Cell Reports (Mar 2023)
The early neutrophil-committed progenitors aberrantly differentiate into immunoregulatory monocytes during emergency myelopoiesis
- Naoki Ikeda,
- Hiroaki Kubota,
- Risa Suzuki,
- Mitsuki Morita,
- Ayana Yoshimura,
- Yuya Osada,
- Keigo Kishida,
- Daiki Kitamura,
- Ayaka Iwata,
- Satoshi Yotsumoto,
- Daisuke Kurotaki,
- Koutarou Nishimura,
- Akira Nishiyama,
- Tomohiko Tamura,
- Takashi Kamatani,
- Tatsuhiko Tsunoda,
- Miyako Murakawa,
- Yasuhiro Asahina,
- Yoshihiro Hayashi,
- Hironori Harada,
- Yuka Harada,
- Asumi Yokota,
- Hideyo Hirai,
- Takao Seki,
- Makoto Kuwahara,
- Masakatsu Yamashita,
- Shigeyuki Shichino,
- Masato Tanaka,
- Kenichi Asano
Affiliations
- Naoki Ikeda
- Laboratory of Immune Regulation, School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Tokyo 192-0392, Japan
- Hiroaki Kubota
- Laboratory of Immune Regulation, School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Tokyo 192-0392, Japan
- Risa Suzuki
- Laboratory of Immune Regulation, School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Tokyo 192-0392, Japan
- Mitsuki Morita
- Laboratory of Immune Regulation, School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Tokyo 192-0392, Japan
- Ayana Yoshimura
- Laboratory of Immune Regulation, School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Tokyo 192-0392, Japan
- Yuya Osada
- Laboratory of Immune Regulation, School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Tokyo 192-0392, Japan
- Keigo Kishida
- Laboratory of Immune Regulation, School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Tokyo 192-0392, Japan
- Daiki Kitamura
- Laboratory of Immune Regulation, School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Tokyo 192-0392, Japan
- Ayaka Iwata
- Laboratory of Immune Regulation, School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Tokyo 192-0392, Japan
- Satoshi Yotsumoto
- Laboratory of Immune Regulation, School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Tokyo 192-0392, Japan
- Daisuke Kurotaki
- Department of Immunology, Yokohama City University Graduate School of Medicine, Kanagawa 236-0004, Japan; Laboratory of Chromatin Organization in Immune Cell Development, International Research Center for Medical Sciences, Kumamoto University, Kumamoto 860-8555, Japan
- Koutarou Nishimura
- Department of Immunology, Yokohama City University Graduate School of Medicine, Kanagawa 236-0004, Japan
- Akira Nishiyama
- Department of Immunology, Yokohama City University Graduate School of Medicine, Kanagawa 236-0004, Japan
- Tomohiko Tamura
- Department of Immunology, Yokohama City University Graduate School of Medicine, Kanagawa 236-0004, Japan
- Takashi Kamatani
- Laboratory for Medical Science Mathematics, Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo 113-0032, Japan; Division of Precision Cancer Medicine, Tokyo Medical and Dental University, Tokyo 113-8519, Japan; Division of Pulmonary Medicine, Department of Medicine, Keio University School of Medicine, Tokyo 160-8582, Japan; Department of AI Technology Development, M&D Data Science Center, Tokyo Medical and Dental University, Tokyo 101-0062, Japan
- Tatsuhiko Tsunoda
- Laboratory for Medical Science Mathematics, Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo 113-0032, Japan; Laboratory for Medical Science Mathematics, RIKEN Center for Integrative Medical Sciences, Kanagawa 230-0045, Japan
- Miyako Murakawa
- Department of Gastroenterology and Hepatology, Tokyo Medical and Dental University, Tokyo 113-8519, Japan
- Yasuhiro Asahina
- Department of Gastroenterology and Hepatology, Tokyo Medical and Dental University, Tokyo 113-8519, Japan; Department of Liver Disease Control, Tokyo Medical and Dental University, Tokyo 113-8519, Japan
- Yoshihiro Hayashi
- Laoratory of Oncology, School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Tokyo 192-0392, Japan
- Hironori Harada
- Laoratory of Oncology, School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Tokyo 192-0392, Japan
- Yuka Harada
- Department of Clinical Laboratory, Tokyo Metropolitan Cancer and Infectious Diseases Center, Komagome Hospital, Tokyo 113-8677, Japan
- Asumi Yokota
- Laboratory of Stem Cells Regulation, School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Tokyo 192-0392, Japan
- Hideyo Hirai
- Laboratory of Stem Cells Regulation, School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Tokyo 192-0392, Japan
- Takao Seki
- Department of Biochemistry, Toho University School of Medicine, Tokyo 143-8540, Japan
- Makoto Kuwahara
- Department of Immunology, Graduate School of Medicine, Ehime University, Ehime 791-0295, Japan
- Masakatsu Yamashita
- Department of Immunology, Graduate School of Medicine, Ehime University, Ehime 791-0295, Japan
- Shigeyuki Shichino
- Division of Molecular Regulation of Inflammatory and Immune Diseases, Research Institute for Biomedical Sciences, Tokyo University of Science, Chiba 278-0022, Japan
- Masato Tanaka
- Laboratory of Immune Regulation, School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Tokyo 192-0392, Japan; Corresponding author
- Kenichi Asano
- Laboratory of Immune Regulation, School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Tokyo 192-0392, Japan; Corresponding author
- Journal volume & issue
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Vol. 42,
no. 3
p. 112165
Abstract
Summary: Inflammatory stimuli cause a state of emergency myelopoiesis leading to neutrophil-like monocyte expansion. However, their function, the committed precursors, or growth factors remain elusive. In this study we find that Ym1+Ly6Chi monocytes, an immunoregulatory entity of neutrophil-like monocytes, arise from progenitors of neutrophil 1 (proNeu1). Granulocyte-colony stimulating factor (G-CSF) favors the production of neutrophil-like monocytes through previously unknown CD81+CX3CR1lo monocyte precursors. GFI1 promotes the differentiation of proNeu2 from proNeu1 at the cost of producing neutrophil-like monocytes. The human counterpart of neutrophil-like monocytes that also expands in response to G-CSF is found in CD14+CD16− monocyte fraction. The human neutrophil-like monocytes are discriminated from CD14+CD16− classical monocytes by CXCR1 expression and the capacity to suppress T cell proliferation. Collectively, our findings suggest that the aberrant expansion of neutrophil-like monocytes under inflammatory conditions is a process conserved between mouse and human, which may be beneficial for the resolution of inflammation.