Recurrent SMARCB1 Mutations Reveal a Nucleosome Acidic Patch Interaction Site That Potentiates mSWI/SNF Complex Chromatin Remodeling

Cell. 2019 Nov 27;179(6):1342-1356.e23. doi: 10.1016/j.cell.2019.10.044. Epub 2019 Nov 20.

Abstract

Mammalian switch/sucrose non-fermentable (mSWI/SNF) complexes are multi-component machines that remodel chromatin architecture. Dissection of the subunit- and domain-specific contributions to complex activities is needed to advance mechanistic understanding. Here, we examine the molecular, structural, and genome-wide regulatory consequences of recurrent, single-residue mutations in the putative coiled-coil C-terminal domain (CTD) of the SMARCB1 (BAF47) subunit, which cause the intellectual disability disorder Coffin-Siris syndrome (CSS), and are recurrently found in cancers. We find that the SMARCB1 CTD contains a basic α helix that binds directly to the nucleosome acidic patch and that all CSS-associated mutations disrupt this binding. Furthermore, these mutations abrogate mSWI/SNF-mediated nucleosome remodeling activity and enhancer DNA accessibility without changes in genome-wide complex localization. Finally, heterozygous CSS-associated SMARCB1 mutations result in dominant gene regulatory and morphologic changes during iPSC-neuronal differentiation. These studies unmask an evolutionarily conserved structural role for the SMARCB1 CTD that is perturbed in human disease.

Keywords: ATP-dependent chromatin remodeling; BAF complex; Coffin-Siris syndrome; SMARCB1 (BAF47); chromatin accessibility; intellectual disability; mammalian SWI/SNF complexes; nucleosome acidic patch; nucleosome remodeling; structure.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Chromatin Assembly and Disassembly / genetics*
  • Chromosomal Proteins, Non-Histone / metabolism*
  • Enhancer Elements, Genetic / genetics
  • Female
  • Genome, Human
  • HEK293 Cells
  • HeLa Cells
  • Heterozygote
  • Humans
  • Male
  • Models, Molecular
  • Mutant Proteins / chemistry
  • Mutant Proteins / metabolism
  • Mutation / genetics*
  • Nucleosomes / metabolism*
  • Protein Binding
  • Protein Domains
  • SMARCB1 Protein / chemistry
  • SMARCB1 Protein / genetics*
  • SMARCB1 Protein / metabolism
  • Transcription Factors / metabolism*

Substances

  • Chromosomal Proteins, Non-Histone
  • Mutant Proteins
  • Nucleosomes
  • SMARCB1 Protein
  • SMARCB1 protein, human
  • SWI-SNF-B chromatin-remodeling complex
  • Transcription Factors