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Controlled Decompression Alleviates Motor Dysfunction by Regulating Microglial Polarization via the HIF-1α Signaling Pathway in Intracranial Hypertension

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Abstract

Decompressive craniectomy (DC) is a major form of surgery that is used to reduce intracranial hypertension (IH), the most frequent cause of death and disability following severe traumatic brain injury (sTBI) and stroke. Our previous research showed that controlled decompression (CDC) was more effective than rapid decompression (RDC) with regard to reducing the incidence of complications and improving outcomes after sTBI; however, the specific mechanisms involved have yet to be elucidated. In the present study, we investigated the effects of CDC in regulating inflammation after IH and attempted to identify the mechanisms involved. Analysis showed that CDC was more effective than RDC in alleviating motor dysfunction and neuronal death in a rat model of traumatic intracranial hypertension (TIH) created by epidural balloon pressurization. Moreover, RDC induced M1 microglia polarization and the release of pro-inflammatory cytokines. However, CDC treatment resulted in microglia primarily polarizing into the M2 phenotype and induced the significant release of anti-inflammatory cytokines. Mechanistically, the establishment of the TIH model led to the increased expression of hypoxia-inducible factor-1α (HIF-1α); CDC ameliorated cerebral hypoxia and reduced the expression of HIF-1α. In addition, 2-methoxyestradiol (2-ME2), a specific inhibitor of HIF-1α, significantly attenuated RDC-induced inflammation and improved motor function by promoting M1 to M2 phenotype transformation in microglial and enhancing the release of anti-inflammatory cytokines. However, dimethyloxaloylglycine (DMOG), an agonist of HIF-1α, abrogated the protective effects of CDC treatment by suppressing M2 microglia polarization and the release of anti-inflammatory cytokines. Collectively, our results indicated that CDC effectively alleviated IH-induced inflammation, neuronal death, and motor dysfunction by regulating HIF-1α-mediated microglial phenotype polarization. Our findings provide a better understanding of the mechanisms that underlie the protective effects of CDC and promote clinical translational research for HIF-1α in IH.

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Data Availability

All data generated or analyzed during this study are included in this published article. The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Funding

The current study was funded by the National Natural Science Foundation of China (No.81871589), the Military Logistics Scientific Research Project (No. CLB20J027), Wuxi Municipal Bureau on Science and Technology (N20202037), the Key scientific research project of Jiangsu Provincial Health Commission (K2019018), the Wuxi Municipal Social Development Science and Technology Demonstration Project (N20201008), the Natural Science Foundation of Jiangsu Province (BK20221206), and the Young Elite Scientists Sponsorship Program of Jiangsu Province (TJ-2022-028).

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  1. Department of Neurosurgery, The 904th Hospital of PLA, Wuxi Clinical College of Anhui Medical University, Wuxi, 214044, Jiangsu, China

    Jie Zheng, Chenxu Zhang, Yonghui Wu, Chonghui Zhang, Yuanyuan Che, Wang Zhang, Yang Yang, Jie Zhu, Likun Yang & Yuhai Wang

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Contributions

YHW, LKY, and JZ contributed to the conception and design of the study. JZ, YY, CXZ, YHW, CHZ, YYC, and WZ acquired and analyzed the data. JZ and YHW drafted a significant portion of the manuscript or figures. All authors read and approved the present version of the manuscript to be published.

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Correspondence to Jie Zhu, Likun Yang or Yuhai Wang.

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All experiments are reported in compliance with the Animal Research: Reporting of In Vivo Experiments (ARRIVE) guidelines. The experimental protocols were approved by the Laboratory Animal Welfare and Ethics Committee of the 904th Hospital of PLA (20220215) and performed according to the Guide for the Care and Use of Laboratory Animals.

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Jie Zheng, Chenxu Zhang, and Yonghui Wu contributed equally to this manuscript.

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Zheng, J., Zhang, C., Wu, Y. et al. Controlled Decompression Alleviates Motor Dysfunction by Regulating Microglial Polarization via the HIF-1α Signaling Pathway in Intracranial Hypertension. Mol Neurobiol 60, 5607–5623 (2023). https://doi.org/10.1007/s12035-023-03416-6

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  • DOI: https://doi.org/10.1007/s12035-023-03416-6

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