Intracellular Growth of Legionella pneumophila in Dictyostelium discoideum, a System for Genetic Analysis of Host-Pathogen Interactions
Open accessAbstract
Conditions were established in which Legionella pneumophila, an intracellular bacterial pathogen, could replicate within the unicellular organism Dictyostelium discoideum. By several criteria,L. pneumophila grew by the same mechanism within D. discoideum as it does in amoebae and macrophages. Bacteria grew within membrane-bound vesicles associated with rough endoplasmic reticulum, and L. pneumophila dot/icm mutants, blocked for growth in macrophages and amoebae, also did not grow in D. discoideum. Internalized L. pneumophila avoided degradation by D. discoideum and showed evidence of reduced fusion with endocytic compartments. The ability of L. pneumophila to grow within D. discoideum depended on the growth state of the cells.D. discoideum grown as adherent monolayers was susceptible to L. pneumophila infection and to contact-dependent cytotoxicity during high-multiplicity infections, whereas D. discoideum grown in suspension was relatively resistant to cytotoxicity and did not support intracellular growth. Some known D. discoideum mutants were examined for their effect on growth of L. pneumophila. The coronin mutant and the myoA/B double myosin I mutant were more permissive than wild-type strains for intracellular growth. Growth of L. pneumophila in a G β mutant was slightly reduced compared to the parent strain. This work demonstrates the usefulness of the L. pneumophila-D. discoideum system for genetic analysis of host-pathogen interactions.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Several bacterial pathogens for humans, such as legionella, mycobacteria and salmonella, are pathogenic also for Dictyostelium.
“Several bacterial pathogens for humans, such as legionella, mycobacteria and salmonella, are pathogenic also for Dictyostelium, favouring the use of this model to study host-pathogen interactions [9-19].”
From Genome-wide transcriptional changes induced by phagocytosis or growth on bacteria in Dictyostelium (2008) · cites this paper as [10]
Cites
Lemaître, B., Nicolas, E., Michaut, L., Reichhart, J., & Hoffmann, J. A. (1996) · Cell · doi:10.1016/s0092-8674(00)80172-5 · Cited by 4,027 · see citing works
FACS-optimized mutants of the green fluorescent protein (GFP)
Cormack, B. P., Valdivia, R. H., & Falkow, S. (1996) · Gene · doi:10.1016/0378-1119(95)00685-0 · Cited by 2,621 · see citing works
Tan, M., Mahajan‐Miklos, S., & Ausubel, F. M. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.2.715 · Cited by 1,008 · see citing works
Disruption of the Dictyostelium Myosin Heavy Chain Gene by Homologous Recombination
Lozanne, A. D., & Spudich, J. A. (1987) · Science · doi:10.1126/science.3576222 · Cited by 988 · see citing works
The Toll-receptor family and control of innate immunity.
Kopp, E., & Medzhitov, R. (1999) · Current Opinion in Immunology · doi:10.1016/s0952-7915(99)80003-x · Cited by 734 · see citing works
Conjugative Transfer by the Virulence System of Legionella pneumophila
Vogel, J. P., Andrews, H. L., Wong, S. K., & Isberg, R. R. (1998) · Science · doi:10.1126/science.279.5352.873 · Cited by 721 · see citing works
Self-citationHorwitz, M. A. (1983) · The Journal of Experimental Medicine · doi:10.1084/jem.158.6.2108 · Cited by 705 · see citing works
Horwitz, M. A. (1983) · The Journal of Experimental Medicine · doi:10.1084/jem.158.4.1319 · Cited by 659 · see citing works
Berger, K. H., & Isberg, R. R. (1993) · Molecular Microbiology · doi:10.1111/j.1365-2958.1993.tb01092.x · Cited by 646 · see citing works
Self-citationCharcoal-yeast extract agar: primary isolation medium for Legionella pneumophila
FEELEY, J. C., Gibson, R. J., GORMAN, G. W., Langford, N. C., Rasheed, J. K., Mackel, D. C., & Baine, W. B. (1979) · Journal of Clinical Microbiology · doi:10.1128/jcm.10.4.437-441.1979 · Cited by 643 · see citing works
Horwitz, M. A., & Silverstein, S. C. (1980) · Journal of Clinical Investigation · doi:10.1172/jci109874 · Cited by 639 · see citing works
Sussman, M. (1987) · Methods in cell biology · doi:10.1016/s0091-679x(08)61635-0 · Cited by 599 · 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
The molecular ecology of legionellae
Fields, B. S. (1996) · Trends in Microbiology · doi:10.1016/0966-842x(96)10041-x · Cited by 543 · see citing works
Association of Legionella pneumophila with the macrophage endoplasmic reticulum
Swanson, M. S., & Isberg, R. R. (1995) · Infection and Immunity · doi:10.1128/iai.63.9.3609-3620.1995 · Cited by 540 · see citing works
Self-citationSegal, G., Purcell, M., & Shuman, H. A. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.4.1669 · Cited by 540 · see citing works
A series of wide-host-range low-copy-number vectors that allow direct screening for recombinants
Morales, V. M., Bäckman, A., & Bagdasarian, M. (1991) · Gene · doi:10.1016/0378-1119(91)90007-x · Cited by 509 · see citing works
Sexuality and the genetics of bacteria.
Jacob, F., & Wollman, E. (1961) · Virtual Defense Library (Ministerio de Defensa) · Cited by 447 · see citing works
Legionella pneumophila inhibits acidification of its phagosome in human monocytes.
Horwitz, M. A., & Maxfield, F. R. (1984) · The Journal of Cell Biology · doi:10.1083/jcb.99.6.1936 · Cited by 382 · see citing works
Expression of Legionella pneumophila Virulence Traits in Response to Growth Conditions
Byrne, B. G., & Swanson, M. S. (1998) · Infection and Immunity · doi:10.1128/iai.66.7.3029-3034.1998 · Cited by 364 · see citing works
Roy, C. R., Berger, K. H., & Isberg, R. R. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00841.x · Cited by 357 · see citing works
Self-citationManiak, M., Rauchenberger, R., Albrecht, R., Murphy, J., & Gerisch, G. (1995) · Cell · doi:10.1016/0092-8674(95)90207-4 · Cited by 354 · see citing works
Segal, G., & Shuman, H. A. (1999) · Infection and Immunity · doi:10.1128/iai.67.5.2117-2124.1999 · Cited by 303 · see citing works
Berger, K. H., Merriam, J., & Isberg, R. R. (1994) · Molecular Microbiology · doi:10.1111/j.1365-2958.1994.tb01317.x · Cited by 256 · see citing works
Self-citationFluid-phase uptake by macropinocytosis in Dictyostelium
Hacker, U., Albrecht, R., & Maniak, M. (1997) · Journal of Cell Science · doi:10.1242/jcs.110.2.105 · Cited by 251 · see citing works
de Hostos, E. L., Rehfuess, C., Bradtke, B., Waddell, D. R., Albrecht, R., Murphy, J., & Gerisch, G. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.120.1.163 · Cited by 250 · see citing works
Sensitivity of Dictyostelium discoideum to nucleic acid analogues
Loomis, W. F. (1971) · Experimental Cell Research · doi:10.1016/0014-4827(71)90107-8 · Cited by 238 · see citing works
Gao, L., Harb, O. S., & Kwaik, Y. A. (1997) · Infection and Immunity · doi:10.1128/iai.65.11.4738-4746.1997 · Cited by 235 · see citing works
Evidence for pore‐forming ability by Legionella pneumophila
Kirby, J. E., Vogel, J. P., Andrews, H. L., & Isberg, R. R. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00680.x · Cited by 234 · see citing works
Self-citationThe G protein beta subunit is essential for multiple responses to chemoattractants in Dictyostelium.
Wu, L., Valkema, R., Haastert, P. J. V., & Devreotes, P. N. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.129.6.1667 · Cited by 209 · see citing works
Andrews, H. L., Vogel, J. P., & Isberg, R. R. (1998) · Infection and Immunity · doi:10.1128/iai.66.3.950-958.1998 · Cited by 208 · see citing works
Self-citationDictyostelium myosin I double mutants exhibit conditional defects in pinocytosis.
Novak, K. D., Peterson, M., Reedy, M. C., & Titus, M. A. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.131.5.1205 · Cited by 192 · see citing works
Brand, B. C., Sadosky, A., & Shuman, H. A. (1994) · Molecular Microbiology · doi:10.1111/j.1365-2958.1994.tb01316.x · Cited by 184 · see citing works
A DESCRIPTIVE STUDY OF THE DEVELOPMENT OF THE SLIME MOLD DICTYOSTELIUM DISCOIDEUM
Bonner, J. T. (1944) · American Journal of Botany · doi:10.1002/j.1537-2197.1944.tb08016.x · Cited by 178 · see citing works
Characterization of a new region required for macrophage killing by Legionella pneumophila
Segal, G., & Shuman, H. A. (1997) · Infection and Immunity · doi:10.1128/iai.65.12.5057-5066.1997 · Cited by 170 · see citing works
Demonstration of the Agent of Legionnaires’ Disease in Tissue
Chandler, F. W., Hicklin, M. D., & Blackmon, J. A. (1977) · New England Journal of Medicine · doi:10.1056/nejm197712012972206 · Cited by 159 · see citing works
The unconventional myosin encoded by the myoA gene plays a role in Dictyostelium motility.
Titus, M. A., Wessels, D. J., Spudich, J. A., & Soll, D. R. (1993) · Molecular Biology of the Cell · doi:10.1091/mbc.4.2.233 · Cited by 147 · see citing works
Myosin IB null mutants of Dictyostelium exhibit abnormalities in motility
Wessels, D. J., Murray, J. W., Jung, G., Hammer, J. A., & Soll, D. R. (1991) · Cell Motility and the Cytoskeleton · doi:10.1002/cm.970200406 · Cited by 143 · see citing works
Peracino, B., Borleis, J., Jin, T., Westphal, M., Schwartz, J.-M., Wu, L., Bracco, E., Gerisch, G., Devreotes, P., & Bozzaro, S. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.141.7.1529 · Cited by 129 · see citing works
Wiater, L. A., Dunn, K. W., Maxfield, F. R., & Shuman, H. A. (1998) · Infection and Immunity · doi:10.1128/iai.66.9.4450-4460.1998 · Cited by 126 · see citing works
Zhou, K., Takegawa, K., Emr, S. D., & Firtel, R. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.10.5645 · Cited by 126 · see citing works
Nash, T., Libby, D. M., & Horwitz, M. A. (1988) · The Journal of Immunology · doi:10.4049/jimmunol.140.11.3978 · Cited by 121 · see citing works
Identification of Legionella pneumophila mutants that have aberrant intracellular fates
Swanson, M. S., & Isberg, R. R. (1996) · Infection and Immunity · doi:10.1128/iai.64.7.2585-2594.1996 · Cited by 121 · see citing works
Self-citationEvidence for apoptosis of human macrophage-like HL-60 cells by Legionella pneumophila infection
Müller, A., Hacker, J. H., & Brand, B. C. (1996) · Infection and Immunity · doi:10.1128/iai.64.12.4900-4906.1996 · Cited by 115 · see citing works
TheLegionella pneumophila icmGCDJBFGenes Are Required for Killing of Human Macrophages
Purcell, M., & Shuman, H. A. (1998) · Infection and Immunity · doi:10.1128/iai.66.5.2245-2255.1998 · Cited by 112 · see citing works
Role of PKA in the Timing of Developmental Events in Dictyostelium Cells
Loomis, W. F. (1998) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.62.3.684-694.1998 · Cited by 106 · see citing works
Vacuolar H+-ATPase of Dictyostelium discoideum A monoclonal antibody study
Fok, A. K., Clarke, M., Ma, L., & Allen, R. D. (1993) · Journal of Cell Science · doi:10.1242/jcs.106.4.1103 · Cited by 83 · see citing works
Buczynski, G., Bush, J., Zhang, L., Rodriguez‐Paris, J., & Cardelli, J. A. (1997) · Molecular Biology of the Cell · doi:10.1091/mbc.8.7.1343 · Cited by 78 · see citing works
Self-citationTaking the plunge: terminal differentiation in Dictyostelium
Thomason, P. A., Traynor, D., & Kay, R. R. (1999) · Trends in Genetics · doi:10.1016/s0168-9525(98)01635-7 · Cited by 70 · see citing works
Use of Salt to Isolate Legionella pneumophila Mutants Unable to Replicate in Macrophages
Vogel, J. P., Roy, C. R., & Isberg, R. R. (1996) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1996.tb52975.x · Cited by 69 · see citing works
Self-citationElectrophoretic karyotype for Dictyostelium discoideum.
Cox, E. H., Vocke, C. D., Walter, S., Gregg, K., & Bain, E. S. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.21.8247 · Cited by 63 · see citing works
Temesvari, L. A., Rodriguez‐Paris, J., Bush, J., Steck, T. L., & Cardelli, J. A. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)47307-3 · Cited by 60 · see citing works
Self-citationIntegrated maps of the chromosomes in Dictyostelium discoideum.
Loomis, W. F., Welker, D. L., Hughes, J., Maghakian, D., & Kuspa, A. (1995) · Genetics · doi:10.1093/genetics/141.1.147 · Cited by 53 · see citing works
Genetics of Growth in Axenic Medium of the Cellular Slime Mould Dictyostelium discoideum
Williams, K. L., Kessin, R. H., & Newell, P. C. (1974) · Nature · doi:10.1038/247142a0 · Cited by 53 · see citing works
Phagosomal Proteins of Dictyostelium discoideum
REZABEK, B. L., Rodriguez‐Paris, J., Cardelli, J. A., & Chia, C. P. (1997) · Journal of Eukaryotic Microbiology · doi:10.1111/j.1550-7408.1997.tb05668.x · Cited by 35 · see citing works
Self-citationChapter 6 Endocytosis and Recognition Mechanisms in Dictyostelium discoideum
Vogel, G. (1987) · Methods in cell biology · doi:10.1016/s0091-679x(08)61640-4 · Cited by 25 · see citing works
Characterization of lysosomal membrane proteins of Dictyostelium discoideum
Temesvari, L. A., Rodriguez‐Paris, J., Bush, J., Steck, T. L., & Caradelli, J. (1994) · TigerPrints (Clemson University) · Cited by 21 · see citing works
Techniques for the visualisation of cytoskeletal components in Dictyostelium discoideum
de Priester, W. (1991) · Electron Microscopy Reviews · doi:10.1016/0892-0354(91)90009-2 · Cited by 6 · see citing works
Flagged first, then by citations
1 of the 59 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Legionella and Legionnaires' Disease: 25 Years of Investigation
Fields, B. S., Benson, R. F., & Besser, R. E. (2002) · Clinical Microbiology Reviews · doi:10.1128/cmr.15.3.506-526.2002 · Cited by 1,601 · see citing works
The genome of the social amoeba Dictyostelium discoideum
Eichinger, L., Pachebat, J. A., Glöckner, G., Rajandream, M.-A., Sucgang, R., Berriman, M., Song, J., Olsen, R., Szafranski, K., Xu, Q., et al. (2005) · Nature · doi:10.1038/nature03481 · Cited by 1,351 · see citing works
Pukatzki, S. U., Ma, A. T., Sturtevant, D., Krastins, B., Sarracino, D. A., Nelson, W. C., Heidelberg, J. F., & Mekalanos, J. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510322103 · Cited by 1,116 · see citing works
Microorganisms Resistant to Free-Living Amoebae
Greub, G., & Raoult, D. (2004) · Clinical Microbiology Reviews · doi:10.1128/cmr.17.2.413-433.2004 · Cited by 1,066 · see citing works
Amoebae as Training Grounds for Intracellular Bacterial Pathogens
Molmeret, M., Horn, M., Wagner, M., Šantić, M., & Kwaik, Y. A. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.1.20-28.2005 · Cited by 550 · see citing works
Luo, Z., & Isberg, R. R. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0304916101 · Cited by 479 · see citing works
Self-citationThe phagosome: compartment with a license to kill
Haas, A. (2007) · Traffic · doi:10.1111/j.1600-0854.2006.00531.x · Cited by 450 · see citing works
Zhu, W., Banga, S., Tan, Y., Zheng, C. C., Stephenson, R. E., Gately, J. M., & Luo, Z. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017638 · Cited by 304 · see citing works
Caenorhabditis elegans is a model host for Salmonella typhimurium
Labrousse, A. M., Chauvet, S., Couillault, C., Kurz, C. L., & Ewbank, J. J. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00833-2 · Cited by 301 · see citing works
Legionella pneumophila: an aquatic microbe goes astray
Steinert, M., Hentschel, U., & Hacker, J. H. (2002) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2002.tb00607.x · Cited by 292 · see citing works
Weber, S. S., Ragaz, C., Reus, K., Nyfeler, Y., & Hilbi, H. (2006) · PLoS Pathogens · doi:10.1371/journal.ppat.0020046 · Cited by 292 · see citing works
Pukatzki, S., Kessin, R. H., & Mekalanos, J. J. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.052704399 · Cited by 289 · see citing works
Pseudomonas aeruginosaVirulence Analyzed in aDictyostelium discoideumHost System
Cosson, P., Zulianello, L., Join‐Lambert, O., Faurisson, F., Gebbie, L. K., Benghezal, M., van Delden, C., Curty, L. K., & Köhler, T. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.11.3027-3033.2002 · Cited by 268 · see citing works
Silkworm larvae as an animal model of bacterial infection pathogenic to humans
Kaito, C., Akimitsu, N., Watanabe, H., & Sekimizu, K. (2002) · Microbial Pathogenesis · doi:10.1006/mpat.2002.0494 · Cited by 264 · see citing works
Jia, K., Thomas, C., Akbar, M., Sun, Q., ADAMS-HUET, B. A., Gilpin, C. J., & Levine, B. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0813319106 · Cited by 221 · see citing works
The Icm/Dot type-IV secretion systems ofLegionella pneumophilaandCoxiella burnetii
Segal, G., Feldman, M., & Zusman, T. (2004) · FEMS Microbiology Reviews · doi:10.1016/j.femsre.2004.07.001 · Cited by 218 · see citing works
Derré, I., & Isberg, R. R. (2004) · Infection and Immunity · doi:10.1128/iai.72.5.3048-3053.2004 · Cited by 213 · see citing works
Self-citationFrom Many Hosts, One Accidental Pathogen: The Diverse Protozoan Hosts of Legionella
Boamah, D. K., Zhou, G., Ensminger, A. W., & O’Connor, T. J. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00477 · Cited by 201 · see citing works
Ragaz, C., Pietsch, H., Urwyler, S., Tiaden, A. N., Weber, S. S., & Hilbi, H. (2008) · Cellular Microbiology · doi:10.1111/j.1462-5822.2008.01219.x · Cited by 207 · see citing works
Environmental predators as models for bacterial pathogenesis
Hilbi, H., Weber, S. S., Ragaz, C., Nyfeler, Y., & Urwyler, S. (2007) · Environmental Microbiology · doi:10.1111/j.1462-2920.2007.01238.x · Cited by 197 · see citing works
Miyata, S. T., Kitaoka, M., Brooks, T. M., McAuley, S. B., & Pukatzki, S. (2011) · Infection and Immunity · doi:10.1128/iai.01266-10 · Cited by 205 · see citing works
NF-κB translocation prevents host cell death after low-dose challenge byLegionella pneumophila
Losick, V. P., & Isberg, R. R. (2006) · The Journal of Experimental Medicine · doi:10.1084/jem.20060766 · Cited by 194 · see citing works
Self-citationIcm/Dot‐dependent upregulation of phagocytosis by Legionella pneumophila
Hilbi, H., Segal, G., & Shuman, H. A. (2001) · Molecular Microbiology · doi:10.1046/j.1365-2958.2001.02645.x · Cited by 194 · see citing works
O’Connor, T. J., Adepoju, Y., Boyd, D. H., & Isberg, R. R. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1111678108 · Cited by 189 · see citing works
Self-citationImmune-like Phagocyte Activity in the Social Amoeba
Chen, G., Zhuchenko, O., & Kuspa, A. (2007) · Science · doi:10.1126/science.1143991 · Cited by 205 · see citing works
Mairey, É., Genovesio, A., Donnadieu, E., Bernard, C., Jaubert, F., Pinard, E., Seylaz, J., Olivo‐Marín, J., Nassif, X., & Duménil, G. (2006) · The Journal of Experimental Medicine · doi:10.1084/jem.20060482 · Cited by 185 · see citing works
Tiaden, A. N., Spirig, T., Weber, S. S., Brüggemann, H., Bosshard, R., Buchrieser, C., & Hilbi, H. (2007) · Cellular Microbiology · doi:10.1111/j.1462-5822.2007.01005.x · Cited by 175 · see citing works
Drosophila melanogaster Is a Genetically Tractable Model Host for Mycobacterium marinum
Dionne, M., Ghori, N., & Schneider, D. S. (2003) · Infection and Immunity · doi:10.1128/iai.71.6.3540-3550.2003 · Cited by 181 · see citing works
The Role of the Immune System Beyond the Fight Against Infection
Sattler, S. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-57613-8_1 · Cited by 167 · see citing works
Mampel, J., Spirig, T., Weber, S. S., Haagensen, J. A. J., Molin, S., & Hilbi, H. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.72.4.2885-2895.2006 · Cited by 164 · see citing works
Steenbergen, J. N., Nosanchuk, J. D., Malliaris, S. D., & Casadevall, A. (2003) · Infection and Immunity · doi:10.1128/iai.71.9.4862-4872.2003 · Cited by 156 · see citing works
Cardelli, J. (2001) · Traffic · doi:10.1034/j.1600-0854.2001.002005311.x · Cited by 150 · see citing works
Self-citationHélaine, S., Carbonnelle, É., Prouvensier, L., Béretti, J., Nassif, X., & Pelicic, V. (2004) · Molecular Microbiology · doi:10.1111/j.1365-2958.2004.04372.x · Cited by 149 · see citing works
Dictyostelium as host model for pathogenesis
Steinert, M., & Heuner, K. (2005) · Cellular Microbiology · doi:10.1111/j.1462-5822.2005.00493.x · Cited by 144 · see citing works
Water ecology of Legionella and protozoan: environmental and public health perspectives
Borella, P., Guerrieri, E., Marchesi, I., Bondi, M., & Messi, P. (2005) · Biotechnology annual review · doi:10.1016/s1387-2656(05)11011-4 · Cited by 139 · see citing works
From Grazing Resistance to Pathogenesis: The Coincidental Evolution of Virulence Factors
Adiba, S., Nizak, C., van Baalen, M., Denamur, É., & Depaulis, F. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011882 · Cited by 136 · see citing works
Weber, S. S., Ragaz, C., & Hilbi, H. (2008) · Cellular Microbiology · doi:10.1111/j.1462-5822.2008.01266.x · Cited by 133 · see citing works
Hagedorn, M., & Soldati, T. (2007) · Cellular Microbiology · doi:10.1111/j.1462-5822.2007.00993.x · Cited by 126 · see citing works
Aubert, D., Flannagan, R. S., & Valvano, M. A. (2008) · Infection and Immunity · doi:10.1128/iai.01338-07 · Cited by 132 · see citing works
Liu, Y., & Luo, Z. (2006) · Infection and Immunity · doi:10.1128/iai.01278-06 · Cited by 131 · see citing works
Solomon, J. M., Leung, G. S., & Isberg, R. R. (2003) · Infection and Immunity · doi:10.1128/iai.71.6.3578-3586.2003 · Cited by 127 · see citing works
Self-citationDrosophila melanogaster as a model host for Staphylococcus aureus infection
Needham, A. J., Kibart, M., Crossley, H., Ingham, P. W., & Foster, S. J. (2004) · Microbiology · doi:10.1099/mic.0.27116-0 · Cited by 129 · see citing works
Otto, G. P., Wu, M., Clarke, M., Lu, H. X., Anderson, O. R., Hilbi, H., Shuman, H. A., & Kessin, R. H. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03826.x · Cited by 124 · see citing works
The Professional Phagocyte Dictyostelium discoideum as a Model Host for Bacterial Pathogens
Bozzaro, S., & Eichinger, L. (2011) · Current Drug Targets · doi:10.2174/138945011795677782 · Cited by 120 · see citing works
Aggravating Genetic Interactions Allow a Solution to Redundancy in a Bacterial Pathogen
O’Connor, T. J., Boyd, D. H., Dorer, M. S., & Isberg, R. R. (2012) · Science · doi:10.1126/science.1229556 · Cited by 120 · see citing works
Self-citationDynamic properties of Legionella-containing phagosomes in Dictyostelium amoebae
Lu, H. X., & Clarke, M. (2005) · Cellular Microbiology · doi:10.1111/j.1462-5822.2005.00528.x · Cited by 118 · see citing works
Use of Galleria mellonella as a Model Organism to Study Legionella pneumophila Infection
Harding, C. R., Schroeder, G. N., Collins, J. W., & Frankel, G. M. (2013) · Journal of Visualized Experiments · doi:10.3791/50964 · Cited by 121 · see citing works
Escoll, P., Rolando, M., Gómez-Valero, L., & Buchrieser, C. (2013) · Current topics in microbiology and immunology · doi:10.1007/82_2013_351 · Cited by 113 · see citing works
Solomon, J. M., & Isberg, R. R. (2000) · Trends in Microbiology · doi:10.1016/s0966-842x(00)01852-7 · Cited by 112 · see citing works
Self-citationDictyostelium transcriptional host cell response upon infection with Legionella
Farbrother, P., Wagner, C., Na, J., Tunggal, B., Morio, T., Urushihara, H., Tanaka, Y., Schleicher, M., Steinert, M., & Eichinger, L. (2006) · Cellular Microbiology · doi:10.1111/j.1462-5822.2005.00633.x · Cited by 112 · see citing works
Legionella pneumophila Pathogenesis in the Galleria mellonella Infection Model
Harding, C. R., Schroeder, G. N., Reynolds, S. E., Kosta, A., Collins, J. W., Mousnier, A., & Frankel, G. M. (2012) · Infection and Immunity · doi:10.1128/iai.00510-12 · Cited by 107 · see citing works
VBNC Legionella pneumophila cells are still able to produce virulence proteins
Alleron, L., Khemiri, A., Koubar, M., Lacombe, C., Coquet, L., Cosette, P., Jouenne, T., & Frère, J. (2013) · Water Research · doi:10.1016/j.watres.2013.08.032 · Cited by 111 · see citing works
Acanthamoeba and Dictyostelium as Cellular Models for Legionella Infection
Swart, A. L., Harrison, C. F., Eichinger, L., Steinert, M., & Hilbi, H. (2018) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2018.00061 · Cited by 105 · see citing works
Various bacterial pathogens and symbionts infect the amoeba Dictyostelium discoideum
Skriwan, C., Fajardo, M., Hägele, S., Horn, M., Wagner, M., Michel, R., Krohne, G., Schleicher, M., Hacker, J., & Steinert, M. (2002) · International Journal of Medical Microbiology · doi:10.1078/1438-4221-00177 · Cited by 109 · see citing works
Melican, K., Veloso, P. M., Martin, T., Bruneval, P., & Duménil, G. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003139 · Cited by 108 · see citing works
The Ecology and Evolution of Amoeba-Bacterium Interactions
Shi, Y., Queller, D. C., Tian, Y., Zhang, S., Yan, Q., He, Z., He, Z., Wu, C., Wang, C., & Shu, L. (2020) · Applied and Environmental Microbiology · doi:10.1128/aem.01866-20 · Cited by 108 · see citing works
Phagocytosis: the convoluted way from nutrition to adaptive immunity
Desjardins, M., Houde, M., & Gagnon, E. (2005) · Immunological Reviews · doi:10.1111/j.0105-2896.2005.00319.x · Cited by 107 · see citing works
Zusman, T., Gal‐Mor, O., & Segal, G. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.1.67-75.2002 · Cited by 106 · see citing works
Berk, S. G., Faulkner, G., Garduño, E., Joy, M. C., Ortiz-Jiménez, M. A., & Garduño, R. A. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.01214-07 · Cited by 99 · see citing works
Proteomics Fingerprinting of Phagosome Maturation and Evidence for the Role of a Gα during Uptake
Gotthardt, D., Blancheteau, V., Bosserhoff, A., Ruppert, T., Delorenzi, M., & Soldati, T. (2006) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m600113-mcp200 · Cited by 98 · see citing works
Steiner, B., Weber, S., & Hilbi, H. (2017) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2017.08.004 · Cited by 94 · see citing works
Chapter 6 Phagocytosis and Host–Pathogen Interactions in Dictyostelium with a Look at Macrophages
Bozzaro, S., Bucci, C., & Steinert, M. (2008) · International review of cytology · doi:10.1016/s1937-6448(08)01206-9 · Cited by 94 · see citing works
Function and Mechanism of Action of <i>Dictyostelium</i> Nramp1 (Slc11a1) in Bacterial Infection
Peracino, B., Wagner, C., Balest, A., Balbo, A., Pergolizzi, B., Noegel, A. A., Steinert, M., & Bozzaro, S. (2006) · Traffic · doi:10.1111/j.1600-0854.2005.00356.x · Cited by 96 · see citing works
Simple system – substantial share: The use of Dictyostelium in cell biology and molecular medicine
Müller‐Taubenberger, A., Kortholt, A., & Eichinger, L. (2012) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2012.10.003 · Cited by 94 · see citing works
Dictyostelium Finds New Roles to Model
Williams, J. G. (2010) · Genetics · doi:10.1534/genetics.110.119297 · Cited by 90 · see citing works
Derré, I., & Isberg, R. R. (2005) · Infection and Immunity · doi:10.1128/iai.73.7.4370-4380.2005 · Cited by 93 · see citing works
Self-citationPathogen–host interactions in Dictyostelium, Legionella, Mycobacterium and other pathogens
Steinert, M. (2010) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2010.11.003 · Cited by 89 · see citing works
Regulation of phagocytosis and endo-phagosomal trafficking pathways in Dictyostelium discoideum
Rupper, A., & Cardelli, J. (2001) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/s0304-4165(01)00106-4 · Cited by 103 · see citing works
Self-citationProteomic analysis of Legionella-containing phagosomes isolated from Dictyostelium
Shevchuk, O., Batzilla, C. F., Hägele, S., Kusch, H., Engelmann, S., Hecker, M., Haas, A., Heuner, K., Glöckner, G., & Steinert, M. (2009) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2009.03.006 · Cited by 87 · see citing works
de Pace, F., de Paiva, J. B., Nakazato, G., Lancellotti, M., Sircili, M. P., Stehling, E. G., da Silveira, W. D., & Sperandio, V. (2011) · Microbiology · doi:10.1099/mic.0.050005-0 · Cited by 86 · see citing works
Behets, J., Declerck, P., Delaedt, Y., Creemers, B., & Ollevier, F. (2006) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2006.07.002 · Cited by 83 · see citing works
GarcÃa-Lara, J., Needham, A. J., & Foster, S. J. (2004) · FEMS Immunology & Medical Microbiology · doi:10.1016/j.femsim.2004.11.003 · Cited by 79 · see citing works
Lamothe, J., Thyssen, S. M., & Valvano, M. A. (2004) · Cellular Microbiology · doi:10.1111/j.1462-5822.2004.00424.x · Cited by 79 · see citing works
Increasing Diversity within Chlamydiae
Corsaro, D., Valassina, M., & Venditti, D. (2003) · Critical Reviews in Microbiology · doi:10.1080/713610404 · Cited by 77 · see citing works
Isaac, D. T., Laguna, R. K., Valtz, N., & Isberg, R. R. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1511389112 · Cited by 72 · see citing works
Self-citationLi, Z., Solomon, J. M., & Isberg, R. R. (2005) · Cellular Microbiology · doi:10.1111/j.1462-5822.2004.00472.x · Cited by 72 · see citing works
Self-citationDiverse protist grazers select for virulence-related traits in Legionella
Amaro, F., Wang, W., Gilbert, J. A., Anderson, O. R., & Shuman, H. A. (2015) · The ISME Journal · doi:10.1038/ismej.2014.248 · Cited by 73 · see citing works
Nasser, W., Santhanam, B., Miranda, E. R., Parikh, A., Juneja, K., Rot, G., Dinh, C., Chen, R., Zupan, B., Shaulsky, G., et al. (2013) · Current Biology · doi:10.1016/j.cub.2013.04.034 · Cited by 73 · see citing works
Fajardo, M., Schleicher, M., Noegel, A., Bozzaro, S., Killinger, S., Heuner, K., Hacker, J., & Steinert, M. (2004) · Microbiology · doi:10.1099/mic.0.27111-0 · Cited by 73 · see citing works
Genome-wide transcriptional changes induced by phagocytosis or growth on bacteria in Dictyostelium
Sillo, A., Bloomfield, G., Balest, A., Balbo, A., Pergolizzi, B., Peracino, B., Skelton, J., Ivens, A., & Bozzaro, S. (2008) · BMC Genomics · doi:10.1186/1471-2164-9-291 · Cited by 69 · see citing works
Harris, E. N., & Cardelli, J. A. (2002) · Journal of Cell Science · doi:10.1242/jcs.00050 · Cited by 70 · see citing works
Self-citationTosetti, N., Croxatto, A., & Greub, G. (2014) · Microbial Pathogenesis · doi:10.1016/j.micpath.2014.07.009 · Cited by 68 · see citing works
Stewart, C. R., Rossier, O., & Cianciotto, N. P. (2008) · Journal of Bacteriology · doi:10.1128/jb.01531-08 · Cited by 68 · see citing works
Zhang, H., Gómez-García, M. R., Brown, M. R., & Kornberg, A. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0500023102 · Cited by 68 · see citing works
Pan, Y., Lin, T., Hsu, C., & Wang, J. (2010) · Infection and Immunity · doi:10.1128/iai.00906-10 · Cited by 66 · see citing works
ER remodeling by the large GTPase atlastin promotes vacuolar growth of Legionella pneumophila
Steiner, B., Swart, A. L., Welin, A., Weber, S., Personnic, N., Kaech, A., Freyre, C. A. C., Ziegler, U., Klemm, R. W., & Hilbi, H. (2017) · EMBO Reports · doi:10.15252/embr.201743903 · Cited by 62 · see citing works
Evolution of the Arsenal of Legionella pneumophila Effectors To Modulate Protist Hosts
Best, A., & Kwaik, Y. A. (2018) · mBio · doi:10.1128/mbio.01313-18 · Cited by 67 · see citing works
Dey, R., Bodennec, J., Mameri, M. R., & Pernin, P. (2008) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2008.01387.x · Cited by 65 · see citing works
Genetic Models in Pathogenesis
Pradel, E., & Ewbank, J. J. (2004) · Annual Review of Genetics · doi:10.1146/annurev.genet.38.072902.092528 · Cited by 64 · see citing works
Asrat, S., Dugan, A. S., & Isberg, R. R. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004229 · Cited by 63 · see citing works
Self-citationRao, C., Benhabib, H., & Ensminger, A. W. (2013) · PLoS ONE · doi:10.1371/journal.pone.0064129 · Cited by 63 · see citing works
Jules, M., & Buchrieser, C. (2007) · FEBS Letters · doi:10.1016/j.febslet.2007.05.026 · Cited by 63 · see citing works
Price, C. T. D., Khodor, S. A., Al‐Quadan, T., & Kwaik, Y. A. (2010) · Infection and Immunity · doi:10.1128/iai.01450-09 · Cited by 63 · see citing works
Tyson, J. Y., Pearce, M. M., Vargas, P., Bagchi, S., Mulhern, B. J., & Cianciotto, N. P. (2013) · Infection and Immunity · doi:10.1128/iai.00045-13 · Cited by 60 · see citing works
Diversity of Free-Living Environmental Bacteria and Their Interactions With a Bactivorous Amoeba
Brock, D. A., Haselkorn, T. S., Garcia, J. R., Bashir, U., Douglas, T. E., Galloway, J., Brodie, F., Queller, D. C., & Strassmann, J. E. (2018) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2018.00411 · Cited by 59 · see citing works
Rankin, S., Li, Z., & Isberg, R. R. (2002) · Infection and Immunity · doi:10.1128/iai.70.7.3637-3648.2002 · Cited by 58 · see citing works
Self-citationVanRheenen, S. M., Duménil, G., & Isberg, R. R. (2004) · Infection and Immunity · doi:10.1128/iai.72.10.5972-5982.2004 · Cited by 58 · see citing works
Self-citationLiu, L., Hao, S., Lan, R., Wang, G., Xiao, D., Sun, H., & Xu, J. (2015) · Infection and Immunity · doi:10.1128/iai.03071-14 · Cited by 56 · see citing works
Zusman, T., Feldman, M., Halperin, E., & Segal, G. (2004) · Infection and Immunity · doi:10.1128/iai.72.6.3398-3409.2004 · Cited by 55 · see citing works
Valster, R. M., Wullings, B. A., & van der Kooij, D. (2010) · Applied and Environmental Microbiology · doi:10.1128/aem.00926-10 · Cited by 54 · see citing works
- Authors
- Solomon, J. M., Rupper, A., Cardelli, J. A., & Isberg, R. R.
- Affiliations
- Tufts University (US)
- Louisiana State University (US)
- Venue
- Infection and Immunity
- Publisher
- American Society for Microbiology
- Published
- 2000-05
- Volume
- 68
- Issue
- 5
- Pages
- 2939-2947
- ISSN
- 0019-9567 (ISSN-L)
- 1098-5522
- PMC
- PMC97507
- OpenAlex
- W2104752214
- Cited by
- 215
- References
- 59
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 3 · 2023: 2 · 2022: 1 · 2021: 2 · 2020: 6 · 2019: 4 · 2018: 7 · 2017: 8 · 2016: 2 · 2015: 6 · 2014: 13 · 2013: 15 · 2012: 6
- FWCI
- 7.33
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Infection and Immunity (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Minnesota
- University of Connecticut
- Johns Hopkins University
- Medical Research Council
- National Institute of Diabetes and Digestive and Kidney Diseases (DK-39232)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Legionella and Acanthamoeba research
- Life Sciences › Immunology and Microbiology › Microbiology › Microbial infections and disease research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- Legionella pneumophila, Dictyostelium discoideum, intracellular bacterial growth, host-pathogen interaction, Dot/Icm system, rough endoplasmic reticulum, membrane vesicles, endocytic compartments, G protein beta subunit
- MeSH terms
- Animals, Culture Media, Dictyostelium, Genes, Bacterial, Intracellular Fluid, Intracellular Membranes, Lysosomes, Membrane Proteins, Legionella pneumophila
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