ESX-1 and phthiocerol dimycocerosates of Mycobacterium tuberculosis act in concert to cause phagosomal rupture and host cell apoptosis
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Although phthiocerol dimycocerosates (DIM) are major virulence factors of Mycobacterium tuberculosis (Mtb), the causative agent of human tuberculosis, little is known about their mechanism of action. Localized in the outer membrane of mycobacterial pathogens, DIM are predicted to interact with host cell membranes. Interaction with eukaryotic membranes is a property shared with another virulence factor of Mtb, the early secretory antigenic target EsxA (also known as ESAT-6). This small protein, which is secreted by the type VII secretion system ESX-1 (T7SS/ESX-1), is involved in phagosomal rupture and cell death induced by virulent mycobacteria inside host phagocytes. In this work, by the use of several knock-out or knock-in mutants of Mtb or Mycobacterium bovis BCG strains and different cell biological assays, we present conclusive evidence that ESX-1 and DIM act in concert to induce phagosomal membrane damage and rupture in infected macrophages, ultimately leading to host cell apoptosis. These results identify an as yet unknown function for DIM in the infection process and open up a new research field for the study of the interaction of lipid and protein virulence factors of Mtb.
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Besides ESX-1, the mycobacterial virulence lipids phthiocerol dimycocerosates also contribute to phagosomal rupture.
“However, ESX-1 is not the only factor involved in the process; it has been shown that besides ESX-1, the mycobacterial virulence lipids phthiocerol dimycocerosates also contribute to phagosomal rupture (76)(77)(78).”
From ESX/Type VII Secretion Systems—An Important Way Out for Mycobacterial Proteins (2019) · cites this paper as [76]
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Self-citationMittal, E., Skowyra, M. L., Uwase, G., Tinaztepe, E., Mehra, A., Köster, S., Hanson, P. I., & Philips, J. A. (2018) · mBio · doi:10.1128/mbio.01765-18 · Cited by 110 · see citing works
Barczak, A. K., Avraham, R., Singh, S., Luo, S. S., Zhang, W. R., Bray, M.-A., Hinman, A. E., Thompson, M., Nietupski, R. M., Golas, A., et al. (2017) · PLOS Pathogens · doi:10.1371/journal.ppat.1006363 · Cited by 120 · see citing works
Evolution of virulence in the Mycobacterium tuberculosis complex
Orgeur, M., & Brosch, R. (2018) · Current Opinion in Microbiology · doi:10.1016/j.mib.2017.11.021 · Cited by 107 · see citing works
Self-citationToxin secretion and trafficking by Mycobacterium tuberculosis
Pajuelo, D., Tak, U., Zhang, L., Danilchanka, O., Tischler, A. D., & Niederweis, M. (2021) · Nature Communications · doi:10.1038/s41467-021-26925-1 · Cited by 63 · see citing works
ESX/Type VII Secretion Systems—An Important Way Out for Mycobacterial Proteins
Vaziri, F., & Brosch, R. (2019) · Microbiology Spectrum · doi:10.1128/microbiolspec.psib-0029-2019 · Cited by 50 · see citing works
Self-citationEsx Systems and the Mycobacterial Cell Envelope: What's the Connection?
Bosserman, R. E., & Champion, P. A. (2017) · Journal of Bacteriology · doi:10.1128/jb.00131-17 · Cited by 42 · see citing works
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- Authors
- Augenstreich, J., Arbues, A., Simeone, R., Haanappel, E., Wegener, A., Sayes, F., Le Chevalier, F., Chalut, C., Malaga, W., Guilhot, C., Brosch, R., & Astarie-Dequeker, C.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Institut de Pharmacologie et de Biologie Structurale (IPBS); CNRS-Université de Toulouse (UPS); Toulouse France
- Unit for Integrated Mycobacterial Pathogenomics; Institut Pasteur; Paris France
- Institut Pasteur (FR)
- Corresponding author
- Brosch, Roland
- ORCID
- Venue
- Cellular Microbiology
- Publisher
- Wiley
- Published
- 2017-02-15
- Volume
- 19
- Issue
- 7
- Pages
- e12726
- ISSN
- 1462-5814 (ISSN-L)
- OpenAlex
- W2580358075
- Cited by
- 240
- References
- 85
- Citations by year
- 2026: 26 · 2025: 19 · 2024: 25 · 2023: 25 · 2022: 30 · 2021: 23 · 2020: 31 · 2019: 23 · 2018: 22 · 2017: 15
- FWCI
- 19.15
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cellular Microbiology (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, other-oa)
- Funders
- TRI-Genotoul Imaging facility (Toulouse, France)
- BEI Resources, NIAID, NIH: Recombinant Protein Reference Standard, NR-14868
- European Community's (TBVAC2020, 643381)
- Agence Nationale de la Recherche (ANR-10-LABX-62-IBEID, ANR-14-JAMR-001-02, ANR-16-CE15-0003)
- Fondation pour la Recherche Médicale (DEQ20090515399, DEQ20130326471, ING20140129051)
- Centre National de la Recherche Scientifique
- Topics
- Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
- Health Sciences › Medicine › Epidemiology › Mycobacterium research and diagnosis
- Health Sciences › Medicine › Surgery › Infectious Diseases and Tuberculosis
- Keywords
- Mycobacterium tuberculosis, phthiocerol dimycocerosate, ESX-1, ESAT-6, type VII secretion system, host cell apoptosis, macrophages, virulence factors, protein-lipid interactions, Mycobacterium bovis BCG, membrane damage
- MeSH terms
- THP-1 Cells, Antigens, Bacterial, Bacterial Proteins, Cell Membrane, Humans, Lipids, Macrophages, Mycobacterium bovis, Mycobacterium tuberculosis, Phagosomes, Apoptosis, Virulence Factors, Cell Line, Tumor
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