Tubercle bacilli rely on a type VII army for pathogenicity
Abstract
Mycobacteria, such as the major human pathogen Mycobacterium tuberculosis, have a highly unusual and characteristic diderm cell envelope that protects them against harmful conditions. Protein secretion across this hydrophobic barrier requires specialized secretion systems. Recently, a type VII secretion (T7S) pathway has been identified that fulfills this function. Pathogenic mycobacteria have up to five different T7S systems, some of which play a crucial role in virulence. The interactions between secreted substrates and host molecules are only starting to become clear and will help in furthering our understanding of the persistence of these enigmatic pathogens. In this review, we discuss current knowledge on the role of T7S systems in mycobacterial virulence.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
A number of secreted effectors, including EsxA (ESAT-6), EsxB (CFP-10), EspA, EspC, and PE/PPE proteins, have been suggested to intervene in host cellular and immune signaling pathways.
“Indeed, a number of secreted effectors, including EsxA (ESAT-6), EsxB (CFP-10), and ESX-1 secretion-associated proteins (Esp), such as EspA or EspC, as well as proteins that carry the characteristic N-terminal motifs Pro-Glu (PE) and Pro-Pro-Glu (PPE), have been suggested to intervene in host cellular and immune signaling pathways (11,24,25).”
From ESX/Type VII Secretion Systems—An Important Way Out for Mycobacterial Proteins (2019) · cites this paper as [24]
Cites
1 retracted
A β-Lactamase Based Reporter System for ESX Dependent Protein Translocation in Mycobacteria
Rosenberger, T., Brülle, J. K., & Sander, P. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035453 · Cited by 4 · see citing works
RetractedGenes 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 · see citing works
Genetic requirements for mycobacterial survival during infection
Sassetti, C. M., & Rubin, E. J. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2134250100 · Cited by 1,327 · see citing works
Molecular analysis of genetic differences between Mycobacterium bovis BCG and virulent M. bovis
Mahairas, G. G., Sabo, P. J., Hickey, M. J., Singh, D. C., & Stover, C. K. (1996) · Journal of Bacteriology · doi:10.1128/jb.178.5.1274-1282.1996 · Cited by 1,103 · see citing works
M. tuberculosis and M. leprae Translocate from the Phagolysosome to the Cytosol in Myeloid Cells
van der Wel, N., Hava, D., Houben, D., Fluitsma, D., van Zon, M., Pierson, J., Brenner, M., & Peters, P. J. (2007) · Cell · doi:10.1016/j.cell.2007.05.059 · Cited by 960 · see citing works
Revisiting the role of the granuloma in tuberculosis
Ramakrishnan, L. (2012) · Nature reviews. Immunology · doi:10.1038/nri3211 · Cited by 887 · see citing works
Mycobacterium tuberculosis: here today, and here tomorrow
Russell, D. G. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35085034 · Cited by 781 · see citing works
Type VII secretion — mycobacteria show the way
Abdallah, A. M., Gey van Pittius, N. C., DiGiuseppe Champion, P. A., Cox, J., Luirink, J., Vandenbroucke-Grauls, C. M. J. E., Appelmelk, B. J., & Bitter, W. (2007) · Nature Reviews Microbiology · doi:10.1038/nrmicro1773 · Cited by 763 · see citing works
Self-citationHsu, 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 · see citing works
Recombinant BCG exporting ESAT-6 confers enhanced protection against tuberculosis
Pym, A. S., Brodin, P., Majlessi, L., Brosch, R., Demangel, C., Williams, A., Griffiths, K. E., Marchal, G., Leclerc, C., & Cole, S. T. (2003) · Nature Medicine · doi:10.1038/nm859 · Cited by 644 · see citing works
Deletion of RD1 from<i>Mycobacterium tuberculosis</i>Mimics Bacille Calmette‐Guérin Attenuation
Lewis, K. N., Liao, R., Guinn, K. M., Hickey, M. J., Smith, S., Behr, M. A., & Sherman, D. R. (2003) · The Journal of Infectious Diseases · doi:10.1086/345862 · Cited by 588 · see citing works
Sørensen, A. L., Nagai, S., Houen, G., Andersen, P., & Andersen, A. B. (1995) · Infection and Immunity · doi:10.1128/iai.63.5.1710-1717.1995 · Cited by 586 · see citing works
Stinear, T. P., Seemann, T., Harrison, P. F., Jenkin, G. A., Davies, J. K., Johnson, P. D. R., Abdellah, Z., Arrowsmith, C., Chillingworth, T., Churcher, C., et al. (2008) · Genome Research · doi:10.1101/gr.075069.107 · Cited by 570 · see citing works
Stanley, S. A., Raghavan, S., Hwang, W. W., & Cox, J. S. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2235593100 · Cited by 570 · see citing works
Phagosomal Rupture by Mycobacterium tuberculosis Results in Toxicity and Host Cell Death
Simeone, R., Bobard, A., Lippmann, J., Bitter, W., Majlessi, L., Brosch, R., & Enninga, J. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002507 · Cited by 561 · see citing works
Self-citationGuinn, K. M., Hickey, M. J., Mathur, S. K., Zakel, K. L., Grotzke, J. E., Lewinsohn, D. M., Smith, S., & Sherman, D. R. (2004) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03844.x · Cited by 508 · see citing works
Rodríguez, G. M., Voskuil, M. I., Gold, B., Schoolnik, G. K., & Smith, I. (2002) · Infection and Immunity · doi:10.1128/iai.70.7.3371-3381.2002 · Cited by 491 · see citing works
van Pittius, N. C. G., Sampson, S. L., Lee, H., Kim, Y., van Helden, P. D., & Warren, R. M. (2006) · BMC Evolutionary Biology · doi:10.1186/1471-2148-6-95 · Cited by 423 · see citing works
ESX‐1‐mediated translocation to the cytosol controls virulence of mycobacteria
Houben, D., Demangel, C., van Ingen, J., Pérez, J., Baldeón, L., Abdallah, A. M., Caleechurn, L., Bottai, D., van Zon, M., de Punder, K., et al. (2012) · Cellular Microbiology · doi:10.1111/j.1462-5822.2012.01799.x · Cited by 415 · see citing works
Self-citationMutually dependent secretion of proteins required for mycobacterial virulence.
Fortune, S. M., Jaeger, A., Sarracino, D. A., Chase, M. R., Sassetti, C. M., Sherman, D. R., Bloom, B. R., & Rubin, E. J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504922102 · Cited by 396 · see citing works
Gao, L., Guo, S., McLaughlin, B., Morisaki, H., Engel, J. N., & Brown, E. J. (2004) · Molecular Microbiology · doi:10.1111/j.1365-2958.2004.04261.x · Cited by 395 · see citing works
Stinear, T. P., Seemann, T., Pidot, S. J., Frigui, W., Reysset, G., Garnier, T., Meurice, G., Simon, D., Bouchier, C., Ma, L., et al. (2007) · Genome Research · doi:10.1101/gr.5942807 · Cited by 392 · see citing works
The ESAT-6 gene cluster of Mycobacterium tuberculosis and other high G+C Gram-positive bacteria
Gey van Pittius, N. C., Gamieldien, J., Hide, W., Brown, G. D., Siezen, R. J., & Beyers, A. D. (2001) · Genome Biology · doi:10.1186/gb-2001-2-10-research0044 · Cited by 375 · see citing works
Lamichhane, G., Matteo Zignol, E., Blades, N. J., Geiman, D. E., Dougherty, A. B., Grosset, J. H. E., Broman, K. W., & Bishai, W. R. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1231432100 · Cited by 357 · see citing works
Renshaw, P. S., Panagiotidou, P., Whelan, A. O., Gordon, S. V., Hewinson, R. G., Williamson, R. A., & Carr, M. D. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m201625200 · Cited by 337 · see citing works
Swaim, L. E., Connolly, L. E., Volkman, H. E., Humbert, O., Born, D. E., & Ramakrishnan, L. (2006) · Infection and Immunity · doi:10.1128/iai.00887-06 · Cited by 329 · see citing works
Mycobacterial Esx-3 is required for mycobactin-mediated iron acquisition
Siegrist, M. S., Unnikrishnan, M., McConnell, M. J., Borowsky, M. L., Cheng, T., Siddiqi, N., Fortune, S. M., Moody, D. B., & Rubin, E. J. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900589106 · Cited by 329 · see citing works
de Jonge, M. I., Pehau‐Arnaudet, G., Fretz, M. M., Félix, R., Bottai, D., Brodin, P. M., Honoré, N., Marchal, G., Jiskoot, W., England, P., et al. (2007) · Journal of Bacteriology · doi:10.1128/jb.00469-07 · Cited by 316 · see citing works
Comprehensive analysis of exported proteins from Mycobacterium tuberculosis H37Rv
Målen, H., Berven, F. S., Fladmark, K. E., & Wiker, H. G. (2007) · PROTEOMICS · doi:10.1002/pmic.200600853 · Cited by 314 · see citing works
Brodin, P. M., Majlessi, L., Marsollier, L., de Jonge, M. I., Bottai, D., Demangel, C., Hinds, J., Neyrolles, O., Butcher, P. D., Leclerc, C., et al. (2005) · Infection and Immunity · doi:10.1128/iai.74.1.88-98.2006 · Cited by 312 · see citing works
Analysis of the proteome of Mycobacterium tuberculosis in silico
Tekaia, F., Gordon, S. V., Garnier, T., Brosch, R., Barrell, B. G., & Cole, S. T. (1999) · Tubercle and Lung Disease · doi:10.1054/tuld.1999.0220 · Cited by 311 · see citing works
Tuberculous Granuloma Formation Is Enhanced by a Mycobacterium Virulence Determinant
Volkman, H. E., Clay, H., Beery, D., Chang, J. C., Sherman, D. R., & Ramakrishnan, L. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020367 · Cited by 311 · see citing works
Systematic Genetic Nomenclature for Type VII Secretion Systems
Bitter, W., Houben, E. N. G., Bottai, D., Brodin, P., Brown, E. J., Cox, J. S., Derbyshire, K., Fortune, S. M., Gao, L.-Y., Liu, J., et al. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000507 · Cited by 307 · see citing works
Self-citationSani, M., Houben, E. N. G., Geurtsen, J., Pierson, J., de Punder, K., van Zon, M., Wever, B., Piersma, S. R., Jiménez, C. R., Daffé, M., et al. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1000794 · Cited by 306 · see citing works
Self-citationSmith, J., Manoranjan, J., Pan, M., Bohsali, A., Xu, J., Liu, J., McDonald, K. L., Szyk, A., LaRonde-LeBlanc, N. A., & Gao, L. (2008) · Infection and Immunity · doi:10.1128/iai.00614-08 · Cited by 291 · see citing works
Control of M. tuberculosis ESAT-6 Secretion and Specific T Cell Recognition by PhoP
Frigui, W., Bottai, D., Majlessi, L., Monot, M., Josselin, E., Brodin, P. M., Garnier, T., Gicquel, B., Martı́n, C., Leclerc, C., et al. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.0040033 · Cited by 283 · see citing works
Abdallah, A. M., Verboom, T., Weerdenburg, E. M., van Pittius, N. C. G., Mahasha, P. W., Jiménez, C. R., Parra, M., Cadieux, N., Brennan, M. J., Appelmelk, B. J., et al. (2009) · Molecular Microbiology · doi:10.1111/j.1365-2958.2009.06783.x · Cited by 268 · see citing works
Self-citationMycobacterial PE/PPE Proteins at the Host-Pathogen Interface
Sampson, S. L. (2011) · Clinical and Developmental Immunology · doi:10.1155/2011/497203 · Cited by 258 · see citing works
Global Analysis of theMycobacterium tuberculosisZur (FurB) Regulon
Maciag, A. E., Dainese, E., Rodríguez, G. M., Milano, A., Provvedi, R., Pasca, M. R., Smith, I., Palù, G., Riccardi, G., & Manganelli, R. (2006) · Journal of Bacteriology · doi:10.1128/jb.01190-06 · Cited by 257 · see citing works
A specific secretion system mediates PPE41 transport in pathogenic mycobacteria
Abdallah, A. M., Verboom, T., Hannes, F., Safi, M., Strong, M., Eisenberg, D. S., Musters, R. J. P., Vandenbroucke‐Grauls, C. M. J. E., Appelmelk, B. J., Luirink, J., et al. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05409.x · Cited by 234 · see citing works
Self-citationInfection by Tubercular Mycobacteria Is Spread by Nonlytic Ejection from Their Amoeba Hosts
Hagedorn, M., Rohde, K. H., Russell, D. G., & Soldati, T. (2009) · Science · doi:10.1126/science.1169381 · Cited by 222 · see citing works
Bottai, D., Di Luca, M., Majlessi, L., Frigui, W., Simeone, R., Sayes, F., Bitter, W., Brennan, M. J., Leclerc, C., Batoni, G., et al. (2012) · Molecular Microbiology · doi:10.1111/j.1365-2958.2012.08001.x · Cited by 210 · see citing works
Self-citationCritical role for NLRP3 in necrotic death triggered by <i>Mycobacterium tuberculosis</i>
Wong, K., & Jacobs Jr, W. R. (2011) · Cellular Microbiology · doi:10.1111/j.1462-5822.2011.01625.x · Cited by 209 · see citing works
Sweeney, K. A., Dao, D. N., Goldberg, M. F., Hsu, T., Venkataswamy, M. M., Henao-Tamayo, M. I., Ordway, D. J., Sellers, R. S., Jain, P., Chen, B., et al. (2011) · Nature Medicine · doi:10.1038/nm.2420 · Cited by 208 · see citing works
Secreted transcription factor controls Mycobacterium tuberculosis virulence
Raghavan, S., Manzanillo, P., Chan, K., Dovey, C., & Cox, J. S. (2008) · Nature · doi:10.1038/nature07219 · Cited by 202 · see citing works
Serafini, A., Boldrin, F., Palù, G., & Manganelli, R. (2009) · Journal of Bacteriology · doi:10.1128/jb.00756-09 · Cited by 198 · see citing works
Koo, I. C., Wang, C., Raghavan, S., Morisaki, J. H., Cox, J. S., & Brown, E. J. (2008) · Cellular Microbiology · doi:10.1111/j.1462-5822.2008.01177.x · Cited by 198 · see citing works
A mycobacterium ESX-1-secreted virulence factor with unique requirements for export.
McLaughlin, B., Chon, J. S., MacGurn, J. A., Carlsson, F., Cheng, T. L., Cox, J. S., & Brown, E. J. (2007) · PLoS Pathogens · doi:10.1371/journal.ppat.0030105 · Cited by 196 · see citing works
General secretion signal for the mycobacterial type VII secretion pathway
Daleke, M. H., Ummels, R., Bawono, P., Heringa, J., Vandenbroucke‐Grauls, C. M. J. E., Luirink, J., & Bitter, W. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1119453109 · Cited by 192 · see citing works
Self-citationA non‐RD1 gene cluster is required for Snm secretion in <i>Mycobacterium tuberculosis</i>
MacGurn, J. A., Raghavan, S., Stanley, S. A., & Cox, J. S. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.04800.x · Cited by 186 · see citing works
Brodin, P. M., Poquet, Y., Levillain, F., Péguillet, I., Larrouy-Maumus, G. J., Gilleron, M., Ewann, F., Christophe, T., Fenistein, D., Jang, J., et al. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1001100 · Cited by 186 · see citing works
MacGurn, J. A., & Cox, J. S. (2007) · Infection and Immunity · doi:10.1128/iai.01872-06 · Cited by 183 · see citing works
The ESAT-6/CFP-10 secretion system of Mycobacterium marinum modulates phagosome maturation
Tan, T., Lee, W. L., Alexander, D. C., Grinstein, S., & Liu, J. (2006) · Cellular Microbiology · doi:10.1111/j.1462-5822.2006.00721.x · Cited by 172 · see citing works
The Mycobacterial Cell Envelope
(2008) · ASM Press eBooks · doi:10.1128/9781555815783 · Cited by 170 · see citing works
Host-Detrimental Role of Esx-1-Mediated Inflammasome Activation in Mycobacterial Infection
Carlsson, F., Kim, J., Dumitru, C. D., Barck, K. H., Carano, R. A. D., Sun, M., Diehl, L. J., & Brown, E. J. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1000895 · Cited by 160 · see citing works
Converse, S. E., & Cox, J. S. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.4.1238-1245.2005 · Cited by 154 · see citing works
Abdallah, A. M., Bestebroer, J., Savage, N. D. L., de Punder, K., van Zon, M., Wilson, L., Korbee, C. J., van der Sar, A. M., Ottenhoff, T. H. M., van der Wel, N. N., et al. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1101457 · Cited by 152 · see citing works
Self-citationChampion, P. A. D., Champion, M. M., Manzanillo, P. S., & Cox, J. S. (2009) · Molecular Microbiology · doi:10.1111/j.1365-2958.2009.06821.x · Cited by 149 · see citing works
Ohol, Y. M., Goetz, D. H., Chan, K., Shiloh, M. U., Craik, C. S., & Cox, J. S. (2010) · Cell Host & Microbe · doi:10.1016/j.chom.2010.02.006 · Cited by 149 · see citing works
Daleke, M. H., Cascioferro, A., de Punder, K., Ummels, R., Abdallah, A. M., van der Wel, N. N., Peters, P. J., Luirink, J., Manganelli, R., & Bitter, W. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.204966 · Cited by 146 · see citing works
Self-citationMillington, K. A., Fortune, S. M., Low, J., Garces, A., Hingley‐Wilson, S., Wickremasinghe, M., Kon, O. M., & Lalvani, A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1015153108 · Cited by 141 · see citing works
Virulence Regulator EspR of Mycobacterium tuberculosis Is a Nucleoid-Associated Protein
Blasco, B., Chen, J. M., Hartkoorn, R. C., Sala, C., Uplekar, S. M., Rougemont, J., Pojer, F., & Cole, S. T. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002621 · Cited by 138 · see citing works
The ESX-5 Secretion System of Mycobacterium marinum Modulates the Macrophage Response
Abdallah, A. M., Savage, N. D. L., van Zon, M., Wilson, L., Vandenbroucke‐Grauls, C. M. J. E., van der Wel, N. N., Ottenhoff, T. H. M., & Bitter, W. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.10.7166 · Cited by 137 · see citing works
Self-citationCoros, A., Callahan, B., Battaglioli, E., & Derbyshire, K. M. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06299.x · Cited by 137 · see citing works
Flint, J. L., Kowalski, J. C., Karnati, P. K., & Derbyshire, K. M. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0404892101 · Cited by 134 · see citing works
Xu, J., Laine, O., Masciocchi, M., Manoranjan, J., Smith, J., Du, S., Edwards, N., Zhu, X., Fenselau, C., & Gao, L. (2007) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.05959.x · Cited by 127 · see citing works
Sayes, F., Sun, L., Luca, M. D., Siméone, R., Degaiffier, N., Fiette, L., Esin, S., Brosch, R., Bottai, D., Leclerc, C., et al. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.03.003 · Cited by 116 · see citing works
Polar Localization of Virulence-Related Esx-1 Secretion in Mycobacteria
Carlsson, F., Joshi, S. A., Rangell, L. K., & Brown, E. J. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000285 · Cited by 113 · see citing works
PE_PGRS30 is required for the full virulence of Mycobacterium tuberculosis
Iantomasi, R., Sali, M., Cascioferro, A., Palucci, I., Zumbo, A., Soldini, S., Rocca, S., Greco, E., Maulucci, G., Spirito, M. D., et al. (2011) · Cellular Microbiology · doi:10.1111/j.1462-5822.2011.01721.x · Cited by 108 · see citing works
Stoop, E. J. M., Schipper, T., Huber, S. K. R., Nezhinsky, A. E., Verbeek, F. J., Gurcha, S. S., Besra, G. S., Vandenbroucke‐Grauls, C. M. J. E., Bitter, W., & van der Sar, A. M. (2011) · Disease Models & Mechanisms · doi:10.1242/dmm.006676 · Cited by 104 · see citing works
Self-citationEspD Is Critical for the Virulence-Mediating ESX-1 Secretion System in Mycobacterium tuberculosis
Chen, J. M., Boy‐Röttger, S., Dhar, N., Sweeney, N. P., Buxton, R. S., Pojer, F., Rosenkrands, I., & Cole, S. T. (2011) · Journal of Bacteriology · doi:10.1128/jb.06417-11 · Cited by 80 · see citing works
Bottai, D., Majlessi, L., Siméone, R., Frigui, W., Laurent‐Winter, C., Lenormand, P., Chen, J. M., Rosenkrands, I., Huerre, M., Leclerc, C., et al. (2011) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiq089 · Cited by 74 · see citing works
Agarwal, N., Woolwine, S. C., Tyagi, S. K., & Bishai, W. R. (2006) · Infection and Immunity · doi:10.1128/iai.01395-06 · Cited by 71 · see citing works
Lightbody, K. L., Ilghari, D., Waters, L. C., Carey, G., Bailey, M. A., Williamson, R. A., Renshaw, P. S., & Carr, M. D. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m800123200 · Cited by 69 · see citing works
ESX-5-deficient Mycobacterium marinum is hypervirulent in adult zebrafish
Weerdenburg, E. M., Abdallah, A. M., Mitra, S., de Punder, K., van der Wel, N. N., Bird, S., Appelmelk, B. J., Bitter, W., & van der Sar, A. M. (2012) · Cellular Microbiology · doi:10.1111/j.1462-5822.2012.01755.x · Cited by 67 · see citing works
Self-citationPE_PGRS proteins are differentially expressed by Mycobacterium tuberculosis in host tissues
Delogu, G., Sanguinetti, M., Pusceddu, C., Bua, A., Brennan, M. J., Zanetti, S., & Fadda, G. (2006) · Microbes and Infection · doi:10.1016/j.micinf.2006.03.015 · Cited by 64 · see citing works
Srivastava, V., Rouanet, C., Srivastava, R., Bethunaickan, R., Locht, C., & Srivastava, B. S. (2007) · Microbiology · doi:10.1099/mic.0.2006/000547-0 · Cited by 57 · see citing works
Das, C., Ghosh, T. S., & Mande, S. S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027980 · Cited by 38 · see citing works
Transcriptional analysis of ESAT-6 cluster 3 in Mycobacterium smegmatis
Maciag, A. E., Piazza, A., Riccardi, G., & Milano, A. (2009) · BMC Microbiology · doi:10.1186/1471-2180-9-48 · Cited by 34 · see citing works
Type VII secretion in mycobacteria: classification in line with cell envelope structure
Bitter, W., Houben, E. N. G., Luirink, J., & Appelmelk, B. J. (2009) · Trends in Microbiology · doi:10.1016/j.tim.2009.05.007 · Cited by 30 · see citing works
Self-citationSingh, V. K., Srivastava, V., Singh, V., et al. (2011) · Vaccine · doi:10.1016/j.vaccine.2011.04.086 · Cited by 16 · see citing works
Quadri, L. E. N. (2014) · ASM Press eBooks · doi:10.1128/9781555815783.ch10 · Cited by 9 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Wassermann, R., Gulen, M. F., Sala, C., Perin, S. G., Lou, Y., Rybniker, J., Schmid-Burgk, J. L., Schmidt, T., Hornung, V., Cole, S. T., et al. (2015) · Cell Host & Microbe · doi:10.1016/j.chom.2015.05.003 · Cited by 401 · see citing works
Take five — Type VII secretion systems of Mycobacteria
Houben, E. N. G., Korotkov, K. V., & Bitter, W. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2013.11.003 · Cited by 223 · see citing works
Self-citationTufariello, 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
Ates, 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
Self-citationThe ESX-3 Secretion System Is Necessary for Iron and Zinc Homeostasis in Mycobacterium tuberculosis
Serafini, A., Pisu, D., Palù, G., Rodriguez, G. M., & Manganelli, R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078351 · Cited by 131 · see citing works
Release 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
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
Animal Models of Tuberculosis: Zebrafish
van Leeuwen, L. M., van der Sar, A. M., & Bitter, W. (2015) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a018580 · Cited by 53 · see citing works
Self-citationESX/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
- Authors
- Stoop, E. J. M., Bitter, W., & van der Sar, A. M.
- Affiliations
- Amsterdam UMC Location Vrije Universiteit Amsterdam (NL)
- Venue
- Trends in Microbiology
- Publisher
- Elsevier BV
- Published
- 2012-10
- Volume
- 20
- Issue
- 10
- Pages
- 477-484
- ISSN
- 0966-842X (ISSN-L)
- OpenAlex
- W2012732153
- Cited by
- 90
- References
- 82
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 2 · 2023: 3 · 2022: 3 · 2021: 4 · 2020: 6 · 2019: 6 · 2018: 5 · 2017: 2 · 2016: 15 · 2015: 10 · 2014: 13 · 2013: 12 · 2012: 1
- FWCI
- 1.43
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Trends in Microbiology (publishedVersion)
- PubMed (publishedVersion)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
- VU Research Portal (publishedVersion)
- Digital Academic REpository of VU University Amsterdam (Vrije Universiteit Amsterdam) (submittedVersion)
- Pure Amsterdam UMC (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Ministerie van Economische Zaken
- Ministerie van Onderwijs, Cultuur en Wetenschap
- 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, Mycobacterium tuberculosis, mycobacteria, virulence factors, protein secretion, host-pathogen interaction, bacterial pathogenicity
- MeSH terms
- Bacterial Proteins, Humans, Models, Biological, Mycobacterium tuberculosis, Protein Transport, Virulence Factors, Bacterial Secretion Systems
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review