St3gal5-mediated sialylation of glyco-CD177 on neutrophils restricts neuroinflammation following CNS injury

T Tingting Huang (Shanghai Key Laboratory of Atmospheric Particle Pollution and Prevention, National Observations and Research Station for Wetland Ecosystems of the Yangtze Estuary, IRDR International Center of Excellence on Risk Interconnectivity and Governance on Weather, Department of Environmental Science & Engineering) W Wanqing Xie Y Yunlu Guo (Department of Anesthesiology, Clinical Research Center, Renji Hospital, Shanghai Jiao Tong University School of Medicine) Y Yan Li J Jiemin Yin (Department of Anesthesiology, Clinical Research Center, Renji Hospital, Shanghai Jiao Tong University School of Medicine) X Xia Jin (Department of Anesthesiology, Clinical Research Center, Renji Hospital, Shanghai Jiao Tong University School of Medicine) Y Yezhi Ma (Department of Anesthesiology, Clinical Research Center, Renji Hospital, Shanghai Jiao Tong University School of Medicine) Y Yueman Zhang (Department of Anesthesiology, Clinical Research Center, Renji Hospital, Shanghai Jiao Tong University School of Medicine) D Dan Huang (School of Chemistry and Chemical Engineering, State Key Laboratory of Luminescent Materials and Devices) C Caiyang Chen (Department of Anesthesiology, Clinical Research Center, Renji Hospital, Shanghai Jiao Tong University School of Medicine) X Xin Wang Z Ziyu Zhu (Department of Anesthesiology, Clinical Research Center, Renji Hospital, Shanghai Jiao Tong University School of Medicine) Y Yu Gan (Shanghai Cancer Institute, Renji Hospital, Shanghai Jiao Tong University School of Medicine) A Arthur Liesz (Institute for Stroke and Dementia Research, University Hospital, Ludwig-Maximilians-Universität München) W Weifeng Yu (Department of Anesthesiology, Clinical Research Center, Renji Hospital, Shanghai Jiao Tong University School of Medicine) J Junying Yuan P Peiying Li (Department of Anesthesiology, Clinical Research Center, Renji Hospital, Shanghai Jiao Tong University School of Medicine)

Abstract

Neutrophils are the most abundant circulating leukocyte population that play critical roles in neuroinflammation following central nervous system (CNS) injury. CD177, a glycoprotein on neutrophils, is emerging as an important immune regulator which can fundamentally affect multiple human inflammatory diseases. However, the role and regulatory mechanism of CD177 glycobiology of neutrophils in neuroinflammation remain elusive. Here, we show that CD177 + neutrophils expand significantly and infiltrate the injured brain following CNS injury both in the human and mouse. Using single-cell RNA sequencing and genetic approaches, we find CD177 + neutrophils as an anti-inflammatory subset that is critical for modulating neuroinflammation after CNS injury. We further identify St3gal5, a sialyltransferase (ST), that can mediate the sialylation and cell surface presentation of glyco-CD177 on neutrophils. Glycoproteomics reveal downregulated sialylation levels in St3gal5-deficient neutrophils. Neutrophil-specific depletion of St3gal5 prevents the cell surface presentation of CD177 on brain-infiltrated neutrophils and exacerbates neuroinflammation. Administration of the FDA-approved anticonvulsant valproic acid (VPA), an St3gal5 upregulator, promotes the glycosylation of neutrophils and attenuates neuroinflammation following CNS injury. Our study reveals a glycoimmuno-regulatory effect of neutrophils and suggests VPA as a neutrophil glycobiology targeting approach to combat neuroinflammation following CNS injury.

Article Details

Volume / Issue Vol. 122, Issue 16
Published April 22, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (17)

T

Tingting Huang

Shanghai Key Laboratory of Atmospheric Particle Pollution and Prevention, National Observations and Research Station for Wetland Ecosystems of the Yangtze Estuary, IRDR International Center of Excellence on Risk Interconnectivity and Governance on Weather, Department of Environmental Science & Engineering

W

Wanqing Xie

Y

Yunlu Guo

Department of Anesthesiology, Clinical Research Center, Renji Hospital, Shanghai Jiao Tong University School of Medicine

Y

Yan Li

J

Jiemin Yin

Department of Anesthesiology, Clinical Research Center, Renji Hospital, Shanghai Jiao Tong University School of Medicine

X

Xia Jin

Department of Anesthesiology, Clinical Research Center, Renji Hospital, Shanghai Jiao Tong University School of Medicine

Y

Yezhi Ma

Department of Anesthesiology, Clinical Research Center, Renji Hospital, Shanghai Jiao Tong University School of Medicine

Y

Yueman Zhang

Department of Anesthesiology, Clinical Research Center, Renji Hospital, Shanghai Jiao Tong University School of Medicine

D

Dan Huang

School of Chemistry and Chemical Engineering, State Key Laboratory of Luminescent Materials and Devices

C

Caiyang Chen

Department of Anesthesiology, Clinical Research Center, Renji Hospital, Shanghai Jiao Tong University School of Medicine

X

Xin Wang

Z

Ziyu Zhu

Department of Anesthesiology, Clinical Research Center, Renji Hospital, Shanghai Jiao Tong University School of Medicine

Y

Yu Gan

Shanghai Cancer Institute, Renji Hospital, Shanghai Jiao Tong University School of Medicine

A

Arthur Liesz

Institute for Stroke and Dementia Research, University Hospital, Ludwig-Maximilians-Universität München

W

Weifeng Yu

Department of Anesthesiology, Clinical Research Center, Renji Hospital, Shanghai Jiao Tong University School of Medicine

J

Junying Yuan

P

Peiying Li

Department of Anesthesiology, Clinical Research Center, Renji Hospital, Shanghai Jiao Tong University School of Medicine