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

Jie Zheng1, Chenxu Zhang1, Yonghui Wu1

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

Molecular Neurobiology
|June 16, 2023
PubMed

Insights

Controlled decompression (CDC) reduces inflammation and neuronal death after traumatic intracranial hypertension (TIH) by shifting microglia to an anti-inflammatory M2 state, unlike rapid decompression (RDC). This mechanism involves regulating hypoxia-inducible factor-1α (HIF-1α).

Area of Science:

  • Neuroscience
  • Surgical Research
  • Inflammation Biology

Background:

  • Decompressive craniectomy (DC) is crucial for managing intracranial hypertension (IH) after severe traumatic brain injury (sTBI) and stroke.
  • Controlled decompression (CDC) shows promise over rapid decompression (RDC) in improving outcomes, but underlying mechanisms require elucidation.
  • Inflammation and microglial polarization are key factors in brain injury progression following IH.

Purpose of the Study:

  • To investigate the effects of CDC on regulating inflammation in a rat model of traumatic intracranial hypertension (TIH).
  • To identify the specific molecular mechanisms, particularly involving hypoxia-inducible factor-1α (HIF-1α), by which CDC exerts its protective effects.
  • To compare the impact of CDC versus RDC on microglial polarization and cytokine release.

Main Methods:

  • Established a rat model of TIH using epidural balloon pressurization.
  • Administered CDC and RDC, assessing motor function, neuronal death, and inflammatory markers.
  • Analyzed microglial polarization (M1 vs. M2 phenotypes) and cytokine profiles.
  • Investigated the role of HIF-1α using specific inhibitors (2-methoxyestradiol, 2-ME2) and agonists (dimethyloxaloylglycine, DMOG).

Main Results:

  • CDC significantly alleviated motor dysfunction and neuronal death compared to RDC.
  • RDC promoted pro-inflammatory M1 microglia polarization and cytokine release, while CDC induced anti-inflammatory M2 polarization and cytokine release.
  • CDC reduced HIF-1α expression, and manipulating HIF-1α levels (via 2-ME2 or DMOG) confirmed its role in mediating CDC's anti-inflammatory and neuroprotective effects.
  • CDC ameliorated cerebral hypoxia and reduced HIF-1α expression.

Conclusions:

  • Controlled decompression (CDC) effectively mitigates inflammation, neuronal death, and motor deficits in a rat model of traumatic intracranial hypertension (TIH).
  • The protective mechanisms of CDC involve the regulation of HIF-1α-mediated microglial phenotype polarization towards an anti-inflammatory M2 state.
  • These findings enhance understanding of CDC's benefits and support further clinical research into HIF-1α targeted therapies for IH.

Keywords:
Controlled decompressionHIF-1αInflammationIntracranial hypertensionMicroglial polarization

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