FSHD2- and BAMS-associated mutations confer opposing effects on SMCHD1 function

J Biol Chem. 2018 Jun 22;293(25):9841-9853. doi: 10.1074/jbc.RA118.003104. Epub 2018 May 10.

Abstract

Structural maintenance of chromosomes flexible hinge domain-containing 1 (Smchd1) plays important roles in epigenetic silencing and normal mammalian development. Recently, heterozygous mutations in SMCHD1 have been reported in two disparate disorders: facioscapulohumeral muscular dystrophy type 2 (FSHD2) and Bosma arhinia microphthalmia syndrome (BAMS). FSHD2-associated mutations lead to loss of function; however, whether BAMS is associated with loss- or gain-of-function mutations in SMCHD1 is unclear. Here, we have assessed the effect of SMCHD1 missense mutations from FSHD2 and BAMS patients on ATP hydrolysis activity and protein conformation and the effect of BAMS mutations on craniofacial development in a Xenopus model. These data demonstrated that FSHD2 mutations only result in decreased ATP hydrolysis, whereas many BAMS mutations can result in elevated ATPase activity and decreased eye size in Xenopus Interestingly, a mutation reported in both an FSHD2 patient and a BAMS patient results in increased ATPase activity and a smaller Xenopus eye size. Mutations in the extended ATPase domain increased catalytic activity, suggesting critical regulatory intramolecular interactions and the possibility of targeting this region therapeutically to boost SMCHD1's activity to counter FSHD.

Keywords: ATPase; SMC; Xenopus; craniofacial development; epigenetics; hinge domain; muscular dystrophy; small-angle X-ray scattering (SAXS).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphatases
  • Adenosine Triphosphate / metabolism*
  • Amino Acid Sequence
  • Animals
  • Choanal Atresia / genetics*
  • Choanal Atresia / pathology
  • Chromosomal Proteins, Non-Histone / chemistry*
  • Chromosomal Proteins, Non-Histone / genetics
  • Chromosomal Proteins, Non-Histone / metabolism*
  • Crystallography, X-Ray
  • Eye Diseases / genetics
  • Eye Diseases / metabolism
  • Eye Diseases / pathology*
  • Humans
  • Mice
  • Microphthalmos / genetics*
  • Microphthalmos / pathology
  • Muscular Dystrophy, Facioscapulohumeral / genetics*
  • Muscular Dystrophy, Facioscapulohumeral / pathology
  • Mutation, Missense*
  • Nose / abnormalities*
  • Nose / pathology
  • Protein Conformation
  • Protein Domains
  • Sequence Homology
  • Xenopus laevis

Substances

  • Chromosomal Proteins, Non-Histone
  • SmcHD1 protein, mouse
  • Adenosine Triphosphate
  • Adenosine Triphosphatases

Supplementary concepts

  • Arhinia, choanal atresia, and microphthalmia

Associated data

  • PDB/2CG9