Local sympathetic neurons promote neutrophil egress from the bone marrow at the onset of acute inflammation

Ao, Tomoka; Kikuta, Junichi; Sudo, Takao; Uchida, Yutaka; Kobayashi, Kenta; Ishii, Masaru

doi:https://doi.org/10.1093/intimm/dxaa025

Local sympathetic neurons promote neutrophil egress from the bone marrow at the onset of acute inflammation

Ao, Tomoka; Kikuta, Junichi; Sudo, Takao et al.

International immunology, 2020, 32(11), 727-736

Number of Access:867（2025-08-18 14:25 Counts）

Identifier to cite or link to this item: https://hdl.handle.net/11094/78250

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Title	Local sympathetic neurons promote neutrophil egress from the bone marrow at the onset of acute inflammation
Creator	CreatorName Ao, Tomoka
	NRID 1000060710069 1000060710069 researchmap permalink jkikuta jkikuta Scopus Author ID 36637603800 36637603800 CreatorName Kikuta, Junichi
	NRID 1000080631184 1000080631184 researchmap permalink kik kik Scopus Author ID 36497716100 36497716100 CreatorName Sudo, Takao
	CreatorName Uchida, Yutaka
	NRID 1000070315662 1000070315662 CreatorName Kobayashi, Kenta
	NRID 1000010324758 1000010324758 researchmap permalink read0076684 read0076684 Scopus Author ID 35074093500 35074093500 CreatorName Ishii, Masaru
Subject	bone marrow
	endothelium
	intravital imaging
	neutrophil egress
	sympathetic neuron
Description	This is a pre-copyedited, author-produced version of an article accepted for publication in International Immunology following peer review. The version of record Tomoka Ao, Junichi Kikuta, Takao Sudo, Yutaka Uchida, Kenta Kobayashi, Masaru Ishii, Local sympathetic neurons promote neutrophil egress from the bone marrow at the onset of acute inflammation, International Immunology, Volume 32, Issue 11, November 2020, Pages 727–736. is available online at: https://doi.org/10.1093/intimm/dxaa025.
Abstract	The sympathetic nervous system plays critical roles in the differentiation, maturation and recruitment of immune cells under homeostatic conditions, and in responses to environmental stimuli, although its role in the migratory control of immune cells during acute inflammation remains unclear. In this study, using an advanced intravital bone imaging system established in our laboratory, we demonstrated that the sympathetic nervous system locally regulates neutrophil egress from the bone marrow for mobilization to inflammatory foci. We found that sympathetic neurons were located close to blood vessels in the bone marrow cavity; moreover, upon lipopolysaccharide (LPS) administration, local sympathectomy delayed neutrophil egress from the bone marrow and increased the proportion of neutrophils that remained in place. We also showed that vascular endothelial cells produced C-X-C motif chemokine ligand 1 (CXCL1), which is responsible for neutrophil egress out of the bone marrow. Its expression was up-regulated during acute inflammation, and was suppressed by β-adrenergic receptor blockade, which was accompanied with inhibition of neutrophil egress into the systemic circulation. Furthermore, systemic β-adrenergic signaling blockade decreased the recruitment of neutrophils in the lung under conditions of acute systemic inflammation. Taken together, the results of this study first suggested a new regulatory system, wherein local sympathetic nervous activation promoted neutrophil egress by enhancing Cxcl1 expression in bone marrow endothelial cells in a β-adrenergic signaling-dependent manner, contributing to the recruitment of neutrophils at the onset of inflammation in vivo.
Publisher	The Japanese Society for Immunology
Source Title	International immunology
Volume (Issue)	32(11)
Page	727-736
Date of Issued	2020-10-20
Language	English
Handle URL	https://hdl.handle.net/11094/78250
PISSN	09538178
eISSN	14602377
Relation.isVersionOf	DOI (Publisher Version) https://doi.org/10.1093/intimm/dxaa025
Relation.isIdenticalTo	PMID 32275057
Access Rights	open access
oaire:version	Accepted Manuscript
Category	学術雑誌論文 Journal Article

Resource Type	journal article
Local Type	Journal Article
DCMI Type	Text
DCTERMS.bibliographicCitation	International immunology. 2020, 32(11), p. 727-736
DC.title	Local sympathetic neurons promote neutrophil egress from the bone marrow at the onset of acute inflammation
DC.creator	Ao, Tomoka
	Kikuta, Junichi
	Sudo, Takao
	Uchida, Yutaka
	Kobayashi, Kenta
	Ishii, Masaru
DC.publisher	The Japanese Society for Immunology
DC.language' scheme='DCTERMS.RFC1766	English
DC.type' scheme='DCTERMS.DCMIType	Text
DCTERMS.issued' scheme='DCTERMS.W3CDTF	2020-10-20
DC.identifier	https://doi.org/10.1093/intimm/dxaa025
DC.subject	bone marrow
	endothelium
	intravital imaging
	neutrophil egress
	sympathetic neuron
DC.description	This is a pre-copyedited, author-produced version of an article accepted for publication in International Immunology following peer review. The version of record Tomoka Ao, Junichi Kikuta, Takao Sudo, Yutaka Uchida, Kenta Kobayashi, Masaru Ishii, Local sympathetic neurons promote neutrophil egress from the bone marrow at the onset of acute inflammation, International Immunology, Volume 32, Issue 11, November 2020, Pages 727–736. is available online at: https://doi.org/10.1093/intimm/dxaa025.
DCTERMS.abstract	The sympathetic nervous system plays critical roles in the differentiation, maturation and recruitment of immune cells under homeostatic conditions, and in responses to environmental stimuli, although its role in the migratory control of immune cells during acute inflammation remains unclear. In this study, using an advanced intravital bone imaging system established in our laboratory, we demonstrated that the sympathetic nervous system locally regulates neutrophil egress from the bone marrow for mobilization to inflammatory foci. We found that sympathetic neurons were located close to blood vessels in the bone marrow cavity; moreover, upon lipopolysaccharide (LPS) administration, local sympathectomy delayed neutrophil egress from the bone marrow and increased the proportion of neutrophils that remained in place. We also showed that vascular endothelial cells produced C-X-C motif chemokine ligand 1 (CXCL1), which is responsible for neutrophil egress out of the bone marrow. Its expression was up-regulated during acute inflammation, and was suppressed by β-adrenergic receptor blockade, which was accompanied with inhibition of neutrophil egress into the systemic circulation. Furthermore, systemic β-adrenergic signaling blockade decreased the recruitment of neutrophils in the lung under conditions of acute systemic inflammation. Taken together, the results of this study first suggested a new regulatory system, wherein local sympathetic nervous activation promoted neutrophil egress by enhancing Cxcl1 expression in bone marrow endothelial cells in a β-adrenergic signaling-dependent manner, contributing to the recruitment of neutrophils at the onset of inflammation in vivo.
DC.format	78250
citation_title	Local sympathetic neurons promote neutrophil egress from the bone marrow at the onset of acute inflammation
citation_author	Ao, Tomoka
	Kikuta, Junichi
	Sudo, Takao
	Uchida, Yutaka
	Kobayashi, Kenta
	Ishii, Masaru
citation_publisher	The Japanese Society for Immunology
citation_language	English
citation_date	2020-10-20
citation_journal_title	International immunology
citation_volume	32
citation_issue	11
citation_firstpage	727
citation_lastpage	736
citation_doi	https://doi.org/10.1093/intimm/dxaa025
citation_pmid	32275057
citation_public_url	https://hdl.handle.net/11094/78250

Local sympathetic neurons promote neutrophil egress from the bone marrow at the onset of acute inflammation

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