Angiotensin II induces calcium/calcineurin signaling and podocyte injury by downregulating microRNA-30 family members

J Mol Med (Berl). 2017 Aug;95(8):887-898. doi: 10.1007/s00109-017-1547-z. Epub 2017 May 24.

Abstract

Angiotensin II (AngII) is capable of inducing calcium/calcineurin signaling and podocyte injury; however, the precise underlying mechanism is not well understood. Because we have previously demonstrated that microRNA-30s (miR-30s) inhibit calcium/calcineurin signaling in podocytes, we hypothesize that AngII may induce podocyte injury by downregulating miR-30s and thereby activating calcium/calcineurin signaling. To test this hypothesis, we used an AngII-induced podocyte injury mouse model. The mice were treated with AngII via infusion for 28 days, which resulted in hypertension, albuminuria, and glomerular damage. AngII treatment also resulted in a significant reduction of miR-30s and upregulation of calcium/calcineurin signaling components, including TRPC6, PPP3CA, PPP3CB, PPP3R1, and NFATC3, which are the known targets of miR-30s in podocytes. The delivery of miR-30a-expressing lentivirus to the podocytes on day 14 of the infusion ameliorated the AngII-induced podocyte and glomerular injury and attenuated the upregulation of the calcium/calcineurin signaling components. Similarly, treatment with losartan, which is an AngII receptor blocker, also prevented AngII-induced podocyte injury and calcium/calcineurin signaling activation. Notably, losartan was found to sustain miR-30 levels during AngII treatment both in vivo and in vitro. In conclusion, the effect of AngII on podocytes is in part mediated by miR-30s through calcium/calcineurin signaling, a novel mechanism underlying AngII-induced podocyte injury.

Key messages: • AngII infusion resulted in downregulation of miR-30s in podocytes. • Exogenous miR-30a delivery mitigated the glomerular and podocyte injuries induced by AngII. • Both miR-30a and losartan prevented AngII-induced activation of calcium-calcineurin signaling.

Keywords: Angiotensin II; Calcium/calcineurin signaling; Podocytes; miR-30.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiotensin II / pharmacology*
  • Angiotensin II Type 1 Receptor Blockers / pharmacology
  • Animals
  • Calcineurin / metabolism*
  • Calcium / metabolism*
  • Calcium Signaling / drug effects
  • Cells, Cultured
  • Down-Regulation
  • Humans
  • Hypertension / metabolism
  • Hypertension / pathology
  • Kidney Diseases / metabolism
  • Kidney Diseases / pathology
  • Kidney Glomerulus / drug effects
  • Kidney Glomerulus / metabolism
  • Kidney Glomerulus / pathology
  • Losartan / pharmacology
  • Male
  • Mice, Inbred C57BL
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Podocytes / drug effects
  • Podocytes / metabolism*
  • Podocytes / pathology

Substances

  • Angiotensin II Type 1 Receptor Blockers
  • MicroRNAs
  • Angiotensin II
  • Calcineurin
  • Losartan
  • Calcium