Myeloid HO-1 modulates macrophage polarization and protects against ischemia-reperfusion injury

JCI Insight. 2018 Oct 4;3(19):e120596. doi: 10.1172/jci.insight.120596.

Abstract

Macrophages polarize into heterogeneous proinflammatory M1 and antiinflammatory M2 subtypes. Heme oxygenase 1 (HO-1) protects against inflammatory processes such as ischemia-reperfusion injury (IRI), organ transplantation, and atherosclerosis. To test our hypothesis that HO-1 regulates macrophage polarization and protects against IRI, we generated myeloid-specific HO-1-knockout (mHO-1-KO) and -transgenic (mHO-1-Tg) mice, with deletion or overexpression of HO-1, in various macrophage populations. Bone marrow-derived macrophages (BMDMs) from mHO-1-KO mice, treated with M1-inducing LPS or M2-inducing IL-4, exhibited increased mRNA expression of M1 (CXCL10, IL-1β, MCP1) and decreased expression of M2 (Arg1 and CD163) markers as compared with controls, while BMDMs from mHO-1-Tg mice displayed the opposite. A similar pattern was observed in the hepatic M1/M2 expression profile in a mouse model of liver IRI. mHO-1-KO mice displayed increased hepatocellular damage, serum AST/ALT levels, Suzuki's histological score of liver IRI, and neutrophil and macrophage infiltration, while mHO-1-Tg mice exhibited the opposite. In human liver transplant biopsies, subjects with higher HO-1 levels showed lower expression of M1 markers together with decreased hepatocellular damage and improved outcomes. In conclusion, myeloid HO-1 expression modulates macrophage polarization, and protects against liver IRI, at least in part by favoring an M2 phenotype.

Keywords: Hepatology; Inflammation; Innate immunity.

Publication types

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

MeSH terms

  • Adolescent
  • Adult
  • Allografts / blood supply
  • Allografts / cytology
  • Allografts / pathology
  • Animals
  • Biopsy
  • Disease Models, Animal
  • Female
  • Graft Rejection / diagnosis
  • Graft Rejection / immunology*
  • Graft Rejection / pathology
  • Heme Oxygenase-1 / genetics
  • Heme Oxygenase-1 / metabolism*
  • Humans
  • Liver / blood supply
  • Liver / cytology
  • Liver / pathology
  • Liver Function Tests
  • Liver Transplantation / adverse effects*
  • Macrophages / immunology*
  • Macrophages / metabolism
  • Male
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Mice
  • Mice, Knockout
  • Middle Aged
  • Reperfusion Injury / diagnosis
  • Reperfusion Injury / immunology*
  • Reperfusion Injury / pathology
  • Signal Transduction / immunology
  • Young Adult

Substances

  • Membrane Proteins
  • HMOX1 protein, human
  • Heme Oxygenase-1
  • Hmox1 protein, mouse