Proximity-dependent proteomics of the Chlamydia trachomatis inclusion membrane reveals functional interactions with endoplasmic reticulum exit sites

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.

doi:10.1371/journal.ppat.1007698

Title: Proximity-dependent proteomics of the Chlamydia trachomatis inclusion membrane reveals functional interactions with endoplasmic reticulum exit sites

Journal Article · Wed Apr 03 00:00:00 EDT 2019 · PLoS Pathogens

DOI:https://doi.org/10.1371/journal.ppat.1007698· OSTI ID:1530860

Dickinson, Mary S.;

;

; Coombes, Brian K.

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.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1530860

Report Number(s):: PNNL-SA-132851

Journal Information:: PLoS Pathogens, Vol. 15, Issue 4; ISSN 1553-7374

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 20 works

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Expression of the Effector Protein IncD in Chlamydia trachomatis Mediates Recruitment of the Lipid Transfer Protein CERT and the Endoplasmic Reticulum-Resident Protein VAPB to the Inclusion Membrane Agaisse, Hervé; Derré, Isabelle Infection and Immunity, Vol. 82, Issue 5 https://doi.org/10.1128/iai.01530-14	journal	March 2014
Global Stage-Specific Gene Regulation during the Developmental Cycle of Chlamydia trachomatis Nicholson, T. L.; Olinger, L.; Chong, K. Journal of Bacteriology, Vol. 185, Issue 10 https://doi.org/10.1128/jb.185.10.3179-3189.2003	journal	May 2003
Phosphatidylinositol 3-kinase and COPII generate LC3 lipidation vesicles from the ER-Golgi intermediate compartment Ge, Liang; Zhang, Min; Schekman, Randy eLife, Vol. 3 https://doi.org/10.7554/elife.04135	journal	November 2014

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Uncovering the In Vivo Proxisome Using Proximity‐Tagging Methods Santin, Yoann G. BioEssays, Vol. 41, Issue 12 https://doi.org/10.1002/bies.201900131	journal	October 2019
Proximity Labeling To Map Host-Pathogen Interactions at the Membrane of a Bacterium-Containing Vacuole in Chlamydia trachomatis -Infected Human Cells Olson, Macy G.; Widner, Ray E.; Jorgenson, Lisa M. Infection and Immunity, Vol. 87, Issue 11 https://doi.org/10.1128/iai.00537-19	journal	August 2019
A renewed tool kit to explore Chlamydia pathogenesis: from molecular genetics to new infection models Dolat, Lee; Valdivia, Raphael H. F1000Research, Vol. 8 https://doi.org/10.12688/f1000research.18832.1	journal	January 2019

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