Cancer cell–autonomous contribution of type I interferon signaling to the efficacy of chemotherapy

Antonella Sistigu; Takahiro Yamazaki; Erika Vacchelli; Kariman Chaba; David P. Enot; Julien Adam; Ilio Vitale; Aicha Goubar; Elisa E. Baracco; Catarina Remédios; Laetitia Fend; Dalil Hannani; Laetitia Aymeric; Yuting Ma; Mireia Niso-Santano; Oliver Kepp; Joachim L. Schultze; Thomas Tüting; Filippo Belardelli; Laura Bracci; Valentina La Sorsa; Giovanna Ziccheddu; Paola Sestili; Francesca Urbani; Mauro Delorenzi; Magali Lacroix-Triki; Virginie Quidville; Rosa Conforti; Jean Philippe Spano; Lajos Pusztai; Vichnou Poirier-Colame; Suzette Delaloge; Frederique Penault-Llorca; Sylvain Ladoire; Laurent Arnould; Joanna Cyrta; Marie Charlotte Dessoliers; Alexander Eggermont; Marco E. Bianchi; Mikael Pittet; Camilla Engblom; Christina Pfirschke; Xavier Préville; Gilles Uzè; Robert D. Schreiber; Melvyn T. Chow; Mark J. Smyth; Enrico Proietti; Fabrice André; Guido Kroemer; Laurence Zitvogel

doi:10.1038/nm.3708

Cancer cell–autonomous contribution of type I interferon signaling to the efficacy of chemotherapy

Antonella Sistigu, Takahiro Yamazaki, Erika Vacchelli, Kariman Chaba, David P. Enot, Julien Adam, Ilio Vitale, Aicha Goubar, Elisa E. Baracco, Catarina Remédios, Laetitia Fend, Dalil Hannani, Laetitia Aymeric, Yuting Ma, Mireia Niso-Santano, Oliver Kepp, Joachim L. Schultze, Thomas Tüting, Filippo Belardelli, Laura BracciValentina La Sorsa, Giovanna Ziccheddu, Paola Sestili, Francesca Urbani, Mauro Delorenzi, Magali Lacroix-Triki, Virginie Quidville, Rosa Conforti, Jean Philippe Spano, Lajos Pusztai, Vichnou Poirier-Colame, Suzette Delaloge, Frederique Penault-Llorca, Sylvain Ladoire, Laurent Arnould, Joanna Cyrta, Marie Charlotte Dessoliers, Alexander Eggermont, Marco E. Bianchi, Mikael Pittet, Camilla Engblom, Christina Pfirschke, Xavier Préville, Gilles Uzè, Robert D. Schreiber, Melvyn T. Chow, Mark J. Smyth, Enrico Proietti, Fabrice André, Guido Kroemer, Laurence Zitvogel

Résultats de recherche: Contribution à un journal › Article › Revue par des pairs

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Résumé

Some of the anti-neoplastic effects of anthracyclines in mice originate from the induction of innate and T cell–mediated anticancer immune responses. Here we demonstrate that anthracyclines stimulate the rapid production of type I interferons (IFNs) by malignant cells after activation of the endosomal pattern recognition receptor Toll-like receptor 3 (TLR3). By binding to IFN-α and IFN-β receptors (IFNARs) on neoplastic cells, type I IFNs trigger autocrine and paracrine circuitries that result in the release of chemokine (C-X-C motif) ligand 10 (CXCL10). Tumors lacking Tlr3 or Ifnar failed to respond to chemotherapy unless type I IFN or Cxcl10, respectively, was artificially supplied. Moreover, a type I IFN–related signature predicted clinical responses to anthracycline-based chemotherapy in several independent cohorts of patients with breast carcinoma characterized by poor prognosis. Our data suggest that anthracycline-mediated immune responses mimic those induced by viral pathogens. We surmise that such 'viral mimicry' constitutes a hallmark of successful chemotherapy.

langue originale	Anglais
Pages (de - à)	1301-1309
Nombre de pages	9
journal	Nature Medicine
Volume	20
Numéro de publication	11
Les DOIs	https://doi.org/10.1038/nm.3708
état	Publié - 1 nov. 2014

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10.1038/nm.3708

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Sistigu, A., Yamazaki, T., Vacchelli, E., Chaba, K., Enot, D. P., Adam, J., Vitale, I., Goubar, A., Baracco, E. E., Remédios, C., Fend, L., Hannani, D., Aymeric, L., Ma, Y., Niso-Santano, M., Kepp, O., Schultze, J. L., Tüting, T., Belardelli, F., ... Zitvogel, L. (2014). Cancer cell–autonomous contribution of type I interferon signaling to the efficacy of chemotherapy. Nature Medicine, 20(11), 1301-1309. https://doi.org/10.1038/nm.3708

@article{e54857ce19e6422dae108ee8d45ce591,

title = "Cancer cell–autonomous contribution of type I interferon signaling to the efficacy of chemotherapy",

abstract = "Some of the anti-neoplastic effects of anthracyclines in mice originate from the induction of innate and T cell–mediated anticancer immune responses. Here we demonstrate that anthracyclines stimulate the rapid production of type I interferons (IFNs) by malignant cells after activation of the endosomal pattern recognition receptor Toll-like receptor 3 (TLR3). By binding to IFN-α and IFN-β receptors (IFNARs) on neoplastic cells, type I IFNs trigger autocrine and paracrine circuitries that result in the release of chemokine (C-X-C motif) ligand 10 (CXCL10). Tumors lacking Tlr3 or Ifnar failed to respond to chemotherapy unless type I IFN or Cxcl10, respectively, was artificially supplied. Moreover, a type I IFN–related signature predicted clinical responses to anthracycline-based chemotherapy in several independent cohorts of patients with breast carcinoma characterized by poor prognosis. Our data suggest that anthracycline-mediated immune responses mimic those induced by viral pathogens. We surmise that such 'viral mimicry' constitutes a hallmark of successful chemotherapy.",

author = "Antonella Sistigu and Takahiro Yamazaki and Erika Vacchelli and Kariman Chaba and Enot, {David P.} and Julien Adam and Ilio Vitale and Aicha Goubar and Baracco, {Elisa E.} and Catarina Rem{\'e}dios and Laetitia Fend and Dalil Hannani and Laetitia Aymeric and Yuting Ma and Mireia Niso-Santano and Oliver Kepp and Schultze, {Joachim L.} and Thomas T{\"u}ting and Filippo Belardelli and Laura Bracci and {La Sorsa}, Valentina and Giovanna Ziccheddu and Paola Sestili and Francesca Urbani and Mauro Delorenzi and Magali Lacroix-Triki and Virginie Quidville and Rosa Conforti and Spano, {Jean Philippe} and Lajos Pusztai and Vichnou Poirier-Colame and Suzette Delaloge and Frederique Penault-Llorca and Sylvain Ladoire and Laurent Arnould and Joanna Cyrta and Dessoliers, {Marie Charlotte} and Alexander Eggermont and Bianchi, {Marco E.} and Mikael Pittet and Camilla Engblom and Christina Pfirschke and Xavier Pr{\'e}ville and Gilles Uz{\`e} and Schreiber, {Robert D.} and Chow, {Melvyn T.} and Smyth, {Mark J.} and Enrico Proietti and Fabrice Andr{\'e} and Guido Kroemer and Laurence Zitvogel",

year = "2014",

month = nov,

day = "1",

doi = "10.1038/nm.3708",

language = "English",

volume = "20",

pages = "1301--1309",

journal = "Nature Medicine",

issn = "1078-8956",

number = "11",

}

Sistigu, A, Yamazaki, T, Vacchelli, E, Chaba, K, Enot, DP, Adam, J, Vitale, I, Goubar, A, Baracco, EE, Remédios, C, Fend, L, Hannani, D, Aymeric, L, Ma, Y, Niso-Santano, M, Kepp, O, Schultze, JL, Tüting, T, Belardelli, F, Bracci, L, La Sorsa, V, Ziccheddu, G, Sestili, P, Urbani, F, Delorenzi, M, Lacroix-Triki, M, Quidville, V, Conforti, R, Spano, JP, Pusztai, L, Poirier-Colame, V, Delaloge, S, Penault-Llorca, F, Ladoire, S, Arnould, L, Cyrta, J, Dessoliers, MC, Eggermont, A, Bianchi, ME, Pittet, M, Engblom, C, Pfirschke, C, Préville, X, Uzè, G, Schreiber, RD, Chow, MT, Smyth, MJ, Proietti, E, André, F, Kroemer, G & Zitvogel, L 2014, 'Cancer cell–autonomous contribution of type I interferon signaling to the efficacy of chemotherapy', Nature Medicine, VOL. 20, Numéro 11, p. 1301-1309. https://doi.org/10.1038/nm.3708

TY - JOUR

T1 - Cancer cell–autonomous contribution of type I interferon signaling to the efficacy of chemotherapy

AU - Sistigu, Antonella

AU - Yamazaki, Takahiro

AU - Vacchelli, Erika

AU - Chaba, Kariman

AU - Enot, David P.

AU - Adam, Julien

AU - Vitale, Ilio

AU - Goubar, Aicha

AU - Baracco, Elisa E.

AU - Remédios, Catarina

AU - Fend, Laetitia

AU - Hannani, Dalil

AU - Aymeric, Laetitia

AU - Ma, Yuting

AU - Niso-Santano, Mireia

AU - Kepp, Oliver

AU - Schultze, Joachim L.

AU - Tüting, Thomas

AU - Belardelli, Filippo

AU - Bracci, Laura

AU - La Sorsa, Valentina

AU - Ziccheddu, Giovanna

AU - Sestili, Paola

AU - Urbani, Francesca

AU - Delorenzi, Mauro

AU - Lacroix-Triki, Magali

AU - Quidville, Virginie

AU - Conforti, Rosa

AU - Spano, Jean Philippe

AU - Pusztai, Lajos

AU - Poirier-Colame, Vichnou

AU - Delaloge, Suzette

AU - Penault-Llorca, Frederique

AU - Ladoire, Sylvain

AU - Arnould, Laurent

AU - Cyrta, Joanna

AU - Dessoliers, Marie Charlotte

AU - Eggermont, Alexander

AU - Bianchi, Marco E.

AU - Pittet, Mikael

AU - Engblom, Camilla

AU - Pfirschke, Christina

AU - Préville, Xavier

AU - Uzè, Gilles

AU - Schreiber, Robert D.

AU - Chow, Melvyn T.

AU - Smyth, Mark J.

AU - Proietti, Enrico

AU - André, Fabrice

AU - Kroemer, Guido

AU - Zitvogel, Laurence

PY - 2014/11/1

Y1 - 2014/11/1

N2 - Some of the anti-neoplastic effects of anthracyclines in mice originate from the induction of innate and T cell–mediated anticancer immune responses. Here we demonstrate that anthracyclines stimulate the rapid production of type I interferons (IFNs) by malignant cells after activation of the endosomal pattern recognition receptor Toll-like receptor 3 (TLR3). By binding to IFN-α and IFN-β receptors (IFNARs) on neoplastic cells, type I IFNs trigger autocrine and paracrine circuitries that result in the release of chemokine (C-X-C motif) ligand 10 (CXCL10). Tumors lacking Tlr3 or Ifnar failed to respond to chemotherapy unless type I IFN or Cxcl10, respectively, was artificially supplied. Moreover, a type I IFN–related signature predicted clinical responses to anthracycline-based chemotherapy in several independent cohorts of patients with breast carcinoma characterized by poor prognosis. Our data suggest that anthracycline-mediated immune responses mimic those induced by viral pathogens. We surmise that such 'viral mimicry' constitutes a hallmark of successful chemotherapy.

AB - Some of the anti-neoplastic effects of anthracyclines in mice originate from the induction of innate and T cell–mediated anticancer immune responses. Here we demonstrate that anthracyclines stimulate the rapid production of type I interferons (IFNs) by malignant cells after activation of the endosomal pattern recognition receptor Toll-like receptor 3 (TLR3). By binding to IFN-α and IFN-β receptors (IFNARs) on neoplastic cells, type I IFNs trigger autocrine and paracrine circuitries that result in the release of chemokine (C-X-C motif) ligand 10 (CXCL10). Tumors lacking Tlr3 or Ifnar failed to respond to chemotherapy unless type I IFN or Cxcl10, respectively, was artificially supplied. Moreover, a type I IFN–related signature predicted clinical responses to anthracycline-based chemotherapy in several independent cohorts of patients with breast carcinoma characterized by poor prognosis. Our data suggest that anthracycline-mediated immune responses mimic those induced by viral pathogens. We surmise that such 'viral mimicry' constitutes a hallmark of successful chemotherapy.

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U2 - 10.1038/nm.3708

DO - 10.1038/nm.3708

M3 - Article

C2 - 25344738

AN - SCOPUS:84913586780

SN - 1078-8956

VL - 20

SP - 1301

EP - 1309

JO - Nature Medicine

JF - Nature Medicine

IS - 11

ER -