Structure of the branched intermediate in protein splicing

Proc Natl Acad Sci U S A. 2014 Jun 10;111(23):8422-7. doi: 10.1073/pnas.1402942111. Epub 2014 Apr 28.

Abstract

Inteins are autoprocessing domains that cut themselves out of host proteins in a traceless manner. This process, known as protein splicing, involves multiple chemical steps that must be coordinated to ensure fidelity in the process. The committed step in splicing involves attack of a conserved Asn side-chain amide on the adjacent backbone amide, leading to an intein-succinimide product and scission of that peptide bond. This cleavage reaction is stimulated by formation of a branched intermediate in the splicing process. The mechanism by which the Asn side-chain becomes activated as a nucleophile is not understood. Here we solve the crystal structure of an intein trapped in the branched intermediate step in protein splicing. Guided by this structure, we use protein-engineering approaches to show that intein-succinimide formation is critically dependent on a backbone-to-side-chain hydrogen-bond. We propose that this interaction serves to both position the side-chain amide for attack and to activate its nitrogen as a nucleophile. Collectively, these data provide an unprecedented view of an intein poised to carry out the rate-limiting step in protein splicing, shedding light on how a nominally nonnucleophilic group, a primary amide, can become activated in a protein active site.

Keywords: expressed; protein semisynthesis.

Publication types

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

MeSH terms

  • Amides / chemistry
  • Amides / metabolism
  • Amino Acid Sequence
  • Asparagine / chemistry
  • Asparagine / genetics
  • Asparagine / metabolism
  • Catalytic Domain
  • DNA Gyrase / chemistry
  • DNA Gyrase / genetics
  • DNA Gyrase / metabolism
  • Electrophoresis, Polyacrylamide Gel
  • Exteins / genetics*
  • Hydrogen Bonding
  • Inteins / genetics*
  • Kinetics
  • Models, Molecular
  • Molecular Sequence Data
  • Molecular Structure
  • Mutation
  • Protein Splicing*
  • Protein Structure, Secondary
  • Protein Structure, Tertiary
  • Proteins / chemistry
  • Proteins / genetics*
  • Proteins / metabolism
  • Spectrometry, Mass, Electrospray Ionization

Substances

  • Amides
  • Proteins
  • Asparagine
  • DNA Gyrase

Associated data

  • PDB/4OZ6