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microRNA overexpression in slow transit constipation leads to reduced NaV1.5 current and altered smooth muscle contractility

Gut. 2020 May;69(5):868-876. doi: 10.1136/gutjnl-2019-318747. Epub 2019 Nov 22.

Abstract

Objective: This study was designed to evaluate the roles of microRNAs (miRNAs) in slow transit constipation (STC).

Design: All human tissue samples were from the muscularis externa of the colon. Expression of 372 miRNAs was examined in a discovery cohort of four patients with STC versus three age/sex-matched controls by a quantitative PCR array. Upregulated miRNAs were examined by quantitative reverse transcription qPCR (RT-qPCR) in a validation cohort of seven patients with STC and age/sex-matched controls. The effect of a highly differentially expressed miRNA on a custom human smooth muscle cell line was examined in vitro by RT-qPCR, electrophysiology, traction force microscopy, and ex vivo by lentiviral transduction in rat muscularis externa organotypic cultures.

Results: The expression of 13 miRNAs was increased in STC samples. Of those miRNAs, four were predicted to target SCN5A, the gene that encodes the Na+ channel NaV1.5. The expression of SCN5A mRNA was decreased in STC samples. Let-7f significantly decreased Na+ current density in vitro in human smooth muscle cells. In rat muscularis externa organotypic cultures, overexpression of let-7f resulted in reduced frequency and amplitude of contraction.

Conclusions: A small group of miRNAs is upregulated in STC, and many of these miRNAs target the SCN5A-encoded Na+ channel NaV1.5. Within this set, a novel NaV1.5 regulator, let-7f, resulted in decreased NaV1.5 expression, current density and reduced motility of GI smooth muscle. These results suggest NaV1.5 and miRNAs as novel diagnostic and potential therapeutic targets in STC.

Keywords: constipation; genetics; intestinal ion transport; intestinal motility; motility disorders.

Publication types

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

MeSH terms

  • Adult
  • Aged
  • Biopsy, Needle
  • Case-Control Studies
  • Colon / pathology
  • Constipation / physiopathology*
  • Female
  • Gastrointestinal Motility / genetics
  • Gene Expression Regulation*
  • Humans
  • Immunohistochemistry
  • MicroRNAs / genetics*
  • Microtubule-Associated Proteins / genetics*
  • Middle Aged
  • Muscle Contraction / genetics*
  • Muscle Contraction / physiology
  • Muscle, Smooth
  • RNA, Messenger / genetics
  • Real-Time Polymerase Chain Reaction / methods
  • Reference Values
  • Sampling Studies
  • Up-Regulation

Substances

  • MicroRNAs
  • Microtubule-Associated Proteins
  • NAV1 protein, human
  • RNA, Messenger