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Take five — Type VII secretion systems of Mycobacteria
Open accessAbstract
Mycobacteria use type VII secretion (T7S) systems to secrete proteins across their complex cell envelope. Pathogenic mycobacteria, such as the notorious pathogen Mycobacterium tuberculosis, have up to five of these secretion systems, named ESX-1 to ESX-5. At least three of these secretion systems are essential for mycobacterial virulence and/or viability. Elucidating T7S is therefore essential to understand the success of M. tuberculosis and other pathogenic mycobacteria as pathogens, and could be instrumental to identify novel targets for drug- and vaccine-development. Recently, significant progress has been achieved in the identification of T7S substrates and a general secretion motif. In addition, a start has been made with unraveling the mechanism of secretion and the structural analysis of the different subunits. This review summarizes these recent findings, which are incorporated in a working model of this complex machinery. This article is part of a Special Issue entitled: Protein trafficking and secretion in bacteria. Guest Editors: Anastassios Economou and Ross Dalbey.
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“ESX-4 is one of the least well-characterized ESX systems, although it is considered the most ancestral esx locus in mycobacteria (21,82).”
From ESX/Type VII Secretion Systems—An Important Way Out for Mycobacterial Proteins (2019) · cites this paper as [82]
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Phosphate starvation: a novel signal that triggers ESX‐5 secretion in Mycobacterium tuberculosis
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“The ESX systems also require ATP for the transport of proteins (Houben et al., 2014), and perhaps priority for protein secretion during Pi limitation goes to ESX-5.”
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Cardenal‐Muñoz, E., Barisch, C., Lefrançois, L. H., López-Jiménez, A. T., & Soldati, T. (2018) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00529 · Cited by 52
“avium (Houben et al., 2014) does not escape its MCV (Hagedorn et al.”
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“Keywords: M. tuberculosis, PE32/PPE65, CD4+ T cells, CD8+ T cells, IgG subtyping INTRODUCTION Tuberculosis (TB), caused by the bacterium Mycobacterium tuberculosis (M. tuberculosis), despite being completely curable, claimed more than 1.5 million human lives in 2013 alone (Zumla et al., 2015) and…”
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Zondervan, N. A., van Dam, J. C. J., Schaap, P. J., dos Santos, V. A. P. M., & Diez, M. S. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19020347 · Cited by 49
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Abreu, R. B., Giri, P. K., & Quinn, F. D. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01553 · Cited by 44
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“diphtheriae genomes, suggesting these are the principal substrates for this specialised secretion system, which is known to influence virulence in related bacteria [63].”
BackgroundResultWinglee, K., Manson, A. L., Maïga, M., Abeel, T., Shea, T., Desjardins, C. A., Diarra, B., Baya, B., Sanogo, M., Diallo, S., et al. (2016) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0004332 · Cited by 39
“Mycobacteria have five ESX secretion systems, also known as type VII secretion systems, which secrete small proteins across the bacterial cell envelope and are important to mycobacterial virulence [98, 99].”
BackgroundType VII Secretion Substrates of Pathogenic Mycobacteria Are Processed by a Surface Protease
Burggraaf, M. J., Speer, A., Meijers, A. S., Ummels, R., van der Sar, A. M., Korotkov, K. V., Bitter, W., & Kuijl, C. P. (2019) · mBio · doi:10.1128/mbio.01951-19 · Cited by 40
“This unique cell envelope is highly impermeable and requires specialized secretion systems for protein transport to the cell surface (2, 3).”
Self-citationLafuente, B. I., Ummels, R., Kuijl, C. P., Bitter, W., & Speer, A. (2021) · mBio · doi:10.1128/mbio.02983-20 · Cited by 41
“genome and/or located within the ESX loci (9).”
BackgroundInfluentialSelf-citationBacterial secretion chaperones: the mycobacterial type VII case
Phan, T. H., & Houben, E. N. G. (2018) · FEMS Microbiology Letters · doi:10.1093/femsle/fny197 · Cited by 37
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“1C), which encodes for ESAT6, a protein secreted by the ESX1 system that plays a 327 direct role in virulence by rupturing the phagosomal membrane of the host cell [51,52].”
BackgroundResultMendum, T. A., Wu, H., Kierzek, A. M., & Stewart, G. R. (2015) · BMC Genomics · doi:10.1186/s12864-015-1569-2 · Cited by 38
“phthiocerol dimycolates (pDIMs) [44], phenolic glycolipids (PGLs) [45] and sulfolipids; cholesterol metabolism [46-48] and ESX systems [49] (Figure 2c and Figure 3).”
Bosserman, R. E., Nicholson, K. R., Champion, M. M., & Champion, P. A. D. (2019) · Journal of Bacteriology · doi:10.1128/jb.00760-18 · Cited by 38
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“However, PE/PPE proteins can only be found in the genus of Mycobacterium, whereas the homologs of the Esx substrates and the EccC core component can be found in a more diverse repertoire of Gram-positive species (1, 20, 50).”
BackgroundSelf-citationStreptococcus pneumoniae GAPDH Is Released by Cell Lysis and Interacts with Peptidoglycan
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“pneumoniae [51].”
Isolation of a Membrane Protein Complex for Type VII Secretion in Staphylococcus aureus
Aly, K. A., Anderson, M. C., Ohr, R. J., & Missiakas, D. M. (2017) · Journal of Bacteriology · doi:10.1128/jb.00482-17 · Cited by 31
Bobrovskyy, M., Willing, S. E., Schneewind, O., & Missiakas, D. M. (2018) · Journal of Bacteriology · doi:10.1128/jb.00268-18 · Cited by 33
“Mycobacterial genomes harbor up to five different T7SS gene clusters, designated ESX-1 through ESX-5 (48).”
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The EXIT Strategy: an Approach for Identifying Bacterial Proteins Exported during Host Infection
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Conserved ESX-1 Substrates EspE and EspF Are Virulence Factors That Regulate Gene Expression
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“similar to other ESX-1 substrates (47).”
Yimer, S. A., Kalayou, S., Homberset, H., Birhanu, A. G., Riaz, T., Zegeye, E. D., Lutter, T., Abebe, M., Holm‐Hansen, C., Aseffa, A., et al. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.550760 · Cited by 30
Modulation of the Activity of Mycobacterium tuberculosis LipY by Its PE Domain
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“On one hand, PE proteins are known to form dimers with their cognate PPE partner for recognition and exportation by unique type VII secretion systems[8, 29].”
BackgroundProtein Export into and across the Atypical Diderm Cell Envelope of Mycobacteria
van Winden, V. J. C., Houben, E. N. G., & Braunstein, M. (2019) · Microbiology Spectrum · doi:10.1128/microbiolspec.gpp3-0043-2018 · Cited by 28
“mycobacteria, Microbiol Spectrum 7(4):GPP3-0043-2018.”
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“In response to the capability of host cells to eliminate them, pathogenic mycobacteria have evolved mechanisms for the manipulation of the host immune response by secretion of virulence factors through specialized secretion systems (Baxt et al., 2013; Houben et al., 2013).”
BackgroundPinheiro, J. C., Reis, O., Vieira, A. R., Moranguinho, I., Moreno, L. Z., Carvalho, F., Pucciarelli, M. G., del Portillo, F. G., Sousa, S., & Cabanes, D. (2016) · Virulence · doi:10.1080/21505594.2016.1244589 · Cited by 25
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Srinivasan, L., Gurses, S. A., Hurley, B. E., Miller, J. L., Karakousis, P. C., & Briken, V. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1005652 · Cited by 22
“The mycobacterial type VII secretion system, ESX-5, is involved in the secretion of proteins containing Pro-Pro-Glu (PPE), Pro-Glu (PE) and polymorphic GC-rich sequences (PGRS) and has been implicated in cell lysis after Mtb escapes from the phagosome [39,85].”
BackgroundTargeting mitochondria: how intravacuolar bacterial pathogens manipulate mitochondria
Fielden, L. F., Kang, Y., Newton, H. J., & Stojanovski, D. (2016) · Cell and Tissue Research · doi:10.1007/s00441-016-2475-x · Cited by 25
“We will also discuss the relationship between these pathogens and mitochondria in terms of the mechanisms utilised to control mitochondrial activities and the challenges in studying this phenomenon.”
BackgroundInsight into the biology of Mycobacterium mucogenicum and Mycobacterium neoaurum clade members
Behra, P. R. K., Pettersson, B. M. F., Ramesh, M., Dasgupta, S., & Kirsebom, L. A. (2019) · Scientific Reports · doi:10.1038/s41598-019-55464-5 · Cited by 23
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Zhang, Y., Kitajima, M., Whittle, A. J., & Liu, W. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.02036 · Cited by 23
“tuberculosis, the reported VFs included: the T7SS, also known as the ESX pathway (ESX-1 to ESX-5) to secrete proteins across their complex cell envelope (Houben et al., 2014);”
BackgroundMethodPatterns and Processes of Mycobacterium bovis Evolution Revealed by Phylogenomic Analyses
Patané, J. S. L., Martins, J., Castelão, A. B. C., Nishibe, C., Montera, L., Bigi, F., Zumárraga, M. J., Cataldi, Á., Júnior, A. A. F., Roxo, E., et al. (2017) · Genome Biology and Evolution · doi:10.1093/gbe/evx022 · Cited by 22
“We highlight esxassociated genes (important constituents for the secretion of virulence factors; Houben et al. 2014); PPE proteins, which are themselves important virulence factors (Sampson 2011; Akhter et al. 2012; McEvoy et al. 2012); eight copies of Acyl-CoA dehydrogenases, reinforcing the…”
BackgroundInfluentialSpecies‐specific secretion of ESX‐5 type VII substrates is determined by the linker 2 of EccC 5
Bunduc, C. M., Ummels, R., Bitter, W., & Houben, E. N. G. (2020) · Molecular Microbiology · doi:10.1111/mmi.14496 · Cited by 22
“Pathogenic mycobacteria can have up to five T7SSs, named ESX-1 to ESX-5 (Houben et al., 2014), of which three, i.e., ESX-1, ESX-3 and ESX-5, have been shown to be functional (Pym et al., 2002; Stanley et al., 2003; Abdallah et al., 2006; Siegrist et al., 2009; Simeone et al., 2012).”
BackgroundSelf-citationPandey, H., Fatma, F., Yabaji, S. M., Kumari, M., Tripathi, S., Srivastava, K., Tripathi, D. K., Kant, S., Srivastava, K. K., & Arora, A. (2018) · Tuberculosis · doi:10.1016/j.tube.2018.02.002 · Cited by 20
Metadata
- Authors
- Houben, E. N. G., Korotkov, K. V., & Bitter, W.
- Affiliations
- Vrije Universiteit Amsterdam (NL)
- University of Kentucky (US)
- Corresponding author
- Houben, Edith N.G.
- Venue
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research
- Publisher
- Elsevier BV
- Published
- 2014-08
- Volume
- 1843
- Issue
- 8
- Pages
- 1707-1716
- ISSN
- 0167-4889 (ISSN-L)
- OpenAlex
- W2107983230
- Cited by
- 223
- References
- 93
- Citations by year
- 2026: 6 · 2025: 15 · 2024: 8 · 2023: 5 · 2022: 9 · 2021: 37 · 2020: 19 · 2019: 21 · 2018: 20 · 2017: 22 · 2016: 30 · 2015: 24 · 2014: 7
- FWCI
- 2.64
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research (publishedVersion)
- PubMed (publishedVersion)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
- VU Research Portal (publishedVersion, other-oa)
- Pure Amsterdam UMC (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- National Institute of General Medical Sciences (P20GM103486)
- Netherlands Organization for Scientific Research (NWO)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Health Sciences › Medicine › Epidemiology › Mycobacterium research and diagnosis
- Keywords
- type VII secretion system, ESX secretion system, Mycobacterium tuberculosis, mycobacterial virulence, bacterial protein secretion, secretion mechanism, ESX-1, therapeutic target, vaccine targets
- MeSH terms
- Bacterial Proteins, Cell Wall, Humans, Mycobacterium tuberculosis, Tuberculosis, Protein Structure, Tertiary, Molecular Chaperones, Protein Transport, Bacterial Secretion Systems
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