Gut-derived macrophages link intestinal damage to brain injury after cardiac arrest through TREM1 signaling

Cell Mol Immunol. 2025 Apr;22(4):437-455. doi: 10.1038/s41423-025-01263-0. Epub 2025 Feb 21.

Abstract

Brain injury is the leading cause of death and disability in survivors of cardiac arrest, where neuroinflammation triggered by infiltrating macrophages plays a pivotal role. Here, we seek to elucidate the origin of macrophages infiltrating the brain and their mechanism of action after cardiac arrest/cardiopulmonary resuscitation (CA/CPR). Wild-type or photoconvertible Cd68-Cre:R26-LSL-KikGR mice were subjected to 10-min CA/CPR, and the migration of gut-derived macrophages into brain was assessed. Transcriptome sequencing was performed to identify the key proinflammatory signal of macrophages infiltrating the brain, triggering receptor expressed on myeloid cells 1 (TREM1). Upon drug intervention, the effects of TREM1 on post-CA/CPR brain injury were further evaluated. 16S rRNA sequencing was used to detect gut dysbiosis after CA/CPR. Through photoconversion experiments, we found that small intestine-derived macrophages infiltrated the brain and played a crucial role in triggering secondary brain injury after CA/CPR. The infiltrating peripheral macrophages showed upregulated TREM1 levels, and we further revealed the crucial role of gut-derived TREM1+ macrophages in post-CA/CPR brain injury through a drug intervention targeting TREM1. Moreover, a close correlation between upregulated TREM1 expression and poor neurological outcomes was observed in CA survivors. Mechanistically, CA/CPR caused a substantial expansion of Enterobacter at the early stage, which ignited intestinal TREM1 signaling via the activation of Toll-like receptor 4 on macrophages through the release of lipopolysaccharide. Our findings reveal essential crosstalk between the gut and brain after CA/CPR and underscore the potential of targeting TREM1+ small intestine-derived macrophages as a novel therapeutic strategy for mitigating post-CA/CPR brain injury.

Keywords: Brain injury; Cardiac arrest; Intestinal injury; Macrophage trafficking; TREM1.

MeSH terms

  • Animals
  • Brain Injuries* / etiology
  • Brain Injuries* / metabolism
  • Brain Injuries* / pathology
  • Gastrointestinal Microbiome
  • Heart Arrest* / complications
  • Heart Arrest* / pathology
  • Intestines* / pathology
  • Macrophages* / immunology
  • Macrophages* / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Signal Transduction*
  • Triggering Receptor Expressed on Myeloid Cells-1* / metabolism

Substances

  • Triggering Receptor Expressed on Myeloid Cells-1
  • TREM1 protein, mouse