Roles of Periplasmic Chaperone Proteins in the Biogenesis of Serine Protease Autotransporters of Enterobacteriaceae
10.1128/jb.00754-09
Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

ABSTRACT The serine protease autotransporters of Enterobacteriaceae (SPATEs) represent a large family of virulence factors. The prevailing model for autotransporter secretion comprises entry to the periplasm via the Sec apparatus, followed by an obscure series of steps in which the C terminus of the periplasmic species inserts into the outer membrane as a β-barrel protein, accompanied by translocation of the passenger domain to the bacterial cell surface. Little is known about the fate of the autotransporter proteins in the periplasm, including whether accessory periplasmic proteins are involved in translocation to the external milieu. Here we studied the role of the major periplasmic chaperones in the biogenesis of EspP, a prototype SPATE protein produced by Escherichia coli O157:H7. The yeast two-hybrid approach, secretion analysis of chaperone mutant strains, and surface plasmon resonance analysis (SPR) revealed direct protein-protein interactions between the periplasmic SurA and DegP chaperones and either the EspP-β or EspP passenger domains. The secretion of EspP was moderately reduced in the surA and skp mutant strains but severely impaired in the degP background. Site-directed mutagenesis of highly conserved aromatic amino acid residues in the SPATE family resulted in ∼80% reduction of EspP secretion. Synthetic peptides containing aromatic residues derived from the EspP passenger domain blocked DegP and SurA binding to the passenger domain. SPR suggested direct protein-protein interaction between periplasmic chaperones and the unfolded EspP passenger domain. Our data suggest that translocation of AT proteins may require accessory factors, calling into question the moniker “autotransporter.”

Bibliography

Ruiz-Perez, F., Henderson, I. R., Leyton, D. L., Rossiter, A. E., Zhang, Y., & Nataro, J. P. (2009). Roles of Periplasmic Chaperone Proteins in the Biogenesis of Serine Protease Autotransporters of Enterobacteriaceae. Journal of Bacteriology, 191(21), 6571–6583.

Authors 6
  1. Fernando Ruiz-Perez (first)
  2. Ian R. Henderson (additional)
  3. Denisse L. Leyton (additional)
  4. Amanda E. Rossiter (additional)
  5. Yinghua Zhang (additional)
  6. James P. Nataro (additional)
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Dates
Type When
Created 15 years, 11 months ago (Sept. 4, 2009, 10:09 p.m.)
Deposited 4 years, 1 month ago (July 29, 2021, 1:09 p.m.)
Indexed 4 weeks ago (Aug. 5, 2025, 8:39 a.m.)
Issued 15 years, 10 months ago (Nov. 1, 2009)
Published 15 years, 10 months ago (Nov. 1, 2009)
Published Print 15 years, 10 months ago (Nov. 1, 2009)
Funders 0

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@article{Ruiz_Perez_2009, title={Roles of Periplasmic Chaperone Proteins in the Biogenesis of Serine Protease Autotransporters of Enterobacteriaceae}, volume={191}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.00754-09}, DOI={10.1128/jb.00754-09}, number={21}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Ruiz-Perez, Fernando and Henderson, Ian R. and Leyton, Denisse L. and Rossiter, Amanda E. and Zhang, Yinghua and Nataro, James P.}, year={2009}, month=nov, pages={6571–6583} }