Mycobacterium tuberculosis Type VII Secreted Effector EsxH Targets Host ESCRT to Impair Trafficking
Open accessAbstract
Mycobacterium tuberculosis (Mtb) disrupts anti-microbial pathways of macrophages, cells that normally kill bacteria. Over 40 years ago, D'Arcy Hart showed that Mtb avoids delivery to lysosomes, but the molecular mechanisms that allow Mtb to elude lysosomal degradation are poorly understood. Specialized secretion systems are often used by bacterial pathogens to translocate effectors that target the host, and Mtb encodes type VII secretion systems (TSSSs) that enable mycobacteria to secrete proteins across their complex cell envelope; however, their cellular targets are unknown. Here, we describe a systematic strategy to identify bacterial virulence factors by looking for interactions between the Mtb secretome and host proteins using a high throughput, high stringency, yeast two-hybrid (Y2H) platform. Using this approach we identified an interaction between EsxH, which is secreted by the Esx-3 TSSS, and human hepatocyte growth factor-regulated tyrosine kinase substrate (Hgs/Hrs), a component of the endosomal sorting complex required for transport (ESCRT). ESCRT has a well-described role in directing proteins destined for lysosomal degradation into intraluminal vesicles (ILVs) of multivesicular bodies (MVBs), ensuring degradation of the sorted cargo upon MVB-lysosome fusion. Here, we show that ESCRT is required to deliver Mtb to the lysosome and to restrict intracellular bacterial growth. Further, EsxH, in complex with EsxG, disrupts ESCRT function and impairs phagosome maturation. Thus, we demonstrate a role for a TSSS and the host ESCRT machinery in one of the central features of tuberculosis pathogenesis.
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Certain ESX-3-secreted effectors can block ESCRT-dependent receptor trafficking to the lysosome.
“Intriguingly, certain ESX-3-secreted effectors can block ESCRT-dependent receptor trafficking to the lysosome (80).”
From ESX/Type VII Secretion Systems—An Important Way Out for Mycobacterial Proteins (2019) · cites this paper as [80]
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Towards a proteome-scale map of the human protein–protein interaction network
Rual, J.-F. M., Venkatesan, K., Hao, T., Hirozane-Kishikawa, T., Dricot, A., Li, N., Berriz, G. F., Gibbons, F. D., Dreze, M., Ayivi-Guedehoussou, N., et al. (2005) · Nature · doi:10.1038/nature04209 · Cited by 2,904 · see citing works
Self-citationHenne, W. M., Buchkovich, N. J., & Emr, S. D. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.05.015 · Cited by 1,505 · see citing works
The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins
Raiborg, C., & Stenmark, H. (2009) · Nature · doi:10.1038/nature07961 · Cited by 1,408 · see citing works
High-Quality Binary Protein Interaction Map of the Yeast Interactome Network
Yu, H., Braun, P., Yıldırım, M. A., Lemmens, I., Venkatesan, K., Sahalie, J., Hirozane-Kishikawa, T., Gebreab, F., Li, N., Simonis, N., et al. (2008) · Science · doi:10.1126/science.1158684 · Cited by 1,392 · see citing works
Self-citationSturgill-Koszycki, S., Schlesinger, P. H., Chakraborty, P., Haddix, P. L., Collins, H. L., Fok, A. K., Allen, R. D., Gluck, S. L., Heuser, J., & Russell, D. G. (1994) · Science · doi:10.1126/science.8303277 · Cited by 1,302 · see citing works
Receptor downregulation and multivesicular-body sorting
Katzmann, D. J., Odorizzi, G., & Emr, S. D. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm973 · Cited by 1,201 · see citing works
Armstrong, J. A., & Hart, P. D. (1971) · The Journal of Experimental Medicine · doi:10.1084/jem.134.3.713 · Cited by 991 · 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
Antimicrobial mechanisms of phagocytes and bacterial evasion strategies
Flannagan, R. S., Cosío, G., & Grinstein, S. (2009) · Nature Reviews Microbiology · doi:10.1038/nrmicro2128 · Cited by 947 · see citing works
An empirical framework for binary interactome mapping
Venkatesan, K., Rual, J.-F. M., Vázquez, A., Stelzl, U., Lemmens, I. H., Hirozane-Kishikawa, T., Hao, T., Zenkner, M., Xin, X., Goh, K. I., et al. (2008) · Nature Methods · doi:10.1038/nmeth.1280 · Cited by 907 · see citing works
Self-citationThurston, T. L. M., Ryzhakov, G., Bloor, S., von Muhlinen, N., & Randow, F. (2009) · Nature Immunology · doi:10.1038/ni.1800 · Cited by 872 · see citing works
Liang, C., Lee, J.-S., Inn, K.-S., Gack, M. U., Li, Q., Roberts, E. A., Vergne, I., Deretic, V., Feng, P., Akazawa, C., et al. (2008) · Nature Cell Biology · doi:10.1038/ncb1740 · Cited by 792 · 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
Watson, R. O., Manzanillo, P. S., & Cox, J. S. (2012) · Cell · doi:10.1016/j.cell.2012.06.040 · Cited by 755 · see citing works
Hsu, T., Hingley-Wilson, S. M., Chen, B., Chen, M., Dai, A. Z., Morin, P. M., Marks, C. B., Padiyar, J., Goulding, C., Gingery, M., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1635213100 · Cited by 731 · see citing works
Pym, A. S., Brodin, P., Brosch, R., Huerre, M., & Cole, S. T. (2002) · Molecular Microbiology · doi:10.1046/j.1365-2958.2002.03237.x · Cited by 729 · see citing works
A Coat Protein on Phagosomes Involved in the Intracellular Survival of Mycobacteria
Ferrari, G., Langen, H., Naito, M., & Pieters, J. (1999) · Cell · doi:10.1016/s0092-8674(00)80754-0 · Cited by 579 · see citing works
Mechanism of phagolysosome biogenesis block by viable Mycobacterium tuberculosis
Vergne, I., Chua, J., Lee, H.-H., Lucas, M., Belisle, J. T., & Deretic, V. P. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0409716102 · Cited by 537 · see citing works
Guinn, 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
Manzanillo, P. S., Shiloh, M. U., Portnoy, D. A., & Cox, J. S. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.03.007 · Cited by 456 · see citing works
Mycobacterium tuberculosis Prevents Inflammasome Activation
Master, S. S., Rampini, S. K., Davis, A. S., Keller, C., Ehlers, S., Springer, B., Timmins, G. S., Sander, P., & Deretic, V. P. (2008) · Cell Host & Microbe · doi:10.1016/j.chom.2008.03.003 · Cited by 421 · see citing works
Wong, D., Bach, H., Sun, J., Hmama, Z., & Av‐Gay, Y. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1109201108 · Cited by 417 · see citing works
Tuberculosis Pathogenesis and Immunity
Philips, J. A., & Ernst, J. (2011) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-011811-132458 · Cited by 415 · see citing works
Self-citationLongva, K. E., Blystad, F. D., Stang, E., Larsen, A. M., Johannessen, L. E., & Madshus, I. H. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200106056 · Cited by 385 · see citing works
Drosophila RNAi Screen Reveals CD36 Family Member Required for Mycobacterial Infection
Philips, J. A., Rubin, E. J., & Perrimon, N. (2005) · Science · doi:10.1126/science.1116006 · Cited by 370 · see citing works
Self-citationBach, H., Papavinasasundaram, K. G., Wong, D., Hmama, Z., & Av‐Gay, Y. (2008) · Cell Host & Microbe · doi:10.1016/j.chom.2008.03.008 · Cited by 333 · 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
TSG101 interaction with HRS mediates endosomal trafficking and receptor down-regulation
Lu, Q., Hope, L. W., Brasch, M. A., Reinhard, C., & Cohen, S. N. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0932599100 · Cited by 319 · see citing works
Pandey, A. K., Yang, Y., Jiang, Z., Fortune, S. M., Coulombe, F., Behr, M. A., Fitzgerald, K. A., Sassetti, C. M., & Kelliher, M. A. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000500 · Cited by 292 · 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
HIV Gag mimics the Tsg101-recruiting activity of the human Hrs protein
Pornillos, O., Higginson, D. S., Stray, K. M., Fisher, R. D., Garrus, J. E., Payne, M., He, G.-P., Wang, H. E., Morham, S. G., & Sundquist, W. I. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200302138 · Cited by 258 · 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
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
Serafini, A., Boldrin, F., Palù, G., & Manganelli, R. (2009) · Journal of Bacteriology · doi:10.1128/jb.00756-09 · Cited by 198 · see citing works
Shembade, N., Harhaj, N. S., Liebl, D. J., & Harhaj, E. W. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601823 · Cited by 191 · see citing works
Hrs Is Associated with STAM, a Signal-transducing Adaptor Molecule
Asao, H., Sasaki, Y., Arita, T., et al. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.52.32785 · Cited by 188 · 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
Skjøt, R. L. V., Brock, I., Arend, S. M., Munk, M. E., Theisen, M., Ottenhoff, T. H. M., & Andersen, P. L. (2002) · Infection and Immunity · doi:10.1128/iai.70.10.5446-5453.2002 · Cited by 169 · see citing works
Prokayrotic Ubiquitin-Like Protein (Pup) Proteome of Mycobacterium tuberculosis
Festa, R. A., McAllister, F. E., Pearce, M. J., Mintseris, J., Burns, K. E., Gygi, S. P., & Darwin, K. H. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008589 · Cited by 142 · see citing works
Venugopal, A., Bryk, R., Shi, S., Rhee, K. Y., Rath, P., Schnappinger, D., Ehrt, S., & Nathan, C. (2011) · Cell Host & Microbe · doi:10.1016/j.chom.2010.12.004 · Cited by 139 · 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
Coros, 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
Sun, J., Wang, X., Lau, A., Liao, T.-Y. A., Bucci, C., & Hmama, Z. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008769 · Cited by 126 · see citing works
Banaei, N., Kincaid, E., Buchwald, U. K., Jacobs, W. R., & Ernst, J. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.5.3019 · Cited by 120 · see citing works
Mayers, J. R., Fyfe, I., Schuh, A. L., Chapman, E. R., Edwardson, J. M., & Audhya, A. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.185363 · Cited by 100 · see citing works
Acquisition of Hrs, an Essential Component of Phagosomal Maturation, Is Impaired by Mycobacteria
Vieira, O. V., Harrison, R. E., Scott, C. C., et al. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.10.4593-4604.2004 · Cited by 96 · see citing works
Hervás‐Stubbs, S., Majlessi, L., Simsova, M., Morová, J., Rojas, M.-J., Nouzé, C., Brodin, P. M., Šebo, P., & Leclerc, C. (2006) · Infection and Immunity · doi:10.1128/iai.02086-05 · Cited by 96 · see citing works
Sun, J., Deghmane, A., Soualhine, H., Hong, T., Bucci, C., Solodkin, A., & Hmama, Z. (2007) · Journal of Leukocyte Biology · doi:10.1189/jlb.0507289 · Cited by 92 · see citing works
ESCRT factors restrict mycobacterial growth
Philips, J. A., Porto, M., Wang, H., Rubin, E. J., & Perrimon, N. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707206105 · Cited by 89 · see citing works
Self-citationSolution Structure of the Mycobacterium tuberculosis EsxG·EsxH Complex
Ilghari, D., Lightbody, K. L., Veverka, V., Waters, L. C., Muskett, F. W., Renshaw, P. S., & Carr, M. D. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.248732 · Cited by 88 · see citing works
Deghmane, A., Soualhine, H., Bach, H., Sendide, K., Itoh, S., Tam, A. J. C., Noubir, S., Talal, A., Lo, R., Toyoshima, S., et al. (2007) · Journal of Cell Science · doi:10.1242/jcs.006221 · Cited by 86 · see citing works
EGF and amphiregulin differentially regulate Cbl recruitment to endosomes and EGF receptor fate
Stern, K. A., Place, T. L., & Lill, N. L. (2008) · Biochemical Journal · doi:10.1042/bj20071505 · Cited by 78 · see citing works
Crystallographic and Functional Analysis of the ESCRT-I /HIV-1 Gag PTAP Interaction
Im, Y. J., Kuo, L. S., Ren, X., Burgos, P. V., Zhao, X. Z., Liu, F., Burke, T. R., Bonifacino, J. S., Freed, E. O., & Hurley, J. H. (2010) · Structure · doi:10.1016/j.str.2010.08.010 · Cited by 76 · 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
Obscurin and KCTD6 regulate cullin-dependent small ankyrin-1 (sAnk1.5) protein turnover
Lange, S., Perera, S., Teh, P., & Chen, J. (2012) · Molecular Biology of the Cell · doi:10.1091/mbc.e12-01-0052 · Cited by 69 · see citing works
NF-κB and STAT3 signaling hubs for lung innate immunity
Quinton, L. J., & Mizgerd, J. P. (2011) · Cell and Tissue Research · doi:10.1007/s00441-010-1044-y · Cited by 65 · see citing works
Ms, M., Кондратов, К. А., & Корнилова, Е. С. (2005) · Cell Biology International · doi:10.1016/j.cellbi.2005.09.003 · Cited by 63 · see citing works
Hrs-2 Regulates Receptor-mediated Endocytosis via Interactions with Eps15
Bean, A. J., Davanger, S., Chou, M. F., Gerhardt, B., Tsujimoto, S., & Chang, Y. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.20.15271 · Cited by 61 · see citing works
Self-citationLightbody, K. L., Renshaw, P. S., Collins, M. D., WRIGHT, R., HUNT, D., Gordon, S. V., Hewinson, R. G., Buxton, R. S., WILLIAMSON, R., & Carr, M. D. (2004) · FEMS Microbiology Letters · doi:10.1016/j.femsle.2004.07.043 · Cited by 53 · see citing works
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Wegner, C. S., Rodahl, L. M., & Stenmark, H. (2011) · Traffic · doi:10.1111/j.1600-0854.2011.01210.x · Cited by 52 · see citing works
Bouamr, F., Houck-Loomis, B. R., Santos, M. D. L., Casaday, R. J., Johnson, M. C., & Goff, S. P. (2006) · Journal of Virology · doi:10.1128/jvi.01413-06 · Cited by 36 · see citing works
Purdy, G. E., Owens, R. M., Bennett, L., et al. (2005) · Cellular Microbiology · doi:10.1111/j.1462-5822.2005.00580.x · Cited by 32 · see citing works
Callahan, B. P., Nguyen, K., Collins, A. M., Valdes, K. M., Caplow, M., Crossman, D. K., Steyn, A. J. C., Eisele, L. E., & Derbyshire, K. M. (2009) · Journal of Bacteriology · doi:10.1128/jb.01032-09 · Cited by 28 · see citing works
Distinct Protein Domains Are Responsible for the Interaction of Hrs-2 with SNAP-25
Tsujimoto, S., & Bean, A. J. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.4.2938 · Cited by 23 · see citing works
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Hubner, M., & Peter, M. (2012) · Cellular Logistics · doi:10.4161/cl.20372 · Cited by 13 · see citing works
McMath, L. M., Habel, J. E., Sankaran, B., et al. (2010) · Acta Crystallographica Section F Structural Biology and Crystallization Communications · doi:10.1107/s1744309110042958 · Cited by 10 · see citing works
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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
Self-citationKöster, S., Upadhyay, S., Chandra, P., Papavinasasundaram, K., Yang, G., Hassan, A., Grigsby, S. J., Mittal, E., Park, H. S., Jones, V., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1707792114 · Cited by 208 · see citing works
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Ge, P., Lei, Z., Yu, Y., Lu, Z., Qiang, L., Chai, Q., Zhang, Y., Zhao, D., Li, B., Pang, Y., et al. (2022) · Autophagy · doi:10.1080/15548627.2021.1938912 · Cited by 132 · see citing works
Mittal, E., Skowyra, M. L., Uwase, G., Tinaztepe, E., Mehra, A., Köster, S., Hanson, P. I., & Philips, J. A. (2018) · mBio · doi:10.1128/mbio.01765-18 · Cited by 110 · see citing works
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- Authors
- Mehra, A., Zahra, A., Thompson, V., Sirisaengtaksin, N., Wells, A., Porto, M., Köster, S., Penberthy, K., Kubota, Y., Dricot, A., Rogan, D., Vidal, M., Hill, D. E., Bean, A. J., & Philips, J. A.
- Affiliations
- New York University (US)
- The University of Texas Health Science Center at Houston (US)
- Harvard University (US)
- The University of Texas MD Anderson Cancer Center (US)
- Corresponding author
- Philips, Jennifer A.
- ORCID
- Venue
- PLoS Pathogens
- Publisher
- Public Library of Science (PLoS)
- Published
- 2013-10-31
- Volume
- 9
- Issue
- 10
- Pages
- e1003734
- ISSN
- 1553-7366 (ISSN-L)
- 1553-7374
- PMC
- PMC3814348
- OpenAlex
- W2171774303
- Cited by
- 192
- References
- 67
- Citations by year
- 2026: 13 · 2025: 13 · 2024: 14 · 2023: 13 · 2022: 13 · 2021: 18 · 2020: 9 · 2019: 18 · 2018: 19 · 2017: 16 · 2016: 19 · 2015: 15 · 2014: 12
- FWCI
- 11.14
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Pathogens (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- Doris Duke Charitable Foundation
- Infectious Diseases Society of America
- Memorial Sloan-Kettering Cancer Center
- York University
- University of Leicester
- National Institutes of Health (HG001715)
- School of Medicine, New York University
- Weill Cornell Medical College
- National Human Genome Research Institute (U01HG001715, HG004233, R01HG001715, U41HG001715, P50HG004233, HG001715)
- National Institute of Allergy and Infectious Diseases (AI087682, R01AI087682)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- Mycobacterium tuberculosis, type VII secretion system, ESCRT, Hrs, HgS, phagosome maturation, lysosomal degradation, multivesicular bodies, intraluminal vesicles, bacterial virulence factors, host-pathogen interaction, intracellular bacterial growth, yeast two-hybrid screen
- MeSH terms
- Animals, Bacterial Proteins, Cell Wall, Humans, Intracellular Membranes, Lysosomes, Membrane Fusion, Mycobacterium tuberculosis, Phosphoproteins, Endosomes, Tuberculosis, Mice, Endosomal Sorting Complexes Required for Transport, HEK293 Cells, 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 ›
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