Reactive oxygen species promote tubular injury in diabetic nephropathy: The role of the mitochondrial ros-txnip-nlrp3 biological axis

Redox Biol. 2018 Jun:16:32-46. doi: 10.1016/j.redox.2018.02.013. Epub 2018 Feb 15.

Abstract

NLRP3/IL-1β activation via thioredoxin (TRX)/thioredoxin-interacting protein (TXNIP) following mitochondria ROS (mtROS) overproduction plays a key role in inflammation. However, the involvement of this process in tubular damage in the kidneys of patients with diabetic nephropathy (DN) is unclear. Here, we demonstrated that mtROS overproduction is accompanied by decreases in TRX expression and TXNIP up-regulation. In addition, we discovered that mtROS overproduction is also associated with increases in NLRP3/IL-1β and TGF-β expression in the kidneys of patients with DN and db/db mice. We reversed these changes in db/db mice by administering a peritoneal injection of MitoQ, an antioxidant targeting mtROS. Similar results were observed in human tubular HK-2 cells subjected to high-glucose (HG) conditions and treated with MitoQ. Treating HK-2 cells with MitoQ suppressed the dissociation of TRX from TXNIP and subsequently blocked the interaction between TXNIP and NLRP3, leading to the inhibition of NLRP3 inflammasome activation and IL-1β maturation. The effects of MitoQ were enhanced by pretreatment with TXNIP siRNA and abolished by pretreatment with monosodium urate (MSU) and TRX siRNA in vitro. These results suggest that mitochondrial ROS-TXNIP/NLRP3/IL-1β axis activation is responsible for tubular oxidative injury, which can be ameliorated by MitoQ via the inhibition of mtROS overproduction.

Keywords: Diabetic nephropathy; MitoQ; Mitochondria; NLRP3 inflammasome; Reactive oxygen species (ROS); TRX/TXNIP.

Publication types

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

MeSH terms

  • Animals
  • Carrier Proteins / genetics*
  • Diabetic Nephropathies / genetics
  • Diabetic Nephropathies / metabolism*
  • Diabetic Nephropathies / pathology
  • Gene Expression Regulation / drug effects
  • Humans
  • Inflammasomes / genetics
  • Inflammasomes / metabolism
  • Interleukin-1beta / genetics*
  • Kidney Tubules / injuries
  • Kidney Tubules / metabolism
  • Kidney Tubules / pathology
  • Mice
  • Mice, Inbred NOD
  • Mitochondria / drug effects
  • Mitochondria / genetics
  • Mitochondria / metabolism
  • NLR Family, Pyrin Domain-Containing 3 Protein / genetics*
  • Organophosphorus Compounds / administration & dosage
  • RNA, Small Interfering / genetics
  • Reactive Oxygen Species / metabolism*
  • Signal Transduction / drug effects
  • Thioredoxins / genetics*
  • Ubiquinone / administration & dosage
  • Ubiquinone / analogs & derivatives

Substances

  • Carrier Proteins
  • IL1B protein, mouse
  • Inflammasomes
  • Interleukin-1beta
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Nlrp3 protein, mouse
  • Organophosphorus Compounds
  • RNA, Small Interfering
  • Reactive Oxygen Species
  • Txnip protein, mouse
  • Ubiquinone
  • mitoquinone
  • Thioredoxins