Desert hedgehog-primary cilia cross talk shapes mitral valve tissue by organizing smooth muscle actin

Dev Biol. 2020 Jul 1;463(1):26-38. doi: 10.1016/j.ydbio.2020.03.003. Epub 2020 Mar 6.

Abstract

Non-syndromic mitral valve prolapse (MVP) is the most common heart valve disease affecting 2.4% of the population. Recent studies have identified genetic defects in primary cilia as causative to MVP, although the mechanism of their action is currently unknown. Using a series of gene inactivation approaches, we define a paracrine mechanism by which endocardially-expressed Desert Hedgehog (DHH) activates primary cilia signaling on neighboring valve interstitial cells. High-resolution imaging and functional assays show that DHH de-represses smoothened at the primary cilia, resulting in kinase activation of RAC1 through the RAC1-GEF, TIAM1. Activation of this non-canonical hedgehog pathway stimulates α-smooth actin organization and ECM remodeling. Genetic or pharmacological perturbation of this pathway results in enlarged valves that progress to a myxomatous phenotype, similar to valves seen in MVP patients. These data identify a potential molecular origin for MVP as well as establish a paracrine DHH-primary cilium cross-talk mechanism that is likely applicable across developmental tissue types.

Keywords: Desert hedgehog signaling; Myxomatous degeneration; Primary cilia; Valve development.

Publication types

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

MeSH terms

  • Actins / metabolism
  • Animals
  • Cilia / metabolism*
  • Extracellular Matrix / metabolism
  • Heart Valve Diseases
  • Hedgehog Proteins / metabolism*
  • Hedgehog Proteins / physiology
  • Mice
  • Mitral Valve / embryology*
  • Mitral Valve Prolapse / genetics
  • Mitral Valve Prolapse / metabolism
  • Muscle, Smooth / metabolism
  • Muscle, Smooth / physiology
  • Myocytes, Smooth Muscle / metabolism
  • Neuropeptides / metabolism
  • Phenotype
  • Signal Transduction
  • Transcription Factors / metabolism
  • rac1 GTP-Binding Protein / metabolism

Substances

  • Actins
  • Hedgehog Proteins
  • Neuropeptides
  • Rac1 protein, mouse
  • Transcription Factors
  • rac1 GTP-Binding Protein