IL-5-producing CD4 + T cells and eosinophils cooperate to enhance response to immune checkpoint blockade in breast cancer
Immune checkpoint blockade (ICB) has heralded a new era in cancer therapy. Research into the mechanisms underlying response to ICB has predominantly focused on T cells; however, effective immune responses require tightly regulated crosstalk between innate and adaptive immune cells. Here, we combine...
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| Published in: | Cancer cell Vol. 41; no. 1; p. 106 |
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| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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United States
09.01.2023
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| ISSN: | 1878-3686, 1878-3686 |
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| Abstract | Immune checkpoint blockade (ICB) has heralded a new era in cancer therapy. Research into the mechanisms underlying response to ICB has predominantly focused on T cells; however, effective immune responses require tightly regulated crosstalk between innate and adaptive immune cells. Here, we combine unbiased analysis of blood and tumors from metastatic breast cancer patients treated with ICB with mechanistic studies in mouse models of breast cancer. We observe an increase in systemic and intratumoral eosinophils in patients and mice responding to ICB treatment. Mechanistically, ICB increased IL-5 production by CD4
T cells, stimulating elevated eosinophil production from the bone marrow, leading to systemic eosinophil expansion. Additional induction of IL-33 by ICB-cisplatin combination or recombinant IL-33 promotes intratumoral eosinophil infiltration and eosinophil-dependent CD8
T cell activation to enhance ICB response. This work demonstrates the critical role of eosinophils in ICB response and provides proof-of-principle for eosinophil engagement to enhance ICB efficacy. |
|---|---|
| AbstractList | Immune checkpoint blockade (ICB) has heralded a new era in cancer therapy. Research into the mechanisms underlying response to ICB has predominantly focused on T cells; however, effective immune responses require tightly regulated crosstalk between innate and adaptive immune cells. Here, we combine unbiased analysis of blood and tumors from metastatic breast cancer patients treated with ICB with mechanistic studies in mouse models of breast cancer. We observe an increase in systemic and intratumoral eosinophils in patients and mice responding to ICB treatment. Mechanistically, ICB increased IL-5 production by CD4+ T cells, stimulating elevated eosinophil production from the bone marrow, leading to systemic eosinophil expansion. Additional induction of IL-33 by ICB-cisplatin combination or recombinant IL-33 promotes intratumoral eosinophil infiltration and eosinophil-dependent CD8+ T cell activation to enhance ICB response. This work demonstrates the critical role of eosinophils in ICB response and provides proof-of-principle for eosinophil engagement to enhance ICB efficacy.Immune checkpoint blockade (ICB) has heralded a new era in cancer therapy. Research into the mechanisms underlying response to ICB has predominantly focused on T cells; however, effective immune responses require tightly regulated crosstalk between innate and adaptive immune cells. Here, we combine unbiased analysis of blood and tumors from metastatic breast cancer patients treated with ICB with mechanistic studies in mouse models of breast cancer. We observe an increase in systemic and intratumoral eosinophils in patients and mice responding to ICB treatment. Mechanistically, ICB increased IL-5 production by CD4+ T cells, stimulating elevated eosinophil production from the bone marrow, leading to systemic eosinophil expansion. Additional induction of IL-33 by ICB-cisplatin combination or recombinant IL-33 promotes intratumoral eosinophil infiltration and eosinophil-dependent CD8+ T cell activation to enhance ICB response. This work demonstrates the critical role of eosinophils in ICB response and provides proof-of-principle for eosinophil engagement to enhance ICB efficacy. Immune checkpoint blockade (ICB) has heralded a new era in cancer therapy. Research into the mechanisms underlying response to ICB has predominantly focused on T cells; however, effective immune responses require tightly regulated crosstalk between innate and adaptive immune cells. Here, we combine unbiased analysis of blood and tumors from metastatic breast cancer patients treated with ICB with mechanistic studies in mouse models of breast cancer. We observe an increase in systemic and intratumoral eosinophils in patients and mice responding to ICB treatment. Mechanistically, ICB increased IL-5 production by CD4 T cells, stimulating elevated eosinophil production from the bone marrow, leading to systemic eosinophil expansion. Additional induction of IL-33 by ICB-cisplatin combination or recombinant IL-33 promotes intratumoral eosinophil infiltration and eosinophil-dependent CD8 T cell activation to enhance ICB response. This work demonstrates the critical role of eosinophils in ICB response and provides proof-of-principle for eosinophil engagement to enhance ICB efficacy. |
| Author | Kersten, Kelly Voest, Emile E Spagnuolo, Lorenzo Thommen, Daniela S Afonina, Inna S Vrijland, Kim Garner, Hannah Kos, Kevin de Visser, Karin E Wessels, Lodewyk F A Isaeva, Olga I Beyaert, Rudi Kaptein, Paulien Hoes, Louisa Pastoors, Dorien Chalabi, Myriam Hau, Cheei-Sing Kaldenbach, Daphne Klaver, Chris Kok, Marleen Duijst, Maxime van Dyk, Ewald Raeven, Elisabeth A M Baas, Paul Brüggemann, Marieke Voorwerk, Leonie Theelen, Willemijn S M E Blomberg, Olga S Bakker, Noor |
| Author_xml | – sequence: 1 givenname: Olga S surname: Blomberg fullname: Blomberg, Olga S organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands; Oncode Institute, Utrecht, the Netherlands; Department of Immunology, Leiden University Medical Centre, Leiden, the Netherlands – sequence: 2 givenname: Lorenzo surname: Spagnuolo fullname: Spagnuolo, Lorenzo organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands; Oncode Institute, Utrecht, the Netherlands – sequence: 3 givenname: Hannah surname: Garner fullname: Garner, Hannah organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands; Oncode Institute, Utrecht, the Netherlands – sequence: 4 givenname: Leonie surname: Voorwerk fullname: Voorwerk, Leonie organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands – sequence: 5 givenname: Olga I surname: Isaeva fullname: Isaeva, Olga I organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands; Division of Molecular Carcinogenesis, The Netherlands Cancer Institute, Amsterdam, the Netherlands – sequence: 6 givenname: Ewald surname: van Dyk fullname: van Dyk, Ewald organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands; Oncode Institute, Utrecht, the Netherlands; Division of Molecular Carcinogenesis, The Netherlands Cancer Institute, Amsterdam, the Netherlands – sequence: 7 givenname: Noor surname: Bakker fullname: Bakker, Noor organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands; Oncode Institute, Utrecht, the Netherlands – sequence: 8 givenname: Myriam surname: Chalabi fullname: Chalabi, Myriam organization: Division of Molecular Oncology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands; Department of Gastrointestinal Oncology, The Netherlands Cancer Institute, Amsterdam, the Netherlands; Department of Medical Oncology, The Netherlands Cancer Institute, Amsterdam, the Netherlands – sequence: 9 givenname: Chris surname: Klaver fullname: Klaver, Chris organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands – sequence: 10 givenname: Maxime surname: Duijst fullname: Duijst, Maxime organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands – sequence: 11 givenname: Kelly surname: Kersten fullname: Kersten, Kelly organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands – sequence: 12 givenname: Marieke surname: Brüggemann fullname: Brüggemann, Marieke organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands – sequence: 13 givenname: Dorien surname: Pastoors fullname: Pastoors, Dorien organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands; Oncode Institute, Utrecht, the Netherlands – sequence: 14 givenname: Cheei-Sing surname: Hau fullname: Hau, Cheei-Sing organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands; Oncode Institute, Utrecht, the Netherlands – sequence: 15 givenname: Kim surname: Vrijland fullname: Vrijland, Kim organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands; Oncode Institute, Utrecht, the Netherlands – sequence: 16 givenname: Elisabeth A M surname: Raeven fullname: Raeven, Elisabeth A M organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands; Oncode Institute, Utrecht, the Netherlands – sequence: 17 givenname: Daphne surname: Kaldenbach fullname: Kaldenbach, Daphne organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands; Oncode Institute, Utrecht, the Netherlands – sequence: 18 givenname: Kevin surname: Kos fullname: Kos, Kevin organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands; Oncode Institute, Utrecht, the Netherlands; Department of Immunology, Leiden University Medical Centre, Leiden, the Netherlands – sequence: 19 givenname: Inna S surname: Afonina fullname: Afonina, Inna S organization: VIB-UGent Center for Inflammation Research, Ghent University, Ghent, Belgium; Department of Biomedical Molecular Biology, Ghent University, Ghent, Belgium – sequence: 20 givenname: Paulien surname: Kaptein fullname: Kaptein, Paulien organization: Division of Molecular Oncology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands – sequence: 21 givenname: Louisa surname: Hoes fullname: Hoes, Louisa organization: Oncode Institute, Utrecht, the Netherlands; Division of Molecular Oncology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands; Department of Medical Oncology, The Netherlands Cancer Institute, Amsterdam, the Netherlands – sequence: 22 givenname: Willemijn S M E surname: Theelen fullname: Theelen, Willemijn S M E organization: Department of Thoracic Oncology, The Netherlands Cancer Institute, Amsterdam, the Netherlands – sequence: 23 givenname: Paul surname: Baas fullname: Baas, Paul organization: Department of Thoracic Oncology, The Netherlands Cancer Institute, Amsterdam, the Netherlands – sequence: 24 givenname: Emile E surname: Voest fullname: Voest, Emile E organization: Oncode Institute, Utrecht, the Netherlands; Division of Molecular Oncology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands; Department of Medical Oncology, The Netherlands Cancer Institute, Amsterdam, the Netherlands – sequence: 25 givenname: Rudi surname: Beyaert fullname: Beyaert, Rudi organization: VIB-UGent Center for Inflammation Research, Ghent University, Ghent, Belgium; Department of Biomedical Molecular Biology, Ghent University, Ghent, Belgium – sequence: 26 givenname: Daniela S surname: Thommen fullname: Thommen, Daniela S organization: Division of Molecular Oncology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands – sequence: 27 givenname: Lodewyk F A surname: Wessels fullname: Wessels, Lodewyk F A organization: Oncode Institute, Utrecht, the Netherlands; Division of Molecular Carcinogenesis, The Netherlands Cancer Institute, Amsterdam, the Netherlands – sequence: 28 givenname: Karin E surname: de Visser fullname: de Visser, Karin E email: k.d.visser@nki.nl organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands; Oncode Institute, Utrecht, the Netherlands; Department of Immunology, Leiden University Medical Centre, Leiden, the Netherlands. Electronic address: k.d.visser@nki.nl – sequence: 29 givenname: Marleen surname: Kok fullname: Kok, Marleen email: m.kok@nki.nl organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute, Amsterdam, the Netherlands; Department of Medical Oncology, The Netherlands Cancer Institute, Amsterdam, the Netherlands. Electronic address: m.kok@nki.nl |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36525971$$D View this record in MEDLINE/PubMed |
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| Keywords | myeloid cells CD4(+) T cells IL-5 breast cancer eosinophils IL-33 immune checkpoint blockade |
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| SubjectTerms | Animals Antigen Presentation CD4-Positive T-Lymphocytes - pathology CD8-Positive T-Lymphocytes Eosinophils - pathology Immune Checkpoint Inhibitors - therapeutic use Interleukin-33 Interleukin-5 - therapeutic use Mice Neoplasms - drug therapy |
| Title | IL-5-producing CD4 + T cells and eosinophils cooperate to enhance response to immune checkpoint blockade in breast cancer |
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