The differential affinity of the usher for chaperone-subunit complexes is required for assembly of complete pili

Qinyuan Li, Tony W. Ng, Karen W. Dodson, Stephane Shu Kin So, Ken Michael Bayle, Jerome S. Pinkner, Suzanne Scarlata, Scott J. Hultgren, David G. Thanassi

Research output: Contribution to journalArticle

22 Citations (Scopus)

Abstract

Attachment to host cells via adhesive surface structures is a prerequisite for the pathogenesis of many bacteria. Uropathogenic Escherichia coli assemble P and type 1 pili for attachment to the host urothelium. Assembly of these pili requires the conserved chaperone/usher pathway, in which a periplasmic chaperone controls the folding of pilus subunits and an outer membrane usher provides a platform for pilus assembly and secretion. The usher has differential affinity for pilus subunits, with highest affinity for the tip-localized adhesin. Here, we identify residues F21 and R652 of the P pilus usher PapC as functioning in the differential affinity of the usher. R652 is important for high-affinity binding to the adhesin whereas F21 is important for limiting affinity for the PapA major rod subunit. PapC mutants in these residues are specifically defective for pilus assembly in the presence of PapA, demonstrating that differential affinity of the usher is required for assembly of complete pili. Analysis of PapG deletion mutants demonstrated that the adhesin is not required to initiate P pilus biogenesis. Thus, the differential affinity of the usher may be critical to ensure assembly of functional pilus fibres.

Original languageEnglish (US)
Pages (from-to)159-172
Number of pages14
JournalMolecular Microbiology
Volume76
Issue number1
DOIs
StatePublished - 2010

Fingerprint

Uropathogenic Escherichia coli
Urothelium
Adhesives
Bacteria
Membranes
F21

ASJC Scopus subject areas

  • Molecular Biology
  • Microbiology
  • Medicine(all)

Cite this

The differential affinity of the usher for chaperone-subunit complexes is required for assembly of complete pili. / Li, Qinyuan; Ng, Tony W.; Dodson, Karen W.; So, Stephane Shu Kin; Bayle, Ken Michael; Pinkner, Jerome S.; Scarlata, Suzanne; Hultgren, Scott J.; Thanassi, David G.

In: Molecular Microbiology, Vol. 76, No. 1, 2010, p. 159-172.

Research output: Contribution to journalArticle

Li, Q, Ng, TW, Dodson, KW, So, SSK, Bayle, KM, Pinkner, JS, Scarlata, S, Hultgren, SJ & Thanassi, DG 2010, 'The differential affinity of the usher for chaperone-subunit complexes is required for assembly of complete pili', Molecular Microbiology, vol. 76, no. 1, pp. 159-172. https://doi.org/10.1111/j.1365-2958.2010.07089.x
Li, Qinyuan ; Ng, Tony W. ; Dodson, Karen W. ; So, Stephane Shu Kin ; Bayle, Ken Michael ; Pinkner, Jerome S. ; Scarlata, Suzanne ; Hultgren, Scott J. ; Thanassi, David G. / The differential affinity of the usher for chaperone-subunit complexes is required for assembly of complete pili. In: Molecular Microbiology. 2010 ; Vol. 76, No. 1. pp. 159-172.
@article{c4ff0817087a4bf18e2113f72e04edd2,
title = "The differential affinity of the usher for chaperone-subunit complexes is required for assembly of complete pili",
abstract = "Attachment to host cells via adhesive surface structures is a prerequisite for the pathogenesis of many bacteria. Uropathogenic Escherichia coli assemble P and type 1 pili for attachment to the host urothelium. Assembly of these pili requires the conserved chaperone/usher pathway, in which a periplasmic chaperone controls the folding of pilus subunits and an outer membrane usher provides a platform for pilus assembly and secretion. The usher has differential affinity for pilus subunits, with highest affinity for the tip-localized adhesin. Here, we identify residues F21 and R652 of the P pilus usher PapC as functioning in the differential affinity of the usher. R652 is important for high-affinity binding to the adhesin whereas F21 is important for limiting affinity for the PapA major rod subunit. PapC mutants in these residues are specifically defective for pilus assembly in the presence of PapA, demonstrating that differential affinity of the usher is required for assembly of complete pili. Analysis of PapG deletion mutants demonstrated that the adhesin is not required to initiate P pilus biogenesis. Thus, the differential affinity of the usher may be critical to ensure assembly of functional pilus fibres.",
author = "Qinyuan Li and Ng, {Tony W.} and Dodson, {Karen W.} and So, {Stephane Shu Kin} and Bayle, {Ken Michael} and Pinkner, {Jerome S.} and Suzanne Scarlata and Hultgren, {Scott J.} and Thanassi, {David G.}",
year = "2010",
doi = "10.1111/j.1365-2958.2010.07089.x",
language = "English (US)",
volume = "76",
pages = "159--172",
journal = "Molecular Microbiology",
issn = "0950-382X",
publisher = "Wiley-Blackwell",
number = "1",

}

TY - JOUR

T1 - The differential affinity of the usher for chaperone-subunit complexes is required for assembly of complete pili

AU - Li, Qinyuan

AU - Ng, Tony W.

AU - Dodson, Karen W.

AU - So, Stephane Shu Kin

AU - Bayle, Ken Michael

AU - Pinkner, Jerome S.

AU - Scarlata, Suzanne

AU - Hultgren, Scott J.

AU - Thanassi, David G.

PY - 2010

Y1 - 2010

N2 - Attachment to host cells via adhesive surface structures is a prerequisite for the pathogenesis of many bacteria. Uropathogenic Escherichia coli assemble P and type 1 pili for attachment to the host urothelium. Assembly of these pili requires the conserved chaperone/usher pathway, in which a periplasmic chaperone controls the folding of pilus subunits and an outer membrane usher provides a platform for pilus assembly and secretion. The usher has differential affinity for pilus subunits, with highest affinity for the tip-localized adhesin. Here, we identify residues F21 and R652 of the P pilus usher PapC as functioning in the differential affinity of the usher. R652 is important for high-affinity binding to the adhesin whereas F21 is important for limiting affinity for the PapA major rod subunit. PapC mutants in these residues are specifically defective for pilus assembly in the presence of PapA, demonstrating that differential affinity of the usher is required for assembly of complete pili. Analysis of PapG deletion mutants demonstrated that the adhesin is not required to initiate P pilus biogenesis. Thus, the differential affinity of the usher may be critical to ensure assembly of functional pilus fibres.

AB - Attachment to host cells via adhesive surface structures is a prerequisite for the pathogenesis of many bacteria. Uropathogenic Escherichia coli assemble P and type 1 pili for attachment to the host urothelium. Assembly of these pili requires the conserved chaperone/usher pathway, in which a periplasmic chaperone controls the folding of pilus subunits and an outer membrane usher provides a platform for pilus assembly and secretion. The usher has differential affinity for pilus subunits, with highest affinity for the tip-localized adhesin. Here, we identify residues F21 and R652 of the P pilus usher PapC as functioning in the differential affinity of the usher. R652 is important for high-affinity binding to the adhesin whereas F21 is important for limiting affinity for the PapA major rod subunit. PapC mutants in these residues are specifically defective for pilus assembly in the presence of PapA, demonstrating that differential affinity of the usher is required for assembly of complete pili. Analysis of PapG deletion mutants demonstrated that the adhesin is not required to initiate P pilus biogenesis. Thus, the differential affinity of the usher may be critical to ensure assembly of functional pilus fibres.

UR - http://www.scopus.com/inward/record.url?scp=77950192168&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=77950192168&partnerID=8YFLogxK

U2 - 10.1111/j.1365-2958.2010.07089.x

DO - 10.1111/j.1365-2958.2010.07089.x

M3 - Article

C2 - 20199591

AN - SCOPUS:77950192168

VL - 76

SP - 159

EP - 172

JO - Molecular Microbiology

JF - Molecular Microbiology

SN - 0950-382X

IS - 1

ER -