The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site

EMBO J. 2002 Mar 1;21(5):885-97. doi: 10.1093/emboj/21.5.885.

Abstract

Cell attachment and membrane penetration are functions of the rotavirus outer capsid spike protein, VP4. An activating tryptic cleavage of VP4 produces the N-terminal fragment, VP8*, which is the viral hemagglutinin and an important target of neutralizing antibodies. We have determined, by X-ray crystallography, the atomic structure of the VP8* core bound to sialic acid and, by NMR spectroscopy, the structure of the unliganded VP8* core. The domain has the beta-sandwich fold of the galectins, a family of sugar binding proteins. The surface corresponding to the galectin carbohydrate binding site is blocked, and rotavirus VP8* instead binds sialic acid in a shallow groove between its two beta-sheets. There appears to be a small induced fit on binding. The residues that contact sialic acid are conserved in sialic acid-dependent rotavirus strains. Neutralization escape mutations are widely distributed over the VP8* surface and cluster in four epitopes. From the fit of the VP8* core into the virion spikes, we propose that VP4 arose from the insertion of a host carbohydrate binding domain into a viral membrane interaction protein.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Amino Acid Sequence
  • Binding Sites
  • Capsid / chemistry*
  • Capsid / physiology
  • Capsid Proteins*
  • Carbohydrate Metabolism*
  • Consensus Sequence
  • Crystallography, X-Ray
  • Epitopes / chemistry
  • Evolution, Molecular
  • Galectins
  • Hemagglutinins / chemistry
  • Hemagglutinins, Viral / biosynthesis
  • Hemagglutinins, Viral / chemistry
  • Hydrogen Bonding
  • Models, Molecular
  • Molecular Sequence Data
  • N-Acetylneuraminic Acid / metabolism*
  • Nuclear Magnetic Resonance, Biomolecular
  • Peptide Fragments / chemistry
  • Protein Binding
  • Protein Conformation
  • Protein Folding
  • Protein Structure, Secondary
  • Protein Structure, Tertiary
  • RNA-Binding Proteins / biosynthesis
  • RNA-Binding Proteins / chemistry
  • Recombinant Fusion Proteins / chemistry
  • Rotavirus / chemistry*
  • Rotavirus / physiology
  • Structure-Activity Relationship
  • Substrate Specificity
  • Viral Nonstructural Proteins / biosynthesis
  • Viral Nonstructural Proteins / chemistry
  • Virion / chemistry
  • Virion / ultrastructure

Substances

  • Capsid Proteins
  • Epitopes
  • Galectins
  • Hemagglutinins
  • Hemagglutinins, Viral
  • Peptide Fragments
  • RNA-Binding Proteins
  • Recombinant Fusion Proteins
  • VP4 protein, Rotavirus
  • Viral Nonstructural Proteins
  • nsp1 protein, Rotavirus
  • NS35 protein, rotavirus
  • N-Acetylneuraminic Acid

Associated data

  • PDB/1KRI