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.
“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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Self-citationCrystal structure of the Yersinia type III secretion protein YscE
Phan, J., Austin, B. P., & Waugh, D. S. (2005) · Protein Science · doi:10.1110/ps.051706105 · Cited by 20 · see citing works
Bacterial Secretion Chaperones
Fattori, J., Prando, A., Martins, A. M., Rodrigues, F. H. D. S., & Tasić, L. (2011) · Protein and Peptide Letters · doi:10.2174/092986611794475048 · Cited by 13 · see citing works
Buxton, R. S., Green, J. D., Hunt, D. M., Kahramanoglou, C., Stapleton, M. R., & Sweeney, N. P. (2012) · Virulence · doi:10.4161/viru.20918 · Cited by 5 · see citing works
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Secretion systems in Gram-negative bacteria: Structural and mechanistic insights
Costa, T. R. D., Felisberto-Rodrigues, C., Meir, A., Prevost, M. S., Redzej, A., Trokter, M., & Waksman, G. (2015) · Nature Reviews Microbiology · doi:10.1038/nrmicro3456 · Cited by 1,132 · see citing works
Bacterial Secretion Systems: An Overview
Green, E. R., & Mecsas, J. C. (2016) · Microbiology Spectrum · doi:10.1128/microbiolspec.vmbf-0012-2015 · Cited by 1,090 · see citing works
ESX secretion systems: mycobacterial evolution to counter host immunity
Gröschel, M. I., Sayes, F., Simeone, R., Majlessi, L., & Brosch, R. (2016) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2016.131 · Cited by 382 · see citing works
Dallenga, T. K., Repnik, U., Corleis, B., Eich, J., Reimer, R., Griffiths, G. W., & Schaible, U. E. (2017) · Cell Host & Microbe · doi:10.1016/j.chom.2017.09.003 · Cited by 231 · see citing works
“The RD1 region encodes for certain virulence-associated gene products, including the ESAT-6/EsxA-CFP10 complex and its respective secretion apparatus components ESX1-5 (Houben et al., 2014; Parkash et al., 2009).”
Ohno, H. (2015) · The Journal of Biochemistry · doi:10.1093/jb/mvv121 · Cited by 224 · see citing works
Tufariello, J. M., Chapman, J. R., Kerantzas, C. A., Wong, K.-W., Vilchèze, C., Jones, C. M., Cole, L. E., Tinaztepe, E., Thompson, V., Fenyö, D., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1523321113 · Cited by 215 · see citing works
Simeone, R., Sayes, F., Song, O., Gröschel, M. I., Brodin, P., Brosch, R., & Majlessi, L. (2015) · PLOS Pathogens · doi:10.1371/journal.ppat.1004650 · Cited by 198 · see citing works
“The pathogenic potential ofMycobacterium tuberculosis (Mtb), the etiologic agent of human tuberculosis (TB), depends largely on the type VII secretion system ESX-1 [1,2], which is responsible for the secretion of the 6-kDa Early Secreted Antigenic Target (ESAT-6), its protein partner, the 10-kDa Culture Filtrate Prote…”
BackgroundAtes, L. S., Ummels, R., Commandeur, S., van der Weerd, R., Sparrius, M., Weerdenburg, E., Alber, M., Kalscheuer, R., Piersma, S. R., Abdallah, A. M., et al. (2015) · PLOS Genetics · doi:10.1371/journal.pgen.1005190 · Cited by 185 · see citing works
“tuberculosis, the vaccine strain Mycobacterium bovis BCG, the closely related fish pathogenMycobacterium marinum and the evolutionary more distant and avirulentMycobacterium smegmatis [12–14].”
BackgroundSelf-citationBacterial Secretion Systems: An Overview
Green, E. R., & Mecsas, J. C. (2016) · ASM Press eBooks · doi:10.1128/9781555819286.ch8 · Cited by 151 · see citing works
Rosenberg, O. S., Dovala, D., Li, X., Connolly, L., Bendebury, A., Finer-Moore, J., Holton, J., Cheng, Y., Stroud, R. M., & Cox, J. S. (2015) · Cell · doi:10.1016/j.cell.2015.03.040 · Cited by 134 · see citing works
“…et al., 2014; Waksman, 2012), is required for virulence of several bacterial pathogens, including Mycobacte- rium tuberculosis (Guinn et al., 2004; Houben et al., 2014; Hsu et al., 2003; Stanley et al., 2003),Mycobacteriummarinum (Davis and Ramakrishnan, 2009; Gao et al., 2004), and…”
An outer membrane channel protein of Mycobacterium tuberculosis with exotoxin activity
Danilchanka, O., Sun, J., Pavlenok, M., Maueröder, C., Speer, A., Siroy, A., Marrero, J., Trujillo, C., Mayhew, D. L., Doornbos, K. S., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1400136111 · Cited by 131 · see citing works
“Although inner membrane proteins of ESX secretion systems have been characterized (16), channel proteins that are required for protein translocation across the outer membrane are currently unknown in M.”
BackgroundSporulation, bacterial cell envelopes and the origin of life
Tocheva, E. I., Ortega, D. R., & Jensen, G. J. (2016) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2016.85 · Cited by 121 · see citing works
Small Molecules That Sabotage Bacterial Virulence
Johnson, B. K., & Abramovitch, R. B. (2017) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2017.01.004 · Cited by 131 · see citing works
“Importantly, the inability to secrete these proteins is associated with the attenuation of the live-vaccine strain Mycobacterium bovis BCG [114].”
BackgroundInfluentialSchmid‐Hempel, P. (2021) · doi:10.1093/oso/9780198832140.001.0001 · Cited by 130 · see citing works
Beckham, K. S. H., Ciccarelli, L., Bunduc, C. M., Mertens, H. D. T., Ummels, R., Lugmayr, W., Mayr, J., Rettel, M., Savitski, M. M., Svergun, D. I., et al. (2017) · Nature Microbiology · doi:10.1038/nmicrobiol.2017.47 · Cited by 112 · see citing works
“tuberculosis were further modified by (1) replacing the hygromycin resistance cassette by a streptomycin resistance gene; (2) introducing the pAL5000 origin of replication24 by homologous recombination via a commercial kit (Clontech In-Fusion); and (3) deletion of the Hsp60 promoter.”
MethodSelf-citationPET/CT imaging of Mycobacterium tuberculosis infection
Ankrah, A. O., van der Werf, T. S., de Vries, E. F. J., Dierckx, R., Sathekge, M. M., & Glaudemans, A. W. J. M. (2016) · Clinical and Translational Imaging · doi:10.1007/s40336-016-0164-0 · Cited by 122 · see citing works
“This protective outer membrane plays an important role in securing the bacillus’ integrity in the face of harsh environmental conditions [25].”
BackgroundBarczak, 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
“To determine whether PDIM’s disruption of ESX-1-mediated secretion was generalizable to other ESX secretion systems implicated in virulence [37,38], we next tested whether loss of PDIM disrupts secretion of ESX-3 and ESX-5 substrates.”
BackgroundEkiert, D. C., & Cox, J. S. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1409345111 · Cited by 116 · see citing works
Li, J., Tai, C., Deng, Z., Zhong, W., He, Y. O., & Ou, H. (2016) · Briefings in Bioinformatics · doi:10.1093/bib/bbw141 · Cited by 117 · see citing works
The Enigmatic Esx Proteins: Looking Beyond Mycobacteria
Unnikrishnan, M., Constantinidou, C., Palmer, T., & Pallen, M. J. (2016) · Trends in Microbiology · doi:10.1016/j.tim.2016.11.004 · Cited by 112 · see citing works
“ESX-5, which have broadly similar features [5, 8].”
BackgroundInfluentialSerafini, A., Tan, L., Horswell, S. D., Howell, S. A., Greenwood, D. J., Hunt, D. M., Phan, M., Schembri, M. A., Monteleone, M. M., Montague, C. R., et al. (2019) · Molecular Microbiology · doi:10.1111/mmi.14362 · Cited by 108 · see citing works
“Finally, effectors of ESX-1 secretion system (EsxA and EsxB), essential for Mtb virulence (Houben et al., 2014), are differentially regulated in lactate and pyruvate compared to glucose.”
BackgroundType VII Secretion: A Highly Versatile Secretion System
Ates, L. S., Houben, E. N. G., & Bitter, W. (2016) · Microbiology Spectrum · doi:10.1128/microbiolspec.vmbf-0011-2015 · Cited by 100 · see citing works
“These bacteria therefore have a diderm envelope similar to mycobacteria and usually have a locus potentially coding for a T7S system (128).”
BackgroundSelf-citationProtection and pathology in TB: learning from the zebrafish model
Meijer, A. H. (2015) · Seminars in Immunopathology · doi:10.1007/s00281-015-0522-4 · Cited by 99 · see citing works
“Mtb and Mm use type VII secretion systems, named ESX-1 to ESX-5, to secrete proteins across their lipid-rich cell wall [48].”
BackgroundBehzadi, P. (2019) · Folia Microbiologica · doi:10.1007/s12223-019-00719-x · Cited by 97 · see citing works
Korotkova, N., Freire, D. M., Phan, T. H., Ummels, R., Creekmore, C. C., Evans, T. J., Wilmanns, M., Bitter, W., Parret, A. H. A., Houben, E. N. G., et al. (2014) · Molecular Microbiology · doi:10.1111/mmi.12770 · Cited by 95 · see citing works
“strates that lack classical signal sequences (Houben et al., 2014).”
BackgroundInfluentialSelf-citationComprehensive analysis of iron utilization by Mycobacterium tuberculosis
Zhang, L., Hendrickson, R. C., Meikle, V., Lefkowitz, E. J., Ioerger, T. R., & Niederweis, M. (2020) · PLoS Pathogens · doi:10.1371/journal.ppat.1008337 · Cited by 92 · see citing works
“The ESX-3 system, one of five type VII secretion systems of Mtb [16], also plays an important role in iron acquisition by Mtb [17,18,19].”
BackgroundRelease of mycobacterial antigens
Majlessi, L., Prados‐Rosales, R., Casadevall, A., & Brosch, R. (2015) · Immunological Reviews · doi:10.1111/imr.12251 · Cited by 93 · see citing works
“The resultant anti-parallel four-helix bundle constitutes a characteristic feature of the substrates of the T7S systems (56, 59).”
BackgroundPal, R., Bisht, M. K., & Mukhopadhyay, S. (2022) · FEBS Journal · doi:10.1111/febs.16369 · Cited by 94 · see citing works
Structure of EspB from the ESX-1 Type VII Secretion System and Insights into its Export Mechanism
Solomonson, M., Setiaputra, D., Makepeace, K. A. T., Lameignère, E., Petrotchenko, E. V., Conrady, D. G., Bergeron, J. R. C., Vuckovic, M., DiMaio, F., Borchers, C. H., et al. (2015) · Structure · doi:10.1016/j.str.2015.01.002 · Cited by 89 · see citing works
Interaction of Mycobacterium tuberculosis with Host Cell Death PathwaysPreprint
Srinivasan, L., Ahlbrand, S. E., & Briken, V. (2014) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a022459 · Cited by 89 · see citing works
“The ESX-5 system has also been implicated in the induction of host cell necrosis and inflammasome activation (Abdallah et al. 2011).”
Intercellular communication and conjugation are mediated by ESX secretion systems in mycobacteria
Gray, T. A., Clark, R. R., Boucher, N., Lapierre, P., Smith, C., & Derbyshire, K. M. (2016) · Science · doi:10.1126/science.aag0828 · Cited by 84 · see citing works
Blending genomes: distributive conjugal transfer in mycobacteria, a sexier form of HGT
Gray, T. A., & Derbyshire, K. M. (2018) · Molecular Microbiology · doi:10.1111/mmi.13971 · Cited by 70 · see citing works
“The core components (Ecc) and secretion substrates (EsxBA, EspB, PE/PPE) encoded by each paralogous locus are dedicated to that specific apparatus, creating a series of operationally similar, but functionally non-redundant, secretion systems (Bitter et al., 2009; Houben et al., 2014).”
BackgroundPeabody, M. A., Laird, M. R., Vlasschaert, C., Lo, R., & Brinkman, F. S. L. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1271 · Cited by 78 · see citing works
“This is believed not only because the Corynebacteriales are within the phylum Actinobacteria where the rest of the known microbes have classic Gram-positive cell envelopes, but also because the composition and biogenesis of the outer membrane is completely different from traditional classic Gram-negative outer membran…”
BackgroundFortuin, S., Tomazella, G. G., Nagaraj, N., Sampson, S. L., van Pittius, N. C. G., Soares, N. C., Wiker, H. G., de Souza, G. A., & Warren, R. M. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00006 · Cited by 80 · see citing works
van Winden, V. J. C., Ummels, R., Piersma, S. R., Jiménez, C. R., Korotkov, K. V., Bitter, W., & Houben, E. N. G. (2016) · mBio · doi:10.1128/mbio.01471-16 · Cited by 66 · see citing works
“The fifth conserved component with a predicted transmembrane domain is the subtilisin-like protease mycosin (MycP), which is among the most conserved T7S components (21).”
BackgroundSelf-citationMechanism of ESAT-6 membrane interaction and its roles in pathogenesis of Mycobacterium tuberculosis
Peng, X., & Sun, J. (2015) · Toxicon · doi:10.1016/j.toxicon.2015.10.003 · Cited by 68 · see citing works
“The ESX-1 secretion system and release of mycobacterial antigens through ESX-1 have been extensively discussed in several recent excellent reviews (Cambier et al., 2014; E. N. G. Houben et al., 2014; Majlessi et al., 2015; Simeone et al., 2015a; Stanley and Cox, 2013).”
BackgroundThe Rich Tapestry of Bacterial Protein Translocation Systems
Christie, P. J. (2019) · The Protein Journal · doi:10.1007/s10930-019-09862-3 · Cited by 64 · see citing works
Martínez‐García, P. M., Ramos, C., & Rodríguez‐Palenzuela, P. (2015) · PLoS ONE · doi:10.1371/journal.pone.0119317 · Cited by 62 · see citing works
“Similarly, Gram-positive bacteria with a cell wall heavily modified by lipids, such as mycobacteria, have also evolved refined machineries for protein secretion [4].”
BackgroundVerma, R., Pinto, S. M., Patil, A. H., Advani, J., Subba, P., Kumar, M., Sharma, J. N., Dey, G., Ravikumar, R., Buggi, S., et al. (2017) · Journal of Proteome Research · doi:10.1021/acs.jproteome.6b00983 · Cited by 60 · see citing works
Intestinal M cells: Tireless samplers of enteric microbiota
Kanaya, T., Williams, I. R., & Ohno, H. (2019) · Traffic · doi:10.1111/tra.12707 · Cited by 60 · see citing works
Type VII Secretion Systems in Gram-Positive Bacteria
Bottai, D., Gröschel, M. I., & Brosch, R. (2015) · Current topics in microbiology and immunology · doi:10.1007/82_2015_5015 · Cited by 57 · see citing works
“…identified by in silico analyses in other closely related high-C+G bacterial species (Actinobacteria), as well as in more distantly related Gram-positive bacteria belonging to the low-C+G group (Firmicutes) of Gram-positive bacteria (Gey Van Pittius et al. 2001; Pallen 2002; Houben et al. 2014).”
BackgroundA Duplicated ESAT-6 Region of ESX-5 Is Involved in Protein Export and Virulence of Mycobacteria
Shah, S., Cannon, J. R., Fenselau, C., & Briken, V. (2015) · Infection and Immunity · doi:10.1128/iai.00827-15 · Cited by 56 · see citing works
“Another characteristic of ESX and PE/PPE secretion substrates is the formation of heterodimers, which are essential for successful secretion and result in the generation of a characteristic four-helix bundle (5).”
BackgroundInfluentialBachmann, N. L., Salamzade, R., Manson, A. L., Whittington, R. J., Sintchenko, V., Earl, A. M., & Marais, B. J. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.03019 · Cited by 58 · see citing works
Phosphate starvation: a novel signal that triggers ESX‐5 secretion in Mycobacterium tuberculosis
Elliott, S. R., & Tischler, A. D. (2016) · Molecular Microbiology · doi:10.1111/mmi.13332 · Cited by 54 · see citing works
“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.”
BackgroundInfluentialWhen Dicty Met Myco, a (Not So) Romantic Story about One Amoeba and Its Intracellular Pathogen
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 50 · see citing works
“avium (Houben et al., 2014) does not escape its MCV (Hagedorn et al.”
BackgroundKhubaib, M., Sheikh, J. A., Pandey, S., Battu, S., Bhuwan, M., Khan, N., Hasnain, S. E., & Ehtesham, N. Z. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00719 · Cited by 56 · see citing works
“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…”
InfluentialInhibiting Mycobacterium tuberculosis within and without
Cole, S. T. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0506 · Cited by 55 · see citing works
Modular Organization of the ESX-5 Secretion System in Mycobacterium tuberculosis
Shah, S., & Briken, V. (2016) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2016.00049 · Cited by 54 · see citing works
“This property of co-dependency seems to be confined to the Esx and Esp proteins of the ESX-1 system, since there is no such evidence for this phenomenon in the ESX-5 system (Sampson, 2011; Houben et al., 2014).”
BackgroundThe Mycobacterium tuberculosis transcriptional landscape under genotoxic stress
Namouchi, A., Gómez-Muñoz, M., Frye, S. A., Moen, L. V., Rognes, T., Tønjum, T., & Balasingham, S. V. (2016) · BMC Genomics · doi:10.1186/s12864-016-3132-1 · Cited by 52 · see citing works
“The T7SS, a mycobacterial specialised secretion machinery, translocates different effectors throughout the cell wall [45, 46] and plays a major role in the virulence of Mtb [45, 47].”
BackgroundESX/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
Structure and Function of the Mycobacterial Type VII Secretion Systems
Bunduc, C. M., Bitter, W., & Houben, E. N. G. (2020) · Annual Review of Microbiology · doi:10.1146/annurev-micro-012420-081657 · Cited by 50 · see citing works
“Nevertheless, we are only starting to get real mechanistic insight into substrate recognition by and transport throughT7SSs, as studies to address this are complicated due to the intricate interplay between various substrates and the localization of the T7SS membrane complex in the relatively inaccessible mycobacteria…”
BackgroundInfluentialSelf-citationComparative genome analyses of mycobacteria give better insights into their evolution
Wee, W. Y., Dutta, A., & Choo, S. W. (2017) · PLoS ONE · doi:10.1371/journal.pone.0172831 · Cited by 52 · see citing works
Structure of EspB, a secreted substrate of the ESX-1 secretion system of Mycobacterium tuberculosis
Korotkova, N., Piton, J., Wagner, J. M., Boy‐Röttger, S., Japaridze, A., Evans, T. J., Cole, S. T., Pojer, F., & Korotkov, K. V. (2015) · Journal of Structural Biology · doi:10.1016/j.jsb.2015.06.003 · Cited by 51 · see citing works
“, 1998), and three systems (ESX-1, ESX-3 and ESX-5) have been shown to be active in secretion (Houben et al., 2014).”
Self-citationEisenreich, W., Rudel, T., Heesemann, J., & Goebel, W. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00316 · Cited by 50 · see citing works
“These pathogens possess type 7 protein secretion systems (ESX/T7SS) that secrete proteins some of which are clearly involved in pathogenicity and host cell interaction (Simeone et al., 2009; Houben et al., 2014).”
BackgroundRegulation of Three Virulence Strategies of Mycobacterium tuberculosis: A Success Story
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 48 · see citing works
“The ESX-3 secretion system is the only one of the five ESX systems that is essential for in vitro growth of Mtb [94,95].”
BackgroundMycobacterium tuberculosis in the Face of Host-Imposed Nutrient Limitation
Berney, M., & Berney‐Meyer, L. (2017) · Microbiology Spectrum · doi:10.1128/microbiolspec.tbtb2-0030-2016 · Cited by 47 · see citing works
Ferrell, K. C., Johansen, M. D., Triccas, J. A., & Counoupas, C. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.842017 · Cited by 45 · see citing works
Bosserman, R. E., Nguyen, T. T. M., Sanchez, K. G., Chirakos, A. E., Ferrell, M. J., Thompson, C. R., Champion, M. M., Abramovitch, R. B., & Champion, P. A. D. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1710167114 · Cited by 44 · see citing works
Extensive genomic diversity among Mycobacterium marinum strains revealed by whole genome sequencing
Das, S., Pettersson, B. M. F., Behra, P. R. K., Mallick, A., Cheramie, M. N., Ramesh, M., Shirreff, L., DuCote, T. J., Dasgupta, S., Ennis, D. G., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-30152-y · Cited by 49 · see citing works
Luò, T., Xu, P., Zhang, Y., Porter, J. L., Ghanem, M., Liu, Q., Jiang, Y. Z., Li, J., Miao, Q., Hu, B., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-22760-6 · Cited by 47 · see citing works
Transcriptome analysis of mycobacteria in sputum samples of pulmonary tuberculosis patients
Sharma, S., Ryndak, M. B., Aggarwal, A. N., Yadav, R., Sethi, S. K., Masih, S., Laal, S., & Verma, I. (2017) · PLoS ONE · doi:10.1371/journal.pone.0173508 · Cited by 45 · see citing works
Esx 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
ESX secretion system: The gatekeepers of mycobacterial survivability and pathogenesis
Roy, S., Ghatak, D., Das, P., & Dasgupta, S. B. (2020) · European Journal of Microbiology and Immunology · doi:10.1556/1886.2020.00028 · Cited by 41 · see citing works
“Thorough knowledge of the mycobacterial protein export systems would help to understand the physiology and pathogenesis of Mtb and thereby aid in future drug development [8, 9].”
BackgroundHost-Pathogen Interaction as a Novel Target for Host-Directed Therapies in Tuberculosis
Abreu, R. B., Giri, P. K., & Quinn, F. D. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01553 · Cited by 43 · see citing works
“ESAT6/CF10 proteins, secreted by ESX-1 T7SS, have cell membrane lysis properties (132) and likely are involved in bacterial escape from the phagosome to the cytoplasm in dendritic cells (12, 133, 134).”
BackgroundSangal, V., Blom, J., Sutcliffe, I. C., von Hunolstein, C., Burkovski, A., & Hoskisson, P. A. (2015) · BMC Genomics · doi:10.1186/s12864-015-1980-8 · Cited by 42 · see citing works
“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 · see citing works
“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 · see citing works
“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 39 · see citing works
“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 · see citing works
Self-citationSoto-Ramírez, M. D., Aguilar-Ayala, D. A., García-Morales, L., Rodriguez-Peredo, S. M., Badillo-López, C., Rios-Muñiz, D. E., Meza-Segura, M., Rivera-Morales, G. Y., León-Solís, L. E., Cerna-Cortés, J. F., et al. (2016) · Tuberculosis · doi:10.1016/j.tube.2016.12.004 · Cited by 38 · see citing works
“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 · see citing works
“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 36 · see citing works
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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
Terrasse, R., Amoroso, A. M., Vernet, T., & Guilmi, A. M. D. (2015) · PLoS ONE · doi:10.1371/journal.pone.0125377 · Cited by 32 · see citing works
“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 30 · see citing works
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“Mycobacterial genomes harbor up to five different T7SS gene clusters, designated ESX-1 through ESX-5 (48).”
BackgroundClark, R. R., Judd, J., Lasek-Nesselquist, E., Montgomery, S. A., Hoffmann, J. G., Derbyshire, K. M., & Gray, T. A. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1804227115 · Cited by 29 · see citing works
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The EXIT Strategy: an Approach for Identifying Bacterial Proteins Exported during Host Infection
Perkowski, E. F., Zulauf, K. E., Weerakoon, D. R., Hayden, J., Ioerger, T. R., Oreper, D., Gomez, S. M., Sacchettini, J. C., & Braunstein, M. (2017) · mBio · doi:10.1128/mbio.00333-17 · Cited by 30 · see citing works
Lagune, M., Petit, C., Sotomayor, F. V., Johansen, M. D., Beckham, K. S. H., Ritter, C., Girard-Misguich, F., Wilmanns, M., Kremer, L., Maurer, F. P., et al. (2021) · Microbiology · doi:10.1099/mic.0.001054 · Cited by 27 · see citing works
Conserved ESX-1 Substrates EspE and EspF Are Virulence Factors That Regulate Gene Expression
Chirakos, A. E., Nicholson, K. R., Huffman, A., & Champion, P. A. D. (2020) · Infection and Immunity · doi:10.1128/iai.00289-20 · Cited by 26 · see citing works
“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 29 · see citing works
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 26 · see citing works
“mycobacteria, Microbiol Spectrum 7(4):GPP3-0043-2018.”
BackgroundInfluentialSelf-citationHosseini, R., Lamers, G. E. M., Soltani, H. M., Meijer, A. H., Spaink, H. P., & Schaaf, M. J. M. (2016) · Journal of Cell Science · doi:10.1242/jcs.135194 · Cited by 24 · see citing works
“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 · see citing works
Tuukkanen, A. T., Freire, D. M., Chan, S., Arbing, M. A., Reed, R. W., Evans, T. J., Zenkevičiūtė, G., Kim, J. S., Kahng, S., Sawaya, M. R., et al. (2018) · Journal of Molecular Biology · doi:10.1016/j.jmb.2018.11.003 · Cited by 25 · see citing works
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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 · see citing works
“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
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“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 · see citing works
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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 22 · see citing works
“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 21 · see citing works
“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 21 · see citing works
“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 19 · see citing works
- 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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