A novel "clip-and-link" activity of repeat in toxin (RTX) proteins from gram-negative pathogens. Covalent protein cross-linking by an Asp-Lys isopeptide bond upon calcium-dependent processing at an Asp-Pro bond

J Biol Chem. 2004 Jun 11;279(24):24944-56. doi: 10.1074/jbc.M314013200. Epub 2004 Mar 24.

Abstract

Clinical isolates of Neisseria meningitidis produce a repeat in toxin (RTX) protein, FrpC, of unknown biological activity. Here we show that physiological concentrations of calcium ions induce a novel type of autocatalytic cleavage of the peptide bond between residues Asp(414) and Pro(415) of FrpC that is insensitive to inhibitors of serine, cysteine, aspartate, and metalloproteases. Moreover, as a result of processing, the newly generated amino-terminal fragment of FrpC can be covalently linked to another protein molecule by a novel type of Asp-Lys isopeptide bond that forms between the carboxyl group of its carboxyl-terminal Asp(414) residue and the epsilon-amino group of an internal lysine of another FrpC molecule. Point substitutions of negatively charged residues possibly involved in calcium binding (D499K, D510A, D521K, and E532A) dramatically reduced the self-processing activity of FrpC. The segment necessary and sufficient for FrpC processing was localized by deletion mutagenesis within residues 400-657, and sequences homologous to this segment were identified in several other RTX proteins. The same type of calcium-dependent processing and cross-linking activity was observed also for the purified ApxIVA protein of Actinobacillus pleuropneumoniae. These results define a protein cleavage and cross-linking module of a new class of RTX proteins of Gram-negative pathogens of man, animals, and plants. In the calcium-rich environments colonized by these bacteria this novel activity is likely to be of biological importance.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / metabolism
  • Calcium / pharmacology*
  • Catalysis
  • Cytotoxins / chemistry*
  • Cytotoxins / metabolism
  • Gram-Negative Bacteria / pathogenicity*
  • Membrane Proteins / chemistry*
  • Membrane Proteins / metabolism
  • Molecular Sequence Data
  • Molecular Weight
  • Tosyllysine Chloromethyl Ketone / pharmacology
  • Tosylphenylalanyl Chloromethyl Ketone / pharmacology

Substances

  • Bacterial Proteins
  • Cytotoxins
  • Membrane Proteins
  • frpC protein, Neisseria meningitidis
  • Tosyllysine Chloromethyl Ketone
  • Tosylphenylalanyl Chloromethyl Ketone
  • Calcium