Type 1 innate lymphoid cell–immature neutrophil axis suppresses acute tissue inflammation

Abstract Immature neutrophils (imNeu) are a minor population of circulating neutrophils that migrate from the bone marrow (BM) into the circulation and inflamed tissues during infection, injury, physical stress, and cancer. However, the underlying mechanism of their mobilization from BM and its path...

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Main Authors: Kenshiro Matsuda, Natsuki Ide, Yan Xu, Ayana Iijima, Akira Shibuya
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-61504-8
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author Kenshiro Matsuda
Natsuki Ide
Yan Xu
Ayana Iijima
Akira Shibuya
author_facet Kenshiro Matsuda
Natsuki Ide
Yan Xu
Ayana Iijima
Akira Shibuya
author_sort Kenshiro Matsuda
collection DOAJ
description Abstract Immature neutrophils (imNeu) are a minor population of circulating neutrophils that migrate from the bone marrow (BM) into the circulation and inflamed tissues during infection, injury, physical stress, and cancer. However, the underlying mechanism of their mobilization from BM and its pathophysiological significance remains incompletely understood. Here, we show that interferon-gamma (IFN-γ) derived from type 1 innate lymphoid cells (ILC1) enhances the migration of imNeu, but not mature neutrophils, from the BM into inflamed liver tissue with ischemia–reperfusion injury and the blood circulation during polymicrobial sepsis in mice. Mechanistically, the scaffold protein Ahnak, which is specifically expressed in imNeu, underpins Smad7 nuclear translocation in response to IFN-γ, thus downregulating C-X-C chemokine receptor 4 expression critical for neutrophil retention in the BM. Furthermore, imNeu produce interleukin-10 to ameliorate tissue inflammation. Our findings thus reveal the ILC1–imNeu axis that protects tissues from acute inflammation due to injury or microbial infection.
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publishDate 2025-07-01
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spelling doaj-art-cefb9acb0a7f4961ade1e6bae7fdca4b2025-08-20T03:46:15ZengNature PortfolioNature Communications2041-17232025-07-0116111610.1038/s41467-025-61504-8Type 1 innate lymphoid cell–immature neutrophil axis suppresses acute tissue inflammationKenshiro Matsuda0Natsuki Ide1Yan Xu2Ayana Iijima3Akira Shibuya4Department of Immunology, Institute of Medicine, University of TsukubaDepartment of Immunology, Institute of Medicine, University of TsukubaDepartment of Immunology, Institute of Medicine, University of TsukubaDepartment of Immunology, Institute of Medicine, University of TsukubaDepartment of Immunology, Institute of Medicine, University of TsukubaAbstract Immature neutrophils (imNeu) are a minor population of circulating neutrophils that migrate from the bone marrow (BM) into the circulation and inflamed tissues during infection, injury, physical stress, and cancer. However, the underlying mechanism of their mobilization from BM and its pathophysiological significance remains incompletely understood. Here, we show that interferon-gamma (IFN-γ) derived from type 1 innate lymphoid cells (ILC1) enhances the migration of imNeu, but not mature neutrophils, from the BM into inflamed liver tissue with ischemia–reperfusion injury and the blood circulation during polymicrobial sepsis in mice. Mechanistically, the scaffold protein Ahnak, which is specifically expressed in imNeu, underpins Smad7 nuclear translocation in response to IFN-γ, thus downregulating C-X-C chemokine receptor 4 expression critical for neutrophil retention in the BM. Furthermore, imNeu produce interleukin-10 to ameliorate tissue inflammation. Our findings thus reveal the ILC1–imNeu axis that protects tissues from acute inflammation due to injury or microbial infection.https://doi.org/10.1038/s41467-025-61504-8
spellingShingle Kenshiro Matsuda
Natsuki Ide
Yan Xu
Ayana Iijima
Akira Shibuya
Type 1 innate lymphoid cell–immature neutrophil axis suppresses acute tissue inflammation
Nature Communications
title Type 1 innate lymphoid cell–immature neutrophil axis suppresses acute tissue inflammation
title_full Type 1 innate lymphoid cell–immature neutrophil axis suppresses acute tissue inflammation
title_fullStr Type 1 innate lymphoid cell–immature neutrophil axis suppresses acute tissue inflammation
title_full_unstemmed Type 1 innate lymphoid cell–immature neutrophil axis suppresses acute tissue inflammation
title_short Type 1 innate lymphoid cell–immature neutrophil axis suppresses acute tissue inflammation
title_sort type 1 innate lymphoid cell immature neutrophil axis suppresses acute tissue inflammation
url https://doi.org/10.1038/s41467-025-61504-8
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