Carbon monoxide confers protection in sepsis by enhancing beclin 1-dependent autophagy and phagocytosis

Antioxid Redox Signal. 2014 Jan 20;20(3):432-42. doi: 10.1089/ars.2013.5368. Epub 2013 Oct 5.

Abstract

Aims: Sepsis, a systemic inflammatory response to infection, represents the leading cause of death in critically ill patients. However, the pathogenesis of sepsis remains incompletely understood. Carbon monoxide (CO), when administered at low physiologic doses, can modulate cell proliferation, apoptosis, and inflammation in pre-clinical tissue injury models, though its mechanism of action in sepsis remains unclear.

Results: CO (250 ppm) inhalation increased the survival of C57BL/6J mice injured by cecal ligation and puncture (CLP) through the induction of autophagy, the down-regulation of pro-inflammatory cytokines, and by decreasing the levels of bacteria in blood and vital organs, such as the lung and liver. Mice deficient in the autophagic protein, Beclin 1 (Becn1(+/-)) were more susceptible to CLP-induced sepsis, and unresponsive to CO therapy, relative to their corresponding wild-type (Becn1(+/+)) littermate mice. In contrast, mice deficient in autophagic protein microtubule-associated protein-1 light chain 3B (LC3B) (Map1lc3b(-/-)) and their corresponding wild-type (Map1lc3b(+/+)) mice showed no differences in survival or response to CO, during CLP-induced sepsis. CO enhanced bacterial phagocytosis in Becn1(+/+) but not Becn1(+/-) mice in vivo and in corresponding cultured macrophages. CO also enhanced Beclin 1-dependent induction of macrophage protein signaling lymphocyte-activation molecule, a regulator of phagocytosis.

Innovation: Our findings demonstrate a novel protective effect of CO in sepsis, dependent on autophagy protein Beclin 1, in a murine model of CLP-induced polymicrobial sepsis.

Conclusion: CO increases the survival of mice injured by CLP through systemic enhancement of autophagy and phagocytosis. Taken together, we suggest that CO gas may represent a novel therapy for patients with sepsis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Apoptosis Regulatory Proteins / genetics*
  • Apoptosis Regulatory Proteins / metabolism
  • Autophagy / drug effects
  • Beclin-1
  • Carbon Monoxide / administration & dosage*
  • Carbon Monoxide / metabolism
  • Cell Proliferation / drug effects
  • Humans
  • Inflammation / drug therapy
  • Inflammation / pathology
  • Liver / drug effects
  • Liver / microbiology
  • Lung / drug effects
  • Lung / microbiology
  • Mice
  • Phagocytosis / drug effects*
  • Punctures / adverse effects
  • Sepsis / metabolism*
  • Sepsis / pathology
  • Wounds and Injuries / drug therapy
  • Wounds and Injuries / microbiology

Substances

  • Apoptosis Regulatory Proteins
  • Beclin-1
  • Becn1 protein, mouse
  • Carbon Monoxide