A Membrane-Tethered Ubiquitination Pathway Regulates Hedgehog Signaling and Heart Development

Dev Cell. 2020 Nov 23;55(4):432-449.e12. doi: 10.1016/j.devcel.2020.08.012. Epub 2020 Sep 22.

Abstract

The etiology of congenital heart defects (CHDs), which are among the most common human birth defects, is poorly understood because of its complex genetic architecture. Here, we show that two genes implicated in CHDs, Megf8 and Mgrn1, interact genetically and biochemically to regulate the strength of Hedgehog signaling in target cells. MEGF8, a transmembrane protein, and MGRN1, a RING superfamily E3 ligase, assemble to form a receptor-like ubiquitin ligase complex that catalyzes the ubiquitination and degradation of the Hedgehog pathway transducer Smoothened. Homozygous Megf8 and Mgrn1 mutations increased Smoothened abundance and elevated sensitivity to Hedgehog ligands. While mice heterozygous for loss-of-function Megf8 or Mgrn1 mutations were normal, double heterozygous embryos exhibited an incompletely penetrant syndrome of CHDs with heterotaxy. Thus, genetic interactions can arise from biochemical mechanisms that calibrate morphogen signaling strength, a conclusion broadly relevant for the many human diseases in which oligogenic inheritance is emerging as a mechanism for heritability.

Keywords: Hedgehog signaling; Smoothened; congenital heart disease; heart development; heterotaxy; left-right patterning; morphogen; oligogenic inheritance; primary cilia; ubiquitin.

Publication types

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

MeSH terms

  • Alleles
  • Animals
  • Embryo, Mammalian / metabolism
  • Epistasis, Genetic
  • Gene Dosage
  • Heart / embryology*
  • Hedgehog Proteins / metabolism*
  • Membrane Proteins / metabolism
  • Mice
  • Mutation / genetics
  • NIH 3T3 Cells
  • Phenotype
  • Protein Binding
  • Signal Transduction*
  • Smoothened Receptor / metabolism
  • Ubiquitin-Protein Ligases / metabolism
  • Ubiquitination*

Substances

  • Hedgehog Proteins
  • MEGF8 protein, mouse
  • Membrane Proteins
  • Smo protein, mouse
  • Smoothened Receptor
  • E3 ubiquitin ligase RNF157, mouse
  • Mgrn1 protein, mouse
  • Ubiquitin-Protein Ligases