Release of extracellular DNA influences renal ischemia reperfusion injury by platelet activation and formation of neutrophil extracellular traps

Kidney Int. 2017 Feb;91(2):352-364. doi: 10.1016/j.kint.2016.08.006. Epub 2016 Sep 28.

Abstract

Acute kidney injury is often the result of ischemia reperfusion injury, which leads to activation of coagulation and inflammation, resulting in necrosis of renal tubular epithelial cells. Platelets play a central role in coagulation and inflammatory processes, and it has been shown that platelet activation exacerbates acute kidney injury. However, the mechanism of platelet activation during ischemia reperfusion injury and how platelet activation leads to tissue injury are largely unknown. Here we found that renal ischemia reperfusion injury in mice leads to increased platelet activation in immediate proximity of necrotic cell casts. Furthermore, platelet inhibition by clopidogrel decreased cell necrosis and inflammation, indicating a link between platelet activation and renal tissue damage. Necrotic tubular epithelial cells were found to release extracellular DNA, which, in turn, activated platelets, leading to platelet-granulocyte interaction and formation of neutrophil extracellular traps ex vivo. Renal ischemia reperfusion injury resulted in increased DNA-platelet and DNA-platelet-granulocyte colocalization in tissue and elevated levels of circulating extracellular DNA and platelet factor 4 in mice. After renal ischemia reperfusion injury, neutrophil extracellular traps were formed within renal tissue, which decreased when mice were treated with the platelet inhibitor clopidogrel. Thus, during renal ischemia reperfusion injury, necrotic cell-derived DNA leads to platelet activation, platelet-granulocyte interaction, and subsequent neutrophil extracellular trap formation, leading to renal inflammation and further increase in tissue injury.

Keywords: acute kidney injury; inflammation; ischemia reperfusion; platelets; renal pathology.

MeSH terms

  • Animals
  • Blood Platelets / drug effects
  • Blood Platelets / metabolism*
  • Cell Line
  • Clopidogrel
  • DNA / genetics
  • DNA / metabolism*
  • Disease Models, Animal
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism*
  • Epithelial Cells / pathology
  • Extracellular Traps / metabolism*
  • Humans
  • Kidney Tubular Necrosis, Acute / genetics
  • Kidney Tubular Necrosis, Acute / metabolism*
  • Kidney Tubular Necrosis, Acute / pathology
  • Kidney Tubular Necrosis, Acute / prevention & control
  • Kidney Tubules / drug effects
  • Kidney Tubules / metabolism*
  • Kidney Tubules / pathology
  • Male
  • Mice, Inbred C57BL
  • Nephritis / genetics
  • Nephritis / metabolism
  • Nephritis / pathology
  • Platelet Activation* / drug effects
  • Platelet Aggregation Inhibitors / pharmacology
  • Platelet Factor 4 / metabolism
  • Reperfusion Injury / genetics
  • Reperfusion Injury / metabolism*
  • Reperfusion Injury / pathology
  • Reperfusion Injury / prevention & control
  • Signal Transduction
  • Ticlopidine / analogs & derivatives
  • Ticlopidine / pharmacology
  • Time Factors

Substances

  • Platelet Aggregation Inhibitors
  • Platelet Factor 4
  • DNA
  • Clopidogrel
  • Ticlopidine