The pilus usher controls protein interactions via domain masking and is functional as an oligomer
Abstract
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.
- Authors:
-
- 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)
- Publication Date:
- Research Org.:
- Brookhaven National Laboratory (BNL), Upton, NY (United States)
- Sponsoring Org.:
- National Institute of Health
- OSTI Identifier:
- 1215608
- Report Number(s):
- BNL-108346-2015-JA
Journal ID: ISSN 1545-9993; 600301010
- Grant/Contract Number:
- SC00112704
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Structural & Molecular Biology
- Additional Journal Information:
- Journal Volume: 22; Journal Issue: 7; Journal ID: ISSN 1545-9993
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; membrane proteins; pathogens; protein translocation
Citation Formats
Werneburg, Glenn T., Li, Huilin, Henderson, Nadine S., Portnoy, Erica B., Sarowar, Samema, Hultgren, Scott J., and Thanassi, David G. The pilus usher controls protein interactions via domain masking and is functional as an oligomer. United States: N. p., 2015.
Web. doi:10.1038/nsmb.3044.
Werneburg, Glenn T., Li, Huilin, Henderson, Nadine S., Portnoy, Erica B., Sarowar, Samema, Hultgren, Scott J., & Thanassi, David G. The pilus usher controls protein interactions via domain masking and is functional as an oligomer. United States. https://doi.org/10.1038/nsmb.3044
Werneburg, Glenn T., Li, Huilin, Henderson, Nadine S., Portnoy, Erica B., Sarowar, Samema, Hultgren, Scott J., and Thanassi, David G. Mon .
"The pilus usher controls protein interactions via domain masking and is functional as an oligomer". United States. https://doi.org/10.1038/nsmb.3044. https://www.osti.gov/servlets/purl/1215608.
@article{osti_1215608,
title = {The pilus usher controls protein interactions via domain masking and is functional as an oligomer},
author = {Werneburg, Glenn T. and Li, Huilin and Henderson, Nadine S. and Portnoy, Erica B. and Sarowar, Samema and Hultgren, Scott J. and Thanassi, David G.},
abstractNote = {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.},
doi = {10.1038/nsmb.3044},
journal = {Nature Structural & Molecular Biology},
number = 7,
volume = 22,
place = {United States},
year = {Mon Jun 08 00:00:00 EDT 2015},
month = {Mon Jun 08 00:00:00 EDT 2015}
}
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