Structural insight and characterization of human Twinkle helicase in mitochondrial disease

Proc Natl Acad Sci U S A. 2022 Aug 9;119(32):e2207459119. doi: 10.1073/pnas.2207459119. Epub 2022 Aug 1.

Abstract

Twinkle is the mammalian helicase vital for replication and integrity of mitochondrial DNA. Over 90 Twinkle helicase disease variants have been linked to progressive external ophthalmoplegia and ataxia neuropathies among other mitochondrial diseases. Despite the biological and clinical importance, Twinkle represents the only remaining component of the human minimal mitochondrial replisome that has yet to be structurally characterized. Here, we present 3-dimensional structures of human Twinkle W315L. Employing cryo-electron microscopy (cryo-EM), we characterize the oligomeric assemblies of human full-length Twinkle W315L, define its multimeric interface, and map clinical variants associated with Twinkle in inherited mitochondrial disease. Cryo-EM, crosslinking-mass spectrometry, and molecular dynamics simulations provide insight into the dynamic movement and molecular consequences of the W315L clinical variant. Collectively, this ensemble of structures outlines a framework for studying Twinkle function in mitochondrial DNA replication and associated disease states.

Keywords: Twinkle helicase; cryo-electron microscopy; mitochondrial DNA; mitochondrial DNA replication; progressive external ophthalmoplegia.

Publication types

  • Research Support, N.I.H., Intramural
  • Research Support, N.I.H., Extramural

MeSH terms

  • Cryoelectron Microscopy*
  • DNA Helicases* / chemistry
  • DNA Helicases* / genetics
  • DNA Helicases* / metabolism
  • DNA Helicases* / ultrastructure
  • DNA Replication
  • DNA, Mitochondrial / biosynthesis
  • Humans
  • Mass Spectrometry
  • Mitochondrial Diseases* / genetics
  • Mitochondrial Proteins* / chemistry
  • Mitochondrial Proteins* / genetics
  • Mitochondrial Proteins* / metabolism
  • Mitochondrial Proteins* / ultrastructure
  • Molecular Dynamics Simulation
  • Mutant Proteins / chemistry
  • Mutant Proteins / genetics
  • Mutant Proteins / metabolism
  • Mutant Proteins / ultrastructure
  • Protein Multimerization*

Substances

  • DNA, Mitochondrial
  • Mitochondrial Proteins
  • Mutant Proteins
  • DNA Helicases
  • TWNK protein, human