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Abstract
Efferocytosis, or phagocytic clearance of dead/dying cells by brain-resident microglia and/or infiltrating macrophages, is instrumental for inflammation resolution and restoration of brain homeostasis after stroke. Here, we identify the signal transducer and activator of transcription 6/arginase1 (STAT6/Arg1) signaling axis as a potentially novel mechanism that orchestrates microglia/macrophage responses in the ischemic brain. Activation of STAT6 was observed in microglia/macrophages in the ischemic territory in a mouse model of stroke and in stroke patients. STAT6 deficiency resulted in reduced clearance of dead/dying neurons, increased inflammatory gene signature in microglia/macrophages, and enlarged infarct volume early after experimental stroke. All of these pathological changes culminated in an increased brain tissue loss and exacerbated long-term functional deficits. Combined in vivo analyses using BM chimeras and in vitro experiments using microglia/macrophage-neuron cocultures confirmed that STAT6 activation in both microglia and macrophages was essential for neuroprotection. Adoptive transfer of WT macrophages into STAT6-KO mice reduced accumulation of dead neurons in the ischemic territory and ameliorated brain infarction. Furthermore, decreased expression of Arg1 in STAT6–/– microglia/macrophages was responsible for impairments in efferocytosis and loss of antiinflammatory modality. Our study suggests that efferocytosis via STAT6/Arg1 modulates microglia/macrophage phenotype, accelerates inflammation resolution, and improves stroke outcomes.
Authors
Wei Cai, Xuejiao Dai, Jie Chen, Jingyan Zhao, Mingyue Xu, Lili Zhang, Boyu Yang, Wenting Zhang, Marcelo Rocha, Toshimasa Nakao, Julia Kofler, Yejie Shi, R. Anne Stetler, Xiaoming Hu, Jun Chen
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Inhibition of STAT6 Activation by AS1517499 Inhibits Expression and Activity of PPARγ in Macrophages to Resolve Acute Inflammation in Mice
Y Lee, K Kim, M Kim, Y Ahn, J Kang |
Biomolecules | 2022 |
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Interaction between macrophages and ferroptosis
Y Yang, Y Wang, L Guo, W Gao, T Tang, M Yan |
Cell Death and Disease | 2022 |
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IL-33/ST2 Axis Protects Against Traumatic Brain Injury Through Enhancing the Function of Regulatory T Cells
D Xie, W Miao, F Xu, C Yuan, S Li, C Wang, A Junagade, X Hu |
Frontiers in immunology | 2022 |
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Macrophage-based delivery of interleukin-13 improves functional and histopathological outcomes following spinal cord injury
J Broeckhoven, C Erens, D Sommer, E Scheijen, S Sanchez, P Vidal, D Dooley, E Breedam, A Quarta, P Ponsaerts, S Hendrix, S Lemmens |
Journal of Neuroinflammation | 2022 |
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Interleukin 13 promotes long-term recovery after ischemic stroke by inhibiting the activation of STAT3
D Chen, J Li, Y Huang, P Wei, W Miao, Y Yang, Y Gao |
Journal of Neuroinflammation | 2022 |
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Neuroinflammation, Stem Cells, and Stroke
S Anthony, D Cabantan, M Monsour, C Borlongan |
Stroke; a journal of cerebral circulation | 2022 |
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Mesenchymal Stem Cells Improve Cognitive Impairment and Reduce Aβ Deposition via Promoting AQP4 Polarity and Relieving Neuroinflammation in Rats With Chronic Hypertension-Induced Cerebral Small-Vessel Disease
Liu XL, Ouyang FB, Hu LT, Sun P, Yang J, Sun YJ, Liao MS, Lan LF, Pei Z, Fan YH |
Frontiers in aging neuroscience | 2022 |
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Soluble SIRP-Alpha Promotes Murine Acute Lung Injury Through Suppressing Macrophage Phagocytosis
Shen Q, Zhao L, Pan L, Li D, Chen G, Chen Z, Jiang Z |
Frontiers in immunology | 2022 |
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Phagocytic microglia and macrophages in brain injury and repair
Yu F, Wang Y, Stetler AR, Leak RK, Hu X, Chen J |
CNS Neuroscience & Therapeutics | 2022 |
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β-Adrenoceptor Blockade Moderates Neuroinflammation in Male and Female EAE Rats and Abrogates Sexual Dimorphisms in the Major Neuroinflammatory Pathways by Being More Efficient in Males.
Pilipović I, Stojić-Vukanić Z, Prijić I, Jasnić N, Djordjević J, Leposavić G |
Cellular and Molecular Neurobiology | 2022 |
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The lymphocyte-to-monocyte ratio predicts intracranial atherosclerotic stenosis plaque instability
Wu XB, Huang LX, Huang ZR, Lu LM, Luo B, Cai WQ, Liu AM, Wang SW |
Frontiers in immunology | 2022 |
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Suppression of osteoclast multinucleation via a posttranscriptional regulation–based spatiotemporally selective delivery system
Wang Q, Wang H, Yan H, Tian H, Wang Y, Yu W, Dai Z, Chen P, Liu Z, Tang R, Jiang C, Fan S, Liu X, Lin X |
Science Advances | 2022 |
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The role of microglial/macrophagic salt-inducible kinase 3 on normal and excessive phagocytosis after transient focal cerebral ischemia
Wang K, Wang C, Chen D, Huang Y, Li J, Wei P, Shi Z, Zhang Y, Gao Y |
Cellular and Molecular Life Sciences | 2022 |
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Bioinformatics analysis to identify potential biomarkers and therapeutic targets for ST-segment–elevation myocardial infarction-related ischemic stroke
Feng S, Li R, Zhou Q, Qu F, Hu W, Liu X |
Frontiers in neurology | 2022 |
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Microglia-mediated neuroinflammation and neuroplasticity after stroke
Wang Y, Leak RK, Cao G |
Frontiers in cellular neuroscience | 2022 |
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Microglial phagocytosis and regulatory mechanisms after stroke
Chen W, Zhang Y, Zhai X, Xie L, Guo Y, Chen C, Li Y, Wang F, Zhu Z, Zheng L, Wan J, Li P |
Journal of Cerebral Blood Flow & Metabolism | 2022 |
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Brain‐associated innate leukocytes display diverse inflammatory states following experimental stroke
Wanrooy BJ, Wen SW, Shim R, Wilson JL, Prame Kumar K, Wong CH |
Immunology and Cell Biology | 2022 |
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Roles of peripheral immune cells in the recovery of neurological function after ischemic stroke
Zhang Z, Lv M, Zhou X, Cui Y |
Frontiers in cellular neuroscience | 2022 |
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Depletion of Arg1-Positive Microglia/Macrophages Exacerbates Cerebral Ischemic Damage by Facilitating the Inflammatory Response
Li T, Zhao J, Gao H |
International journal of molecular sciences | 2022 |
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Interleukin-33 regulates the functional state of microglia
Xiong T, Wang X, Zha Y, Wang Y |
Frontiers in cellular neuroscience | 2022 |
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Ferroptosis-related differentially expressed genes serve as new biomarkers in ischemic stroke and identification of therapeutic drugs
Zhang Y, Zhang Y, Yao R, He X, Zhao L, Zuo X, Lu B, Pang Z |
Frontiers in Nutrition | 2022 |
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Microglia autophagy in ischemic stroke: A double-edged sword
Peng L, Hu G, Yao Q, Wu J, He Z, Law BY, Hu G, Zhou X, Du J, Wu A, Yu L |
Frontiers in immunology | 2022 |
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Controlling Macrophage Polarization to Modulate Inflammatory Cues Using Immune-Switch Nanoparticles.
Almeida AF, Miranda MS, Vinhas A, Gonçalves AI, Gomes ME, Rodrigues MT |
International journal of molecular sciences | 2022 |
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Efferocytosis Mediated Modulation of Injury after Neonatal Brain Hypoxia-Ischemia
JK Mike, DM Ferriero |
Cells | 2021 |
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Neural Stem Cells for Early Ischemic Stroke
MH Hamblin, JP Lee |
International journal of molecular sciences | 2021 |
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Treadmill Exercise Attenuates Cerebral Ischemia–Reperfusion Injury by Promoting Activation of M2 Microglia via Upregulation of Interleukin-4
J Lu, J Wang, L Yu, R Cui, Y Zhang, H Ding, G Yan |
Frontiers in Cardiovascular Medicine | 2021 |
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Neuronal Loss after Stroke Due to Microglial Phagocytosis of Stressed Neurons
GC Brown |
International journal of molecular sciences | 2021 |
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Myeloid Arginase 1 Insufficiency Exacerbates Amyloid-β Associated Neurodegenerative Pathways and Glial Signatures in a Mouse Model of Alzheimer’s Disease: A Targeted Transcriptome Analysis
C Ma, JB Hunt, A Kovalenko, H Liang, ML Selenica, MB Orr, B Zhang, JC Gensel, DJ Feola, MN Gordon, D Morgan, PC Bickford, DC Lee |
Frontiers in immunology | 2021 |
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Central nervous system diseases related to pathological microglial phagocytosis
K Wang, J Li, Y Zhang, Y Huang, D Chen, Z Shi, AD Smith, W Li, Y Gao |
CNS Neuroscience & Therapeutics | 2021 |
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Microglia as the Critical Regulators of Neuroprotection and Functional Recovery in Cerebral Ischemia
BP Gaire |
Cellular and Molecular Neurobiology | 2021 |
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Efferocytosis in the Central Nervous System
J Zhao, W Zhang, T Wu, H Wang, J Mao, J Liu, Z Zhou, X Lin, H Yan, Q Wang |
Frontiers in Cell and Developmental Biology | 2021 |
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Microglial lnc-U90926 facilitates neutrophil infiltration in ischemic stroke via MDH2/CXCL2 axis
J Chen, J Jin, , H Yu, X Zhu, L Yu, Y Chen, P Liu, X Dong, X Cao, Y Gu, X Bao, S Xia, Y Xu |
Molecular Therapy | 2021 |
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Emerging Role of LncRNAs in Ischemic Stroke—Novel Insights into the Regulation of Inflammation
Y Pan, Q Jiao, W Wei, T Zheng, X Yang, W Xin |
Journal of inflammation research | 2021 |
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Microglial/Macrophage polarization and function in brain injury and repair after stroke
J Lyu, D Xie, TN Bhatia, RK Leak, X Hu, X Jiang |
CNS Neuroscience & Therapeutics | 2021 |
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Arginase 1 Insufficiency Precipitates Amyloid-β Deposition and Hastens Behavioral Impairment in a Mouse Model of Amyloidosis
C Ma, JB Hunt, ML Selenica, A Sanneh, LA Sandusky-Beltran, M Watler, R Daas, A Kovalenko, H Liang, D Placides, C Cao, X Lin, MB Orr, B Zhang, JC Gensel, DJ Feola, MN Gordon, D Morgan, PC Bickford, DC Lee |
Frontiers in immunology | 2021 |
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Tracheal aspirate RNA sequencing identifies distinct immunological features of COVID-19 ARDS
A Sarma, SA Christenson, A Byrne, E Mick, AO Pisco, C DeVoe, T Deiss, R Ghale, BS Zha, A Tsitsiklis, A Jauregui, F Moazed, AM Detweiler, N Spottiswoode, P Sinha, N Neff, M Tan, PH Serpa, A Willmore, KM Ansel, JG Wilson, A Leligdowicz, ER Siegel, M Sirota, JL DeRisi, MA Matthay, Y Abe-Jones, S Asthana, A Beagle, T Bhakta, S Bhide, C Cai, S Caldera, C Calfee, M Calvo, S Carrillo, A Cattamanchi, S Chak, V Chan, N Chew, S Christenson, Z Collins, A Combes, T Courau, S Darmanis, D Erle, A Esmaili, GK Fragiadakis, R Ghale, J Giberson, A Gonzalez, PH Serpa, C Hendrickson, K Hiam, K Hu, B Huang, A Jauregui, C Jones, N Jones, K Kangelaris, M Krummel, N Kumar, D Kushnoor, T Lea, D Lee, D Lee, KD Liu, Y Liu, S Mahboob, M Matthay, J Milush, P Muñoz-Sandoval, V Nguyen, G Ortiz, R Parada, M Phelps, L Pierce, P Prasad, A Rao, S Rashid, G Reeder, N Rodriguez, B Samad, D Scarlet, C Shaw, A Shen, A Sigman, M Spitzer, Y Sun, S Sunshine, K Tang, LT Altamirano, J Tsui, E Tumurbaatar, K Turner, A Ward, A Willmore, M Wilson, J Winkler, R Withers, K Wong, P Woodruff, J Ye, K Yee, M Yu, S Zha, J Zhan, M Zhou, WS Zhu, CM Hendrickson, KN Kangelaris, MF Krummel, PG Woodruff, DJ Erle, CS Calfee, CR Langelier |
Nature Communications | 2021 |
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Genetic Deletion of mGlu3 Metabotropic Glutamate Receptors Amplifies Ischemic Brain Damage and Associated Neuroinflammation in Mice
F Mastroiacovo, M Zinni, G Mascio, V Bruno, G Battaglia, J Pansiot, T Imbriglio, J Mairesse, O Baud, F Nicoletti |
Frontiers in neurology | 2021 |
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Intranasal delivery of interleukin-4 attenuates chronic cognitive deficits via beneficial microglial responses in experimental traumatic brain injury
H Pu, C Ma, Y Zhao, Y Wang, W Zhang, W Miao, F Yu, X Hu, Y Shi, RK Leak, TK Hitchens, CE Dixon, MV Bennett, J Chen |
Journal of Cerebral Blood Flow & Metabolism | 2021 |
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High-salt diet downregulates TREM2 expression and blunts efferocytosis of macrophages after acute ischemic stroke
M Hu, Y Lin, X Men, S Wang, X Sun, Q Zhu, D Lu, S Liu, B Zhang, W Cai, Z Lu |
Journal of Neuroinflammation | 2021 |
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Microglia polarization in ischemic stroke: complex mechanisms and therapeutic interventions
JH Mao, Y Xu, BW Li, YL Yang, Y Peng, F Zhi |
Chinese Medical Journal | 2021 |
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An Integrated Analysis of Network Pharmacology and Experimental Validation to Reveal the Mechanism of Chinese Medicine Formula Naotaifang in Treating Cerebral Ischemia-Reperfusion Injury
T Yang, X Chen, Z Mei, X Liu, Z Feng, J Liao, Y Deng, J Ge |
Drug design, development and therapy | 2021 |
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Imperatorin inhibits mitogen‐activated protein kinase and nuclear factor kappa‐B signaling pathways and alleviates neuroinflammation in ischemic stroke
J Ge, S Deng, Z Xue, P Liu, L Yu, J Li, S Xia, Y Gu, X Bao, Z Lan, Y Xu, X Zhu |
CNS Neuroscience & Therapeutics | 2021 |
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COVID-19 ARDS is characterized by a dysregulated host response that differs from cytokine storm and is modified by dexamethasone
Aartik Sarma, Stephanie Christenson, Eran Mick, Thomas Deiss, Catherine DeVoe, Angela Pisco, Rajani Ghale, Alejandra Jauregui, Ashley Byrne, Farzad Moazed, Natasha Spottiswoode, Pratik Sinha, Beth Zha, Norma Neff, Michelle Tan, Paula Hayakawa Serpa, K Mark Ansel, Jennifer Wilson, Aleksandra Leligdowicz, Emily Seigel, Marina Sirota, Joseph DeRisi, Michael Matthay, Comet Consortium, Carolyn Hendrickson, Kirsten Kangelaris, Matthew Krummel, Prescott Woodruff, David Erle, Carolyn Calfee, Charles Langelier |
Research square | 2021 |
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Preclinical investigation of pegylated arginase 1 as a treatment for retina and brain injury
Fouda AY, Eldahshan W, Xu Z, Lemtalsi T, Shosha E, Zaidi SA, Abdelrahman AA, Cheng PN, Narayanan SP, Caldwell RW, Caldwell RB |
Experimental Neurology | 2021 |
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Latitudinal and longitudinal regulation of tissue macrophages in inflammatory diseases
He X, Tan S, Shao Z, Wang X |
Genes & Diseases | 2021 |
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Macrophage Metabolism of Apoptotic Cell-Derived Arginine Promotes Continual Efferocytosis and Resolution of Injury
A Yurdagul, M Subramanian, X Wang, SB Crown, OR Ilkayeva, L Darville, GK Kolluru, CC Rymond, BD Gerlach, Z Zheng, G Kuriakose, CG Kevil, JM Koomen, JL Cleveland, DM Muoio, I Tabas |
Cell Metabolism | 2020 |
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CDC-derived extracellular vesicles reprogram inflammatory macrophages to an arginase 1-dependent proangiogenic phenotype
KI Mentkowski, A Mursleen, JD Snitzer, LM Euscher, JK Lang |
American journal of physiology. Heart and circulatory physiology | 2020 |
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The CoV-2 outbreak: how hematologists could help to fight Covid-19
S Galimberti, C Baldini, C Baratè, F Ricci, S Balducci, S Grassi, F Ferro, G Buda, E Benedetti, R Fazzi, L Baglietto, E Lucenteforte, AD Paolo, M Petrini |
Pharmacological research : the official journal of the Italian Pharmacological Society | 2020 |
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Macrophage-Associated Lipin-1 Promotes β-Oxidation in Response to Proresolving Stimuli
RM Schilke, CM Blackburn, S Rao, DM Krzywanski, BN Finck, MD Woolard |
ImmunoHorizons | 2020 |
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P2Y6 receptor inhibition aggravates ischemic brain injury by reducing microglial phagocytosis
RX Wen, H Shen, SX Huang, LP Wang, ZW Li, P Peng, M Mamtilahun, YH Tang, FX Shen, HL Tian, GY Yang, ZJ Zhang |
CNS Neuroscience & Therapeutics | 2020 |
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Genome-wide transcriptomic analysis of microglia reveals impaired responses in aged mice after cerebral ischemia
L Shi, M Rocha, W Zhang, M Jiang, S Li, Q Ye, SH Hassan, L Liu, MN Adair, J Xu, J Luo, X Hu, LR Wechsler, J Chen, Y Shi |
Journal of Cerebral Blood Flow & Metabolism | 2020 |
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Interleukin 4 Affects Epilepsy by Regulating Glial Cells: Potential and Possible Mechanism
L Chen, L Zhu, D Lu, Z Wu, Y Han, P Xu, L Chang, Q Wu |
Frontiers in molecular neuroscience | 2020 |
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Microglia/macrophage polarization: Fantasy or evidence of functional diversity?
X Hu |
Journal of Cerebral Blood Flow & Metabolism | 2020 |
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Inflammatory factors and amyloid β-induced microglial polarization promote inflammatory crosstalk with astrocytes
L Xie, N Zhang, Q Zhang, C Li, AF Sandhu, G Williams, S Lin, PR Lv, Y Liu, Q Wu, S Yu |
Aging | 2020 |
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Macrophages reprogram after ischemic stroke and promote efferocytosis and inflammation resolution in the mouse brain
W Zhang, J Zhao, R Wang, M Jiang, Q Ye, AD Smith, J Chen, Y Shi |
CNS Neuroscience & Therapeutics | 2019 |
