The TREM1-AQP4 axis mediates neuroinflammatory injury and brain edema after experimental subarachnoid hemorrhage

TREM1-AQP4轴介导实验性蛛网膜下腔出血后的神经炎症损伤和脑水肿

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Abstract

OBJECTIVE: Secondary brain injury following subarachnoid hemorrhage (SAH) is a major factor contributing to poor patient outcomes, with neuroinflammation and cerebral edema representing core pathological mechanisms. Triggering receptor expressed on myeloid cells-1 (TREM1), a major inflammatory amplifier in innate immunity, remains poorly understood in SAH regarding its specific role, cellular targets, and association with aquaporin-4 (AQP4), a key molecule involved in cerebral edema. To determine how TREM1 governs neuroinflammatory injury after experimental SAH and to investigate whether it acts by driving microglial activation and modulating AQP4 expression. METHODS: An SAH model was established in rats via internal carotid artery puncture. TREM1 expression was specifically upregulated or downregulated in vivo through lateral ventricle injection of adeno-associated virus (AAV). Animals were randomly allocated to sham surgery, SAH empty vector control, SAH TREM1 overexpression, and SAH TREM1 knockdown groups. Twenty-four hours post-SAH, neurological function was evaluated with the modified Garcia score and balance beam test; brain water content was quantified from the wet-to-dry weight ratio; HE-stained sections were examined for neuronal morphology; western blot and real-time quantitative PCR (qRT-PCR) were employed to detect the expressions of TREM1, Iba1, GFAP, AQP4, NeuN, cleaved Caspase-3, IL-6, and IL-13; immunofluorescence staining was performed for localization and semi-quantitative analysis. RESULTS: Following subarachnoid hemorrhage (SAH), TREM1 expression is significantly upregulated in brain tissue, with its levels negatively correlated with neurological deficits. Functional and molecular studies demonstrate that TREM1 inhibition improves neurological function, reduces cerebral edema, and mitigates neuronal apoptosis, whereas overexpression exacerbates injury. Mechanistic studies reveal that TREM1 exacerbates secondary brain injury by promoting microglial hyperactivation and inflammatory responses, while simultaneously upregulating astrocytic AQP4 expression. CONCLUSION: This study preliminarily indicates that TREM1 inhibition is associated with reduced neuroinflammation and concomitant downregulation of AQP4. These findings suggest that the "TREM1-AQP4" axis may represent an intrinsically connected pathological pathway that jointly contributes to brain injury following SAH. Although this hypothesis requires direct validation, targeting TREM1 demonstrates potential therapeutic value in improving outcomes through synergistic anti-inflammatory and anti-edematous effects.

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