Nuclear localization of platelet activating factor receptor accounts for microglial phagocytosis in ischemic stroke

Ischemic stroke (IS) is a leading cause of global morbidity and mortality. A critical strategy for improving the prognosis of IS involves mitigating neuronal loss to enhance neuroplasticity, with microglia playing a vital role in neuronal survival. The platelet activating factor receptor (PTAFR) par...

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Main Authors: Xi-Yue Zhang, Hang Xu, Xue-Wei Ren, Qin-Xin Li, Chen Hong, Ye-Fan Chen, Jin Yang, Juan Ji, Ruo-Bing Guo, Xiu-Lan Sun
Format: Article
Language:English
Published: Elsevier 2025-09-01
Series:Neurobiology of Disease
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Online Access:http://www.sciencedirect.com/science/article/pii/S0969996125002360
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author Xi-Yue Zhang
Hang Xu
Xue-Wei Ren
Qin-Xin Li
Chen Hong
Ye-Fan Chen
Jin Yang
Juan Ji
Ruo-Bing Guo
Xiu-Lan Sun
author_facet Xi-Yue Zhang
Hang Xu
Xue-Wei Ren
Qin-Xin Li
Chen Hong
Ye-Fan Chen
Jin Yang
Juan Ji
Ruo-Bing Guo
Xiu-Lan Sun
author_sort Xi-Yue Zhang
collection DOAJ
description Ischemic stroke (IS) is a leading cause of global morbidity and mortality. A critical strategy for improving the prognosis of IS involves mitigating neuronal loss to enhance neuroplasticity, with microglia playing a vital role in neuronal survival. The platelet activating factor receptor (PTAFR) participates in the pathological processes underlying IS; however, little is known about its mechanism in pathological stress. In this study, we investigated the potential role of PTAFR in regulating the microglia/macrophage phagocytosis of neurons, aiming to identify new therapeutic strategies for IS. The mRNA and protein expression levels of PTAFR were upregulated, peaking on day 5 post-ischemic stroke and gradually returning to baseline levels thereafter. PTAFR was found to mediate interactions between the microglia/macrophage and neurons in IS. Notably, the inhibition of phagocytosis of stressed-but-viable neurons following IS depends on the nuclear localization of PTAFR. Mechanistically, nuclear PTAFR recruited the transcription factor Specificity Protein 1 (SP1) to initiate the transcription of milk fat globule EGF factor 8 (MFGE8). In comparison to the membrane-impermeable antagonist Ginkgolide B, the membrane-permeable PTAFR antagonist Apafant significantly enhances neurological recovery in IS model mice. This effect is achieved by inhibiting PTAFR nuclear translocation, which reduces microglia/macrophage phagocytosis of stressed-but-viable neurons. Our findings provide insight into the mechanism of nuclear PTAFR-mediated microglia/macrophage phagocytosis and have significant implications for the selection of PTAFR antagonists in the treatment of ischemic stroke, particularly those targeting nuclear receptors.
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spelling doaj-art-ade867ad99ab4392b42e538447fbeab22025-08-20T03:13:42ZengElsevierNeurobiology of Disease1095-953X2025-09-0121310702010.1016/j.nbd.2025.107020Nuclear localization of platelet activating factor receptor accounts for microglial phagocytosis in ischemic strokeXi-Yue Zhang0Hang Xu1Xue-Wei Ren2Qin-Xin Li3Chen Hong4Ye-Fan Chen5Jin Yang6Juan Ji7Ruo-Bing Guo8Xiu-Lan Sun9Neuroprotective Drug Discovery Key Laboratory, Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, ChinaNeuroprotective Drug Discovery Key Laboratory, Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, ChinaNeuroprotective Drug Discovery Key Laboratory, Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, ChinaNeuroprotective Drug Discovery Key Laboratory, Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, ChinaNeuroprotective Drug Discovery Key Laboratory, Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, ChinaNeuroprotective Drug Discovery Key Laboratory, Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, ChinaNeuroprotective Drug Discovery Key Laboratory, Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, ChinaNeuroprotective Drug Discovery Key Laboratory, Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, ChinaDepartment of Pharmacy, General Hospital of Ningxia Medical University, Yinchuan, China; Corresponding author at: General Hospital of Ningxia Medical University, Yinchuan, Ningxia 750004, China.Neuroprotective Drug Discovery Key Laboratory, Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, China; Nanjing University of Chinese Medicine, the Affiliated Hospital of Nanjing University of Chinese Medicine, Nanjing, China; Corresponding author at: Nanjing Medical University, Nanjing, Jiangsu 211166, China.Ischemic stroke (IS) is a leading cause of global morbidity and mortality. A critical strategy for improving the prognosis of IS involves mitigating neuronal loss to enhance neuroplasticity, with microglia playing a vital role in neuronal survival. The platelet activating factor receptor (PTAFR) participates in the pathological processes underlying IS; however, little is known about its mechanism in pathological stress. In this study, we investigated the potential role of PTAFR in regulating the microglia/macrophage phagocytosis of neurons, aiming to identify new therapeutic strategies for IS. The mRNA and protein expression levels of PTAFR were upregulated, peaking on day 5 post-ischemic stroke and gradually returning to baseline levels thereafter. PTAFR was found to mediate interactions between the microglia/macrophage and neurons in IS. Notably, the inhibition of phagocytosis of stressed-but-viable neurons following IS depends on the nuclear localization of PTAFR. Mechanistically, nuclear PTAFR recruited the transcription factor Specificity Protein 1 (SP1) to initiate the transcription of milk fat globule EGF factor 8 (MFGE8). In comparison to the membrane-impermeable antagonist Ginkgolide B, the membrane-permeable PTAFR antagonist Apafant significantly enhances neurological recovery in IS model mice. This effect is achieved by inhibiting PTAFR nuclear translocation, which reduces microglia/macrophage phagocytosis of stressed-but-viable neurons. Our findings provide insight into the mechanism of nuclear PTAFR-mediated microglia/macrophage phagocytosis and have significant implications for the selection of PTAFR antagonists in the treatment of ischemic stroke, particularly those targeting nuclear receptors.http://www.sciencedirect.com/science/article/pii/S0969996125002360Nuclear PTAFRMicrogliaPhagocytosisIschemic strokeMFGE8
spellingShingle Xi-Yue Zhang
Hang Xu
Xue-Wei Ren
Qin-Xin Li
Chen Hong
Ye-Fan Chen
Jin Yang
Juan Ji
Ruo-Bing Guo
Xiu-Lan Sun
Nuclear localization of platelet activating factor receptor accounts for microglial phagocytosis in ischemic stroke
Neurobiology of Disease
Nuclear PTAFR
Microglia
Phagocytosis
Ischemic stroke
MFGE8
title Nuclear localization of platelet activating factor receptor accounts for microglial phagocytosis in ischemic stroke
title_full Nuclear localization of platelet activating factor receptor accounts for microglial phagocytosis in ischemic stroke
title_fullStr Nuclear localization of platelet activating factor receptor accounts for microglial phagocytosis in ischemic stroke
title_full_unstemmed Nuclear localization of platelet activating factor receptor accounts for microglial phagocytosis in ischemic stroke
title_short Nuclear localization of platelet activating factor receptor accounts for microglial phagocytosis in ischemic stroke
title_sort nuclear localization of platelet activating factor receptor accounts for microglial phagocytosis in ischemic stroke
topic Nuclear PTAFR
Microglia
Phagocytosis
Ischemic stroke
MFGE8
url http://www.sciencedirect.com/science/article/pii/S0969996125002360
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