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Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti–CTLA-4 therapy against melanoma

Treatment with monoclonal antibody specific for cytotoxic T lymphocyte–associated antigen 4 (CTLA-4), an inhibitory receptor expressed by T lymphocytes, has emerged as an effective therapy for the treatment of metastatic melanoma. Although subject to debate, current models favor a mechanism of activ...

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Autores principales: Simpson, Tyler R., Li, Fubin, Montalvo-Ortiz, Welby, Sepulveda, Manuel A., Bergerhoff, Katharina, Arce, Frederick, Roddie, Claire, Henry, Jake Y., Yagita, Hideo, Wolchok, Jedd D., Peggs, Karl S., Ravetch, Jeffrey V., Allison, James P., Quezada, Sergio A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Rockefeller University Press 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3754863/
https://www.ncbi.nlm.nih.gov/pubmed/23897981
http://dx.doi.org/10.1084/jem.20130579
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author Simpson, Tyler R.
Li, Fubin
Montalvo-Ortiz, Welby
Sepulveda, Manuel A.
Bergerhoff, Katharina
Arce, Frederick
Roddie, Claire
Henry, Jake Y.
Yagita, Hideo
Wolchok, Jedd D.
Peggs, Karl S.
Ravetch, Jeffrey V.
Allison, James P.
Quezada, Sergio A.
author_facet Simpson, Tyler R.
Li, Fubin
Montalvo-Ortiz, Welby
Sepulveda, Manuel A.
Bergerhoff, Katharina
Arce, Frederick
Roddie, Claire
Henry, Jake Y.
Yagita, Hideo
Wolchok, Jedd D.
Peggs, Karl S.
Ravetch, Jeffrey V.
Allison, James P.
Quezada, Sergio A.
author_sort Simpson, Tyler R.
collection PubMed
description Treatment with monoclonal antibody specific for cytotoxic T lymphocyte–associated antigen 4 (CTLA-4), an inhibitory receptor expressed by T lymphocytes, has emerged as an effective therapy for the treatment of metastatic melanoma. Although subject to debate, current models favor a mechanism of activity involving blockade of the inhibitory activity of CTLA-4 on both effector (T eff) and regulatory (T reg) T cells, resulting in enhanced antitumor effector T cell activity capable of inducing tumor regression. We demonstrate, however, that the activity of anti–CTLA-4 antibody on the T reg cell compartment is mediated via selective depletion of T reg cells within tumor lesions. Importantly, T reg cell depletion is dependent on the presence of Fcγ receptor–expressing macrophages within the tumor microenvironment, indicating that T reg cells are depleted in trans in a context-dependent manner. Our results reveal further mechanistic insight into the activity of anti-CTLA-4–based cancer immunotherapy, and illustrate the importance of specific features of the local tumor environment on the final outcome of antibody-based immunomodulatory therapies.
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spelling pubmed-37548632014-02-26 Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti–CTLA-4 therapy against melanoma Simpson, Tyler R. Li, Fubin Montalvo-Ortiz, Welby Sepulveda, Manuel A. Bergerhoff, Katharina Arce, Frederick Roddie, Claire Henry, Jake Y. Yagita, Hideo Wolchok, Jedd D. Peggs, Karl S. Ravetch, Jeffrey V. Allison, James P. Quezada, Sergio A. J Exp Med Article Treatment with monoclonal antibody specific for cytotoxic T lymphocyte–associated antigen 4 (CTLA-4), an inhibitory receptor expressed by T lymphocytes, has emerged as an effective therapy for the treatment of metastatic melanoma. Although subject to debate, current models favor a mechanism of activity involving blockade of the inhibitory activity of CTLA-4 on both effector (T eff) and regulatory (T reg) T cells, resulting in enhanced antitumor effector T cell activity capable of inducing tumor regression. We demonstrate, however, that the activity of anti–CTLA-4 antibody on the T reg cell compartment is mediated via selective depletion of T reg cells within tumor lesions. Importantly, T reg cell depletion is dependent on the presence of Fcγ receptor–expressing macrophages within the tumor microenvironment, indicating that T reg cells are depleted in trans in a context-dependent manner. Our results reveal further mechanistic insight into the activity of anti-CTLA-4–based cancer immunotherapy, and illustrate the importance of specific features of the local tumor environment on the final outcome of antibody-based immunomodulatory therapies. The Rockefeller University Press 2013-08-26 /pmc/articles/PMC3754863/ /pubmed/23897981 http://dx.doi.org/10.1084/jem.20130579 Text en © 2013 Simpson et al. This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 3.0 Unported license, as described at http://creativecommons.org/licenses/by-nc-sa/3.0/).
spellingShingle Article
Simpson, Tyler R.
Li, Fubin
Montalvo-Ortiz, Welby
Sepulveda, Manuel A.
Bergerhoff, Katharina
Arce, Frederick
Roddie, Claire
Henry, Jake Y.
Yagita, Hideo
Wolchok, Jedd D.
Peggs, Karl S.
Ravetch, Jeffrey V.
Allison, James P.
Quezada, Sergio A.
Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti–CTLA-4 therapy against melanoma
title Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti–CTLA-4 therapy against melanoma
title_full Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti–CTLA-4 therapy against melanoma
title_fullStr Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti–CTLA-4 therapy against melanoma
title_full_unstemmed Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti–CTLA-4 therapy against melanoma
title_short Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti–CTLA-4 therapy against melanoma
title_sort fc-dependent depletion of tumor-infiltrating regulatory t cells co-defines the efficacy of anti–ctla-4 therapy against melanoma
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3754863/
https://www.ncbi.nlm.nih.gov/pubmed/23897981
http://dx.doi.org/10.1084/jem.20130579
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