Listeria monocytogenes virulence factors, including listeriolysin O, are secreted in biologically active extracellular vesicles

Coelho, Carolina; Brown, Lisa; Maryam, Maria; Vij, Raghav; Smith, Daniel F. Q.; Burnet, Meagan C.; Kyle, Jennifer E.; Heyman, Heino M.; Ramirez, Jasmine; Prados-Rosales, Rafael; Lauvau, Gregoire; Nakayasu, Ernesto S.; Brady, Nathan R.; Hamacher-Brady, Anne; Coppens, Isabelle; Casadevall, Arturo

doi:10.1074/jbc.RA118.006472

Title: Listeria monocytogenes virulence factors, including listeriolysin O, are secreted in biologically active extracellular vesicles

Journal Article · Tue Jan 01 00:00:00 EST 2019 · Journal of Biological Chemistry

DOI:https://doi.org/10.1074/jbc.RA118.006472· OSTI ID:1765007

; Brown, Lisa; Maryam, Maria;

; Smith, Daniel F. Q.; Burnet, Meagan C.; Kyle, Jennifer E.; Heyman, Heino M.; Ramirez, Jasmine; Prados-Rosales, Rafael; Lauvau, Gregoire;

; Brady, Nathan R.; Hamacher-Brady, Anne; Coppens, Isabelle;

Outer membrane vesicles (OMVs) produced by Gram-negative bacteria have been studied for half a century but the possibility that Gram-positive bacteria made extracellular vesicles (EVs) was not pursued due to the assumption that the thick peptidoglycan cell wall would prevent their release to the extracellular environment. However, following discovery in fungi, which also have cell walls, EVs have now been described in a variety of Gram-positive bacteria. EVs purified from Gram-positive bacteria have been implicated in virulence, toxin release, and delivery of molecules to host cells, eliciting immune responses, and transfer of antibiotic resistance. Listeria monocytogenes is a Gram-positive bacterium that is the etiological agent of listeriosis. Here we report that L. monocytogenes produces extracellular EVs with similar size and morphology to EVs from other microorganisms, with average diameter of approximately 20-200 nm. EV composition analyzed using a simultaneous metabolite, protein, and lipid extraction (MPLEx) multi-omics approach. Listeriolysin-O (LLO) was recently reported to be associated with EVs; we confirm this finding and report that EVs contain phosphatidylinositol-specific phospholipase C (PI-PLC). Cell free EV preparations were toxic to mammalian cells demonstrating biological activity of the EV and a complex EV-LLO-PI-PLC association. High-resolution fluorescence imaging revealed L. monocytogenes derived lipid structures colocalizing with LLO in infected human epithelial cells, a finding consistent with intracellular EV-mediated secretion of LLO. Furthermore these results demonstrate that L. monocytogenes, like other toxin-producing Gram-positive bacteria, utilize EVs for toxin release and implicate these structures in mammalian cytotoxicity.

View Journal Article

Cite

Export

Save

Research Organization:: Pacific Northwest National Lab. (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1765007

Alternate ID(s):: OSTI ID: 1502052

Report Number(s):: PNNL-SA-128462; S002192582038858X; PII: S002192582038858X

Journal Information:: Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Vol. 294 Journal Issue: 4; ISSN 0021-9258

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 64 works

Citation information provided by
Web of Science

References (70)

Extracellular S treptomyces lividans vesicles: composition, biogenesis and antimicrobial activity : Vesicles of streptomycetes Schrempf, Hildgund; Merling, Philipp Microbial Biotechnology, Vol. 8, Issue 4 https://doi.org/10.1111/1751-7915.12274	journal	April 2015
LIQUID: an-open source software for identifying lipids in LC-MS/MS-based lipidomics data Kyle, Jennifer E.; Crowell, Kevin L.; Casey, Cameron P. Bioinformatics, Vol. 33, Issue 11 https://doi.org/10.1093/bioinformatics/btx046	journal	January 2017
MetaboAnalyst 3.0—making metabolomics more meaningful Xia, Jianguo; Sinelnikov, Igor V.; Han, Beomsoo Nucleic Acids Research, Vol. 43, Issue W1 https://doi.org/10.1093/nar/gkv380	journal	April 2015
An automated method to quantify and visualize colocalized fluorescent signals Jaskolski, Frédéric; Mulle, Christophe; Manzoni, Olivier J. Journal of Neuroscience Methods, Vol. 146, Issue 1 https://doi.org/10.1016/j.jneumeth.2005.01.012	journal	July 2005
Membrane Vesicle Release in Bacteria, Eukaryotes, and Archaea: a Conserved yet Underappreciated Aspect of Microbial Life Deatherage, Brooke L.; Cookson, Brad T. Infection and Immunity, Vol. 80, Issue 6 https://doi.org/10.1128/IAI.06014-11	journal	March 2012
In vitro model of penetration and intracellular growth of Listeria monocytogenes in the human enterocyte-like cell line Caco-2. Gaillard, J. L.; Berche, P.; Mounier, J. Infection and Immunity, Vol. 55, Issue 11 https://doi.org/10.1128/IAI.55.11.2822-2829.1987	journal	January 1987
Enterotoxigenic Escherichia coli Secretes Active Heat-labile Enterotoxin via Outer Membrane Vesicles Horstman, Amanda L.; Kuehn, Meta J. Journal of Biological Chemistry, Vol. 275, Issue 17 https://doi.org/10.1074/jbc.275.17.12489	journal	April 2000
A Novel Role of Listeria monocytogenes Membrane Vesicles in Inhibition of Autophagy and Cell Death Vdovikova, Svitlana; Luhr, Morten; Szalai, Paula Frontiers in Cellular and Infection Microbiology, Vol. 7 https://doi.org/10.3389/fcimb.2017.00154	journal	May 2017
Polar lipids of four listeria species containing L-lysylcardiolipin, a novel lipid structure, and other unique phospholipids Fischer, W.; Leopold, K. International Journal of Systematic Bacteriology, Vol. 49, Issue 2 https://doi.org/10.1099/00207713-49-2-653	journal	April 1999
Legionella pneumophila infection activates bystander cells differentially by bacterial and host cell vesicles Jung, Anna Lena; Herkt, Christina Elena; Schulz, Christine Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-06443-1	journal	July 2017
DAnTE: a statistical tool for quantitative analysis of -omics data Polpitiya, A. D.; Qian, W. -J.; Jaitly, N. Bioinformatics, Vol. 24, Issue 13 https://doi.org/10.1093/bioinformatics/btn217	journal	May 2008
Through the wall: extracellular vesicles in Gram-positive bacteria, mycobacteria and fungi Brown, Lisa; Wolf, Julie M.; Prados-Rosales, Rafael Nature Reviews Microbiology, Vol. 13, Issue 10 https://doi.org/10.1038/nrmicro3480	journal	September 2015
Coordinated Regulation of Cold-Induced Changes in Fatty Acids with Cardiolipin and Phosphatidylglycerol Composition among Phospholipid Species for the Food Pathogen Listeria monocytogenes Mastronicolis, S. K.; Arvanitis, N.; Karaliota, A. Applied and Environmental Microbiology, Vol. 74, Issue 14 https://doi.org/10.1128/AEM.02041-07	journal	May 2008
Genes involved in Listeria monocytogenes biofilm formation at a simulated food processing plant temperature of 15°C Piercey, Marta J.; Hingston, Patricia A.; Truelstrup Hansen, Lisbeth International Journal of Food Microbiology, Vol. 223 https://doi.org/10.1016/j.ijfoodmicro.2016.02.009	journal	April 2016
Characterization of a BODIPY-labeled {fl}uorescent fatty acid analogue. Binding to fatty acid-binding proteins, intracellular localization, and metabolism Thumser, Alfred E.; Storch, Judith Molecular and Cellular Biochemistry, Vol. 299, Issue 1-2 https://doi.org/10.1007/s11010-005-9041-2	journal	April 2006
Extracellular Vesicles Released from Mycobacterium tuberculosis-Infected Neutrophils Promote Macrophage Autophagy and Decrease Intracellular Mycobacterial Survival Alvarez-Jiménez, Violeta D.; Leyva-Paredes, Kahiry; García-Martínez, Mariano Frontiers in Immunology, Vol. 9 https://doi.org/10.3389/fimmu.2018.00272	journal	February 2018
Outer Membrane Vesicles Mediate Transport of Biologically Active Vibrio cholerae Cytolysin (VCC) from V. cholerae Strains Elluri, Sridhar; Enow, Constance; Vdovikova, Svitlana PLoS ONE, Vol. 9, Issue 9 https://doi.org/10.1371/journal.pone.0106731	journal	September 2014
Listeria monocytogenes transiently alters mitochondrial dynamics during infection Stavru, Fabrizia; Bouillaud, Frédéric; Sartori, Anna Proceedings of the National Academy of Sciences, Vol. 108, Issue 9 https://doi.org/10.1073/pnas.1100126108	journal	February 2011
Structures of Gram-Negative Cell Walls and Their Derived Membrane Vesicles Beveridge, Terry J. Journal of Bacteriology, Vol. 181, Issue 16 https://doi.org/10.1128/JB.181.16.4725-4733.1999	journal	August 1999
Internalin of Listeria monocytogenes with an intact leucine-rich repeat region is sufficient to promote internalization. Lecuit, M.; Ohayon, H.; Braun, L. Infection and immunity, Vol. 65, Issue 12 https://doi.org/10.1128/IAI.65.12.5309-5319.1997	journal	January 1997
MPLEx: a Robust and Universal Protocol for Single-Sample Integrative Proteomic, Metabolomic, and Lipidomic Analyses Nakayasu, Ernesto S.; Nicora, Carrie D.; Sims, Amy C. mSystems, Vol. 1, Issue 3 https://doi.org/10.1128/mSystems.00043-16	journal	May 2016
Extracellular Vesicles Produced by Cryptococcus neoformans Contain Protein Components Associated with Virulence Rodrigues, Marcio L.; Nakayasu, Ernesto S.; Oliveira, Debora L. Eukaryotic Cell, Vol. 7, Issue 1 https://doi.org/10.1128/EC.00370-07	journal	November 2007
Listeriolysin O-induced stimulation of mucin exocytosis in polarized intestinal mucin-secreting cells: evidence for toxin recognition of membrane-associated lipids and subsequent toxin internalization through caveolae Coconnier, Marie-Helene; Lorrot, Mathie; Barbat, Alain Cellular Microbiology, Vol. 2, Issue 6 https://doi.org/10.1046/j.1462-5822.2000.00073.x	journal	December 2000
Purification, characterization, and toxicity of the sulfhydryl-activated hemolysin listeriolysin O from Listeria monocytogenes. Geoffroy, C.; Gaillard, J. L.; Alouf, J. E. Infection and Immunity, Vol. 55, Issue 7 https://doi.org/10.1128/IAI.55.7.1641-1646.1987	journal	January 1987
L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein Kocks, C.; Gouin, E.; Tabouret, M. Cell, Vol. 68, Issue 3 https://doi.org/10.1016/0092-8674(92)90188-I	journal	February 1992
MZmine 2: Modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data Pluskal, Tomáš; Castillo, Sandra; Villar-Briones, Alejandro BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-395	journal	July 2010
BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences Kanehisa, Minoru; Sato, Yoko; Morishima, Kanae Journal of Molecular Biology, Vol. 428, Issue 4 https://doi.org/10.1016/j.jmb.2015.11.006	journal	February 2016
Recombinant broad-range phospholipase C from Listeria monocytogenes exhibits optimal activity at acidic pH Huang, Qiongying; Gershenson, Anne; Roberts, Mary F. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1864, Issue 6 https://doi.org/10.1016/j.bbapap.2016.03.008	journal	June 2016
Extracellular Vesicles Modulate Host-Microbe Responses by Altering TLR2 Activity and Phagocytosis van Bergenhenegouwen, Jeroen; Kraneveld, Aletta D.; Rutten, Lieke PLoS ONE, Vol. 9, Issue 2 https://doi.org/10.1371/journal.pone.0089121	journal	February 2014
Listeriolysin O Secreted by Listeria monocytogenes into the Host Cell Cytosol Is Degraded by the N-End Rule Pathway Schnupf, P.; Zhou, J.; Varshavsky, A. Infection and Immunity, Vol. 75, Issue 11 https://doi.org/10.1128/IAI.00164-07	journal	August 2007
Cytosolic expression of SecA2 is a prerequisite for long-term protective immunity Muraille, Eric; Narni-Mancinelli, Emilie; Gounon, Pierre Cellular Microbiology, Vol. 9, Issue 6 https://doi.org/10.1111/j.1462-5822.2007.00883.x	journal	June 2007
Internalin A can mediate phagocytosis of Listeria monocytogenes by mouse macrophage cell lines Sawyer, Richard T.; Drevets, Douglas A.; Campbell, Priscilla A. Journal of Leukocyte Biology, Vol. 60, Issue 5 https://doi.org/10.1002/jlb.60.5.603	journal	November 1996
Extracellular vesicles produced by the Gram-positive bacterium B acillus subtilis are disrupted by the lipopeptide surfactin : Vesicle production and disruption in Brown, Lisa; Kessler, Anne; Cabezas-Sanchez, Pablo Molecular Microbiology, Vol. 93, Issue 1 https://doi.org/10.1111/mmi.12650	journal	June 2014
Impact of Mycobacterium ulcerans Biofilm on Transmissibility to Ecological Niches and Buruli Ulcer Pathogenesis Marsollier, Laurent; Brodin, Priscille; Jackson, Mary PLoS Pathogens, Vol. 3, Issue 5 https://doi.org/10.1371/journal.ppat.0030062	journal	January 2007
Listeriolysin O: the Swiss army knife of Listeria Hamon, Mélanie Anne; Ribet, David; Stavru, Fabrizia Trends in Microbiology, Vol. 20, Issue 8 https://doi.org/10.1016/j.tim.2012.04.006	journal	August 2012
The two distinct phospholipases C of Listeria monocytogenes have overlapping roles in escape from a vacuole and cell-to-cell spread. Smith, G. A.; Marquis, H.; Jones, S. Infection and immunity, Vol. 63, Issue 11 https://doi.org/10.1128/IAI.63.11.4231-4237.1995	journal	January 1995
Transcription Factor σB Plays an Important Role in the Production of Extracellular Membrane-Derived Vesicles in Listeria monocytogenes Lee, Jung Hwa; Choi, Chi-Won; Lee, Taewon PLoS ONE, Vol. 8, Issue 8 https://doi.org/10.1371/journal.pone.0073196	journal	August 2013
Characterization of Listeria monocytogenes pathogenesis in a strain expressing perfringolysin O in place of listeriolysin O. Jones, S.; Portnoy, D. A. Infection and Immunity, Vol. 62, Issue 12 https://doi.org/10.1128/IAI.62.12.5608-5613.1994	journal	January 1994
Bacterial outer membrane vesicles and the host-pathogen interaction Kuehn, M. J. Genes & Development, Vol. 19, Issue 22 https://doi.org/10.1101/gad.1299905	journal	November 2005
Fatty Acids Regulate Stress Resistance and Virulence Factor Production for Listeria monocytogenes Sun, Y.; Wilkinson, B. J.; Standiford, T. J. Journal of Bacteriology, Vol. 194, Issue 19 https://doi.org/10.1128/JB.00045-12	journal	July 2012
Mutagenesis of Active-Site Histidines ofListeria monocytogenes Phosphatidylinositol-Specific Phospholipase C: Effects on Enzyme Activity and Biological Function Bannam, Trudi; Goldfine, Howard Infection and Immunity, Vol. 67, Issue 1 https://doi.org/10.1128/IAI.67.1.182-186.1999	journal	January 1999
Dual roles of plcA in Listeria monocytogenes pathogenesis Camilli, Andrew; Tilney, Lewis G.; Portnoy, Daniel A. Molecular Microbiology, Vol. 8, Issue 1 https://doi.org/10.1111/j.1365-2958.1993.tb01211.x	journal	April 1993
A Two-Component Regulatory System Impacts Extracellular Membrane-Derived Vesicle Production in Group A Streptococcus Resch, Ulrike; Tsatsaronis, James Anthony; Le Rhun, Anaïs mBio, Vol. 7, Issue 6 https://doi.org/10.1128/mBio.00207-16	journal	November 2016
Characterization of protective extracellular membrane-derived vesicles produced by Streptococcus pneumoniae Olaya-Abril, Alfonso; Prados-Rosales, Rafael; McConnell, Michael J. Journal of Proteomics, Vol. 106 https://doi.org/10.1016/j.jprot.2014.04.023	journal	June 2014
Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes Tilney, L. G. The Journal of Cell Biology, Vol. 109, Issue 4 https://doi.org/10.1083/jcb.109.4.1597	journal	October 1989
Membrane vesicles of Clostridium perfringens type A strains induce innate and adaptive immunity Jiang, Yanlong; Kong, Qingke; Roland, Kenneth L. International Journal of Medical Microbiology, Vol. 304, Issue 3-4 https://doi.org/10.1016/j.ijmm.2014.02.006	journal	May 2014
The Pore-Forming Toxin Listeriolysin O Mediates a Novel Entry Pathway of L. monocytogenes into Human Hepatocytes Vadia, Stephen; Arnett, Eusondia; Haghighat, Anne-Cécile PLoS Pathogens, Vol. 7, Issue 11 https://doi.org/10.1371/journal.ppat.1002356	journal	November 2011
Role of hemolysin for the intracellular growth of Listeria monocytogenes Portnoy, D. A. Journal of Experimental Medicine, Vol. 167, Issue 4 https://doi.org/10.1084/jem.167.4.1459	journal	April 1988
Exosomes - Structure, Biogenesis and Biological Role in Non-Small-Cell Lung Cancer Frydrychowicz, M.; Kolecka-Bednarczyk, A.; Madejczyk, M. Scandinavian Journal of Immunology, Vol. 81, Issue 1 https://doi.org/10.1111/sji.12247	journal	December 2014
The ability of Listeria monocytogenes PI-PLC to facilitate escape from the macrophage phagosome is dependent on host PKCβ Poussin, Mathilde A.; Leitges, Michael; Goldfine, Howard Microbial Pathogenesis, Vol. 46, Issue 1 https://doi.org/10.1016/j.micpath.2008.09.008	journal	January 2009
Understanding how Listeria monocytogenes targets and crosses host barriers Lecuit, M. Clinical Microbiology and Infection, Vol. 11, Issue 6 https://doi.org/10.1111/j.1469-0691.2005.01146.x	journal	June 2005
Bacillus anthracis produces membrane-derived vesicles containing biologically active toxins Rivera, J.; Cordero, R. J. B.; Nakouzi, A. S. Proceedings of the National Academy of Sciences, Vol. 107, Issue 44 https://doi.org/10.1073/pnas.1008843107	journal	October 2010
Role of lipid rafts in E-cadherin– and HGF-R/Met–mediated entry of Listeria monocytogenes into host cells Seveau, Stéphanie; Bierne, Hélène; Giroux, Stéphanie The Journal of Cell Biology, Vol. 166, Issue 5 https://doi.org/10.1083/jcb.200406078	journal	August 2004
A statistical approach to estimate the 3D size distribution of spheres from 2D size distributions Kong, Maiying; Bhattacharya, Rabi N.; James, Christina Geological Society of America Bulletin, Vol. 117, Issue 1 https://doi.org/10.1130/B25000.1	journal	January 2005
FiehnLib: Mass Spectral and Retention Index Libraries for Metabolomics Based on Quadrupole and Time-of-Flight Gas Chromatography/Mass Spectrometry Kind, Tobias; Wohlgemuth, Gert; Lee, Do Yup Analytical Chemistry, Vol. 81, Issue 24 https://doi.org/10.1021/ac9019522	journal	December 2009
Listeria monocytogenes mutants lacking phosphatidylinositol-specific phospholipase C are avirulent Camilli, A. Journal of Experimental Medicine, Vol. 173, Issue 3 https://doi.org/10.1084/jem.173.3.751	journal	March 1991
Distribution and Function of Ap-1 Clathrin Adaptor Complexes in Polarized Epithelial Cells Fölsch, Heike; Pypaert, Marc; Schu, Peter The Journal of Cell Biology, Vol. 152, Issue 3 https://doi.org/10.1083/jcb.152.3.595	journal	February 2001
Serum albumin disrupts Cryptococcus neoformans and Bacillus anthracis extracellular vesicles: Serum disruption of microbial vesicles Wolf, Julie M.; Rivera, Johanna; Casadevall, Arturo Cellular Microbiology, Vol. 14, Issue 5 https://doi.org/10.1111/j.1462-5822.2012.01757.x	journal	February 2012
Staphylococcus aureus α-Toxin-Dependent Induction of Host Cell Death by Membrane-Derived Vesicles Thay, Bernard; Wai, Sun Nyunt; Oscarsson, Jan PLoS ONE, Vol. 8, Issue 1 https://doi.org/10.1371/journal.pone.0054661	journal	January 2013
Differential roles of multiple signal peptidases in the virulence of Listeria monocytogenes: L. monocytogenes type I signal peptidases Bonnemain, Claire; Raynaud, Catherine; Réglier-Poupet, Hélène Molecular Microbiology, Vol. 51, Issue 5 https://doi.org/10.1111/j.1365-2958.2004.03916.x	journal	January 2004
Gram-positive bacteria produce membrane vesicles: Proteomics-based characterization of Staphylococcus aureus-derived membrane vesicles Lee, Eun-Young; Choi, Do-Young; Kim, Dae-Kyum PROTEOMICS, Vol. 9, Issue 24 https://doi.org/10.1002/pmic.200900338	journal	December 2009
Offense and defense: microbial membrane vesicles play both ways MacDonald, Ian A.; Kuehn, Meta J. Research in Microbiology, Vol. 163, Issue 9-10 https://doi.org/10.1016/j.resmic.2012.10.020	journal	November 2012
An RNA Thermosensor Controls Expression of Virulence Genes in Listeria monocytogenes Johansson, Jörgen; Mandin, Pierre; Renzoni, Adriana Cell, Vol. 110, Issue 5 https://doi.org/10.1016/S0092-8674(02)00905-4	journal	September 2002
The MaxQuant computational platform for mass spectrometry-based shotgun proteomics Tyanova, Stefka; Temu, Tikira; Cox, Juergen Nature Protocols, Vol. 11, Issue 12 https://doi.org/10.1038/nprot.2016.136	journal	October 2016
Staphylococcus aureus Produces Membrane-Derived Vesicles That Induce Host Cell Death Gurung, Mamata; Moon, Dong Chan; Choi, Chi Won PLoS ONE, Vol. 6, Issue 11 https://doi.org/10.1371/journal.pone.0027958	journal	November 2011
Types and origins of bacterial membrane vesicles Toyofuku, Masanori; Nomura, Nobuhiko; Eberl, Leo Nature Reviews Microbiology, Vol. 17, Issue 1 https://doi.org/10.1038/s41579-018-0112-2	journal	November 2018
MetaboliteDetector: Comprehensive Analysis Tool for Targeted and Nontargeted GC/MS Based Metabolome Analysis Hiller, Karsten; Hangebrauk, Jasper; Jäger, Christian Analytical Chemistry, Vol. 81, Issue 9 https://doi.org/10.1021/ac802689c	journal	May 2009
How Listeria monocytogenes organizes its surface for virulence Carvalho, Filipe; Sousa, Sandra; Cabanes, Didier Frontiers in Cellular and Infection Microbiology, Vol. 4 https://doi.org/10.3389/fcimb.2014.00048	journal	April 2014
The arsenal of virulence factors deployed by Listeria monocytogenes to promote its cell infection cycle Camejo, Ana; Carvalho, Filipe; Reis, Olga Virulence, Vol. 2, Issue 5 https://doi.org/10.4161/viru.2.5.17703	journal	September 2011
Listeriolysin O Is Necessary and Sufficient to Induce Autophagy during Listeria monocytogenes Infection Meyer-Morse, Nicole; Robbins, Jennifer R.; Rae, Chris S. PLoS ONE, Vol. 5, Issue 1 https://doi.org/10.1371/journal.pone.0008610	journal	January 2010

Cited By (3)

Answers to naysayers regarding microbial extracellular vesicles Coelho, Carolina; Casadevall, Arturo Biochemical Society Transactions, Vol. 47, Issue 4 https://doi.org/10.1042/bst20180252	journal	July 2019
Fungal Extracellular Vesicles as Potential Targets for Immune Interventions Freitas, Mateus Silveira; Bonato, Vânia Luiza Deperon; Pessoni, Andre Moreira mSphere, Vol. 4, Issue 6 https://doi.org/10.1128/msphere.00747-19	journal	October 2019
A Novel Model of Cancer Drug Resistance: Oncosomal Release of Cytotoxic and Antibody-Based Drugs Eguchi, Takanori; Taha, Eman Ahmed; Calderwood, Stuart K. Biology, Vol. 9, Issue 3 https://doi.org/10.3390/biology9030047	journal	March 2020

Similar Records

Structural insights into glutathione-mediated activation of the master regulator PrfA in Listeria monocytogenes

Journal Article · Tue Mar 07 00:00:00 EST 2017 · Protein & Cell · OSTI ID:1765007

Wang, Yong; Feng, Han; Zhu, Yalan; +1 more

A structural comparison of Listeria monocytogenes protein chaperones PrsA1 and PrsA2 reveals molecular features required for virulence

Journal Article · Wed Mar 23 00:00:00 EDT 2016 · Molecular Microbiology · OSTI ID:1765007

Cahoon, Laty A.; Freitag, Nancy E.; Prehna, Gerd

Kinetics of killing Listeria monocytogenes by macrophages: correlation of /sup 3/H-DNA release from labeled bacteria and changes in numbers of viable organisms by mathematical model

Journal Article · Wed Dec 01 00:00:00 EST 1982 · J. Reticuloendothel. Soc.; (United States) · OSTI ID:1765007

Davies, W A

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Exosome (vesicle)
extracellular vesicles
virulence factor
Phospholipase C
Gram-positive bacteria
Listeria monocytogenes
hemolysis
listeriolysin
MPLEx

Title: Listeria monocytogenes virulence factors, including listeriolysin O, are secreted in biologically active extracellular vesicles

Citation Formats

References (70)

Cited By (3)

Similar Records

Related Subjects