The pilus usher controls protein interactions via domain masking and is functional as an oligomer

Werneburg, Glenn T.; Li, Huilin; Henderson, Nadine S.; Portnoy, Erica B.; Sarowar, Samema; Hultgren, Scott J.; Thanassi, David G.

doi:10.1038/nsmb.3044

Title: The pilus usher controls protein interactions via domain masking and is functional as an oligomer

Journal Article · Mon Jun 08 00:00:00 EDT 2015 · Nature Structural & Molecular Biology

DOI:https://doi.org/10.1038/nsmb.3044· OSTI ID:1215608

Werneburg, Glenn T. ^[1]; Li, Huilin ^[2]; Henderson, Nadine S. ^[1]; Portnoy, Erica B. ^[1]; Sarowar, Samema ^[2]; Hultgren, Scott J. ^[3]; Thanassi, David G. ^[1]

Stony Brook Univ., Stony Brook, NY (United States)
Stony Brook Univ., Stony Brook, NY (United States); Brookhaven National Lab. (BNL), Upton, NY (United States)
Washington Univ., St. Louis, MO (United States)

The chaperone/usher (CU) pathway is responsible for biogenesis of organelles termed pili or fimbriae in Gram-negative bacteria. Type 1 pili expressed by uropathogenic Escherichia coli are prototypical structures assembled by the CU pathway. Assembly and secretion of pili by the CU pathway requires a dedicated periplasmic chaperone and a multidomain outer membrane protein termed the usher (FimD). We show that the FimD C-terminal domains provide the high-affinity substrate binding site, but that these domains are masked in the resting usher. Domain masking requires the FimD plug domain, which served as a central switch controlling usher activation. In addition, we demonstrate that usher molecules can act in trans for pilus biogenesis, providing conclusive evidence for a functional usher oligomer. These results reveal mechanisms by which molecular machines such as the usher regulate and harness protein-protein interactions, and suggest that ushers may interact in a cooperative manner during pilus assembly in bacteria.

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Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: National Institute of Health

Grant/Contract Number:: SC00112704

OSTI ID:: 1215608

Report Number(s):: BNL-108346-2015-JA; 600301010

Journal Information:: Nature Structural & Molecular Biology, Vol. 22, Issue 7; ISSN 1545-9993

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 16 works

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UroPathogenic Escherichia coli (UPEC) Infections: Virulence Factors, Bladder Responses, Antibiotic, and Non-antibiotic Antimicrobial Strategies Terlizzi, Maria E.; Gribaudo, Giorgio; Maffei, Massimo E. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01566	journal	August 2017
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Electrostatic networks control plug stabilization in the PapC usher Pham, Thieng; Henderson, Nadine S.; Werneburg, Glenn T. Taylor & Francis https://doi.org/10.6084/m9.figshare.3382111	text	January 2020
Electrostatic networks control plug stabilization in the PapC usher Pham, Thieng; Henderson, Nadine S.; Werneburg, Glenn T. Molecular Membrane Biology, Vol. 32, Issue 5-8 https://doi.org/10.3109/09687688.2016.1160450	journal	November 2015
Structural basis for usher activation and intramolecular subunit transfer in P pilus biogenesis in Escherichia coli Omattage, Natalie S.; Deng, Zengqin; Pinkner, Jerome S. Nature Microbiology, Vol. 3, Issue 12 https://doi.org/10.1038/s41564-018-0255-y	journal	October 2018
A comprehensive guide to pilus biogenesis in Gram-negative bacteria Hospenthal, Manuela K.; Costa, Tiago R. D.; Waksman, Gabriel Nature Reviews Microbiology, Vol. 15, Issue 6 https://doi.org/10.1038/nrmicro.2017.40	journal	May 2017
Electrostatic networks control plug stabilization in the PapC usher Pham, Thieng; Henderson, Nadine S.; Werneburg, Glenn T. Taylor & Francis https://doi.org/10.6084/m9.figshare.3382111.v2	text	January 2020
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