Proximity-dependent proteomics of the Chlamydia trachomatis inclusion membrane reveals functional interactions with endoplasmic reticulum exit sites
Abstract
Chlamydia trachomatis is the most common bacterial sexually transmitted infection, responsible for millions of infections each year. Despite this high prevalence, the elucidation of the molecular mechanisms of Chlamydia pathogenesis has been difficult due to limitations in genetic tools and its intracellular developmental cycle. Within a host epithelial cell, chlamydiae replicate within a vacuole called the inclusion. Many Chlamydia–host interactions are thought to be mediated by the Inc family of type III secreted proteins that are anchored in the inclusion membrane, but their array of host targets are largely unknown. To investigate how the inclusion membrane proteome changes over the course of an infected cell, we have adapted the APEX system of proximity-dependent biotinylation. APEX is capable of specifically labeling proteins within a 20 nm radius in living cells. We transformed C. trachomatis to express the enzyme APEX fused to known inclusion membrane proteins, allowing biotinylation and pull-down of inclusion-associated proteins. Using quantitative mass spectrometry against APEX labeled samples, we identified over 400 proteins associated with the inclusion membrane at early, middle, and late stages of epithelial cell infection. This system was sensitive enough to detect inclusion interacting proteins early in the developmental cycle, at 8 hours post infection, amore »
- Publication Date:
- Research Org.:
- Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)
- OSTI Identifier:
- 1530860
- Report Number(s):
- PNNL-SA-132851
Journal ID: ISSN 1553-7374
- Grant/Contract Number:
- AC05-76RL01830
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS Pathogens
- Additional Journal Information:
- Journal Volume: 15; Journal Issue: 4; Journal ID: ISSN 1553-7374
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Dickinson, Mary S., Anderson, Lindsey N., Webb-Robertson, Bobbie-Jo M., Hansen, Joshua R., Smith, Richard D., Wright, Aaron T., Hybiske, Kevin, and Coombes, Brian K. Proximity-dependent proteomics of the Chlamydia trachomatis inclusion membrane reveals functional interactions with endoplasmic reticulum exit sites. United States: N. p., 2019.
Web. doi:10.1371/journal.ppat.1007698.
Dickinson, Mary S., Anderson, Lindsey N., Webb-Robertson, Bobbie-Jo M., Hansen, Joshua R., Smith, Richard D., Wright, Aaron T., Hybiske, Kevin, & Coombes, Brian K. Proximity-dependent proteomics of the Chlamydia trachomatis inclusion membrane reveals functional interactions with endoplasmic reticulum exit sites. United States. https://doi.org/10.1371/journal.ppat.1007698
Dickinson, Mary S., Anderson, Lindsey N., Webb-Robertson, Bobbie-Jo M., Hansen, Joshua R., Smith, Richard D., Wright, Aaron T., Hybiske, Kevin, and Coombes, Brian K. Wed .
"Proximity-dependent proteomics of the Chlamydia trachomatis inclusion membrane reveals functional interactions with endoplasmic reticulum exit sites". United States. https://doi.org/10.1371/journal.ppat.1007698. https://www.osti.gov/servlets/purl/1530860.
@article{osti_1530860,
title = {Proximity-dependent proteomics of the Chlamydia trachomatis inclusion membrane reveals functional interactions with endoplasmic reticulum exit sites},
author = {Dickinson, Mary S. and Anderson, Lindsey N. and Webb-Robertson, Bobbie-Jo M. and Hansen, Joshua R. and Smith, Richard D. and Wright, Aaron T. and Hybiske, Kevin and Coombes, Brian K.},
abstractNote = {Chlamydia trachomatis is the most common bacterial sexually transmitted infection, responsible for millions of infections each year. Despite this high prevalence, the elucidation of the molecular mechanisms of Chlamydia pathogenesis has been difficult due to limitations in genetic tools and its intracellular developmental cycle. Within a host epithelial cell, chlamydiae replicate within a vacuole called the inclusion. Many Chlamydia–host interactions are thought to be mediated by the Inc family of type III secreted proteins that are anchored in the inclusion membrane, but their array of host targets are largely unknown. To investigate how the inclusion membrane proteome changes over the course of an infected cell, we have adapted the APEX system of proximity-dependent biotinylation. APEX is capable of specifically labeling proteins within a 20 nm radius in living cells. We transformed C. trachomatis to express the enzyme APEX fused to known inclusion membrane proteins, allowing biotinylation and pull-down of inclusion-associated proteins. Using quantitative mass spectrometry against APEX labeled samples, we identified over 400 proteins associated with the inclusion membrane at early, middle, and late stages of epithelial cell infection. This system was sensitive enough to detect inclusion interacting proteins early in the developmental cycle, at 8 hours post infection, a previously intractable time point. Mass spectrometry analysis revealed a novel, early association between C. trachomatis inclusions and endoplasmic reticulum exit sites (ERES), functional regions of the ER where COPII-coated vesicles originate. Pharmacological and genetic disruption of ERES function severely restricted early chlamydial growth and the development of infectious progeny. APEX is therefore a powerful in situ approach for identifying critical protein interactions on the membranes of pathogen-containing vacuoles. Furthermore, the data derived from proteomic mapping of Chlamydia inclusions has illuminated an important functional role for ERES in promoting chlamydial developmental growth.},
doi = {10.1371/journal.ppat.1007698},
journal = {PLoS Pathogens},
number = 4,
volume = 15,
place = {United States},
year = {Wed Apr 03 00:00:00 EDT 2019},
month = {Wed Apr 03 00:00:00 EDT 2019}
}
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