M. tuberculosis and M. leprae Translocate from the Phagolysosome to the Cytosol in Myeloid Cells

van der Wel, Nicole; Hava, David; Houben, Diane; Fluitsma, Donna; van Zon, Maaike; Pierson, Jason; Brenner, Michael; Peters, Peter J.

doi:10.1016/j.cell.2007.05.059

Cited by 960Tuberculosis Research and EpidemiologyLeprosy Research and TreatmentImmune responses and vaccinations

M. tuberculosis and M. leprae Translocate from the Phagolysosome to the Cytosol in Myeloid Cells

Open access

van der Wel, Nicole, Hava, David, Houben, Diane, Fluitsma, Donna, van Zon, Maaike, Pierson, Jason, Brenner, Michael, Peters, Peter J.·2007·Cell

DOI 10.1016/j.cell.2007.05.059

Open this paper in CoChat — free account Open PDF

Abstract

M. tuberculosis and M. leprae are considered to be prototypical intracellular pathogens that have evolved strategies to enable growth in the intracellular phagosomes. In contrast, we show that lysosomes rapidly fuse with the virulent M. tuberculosis- and M. leprae-containing phagosomes of human monocyte-derived dendritic cells and macrophages. After 2 days, M. tuberculosis progressively translocates from phagolysosomes into the cytosol in nonapoptotic cells. Cytosolic entry is also observed for M. leprae but not for vaccine strains such as M. bovis BCG or in heat-killed mycobacteria and is dependent upon secretion of the mycobacterial gene products CFP-10 and ESAT-6. The cytosolic bacterial localization and replication are pathogenic features of virulent mycobacteria, causing significant cell death within a week. This may also reveal a mechanism for MHC-based antigen presentation that is lacking in current vaccine strains.

Integrity signals

Registry

Crossref · 10.1016/j.cell.2007.05.059

Cites

54 of 54 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

The ESX-1 system is involved in bacterial phagosome-to-cytosol transition of M. tuberculosis and host cell death.
“The ESX-1 system was shown to be involved in bacterial phagosome-tocytosol transition of M. tuberculosis and host cell death (66)(67)(68), an important cell biological process that has numerous consequences for the host cell, such as induc-tion of the cGAS/STING/TBK1/IRF-3/type I interferon signalling axis and NLRP3 inflammasome activation (69)(70)(71)(72)(73)(74)(75).”
From ESX/Type VII Secretion Systems—An Important Way Out for Mycobacterial Proteins (2019) · cites this paper as [66]

Apoptosis: A Basic Biological Phenomenon with Wideranging Implications in Tissue Kinetics
Kerr, J. F. R., Wyllie, A. H., & Currie, A. R. (1972) · British Journal of Cancer · doi:10.1038/bjc.1972.33 · Cited by 15,673 · see citing works
Computer visualization of three-dimensional image data using IMOD.
Kremer, J. R., Mastronarde, D., & Mcintosh, J. (1996) · Journal of Structural Biology · doi:10.1006/jsbi.1996.0013 · Cited by 5,770 · see citing works
A new evolutionary scenario for the Mycobacterium tuberculosis complex
Brosch, R., Gordon, S. V., Marmiesse, M., Brodin, P. M., Buchrieser, C., Eiglmeier, K., Garnier, T., Gutierrez, C., Hewinson, R. G., Kremer, K., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.052548299 · Cited by 1,605 · see citing works
Comparative Genomics of BCG Vaccines by Whole-Genome DNA Microarray
Behr, M. A., Wilson, M. A., Gill, W., Salamon, H., Schoolnik, G. K., Rane, S., & Small, P. M. (1999) · Science · doi:10.1126/science.284.5419.1520 · Cited by 1,527 · see citing works
Immunology of tuberculosis.
Flynn, J., & Chan, J. (2003) · Annual Review of Immunology · doi:10.1146/annurev.immunol.19.1.93 · Cited by 1,144 · see citing works
RESPONSE OF CULTURED MACROPHAGES TO MYCOBACTERIUM TUBERCULOSIS , WITH OBSERVATIONS ON FUSION OF LYSOSOMES WITH PHAGOSOMES
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
Bacterial Adhesion and Entry into Host Cells
Pizarro-Cerdá, J., & Cossart, P. (2006) · Cell · doi:10.1016/j.cell.2006.02.012 · Cited by 977 · cited 2× · see citing works
“The prevailing paradigm has remained that M. tuberculosis reside in the endocytic system (Orme, 2004; Vergne et al., 2004; Russell et al., 2002; Kang et al., 2005; Russell, 2001; Pizarro-Cerda and Cossart, 2006).”
Background
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
ER–phagosome fusion defines an MHC class I cross-presentation compartment in dendritic cells
Guermonprez, P., Saveanu, L., Kleijmeer, M. J., Davoust, J. M., Endert, P. V., & Amigorena, S. (2003) · Nature · doi:10.1038/nature01911 · Cited by 753 · see citing works
The primary mechanism of attenuation of bacillus Calmette–Guérin is a loss of secreted lytic function required for invasion of lung interstitial tissue
Hsu, T., Hingley-Wilson, S. M., Chen, B., Chen, M., Dai, A. Z., Morin, P. M., Marks, C. B., Padiyar, J., Goulding, C., Gingery, M., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1635213100 · Cited by 731 · see citing works
Phagosomes are competent organelles for antigen cross-presentation
Houde, M., Bertholet, S., Gagnon, É., Brunet, S., Goyette, G., Laplante, A., Princiotta, M. F., Thibault, P., Sacks, D. L., & Desjardins, M. (2003) · Nature · doi:10.1038/nature01912 · Cited by 700 · see citing works
Segregation of MHC class II molecules from MHC class I molecules in the Golgi complex for transport to lysosomal compartments
Peters, P. J., Neefjes, J., Oorschot, V. M. J., Ploegh, H. L., & Geuze, H. J. (1991) · Nature · doi:10.1038/349669a0 · Cited by 658 · see citing works
Self-citation
FtsZ and the division of prokaryotic cells and organelles
Margolin, W. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1745 · Cited by 632 · see citing works
Deletion of RD1 fromMycobacterium tuberculosisMimics 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
CDlb restricts the response of human CD4−8−T lymphocytes to a microbial antigen
Porcelli, S. A., Morita, C. T., & Brenner, M. B. (1992) · Nature · doi:10.1038/360593a0 · Cited by 572 · see citing works
Self-citation
Acute infection and macrophage subversion by Mycobacterium tuberculosis require a specialized secretion system
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
Increased vaccine efficacy against tuberculosis of recombinant Mycobacterium bovis bacille Calmette-Guerin mutants that secrete listeriolysin
Grode, L. (2005) · Journal of Clinical Investigation · doi:10.1172/jci24617 · Cited by 557 · see citing works
Identification of variable regions in the genomes of tubercle bacilli using bacterial artificial chromosome arrays
Gordon, S. V., Brosch, R., Billault, A., Garnier, T., Eiglmeier, K., & Cole, S. T. (1999) · Molecular Microbiology · doi:10.1046/j.1365-2958.1999.01383.x · Cited by 537 · see citing works
The human macrophage mannose receptor directs Mycobacterium tuberculosis lipoarabinomannan-mediated phagosome biogenesis
Kang, P. B., Azad, A. K., Torrelles, J. B., Kaufman, T. M., Beharka, A. A., Tibesar, E., DesJardin, L. E., & Schlesinger, L. S. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20051239 · Cited by 519 · see citing works
Infection by Mycobacterium tuberculosis promotes human alveolar macrophage apoptosis
Keane, J., Balcewicz-Sablinska, M. K., Remold, H. G., Chupp, G. L., Meek, B., Fenton, M. J., & Kornfeld, H. (1997) · Infection and Immunity · doi:10.1128/iai.65.1.298-304.1997 · Cited by 512 · see citing works
Individual RD1‐region genes are required for export of ESAT‐6/CFP‐10 and for virulence of Mycobacterium tuberculosis
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
A Mycobacterium tuberculosis operon encoding ESAT=6 and a novel low-molecular-mass culture filtrate protein (CFP-10)
Berthet, F., Rasmussen, P. B., Rosenkrands, I., Andersen, P. L., & Gicquel, B. (1998) · Microbiology · doi:10.1099/00221287-144-11-3195 · Cited by 486 · see citing works
Evidence for occurrence of the ESAT-6 protein in Mycobacterium tuberculosis and virulent Mycobacterium bovis and for its absence in Mycobacterium bovis BCG
Harboe, M., Oettinger, T., Wiker, H. G., Rosenkrands, I., & Andersen, P. L. (1996) · Infection and Immunity · doi:10.1128/iai.64.1.16-22.1996 · Cited by 465 · see citing works
CELL BIOLOGY OF MYCOBACTERIUM TUBERCULOSIS PHAGOSOME
Vergne, I., Chua, J., Singh, S., & Deretic, V. P. (2004) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.20.010403.114015 · Cited by 440 · see citing works
Granuloma-Specific Expression of Mycobacterium Virulence Proteins from the Glycine-Rich PE-PGRS Family
Ramakrishnan, L., Federspiel, N. A., & Falkow, S. (2000) · Science · doi:10.1126/science.288.5470.1436 · Cited by 420 · see citing works
Mutually 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
Early phagosomes in dendritic cells form a cellular compartment sufficient for cross presentation of exogenous antigens
Ackerman, A. L., Kyritsis, C., Tampé, R., & Cresswell, P. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1735556100 · Cited by 383 · see citing works
Pathogenesis of tuberculosis: interaction of Mycobacterium tuberculosis with macrophages
McDonough, K. A., Kress, Y., & Bloom, B. R. (1993) · Infection and Immunity · doi:10.1128/iai.61.7.2763-2773.1993 · Cited by 377 · see citing works
Current Protocols in Cell Biology
(2018) · Current Protocols in Cell Biology · doi:10.1002/(issn)1934-2616 · Cited by 359 · see citing works
Dissection of ESAT-6 System 1 of Mycobacterium tuberculosis and Impact on Immunogenicity and Virulence
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
Mycobacterium marinum Escapes from Phagosomes and Is Propelled by Actin-based Motility
Stamm, L. M., Morisaki, J. H., Gao, L., Jeng, R. L., McDonald, K. L., Roth, R. A., Takeshita, S., Heuser, J., Welch, M. D., & Brown, E. J. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20031072 · Cited by 299 · see citing works
Quantitative and Dynamic Assessment of the Contribution of the ER to Phagosome Formation
Touret, N., Paroutis, P., Terebiznik, M. R., Harrison, R. E., Trombetta, S., Pypaert, M., Chow, A. Y., Jiang, A., Shaw, J. E., Yip, C. M., et al. (2005) · Cell · doi:10.1016/j.cell.2005.08.018 · Cited by 285 · see citing works
Self-citation
The Listeria monocytogenes hemolysin has an acidic pH optimum to compartmentalize activity and prevent damage to infected host cells
Glomski, I. J., Gedde, M. M., Tsang, A. W., Swanson, J. A., & Portnoy, D. A. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200201081 · Cited by 281 · see citing works
Macrophage Apoptosis in Response to High Intracellular Burden of Mycobacterium tuberculosis Is Mediated by a Novel Caspase-Independent Pathway
Lee, J., Remold, H. G., Ieong, M. H., & Kornfeld, H. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.7.4267 · Cited by 238 · see citing works
Genomic Deletions Suggest a Phylogeny for theMycobacterium tuberculosisComplex
Mostowy, S., Cousins, D., Brinkman, J., Aranaz, A., & Behr, M. A. (2002) · The Journal of Infectious Diseases · doi:10.1086/341068 · Cited by 235 · see citing works
THP-1 Cell Apoptosis in Response to Mycobacterial Infection
Riendeau, C. J., & Kornfeld, H. (2002) · Infection and Immunity · doi:10.1128/iai.71.1.254-259.2003 · Cited by 224 · see citing works
Actin-dependent movement of bacterial pathogens
Stevens, J. M., Galyov, E. E., & Stevens, M. P. (2006) · Nature Reviews Microbiology · doi:10.1038/nrmicro1320 · Cited by 222 · see citing works
The ESAT6 protein of Mycobacterium tuberculosis induces apoptosis of macrophages by activating caspase expression
Derrick, S. C., & Morris, S. L. (2007) · Cellular Microbiology · doi:10.1111/j.1462-5822.2007.00892.x · Cited by 212 · see citing works
Molecular basis of listeriolysin O pH dependence
Schuerch, D. W., Wilson-Kubalek, E. M., & Tweten, R. K. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0500558102 · Cited by 201 · see citing works
Mycobacterium and the coat of many lipids
Russell, D. G., Mwandumba, H. C., & Rhoades, E. E. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200205034 · Cited by 162 · see citing works
DISTINCT mdm2/p53 EXPRESSION PATTERNS IN LIPOSARCOMA SUBGROUPS: IMPLICATIONS FOR DIFFERENT PATHOGENETIC MECHANISMS
Pilotti, S., Torre, G. D., Lavarino, C. E., Palma, S. D., Sozzi, G., Minoletti, F., Rao, S., PASQUINI, G., Azzarelli, A., Rilke, F. O., et al. (1997) · The Journal of Pathology · doi:10.1002/(sici)1096-9896(199701)181:1 · Cited by 149 · see citing works
Influence of ESAT-6 Secretion System 1 (RD1) of Mycobacterium tuberculosis on the Interaction between Mycobacteria and the Host Immune System
Majlessi, L., Brodin, P. M., Brosch, R., Rojas, M.-J., Khun, H., Huerre, M., Cole, S. T., & Leclerc, C. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.6.3570 · Cited by 128 · see citing works
Long-Term Control of Mycobacterium tuberculosis Infection Is Mediated by Dynamic Immune Responses
Lazarevic, V., Nolt, D. L., & Flynn, J. L. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.2.1107 · Cited by 121 · see citing works
Disruption of phagosomal membranes of normal alveolar macrophages by the H37Rv strain of Mycobacterium tuberculosis. A correlate of virulence.
Myrvik, Q. N., Leake, E. S., & Wright, M. J. (1984) · PubMed · Cited by 114 · see citing works
A Mycobacterial Operon Essential for Virulence In Vivo and Invasion and Intracellular Persistence in Macrophages
Gao, L., Pak, M. A., Kish, R., Kajihara, K. K., & Brown, E. J. (2006) · Infection and Immunity · doi:10.1128/iai.74.3.1757-1767.2006 · Cited by 100 · see citing works
Physical mapping of Mycobacterium bovis BCG Pasteur reveals differences from the genome map of Mycobacterium tuberculosis H37Rv and from M. bovis
Philipp, W. J., Nair, S., Guglielmi, G., Lagranderie, M., Gicquel, B., & Cole, S. T. (1996) · Microbiology · doi:10.1099/13500872-142-11-3135 · Cited by 87 · see citing works
Cryo‐Immunogold Electron Microscopy
Peters, P. J., Bos, E., & Griekspoor, A. (2006) · Current Protocols in Cell Biology · doi:10.1002/0471143030.cb0407s30 · Cited by 77 · see citing works
Self-citation
Role of the WASP family proteins for Mycobacterium marinum actin tail formation
Stamm, L. M., Pak, M. A., Morisaki, J. H., Snapper, S. B., Rottner, K., Lommel, S., & Brown, E. J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504663102 · Cited by 66 · see citing works
Phagosomal membranes of Mycobacterium bovis BCG-immune alveolar macrophages are resistant to disruption by Mycobacterium tuberculosis H37Rv
Leake, E. S., Myrvik, Q. N., & Wright, M. J. (1984) · Infection and Immunity · doi:10.1128/iai.45.2.443-446.1984 · Cited by 48 · see citing works
Adaptive immunity to mycobacteria
Orme, I. M. (2003) · Current Opinion in Microbiology · doi:10.1016/j.mib.2003.11.002 · Cited by 46 · see citing works
The Study ofMycobacterium lepraeInfection in Interferon‐γ Gene–Disrupted Mice as a Model to Explore the Immunopathologic Spectrum of Leprosy
Adams, L. B., Scollard, D. M., Ray, N. A., et al. (2002) · The Journal of Infectious Diseases · doi:10.1086/338002 · Cited by 46 · see citing works
CD1 and Major Histocompatibility Complex II Molecules Follow a Different Course during Dendritic Cell Maturation
van der Wel, N. N., Sugita, M., Fluitsma, D. M., et al. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.e02-11-0744 · Cited by 45 · see citing works
Self-citation
Subcellular localization of mycobacteria in tissues and detection of lipid antigens in organelles using cryo-techniques for light and electron microscopy.
van der Wel, N. N., Fluitsma, D., Dascher, C., Brenner, M., & Peters, P. (2005) · Current Opinion in Microbiology · doi:10.1016/j.mib.2005.04.014 · Cited by 17 · see citing works
Self-citation

Flagged first, then by citations

Sorted by citations

Tuberculosis
Pai, M., Behr, M. A., Dowdy, D., Dheda, K., Divangahi, M., Boehme, C. C., Ginsberg, A., Swaminathan, S., Spigelman, M., Getahun, H., et al. (2016) · Nature Reviews Disease Primers · doi:10.1038/nrdp.2016.76 · Cited by 1,270 · 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
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
Extracellular M. tuberculosis DNA Targets Bacteria for Autophagy by Activating the Host DNA-Sensing Pathway
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
HIV and Tuberculosis: a Deadly Human Syndemic
Kwan, C. K., & Ernst, J. D. (2011) · Clinical Microbiology Reviews · doi:10.1128/cmr.00042-10 · Cited by 720 · 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
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
The mycobacterial cell envelope — a moving target
Dulberger, C. L., Rubin, E. J., & Boutte, C. C. (2020) · Nature Reviews Microbiology · doi:10.1038/s41579-019-0273-7 · Cited by 365 · see citing works
Tryptophan Biosynthesis Protects Mycobacteria from CD4 T-Cell-Mediated Killing
Zhang, Y. J., Reddy, M. C., Ioerger, T. R., Rothchild, A. C., Dartois, V., Schuster, B. M., Trauner, A., Wallis, D., Galaviz, S., Huttenhower, C., et al. (2013) · Cell · doi:10.1016/j.cell.2013.10.045 · Cited by 351 · see citing works
“…transport mechanisms (that have not been defined) or direct access to the cytoplasm through either partial or complete loss of vacuolar integrity, a model consistent with recent observations of Mtb escape into the cytoplasm (Hagedorn et al., 2009; McDonough et al., 1993; van der Wel et al., 2007).”
Comparative pathogenesis of Mycobacterium marinum and Mycobacterium tuberculosis
Tobin, D. M., & Ramakrishnan, L. (2008) · Cellular Microbiology · doi:10.1111/j.1462-5822.2008.01133.x · Cited by 343 · see citing works
Efferocytosis Is an Innate Antibacterial Mechanism
Martin, C. J., Booty, M. G., Rosebrock, T. R., Nunes-Alves, C., Desjardins, D. M., Keren, I., Fortune, S. M., Remold, H. G., & Behar, S. M. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.06.010 · Cited by 285 · see citing works
Plasma membrane damage causes NLRP3 activation and pyroptosis during Mycobacterium tuberculosis infection
Beckwith, K. S., Beckwith, M. S., Ullmann, S., Sætra, R. S., Kim, H., Marstad, A., Åsberg, S. E., Strand, T. A., Haug, M., Niederweis, M., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-16143-6 · Cited by 282 · see citing works
ESX-1 and phthiocerol dimycocerosates of Mycobacterium tuberculosis act in concert to cause phagosomal rupture and host cell apoptosis
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
The Cell Wall Lipid PDIM Contributes to Phagosomal Escape and Host Cell Exit of Mycobacterium tuberculosis
Quigley, J., Hughitt, V. K., Velikovsky, C. A., Mariuzza, R. A., El-Sayed, N. M., & Briken, V. (2017) · mBio · doi:10.1128/mbio.00148-17 · Cited by 234 · see citing works
Critical role for NLRP3 in necrotic death triggered by Mycobacterium tuberculosis
Wong, K., & Jacobs Jr, W. R. (2011) · Cellular Microbiology · doi:10.1111/j.1462-5822.2011.01625.x · Cited by 209 · see citing works
The Macrophage: A Disputed Fortress in the Battle against Mycobacterium tuberculosis
Queval, C. J., Brosch, R., & Simeone, R. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.02284 · Cited by 215 · see citing works
Mycobacterium tuberculosis Type VII Secreted Effector EsxH Targets Host ESCRT to Impair Trafficking
Mehra, A., Zahra, A., Thompson, V., Sirisaengtaksin, N., Wells, A., Porto, M., Köster, S., Penberthy, K., Kubota, Y., Dricot, A., et al. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003734 · Cited by 192 · see citing works
Cytosolic Access of Mycobacterium tuberculosis: Critical Impact of Phagosomal Acidification Control and Demonstration of Occurrence In Vivo
Simeone, R., Sayes, F., Song, O., Gröschel, M. I., Brodin, P., Brosch, R., & Majlessi, L. (2015) · PLOS Pathogens · doi:10.1371/journal.ppat.1004650 · Cited by 198 · see citing works
The mechanisms and consequences of the extra-pulmonary dissemination of Mycobacterium tuberculosis
Krishnan, N., Robertson, B. D., & Thwaites, G. (2010) · Tuberculosis · doi:10.1016/j.tube.2010.08.005 · Cited by 178 · see citing works
Escape of Mycobacterium tuberculosis from oxidative killing by neutrophils: Tubercle bacilli escape neutrophil killing
Corleis, B., Korbel, D., Wilson, R., Bylund, J., Chee, R., & Schaible, U. E. (2012) · Cellular Microbiology · doi:10.1111/j.1462-5822.2012.01783.x · Cited by 150 · see citing works
ESX-1-induced apoptosis is involved in cell-to-cell spread ofMycobacterium tuberculosis: M. tuberculosiskills host cells to spread cell-to-cell
Aguilo, J. I., Alonso, H., Uranga, S., Marinova, D., Arbués, A., de Martino, A., Anel, A., Monzon, M., Badiola, J., Pardo, J., et al. (2013) · Cellular Microbiology · doi:10.1111/cmi.12169 · Cited by 140 · see citing works
Strategies Used by Bacteria to Grow in Macrophages
Mitchell*, G., Chen*, C., & Portnoy, D. A. (2016) · Microbiology Spectrum · doi:10.1128/microbiolspec.mchd-0012-2015 · Cited by 137 · see citing works
The 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
Recombinant BCG Expressing ESX-1 of Mycobacterium marinum Combines Low Virulence with Cytosolic Immune Signaling and Improved TB Protection
Gröschel, M. I., Sayes, F., Shin, S. J., Frigui, W., Pawlik, A., Orgeur, M., Canetti, R., Honoré, N., Simeone, R., van der Werf, T. S., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.02.057 · Cited by 125 · see citing works
Mycobacterium tuberculosis Type VII Secretion System Effectors Differentially Impact the ESCRT Endomembrane Damage Response
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
Abelson Tyrosine Kinase Controls Phagosomal Acidification Required for Killing of Mycobacterium tuberculosis in Human Macrophages
Bruns, H., Stegelmann, F., Fabri, M., Döhner, K., van Zandbergen, G., Wagner, M., Skinner, M., Modlin, R. L., & Stenger, S. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1201538 · Cited by 112 · see citing works
Evolution of virulence in the Mycobacterium tuberculosis complex
Orgeur, M., & Brosch, R. (2018) · Current Opinion in Microbiology · doi:10.1016/j.mib.2017.11.021 · Cited by 107 · 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
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
Mycobacterium tuberculosis and the host cell inflammasome: a complex relationship
Briken, V., Ahlbrand, S. E., & Shah, S. (2013) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2013.00062 · Cited by 92 · 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
ESAT-6–dependent cytosolic pattern recognition drives noncognate tuberculosis control in vivo
Kupz, A., Zedler, U., Stäber, M., Perdomo, C., Dorhoi, A., Brosch, R., & Kaufmann, S. H. E. (2016) · Journal of Clinical Investigation · doi:10.1172/jci84978 · Cited by 67 · see citing works
Cell Walls and Membranes of Actinobacteria
Rahlwes, K. C., Sparks, I. L., & Morita, Y. S. (2019) · Subcellular Biochemistry · doi:10.1007/978-3-030-18768-2_13 · Cited by 65 · 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
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
Esx Systems and the Mycobacterial Cell Envelope: What's the Connection?
Bosserman, R. E., & Champion, P. A. (2017) · Journal of Bacteriology · doi:10.1128/jb.00131-17 · Cited by 42 · see citing works
WASH-driven actin polymerization is required for efficient mycobacterial phagosome maturation arrest: WASH in mycobacterial infection
Kolonko, M., Geffken, A. C., Blumer, T., Hagens, K., Schaible, U. E., & Hagedorn, M. (2014) · Cellular Microbiology · doi:10.1111/cmi.12217 · Cited by 40 · see citing works
EspL is essential for virulence and stabilizes EspE, EspF and EspH levels in Mycobacterium tuberculosis
Sala, C., Odermatt, N. T., Soler-Arnedo, P., Gülen, M. F., von Schultz, S., Benjak, A., & Cole, S. T. (2018) · PLOS Pathogens · doi:10.1371/journal.ppat.1007491 · Cited by 35 · see citing works
The Thyroid Hormone Inactivating Enzyme Type 3 Deiodinase is Present in Bactericidal Granules and the Cytoplasm of Human Neutrophils
van der Spek, A. H., Bloise, F. F., Tigchelaar, W., Dentice, M., Salvatore, D., van der Wel, N. N., Fliers, E., & Boelen, A. (2016) · Endocrinology · doi:10.1210/en.2016-1103 · Cited by 28 · see citing works
Iron acquisition by Mycobacterium tuberculosis residing within myeloid dendritic cells
Olakanmi, O., Kesavalu, B., Abdalla, M. Y., & Britigan, B. E. (2013) · Microbial Pathogenesis · doi:10.1016/j.micpath.2013.09.002 · Cited by 17 · see citing works
Protease domain and transmembrane domain of the type VII secretion mycosin protease determine system-specific functioning in mycobacteria
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

Chemiluminescent activity of macrophages during phagocytosis of different bacterial forms.
Ivanova, E. D., Dimov, V., Bachev, S., et al. (1993) · PubMed
Control of Phagocytosis by Microbial Pathogens
Uribe‐Querol, E., & Rosales, C. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01368 · Cited by 310 · see citing works
Phagocytosis
Uribe‐Querol, E., & Rosales, C. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-818731-9.00049-5 · Cited by 10 · see citing works
Phagocytosis: Our Current Understanding of a Universal Biological Process
Uribe-Querol, E., & Rosales, C. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01066 · Cited by 651 · see citing works
Phagocytosis: A Fundamental Process in Immunity
Rosales, C., & Uribe‐Querol, E. (2017) · BioMed Research International · doi:10.1155/2017/9042851 · Cited by 555 · see citing works

Authors: van der Wel, N., Hava, D., Houben, D., Fluitsma, D., van Zon, M., Pierson, J., Brenner, M., & Peters, P. J.
Affiliations: Brigham and Women's Hospital (US)
The Netherlands Cancer Institute (NL)
Amsterdam UMC Location Vrije Universiteit Amsterdam (NL)
Corresponding author: Peters, Peter J.
ORCID: Hava, David
Brenner, Michael
Peters, Peter J.
Venue: Cell
Publisher: Elsevier BV
Published: 2007-06
Volume: 129
Issue: 7
Pages: 1287-1298
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2007.05.059
OpenAlex: W2121449107
Cited by: 960
References: 54
Citations by year: 2026: 15 · 2025: 33 · 2024: 44 · 2023: 34 · 2022: 49 · 2021: 48 · 2020: 54 · 2019: 65 · 2018: 41 · 2017: 67 · 2016: 52 · 2015: 70 · 2014: 70 · 2013: 65 · 2012: 65
FWCI: 29.15
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 2238 d)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion)
Pure Amsterdam UMC (submittedVersion)
Funders: Damon Runyon Cancer Research Foundation (DRG-1814-04)
Topics: Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
Health Sciences › Medicine › Infectious Diseases › Leprosy Research and Treatment
Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
Keywords: Mycobacterium tuberculosis, Mycobacterium leprae, monocyte-derived dendritic cells, macrophages, CFP-10, ESAT-6, virulence factors, MHC antigen presentation, BCG vaccine strains, intracellular pathogens
MeSH terms: Cell Compartmentation, Cell Division, Cell Movement, Cells, Cultured, Cytosol, Host-Parasite Interactions, Humans, Immunohistochemistry, Intracellular Membranes, Lysosomes, Membrane Proteins, Mycobacterium, Mycobacterium leprae, Mycobacterium tuberculosis, Phagosomes, Biomarkers, Gene Expression Regulation, Bacterial, Cell Death, Antigen Presentation, Myeloid Cells, Microscopy, Electron, Transmission, Cell Proliferation

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

M. tuberculosis and M. leprae Translocate from the Phagolysosome to the Cytosol in Myeloid Cells

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks