mROS-TXNIP axis activates NLRP3 inflammasome to mediate renal injury during ischemic AKI

Int J Biochem Cell Biol. 2018 May:98:43-53. doi: 10.1016/j.biocel.2018.02.015. Epub 2018 Mar 21.

Abstract

Ischemia/reperfusion (I/R) is a critical risk factor for acute kidney injury (AKI). Recent studies provided evidence that tubular epithelial cells (TEC)-associated inflammation aggravates kidney injury and impairs tissue repair after I/R injury. Here we demonstrated that the Nod-like receptor protein 3 (NLRP3) inflammasome is activated by mitochondrial reactive oxygen species (mROS) during I/R injury via direct interactions between the inflammasome and thioredoxin-interacting protein (TXNIP). Firstly, we found that NLRP3 inflammasome activation was induced by I/R injury, peaking at day 3 after reperfusion. Consistent with this observation, NLRP3 deletion significantly attenuated I/R-induced kidney damage and markers of inflammasome activation. Then, we observed mitochondrial dysfunction, characterized by ultrastructural changes and cytochrome C (Cyt c) redistribution. Mitochondria-targeted antioxidant MitoTEMPO prevented mROS overproduction and the decline in mitochondrial membrane potential (MMP) in vitro. MitoTEMPO treatment also inhibited NLRP3 inflammasome activation and co-localization of NLRP3 and TXNIP after simulated ischemia/reperfusion (SI/R) injury. Finally, we transfected HK-2 cells with TXNIP siRNA to explore the role of TXNIP in mROS-induced NLRP3 inflammasome activation. We found that TXNIP siRNA significantly inhibited NLRP3 inflammasome activation. These results demonstrate that NLRP3 inflammasome is activated through the mROS-TXNIP-NLRP3 pathway and provide a potential therapeutic target in ischemic AKI.

Keywords: Ischemic AKI; Mitochondrial dysfunction; NLRP3 inflammasome; TXNIP.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acute Kidney Injury / immunology
  • Acute Kidney Injury / metabolism
  • Acute Kidney Injury / pathology*
  • Animals
  • Antioxidants / metabolism
  • Carrier Proteins / metabolism*
  • Cell Proliferation
  • Cells, Cultured
  • Inflammasomes / immunology
  • Inflammasomes / metabolism*
  • Inflammation / immunology
  • Inflammation / metabolism
  • Inflammation / pathology
  • Interleukin-1beta / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mitochondria / immunology
  • Mitochondria / metabolism
  • Mitochondria / pathology*
  • NLR Family, Pyrin Domain-Containing 3 Protein / physiology*
  • Organophosphorus Compounds / metabolism
  • Piperidines / metabolism
  • Reactive Oxygen Species / metabolism*
  • Reperfusion Injury / immunology
  • Reperfusion Injury / metabolism
  • Reperfusion Injury / pathology*
  • Thioredoxins / metabolism*

Substances

  • Antioxidants
  • Carrier Proteins
  • Inflammasomes
  • Interleukin-1beta
  • MitoTEMPO
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Nlrp3 protein, mouse
  • Organophosphorus Compounds
  • Piperidines
  • Reactive Oxygen Species
  • Txnip protein, mouse
  • Thioredoxins