Polyphyllin I alleviates neuroinflammation after cerebral ischemia–reperfusion injury via facilitating autophagy-mediated M2 microglial polarization

Microglial activation and polarization play a central role in poststroke inflammation and neuronal damage. Modulating microglial polarization from pro-inflammatory to anti-inflammatory phenotype is a promising therapeutic strategy for the treatment of cerebral ischemia. Polyphyllin I (PPI), a steroi...

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Veröffentlicht in:	Molecular medicine (Cambridge, Mass.) Jg. 30; H. 1; S. 59 - 18
Hauptverfasser:	Kang, Chunyang, Sang, Qiuling, Liu, Dingxi, Wang, Libo, Li, Jia, Liu, Xiaoyang
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	London BioMed Central 14.05.2024 Springer Nature B.V BMC
Schlagworte:	Animals Apoptosis Autophagy Autophagy - drug effects Biomedical and Life Sciences Biomedicine Brain Brain Ischemia - drug therapy Brain Ischemia - metabolism Cancer Carotid arteries Cell Polarity - drug effects Cerebral ischemia Cytokines Diosgenin - analogs & derivatives Diosgenin - pharmacology Diosgenin - therapeutic use Disease Models, Animal Infarction, Middle Cerebral Artery - drug therapy Inflammation Ischemia Male Mice Mice, Inbred C57BL Microglia - drug effects Microglia - metabolism Microglial polarization Molecular Medicine Neuroinflammatory Diseases - drug therapy Neuroinflammatory Diseases - etiology Neuroinflammatory Diseases - metabolism NLRP3 inflammasome Polyphyllin I (PPI) Reperfusion Injury - drug therapy Reperfusion Injury - etiology Reperfusion Injury - metabolism Research Article Signal Transduction - drug effects Stroke Surgery Tissues TOR Serine-Threonine Kinases - metabolism Veins & arteries United States > US China Japan Cerebral ischemia NLRP3 inflammasome Microglial polarization Polyphyllin I (PPI) Autophagy
ISSN:	1528-3658, 1076-1551, 1528-3658
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Abstract	Microglial activation and polarization play a central role in poststroke inflammation and neuronal damage. Modulating microglial polarization from pro-inflammatory to anti-inflammatory phenotype is a promising therapeutic strategy for the treatment of cerebral ischemia. Polyphyllin I (PPI), a steroidal saponin, shows multiple bioactivities in various diseases, but the potential function of PPI in cerebral ischemia is not elucidated yet. In our study, the influence of PPI on cerebral ischemia–reperfusion injury was evaluated. Mouse middle cerebral artery occlusion (MCAO) model and oxygen–glucose deprivation and reoxygenation (OGD/R) model were constructed to mimic cerebral ischemia–reperfusion injury in vivo and in vitro. TTC staining, TUNEL staining, RT-qPCR, ELISA, flow cytometry, western blot, immunofluorescence, hanging wire test, rotarod test and foot-fault test, open-field test and Morris water maze test were performed in our study. We found that PPI alleviated cerebral ischemia–reperfusion injury and neuroinflammation, and improved functional recovery of mice after MCAO. PPI modulated microglial polarization towards anti-inflammatory M2 phenotype in MCAO mice in vivo and post OGD/R in vitro. Besides, PPI promoted autophagy via suppressing Akt/mTOR signaling in microglia, while inhibition of autophagy abrogated the effect of PPI on M2 microglial polarization after OGD/R. Furthermore, PPI facilitated autophagy-mediated ROS clearance to inhibit NLRP3 inflammasome activation in microglia, and NLRP3 inflammasome reactivation by nigericin abolished the effect of PPI on M2 microglia polarization. In conclusion, PPI alleviated post-stroke neuroinflammation and tissue damage via increasing autophagy-mediated M2 microglial polarization. Our data suggested that PPI had potential for ischemic stroke treatment.
AbstractList	Microglial activation and polarization play a central role in poststroke inflammation and neuronal damage. Modulating microglial polarization from pro-inflammatory to anti-inflammatory phenotype is a promising therapeutic strategy for the treatment of cerebral ischemia. Polyphyllin I (PPI), a steroidal saponin, shows multiple bioactivities in various diseases, but the potential function of PPI in cerebral ischemia is not elucidated yet. In our study, the influence of PPI on cerebral ischemia–reperfusion injury was evaluated. Mouse middle cerebral artery occlusion (MCAO) model and oxygen–glucose deprivation and reoxygenation (OGD/R) model were constructed to mimic cerebral ischemia–reperfusion injury in vivo and in vitro. TTC staining, TUNEL staining, RT-qPCR, ELISA, flow cytometry, western blot, immunofluorescence, hanging wire test, rotarod test and foot-fault test, open-field test and Morris water maze test were performed in our study. We found that PPI alleviated cerebral ischemia–reperfusion injury and neuroinflammation, and improved functional recovery of mice after MCAO. PPI modulated microglial polarization towards anti-inflammatory M2 phenotype in MCAO mice in vivo and post OGD/R in vitro. Besides, PPI promoted autophagy via suppressing Akt/mTOR signaling in microglia, while inhibition of autophagy abrogated the effect of PPI on M2 microglial polarization after OGD/R. Furthermore, PPI facilitated autophagy-mediated ROS clearance to inhibit NLRP3 inflammasome activation in microglia, and NLRP3 inflammasome reactivation by nigericin abolished the effect of PPI on M2 microglia polarization. In conclusion, PPI alleviated post-stroke neuroinflammation and tissue damage via increasing autophagy-mediated M2 microglial polarization. Our data suggested that PPI had potential for ischemic stroke treatment. Microglial activation and polarization play a central role in poststroke inflammation and neuronal damage. Modulating microglial polarization from pro-inflammatory to anti-inflammatory phenotype is a promising therapeutic strategy for the treatment of cerebral ischemia. Polyphyllin I (PPI), a steroidal saponin, shows multiple bioactivities in various diseases, but the potential function of PPI in cerebral ischemia is not elucidated yet. In our study, the influence of PPI on cerebral ischemia-reperfusion injury was evaluated. Mouse middle cerebral artery occlusion (MCAO) model and oxygen-glucose deprivation and reoxygenation (OGD/R) model were constructed to mimic cerebral ischemia-reperfusion injury in vivo and in vitro. TTC staining, TUNEL staining, RT-qPCR, ELISA, flow cytometry, western blot, immunofluorescence, hanging wire test, rotarod test and foot-fault test, open-field test and Morris water maze test were performed in our study. We found that PPI alleviated cerebral ischemia-reperfusion injury and neuroinflammation, and improved functional recovery of mice after MCAO. PPI modulated microglial polarization towards anti-inflammatory M2 phenotype in MCAO mice in vivo and post OGD/R in vitro. Besides, PPI promoted autophagy via suppressing Akt/mTOR signaling in microglia, while inhibition of autophagy abrogated the effect of PPI on M2 microglial polarization after OGD/R. Furthermore, PPI facilitated autophagy-mediated ROS clearance to inhibit NLRP3 inflammasome activation in microglia, and NLRP3 inflammasome reactivation by nigericin abolished the effect of PPI on M2 microglia polarization. In conclusion, PPI alleviated post-stroke neuroinflammation and tissue damage via increasing autophagy-mediated M2 microglial polarization. Our data suggested that PPI had potential for ischemic stroke treatment.Microglial activation and polarization play a central role in poststroke inflammation and neuronal damage. Modulating microglial polarization from pro-inflammatory to anti-inflammatory phenotype is a promising therapeutic strategy for the treatment of cerebral ischemia. Polyphyllin I (PPI), a steroidal saponin, shows multiple bioactivities in various diseases, but the potential function of PPI in cerebral ischemia is not elucidated yet. In our study, the influence of PPI on cerebral ischemia-reperfusion injury was evaluated. Mouse middle cerebral artery occlusion (MCAO) model and oxygen-glucose deprivation and reoxygenation (OGD/R) model were constructed to mimic cerebral ischemia-reperfusion injury in vivo and in vitro. TTC staining, TUNEL staining, RT-qPCR, ELISA, flow cytometry, western blot, immunofluorescence, hanging wire test, rotarod test and foot-fault test, open-field test and Morris water maze test were performed in our study. We found that PPI alleviated cerebral ischemia-reperfusion injury and neuroinflammation, and improved functional recovery of mice after MCAO. PPI modulated microglial polarization towards anti-inflammatory M2 phenotype in MCAO mice in vivo and post OGD/R in vitro. Besides, PPI promoted autophagy via suppressing Akt/mTOR signaling in microglia, while inhibition of autophagy abrogated the effect of PPI on M2 microglial polarization after OGD/R. Furthermore, PPI facilitated autophagy-mediated ROS clearance to inhibit NLRP3 inflammasome activation in microglia, and NLRP3 inflammasome reactivation by nigericin abolished the effect of PPI on M2 microglia polarization. In conclusion, PPI alleviated post-stroke neuroinflammation and tissue damage via increasing autophagy-mediated M2 microglial polarization. Our data suggested that PPI had potential for ischemic stroke treatment. Abstract Microglial activation and polarization play a central role in poststroke inflammation and neuronal damage. Modulating microglial polarization from pro-inflammatory to anti-inflammatory phenotype is a promising therapeutic strategy for the treatment of cerebral ischemia. Polyphyllin I (PPI), a steroidal saponin, shows multiple bioactivities in various diseases, but the potential function of PPI in cerebral ischemia is not elucidated yet. In our study, the influence of PPI on cerebral ischemia–reperfusion injury was evaluated. Mouse middle cerebral artery occlusion (MCAO) model and oxygen–glucose deprivation and reoxygenation (OGD/R) model were constructed to mimic cerebral ischemia–reperfusion injury in vivo and in vitro. TTC staining, TUNEL staining, RT-qPCR, ELISA, flow cytometry, western blot, immunofluorescence, hanging wire test, rotarod test and foot-fault test, open-field test and Morris water maze test were performed in our study. We found that PPI alleviated cerebral ischemia–reperfusion injury and neuroinflammation, and improved functional recovery of mice after MCAO. PPI modulated microglial polarization towards anti-inflammatory M2 phenotype in MCAO mice in vivo and post OGD/R in vitro. Besides, PPI promoted autophagy via suppressing Akt/mTOR signaling in microglia, while inhibition of autophagy abrogated the effect of PPI on M2 microglial polarization after OGD/R. Furthermore, PPI facilitated autophagy-mediated ROS clearance to inhibit NLRP3 inflammasome activation in microglia, and NLRP3 inflammasome reactivation by nigericin abolished the effect of PPI on M2 microglia polarization. In conclusion, PPI alleviated post-stroke neuroinflammation and tissue damage via increasing autophagy-mediated M2 microglial polarization. Our data suggested that PPI had potential for ischemic stroke treatment.
ArticleNumber	59
Author	Liu, Dingxi Kang, Chunyang Liu, Xiaoyang Wang, Libo Li, Jia Sang, Qiuling
Author_xml	– sequence: 1 givenname: Chunyang surname: Kang fullname: Kang, Chunyang organization: Department of Neurology, China-Japan Union Hospital of Jilin University – sequence: 2 givenname: Qiuling surname: Sang fullname: Sang, Qiuling organization: Department of Neuroelectrophysiology, China-Japan Union Hospital of Jilin University – sequence: 3 givenname: Dingxi surname: Liu fullname: Liu, Dingxi organization: Department of Clinical Medicine, Zunyi Medical University – sequence: 4 givenname: Libo surname: Wang fullname: Wang, Libo organization: Department of Neurology, China-Japan Union Hospital of Jilin University – sequence: 5 givenname: Jia surname: Li fullname: Li, Jia email: lijia33233@jlu.edu.cn organization: Department of Neurology, China-Japan Union Hospital of Jilin University – sequence: 6 givenname: Xiaoyang orcidid: 0009-0005-6184-4869 surname: Liu fullname: Liu, Xiaoyang email: liuxy48@jlu.edu.cn organization: Department of Neurology, China-Japan Union Hospital of Jilin University
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Keywords	Cerebral ischemia NLRP3 inflammasome Microglial polarization Polyphyllin I (PPI) Autophagy
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SubjectTerms	Animals Apoptosis Autophagy Autophagy - drug effects Biomedical and Life Sciences Biomedicine Brain Brain Ischemia - drug therapy Brain Ischemia - metabolism Cancer Carotid arteries Cell Polarity - drug effects Cerebral ischemia Cytokines Diosgenin - analogs & derivatives Diosgenin - pharmacology Diosgenin - therapeutic use Disease Models, Animal Infarction, Middle Cerebral Artery - drug therapy Inflammation Ischemia Male Mice Mice, Inbred C57BL Microglia - drug effects Microglia - metabolism Microglial polarization Molecular Medicine Neuroinflammatory Diseases - drug therapy Neuroinflammatory Diseases - etiology Neuroinflammatory Diseases - metabolism NLRP3 inflammasome Polyphyllin I (PPI) Reperfusion Injury - drug therapy Reperfusion Injury - etiology Reperfusion Injury - metabolism Research Article Signal Transduction - drug effects Stroke Surgery Tissues TOR Serine-Threonine Kinases - metabolism Veins & arteries
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Title	Polyphyllin I alleviates neuroinflammation after cerebral ischemia–reperfusion injury via facilitating autophagy-mediated M2 microglial polarization
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