Semaglultide targets Spp1+ microglia/macrophage to attenuate neuroinflammation following perioperative stroke

Abstract Peripheral surgery evokes neuroimmune activation in the central nervous system and modulates immune cell polarization in the ischemic brain. However, the phenotypic change of microglia and myeloid cells within post-surgical ischemic brain tissue remain poorly defined. Using an integrated ap...

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Main Authors: Yan Li, Qiuyue Fan, Rui Pang, Ling Cai, Jie Qi, Weijie Chen, Yueman Zhang, Chen Chen, Weifeng Yu, Peiying Li
Format: Article
Language:English
Published: BMC 2025-05-01
Series:Journal of Neuroinflammation
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Online Access:https://doi.org/10.1186/s12974-025-03465-9
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author Yan Li
Qiuyue Fan
Rui Pang
Ling Cai
Jie Qi
Weijie Chen
Yueman Zhang
Chen Chen
Weifeng Yu
Peiying Li
author_facet Yan Li
Qiuyue Fan
Rui Pang
Ling Cai
Jie Qi
Weijie Chen
Yueman Zhang
Chen Chen
Weifeng Yu
Peiying Li
author_sort Yan Li
collection DOAJ
description Abstract Peripheral surgery evokes neuroimmune activation in the central nervous system and modulates immune cell polarization in the ischemic brain. However, the phenotypic change of microglia and myeloid cells within post-surgical ischemic brain tissue remain poorly defined. Using an integrated approach that combines single-cell RNA sequencing with comprehensive biological analysis in a perioperative ischemic stroke (PIS) model, we identified a distinct Spp1-positive macrophage/microglia (Spp1+ Mac/MG) subgroup that exhibit enriched anti-inflammatory pathways with distinct lipid metabolic reprogrammed profile. Moreover, using immunofluorescence staining, we identified the expression of Glucagon-like peptide-1 receptor (GLP1R) in Spp1+F4/80+ cells and Spp1+Iba-1+ cells. Intraperitoneal administration of semaglutide, a GLP1R agonist clinically approved for the treatment of type 2 diabetes mellitus, resulted in a significant reduction of cerebral infarct volume in PIS mice compared to that in ischemic stroke (IS) mice. Meanwhile, semaglutide treatment also increased the proportion of Spp1+Edu+Iba-1+ cells 3 days after PIS. Using high-parameter flow cytometry, immunofluorescence staining and RNA sequencing, we demonstrated that semaglutide treatment significantly attenuated the expression of neuroinflammatory markers in mice following PIS. We also found that semaglutide treatment significantly ameliorated sensorimotor dysfunction up to 3 days after PIS in mice. Our current finding reveal a novel protective Spp1+Mac/MG subset after PIS and demonstrated that it can be upregulated by semaglutide. We propose that targeting Spp1+Mac/MG subsets using semaglutide could serve as a promising strategy to attenuate the exacerbated neuroinflammation in PIS.
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spelling doaj-art-cf7258b140204562a28dbb5382eda91d2025-08-20T02:00:07ZengBMCJournal of Neuroinflammation1742-20942025-05-0122112010.1186/s12974-025-03465-9Semaglultide targets Spp1+ microglia/macrophage to attenuate neuroinflammation following perioperative strokeYan Li0Qiuyue Fan1Rui Pang2Ling Cai3Jie Qi4Weijie Chen5Yueman Zhang6Chen Chen7Weifeng Yu8Peiying Li9Department of Anesthesiology, Renji Hospital, Shanghai Jiao Tong University School of MedicineDepartment of Anesthesiology, Renji Hospital, Shanghai Jiao Tong University School of MedicineDepartment of Anesthesiology, Renji Hospital, Shanghai Jiao Tong University School of MedicineDepartment of Anesthesiology, Renji Hospital, Shanghai Jiao Tong University School of MedicineDepartment of Anesthesiology, Renji Hospital, Shanghai Jiao Tong University School of MedicineDepartment of Anesthesiology, Renji Hospital, Shanghai Jiao Tong University School of MedicineDepartment of Anesthesiology, Renji Hospital, Shanghai Jiao Tong University School of MedicineDepartment of Anesthesiology, Renji Hospital, Shanghai Jiao Tong University School of MedicineDepartment of Anesthesiology, Renji Hospital, Shanghai Jiao Tong University School of MedicineDepartment of Anesthesiology, Renji Hospital, Shanghai Jiao Tong University School of MedicineAbstract Peripheral surgery evokes neuroimmune activation in the central nervous system and modulates immune cell polarization in the ischemic brain. However, the phenotypic change of microglia and myeloid cells within post-surgical ischemic brain tissue remain poorly defined. Using an integrated approach that combines single-cell RNA sequencing with comprehensive biological analysis in a perioperative ischemic stroke (PIS) model, we identified a distinct Spp1-positive macrophage/microglia (Spp1+ Mac/MG) subgroup that exhibit enriched anti-inflammatory pathways with distinct lipid metabolic reprogrammed profile. Moreover, using immunofluorescence staining, we identified the expression of Glucagon-like peptide-1 receptor (GLP1R) in Spp1+F4/80+ cells and Spp1+Iba-1+ cells. Intraperitoneal administration of semaglutide, a GLP1R agonist clinically approved for the treatment of type 2 diabetes mellitus, resulted in a significant reduction of cerebral infarct volume in PIS mice compared to that in ischemic stroke (IS) mice. Meanwhile, semaglutide treatment also increased the proportion of Spp1+Edu+Iba-1+ cells 3 days after PIS. Using high-parameter flow cytometry, immunofluorescence staining and RNA sequencing, we demonstrated that semaglutide treatment significantly attenuated the expression of neuroinflammatory markers in mice following PIS. We also found that semaglutide treatment significantly ameliorated sensorimotor dysfunction up to 3 days after PIS in mice. Our current finding reveal a novel protective Spp1+Mac/MG subset after PIS and demonstrated that it can be upregulated by semaglutide. We propose that targeting Spp1+Mac/MG subsets using semaglutide could serve as a promising strategy to attenuate the exacerbated neuroinflammation in PIS.https://doi.org/10.1186/s12974-025-03465-9Perioperative ischemic strokeSpp1+ Mac/MGSemaglutideNeuroinflammation
spellingShingle Yan Li
Qiuyue Fan
Rui Pang
Ling Cai
Jie Qi
Weijie Chen
Yueman Zhang
Chen Chen
Weifeng Yu
Peiying Li
Semaglultide targets Spp1+ microglia/macrophage to attenuate neuroinflammation following perioperative stroke
Journal of Neuroinflammation
Perioperative ischemic stroke
Spp1+ Mac/MG
Semaglutide
Neuroinflammation
title Semaglultide targets Spp1+ microglia/macrophage to attenuate neuroinflammation following perioperative stroke
title_full Semaglultide targets Spp1+ microglia/macrophage to attenuate neuroinflammation following perioperative stroke
title_fullStr Semaglultide targets Spp1+ microglia/macrophage to attenuate neuroinflammation following perioperative stroke
title_full_unstemmed Semaglultide targets Spp1+ microglia/macrophage to attenuate neuroinflammation following perioperative stroke
title_short Semaglultide targets Spp1+ microglia/macrophage to attenuate neuroinflammation following perioperative stroke
title_sort semaglultide targets spp1 microglia macrophage to attenuate neuroinflammation following perioperative stroke
topic Perioperative ischemic stroke
Spp1+ Mac/MG
Semaglutide
Neuroinflammation
url https://doi.org/10.1186/s12974-025-03465-9
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