Inhibition of profibrotic microRNA-21 affects platelets and their releasate

JCI Insight. 2018 Nov 2;3(21):e123335. doi: 10.1172/jci.insight.123335.

Abstract

Fibrosis is a major contributor to organ disease for which no specific therapy is available. MicroRNA-21 (miR-21) has been implicated in the fibrogenetic response, and inhibitors of miR-21 are currently undergoing clinical trials. Here, we explore how miR-21 inhibition may attenuate fibrosis using a proteomics approach. Transfection of miR-21 mimic or inhibitor in murine cardiac fibroblasts revealed limited effects on extracellular matrix (ECM) protein secretion. Similarly, miR-21-null mouse hearts showed an unaltered ECM composition. Thus, we searched for additional explanations as to how miR-21 might regulate fibrosis. In plasma samples from the community-based Bruneck Study, we found a marked correlation of miR-21 levels with several platelet-derived profibrotic factors, including TGF-β1. Pharmacological miR-21 inhibition with an antagomiR reduced the platelet release of TGF-β1 in mice. Mechanistically, Wiskott-Aldrich syndrome protein, a negative regulator of platelet TGF-β1 secretion, was identified as a direct target of miR-21. miR-21-null mice had lower platelet and leukocyte counts compared with littermate controls but higher megakaryocyte numbers in the bone marrow. Thus, to our knowledge this study reports a previously unrecognized effect of miR-21 inhibition on platelets. The effect of antagomiR-21 treatment on platelet TGF-β1 release, in particular, may contribute to the antifibrotic effects of miR-21 inhibitors.

Keywords: Cardiology; Cell Biology; Fibrosis; Noncoding RNAs; Platelets.

Publication types

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

MeSH terms

  • Aged
  • Aged, 80 and over
  • Animals
  • Blood Platelets / drug effects
  • Blood Platelets / metabolism
  • Clinical Trials as Topic
  • Extracellular Matrix / drug effects*
  • Extracellular Matrix / genetics
  • Female
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Fibrosis / genetics*
  • Fibrosis / pathology
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL / genetics
  • MicroRNAs / antagonists & inhibitors*
  • MicroRNAs / genetics
  • MicroRNAs / pharmacology*
  • Middle Aged
  • Myocardium / pathology
  • Prospective Studies
  • Proteomics / methods
  • RNA, Untranslated / genetics
  • Transforming Growth Factor beta1 / genetics
  • Wiskott-Aldrich Syndrome Protein / drug effects
  • Wiskott-Aldrich Syndrome Protein / genetics

Substances

  • MIRN21 microRNA, mouse
  • MicroRNAs
  • RNA, Untranslated
  • TGFB1 protein, human
  • Transforming Growth Factor beta1
  • Wiskott-Aldrich Syndrome Protein