Essential Role of the ESX-5 Secretion System in Outer Membrane Permeability of Pathogenic Mycobacteria
Open accessAbstract
Mycobacteria possess different type VII secretion (T7S) systems to secrete proteins across their unusual cell envelope. One of these systems, ESX-5, is only present in slow-growing mycobacteria and responsible for the secretion of multiple substrates. However, the role of ESX-5 substrates in growth and/or virulence is largely unknown. In this study, we show that esx-5 is essential for growth of both Mycobacterium marinum and Mycobacterium bovis. Remarkably, this essentiality can be rescued by increasing the permeability of the outer membrane, either by altering its lipid composition or by the introduction of the heterologous porin MspA. Mutagenesis of the first nucleotide-binding domain of the membrane ATPase EccC5 prevented both ESX-5-dependent secretion and bacterial growth, but did not affect ESX-5 complex assembly. This suggests that the rescuing effect is not due to pores formed by the ESX-5 membrane complex, but caused by ESX-5 activity. Subsequent proteomic analysis to identify crucial ESX-5 substrates confirmed that all detectable PE and PPE proteins in the cell surface and cell envelope fractions were routed through ESX-5. Additionally, saturated transposon-directed insertion-site sequencing (TraDIS) was applied to both wild-type M. marinum cells and cells expressing mspA to identify genes that are not essential anymore in the presence of MspA. This analysis confirmed the importance of esx-5, but we could not identify essential ESX-5 substrates, indicating that multiple of these substrates are together responsible for the essentiality. Finally, examination of phenotypes on defined carbon sources revealed that an esx-5 mutant is strongly impaired in the uptake and utilization of hydrophobic carbon sources. Based on these data, we propose a model in which the ESX-5 system is responsible for the transport of cell envelope proteins that are required for nutrient uptake. These proteins might in this way compensate for the lack of MspA-like porins in slow-growing mycobacteria.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
ESX-5 was suggested to be crucial for nutrient uptake and for the export of members of the PE and PPE protein families.
“ESX-5 was suggested to be crucial for nutrient uptake and for the export of members of the PE and PPE protein families (9,32,33).”
From ESX/Type VII Secretion Systems—An Important Way Out for Mycobacterial Proteins (2019) · cites this paper as [33]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Bergey's Manual of Systematic Bacteriology
(1990) · Annals of Internal Medicine · doi:10.7326/0003-4819-112-5-391_3 · Cited by 15,633 · see citing works
Cox, J., & Mann, M. (2008) · Nature Biotechnology · doi:10.1038/nbt.1511 · Cited by 14,855 · see citing works
Calamita, E., Schmid, M., Kunz, M., Ndebele-Murisa, M. R., Magadza, C. H. D., Nyambe, I., & Wehrli, B. (2019) · Figshare · doi:10.26181/6153922fe919c · Cited by 4,222 · see citing works
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 · see citing works
A Model for Random Sampling and Estimation of Relative Protein Abundance in Shotgun Proteomics
Liu, H., Sadygov, R. G., & Yates, J. R. (2004) · Analytical Chemistry · doi:10.1021/ac0498563 · Cited by 2,486 · see citing works
Brennan, P. J., & Nikaido, H. (1995) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.64.070195.000333 · Cited by 1,953 · see citing works
New use of BCG for recombinant vaccines
Stover, C. K., de la Cruz, V. F., Fuerst, T. R., Burlein, J. E., Benson, L. A., Bennett, L. T., Bansal, G. P., Young, J. F., Lee, M., Hatfull, G. F., et al. (1991) · Nature · doi:10.1038/351456a0 · Cited by 1,492 · see citing works
Griffin, J. E., Gawronski, J. D., DeJesus, M. A., Ioerger, T. R., Akerley, B. J., & Sassetti, C. M. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002251 · Cited by 1,048 · 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
Simultaneous assay of every Salmonella Typhi gene using one million transposon mutantsPreprint
Langridge, G. C., Phan, M., Turner, D., Perkins, T. T., Parts, L., Haase, J. K., Charles, I. G., Maskell, D. J., Peters, S. E., Gordon Dougan, B., et al. (2009) · Genome Research · doi:10.1101/gr.097097.109 · Cited by 618 · see citing works
Camacho, L. R., Ensergueix, D., Pérez‐Herrán, E., Gicquel, B., & Guilhot, C. (1999) · Molecular Microbiology · doi:10.1046/j.1365-2958.1999.01593.x · Cited by 616 · see citing works
Hoffmann, C., Leis, A., Niederweis, M., Plitzko, J. M., & Engelhardt, H. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0709530105 · Cited by 596 · see citing works
Daniel, J., Maamar, H., Deb, C., Sirakova, T., & Kolattukudy, P. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002093 · Cited by 595 · 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-citationThe MycoBrowser portal: A comprehensive and manually annotated resource for mycobacterial genomes
Kapopoulou, A., Lew, J. M., & Cole, S. T. (2010) · Tuberculosis · doi:10.1016/j.tube.2010.09.006 · Cited by 490 · see citing works
Direct Visualization of the Outer Membrane of Mycobacteria and Corynebacteria in Their Native State
Zuber, B., Chami, M., Houssin, C., Dubochet, J., Griffiths, G., & Daffé, M. (2008) · Journal of Bacteriology · doi:10.1128/jb.01919-07 · Cited by 458 · 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-citationAnalysis of the Phthiocerol Dimycocerosate Locus ofMycobacterium tuberculosis
Camacho, L. R., Constant, P., Raynaud, C., Lanéelle, M., Triccas, J. A., Gicquel, B., Daffé, M., & Guilhot, C. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m100662200 · Cited by 384 · 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
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-citationBardarov, S., Kriakov, J., Carrière, C., Yu, S., Vaamonde, C., McAdam, R. A., Bloom, B. R., Hatfull, G. F., & Jacobs, W. R. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.20.10961 · Cited by 278 · 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
ESX/type VII secretion systems and their role in host–pathogen interaction
Siméone, R., Bottai, D., & Brosch, R. (2009) · Current Opinion in Microbiology · doi:10.1016/j.mib.2008.11.003 · Cited by 250 · 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-citationTake 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 · cited 1× · 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-citationC-Terminal Signal Sequence Promotes Virulence Factor Secretion in Mycobacterium tuberculosis
Champion, P. A. D., Stanley, S. A., Champion, M. M., Brown, E. J., & Cox, J. S. (2006) · Science · doi:10.1126/science.1131167 · Cited by 219 · 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-citationSerafini, A., Boldrin, F., Palù, G., & Manganelli, R. (2009) · Journal of Bacteriology · doi:10.1128/jb.00756-09 · Cited by 198 · see citing works
Gao, L., Laval, F., Lawson, E. H., Groger, R. K., Woodruff, A., Morisaki, J. H., Cox, J. S., Daffé, M., & Brown, E. J. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03667.x · Cited by 194 · 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-citationPham, T. V., Piersma, S. R., Warmoes, M. O., & Jiménez, C. R. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp677 · Cited by 182 · see citing works
Self-citationMycobacterial Cytochrome P450 125 (Cyp125) Catalyzes the Terminal Hydroxylation of C27 Steroids
Capyk, J. K., Kalscheuer, R., Stewart, G. R., Liu, J., Kwon, H., Zhao, R., Okamoto, S., Jacobs, W. R., Eltis, L. D., & Mohn, W. W. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.072132 · Cited by 174 · see citing works
Self-citationEoh, H., & Rhee, K. Y. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1400390111 · Cited by 170 · see citing works
Composition of the type <scp>VII</scp> secretion system membrane complex
Houben, E. N. G., Bestebroer, J., Ummels, R., Wilson, L., Piersma, S. R., Jiménez, C. R., Ottenhoff, T. H. M., Luirink, J., & Bitter, W. (2012) · Molecular Microbiology · doi:10.1111/j.1365-2958.2012.08206.x · Cited by 168 · see citing works
Self-citationRapid Methods and Automation in Microbiology and Immunology
Habermehl, K. ‐. (1985) · Springer eBooks · doi:10.1007/978-3-642-69943-6 · Cited by 166 · see citing works
Cloning of the mspA gene encoding a porin from Mycobacterium smegmatis
Niederweis, M., Ehrt, S., Heinz, C., Klöcker, U., Karosi, S., Swiderek, K. M., Riley, L. W., & Benz, R. (1999) · Molecular Microbiology · doi:10.1046/j.1365-2958.1999.01472.x · Cited by 165 · see citing works
MspA provides the main hydrophilic pathway through the cell wall of Mycobacterium smegmatis
Stahl, C., Kubetzko, S., Kaps, I., Seeber, S., Engelhardt, H., & Niederweis, M. (2001) · Molecular Microbiology · doi:10.1046/j.1365-2958.2001.02394.x · Cited by 163 · see citing works
Sirakova, T. D., Dubey, V. S., Deb, C., Daniel, J., Korotkova, T. A., Abomoelak, B., & Kolattukudy, P. E. (2006) · Microbiology · doi:10.1099/mic.0.28993-0 · Cited by 158 · see citing works
Domenech, P., & Reed, M. B. (2009) · Microbiology · doi:10.1099/mic.0.029199-0 · Cited by 158 · see citing works
Identification of a Novel Multidrug Efflux Pump of Mycobacterium tuberculosis
Danilchanka, O., Mailaender, C., & Niederweis, M. (2008) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00298-08 · Cited by 154 · 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
Agrobacterium VirB10, an ATP energy sensor required for type IV secretion
Cascalès, E., & Christie, P. J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0405843101 · 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-citationARTIST: High-Resolution Genome-Wide Assessment of Fitness Using Transposon-Insertion Sequencing
Pritchard, J. R., Chao, M. C., Abel, S., Davis, B. M., Baranowski, C., Zhang, Y. J., Rubin, E. J., & Waldor, M. K. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004782 · Cited by 146 · see citing works
Escherichia coli-mycobacteria shuttle vectors for operon and gene fusions to lacZ: the pJEM series
Timm, J., Lim, E. M., & Gicquel, B. (1994) · Journal of Bacteriology · doi:10.1128/jb.176.21.6749-6753.1994 · Cited by 141 · 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-citationAn 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
Cascioferro, A., Delogu, G., Colone, M., Sali, M., Stringaro, A., Arancia, G., Fadda, G., Palù, G., & Manganelli, R. (2007) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.06023.x · Cited by 120 · see citing works
Multidrug Resistance of a Porin Deletion Mutant of Mycobacterium smegmatis
Stephan, J., Mailaender, C., Etienne, G., Daffé, M., & Niederweis, M. (2004) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.48.11.4163-4170.2004 · Cited by 120 · see citing works
Yu, J., Tran, V., Li, M., Huang, X., Niu, C., Wang, D., Zhu, J., Wang, J., Gao, Q., & Liu, J. (2012) · Infection and Immunity · doi:10.1128/iai.06370-11 · Cited by 115 · see citing works
The growth rate of Mycobacterium smegmatis depends on sufficient porin‐mediated influx of nutrients
Stephan, J., Bender, J. K., Wolschendorf, F., Hoffmann, C., Roth, E., Mailänder, C., Engelhardt, H., & Niederweis, M. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.04878.x · Cited by 112 · 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
Moncalián, G., Cabezón, E., Alkorta, I., Valle, M., Moro, F., Valpuesta, J., Goñi, F. M., & de la Cruz, F. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.51.36117 · Cited by 106 · see citing works
Efficient switching of mycobacteriophage L5-based integrating plasmids inMycobacterium tuberculosis
Pashley, C. A., & Parish, T. (2003) · FEMS Microbiology Letters · doi:10.1016/s0378-1097(03)00823-1 · Cited by 102 · see citing works
Parish, T., & Stoker, N. G. (1998) · Humana Press eBooks · doi:10.1385/0896034712 · Cited by 96 · see citing works
Preparation of Cell-Wall Fractions from Mycobacteria
Besra, G. S. (2003) · Humana Press eBooks · doi:10.1385/0-89603-471-2:91 · Cited by 94 · see citing works
Improved tetracycline repressors for gene silencing in mycobacteria
Klotzsche, M., Ehrt, S., & Schnappinger, D. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp015 · Cited by 94 · see citing works
Tubercle bacilli rely on a type VII army for pathogenicity
Stoop, E. J. M., Bitter, W., & van der Sar, A. M. (2012) · Trends in Microbiology · doi:10.1016/j.tim.2012.07.001 · Cited by 90 · see citing works
Self-citationStructure 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
Whole gel processing procedure for GeLC-MS/MS based proteomics
Piersma, S. R., Warmoes, M. O., de Wit, M., de Reus, I., Knol, J. C., & Jiménez, C. R. (2013) · Proteome Science · doi:10.1186/1477-5956-11-17 · Cited by 87 · see citing works
Self-citationSpecific Chaperones for the Type VII Protein Secretion Pathway
Daleke, M. H., van der Woude, A. D., Parret, A. H. A., Ummels, R., de Groot, A. M., Watson, D., Piersma, S. R., Jiménez, C. R., Luirink, J., Bitter, W., et al. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.397596 · Cited by 81 · see citing works
Self-citationPurdy, G. E., Niederweis, M., & Russell, D. G. (2009) · Molecular Microbiology · doi:10.1111/j.1365-2958.2009.06801.x · Cited by 75 · see citing works
Kirksey, M., Tischler, A. D., Siméone, R., Hisert, K. B., Uplekar, S. M., Guilhot, C., & McKinney, J. D. (2011) · Infection and Immunity · doi:10.1128/iai.00097-11 · Cited by 73 · 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-citationChaturvedi, R., Bansal, K., Yeddula, N., Kapoor, N., Namineni, S., Togarsimalemath, S. K., Chandra, N. R., Mishra, S., Ajitkumar, P., Joshi, B., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.135251 · Cited by 66 · see citing works
Weerdenburg, E. M., Abdallah, A. M., Rangkuti, F., Ghany, M. A. E., Otto, T. D., Adroub, S. A., Douwe Molenaar, B., Ummels, R., ter Veen, K., van Stempvoort, G., et al. (2015) · Infection and Immunity · doi:10.1128/iai.03050-14 · Cited by 66 · see citing works
Self-citationRole of Porins in Iron Uptake byMycobacterium smegmatis
Jones, C. M., & Niederweis, M. (2010) · Journal of Bacteriology · doi:10.1128/jb.00986-10 · Cited by 65 · see citing works
The ESX-5 Associated eccB5-eccC5 Locus Is Essential for Mycobacterium tuberculosis Viability
Luca, M. D., Bottai, D., Batoni, G., Orgeur, M., Aulicino, A., Counoupas, C., Campa, M., Brosch, R., & Esin, S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0052059 · Cited by 63 · see citing works
Hunter, R. L., Armitige, L. Y., Jagannath, C., & Actor, J. K. (2009) · Tuberculosis · doi:10.1016/s1472-9792(09)70007-1 · Cited by 55 · see citing works
Porins Are Required for Uptake of Phosphates by Mycobacterium smegmatis
Wolschendorf, F., Mahfoud, M., & Niederweis, M. (2007) · Journal of Bacteriology · doi:10.1128/jb.01600-06 · Cited by 50 · see citing works
van der Woude, A. D., Sarkar, D., Bhatt, A., Sparrius, M., Raadsen, S. A., Boon, L., Geurtsen, J., van der Sar, A. M., Luirink, J., Houben, E. N. G., et al. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.336461 · Cited by 47 · see citing works
Self-citationIncreased Phagocytosis of Mycobacterium marinum Mutants Defective in Lipooligosaccharide Production
Alibaud, L., Pawełczyk, J., Gannoun-Zaki, L., Singh, V. K., Rombouts, Y., Drancourt, M., Dziadek, J., Guérardel, Y., & Kremer, L. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.525550 · Cited by 40 · see citing works
Porins limit the intracellular persistence of Mycobacterium smegmatis
Sharbati, S., Stephan, J., Holland, G., Appel, B., Niederweis, M., & Lewin, A. (2005) · Microbiology · doi:10.1099/mic.0.27969-0 · Cited by 38 · see citing works
van der Woude, A. D., Mahendran, K. R., Ummels, R., Piersma, S. R., Pham, T. V., Jiménez, C. R., de Punder, K., van der Wel, N. N., Winterhalter, M., Luirink, J., et al. (2013) · Journal of Bacteriology · doi:10.1128/jb.02236-12 · Cited by 30 · see citing works
Self-citationRapid methods and automation in microbiology and immunology.
Spencer, R. C., Wright, E., & Newsom, S. W. B. (1994) · Cited by 13 · see citing works
Extraction and Chromatographic Analysis of Characteristic Mycobacterial Lipids
Minnikin, D. E., Dobson, G., & Parlett, J. H. (1985) · Springer eBooks · doi:10.1007/978-3-642-69943-6_36 · Cited by 7 · see citing works
Flagged first, then by citations
1 of the 80 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
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
Augenstreich, J., Arbues, A., Simeone, R., Haanappel, E., Wegener, A., Sayes, F., Le Chevalier, F., Chalut, C., Malaga, W., Guilhot, C., et al. (2017) · Cellular Microbiology · doi:10.1111/cmi.12726 · Cited by 240 · see citing works
PE/PPE proteins mediate nutrient transport across the outer membrane of Mycobacterium tuberculosis
Wang, Q., Boshoff, H. I., Harrison, J. R., Ray, P. C., Green, S. R., Wyatt, P. G., & Barry, C. E. (2020) · Science · doi:10.1126/science.aav5912 · Cited by 189 · see citing works
Mutations in ppe38 block PE_PGRS secretion and increase virulence of Mycobacterium tuberculosis
Ates, L. S., Dippenaar, A., Ummels, R., Piersma, S. R., van der Woude, A. D., van der Kuij, K., Chevalier, F. L., Mata‐Espinosa, D., Barrios‐Payán, J., Marquina‐Castillo, B., et al. (2018) · Nature Microbiology · doi:10.1038/s41564-017-0090-6 · Cited by 126 · see citing works
Self-citationDumas, E., Christina Boritsch, E., Vandenbogaert, M., Rodríguez de la Vega, R. C., Thiberge, J.-M., Caro, V., Gaillard, J.-L., Heym, B., Girard-Misguich, F., Brosch, R., et al. (2016) · Genome Biology and Evolution · doi:10.1093/gbe/evw001 · Cited by 112 · 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
New insights into the mycobacterial PE and PPE proteins provide a framework for future research
Ates, L. S. (2019) · Molecular Microbiology · doi:10.1111/mmi.14409 · Cited by 112 · see citing works
Self-citationBeckham, 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
Self-citationType VII secretion systems: structure, functions and transport models
Rivera-Calzada, Á., Famelis, N., Llorca, Ó., & Geibel, S. (2021) · Nature Reviews Microbiology · doi:10.1038/s41579-021-00560-5 · Cited by 105 · see citing works
Type 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
Self-citationAbdallah, A. M., Hill-Cawthorne, G. A., Otto, T. D., Coll, F., Guerra‐Assunção, J. A., Gao, G., Naeem, R., Ansari, H. R., Malas, T. B., Adroub, S. A., et al. (2015) · Scientific Reports · doi:10.1038/srep15443 · Cited by 96 · see citing works
Self-citationGenetic and metabolic regulation of Mycobacterium tuberculosis acid growth arrest
Baker, J. J., & Abramovitch, R. B. (2018) · Scientific Reports · doi:10.1038/s41598-018-22343-4 · Cited by 96 · see citing works
Mycobacteriosis and Infections with Non-tuberculous Mycobacteria in Aquatic Organisms: A Review
Delghandi, M. R., El‐Matbouli, M., & Menanteau‐Ledouble, S. (2020) · Microorganisms · doi:10.3390/microorganisms8091368 · Cited by 92 · see citing works
Ates, L. S., van der Woude, A. D., Bestebroer, J., van Stempvoort, G., Musters, R. J. P., García-Vallejo, J. J., Picavet, D. I., van de Weerd, R., Maletta, M., Kuijl, C. P., et al. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1005696 · Cited by 86 · see citing works
Self-citationAcid Fasting: Modulation of Mycobacterium tuberculosis Metabolism at Acidic pH
Baker, J. J., Dechow, S. J., & Abramovitch, R. B. (2019) · Trends in Microbiology · doi:10.1016/j.tim.2019.06.005 · Cited by 83 · see citing works
White, D. W., Elliott, S. R., Odean, E. J., Bemis, L., & Tischler, A. D. (2018) · mBio · doi:10.1128/mbio.00778-18 · Cited by 77 · see citing works
The plasmid-mediated evolution of the mycobacterial ESX (Type VII) secretion systems
Newton-Foot, M., Warren, R. M., Sampson, S. L., van Helden, P. D., & Gey van Pittius, N. C. (2016) · BMC Evolutionary Biology · doi:10.1186/s12862-016-0631-2 · Cited by 75 · see citing works
Transporters Involved in the Biogenesis and Functionalization of the Mycobacterial Cell Envelope
Jackson, M., Stevens, C. M., Zhang, L., Zgurskaya, H. I., & Niederweis, M. (2020) · Chemical Reviews · doi:10.1021/acs.chemrev.0c00869 · Cited by 68 · see citing works
Santucci, P., Bouzid, F., Smichi, N., Poncin, I., Kremer, L., de Chastellier, C., Drancourt, M., & Canaan, S. (2016) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2016.00122 · Cited by 68 · 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
Self-citationTuberculosis: Past, present and future of the treatment and drug discovery research
Bendre, A. D., Peters, P. J., & Kumar, J. (2021) · Current Research in Pharmacology and Drug Discovery · doi:10.1016/j.crphar.2021.100037 · Cited by 64 · see citing works
Toxin secretion and trafficking by Mycobacterium tuberculosis
Pajuelo, D., Tak, U., Zhang, L., Danilchanka, O., Tischler, A. D., & Niederweis, M. (2021) · Nature Communications · doi:10.1038/s41467-021-26925-1 · Cited by 63 · see citing works
Transposon sequencing: methods and expanding applications
Kwon, Y. M., Ricke, S. C., & Mandal, R. K. (2015) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-015-7037-8 · Cited by 63 · see citing works
The PE-PPE Family of Mycobacterium tuberculosis: Proteins in Disguise
D'Souza, C., Kishore, U., & Tsolaki, A. G. (2022) · Immunobiology · doi:10.1016/j.imbio.2022.152321 · Cited by 58 · see citing works
An ancestral mycobacterial effector promotes dissemination of infection
Saelens, J. W., Sweeney, M. I., Viswanathan, G., Xet-Mull, A. M., Smith, K. L. J., Sisk, D. M., Hu, D. D., Cronin, R. M., Hughes, E. J., Brewer, W. J., et al. (2022) · Cell · doi:10.1016/j.cell.2022.10.019 · Cited by 57 · 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
Structure of the mycobacterial ESX-5 type VII secretion system pore complex
Beckham, K. S. H., Ritter, C., Chojnowski, G., Ziemianowicz, D. S., Mullapudi, E., Rettel, M., Savitski, M. M., Mortensen, S. A., Kosiński, J., & Wilmanns, M. (2021) · Science Advances · doi:10.1126/sciadv.abg9923 · Cited by 57 · see citing works
A 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
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
Evolution and Strain Variation in BCG
Abdallah, A. M., & Behr, M. A. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-64371-7_8 · Cited by 52 · see citing works
Self-citationPPE51 Is Involved in the Uptake of Disaccharides by Mycobacterium tuberculosis
Korycka‐Machała, M., Pawełczyk, J., Borówka, P., Dziadek, B. R., Brzostek, A. M., Kawka, M., Bekier, A., Rykowski, S., Olejniczak, A. B., Strapagiel, D., et al. (2020) · Cells · doi:10.3390/cells9030603 · Cited by 52 · see citing works
The cell envelope of Mycobacterium abscessus and its role in pathogenesis
Parmar, S., & Tocheva, E. I. (2023) · PLoS Pathogens · doi:10.1371/journal.ppat.1011318 · Cited by 51 · see citing works
ESX/Type VII Secretion Systems—An Important Way Out for Mycobacterial Proteins
Vaziri, F., & Brosch, R. (2019) · Microbiology Spectrum · doi:10.1128/microbiolspec.psib-0029-2019 · Cited by 50 · see citing works
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
Self-citationProtein tyrosine kinase, PtkA, is required for Mycobacterium tuberculosis growth in macrophages
Wong, D., Li, W., Chao, J. D., Zhou, P., Narula, G. S., Tsui, C. K. M., Ko, M., Xie, J., Martinez-Frailes, C., & Av‐Gay, Y. (2018) · Scientific Reports · doi:10.1038/s41598-017-18547-9 · Cited by 50 · see citing works
When 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
Ates, L. S., Dippenaar, A., Sayes, F., Pawlik, A., Bouchier, C., Ma, L., Warren, R. M., Sougakoff, W., Majlessi, L., van Heijst, J. W. J., et al. (2018) · Genome Biology and Evolution · doi:10.1093/gbe/evy145 · Cited by 49 · see citing works
Self-citationHealy, C. M., Gouzy, A., & Ehrt, S. (2020) · mBio · doi:10.1128/mbio.03315-19 · Cited by 49 · see citing works
Mielich‐Süss, B., Wagner, R. M., Mietrach, N., Hertlein, T., Marincola, G., Ohlsen, K., Geibel, S., & López, D. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006728 · Cited by 48 · see citing works
Osman, M. M., Pagán, A. J., Shanahan, J. K., & Ramakrishnan, L. (2020) · PLoS ONE · doi:10.1371/journal.pone.0233252 · Cited by 47 · see citing works
PPE51 mediates uptake of trehalose across the mycomembrane of Mycobacterium tuberculosis
Sait, M. R. B., Koliwer‐Brandl, H., Stewart, J. A., Swarts, B. M., Jacobsen, M., Ioerger, T. R., & Kalscheuer, R. (2022) · Scientific Reports · doi:10.1038/s41598-022-06109-7 · Cited by 45 · see citing works
Self-citationBacterial type VII secretion: An important player in host‐microbe and microbe‐microbe interactions
Tran, H. R., Grebenc, D. W., Klein, T. A., & Whitney, J. C. C. (2021) · Molecular Microbiology · doi:10.1111/mmi.14680 · Cited by 45 · see citing works
The Mycobacterium tuberculosis PE15/PPE20 complex transports calcium across the outer membrane
Boradia, V. M., Frando, A., & Grundner, C. (2022) · PLoS Biology · doi:10.1371/journal.pbio.3001906 · Cited by 44 · see citing works
Mycobacterium tuberculosis Resists Stress by Regulating PE19 Expression
Ramakrishnan, P., Aagesen, A. M., McKinney, J. D., & Tischler, A. D. (2015) · Infection and Immunity · doi:10.1128/iai.00942-15 · Cited by 44 · see citing works
Ates, L. S., Sayes, F., Frigui, W., Ummels, R., Damen, M. P. M., Bottai, D., Behr, M. A., van Heijst, J. W. J., Bitter, W., Majlessi, L., et al. (2018) · PLoS Pathogens · doi:10.1371/journal.ppat.1007139 · Cited by 44 · see citing works
Self-citationEsx Systems and the Mycobacterial Cell Envelope: What's the Connection?
Bosserman, R. E., & Champion, P. A. (2017) · Journal of Bacteriology · doi:10.1128/jb.00131-17 · Cited by 42 · see citing works
Phan, T. H., van Leeuwen, L. M., Kuijl, C. P., Ummels, R., van Stempvoort, G., Rubio-Canalejas, A., Piersma, S. R., Jiménez, C. R., van der Sar, A. M., Houben, E. N. G., et al. (2018) · PLoS Pathogens · doi:10.1371/journal.ppat.1007247 · Cited by 42 · see citing works
Self-citationKoliwer‐Brandl, H., Knobloch, P., Barisch, C., Welin, A., Hanna, N., Soldati, T., & Hilbi, H. (2019) · Cellular Microbiology · doi:10.1111/cmi.13008 · Cited by 42 · see citing works
Phan, T. H., Ummels, R., Bitter, W., & Houben, E. N. G. (2017) · Scientific Reports · doi:10.1038/srep42704 · Cited by 41 · see citing works
Self-citationCopin, R., Wang, X., Louie, E., Escuyer, V. E., Coscollá, M., Gagneux, S., Palmer, G. H., & Ernst, J. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1006111 · Cited by 41 · see citing works
Ugalde, S. O., Boot, M., Commandeur, J. N. M., Jennings, P., Bitter, W., & Vos, J. C. (2019) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-019-09697-z · Cited by 41 · see citing works
Self-citationModeling Tubercular ESX-1 Secretion Using Mycobacterium marinum
Chirakos, A. E., Balaram, A., Conrad, W. H., & Champion, P. A. D. (2020) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00082-19 · Cited by 41 · see citing works
Type 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
Self-citationProteo-genetic analysis reveals clear hierarchy of ESX-1 secretion in Mycobacterium marinum
Cronin, R. M., Ferrell, M. J., Cahir, C. W., Champion, M. M., & Champion, P. A. D. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2123100119 · Cited by 40 · see citing works
Lafuente, 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
Self-citationMycobacterial Virulence Factors: Surface-Exposed Lipids and Secreted Proteins
Ly, A., & Liu, J. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21113985 · Cited by 38 · see citing works
Tateishi, Y., Minato, Y., Baughn, A. D., Ohnishi, H., Nishiyama, A., Ozeki, Y., & Matsumoto, S. (2020) · Scientific Reports · doi:10.1038/s41598-020-62287-2 · Cited by 37 · see citing works
Multiplexed Quantitation of Intraphagocyte Mycobacterium tuberculosis Secreted Protein Effectors
Sayes, F., Blanc, C., Ates, L. S., Deboosere, N., Orgeur, M., Le Chevalier, F., Gröschel, M. I., Frigui, W., Song, O.-R., Lo-Man, R., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.03.125 · Cited by 36 · see citing works
Self-citationWagner, J. M., Chan, S., Evans, T. J., Kahng, S., Kim, J. S., Arbing, M. A., Eisenberg, D. S., & Korotkov, K. V. (2016) · BMC Structural Biology · doi:10.1186/s12900-016-0056-6 · Cited by 36 · see citing works
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
Dragset, M. S., Ioerger, T. R., Loevenich, M., Haug, M., Sivakumar, N., Marstad, A., Cardona, P.-J., Klinkenberg, G., Rubin, E. J., Steigedal, M., et al. (2019) · mSystems · doi:10.1128/msystems.00402-19 · Cited by 36 · see citing works
Ehtram, A., Shariq, M., Ali, S., Quadir, N., Sheikh, J. A., Faraz, A., Sharma, T., Ehtesham, N. Z., & Hasnain, S. E. (2021) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2021.151495 · Cited by 36 · see citing works
D iscovery of the type VII ESX‐1 secretion needle?
Ates, L. S., & Brosch, R. (2016) · Molecular Microbiology · doi:10.1111/mmi.13579 · Cited by 33 · see citing works
Self-citationDamen, M. P. M., Phan, T. H., Ummels, R., Rubio-Canalejas, A., Bitter, W., & Houben, E. N. G. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.011682 · Cited by 32 · see citing works
Self-citationThe open pan-genome architecture and virulence landscape of Mycobacterium bovis
Reis, A. C., & Cunha, M. V. (2021) · Microbial Genomics · doi:10.1099/mgen.0.000664 · Cited by 32 · see citing works
Unraveling the mechanisms of intrinsic drug resistance in Mycobacterium tuberculosis
Poulton, N. C., & Rock, J. M. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.997283 · Cited by 31 · see citing works
Crosskey, T., Beckham, K. S. H., & Wilmanns, M. (2019) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2019.11.008 · Cited by 30 · see citing works
A uniform cloning platform for mycobacterial genetics and protein production
Arnold, F. M., Hohl, M., Remm, S., Koliwer‐Brandl, H., Adenau, S., Chusri, S., Sander, P., Hilbi, H., & Seeger, M. A. (2018) · Scientific Reports · doi:10.1038/s41598-018-27687-5 · Cited by 29 · 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
Protein 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
Self-citationPriming mycobacterial ESX-secreted protein B to form a channel-like structure
Gijsbers, A., Vinciauskaite, V., Siroy, A., Gao, Y., Tria, G., Mathew, A., Sánchez‐Puig, N., López‐Iglesias, C., Peters, P. J., & Ravelli, R. B. G. (2021) · Current Research in Structural Biology · doi:10.1016/j.crstbi.2021.06.001 · Cited by 25 · see citing works
Madacki, J., Fiol, G. M., & Brosch, R. (2018) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2018.12.013 · Cited by 25 · see citing works
Boot, M., van Winden, V. J. C., Sparrius, M., van de Weerd, R., Speer, A., Ummels, R., Rustad, T. R., Sherman, D. R., & Bitter, W. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1007131 · Cited by 24 · see citing works
Self-citationMycobacterial virulence: impact on immunogenicity and vaccine research
Kroesen, V. M., Madacki, J., Frigui, W., Sayes, F., & Brosch, R. (2019) · F1000Research · doi:10.12688/f1000research.20572.1 · Cited by 24 · see citing works
Wang, Y., Tang, Y., Lin, C., Zhang, J., Mai, J., Jiang, J. H., Gao, X., Li, Y., Zhao, G., Zhang, L., et al. (2021) · iScience · doi:10.1016/j.isci.2021.103585 · Cited by 23 · see citing works
Assessing heterogeneity in oligomeric AAA+ machines
Sysoeva, T. A. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2374-z · Cited by 23 · see citing works
Zhang, Z., Dong, L., Li, X., Deng, T., & Wang, Q. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1606311 · Cited by 22 · see citing works
Mortimer, T. D., Weber, A. M., & Pepperell, C. S. (2017) · Genome Biology and Evolution · doi:10.1093/gbe/evx001 · Cited by 22 · see citing works
Substrate Interaction with the EssC Coupling Protein of the Type VIIb Secretion System
Mietrach, N., Damián-Aparicio, D., Mielich‐Süss, B., López, D., & Geibel, S. (2020) · Journal of Bacteriology · doi:10.1128/jb.00646-19 · Cited by 22 · see citing works
Introduction: Novel insights into TB research and drug discovery
Grüber, G. (2020) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2020.02.003 · Cited by 22 · see citing works
Bunduc, C. M., Ding, Y., Kuijl, C. P., Marlovits, T. C., Bitter, W., & Houben, E. N. G. (2023) · mSphere · doi:10.1128/msphere.00402-23 · Cited by 21 · see citing works
Self-citationMycobacterial type VII secretion systems
Famelis, N., Geibel, S., & van Tol, D. J. C. (2023) · Biological Chemistry · doi:10.1515/hsz-2022-0350 · Cited by 21 · see citing works
Species‐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
Self-citationMycobacterium marinum as a model for understanding principles of mycobacterial pathogenesis
Menon, A. R., Prest, R. J., Tobin, D. M., & Champion, P. A. D. (2025) · Journal of Bacteriology · doi:10.1128/jb.00047-25 · Cited by 20 · see citing works
Bendre, A. D., Peters, P. J., & Kumar, J. (2021) · The Journal of Membrane Biology · doi:10.1007/s00232-021-00179-w · Cited by 20 · see citing works
The ESX-1 Substrate PPE68 Has a Key Function in ESX-1-Mediated Secretion in Mycobacterium marinum
Damen, M. P. M., Meijers, A. S., Keizer, E., Piersma, S. R., Jiménez, C. R., Kuijl, C. P., Bitter, W., & Houben, E. N. G. (2022) · mBio · doi:10.1128/mbio.02819-22 · Cited by 20 · see citing works
Self-citationTiwari, S., Dutt, T. S., Chen, B., Chen, M., Kim, J., Dai, A. Z., Lukose, R., Shanley, C. A., Fox, A. C., Karger, B. R., et al. (2020) · Vaccine · doi:10.1016/j.vaccine.2020.08.004 · Cited by 20 · see citing works
Dechow, S. J., Baker, J. J., Murto, M., & Abramovitch, R. B. (2022) · Journal of Bacteriology · doi:10.1128/jb.00212-22 · Cited by 19 · see citing works
Yang, G., Luò, T., Sun, C., Yuan, J., Peng, X., Zhang, C., Zhai, X., & Bao, L. (2017) · Journal of Interferon & Cytokine Research · doi:10.1089/jir.2016.0126 · Cited by 19 · see citing works
Measurement of Small Molecule Accumulation into Diderm Bacteria
Ongwae, G. M., Lepori, I., Chordia, M. D., Dalesandro, B. E., Apostolos, A. J., Siegrist, M. S., & Pires, M. M. (2022) · ACS Infectious Diseases · doi:10.1021/acsinfecdis.2c00435 · Cited by 18 · see citing works
Wang, S., Cai, X., Yu, W., Zeng, S., Zhang, J., Guo, L., Gao, Y., Lu, Z., Hameed, H. M. A., Fang, C., et al. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.02763-21 · Cited by 16 · see citing works
Chaiyachat, P., Chaiprasert, A., Nonghanphithak, D., Smithtikarn, S., Kamolwat, P., Pungrassami, P., Reechaipichitkul, W., Ong, R. T., Teo, Y., & Faksri, K. (2021) · International Journal of Antimicrobial Agents · doi:10.1016/j.ijantimicag.2021.106385 · Cited by 16 · see citing works
Evolution of Tuberculosis Pathogenesis
Pepperell, C. S. (2022) · Annual Review of Microbiology · doi:10.1146/annurev-micro-121321-093031 · Cited by 16 · see citing works
A glycine-rich PE_PGRS protein governs mycobacterial actin-based motility
Hill, N. S., & Welch, M. D. (2022) · Nature Communications · doi:10.1038/s41467-022-31333-0 · Cited by 16 · see citing works
Nicholson, K. R., & Champion, P. A. D. (2022) · PLoS Pathogens · doi:10.1371/journal.ppat.1010610 · Cited by 16 · see citing works
van Winden, V. J. C., Damen, M. P. M., Ummels, R., Bitter, W., & Houben, E. N. G. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.007090 · Cited by 15 · see citing works
Self-citationMalik, A. A., Shariq, M., Sheikh, J. A., Jaiswal, U., Fayaz, H., Shrivastava, G., Ehtesham, N. Z., & Hasnain, S. E. (2024) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2024.2411264 · Cited by 15 · see citing works
MceG stabilizes the Mce1 and Mce4 transporters in Mycobacterium tuberculosis
Fieweger, R. A., Wilburn, K. M., Montague, C. R., Roszkowski, E. K., Kelly, C. M., Southard, T. L., Sondermann, H., Nazarova, E. V., & VanderVen, B. C. (2023) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2023.102910 · Cited by 15 · see citing works
Eilertson, B., Maruri, F., Blackman, A., Guo, Y. P., Herrera, M., van der Heijden, Y. F., Shyr, Y., & Sterling, T. R. (2016) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkw168 · Cited by 15 · see citing works
Heijmenberg, I., Husain, A. A., Sathkumara, H. D., Muruganandah, V., Seifert, J., Miranda‐Hernandez, S., Kashyap, R. S., Field, M. A., Gopinath, K., & Kupz, A. (2021) · Vaccine · doi:10.1016/j.vaccine.2021.08.030 · Cited by 15 · see citing works
- Authors
- 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., Abd El Ghany, M., Abdel-Haleem, A. M., Pain, A., Jiménez, C. R., Bitter, W., & Houben, E. N. G.
- Affiliations
- Amsterdam UMC Location Vrije Universiteit Amsterdam (NL)
- Heinrich Heine University Düsseldorf (DE)
- King Abdullah University of Science and Technology (SA)
- Vrije Universiteit Amsterdam (NL)
- Corresponding author
- Houben, Edith N.G.
- ORCID
- Venue
- PLOS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2015-05-04
- Volume
- 11
- Issue
- 5
- Pages
- e1005190
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC4418733
- OpenAlex
- W1508212288
- Cited by
- 185
- References
- 80
- Citations by year
- 2026: 14 · 2025: 19 · 2024: 15 · 2023: 10 · 2022: 21 · 2021: 18 · 2020: 18 · 2019: 18 · 2018: 15 · 2017: 11 · 2016: 19 · 2015: 7
- FWCI
- 13.47
- Type
- journal article
- Language
- en
- Update notices
- correction (2015-05-29)
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
- VU Research Portal (publishedVersion, other-oa)
- Pure Amsterdam UMC (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- King Abdullah University of Science and Technology Repository (King Abdullah University of Science and Technology) (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Jürgen Manchot Stiftung
- European Federation of Pharmaceutical Industries and Associations (FP7/20072013)
- European Commission (115337, 2007–2013, FP7 2007-2013, FP7/2007)
- Innovative Medicines Initiative (FP7/2007‐2013, 115337)
- 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 marinum, Mycobacterium bovis, outer membrane permeability, slow-growing mycobacteria, transposon insertion site sequencing
- MeSH terms
- Type VII Secretion Systems, Ampicillin, Bacterial Proteins, Cell Membrane Permeability, Chromatography, Liquid, DNA Transposable Elements, DNA, Bacterial, Mutation, Mycobacterium bovis, Mycobacterium tuberculosis, Gene Expression Regulation, Bacterial, Sequence Analysis, DNA, Mycobacterium marinum, Drug Resistance, Bacterial, Tandem Mass Spectrometry
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
