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Cancer Immunology Research
Cancer Immunology Research
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Research Articles

Activated Eosinophils Exert Antitumorigenic Activities in Colorectal Cancer

Hadar Reichman, Michal Itan, Perri Rozenberg, Tal Yarmolovski, Eli Brazowski, Chen Varol, Nathan Gluck, Shiran Shapira, Nadir Arber, Udi Qimron, Danielle Karo-Atar, James J. Lee and Ariel Munitz
Hadar Reichman
1Department of Clinical Microbiology and Immunology, the Sackler School of Medicine, Tel Aviv University, Ramat Aviv, Israel.
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Michal Itan
1Department of Clinical Microbiology and Immunology, the Sackler School of Medicine, Tel Aviv University, Ramat Aviv, Israel.
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Perri Rozenberg
1Department of Clinical Microbiology and Immunology, the Sackler School of Medicine, Tel Aviv University, Ramat Aviv, Israel.
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Tal Yarmolovski
1Department of Clinical Microbiology and Immunology, the Sackler School of Medicine, Tel Aviv University, Ramat Aviv, Israel.
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Eli Brazowski
2Research Center for Digestive Tract and Disorders and Liver Diseases, Tel Aviv Sourasky Medical Center, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel.
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Chen Varol
2Research Center for Digestive Tract and Disorders and Liver Diseases, Tel Aviv Sourasky Medical Center, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel.
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  • ORCID record for Chen Varol
Nathan Gluck
2Research Center for Digestive Tract and Disorders and Liver Diseases, Tel Aviv Sourasky Medical Center, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel.
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Shiran Shapira
3Integrated Cancer Prevention Center, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel.
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Nadir Arber
3Integrated Cancer Prevention Center, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel.
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Udi Qimron
1Department of Clinical Microbiology and Immunology, the Sackler School of Medicine, Tel Aviv University, Ramat Aviv, Israel.
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Danielle Karo-Atar
1Department of Clinical Microbiology and Immunology, the Sackler School of Medicine, Tel Aviv University, Ramat Aviv, Israel.
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James J. Lee
4Division of Pulmonary Medicine, Department of Biochemistry and Molecular Biology, Mayo Clinic Arizona, Scottsdale, Arizona.
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Ariel Munitz
1Department of Clinical Microbiology and Immunology, the Sackler School of Medicine, Tel Aviv University, Ramat Aviv, Israel.
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  • ORCID record for Ariel Munitz
  • For correspondence: arielm@tauex.tau.ac.il
DOI: 10.1158/2326-6066.CIR-18-0494 Published March 2019
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Abstract

Immunotherapies targeting T lymphocytes are revolutionizing cancer therapy but only benefit a subset of patients, especially in colorectal cancer. Thus, additional insight into the tumor microenvironment (TME) is required. Eosinophils are bone marrow–derived cells that have been largely studied in the context of allergic diseases and parasite infections. Although tumor-associated eosinophilia has been described in various solid tumors including colorectal cancer, knowledge is still missing regarding eosinophil activities and even the basic question of whether the TME promotes eosinophil recruitment without additional manipulation (e.g., immunotherapy) is unclear. Herein, we report that eosinophils are recruited into developing tumors during induction of inflammation-induced colorectal cancer and in mice with the Apcmin/+ genotype, which develop spontaneous intestinal adenomas. Using adoptive transfer and cytokine neutralization experiments, we demonstrate that the TME supported prolonged eosinophil survival independent of IL5, an eosinophil survival cytokine. Tumor-infiltrating eosinophils consisted of degranulating eosinophils and were essential for tumor rejection independently of CD8+ T cells. Transcriptome and proteomic analysis revealed an IFNγ-linked signature for intratumoral eosinophils that was different from that of macrophages. Our data establish antitumorigenic roles for eosinophils in colorectal cancer. These findings may facilitate the development of pharmacologic treatments that could unleash antitumor responses by eosinophils, especially in colorectal cancer patients displaying eosinophilia.

Footnotes

  • Note: Supplementary data for this article are available at Cancer Immunology Research Online (http://cancerimmunolres.aacrjournals.org/).

  • ↵†Deceased

  • Received July 23, 2018.
  • Revision received October 14, 2018.
  • Accepted December 17, 2018.
  • Published first January 21, 2019.
  • ©2019 American Association for Cancer Research.
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Cancer Immunology Research: 7 (3)
March 2019
Volume 7, Issue 3
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Activated Eosinophils Exert Antitumorigenic Activities in Colorectal Cancer
Hadar Reichman, Michal Itan, Perri Rozenberg, Tal Yarmolovski, Eli Brazowski, Chen Varol, Nathan Gluck, Shiran Shapira, Nadir Arber, Udi Qimron, Danielle Karo-Atar, James J. Lee and Ariel Munitz
Cancer Immunol Res March 1 2019 (7) (3) 388-400; DOI: 10.1158/2326-6066.CIR-18-0494

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Activated Eosinophils Exert Antitumorigenic Activities in Colorectal Cancer
Hadar Reichman, Michal Itan, Perri Rozenberg, Tal Yarmolovski, Eli Brazowski, Chen Varol, Nathan Gluck, Shiran Shapira, Nadir Arber, Udi Qimron, Danielle Karo-Atar, James J. Lee and Ariel Munitz
Cancer Immunol Res March 1 2019 (7) (3) 388-400; DOI: 10.1158/2326-6066.CIR-18-0494
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