TREM-1 Promotes Microglial Pyroptosis and Mitochondrial Fission in Intracerebral Hemorrhage via the PI3K/AKT Pathway

FASEB J. 2025 Oct 15;39(19):e71115. doi: 10.1096/fj.202501909R.

Abstract

TREM-1, a pro-inflammatory factor, aggravates neuroinflammation following intracerebral hemorrhage (ICH). Both pyroptosis and mitochondrial dysfunction play a vital role in the further injury of ICH. However, whether TREM-1 regulates microglial pyroptosis and mitochondrial fission, and the potential mechanisms underlying these processes, remains unclear. A mouse model of ICH was established via stereotactic injection of collagenase VII-S. To knock down TREM-1 in vivo, AAV9-Iba1-TREM-1 was injected into the right basal ganglia. Additionally, the TREM-1-specific inhibitor LP17 was administered intranasally. Neurological function was assessed using behavioral assessments. In vitro, BV2 was stimulated with hemin to mimic ICH. LP17, NLRP3 inhibitor MCC950, TREM-1 agonist antibody Mab1187, and phosphatidylinositol 3-kinase (PI3K) inhibitor LY294002 were used to investigate the mechanisms underlying TREM-1-mediated microglial pyroptosis and mitochondrial fission. Immunofluorescence staining, Western blot, RT-qPCR, and transmission electron microscopy were employed to evaluate microglial pyroptosis and mitochondrial fission. Both pharmacological inhibition and AAV-mediated knockdown of TREM-1 significantly improved neurological function, attenuated microglial pyroptosis and mitochondrial fission in ICH mice. TREM-1 was shown to drive microglial pyroptosis through the NLRP3 inflammasome. Furthermore, the PI3K/AKT signaling pathway was demonstrated to regulate TREM-1-induced microglial pyroptosis and mitochondrial fission. This study provides the first evidence that TREM-1 promotes microglial pyroptosis and mitochondrial fission following ICH via the PI3K/AKT signaling pathway. These findings highlight TREM-1 as a potential therapeutic target for mitigating neuroinflammation and neuronal damage in ICH.

Keywords: TREM‐1; intracerebral hemorrhage; microglial; mitochondrial fission; neuroinflammation; pyroptosis.

MeSH terms

  • Animals
  • Cerebral Hemorrhage* / metabolism
  • Cerebral Hemorrhage* / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Microglia* / physiology
  • Mitochondrial Dynamics / physiology
  • Phosphatidylinositol 3-Kinases / genetics
  • Phosphatidylinositol 3-Kinases / metabolism
  • Proto-Oncogene Proteins c-akt* / genetics
  • Proto-Oncogene Proteins c-akt* / metabolism
  • Pyroptosis
  • Signal Transduction
  • Triggering Receptor Expressed on Myeloid Cells-1* / genetics
  • Triggering Receptor Expressed on Myeloid Cells-1* / metabolism

Substances

  • TREM1 protein, mouse
  • Triggering Receptor Expressed on Myeloid Cells-1
  • Proto-Oncogene Proteins c-akt
  • Phosphatidylinositol 3-Kinases