Allosteric catch bond properties of the fimh adhesin from Salmonella enterica serovar typhimurium

Dagmara I. Kisiela, Jeremy J. Kramer, Veronika Tchesnokova, Pavel Aprikian, Vladimir Yarov-Yarovoy, Steven Clegg, Evgeni V. Sokurenko

Research output: Contribution to journalArticle

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Abstract

Despite sharing the name and the ability to mediate mannosesensitive adhesion, the type 1 fimbrial FimH adhesins of Salmonella Typhimurium and Escherichia coli share only 15% sequence identity. In the present study, we demonstrate that even with this limited identity in primary sequence, these two proteins share remarkable similarity of complex receptor binding and structural properties. In silico simulations suggest that, like E. coli FimH, Salmonella FimH has a two-domain tertiary structure topology, with a mannose-binding pocket located on the apex of a lectin domain. Structural analysis of mutations that enhance S. Typhimurium FimH binding to eukaryotic cells and mannose-BSA demonstrated that they are not located proximal to the predicted mannose-binding pocket but rather occur in the vicinity of the predicted interface between the lectin and pilin domains of the adhesin. This implies that the functional effect of such mutations is indirect and probably allosteric in nature. By analogy with E. coli FimH, we suggest that Salmonella FimH functions as an allosteric catch bond adhesin, where shear-induced separation of the lectin and pilin domains results in a shift from a low affinity to a high affinity binding conformation of the lectin domain. Indeed, we observed shear-enhanced binding of whole bacteria expressing S. Typhimurium type 1 fimbriae. In addition, we observed that anti-FimH antibodies activate rather than inhibit S. Typhimurium FimH mannose binding, consistent with the allosteric catch bond properties of this adhesin.

Original languageEnglish (US)
Pages (from-to)38136-38147
Number of pages12
JournalJournal of Biological Chemistry
Volume286
Issue number44
DOIs
StatePublished - Nov 4 2011
Externally publishedYes

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Salmonella enterica
Salmonella typhimurium
Lectins
Mannose
Fimbriae Proteins
Escherichia coli
Salmonella
Bacterial Adhesins
Mutation
Eukaryotic Cells
Structural analysis
Computer Simulation
Names
Conformations
Structural properties
Anti-Idiotypic Antibodies
Bacteria
Adhesion
Topology
Serogroup

ASJC Scopus subject areas

  • Biochemistry
  • Cell Biology
  • Molecular Biology

Cite this

Kisiela, D. I., Kramer, J. J., Tchesnokova, V., Aprikian, P., Yarov-Yarovoy, V., Clegg, S., & Sokurenko, E. V. (2011). Allosteric catch bond properties of the fimh adhesin from Salmonella enterica serovar typhimurium. Journal of Biological Chemistry, 286(44), 38136-38147. https://doi.org/10.1074/jbc.M111.237511

Allosteric catch bond properties of the fimh adhesin from Salmonella enterica serovar typhimurium. / Kisiela, Dagmara I.; Kramer, Jeremy J.; Tchesnokova, Veronika; Aprikian, Pavel; Yarov-Yarovoy, Vladimir; Clegg, Steven; Sokurenko, Evgeni V.

In: Journal of Biological Chemistry, Vol. 286, No. 44, 04.11.2011, p. 38136-38147.

Research output: Contribution to journalArticle

Kisiela, DI, Kramer, JJ, Tchesnokova, V, Aprikian, P, Yarov-Yarovoy, V, Clegg, S & Sokurenko, EV 2011, 'Allosteric catch bond properties of the fimh adhesin from Salmonella enterica serovar typhimurium', Journal of Biological Chemistry, vol. 286, no. 44, pp. 38136-38147. https://doi.org/10.1074/jbc.M111.237511
Kisiela, Dagmara I. ; Kramer, Jeremy J. ; Tchesnokova, Veronika ; Aprikian, Pavel ; Yarov-Yarovoy, Vladimir ; Clegg, Steven ; Sokurenko, Evgeni V. / Allosteric catch bond properties of the fimh adhesin from Salmonella enterica serovar typhimurium. In: Journal of Biological Chemistry. 2011 ; Vol. 286, No. 44. pp. 38136-38147.
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