Peripheral nervous system microglia-like cells regulate neuronal soma size throughout evolution

Zhisheng Wu; Yiheng Wang; Wei wei Chen; Hua Sun; Xiaoyan Chen; Xiaobo Li; Zeshuai Wang; Weizheng Liang; Shuang Yin Wang; Xuemei Luan; Yijiang Li; Shangjin Huang; Yuteng Liang; Jiaqi Zhang; Zhou Feng Chen; Guanlin Wang; Yun Gao; Yanan Liu; Jun Wang; Zhen Liu; Peng Shi; Cirong Liu; Longbao Lv; Anli Hou; Chenglin Wu; Chen Yao; Zexuan Hong; Ji Dai; Zhonghua Lu; Fan Pan; Xin Chen; Helmut Kettenmann; Ido Amit; John R. Speakman; Yun Chen; Florent Ginhoux; Rongfeng Cui; Tianwen Huang; Hanjie Li

doi:10.1016/j.cell.2025.02.007

Peripheral nervous system microglia-like cells regulate neuronal soma size throughout evolution

Zhisheng Wu, Yiheng Wang, Wei wei Chen, Hua Sun, Xiaoyan Chen, Xiaobo Li, Zeshuai Wang, Weizheng Liang, Shuang Yin Wang, Xuemei Luan, Yijiang Li, Shangjin Huang, Yuteng Liang, Jiaqi Zhang, Zhou Feng Chen, Guanlin Wang, Yun Gao, Yanan Liu, Jun Wang, Zhen LiuPeng Shi, Cirong Liu, Longbao Lv, Anli Hou, Chenglin Wu, Chen Yao, Zexuan Hong, Ji Dai, Zhonghua Lu, Fan Pan, Xin Chen, Helmut Kettenmann, Ido Amit, John R. Speakman, Yun Chen, Florent Ginhoux, Rongfeng Cui, Tianwen Huang, Hanjie Li

Résultats de recherche: Contribution à un journal › Article › Revue par des pairs

Résumé

Microglia, essential in the central nervous system (CNS), were historically considered absent from the peripheral nervous system (PNS). Here, we show a PNS-resident macrophage population that shares transcriptomic and epigenetic profiles as well as an ontogenetic trajectory with CNS microglia. This population (termed PNS microglia-like cells) enwraps the neuronal soma inside the satellite glial cell envelope, preferentially associates with larger neurons during PNS development, and is required for neuronal functions by regulating soma enlargement and axon growth. A phylogenetic survey of 24 vertebrates revealed an early origin of PNS microglia-like cells, whose presence is correlated with neuronal soma size (and body size) rather than evolutionary distance. Consistent with their requirement for soma enlargement, PNS microglia-like cells are maintained in vertebrates with large peripheral neuronal soma but absent when neurons evolve to have smaller soma. Our study thus reveals a PNS counterpart of CNS microglia that regulates neuronal soma size during both evolution and ontogeny.

langue originale	Anglais
journal	Cell
Les DOIs	https://doi.org/10.1016/j.cell.2025.02.007
état	Accepté/sous presse - 1 janv. 2025
Modification externe	Oui

Accès au document

10.1016/j.cell.2025.02.007

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Wu, Z., Wang, Y., Chen, W. W., Sun, H., Chen, X., Li, X., Wang, Z., Liang, W., Wang, S. Y., Luan, X., Li, Y., Huang, S., Liang, Y., Zhang, J., Chen, Z. F., Wang, G., Gao, Y., Liu, Y., Wang, J., ... Li, H. (Accepté/en presse). Peripheral nervous system microglia-like cells regulate neuronal soma size throughout evolution. Cell. https://doi.org/10.1016/j.cell.2025.02.007

@article{382d80098b4941dc95eb3fad92ae4d41,

title = "Peripheral nervous system microglia-like cells regulate neuronal soma size throughout evolution",

abstract = "Microglia, essential in the central nervous system (CNS), were historically considered absent from the peripheral nervous system (PNS). Here, we show a PNS-resident macrophage population that shares transcriptomic and epigenetic profiles as well as an ontogenetic trajectory with CNS microglia. This population (termed PNS microglia-like cells) enwraps the neuronal soma inside the satellite glial cell envelope, preferentially associates with larger neurons during PNS development, and is required for neuronal functions by regulating soma enlargement and axon growth. A phylogenetic survey of 24 vertebrates revealed an early origin of PNS microglia-like cells, whose presence is correlated with neuronal soma size (and body size) rather than evolutionary distance. Consistent with their requirement for soma enlargement, PNS microglia-like cells are maintained in vertebrates with large peripheral neuronal soma but absent when neurons evolve to have smaller soma. Our study thus reveals a PNS counterpart of CNS microglia that regulates neuronal soma size during both evolution and ontogeny.",

keywords = "PNS microglia, evolution, macrophage, microglia, microglia-like cell, microglial lineage, neuron development, neuronal soma size, peripheral microglia, peripheral nervous system",

author = "Zhisheng Wu and Yiheng Wang and Chen, {Wei wei} and Hua Sun and Xiaoyan Chen and Xiaobo Li and Zeshuai Wang and Weizheng Liang and Wang, {Shuang Yin} and Xuemei Luan and Yijiang Li and Shangjin Huang and Yuteng Liang and Jiaqi Zhang and Chen, {Zhou Feng} and Guanlin Wang and Yun Gao and Yanan Liu and Jun Wang and Zhen Liu and Peng Shi and Cirong Liu and Longbao Lv and Anli Hou and Chenglin Wu and Chen Yao and Zexuan Hong and Ji Dai and Zhonghua Lu and Fan Pan and Xin Chen and Helmut Kettenmann and Ido Amit and Speakman, {John R.} and Yun Chen and Florent Ginhoux and Rongfeng Cui and Tianwen Huang and Hanjie Li",

note = "Publisher Copyright: {\textcopyright} 2025 Elsevier Inc.",

year = "2025",

month = jan,

day = "1",

doi = "10.1016/j.cell.2025.02.007",

language = "English",

journal = "Cell",

issn = "0092-8674",

}

Wu, Z, Wang, Y, Chen, WW, Sun, H, Chen, X, Li, X, Wang, Z, Liang, W, Wang, SY, Luan, X, Li, Y, Huang, S, Liang, Y, Zhang, J, Chen, ZF, Wang, G, Gao, Y, Liu, Y, Wang, J, Liu, Z, Shi, P, Liu, C, Lv, L, Hou, A, Wu, C, Yao, C, Hong, Z, Dai, J, Lu, Z, Pan, F, Chen, X, Kettenmann, H, Amit, I, Speakman, JR, Chen, Y, Ginhoux, F, Cui, R, Huang, T & Li, H 2025, 'Peripheral nervous system microglia-like cells regulate neuronal soma size throughout evolution', Cell. https://doi.org/10.1016/j.cell.2025.02.007

TY - JOUR

T1 - Peripheral nervous system microglia-like cells regulate neuronal soma size throughout evolution

AU - Wu, Zhisheng

AU - Wang, Yiheng

AU - Chen, Wei wei

AU - Sun, Hua

AU - Chen, Xiaoyan

AU - Li, Xiaobo

AU - Wang, Zeshuai

AU - Liang, Weizheng

AU - Wang, Shuang Yin

AU - Luan, Xuemei

AU - Li, Yijiang

AU - Huang, Shangjin

AU - Liang, Yuteng

AU - Zhang, Jiaqi

AU - Chen, Zhou Feng

AU - Wang, Guanlin

AU - Gao, Yun

AU - Liu, Yanan

AU - Wang, Jun

AU - Liu, Zhen

AU - Shi, Peng

AU - Liu, Cirong

AU - Lv, Longbao

AU - Hou, Anli

AU - Wu, Chenglin

AU - Yao, Chen

AU - Hong, Zexuan

AU - Dai, Ji

AU - Lu, Zhonghua

AU - Pan, Fan

AU - Chen, Xin

AU - Kettenmann, Helmut

AU - Amit, Ido

AU - Speakman, John R.

AU - Chen, Yun

AU - Ginhoux, Florent

AU - Cui, Rongfeng

AU - Huang, Tianwen

AU - Li, Hanjie

PY - 2025/1/1

Y1 - 2025/1/1

N2 - Microglia, essential in the central nervous system (CNS), were historically considered absent from the peripheral nervous system (PNS). Here, we show a PNS-resident macrophage population that shares transcriptomic and epigenetic profiles as well as an ontogenetic trajectory with CNS microglia. This population (termed PNS microglia-like cells) enwraps the neuronal soma inside the satellite glial cell envelope, preferentially associates with larger neurons during PNS development, and is required for neuronal functions by regulating soma enlargement and axon growth. A phylogenetic survey of 24 vertebrates revealed an early origin of PNS microglia-like cells, whose presence is correlated with neuronal soma size (and body size) rather than evolutionary distance. Consistent with their requirement for soma enlargement, PNS microglia-like cells are maintained in vertebrates with large peripheral neuronal soma but absent when neurons evolve to have smaller soma. Our study thus reveals a PNS counterpart of CNS microglia that regulates neuronal soma size during both evolution and ontogeny.

AB - Microglia, essential in the central nervous system (CNS), were historically considered absent from the peripheral nervous system (PNS). Here, we show a PNS-resident macrophage population that shares transcriptomic and epigenetic profiles as well as an ontogenetic trajectory with CNS microglia. This population (termed PNS microglia-like cells) enwraps the neuronal soma inside the satellite glial cell envelope, preferentially associates with larger neurons during PNS development, and is required for neuronal functions by regulating soma enlargement and axon growth. A phylogenetic survey of 24 vertebrates revealed an early origin of PNS microglia-like cells, whose presence is correlated with neuronal soma size (and body size) rather than evolutionary distance. Consistent with their requirement for soma enlargement, PNS microglia-like cells are maintained in vertebrates with large peripheral neuronal soma but absent when neurons evolve to have smaller soma. Our study thus reveals a PNS counterpart of CNS microglia that regulates neuronal soma size during both evolution and ontogeny.

KW - PNS microglia

KW - evolution

KW - macrophage

KW - microglia

KW - microglia-like cell

KW - microglial lineage

KW - neuron development

KW - neuronal soma size

KW - peripheral microglia

KW - peripheral nervous system

UR - http://www.scopus.com/inward/record.url?scp=105002027458&partnerID=8YFLogxK

U2 - 10.1016/j.cell.2025.02.007

DO - 10.1016/j.cell.2025.02.007

M3 - Article

AN - SCOPUS:105002027458

SN - 0092-8674

JO - Cell

JF - Cell

ER -