Chemotherapy-induced antitumor immunity requires formyl peptide receptor 1

Erika Vacchelli; Yuting Ma; Elisa E. Baracco; Antonella Sistigu; David P. Enot; Federico Pietrocola; Heng Yang; Sandy Adjemian; Kariman Chaba; Michaela Semeraro; Michele Signore; Adele De Ninno; Valeria Lucarini; Francesca Peschiaroli; Luca Businaro; Annamaria Gerardino; Gwenola Manic; Thomas Ulas; Patrick Günther; Joachim L. Schultze; Oliver Kepp; Gautier Stoll; Céline Lefebvre; Claire Mulot; Francesca Castoldi; Sylvie Rusakiewicz; Sylvain Ladoire; Lionel Apetoh; José Manuel Bravo San Pedro; Monica Lucattelli; Cécile Delarasse; Valérie Boige; Michel Ducreux; Suzette Delaloge; Christophe Borg; Fabrice André; Giovanna Schiavoni; Ilio Vitale; Pierre Laurent-Puig; Fabrizio Mattei; Laurence Zitvogel; Guido Kroemer

doi:10.1126/science.aad0779

Chemotherapy-induced antitumor immunity requires formyl peptide receptor 1

Erika Vacchelli, Yuting Ma, Elisa E. Baracco, Antonella Sistigu, David P. Enot, Federico Pietrocola, Heng Yang, Sandy Adjemian, Kariman Chaba, Michaela Semeraro, Michele Signore, Adele De Ninno, Valeria Lucarini, Francesca Peschiaroli, Luca Businaro, Annamaria Gerardino, Gwenola Manic, Thomas Ulas, Patrick Günther, Joachim L. SchultzeOliver Kepp, Gautier Stoll, Céline Lefebvre, Claire Mulot, Francesca Castoldi, Sylvie Rusakiewicz, Sylvain Ladoire, Lionel Apetoh, José Manuel Bravo San Pedro, Monica Lucattelli, Cécile Delarasse, Valérie Boige, Michel Ducreux, Suzette Delaloge, Christophe Borg, Fabrice André, Giovanna Schiavoni, Ilio Vitale, Pierre Laurent-Puig, Fabrizio Mattei, Laurence Zitvogel, Guido Kroemer

Research output: Contribution to journal › Article › peer-review

385 Citations (Scopus)

Abstract

Antitumor immunity driven by intratumoral dendritic cells contributes to the efficacy of anthracycline-based chemotherapy in cancer.We identified a loss-of-function allele of the gene coding for formyl peptide receptor 1 (FPR1) that was associated with poor metastasis-free and overall survival in breast and colorectal cancer patients receiving adjuvant chemotherapy. The therapeutic effects of anthracyclines were abrogated in tumor-bearing Fpr1^-/- mice due to impaired antitumor immunity. Fpr1-deficient dendritic cells failed to approach dying cancer cells and, as a result, could not elicit antitumor T cell immunity. Experiments performed in a microfluidic device confirmed that FPR1 and its ligand, annexin-1, promoted stable interactions between dying cancer cells and human or murine leukocytes. Altogether, these results highlight the importance of FPR1 in chemotherapy-induced anticancer immune responses.

Original language	English
Pages (from-to)	972-978
Number of pages	7
Journal	Science
Volume	350
Issue number	6263
DOIs	https://doi.org/10.1126/science.aad0779
Publication status	Published - 20 Nov 2015

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Vacchelli, E., Ma, Y., Baracco, E. E., Sistigu, A., Enot, D. P., Pietrocola, F., Yang, H., Adjemian, S., Chaba, K., Semeraro, M., Signore, M., Ninno, A. D., Lucarini, V., Peschiaroli, F., Businaro, L., Gerardino, A., Manic, G., Ulas, T., Günther, P., ... Kroemer, G. (2015). Chemotherapy-induced antitumor immunity requires formyl peptide receptor 1. Science, 350(6263), 972-978. https://doi.org/10.1126/science.aad0779

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title = "Chemotherapy-induced antitumor immunity requires formyl peptide receptor 1",

abstract = "Antitumor immunity driven by intratumoral dendritic cells contributes to the efficacy of anthracycline-based chemotherapy in cancer.We identified a loss-of-function allele of the gene coding for formyl peptide receptor 1 (FPR1) that was associated with poor metastasis-free and overall survival in breast and colorectal cancer patients receiving adjuvant chemotherapy. The therapeutic effects of anthracyclines were abrogated in tumor-bearing Fpr1-/- mice due to impaired antitumor immunity. Fpr1-deficient dendritic cells failed to approach dying cancer cells and, as a result, could not elicit antitumor T cell immunity. Experiments performed in a microfluidic device confirmed that FPR1 and its ligand, annexin-1, promoted stable interactions between dying cancer cells and human or murine leukocytes. Altogether, these results highlight the importance of FPR1 in chemotherapy-induced anticancer immune responses.",

author = "Erika Vacchelli and Yuting Ma and Baracco, {Elisa E.} and Antonella Sistigu and Enot, {David P.} and Federico Pietrocola and Heng Yang and Sandy Adjemian and Kariman Chaba and Michaela Semeraro and Michele Signore and Ninno, {Adele De} and Valeria Lucarini and Francesca Peschiaroli and Luca Businaro and Annamaria Gerardino and Gwenola Manic and Thomas Ulas and Patrick G{\"u}nther and Schultze, {Joachim L.} and Oliver Kepp and Gautier Stoll and C{\'e}line Lefebvre and Claire Mulot and Francesca Castoldi and Sylvie Rusakiewicz and Sylvain Ladoire and Lionel Apetoh and Pedro, {Jos{\'e} Manuel Bravo San} and Monica Lucattelli and C{\'e}cile Delarasse and Val{\'e}rie Boige and Michel Ducreux and Suzette Delaloge and Christophe Borg and Fabrice Andr{\'e} and Giovanna Schiavoni and Ilio Vitale and Pierre Laurent-Puig and Fabrizio Mattei and Laurence Zitvogel and Guido Kroemer",

year = "2015",

month = nov,

day = "20",

doi = "10.1126/science.aad0779",

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Vacchelli, E, Ma, Y, Baracco, EE, Sistigu, A, Enot, DP, Pietrocola, F, Yang, H, Adjemian, S, Chaba, K, Semeraro, M, Signore, M, Ninno, AD, Lucarini, V, Peschiaroli, F, Businaro, L, Gerardino, A, Manic, G, Ulas, T, Günther, P, Schultze, JL, Kepp, O, Stoll, G, Lefebvre, C, Mulot, C, Castoldi, F, Rusakiewicz, S, Ladoire, S, Apetoh, L, Pedro, JMBS, Lucattelli, M, Delarasse, C, Boige, V, Ducreux, M, Delaloge, S, Borg, C, André, F, Schiavoni, G, Vitale, I, Laurent-Puig, P, Mattei, F, Zitvogel, L & Kroemer, G 2015, 'Chemotherapy-induced antitumor immunity requires formyl peptide receptor 1', Science, vol. 350, no. 6263, pp. 972-978. https://doi.org/10.1126/science.aad0779

TY - JOUR

T1 - Chemotherapy-induced antitumor immunity requires formyl peptide receptor 1

AU - Vacchelli, Erika

AU - Ma, Yuting

AU - Baracco, Elisa E.

AU - Sistigu, Antonella

AU - Enot, David P.

AU - Pietrocola, Federico

AU - Yang, Heng

AU - Adjemian, Sandy

AU - Chaba, Kariman

AU - Semeraro, Michaela

AU - Signore, Michele

AU - Ninno, Adele De

AU - Lucarini, Valeria

AU - Peschiaroli, Francesca

AU - Businaro, Luca

AU - Gerardino, Annamaria

AU - Manic, Gwenola

AU - Ulas, Thomas

AU - Günther, Patrick

AU - Schultze, Joachim L.

AU - Kepp, Oliver

AU - Stoll, Gautier

AU - Lefebvre, Céline

AU - Mulot, Claire

AU - Castoldi, Francesca

AU - Rusakiewicz, Sylvie

AU - Ladoire, Sylvain

AU - Apetoh, Lionel

AU - Pedro, José Manuel Bravo San

AU - Lucattelli, Monica

AU - Delarasse, Cécile

AU - Boige, Valérie

AU - Ducreux, Michel

AU - Delaloge, Suzette

AU - Borg, Christophe

AU - André, Fabrice

AU - Schiavoni, Giovanna

AU - Vitale, Ilio

AU - Laurent-Puig, Pierre

AU - Mattei, Fabrizio

AU - Zitvogel, Laurence

AU - Kroemer, Guido

PY - 2015/11/20

Y1 - 2015/11/20

N2 - Antitumor immunity driven by intratumoral dendritic cells contributes to the efficacy of anthracycline-based chemotherapy in cancer.We identified a loss-of-function allele of the gene coding for formyl peptide receptor 1 (FPR1) that was associated with poor metastasis-free and overall survival in breast and colorectal cancer patients receiving adjuvant chemotherapy. The therapeutic effects of anthracyclines were abrogated in tumor-bearing Fpr1-/- mice due to impaired antitumor immunity. Fpr1-deficient dendritic cells failed to approach dying cancer cells and, as a result, could not elicit antitumor T cell immunity. Experiments performed in a microfluidic device confirmed that FPR1 and its ligand, annexin-1, promoted stable interactions between dying cancer cells and human or murine leukocytes. Altogether, these results highlight the importance of FPR1 in chemotherapy-induced anticancer immune responses.

AB - Antitumor immunity driven by intratumoral dendritic cells contributes to the efficacy of anthracycline-based chemotherapy in cancer.We identified a loss-of-function allele of the gene coding for formyl peptide receptor 1 (FPR1) that was associated with poor metastasis-free and overall survival in breast and colorectal cancer patients receiving adjuvant chemotherapy. The therapeutic effects of anthracyclines were abrogated in tumor-bearing Fpr1-/- mice due to impaired antitumor immunity. Fpr1-deficient dendritic cells failed to approach dying cancer cells and, as a result, could not elicit antitumor T cell immunity. Experiments performed in a microfluidic device confirmed that FPR1 and its ligand, annexin-1, promoted stable interactions between dying cancer cells and human or murine leukocytes. Altogether, these results highlight the importance of FPR1 in chemotherapy-induced anticancer immune responses.

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U2 - 10.1126/science.aad0779

DO - 10.1126/science.aad0779

M3 - Article

C2 - 26516201

AN - SCOPUS:84947763610

SN - 0036-8075

VL - 350

SP - 972

EP - 978

JO - Science

JF - Science

IS - 6263

ER -

Chemotherapy-induced antitumor immunity requires formyl peptide receptor 1

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