Complement-dependent NADPH oxidase enzyme activation in renal ischemia/reperfusion injury

Free Radic Biol Med. 2014 Sep:74:263-73. doi: 10.1016/j.freeradbiomed.2014.07.003. Epub 2014 Jul 10.

Abstract

NADPH oxidase plays a central role in mediating oxidative stress during heart, liver, and lung ischemia/reperfusion injury, but limited information is available about NADPH oxidase in renal ischemia/reperfusion injury. Our aim was to investigate the activation of NADPH oxidase in a swine model of renal ischemia/reperfusion damage. We induced renal ischemia/reperfusion in 10 pigs, treating 5 of them with human recombinant C1 inhibitor, and we collected kidney biopsies before ischemia and 15, 30, and 60 min after reperfusion. Ischemia/reperfusion induced a significant increase in NADPH oxidase 4 (NOX-4) expression at the tubular level, an upregulation of NOX-2 expression in infiltrating monocytes and myeloid dendritic cells, and 8-oxo-7,8-dihydro-2'-deoxyguanosine synthesis along with a marked upregulation of NADPH-dependent superoxide generation. This burden of oxidative stress was associated with an increase in tubular and interstitial expression of the myofibroblast marker α-smooth muscle actin (α-SMA). Interestingly, NOX-4 and NOX-2 expression and the overall NADPH oxidase activity as well as α-SMA expression and 8-oxo-7,8-dihydro-2'-deoxyguanosine synthesis were strongly reduced in C1-inhibitor-treated animals. In vitro, when we incubated tubular cells with the anaphylotoxin C3a, we observed an enhanced NADPH oxidase activity and α-SMA protein expression, which were both abolished by NOX-4 silencing. In conclusion, our findings suggest that NADPH oxidase is activated during ischemia/reperfusion in a complement-dependent manner and may play a potential role in the pathogenesis of progressive renal damage in this setting.

Keywords: C1 inhibitor; Complement system; Free radicals; NOX-2; NOX-4; Oxidative stress; Renal ischemia–reperfusion injury; Renal transplantation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / genetics
  • Actins / metabolism
  • Animals
  • Cells, Cultured
  • Complement C1 Inactivator Proteins / administration & dosage
  • Complement C1 Inhibitor Protein
  • Complement C3a / metabolism
  • Complement System Proteins / metabolism*
  • Dendritic Cells / physiology*
  • Deoxyadenosines / biosynthesis
  • Deoxyadenosines / genetics
  • Enzyme Activation / drug effects
  • Enzyme Activation / genetics
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / genetics
  • Humans
  • Kidney Tubules / blood supply*
  • Kidney Tubules / metabolism
  • Kidney Tubules / pathology
  • Models, Animal
  • NADPH Oxidases / metabolism*
  • Oxidative Stress
  • RNA, Small Interfering / genetics
  • Reperfusion Injury / enzymology*
  • Reperfusion Injury / immunology
  • Sus scrofa

Substances

  • Actins
  • Complement C1 Inactivator Proteins
  • Complement C1 Inhibitor Protein
  • Deoxyadenosines
  • RNA, Small Interfering
  • SERPING1 protein, human
  • 2'-deoxy-7,8-dihydro-8-oxoadenosine
  • Complement C3a
  • Complement System Proteins
  • NADPH Oxidases