Equilibrium folding of pro-HlyA from Escherichia coli reveals a stable calcium ion dependent folding intermediate

Biochim Biophys Acta. 2014 Sep;1844(9):1500-10. doi: 10.1016/j.bbapap.2014.05.006. Epub 2014 May 24.

Abstract

HlyA from Escherichia coli is a member of the repeats in toxin (RTX) protein family, produced by a wide range of Gram-negative bacteria and secreted by a dedicated Type 1 Secretion System (T1SS). RTX proteins are thought to be secreted in an unfolded conformation and to fold upon secretion by Ca(2+) binding. However, the exact mechanism of secretion, ion binding and folding to the correct native state remains largely unknown. In this study we provide an easy protocol for high-level pro-HlyA purification from E. coli. Equilibrium folding studies, using intrinsic tryptophan fluorescence, revealed the well-known fact that Ca(2+) is essential for stability as well as correct folding of the whole protein. In the absence of Ca(2+), pro-HlyA adopts a non-native conformation. Such molecules could however be rescued by Ca(2+) addition, indicating that these are not dead-end species and that Ca(2+) drives pro-HlyA folding. More importantly, pro-HlyA unfolded via a two-state mechanism, whereas folding was a three-state process. The latter is indicative of the presence of a stable folding intermediate. Analysis of deletion and Trp mutants revealed that the first folding transition, at 6-7M urea, relates to Ca(2+) dependent structural changes at the extreme C-terminus of pro-HlyA, sensed exclusively by Trp914. Since all Trp residues of HlyA are located outside the RTX domain, our results demonstrate that Ca(2+) induced folding is not restricted to the RTX domain. Taken together, Ca(2+) binding to the pro-HlyA RTX domain is required to drive the folding of the entire protein to its native conformation.

Keywords: Calcium; Folding mechanics; HlyA; Protein folding; RTX; Tryptophan fluorescence.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Secretion Systems / physiology
  • Calcium / chemistry*
  • Escherichia coli / chemistry
  • Escherichia coli / genetics
  • Escherichia coli / metabolism*
  • Escherichia coli Proteins / chemistry*
  • Escherichia coli Proteins / genetics
  • Escherichia coli Proteins / metabolism
  • Gene Expression
  • Hemolysin Proteins / chemistry*
  • Hemolysin Proteins / genetics
  • Hemolysin Proteins / metabolism
  • Kinetics
  • Mutation
  • Protein Binding
  • Protein Folding
  • Protein Precursors / chemistry*
  • Protein Precursors / genetics
  • Protein Precursors / metabolism
  • Protein Structure, Secondary
  • Protein Structure, Tertiary
  • Spectrometry, Fluorescence
  • Thermodynamics
  • Tryptophan / chemistry
  • Urea / chemistry

Substances

  • Bacterial Secretion Systems
  • Escherichia coli Proteins
  • Hemolysin Proteins
  • Hlya protein, E coli
  • Protein Precursors
  • Tryptophan
  • Urea
  • Calcium