Cited by 223Tuberculosis Research and EpidemiologyBacterial Genetics and BiotechnologyMycobacterium research and diagnosis

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Take five — Type VII secretion systems of Mycobacteria

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Houben, Edith N.G., Korotkov, Konstantin V., Bitter, Wilbert·2014·Biochimica et Biophysica Acta (BBA) - Molecular Cell Research

DOI 10.1016/j.bbamcr.2013.11.003

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Abstract

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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Bergey's Manual of Systematic Bacteriology
(1990) · Annals of Internal Medicine · doi:10.7326/0003-4819-112-5-391_3 · Cited by 15,633
The Pfam Protein Families Database
Bateman, A. G. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.1.276 · Cited by 14,075
Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence
Cole, S. T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., Gordon, S. V., Eiglmeier, K., Gas, S., Barry, C. E., et al. (1998) · Nature · doi:10.1038/31159 · Cited by 7,847
The Pfam protein families database
Punta, M., Coggill, P. C., Eberhardt, R. Y., Mistry, J., Tate, J., Boursnell, C., Pang, N., Forslund, K., Ceric, G., Clements, J., et al. (2012) · Nucleic Acids Research · doi:10.1093/nar/gkr1065 · Cited by 3,719
Genes required for mycobacterial growth defined by high density mutagenesis
Sassetti, C. M., Boyd, D. H., & Rubin, E. J. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03425.x · Cited by 2,544
The primary mechanism of attenuation of bacillus Calmette–Guérin is a loss of secreted lytic function required for invasion of lung interstitial tissue
Hsu, T., Hingley-Wilson, S. M., Chen, B., Chen, M., Dai, A. Z., Morin, P. M., Marks, C. B., Padiyar, J., Goulding, C., Gingery, M., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1635213100 · Cited by 731
Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti
Pym, A. S., Brodin, P., Brosch, R., Huerre, M., & Cole, S. T. (2002) · Molecular Microbiology · doi:10.1046/j.1365-2958.2002.03237.x · Cited by 729
Toward the structural genomics of complexes: Crystal structure of a PE/PPE protein complex from Mycobacterium tuberculosis
Strong, M., Sawaya, M. R., Wang, S., Phillips, M. L., Cascio, D., & Eisenberg, D. S. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602606103 · Cited by 704
Type VI secretion requires a dynamic contractile phage tail-like structure
Basler, M., Pilhofer, M., Henderson, G. P., Jensen, G. J., & Mekalanos, J. J. (2012) · Nature · doi:10.1038/nature10846 · Cited by 676
Bergey’s Manual of Systematic Bacteriology
Wade, W. E., & Dewhirst, F. E. (2012) · Springer US · Cited by 649

Flagged first, then by citations

Show all 93 references

Research works printed but not linked: 2

Goodfellow, 2012, Order Corynebacteriales ord. nov., vol. 5, 235
Burton, 2010, Membrane-associated DNA transport machines, Cold Spring Harb. Perspect. Biol., 2, a000406, 10.1101/cshperspect.a000406 · DOI

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Gijsbers, A., Eymery, M., Gao, Y., Menart, I., Vinciauskaite, V., Siliqi, D., Peters, P. J., McCarthy, A. A., & Ravelli, R. B. G. (2022) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2022.102761 · Cited by 16
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Self-citation
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BackgroundResultInfluential
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“…relationship between Rv3899c and the ESX-2 system, one of five type VII or ESAT-6 secretion systems (ESX-1 to ESX-5) that ISSN 2053-230X # 2016 International Union of Crystallography are essential for mycobacterial virulence and/or viability (Houben et al., 2014; Newton-Foot et al., 2016).”
Background
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“These proteins belong to WGX100 family, which re type VII secr tion substrates and thought to play a role in pathogenicit in taxonomically closely related bacteria such as Mycobacterium tuberculosis [26,33].”
Background
Mycobacteria produce proteins involved in biofilm formation and growth-affecting processes
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Canestrari, J. G., Gordon, E. C., Bruce, S. A., Lasek‐Nesselquist, E., Schultz, S. R., Marietta, H. A., Biegas, K. J., Swarts, B. M., Champion, M. M., Derbyshire, K. M., et al. (2025) · Molecular Microbiology · doi:10.1111/mmi.70030 · Cited by 4
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“, 2014), which may play a pivotal role in adaptation to intracellular survival within protozoan, including amoebae (Cole et al., 1998; Forrellad et al., 2013; Gey Van Pittius et al., 2001; Houben et al., 2014; Tekaia et al., 1999).”
Background
SINGLE NUCLEOTIDE POLYMORPHISM OF ECCB5GENEOF MYCOBACTERIUM TUBERCULOSIS COMPLEX ISOLATES FROM SUSPECTED PULMONARY TB PATIENTS IN SURABAYA INDONESIA
Kurniawati, S., Soedarsono, S., Aulanni’am, A., & Mertaniasih, N. M. (2018) · African Journal of Infectious Diseases · doi:10.21010/ajid.v12i2.6 · Cited by 3
“The trend of increasing TB incidence could be assosiated with virulence factor of MTBC such as type T7SS (consists of ESX-1 to ESX-5 system) (Forrellad et al., 2013; Houben et al., 2014; Simeone et al., 2015).”
Background
Virulence evolution
Schmid‐Hempel, P. (2021) · Oxford University Press eBooks · doi:10.1093/oso/9780198832140.003.0013 · Cited by 3
Insights into ancestry and adaptive evolution of the Mycobacterium tuberculosis complex from analysis of the emerging pathogen Mycobacterium riyadhensePreprint
Guan, Q., Garbati, M. A., Mfarrej, S., AlMutairi, T., Smyth, A., Singh, A., Fagbo, S. F., Browne, J. A., urRahman, M. A., Alruwaili, A., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/728923 · Cited by 3
“7 at the root node, and then ESX-3, ESX-1, ESX-5 and ESX-2 evolved by horizontal transfer54.”
MethodInfluential
PPE51 modulates membrane integrity in Mycobacterium marinum
Charitou, V., Lafuente, B. I., Habjan, E., Kuijl, C. P., Willemse, J. J., Bitter, W., & Speer, A. (2025) · mBio · doi:10.1128/mbio.01044-25 · Cited by 3
Self-citation
TXSelect: A multi-task learning model to identify secretory effectors
Li, J., Liu, Q., Zou, Q., & Zhan, C. (2025) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1013677 · Cited by 2
“This system has been extensively studied in Mycobacterium species and mediates pathogen-host immune sys-tem interactions, contributing significantly to immune evasion and infection processes [11].”
Protein-Mediated Virulence in Mycobacterium tuberculosis
Farnia, P., Velayati, A. A., Ghanavi, J., & Farnia, P. (2025) · Advances in experimental medicine and biology · doi:10.1007/978-3-031-96883-9_5 · Cited by 3
Host–parasite co-evolution
Schmid‐Hempel, P. (2021) · Oxford University Press eBooks · doi:10.1093/oso/9780198832140.003.0014 · Cited by 2
The chamber of secretome in Mycobacterium tuberculosis as a potential therapeutic target
Dwivedi, M., & Bajpai, K. (2022) · Biotechnology and Genetic Engineering Reviews · doi:10.1080/02648725.2022.2076031 · Cited by 2
“ESX-1, ESX-2, ESX-3, ESX-4 and ESX-5 (Figure 2) (Ates et al., 2016; Houben et al., 2014; Gröschel et al., 2016; Roy et al., 2020).”
BackgroundInfluential
New insights into the domain of unknown function (DUF) of EccC5, the pivotal ATPase providing the secretion driving force to the ESX-5 secretion system
Ceballos-Zúñiga, F., Menéndez, M., & Pérez‐Dorado, I. (2024) · Acta Crystallographica Section D Structural Biology · doi:10.1107/s2059798324004248 · Cited by 2
Exploring the pangenome landscape of Mycobacterium avium complex: insights into phylogeny and lifestyle
Banerjee, A., & Sur, S. (2024) · Biologia · doi:10.1007/s11756-024-01798-z · Cited by 2
“…II secretion system (T2SS), type VII secretion ATPase EccA/AAA-ATPase EccA/EccCa/EccCb, WXG100 family type VII secretion target allows the bacteria to secrete them inside the host cells and are indispensable for the virulence and viability of the cells (Houben et al. 2014; Crosskey et al. 2020).”
What lies beneath: microbial quality of rural groundwater explored by shotgun metagenomics
Mattar, M.-A. M., Eraqi, W. A., Zaki, M., Elkashlan, A. M., Abouzid, K. A. M., Aziz, R. K., Yassin, A. S., & Elbehery, A. H. A. (2025) · Annals of Microbiology · doi:10.1186/s13213-025-01801-1 · Cited by 2
“…PhoP, (encoded by esxN and esxM ), which are crucial for the survival and ability of pathogenic Mycobacterium tuberculosis to cause disease (Houben et al. 2014; He et al. 2016), and (3) nutritional/metabolic factors like RelA, which is a critical regulator in Mycobacterium tuberculosis In…”
Expression and production of soluble Mycobacterium tuberculosis H37Rv mycosin-3
Fang, Z., Schubert, W., & van Pittius, N. C. G. (2016) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2016.02.005 · Cited by 3
The espD Full Gene as a Potential Biomarker in Active Pulmonary Tuberculosis
Mertaniasih, N. M., Dewi, D. N. S. S., Soedarsono, S., Kurniati, A., Rohman, A., Nuha, Z., & Matsumoto, S. (2021) · International Journal of Mycobacteriology · doi:10.4103/ijmy.ijmy_198_21 · Cited by 3
The diversity and natural history of parasites
Schmid‐Hempel, P. (2021) · Oxford University Press eBooks · doi:10.1093/oso/9780198832140.003.0003 · Cited by 2
Characterizing the Intact Prophage of Mycobacterium chelonae Bergey
Sewell, E. (2017) · DigitalCommons (California Polytechnic State University) · Cited by 2
Bacterial Secretion Systems
Maresso, A. W. (2019) · Springer eBooks · doi:10.1007/978-3-030-20464-8_9 · Cited by 2
Recent advances in molecular mechanisms of autophagosome-lysosome fusion and impacts of exogenous factors
Zheng, P., Yuan, W., Xiao, X., Xiong, K., Li, X., Holck, A. L., & Liu, R. (2020) · ES Food & Agroforestry · doi:10.30919/esfaf0012 · Cited by 2
Conserved SQ and QS motifs in bacterial effectors suggest pathogen interplay with the ATM kinase family during infectionPreprint
Sampietro, D., Sámano‐Sánchez, H., Davey, N. E., Sharan, M., Mészáros, B., Gibson, T. J., & Kumar, M. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/364117 · Cited by 3
“Apart from the six TSS’s in Gramnegative bacteria, a seventh one has also been identified exclusively in the members of the genus Mycobacteria (26).”
Background
Editorial: Thematic issue on bacterial protein export: from fundamentals to applications
Anné, J., Karamanou, S., & Economou, A. (2018) · FEMS Microbiology Letters · doi:10.1093/femsle/fny206 · Cited by 2
Virtual Screening of Novel Phytocompound(s) with Potential to Combat Mycobacterium tuberculosis Infection
Khare, D., Aggarwal, A., & Sharma, S. (2022) · Letters in Drug Design & Discovery · doi:10.2174/1570180819666220523152239 · Cited by 1
Protein Architecture and Composition in Mycobacterium tuberculosis
Farnia, P., Velayati, A. A., Ghanavi, J., & Farnia, P. (2025) · Advances in experimental medicine and biology · doi:10.1007/978-3-031-96883-9_3 · Cited by 1
The natural history of defences
Schmid‐Hempel, P. (2021) · Oxford University Press eBooks · doi:10.1093/oso/9780198832140.003.0004 · Cited by 1
Characterizing Mab Cluster R Prophage of Pathogen Mycobacterium abscessus (Mab)
Kimble, M. (2021) · DigitalCommons (California Polytechnic State University) · Cited by 1
Mycobacterium tuberculosis Rv0292 Protein Peptides Could be Included in a Synthetic Anti-tuberculosis Vaccine
Salazar, J. A., Ocampo, M., Castañeda-Ramírez, J. J., Samacá, J., Patarroyo, M. A., & Patarroyo, M. E. (2021) · International Journal of Peptide Research and Therapeutics · doi:10.1007/s10989-021-10292-y · Cited by 1
Specificity
Schmid‐Hempel, P. (2021) · Oxford University Press eBooks · doi:10.1093/oso/9780198832140.003.0007 · Cited by 1
Semantic systems biology of prokaryotes : heterogeneous data integration to understand bacterial metabolism
van Dam, J. C. J. (2019) · doi:10.18174/464871 · Cited by 1
Molecular Characterization of EspB: A Phospholipid Binding Mycobacterium tuberculosis Virulence Factor
Chung, B. (2021) · HARVEST (University of Saskatchewan) · Cited by 1
Environmental Mycobacteria
Asif, H., & Mirsaeidi, M. S. (2020) · Elsevier eBooks · doi:10.1016/b978-0-08-102723-3.00065-2 · Cited by 1
Higher-order organization of bacterial cords and an amyloid-like matrix define the Mycobacterium tuberculosis biofilmPreprint
Lee, B. S., Godejohann, M., Mishra, R., Bousquet, C., Gürtler, F., Deloria, A. J., Liu, M., Leitgeb, R. A., Drexler, W., Weiss, G. L., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.07.687260 · Cited by 2
“Biofilm-associated protection was also observed during RIF treatment (Extended Data Fig.”
Identification of Anti‐infective Compounds Using Amoebae
Harrison, C. F., & Hilbi, H. (2016) · Wiley eBooks · doi:10.1002/9783527682386.ch8
O complexo Mycobacterium avium: caracterização e patogenicidade
de Oliveira, A. S. (2015) · Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT)
Análise genômica comparativa entre cepas de Mycobacterium abscessus subsp. bollettii com perfis distintos de susceptibilidade ao glutaraldeído
Pelegrino, K. D. O. (2017) · doi:10.11606/t.5.2017.tde-22092017-133433
Characterization of a Key Mycobacterium tuberculosis Lipase, LipY
Garrett, C. K. (2019) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/w4gt-1436
FİTOPATOJEN BAKTERİLERE AİT SALGI SİSTEMLERİNİN GENEL ÖZELLİKLERİ
Baş, B. (2019) · Eskişehir Teknik Üniversitesi Bilim ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji · doi:10.18036/estubtdc.599174
Secretome of Microbiota in Extreme Conditions
Mishra, M. S., Singh, R. K., Chauhan, S., & Gupta, P. (2020) · Springer eBooks · doi:10.1007/978-981-15-3028-9_6
Positron emission tomography in infections associated with immune dysfunction
Ankrah, A. O. (2020) · University of Groningen research database (University of Groningen / Centre for Information Technology) · doi:10.33612/diss.144628960
Between-host dynamics (Epidemiology)
Schmid‐Hempel, P. (2021) · Oxford University Press eBooks · doi:10.1093/oso/9780198832140.003.0011
Parasites and their significance
Schmid‐Hempel, P. (2021) · Oxford University Press eBooks · doi:10.1093/oso/9780198832140.003.0001
Within-host dynamics and evolution
Schmid‐Hempel, P. (2021) · Oxford University Press eBooks · doi:10.1093/oso/9780198832140.003.0012
Transmission, infection, and pathogenesis
Schmid‐Hempel, P. (2021) · Oxford University Press eBooks · doi:10.1093/oso/9780198832140.003.0009
Ecology
Schmid‐Hempel, P. (2021) · Oxford University Press eBooks · doi:10.1093/oso/9780198832140.003.0015

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.
ORCID: Houben, Edith N.G.
Korotkov, Konstantin V.
Bitter, Wilbert
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)
DOI: 10.1016/j.bbamcr.2013.11.003
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: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 365 d)
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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Take five — Type VII secretion systems of Mycobacteria

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