostolou I. , von Boehmer H. In vivo instruction of suppressor commitment in naive T cells. J Exp Med 2004; 199: 1401–1408.

Berraondo P. , Nouze C. , Preville X. , Ladant D. , Leclerc C. Eradication of large tumors in mice by a tritherapy targeting the innate, adaptive, and regulatory components of the immune system. Cancer Res 2007; 67: 8847–8855.

Dahlberg P.E. , Schartner J.M. , Timmel A. , Seroogy C.M. Daily subcutaneous injections of peptide induce CD4⁺ CD25⁺ T regulatory cells. Clin Exp Immunol 2007; 149: 226–234.

Maksimow M. , Miiluniemi M. , Marttila-Ichihara F. , Jalkanen S. , Hanninen A. Antigen targeting to endosomal pathway in dendritic cell vaccination activates regulatory T cells and attenuates tumor immunity. Blood 2006; 108: 1298–1305.

Silver P.B. , Agarwal R.K. , Su S.B. Hydrodynamic vaccination with DNA encoding an immunologically privileged retinal antigen protects from autoimmunity through induction of regulatory T cells. J Immunol 2007; 179: 5146–5158.

Zhou G. , Drake C.G. , Levitsky H.I. Amplification of tumor-specific regulatory T cells following therapeutic cancer vaccines. Blood 2006; 107: 628–636.

Curiel T.J. Regulatory T cells and treatment of cancer. Curr Opin Immunol 2008; 20: 241–246.

Visser J. , Nijman H.W. , Hoogenboom B.N. Frequencies and role of regulatory T cells in patients with (pre) malignant cervical neoplasia. Clin Exp Immunol 2007; 150: 199–209.

Wang H.Y. , Wang R.F. Regulatory T cells and cancer. Curr Opin Immunol 2007; 19: 217–223.

Wolf A.M. , Wolf D. , Steurer M. , Gastl G. , Gunsilius E. , Grubeck-Loebenstein B. Increase of regulatory T cells in the peripheral blood of cancer patients. Clin Cancer Res 2003; 9: 606–612.

Feuerer M. , Hill J.A. , Mathis D. , Benoist C. Foxp3⁺ regulatory T cells: differentiation, specification, subphenotypes. Nat Immunol 2009; 10: 689–695.

Kim J.M. , Rasmussen J.P. , Rudensky A.Y. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat Immunol 2007; 8: 191–197.

Mills K.H. Regulatory T cells: friend or foe in immunity to infection? Nat Rev Immunol 2004; 4: 841–855.

Banerjee D.K. , Dhodapkar M.V. , Matayeva E. , Steinman R.M. , Dhodapkar K.M. Expansion of FOXP3^high regulatory T cells by human dendritic cells (DCs) in vitro and after injection of cytokine-matured DCs in myeloma patients. Blood 2006; 108: 2655–2661.

Hussain S.F. , Paterson Y. CD4⁺CD25⁺ regulatory T cells that secrete TGF[beta] and IL-10 are preferentially induced by a vaccine vector. J Immunother 2004; 27: 339–346.

Daemen T. , Regts J. , Holtrop M. , Wilschut J. Immunization strategy against cervical cancer involving an alphavirus vector expressing high levels of a stable fusion protein of human papillomavirus 16 E6 and E7. Gene Ther 2002; 9: 85–94.

Liljeström P. , Garoff H. A new generation of animal cell expression vectors based on the Semliki Forest virus replicon. Biotechnology (N Y) 1991; 9: 1356–1361.

Daemen T. , Riezebos-Brilman A. , Bungener L. , Regts J. , Dontje B. , Wilschut J. Eradication of established HPV16-transformed tumours after immunisation with recombinant Semliki Forest virus expressing a fusion protein of E6 and E7. Vaccine 2003; 21: 1082–1088.

Daemen T. , Riezebos-Brilman A. , Regts J. , Dontje B. , van der Zee A. , Wilschut J. Superior therapeutic efficacy of alphavirus-mediated immunization against human papilloma virus type 16 antigens in a murine tumour model: effects of the route of immunization. Antivir Ther 2004; 9: 733–742.

Riezebos-Brilman A. , Regts J. , Freyschmidt E.J. , Dontje B. , Wilschut J. , Daemen T. Induction of human papilloma virus E6/E7-specific cytotoxic T-lymphocyte activity in immune-tolerant, E6/E7-transgenic mice. Gene Ther 2005; 12: 1410–1414.

Riezebos-Brilman A. , Walczak M. , Regts J. A comparative study on the immunotherapeutic efficacy of recombinant Semliki Forest virus and adenovirus vector systems in a murine model for cervical cancer. Gene Ther 2007; 14: 1695–1704.

Fehérvari Z. , Sakaguchi S. Development and function of CD25⁺CD4⁺ regulatory T cells. Curr Opin Immunol 2004; 16: 203–208.

Sakaguchi S. Naturally arising CD4⁺ regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 2004; 22: 531–562.

Fontenot J.D. , Gavin M.A. , Rudensky A.Y. Foxp3 programs the development and function of CD4⁺CD25⁺ regulatory T cells. Nat Immunol 2003; 4: 330–336.

Hori S. , Nomura T. , Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003; 299: 1057–1061.

Khattri R. , Cox T. , Yasayko S.A. , Ramsdell F. An essential role for Scurfin in CD4⁺CD25⁺ T regulatory cells. Nat Immunol 2003; 4: 337–342.

Sakaguchi S. , Yamaguchi T. , Nomura T. , Ono M. Regulatory T cells and immune tolerance. Cell 2008; 133: 775–787.

Zheng Y. , Rudensky A.Y. Foxp3 in control of the regulatory T cell lineage. Nat Immunol 2007; 8: 457–462.

Morse M.A. , Hobeika A.C. , Osada T. Depletion of human regulatory T cells specifically enhances antigen-specific immune responses to cancer vaccines. Blood 2008; 112: 610–618.

Powell D.J. Jr. , Felipe-Silva A. , Merino M.J. 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 2007; 179: 4919–4928.

Rech A.J. , Vonderheide R.H. Clinical use of anti-CD25 antibody daclizumab to enhance immune responses to tumor antigen vaccination by targeting regulatory T cells. Ann N Y Acad Sci 2009; 1174: 99–106.

Couper K.N. , Blount D.G. , de Souza J.B. , Suffa I. , Belkaid Y. , Riley E.M. Incomplete depletion and rapid regeneration of Foxp3⁺ regulatory T cells following anti-CD25 treatment in malaria-infected mice. J Immunol 2007; 178: 4136–4146.

Kohm A.P. , McMahon J.S. , Podojil J.R. Cutting edge: anti-CD25 monoclonal antibody injection results in the functional inactivation, not depletion, of CD4⁺CD25⁺ T regulatory cells. J Immunol 2006; 176: 3301–3305.

Curtin J.F. , Candolf M. , Fakhouri T.M. Treg depletion inhibits efficacy of cancer immunotherapy: implications for clinical trials. PLoS ONE 2008; 3: e1983.

Yamaguchi T. , Hirota K. , Nagahama K. Control of immune responses by antigen-specific regulatory T cells expressing the folate receptor. Immunity 2007; 27: 145–159.

Chen G. , Li N. , Zang Y.C. Vaccination with selected synovial T cells in rheumatoid arthritis. Arthritis Rheum 2007; 56: 453–463.

Cabrera A. , Saez D. , Cespedes S. , Andrews E. , Onate A. Vaccination with recombinant Semliki Forest virus particles expressing translation initiation factor 3 of Brucella abortus induces protective immunity in BALB/c mice. Immunobiology 2009; 214: 467–474.

Cassetti M.C. , McElhiney S.P. , Shahabi V. Antitumor efficacy of Venezuelan equine encephalitis virus replicon particles encoding mutated HPV16 E6 and E7 genes. Vaccine 2004; 22: 520–527.

Miller A. , Center R.J. , Stambas J. Sindbis virus vectors elicit hemagglutinin-specific humoral and cellular immune responses and offer a dose-sparing strategy for vaccination. Vaccine 2008; 26: 5641–5648.

Riezebos-Brilman A. , de Mare A. , Bungener L. , Huckriede A. , Wilschut J. , Daemen T. Recombinant alphaviruses as vectors for anti-tumour and anti-microbial immunotherapy. J Clin Virol 2006; 35: 233–243.

Zheng M. , Jin N.Y. , Liu Q. Immunogenicity and protective efficacy of Semliki Forest virus replicon-based DNA vaccines encoding goatpox virus structural proteins. Virology 2009; 391: 33–43.

Sutmuller R.P. , den Brok M.H. , Kramer M. Toll-like receptor 2 controls expansion and function of regulatory T cells. J Clin Invest 2006; 116: 485–494.

Tran D.Q. , Andersson J. , Hardwick D. , Bebris L. , Illei G.G. , Shevach E.M. Selective expression of latency-associated peptide (LAP) and IL-1 receptor type I/II (CD121a/ CD121b) on activated human FOXP3⁺ regulatory T cells allows for their purification from expansion cultures. Blood 2009; 113: 5125–5133.

Matsushita N. , Pilon-Thomas S.A. , Martin L.M. , Riker A.I. Comparative methodologies of regulatory T cell depletion in a murine melanoma model. J Immunol Methods 2008; 333: 167–179.

Teng M.W. , Swann J.B. , von Scheidt B. Multiple antitumor mechanisms downstream of prophylactic regulatory T-cell depletion. Cancer Res 2010; 70: 2665–2674.

Tuve S. , Chen B.M. , Liu Y. Combination of tumor site-located CTL-associated antigen-4 blockade and systemic regulatory T-cell depletion induces tumor-destructive immune responses. Cancer Res 2007; 67: 5929–5939.

Chuang C.M. , Hoory T. , Monie A. , Wu A. , Wang M.C. , Hung C.F. Enhancing therapeutic HPV DNA vaccine potency through depletion of CD4⁺CD25⁺ T regulatory cells. Vaccine 2009; 27: 684–689.