PilN binding modulates the structure and binding partners of the Pseudomonas aeruginosa type IVa pilus protein PilM
Abstract
Pseudomonas aeruginosa is an opportunistic bacterial pathogen that expresses type IVa pili. The pilus assembly system, which promotes surface-associated twitching motility and virulence, is composed of inner and outer membrane subcomplexes, connected by an alignment subcomplex composed of PilMNOP. PilM binds to the N terminus of PilN, and we hypothesize that this interaction causes functionally significant structural changes in PilM. To characterize this interaction, we determined the crystal structures of PilM and a PilM chimera where PilM was fused to the first 12 residues of PilN (PilM·PilN(1–12)). Structural analysis, multiangle light scattering coupled with size exclusion chromatography, and bacterial two-hybrid data revealed that PilM forms dimers mediated by the binding of a novel conserved motif in the N terminus of PilM, and binding PilN abrogates this binding interface, resulting in PilM monomerization. Structural comparison of PilM with PilM·PilN(1–12) revealed that upon PilN binding, there is a large domain closure in PilM that alters its ATP binding site. Using biolayer interferometry, we found that the association rate of PilN with PilM is higher in the presence of ATP compared with ADP. Bacterial two-hybrid data suggested the connectivity of the cytoplasmic and inner membrane components of the type IVa pilus machinery inmore »
- Authors:
-
- Univ. of Toronto, Toronto, ON (Canada); Hospital for Sick Children, Toronto, ON (Canada)
- Hospital for Sick Children, Toronto, ON (Canada)
- Brookhaven National Lab. (BNL), Upton, NY (United States)
- Univ. of Toronto, Toronto, ON (Canada)
- McMaster Univ., Hamilton, ON (Canada); Hospital for Sick Children, Toronto, ON (Canada)
- Publication Date:
- Research Org.:
- Brookhaven National Laboratory (BNL), Upton, NY (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1340346
- Report Number(s):
- BNL-112064-2016-JA
Journal ID: ISSN 0021-9258
- Grant/Contract Number:
- SC00112704
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Biological Chemistry
- Additional Journal Information:
- Journal Volume: 291; Journal Issue: 21; Journal ID: ISSN 0021-9258
- Publisher:
- American Society for Biochemistry and Molecular Biology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 36 MATERIALS SCIENCE; ligand-binding protein; protein chimera; Pseudomonas aeruginosa (P. aeruginosa); type IV pili; x-ray crystallography; PilM; PilN
Citation Formats
McCallum, Matthew, Tammam, Stephanie, Little, Dustin J., Robinson, Howard, Koo, Jason, Shah, Megha, Calmettes, Charles, Moraes, Trevor F., Burrows, Lori L., and Howell, P. Lynne. PilN binding modulates the structure and binding partners of the Pseudomonas aeruginosa type IVa pilus protein PilM. United States: N. p., 2016.
Web. doi:10.1074/jbc.M116.718353.
McCallum, Matthew, Tammam, Stephanie, Little, Dustin J., Robinson, Howard, Koo, Jason, Shah, Megha, Calmettes, Charles, Moraes, Trevor F., Burrows, Lori L., & Howell, P. Lynne. PilN binding modulates the structure and binding partners of the Pseudomonas aeruginosa type IVa pilus protein PilM. United States. https://doi.org/10.1074/jbc.M116.718353
McCallum, Matthew, Tammam, Stephanie, Little, Dustin J., Robinson, Howard, Koo, Jason, Shah, Megha, Calmettes, Charles, Moraes, Trevor F., Burrows, Lori L., and Howell, P. Lynne. Mon .
"PilN binding modulates the structure and binding partners of the Pseudomonas aeruginosa type IVa pilus protein PilM". United States. https://doi.org/10.1074/jbc.M116.718353. https://www.osti.gov/servlets/purl/1340346.
@article{osti_1340346,
title = {PilN binding modulates the structure and binding partners of the Pseudomonas aeruginosa type IVa pilus protein PilM},
author = {McCallum, Matthew and Tammam, Stephanie and Little, Dustin J. and Robinson, Howard and Koo, Jason and Shah, Megha and Calmettes, Charles and Moraes, Trevor F. and Burrows, Lori L. and Howell, P. Lynne},
abstractNote = {Pseudomonas aeruginosa is an opportunistic bacterial pathogen that expresses type IVa pili. The pilus assembly system, which promotes surface-associated twitching motility and virulence, is composed of inner and outer membrane subcomplexes, connected by an alignment subcomplex composed of PilMNOP. PilM binds to the N terminus of PilN, and we hypothesize that this interaction causes functionally significant structural changes in PilM. To characterize this interaction, we determined the crystal structures of PilM and a PilM chimera where PilM was fused to the first 12 residues of PilN (PilM·PilN(1–12)). Structural analysis, multiangle light scattering coupled with size exclusion chromatography, and bacterial two-hybrid data revealed that PilM forms dimers mediated by the binding of a novel conserved motif in the N terminus of PilM, and binding PilN abrogates this binding interface, resulting in PilM monomerization. Structural comparison of PilM with PilM·PilN(1–12) revealed that upon PilN binding, there is a large domain closure in PilM that alters its ATP binding site. Using biolayer interferometry, we found that the association rate of PilN with PilM is higher in the presence of ATP compared with ADP. Bacterial two-hybrid data suggested the connectivity of the cytoplasmic and inner membrane components of the type IVa pilus machinery in P. aeruginosa, with PilM binding to PilB, PilT, and PilC in addition to PilN. Pull-down experiments demonstrated direct interactions of PilM with PilB and PilT. As a result, we propose a working model in which dynamic binding of PilN facilitates functionally relevant structural changes in PilM.},
doi = {10.1074/jbc.M116.718353},
journal = {Journal of Biological Chemistry},
number = 21,
volume = 291,
place = {United States},
year = {Mon Mar 28 00:00:00 EDT 2016},
month = {Mon Mar 28 00:00:00 EDT 2016}
}
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