Phagosomal Rupture by Mycobacterium tuberculosis Results in Toxicity and Host Cell Death
Open accessAbstract
Survival within macrophages is a central feature of Mycobacterium tuberculosis pathogenesis. Despite significant advances in identifying new immunological parameters associated with mycobacterial disease, some basic questions on the intracellular fate of the causative agent of human tuberculosis in antigen-presenting cells are still under debate. To get novel insights into this matter, we used a single-cell fluorescence resonance energy transfer (FRET)-based method to investigate the potential cytosolic access of M. tuberculosis and the resulting cellular consequences in an unbiased, quantitative way. Analysis of thousands of THP-1 macrophages infected with selected wild-type or mutant strains of the M. tuberculosis complex unambiguously showed that M. tuberculosis induced a change in the FRET signal after 3 to 4 days of infection, indicating phagolysosomal rupture and cytosolic access. These effects were not seen for the strains M. tuberculosisΔRD1 or BCG, both lacking the ESX-1 secreted protein ESAT-6, which reportedly shows membrane-lysing properties. Complementation of these strains with the ESX-1 secretion system of M. tuberculosis restored the ability to cause phagolysosomal rupture. In addition, control experiments with the fish pathogen Mycobacterium marinum showed phagolysosomal translocation only for ESX-1 intact strains, further validating our experimental approach. Most importantly, for M. tuberculosis as well as for M. marinum we observed that phagolysosomal rupture was followed by necrotic cell death of the infected macrophages, whereas ESX-1 deletion- or truncation-mutants that remained enclosed within phagolysosomal compartments did not induce such cytotoxicity. Hence, we provide a novel mechanism how ESX-1 competent, virulent M. tuberculosis and M. marinum strains induce host cell death and thereby escape innate host defenses and favor their spread to new cells. In this respect, our results also open new research directions in relation with the extracellular localization of M. tuberculosis inside necrotic lesions that can now be tackled from a completely new perspective.
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The ESX-1 system is involved in bacterial phagosome-to-cytosol transition of M. tuberculosis and host cell death.
“The ESX-1 system was shown to be involved in bacterial phagosome-tocytosol transition of M. tuberculosis and host cell death (66)(67)(68), an important cell biological process that has numerous consequences for the host cell, such as induc-tion of the cGAS/STING/TBK1/IRF-3/type I interferon signalling axis and NLRP3 inflammasome activation (69)(70)(71)(72)(73)(74)(75).”
From ESX/Type VII Secretion Systems—An Important Way Out for Mycobacterial Proteins (2019) · cites this paper as [67]
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Self-citation
- Authors
- Simeone, R., Bobard, A., Lippmann, J., Bitter, W., Majlessi, L., Brosch, R., & Enninga, J.
- Affiliations
- Institut Pasteur (FR)
- Vrije Universiteit Amsterdam (NL)
- Inserm (FR)
- Corresponding author
- Brosch, Roland
- Enninga, Jost
- Venue
- PLoS Pathogens
- Publisher
- Public Library of Science (PLoS)
- Published
- 2012-02-02
- Volume
- 8
- Issue
- 2
- Pages
- e1002507
- ISSN
- 1553-7366 (ISSN-L)
- 1553-7374
- PMC
- PMC3271072
- OpenAlex
- W2051792510
- Cited by
- 561
- References
- 58
- Citations by year
- 2026: 20 · 2025: 37 · 2024: 36 · 2023: 33 · 2022: 31 · 2021: 42 · 2020: 47 · 2019: 44 · 2018: 42 · 2017: 50 · 2016: 40 · 2015: 46 · 2014: 38 · 2013: 36 · 2012: 19
- FWCI
- 30.70
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Pathogens (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- VU Research Portal (publishedVersion, other-oa)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (acceptedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- HAL (submittedVersion, cc-by)
- Digital Academic REpository of VU University Amsterdam (Vrije Universiteit Amsterdam) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Pure Amsterdam UMC (submittedVersion, other-oa)
- Funders
- European Commission (201762, 241745)
- Agence Nationale de la Recherche (ANR-09-MIEN-0020)
- FP7 Ideas: European Research Council (261166)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
- Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
- Health Sciences › Medicine › Epidemiology › Mycobacterium research and diagnosis
- Keywords
- Mycobacterium tuberculosis, ESX-1 secretion system, ESAT-6, Mycobacterium marinum, macrophage infection, necrosis, THP-1 macrophages, bacterial virulence, host-pathogen interaction, innate immune evasion
- MeSH terms
- Cell Line, Humans, Macrophages, Mycobacterium Infections, Mycobacterium tuberculosis, Phagosomes, Salmonella typhimurium, Shigella flexneri, Cell Death, Homeodomain Proteins, Mycobacterium marinum, Fluorescence Resonance Energy Transfer, Immune Evasion
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