Eribulin mesylate exerts antitumor effects via CD103

Eribulin mesylate (ERB) is a synthetic analog of halichondrin B, inhibiting tumor cell growth by disrupting microtubule function. Recently, anticancer drugs have been shown to not only act directly on tumor cells but also to exert antitumor effects by modifying the tumor environment. Although ERB ha...

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Main Authors: Kazumasa Oya, Yoshiyuki Nakamura, Rei Watanabe, Ryota Tanaka, Yuki Ichimura, Noriko Kubota, Yutaka Matsumura, Hideaki Tahara, Naoko Okiyama, Manabu Fujimoto, Toshifumi Nomura, Yasuhiro Fujisawa
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Language:English
Published: Taylor & Francis Group 2023-12-01
Series:OncoImmunology
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Online Access:https://www.tandfonline.com/doi/10.1080/2162402X.2023.2218782
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author Kazumasa Oya
Yoshiyuki Nakamura
Rei Watanabe
Ryota Tanaka
Yuki Ichimura
Noriko Kubota
Yutaka Matsumura
Hideaki Tahara
Naoko Okiyama
Manabu Fujimoto
Toshifumi Nomura
Yasuhiro Fujisawa
author_facet Kazumasa Oya
Yoshiyuki Nakamura
Rei Watanabe
Ryota Tanaka
Yuki Ichimura
Noriko Kubota
Yutaka Matsumura
Hideaki Tahara
Naoko Okiyama
Manabu Fujimoto
Toshifumi Nomura
Yasuhiro Fujisawa
author_sort Kazumasa Oya
collection DOAJ
description Eribulin mesylate (ERB) is a synthetic analog of halichondrin B, inhibiting tumor cell growth by disrupting microtubule function. Recently, anticancer drugs have been shown to not only act directly on tumor cells but also to exert antitumor effects by modifying the tumor environment. Although ERB has also been speculated to modify the tumor microenvironment including the immune response to tumors, the precise mechanism remains unclear. In our study, ERB suppressed the tumor growth of MC38 colon cancer in wildtype mice, whereas ERB failed to inhibit the tumor growth in Rag1-deficient mice which lack both B and T cells. Moreover, depletion of either CD4+ or CD8+ T cells abrogated the antitumor effect of ERB, indicating that both CD4+ and CD8+ T cells play an important role in ERB-induced antitumor effects. Furthermore, ERB treatment increased the number of tumor infiltrating lymphocytes (TILs) as well as the expression of activation markers (CD38 and CD69), immune checkpoint molecules (LAG3, TIGIT and Tim3) and cytotoxic molecules (granzyme B and perforin) in TILs. ERB upregulated E-cadherin expression in MC38. CD103 is a ligand of E-cadherin and induces T-cell activation. ERB increased the proportion of CD103+ cells in both CD4+ and CD8+ TILs. The ERB-induced antitumor effect with the increased TIL number and the increased expression of activation markers, inhibitory checkpoint molecules and cytotoxic molecules in TILs was abrogated in CD103-deficient mice. Collectively, these results suggest that ERB exerts antitumor effects by upregulation of E-cadherin expression in tumor cells and subsequent activation of CD103+ TILs.
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spelling doaj-art-e8d35e9ee38e423c8bdae4bb3ecb9b002025-08-20T02:01:30ZengTaylor & Francis GroupOncoImmunology2162-402X2023-12-0112110.1080/2162402X.2023.2218782Eribulin mesylate exerts antitumor effects via CD103Kazumasa Oya0Yoshiyuki Nakamura1Rei Watanabe2Ryota Tanaka3Yuki Ichimura4Noriko Kubota5Yutaka Matsumura6Hideaki Tahara7Naoko Okiyama8Manabu Fujimoto9Toshifumi Nomura10Yasuhiro Fujisawa11The Department of Dermatology, Faculty of Medicine, University of Tsukuba, Tsukuba, JapanThe Department of Dermatology, Faculty of Medicine, University of Tsukuba, Tsukuba, JapanThe Department of Dermatology, Graduate School of Medicine, Osaka University, Osaka, JapanThe Department of Dermatology, Faculty of Medicine, University of Tsukuba, Tsukuba, JapanThe Department of Dermatology, Faculty of Medicine, University of Tsukuba, Tsukuba, JapanThe Department of Dermatology, Faculty of Medicine, University of Tsukuba, Tsukuba, JapanThe Department of Dermatology, Graduate School of Medicine, Osaka University, Osaka, JapanProject Division of Cancer Biomolecular Therapy, Institute of Medical Science, The University of Tokyo, Tokyo, JapanDepartment of Dermatology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo, JapanThe Department of Dermatology, Graduate School of Medicine, Osaka University, Osaka, JapanThe Department of Dermatology, Faculty of Medicine, University of Tsukuba, Tsukuba, JapanThe Department of Dermatology, Faculty of Medicine, University of Tsukuba, Tsukuba, JapanEribulin mesylate (ERB) is a synthetic analog of halichondrin B, inhibiting tumor cell growth by disrupting microtubule function. Recently, anticancer drugs have been shown to not only act directly on tumor cells but also to exert antitumor effects by modifying the tumor environment. Although ERB has also been speculated to modify the tumor microenvironment including the immune response to tumors, the precise mechanism remains unclear. In our study, ERB suppressed the tumor growth of MC38 colon cancer in wildtype mice, whereas ERB failed to inhibit the tumor growth in Rag1-deficient mice which lack both B and T cells. Moreover, depletion of either CD4+ or CD8+ T cells abrogated the antitumor effect of ERB, indicating that both CD4+ and CD8+ T cells play an important role in ERB-induced antitumor effects. Furthermore, ERB treatment increased the number of tumor infiltrating lymphocytes (TILs) as well as the expression of activation markers (CD38 and CD69), immune checkpoint molecules (LAG3, TIGIT and Tim3) and cytotoxic molecules (granzyme B and perforin) in TILs. ERB upregulated E-cadherin expression in MC38. CD103 is a ligand of E-cadherin and induces T-cell activation. ERB increased the proportion of CD103+ cells in both CD4+ and CD8+ TILs. The ERB-induced antitumor effect with the increased TIL number and the increased expression of activation markers, inhibitory checkpoint molecules and cytotoxic molecules in TILs was abrogated in CD103-deficient mice. Collectively, these results suggest that ERB exerts antitumor effects by upregulation of E-cadherin expression in tumor cells and subsequent activation of CD103+ TILs.https://www.tandfonline.com/doi/10.1080/2162402X.2023.2218782antitumor effectCD103eribulin mesylateimmune checkpointresident memory T cells
spellingShingle Kazumasa Oya
Yoshiyuki Nakamura
Rei Watanabe
Ryota Tanaka
Yuki Ichimura
Noriko Kubota
Yutaka Matsumura
Hideaki Tahara
Naoko Okiyama
Manabu Fujimoto
Toshifumi Nomura
Yasuhiro Fujisawa
Eribulin mesylate exerts antitumor effects via CD103
OncoImmunology
antitumor effect
CD103
eribulin mesylate
immune checkpoint
resident memory T cells
title Eribulin mesylate exerts antitumor effects via CD103
title_full Eribulin mesylate exerts antitumor effects via CD103
title_fullStr Eribulin mesylate exerts antitumor effects via CD103
title_full_unstemmed Eribulin mesylate exerts antitumor effects via CD103
title_short Eribulin mesylate exerts antitumor effects via CD103
title_sort eribulin mesylate exerts antitumor effects via cd103
topic antitumor effect
CD103
eribulin mesylate
immune checkpoint
resident memory T cells
url https://www.tandfonline.com/doi/10.1080/2162402X.2023.2218782
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