Objectives: Ischemia-induced lactate accumulation contributes to neuronal injury. However, the mechanisms linking metabolic stress to epigenetic regulation and neuroinflammation remain unclear. This study investigates how lactate triggers neuronal damage via histone lactylation, with a focus on the TRPV1–p300–H3K18la signaling pathway. Methods: Male Sprague-Dawley rats were subjected to transient middle cerebral artery occlusion (tMCAO) with or without TRPV1 or p300 inhibition. Infarct volume, neurological deficits, lactate levels, histone lactylation, proinflammatory gene expression, ATP production, and mitochondrial integrity were assessed. In SH-SY5Y neurons subjected to oxygen-glucose deprivation/reoxygenation (OGD/R), lactate stimulation, gene knockdown, and pharmacologic inhibition were used to probe TRPV1 activation, Ca 2+ influx, H3K18la enrichment (ChIP-qPCR), and cytokine expression. Results: Lactate levels rose rapidly following ischemia, inducing TRPV1 membrane translocation (3.7 ± 0.3-fold vs. Sham, p<0.001), and Ca 2+ influx, which activated the histone acetyltransferase p300 (1.7 ± 0.3-fold). This led to increased histone H3K18 lactylation (2.3 ±0.4), pan-Kla expression (2.4± 0.4, p<0.001), and proinflammatory gene expression, particularly NF-κB. ChIP-qPCR revealed H3K18la enrichment at the NF-κB promoter (2.1 ±0.8-fold), which was significantly suppressed by LDH inhibition (OXA, p<0.001). Pharmacological blockade of TRPV1 (Capsazepine) or p300 (C646) significantly reduced histone lactylation and cytokine expression (NF-κB, IL-1β, and TNF-α), preserved ATP production and the mitochondrial membrane potential (p<0.01), reduced the number of apoptotic neurons (p<0.001), and infarct volume (31%), thus improved neurological outcomes. In vitro, similar suppression of TRPV1–p300 signaling reversed lactate-induced neuronal inflammation and injury. Conclusion: Our study reveals a novel TRPV1–p300–H3K18la epigenetic cascade in which ischemia-induced lactate accumulation acts simultaneously as a metabolic signal and a substrate, converging on histone lactylation to amplify NF-κB–driven neuroinflammation. This mechanism bridges metabolic crises with chromatin remodeling, driving irreversible neuronal injury.
Geng et al. (Thu,) studied this question.