miR-34c-5p and CaMKII are involved in aldosterone-induced fibrosis in kidney collecting duct cells

Am J Physiol Renal Physiol. 2018 Mar 1;314(3):F329-F342. doi: 10.1152/ajprenal.00358.2017. Epub 2017 Oct 25.

Abstract

Mineralocorticoids trigger a profibrotic process in the kidney. In mouse cortical collecting duct cells, the present study addressed two main questions: 1) what are microRNAs (miRNAs) and their target genes that are changed by aldosterone? and 2) what do miRNAs, in response to aldosterone, regulate regarding signaling pathways related to fibrosis? A microarray chip assay was done in cells in the absence or presence of aldosterone treatment (10-6 M; 3 days). The candidate miRNAs were identified by the criteria of >30% of fold change among the significantly changed miRNAs ( P < 0.05). Twenty-nine miRNAs were upregulated (>1.3-fold), and 27 miRNAs were downregulated (<0.7-fold). Putative target genes of identified miRNAs were associated with 74 Kyoto Encyclopedia of Genes and Genomes pathways. Among them, the wingless-related integration site (Wnt) signaling pathway was highly ranked, where 15 mature miRNAs were observed. These miRNAs were further analyzed by real-time quantitative PCR, and among them, miR-130b-3p, miR-34c-5p, and miR-146a-5p were selected. Through the identification of putative target genes of these three miRNAs, mRNA and protein expression of the Ca2+/calmodulin-dependent protein kinase type II β-chain ( Camk2b) gene (a target gene of miR-34c-5p) were found to be increased significantly in aldosterone-treated cells, where fibronectin (FN) and α-smooth muscle actin were induced. When CaMKIIβ small interfering RNA or the miR-34c-5p mimic was transfected, aldosterone-induced FN expression was significantly attenuated, along with reduced CaMKIIβ protein expression. A luciferase reporter assay revealed a decrease of CaMKIIβ translation in cells transfected with miRNA mimics of miR-34c-5p. In conclusion, aldosterone-induced downregulation of miR-34c-5p in the Wnt signaling pathway and a consequent increase of CaMKIIβ expression are likely to be involved in aldosterone-induced fibrosis.

Keywords: CaMKII; Wnt signaling; aldosterone; microRNA.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / metabolism
  • Aldosterone*
  • Animals
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / genetics
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / metabolism*
  • Cell Line
  • Disease Models, Animal
  • Fibronectins / metabolism
  • Fibrosis
  • Gene Expression Profiling / methods
  • Gene Expression Regulation
  • Gene Regulatory Networks
  • Kidney Diseases / chemically induced
  • Kidney Diseases / enzymology*
  • Kidney Diseases / genetics
  • Kidney Diseases / pathology
  • Kidney Tubules, Collecting / enzymology*
  • Kidney Tubules, Collecting / pathology
  • Mice, Inbred C57BL
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Transcriptome
  • Wnt Signaling Pathway

Substances

  • Actins
  • Fibronectins
  • MIRN34a microRNA, mouse
  • MicroRNAs
  • alpha-smooth muscle actin, mouse
  • Aldosterone
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Camk2b protein, mouse