Enhanced activation of interleukin-10, heme oxygenase-1, and AKT in C5aR2-deficient mice is associated with protection from ischemia reperfusion injury-induced inflammation and fibrosis

Kidney Int. 2018 Oct;94(4):741-755. doi: 10.1016/j.kint.2018.04.005. Epub 2018 Jun 21.

Abstract

Severe ischemia reperfusion injury (IRI) results in rapid complement activation, acute kidney injury and progressive renal fibrosis. Little is known about the roles of the C5aR1 and C5aR2 complement receptors in IRI. In this study C5aR1-/- and C5aR2-/- mice were compared to the wild type in a renal IRI model leading to renal fibrosis. C5a receptor expression, kidney morphology, inflammation, and fibrosis were measured in different mouse strains one, seven and 21 days after IRI. Renal perfusion was evaluated by functional magnetic resonance imaging. Protein abundance and phosphorylation were assessed with high content antibody microarrays and Western blotting. C5aR1 and C5aR2 were increased in damaged tubuli and even more in infiltrating leukocytes after IRI in kidneys of wild-type mice. C5aR1-/- and C5aR2-/- animals developed less IRI-induced inflammation and showed better renal perfusion than wild-type mice following IRI. C5aR2-/- mice, in particular, had enhanced tubular and capillary regeneration with less renal fibrosis. Anti-inflammatory IL-10 and the survival/growth kinase AKT levels were especially high in kidneys of C5aR2-/- mice following IRI. LPS caused bone marrow-derived macrophages from C5aR2-/- mice to release IL-10 and to express the stress response enzyme heme oxygenase-1. Thus, C5aR1 and C5aR2 have overlapping actions in which the kidneys of C5aR2-/- mice regenerate better than those in C5aR1-/- mice following IRI. This is mediated, at least in part, by differential production of IL-10, heme oxygenase-1 and AKT.

Keywords: AKT; HO-1; IL-10; complement; fibrosis; ischemia reperfusion injury; regeneration; renal perfusion.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Proliferation / genetics
  • Cells, Cultured
  • Epithelial Cells
  • Fibrosis
  • Heme Oxygenase-1 / metabolism*
  • Inflammation / etiology
  • Interleukin-10 / metabolism*
  • Kidney / diagnostic imaging
  • Kidney Tubules / metabolism
  • Kidney Tubules / pathology*
  • Kidney Tubules / physiopathology
  • Lipopolysaccharides / pharmacology
  • Macrophages / metabolism
  • Magnetic Resonance Imaging
  • Membrane Proteins / metabolism*
  • Mice
  • Mice, Knockout
  • Perfusion Imaging
  • Phosphorylation
  • Protective Factors
  • Proto-Oncogene Proteins c-akt / metabolism*
  • Receptor, Anaphylatoxin C5a / genetics*
  • Receptor, Anaphylatoxin C5a / metabolism
  • Regeneration / genetics
  • Reperfusion Injury / complications
  • Reperfusion Injury / genetics*
  • Up-Regulation

Substances

  • C5ar1 protein, mouse
  • C5ar2 protein, mouse
  • IL10 protein, mouse
  • Lipopolysaccharides
  • Membrane Proteins
  • Receptor, Anaphylatoxin C5a
  • Interleukin-10
  • Heme Oxygenase-1
  • Hmox1 protein, mouse
  • Proto-Oncogene Proteins c-akt