Cited by 838Immunotherapy and Immune ResponsesImmune Response and InflammationCancer Immunotherapy and Biomarkers

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Tumor-infiltrating DCs suppress nucleic acid–mediated innate immune responses through interactions between the receptor TIM-3 and the alarmin HMGB1

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Chiba, Shigeki, Baghdadi, Muhammad, Akiba, Hisaya, Yoshiyama, Hironori, Kinoshita, Ichiro, Dosaka-Akita, Hirotoshi, Fujioka, Yoichiro, Ohba, Yusuke, Gorman, Jacob V, Colgan, John D, Hirashima, Mitsuomi, Uede, Toshimitsu, Takaoka, Akinori, Yagita, Hideo, Jinushi, Masahisa·2012·Nature Immunology

DOI 10.1038/ni.2376PMC PMC3622453

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Abstract

The mechanisms by which tumor microenvironments modulate nucleic acid-mediated innate immunity remain unknown. Here we identify the receptor TIM-3 as key in circumventing the stimulatory effects of nucleic acids in tumor immunity. Tumor-associated dendritic cells (DCs) in mouse tumors and patients with cancer had high expression of TIM-3. DC-derived TIM-3 suppressed innate immune responses through the recognition of nucleic acids by Toll-like receptors and cytosolic sensors via a galectin-9-independent mechanism. In contrast, TIM-3 interacted with the alarmin HMGB1 to interfere with the recruitment of nucleic acids into DC endosomes and attenuated the therapeutic efficacy of DNA vaccination and chemotherapy by diminishing the immunogenicity of nucleic acids released from dying tumor cells. Our findings define a mechanism whereby tumor microenvironments suppress antitumor immunity mediated by nucleic acids.

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Authors: Chiba, S., Baghdadi, M., Akiba, H., Yoshiyama, H., Kinoshita, I., Dosaka-Akita, H., Fujioka, Y., Ohba, Y., Gorman, J. V., Colgan, J. D., Hirashima, M., Uede, T., Takaoka, A., Yagita, H., & Jinushi, M.
Affiliations: Hokkaido University (JP)
Juntendo University (JP)
University of Iowa (US)
Kagawa University (JP)
Corresponding author: Jinushi, Masahisa
ORCID: Baghdadi, Muhammad
Akiba, Hisaya
Yoshiyama, Hironori
Kinoshita, Ichiro
Fujioka, Yoichiro
Ohba, Yusuke
Colgan, John D
Hirashima, Mitsuomi
Takaoka, Akinori
Venue: Nature Immunology
Publisher: Springer Science and Business Media LLC
Published: 2012-07-29
Volume: 13
Issue: 9
Pages: 832-842
ISSN: 1529-2908 (ISSN-L)
1529-2916
DOI: 10.1038/ni.2376
PMC: PMC3622453
OpenAlex: W2112400160
Cited by: 838
References: 50
Citations by year: 2026: 40 · 2025: 53 · 2024: 81 · 2023: 82 · 2022: 83 · 2021: 80 · 2020: 65 · 2019: 63 · 2018: 56 · 2017: 48 · 2016: 53 · 2015: 41 · 2014: 39 · 2013: 39 · 2012: 15
FWCI: 18.74
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: www.springer.com/tdm (tdm)
Locations: Nature Immunology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Institutional Repositories DataBase (IRDB) (submittedVersion)
Hokkaido University Collection of Scholarly and Academic Papers (Hokkaido University) (submittedVersion)
Funders: Japan Society for the Promotion of Science (23590534, 23591132, 23501283, 22590360, 23390090, 22591098, 22240089, 23659196, 21390113)
National Institute of Allergy and Infectious Diseases (R01AI093737, R01AI067489)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
Keywords: TIM-3, HMGB1, tumor-associated dendritic cells, nucleic acid sensing, innate immunity, tumor microenvironment, Toll-like receptors, galectin-9, DNA vaccine, chemotherapy, antitumor immunity, alarmins
MeSH terms: Hepatitis A Virus Cellular Receptor 2, Animals, Dendritic Cells, Enzyme-Linked Immunosorbent Assay, Flow Cytometry, Humans, Immunity, Innate, Immunologic Surveillance, Mice, Inbred C57BL, Microscopy, Fluorescence, Neoplasms, Nucleic Acids, Receptors, Virus, Immunoblotting, Microscopy, Confocal, Reverse Transcriptase Polymerase Chain Reaction, HMGB1 Protein, Receptors, Pattern Recognition, Mice, Tumor Microenvironment

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Tumor-infiltrating DCs suppress nucleic acid–mediated innate immune responses through interactions between the receptor TIM-3 and the alarmin HMGB1

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