Blockade of KCa3.1 potassium channels protects against cisplatin-induced acute kidney injury

Arch Toxicol. 2016 Sep;90(9):2249-2260. doi: 10.1007/s00204-015-1607-5. Epub 2015 Oct 5.

Abstract

Tubular cell apoptosis significantly contributes to cisplatin-induced acute kidney injury (AKI) pathogenesis. Although KCa3.1, a calcium-activated potassium channel, participates in apoptosis, its involvement in cisplatin-induced AKI is unknown. Here, we found that cisplatin treatment triggered an early induction of KCa3.1 expression associated with HK-2 cell apoptosis, the development of renal tubular damage, and apoptosis in mice. Treatment with the highly selective KCa3.1 blocker TRAM-34 suppressed cisplatin-induced HK-2 cell apoptosis. We further assessed whether KCa3.1 mediated cisplatin-induced AKI in genetic knockout and pharmacological blockade mouse models. KCa3.1 deficiency reduced renal function loss, renal tubular damage, and the induction of the apoptotic marker caspase-3 in the kidneys of cisplatin-treated KCa3.1 (-/-) mice. Pharmacological blockade of KCa3.1 by TRAM-34 similarly attenuated cisplatin-induced AKI in mice. Furthermore, we dissected the mechanisms underlying cisplatin-induced apoptosis reduction via KCa3.1 blockade. We found that KCa3.1 blockade attenuated cytochrome c release and the increase in the intrinsic apoptotic mediators Bax, Bak, and caspase-9 after cisplatin treatment. KCa3.1 blocking inhibited the cisplatin-induced activation of the endoplasmic reticulum (ER) stress mediator caspase-12, which is independent of calcium-dependent protease m-calpain activation. Taken together, KCa3.1 blockade protects against cisplatin-induced AKI through the attenuation of apoptosis by interference with intrinsic apoptotic and ER stress-related mediators, providing a potential target for the prevention of cisplatin-induced AKI.

Keywords: Acute kidney injury; Cisplatin; KCa3.1 potassium channel; Tubular cell apoptosis.

MeSH terms

  • Acute Kidney Injury / chemically induced
  • Acute Kidney Injury / genetics
  • Acute Kidney Injury / metabolism
  • Acute Kidney Injury / prevention & control*
  • Animals
  • Apoptosis / drug effects
  • Apoptosis Regulatory Proteins / metabolism
  • Cell Line
  • Cisplatin / toxicity*
  • Cytoprotection
  • Disease Models, Animal
  • Endoplasmic Reticulum Stress / drug effects
  • Humans
  • Intermediate-Conductance Calcium-Activated Potassium Channels / antagonists & inhibitors*
  • Intermediate-Conductance Calcium-Activated Potassium Channels / deficiency
  • Intermediate-Conductance Calcium-Activated Potassium Channels / genetics
  • Intermediate-Conductance Calcium-Activated Potassium Channels / metabolism*
  • Kidney Tubules, Proximal / drug effects*
  • Kidney Tubules, Proximal / metabolism
  • Kidney Tubules, Proximal / pathology
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Potassium Channel Blockers / pharmacology*
  • Pyrazoles / toxicity*
  • Signal Transduction / drug effects
  • Time Factors

Substances

  • Apoptosis Regulatory Proteins
  • Intermediate-Conductance Calcium-Activated Potassium Channels
  • KCNN4 protein, human
  • Kcnn4 protein, mouse
  • Potassium Channel Blockers
  • Pyrazoles
  • TRAM 34
  • Cisplatin