Dictyostelium discoideum: a new host model system for intracellular pathogens of the genus Legionella
Abstract
The soil amoeba Dictyostelium discoideum is a haploid eukaryote that, upon starvation, aggregates and enters a developmental cycle to produce fruiting bodies. In this study, we infected single-cell stages of D. discoideum with different Legionella species. Intracellular growth of Legionella in this new host system was compared with their growth in the natural host Acanthamoeba castellanii. Transmission electron microscopy of infected D. discoideum cells revealed that legionellae reside within the phagosome. Using confocal microscopy, it was observed that replicating, intracellular, green fluorescent protein (GFP)-tagged legionellae rarely co-localized with fluorescent antibodies directed against the lysosomal protein DdLIMP of D. discoideum. This indicates that the bacteria inhibit the fusion of phagosomes and lysosomes in this particular host system. In addition, Legionella infection of D. discoideum inhibited the differentiation of the host into the multicellular fruiting stage. Co-culture studies with profilin-minus D. discoideum mutants and Legionella resulted in higher rates of infection when compared with infections of wild-type amoebae. Because the amoebae are amenable to genetic manipulation as a result of their haploid genome and because a number of cellular markers are available, we show for the first time that D. discoideum is a valuable model system for studying intracellular pathogenesis of microbial pathogens.
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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 [11]
Cites
Molecular Cloning: A Laboratory Manual
Sambrook, J., Fritsch, E., & Maniatis, T. (1989) · UCLA - Biblioteca de Ciencias de la Salud · Cited by 133,589 · see citing works
Molecular cloning: A laboratory manual
Deininger, P. L. (1990) · Analytical Biochemistry · doi:10.1016/0003-2697(90)90595-z · Cited by 84,684 · see citing works
Studies on transformation of Escherichia coli with plasmids
Hanahan, D. (1983) · Journal of Molecular Biology · doi:10.1016/s0022-2836(83)80284-8 · Cited by 11,274 · 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
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
Segal, 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
Steinert, M., Emödy, L., Amann, R., & Hacker, J. (1997) · Applied and Environmental Microbiology · doi:10.1128/aem.63.5.2047-2053.1997 · Cited by 371 · 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
Invasion of Protozoa by Legionella pneumophila and Its Role in Bacterial Ecology and Pathogenesis
Kwaik, Y. A., Gao, L., Stone, B. J., Venkataraman, C., & Harb, O. S. (1998) · Applied and Environmental Microbiology · doi:10.1128/aem.64.9.3127-3133.1998 · Cited by 251 · 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
Haugwitz, M. (1994) · Cell · doi:10.1016/0092-8674(94)90199-6 · Cited by 231 · see citing works
Bozue, J. A., & Johnson, W. (1996) · Infection and Immunity · doi:10.1128/iai.64.2.668-673.1996 · Cited by 212 · see citing works
Legionella-Like Amebal Pathogens––Phylogenetic Status and Possible Role in Respiratory Disease
Adeleke, A., Pruckler, J. M., Benson, R. F., Rowbotham, T. J., Halablab, M., & Fields, B. S. (1996) · Emerging infectious diseases · doi:10.3201/eid0203.960311 · Cited by 125 · see citing works
Wintermeyer, E., Ludwig, B., Steinert, M., Schmidt, B., Fischer, G. S., & Hacker, J. H. (1995) · Infection and Immunity · doi:10.1128/iai.63.12.4576-4583.1995 · Cited by 121 · see citing works
Self-citationDose-Response of Guinea Pigs Experimentally Infected with Aerosols of Legionella pneumophila
Berendt, R. F., Young, H. W., Allen, R. G., & Knutsen, G. L. (1980) · The Journal of Infectious Diseases · doi:10.1093/infdis/141.2.186 · Cited by 109 · see citing works
Fields, B. S., Barbaree, J. M., Sanden, G. N., & Morrill, W. E. (1990) · Infection and Immunity · doi:10.1128/iai.58.9.3139-3142.1990 · Cited by 94 · see citing works
Gao, L., Harb, O. S., & Kwaik, Y. A. (1998) · Infection and Immunity · doi:10.1128/iai.66.3.883-892.1998 · Cited by 90 · see citing works
Hickey, E. K., & Cianciotto, N. P. (1997) · Infection and Immunity · doi:10.1128/iai.65.1.133-143.1997 · Cited by 85 · see citing works
Fatal attraction of mammalian cells to Legionella pneumophila
Kwaik, Y. A. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.01092.x · Cited by 85 · see citing works
Legionella oakridgensis: unusual new species isolated from cooling tower water
Orrison, L. H., Cherry, W. B., Tyndall, R. L., FLIERMANS, C. B., Gough, S. B., Lambert, M. A., McDougal, L. K., Bibb, W. F., & Brenner, D. J. (1983) · Applied and Environmental Microbiology · doi:10.1128/aem.45.2.536-545.1983 · Cited by 81 · see citing works
Dictyostelium discoideumcontains two profilin isoforms that differ in structure and fuction
Haugwitz, M., Noegel, A. A., Rieger, D., Lottspeich, F., & Schleicher, M. (1991) · Journal of Cell Science · doi:10.1242/jcs.100.3.481 · Cited by 72 · see citing works
Self-citationKwaik, Y. A., Fields, B. S., & Engleberg, N. C. (1994) · Infection and Immunity · doi:10.1128/iai.62.5.1860-1866.1994 · Cited by 71 · see citing works
Beckers, M. C., Yoshida, S.-I., Morgan, K., Skamene, E., & Gros, P. (1995) · Mammalian Genome · doi:10.1007/bf00356173 · Cited by 68 · see citing works
Grimm, D., Merkert, H., Ludwig, W., SCHLEIFER, K. H., Hacker, J. H., & Brand, B. C. (1998) · Applied and Environmental Microbiology · doi:10.1128/aem.64.7.2686-2690.1998 · Cited by 65 · see citing works
Self-citationNoegel, A. A., & Luna, J. E. (1995) · Cellular and Molecular Life Sciences · doi:10.1007/bf01944731 · Cited by 58 · see citing works
Hägele, S., Hacker, J., & Brand, B. C. (1998) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1998.tb13298.x · Cited by 53 · see citing works
Self-citationExpression and use of the green fluorescent protein as a reporter system in Legionella pneumophila
Köhler, R., Bubert, A., Goebel, W., Steinert, M., Hacker, J., & Bubert, B. (2000) · Molecular and General Genetics MGG · doi:10.1007/pl00008649 · Cited by 51 · see citing works
Self-citationComparative Analysis of Legionella pneumophila and Legionella micdadei Virulence Traits
Joshi, A., & Swanson, M. S. (1999) · Infection and Immunity · doi:10.1128/iai.67.8.4134-4142.1999 · Cited by 49 · see citing works
How the Listeria monocytogenes ActA protein converts actin polymerization into a motile force
Smith, G. A., & Portnoy, D. A. (1997) · Trends in Microbiology · doi:10.1016/s0966-842x(97)01048-2 · Cited by 49 · see citing works
Karakesisoglou, I., Janssen, K., Eichinger, L., Noegel, A. A., & Schleicher, M. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.145.1.167 · Cited by 47 · see citing works
Self-citationGenetic structure of a natural population of Dictyostelium discoideum, a cellular slime mould
FRANCIS, D., & Eisenberg, R. M. (1993) · Molecular Ecology · doi:10.1111/j.1365-294x.1993.tb00031.x · Cited by 41 · see citing works
Steele, T. W., & McLennan, A. M. (1996) · Applied and Environmental Microbiology · doi:10.1128/aem.62.3.1081-1083.1996 · Cited by 41 · see citing works
Kwaik, Y. A., Venkataraman, C., Harb, O. S., & Gao, L.-Y. (1998) · Applied and Environmental Microbiology · doi:10.1128/aem.64.9.3134-3139.1998 · Cited by 38 · see citing works
A second serogroup of Legionella erythra serologically indistinguishable from Legionella rubrilucens
Saunders, N. A., Doshi, N., & Harrison, T. G. (1992) · Journal of Applied Bacteriology · doi:10.1111/j.1365-2672.1992.tb01833.x · Cited by 14 · see citing works
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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
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
The 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
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
Self-citationWeber, 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
The role of biofilms and protozoa inLegionellapathogenesis: implications for drinking water
Lau, H. Y., & Ashbolt, N. J. (2009) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2009.04208.x · Cited by 285 · 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
Common molecular mechanisms of symbiosis and pathogenesis
Hentschel, U., Steinert, M., & Hacker, J. H. (2000) · Trends in Microbiology · doi:10.1016/s0966-842x(00)01758-3 · Cited by 250 · see citing works
Self-citationThe 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
A star with stripes: zebrafish as an infection model
van der Sar, A. M., Appelmelk, B. J., Vandenbroucke‐Grauls, C. M. J. E., & Bitter, W. (2004) · Trends in Microbiology · doi:10.1016/j.tim.2004.08.001 · Cited by 216 · see citing works
From 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
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
Galka, F., Wai, S. N., Kusch, H., Engelmann, S., Hecker, M., Schmeck, B., Hippenstiel, S., Uhlin, B. E., & Steinert, M. (2008) · Infection and Immunity · doi:10.1128/iai.01396-07 · Cited by 192 · see citing works
Self-citationTiaden, 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
Legionella, Protozoa, and Biofilms: Interactions Within Complex Microbial Systems
Taylor, M., Ross, K., & Bentham, R. (2009) · Microbial Ecology · doi:10.1007/s00248-009-9514-z · Cited by 170 · see citing works
Balczun, C., & Scheid, P. L. (2017) · Viruses · doi:10.3390/v9040065 · Cited by 170 · see citing works
Urwyler, S., Nyfeler, Y., Ragaz, C., Lee, H., Mueller, L. N., Aebersold, R. H., & Hilbi, H. (2008) · Traffic · doi:10.1111/j.1600-0854.2008.00851.x · Cited by 168 · see citing works
Dictyostelium discoideum—a model for many reasons
Annesley, S. J., & Fisher, P. R. (2009) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-009-0111-8 · Cited by 160 · 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
Self-citationNovoa, B., Romero, A., Mulero, V., Rodríguez-Nunez, I., Fernández, I., & Figueras, A. J. (2006) · Vaccine · doi:10.1016/j.vaccine.2006.05.015 · Cited by 141 · 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
Aubert, D., Flannagan, R. S., & Valvano, M. A. (2008) · Infection and Immunity · doi:10.1128/iai.01338-07 · Cited by 132 · see citing works
Cellular microbiology and molecular ecology ofLegionella–amoeba interaction
Richards, A. M., Dwingelo, J. E. V., Price, C. T. D., & Kwaik, Y. A. (2013) · Virulence · doi:10.4161/viru.24290 · Cited by 129 · 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
Kuiper, M. W., Wullings, B. A., Akkermans, A. D. L., Beumer, R. R., & van der Kooij, D. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.11.6826-6833.2004 · Cited by 126 · 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
Yang, C., Wang, Q., Simon, P. N., Liu, J., Liu, L., Dai, X., Zhang, X., Kuang, J., Igarashi, Y., Pan, X., et al. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01202 · Cited by 124 · 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
Towards a molecular understanding of human diseases using Dictyostelium discoideum
Williams, R. S. B., Boeckeler, K., Gräf, R., Müller‐Taubenberger, A., Li, Z., Isberg, R. R., Wessels, D. J., Soll, D. R., Alexander, H., & Alexander, S. (2006) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2006.07.003 · Cited by 123 · see citing works
Gómez-Valero, L., Rusniok, C., Rolando, M., Néou, M., Ravault, D., Demirtas, J., Rouy, Z., Moore, R. J., Chen, H., Petty, N. K., et al. (2014) · Genome biology · doi:10.1186/preaccept-1086350395137407 · Cited by 123 · see citing works
Self-citationThe 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
Dynamic 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
The natural alternative: protozoa as cellular models forLegionellainfection
Hoffmann, C., Harrison, C. F., & Hilbi, H. (2013) · Cellular Microbiology · doi:10.1111/cmi.12235 · Cited by 114 · see citing works
Dictyostelium 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
Self-citationSolomon, J. M., & Isberg, R. R. (2000) · Trends in Microbiology · doi:10.1016/s0966-842x(00)01852-7 · Cited by 112 · see citing works
Relevance of free-living amoebae as hosts for phylogenetically diverse microorganisms
Scheid, P. L. (2014) · Parasitology Research · doi:10.1007/s00436-014-3932-7 · Cited by 111 · see citing works
Factors Mediating Environmental Biofilm Formation by Legionella pneumophila
Khweek, A. A., & Amer, A. O. (2018) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2018.00038 · Cited by 111 · 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
Self-citationThe 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
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
Self-citationLegionella pathogenicity: Genome structure, regulatory networks and the host cell response
Steinert, M., Heuner, K., Buchrieser, C., Albert-Weißenberger, C., & Glöckner, G. (2007) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2007.03.009 · Cited by 105 · see citing works
Self-citationTung, S. M., Ünal, C., Ley, A., Peña, C., Tunggal, B., Noegel, A. A., Krut, O., Steinert, M., & Eichinger, L. (2010) · Cellular Microbiology · doi:10.1111/j.1462-5822.2010.01432.x · Cited by 104 · see citing works
Self-citationErken, M., Lutz, C., & McDougald, D. (2013) · Microbial Ecology · doi:10.1007/s00248-013-0189-0 · Cited by 102 · see citing works
New models for the study of Mycobacterium–host interactions
Pozos, T. C., & Ramakrishnan, L. (2004) · Current Opinion in Immunology · doi:10.1016/j.coi.2004.05.011 · Cited by 100 · 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
Self-citationSimple 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
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
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
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
Self-citationEvolution of the Zebrafish Model: From Development to Immunity and Infectious Disease
Phelps, H. A., & Neely, M. N. (2005) · Zebrafish · doi:10.1089/zeb.2005.2.87 · Cited by 86 · see citing works
Pathogenicity and virulence of Bordetella pertussis and its adaptation to its strictly human host
Belcher, T., Dubois, V., Rivera-Millot, A., Locht, C., & Jacob‐Dubuisson, F. (2021) · Virulence · doi:10.1080/21505594.2021.1980987 · Cited by 83 · see citing works
Denoncourt, A. M., Paquet, V. E., & Charette, S. J. (2014) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00240 · Cited by 83 · see citing works
Feichtmayer, J., Deng, L., & Griebler, C. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.02192 · Cited by 80 · see citing works
Intracellular survival strategies of mutualistic and parasitic prokaryotes
Goebel, W., & Gross, R. (2001) · Trends in Microbiology · doi:10.1016/s0966-842x(01)02040-6 · Cited by 76 · see citing works
Human Lung Tissue Explants Reveal Novel Interactions during Legionella pneumophila Infections
Jäger, J., Marwitz, S., Tiefenau, J. H. J., Rasch, J., Shevchuk, O., Kügler, C., Goldmann, T., & Steinert, M. (2013) · Infection and Immunity · doi:10.1128/iai.00703-13 · Cited by 73 · see citing works
Self-citationFajardo, 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
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
Heuner, K., Dietrich, C., Skriwan, C., Steinert, M., & Hacker, J. H. (2002) · Infection and Immunity · doi:10.1128/iai.70.3.1604-1608.2002 · Cited by 71 · see citing works
Self-citationHarris, E. N., & Cardelli, J. A. (2002) · Journal of Cell Science · doi:10.1242/jcs.00050 · Cited by 70 · 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
Ramarao, N., & Meyer, T. F. (2001) · Infection and Immunity · doi:10.1128/iai.69.4.2604-2611.2001 · Cited by 68 · 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
Jules, M., & Buchrieser, C. (2007) · FEBS Letters · doi:10.1016/j.febslet.2007.05.026 · 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
Ancient bacteria–amoeba relationships and pathogenic animal bacteria
Strassmann, J. E., & Shu, L. (2017) · PLoS Biology · doi:10.1371/journal.pbio.2002460 · Cited by 60 · see citing works
Deficiency of Huntingtin Has Pleiotropic Effects in the Social Amoeba Dictyostelium discoideum
Myre, M. A., Lumsden, A. L., Thompson, M. N., Wasco, W., MacDonald, M. E., & Gusella, J. F. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002052 · Cited by 57 · see citing works
Peracino, B., Balest, A., & Bozzaro, S. (2010) · Journal of Cell Science · doi:10.1242/jcs.072124 · Cited by 56 · 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
Conserved features of endocytosis in Dictyostelium
Maniak, M. (2002) · International Review of Cytology · doi:10.1016/s0074-7696(02)21014-1 · Cited by 52 · see citing works
Robertson, P., Abdelhady, H., & Garduño, R. A. (2014) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00670 · Cited by 51 · see citing works
Saxer, G., Havlak, P., Fox, S. A., Quance, M. A., Gupta, S., Fofanov, Y., Strassmann, J. E., & Queller, D. C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0046759 · Cited by 51 · see citing works
Shadrach, W. S., Rydzewski, K., Laube, U., Holland, G., Özel, M., Kiderlen, A. F., & Flieger, A. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.5.2244-2249.2005 · Cited by 50 · see citing works
Peracino, B., Buracco, S., & Bozzaro, S. (2012) · Journal of Cell Science · doi:10.1242/jcs.116210 · Cited by 50 · see citing works
Francione, L. M., Smith, P. K., Accari, S. L., Taylor, P. E., Bokko, P. B., Bozzaro, S., Beech, P. L., & Fisher, P. R. (2009) · Disease Models & Mechanisms · doi:10.1242/dmm.003319 · Cited by 50 · see citing works
Albers, U., Reus, K., Shuman, H. A., & Hilbi, H. (2005) · Microbiology · doi:10.1099/mic.0.27563-0 · Cited by 50 · see citing works
Amoebae and Legionella pneumophila in saline environments
Gast, R. J., Moran, D. M., Dennett, M. R., Wurtsbaugh, W. A., & Amaral‐Zettler, L. (2011) · Journal of Water and Health · doi:10.2166/wh.2010.103 · Cited by 48 · see citing works
Taylor, D. L., Bendor, L., Linz, B., Rivera, I., Ryman, V. E., Dewan, K. K., Wagner, S. M., Wilson, E. F., Hilburger, L. J., Cuff, L. E., et al. (2017) · PLoS Biology · doi:10.1371/journal.pbio.2000420 · Cited by 47 · see citing works
Yan, L., Cerny, R. L., & Cirillo, J. D. (2004) · Eukaryotic Cell · doi:10.1128/ec.3.3.567-578.2004 · Cited by 45 · see citing works
Free-Living Amoebae as Human Parasites and Hosts for Pathogenic Microorganisms
Scheid, P. L. (2018) · International Conference on Efficient & Sustainable Water Systems Management toward Worth Living Development (EWaS) · doi:10.3390/proceedings2110692 · Cited by 45 · see citing works
Recent insights into host-pathogen interactions fromDictyostelium
Clarke, M. (2009) · Cellular Microbiology · doi:10.1111/j.1462-5822.2009.01413.x · Cited by 44 · see citing works
Hasselbring, B. M., Patel, M. K., & Schell, M. A. (2011) · Infection and Immunity · doi:10.1128/iai.01233-10 · Cited by 42 · see citing works
Cross-Species Infections and Their Analysis
Tan, M. (2002) · Annual Review of Microbiology · doi:10.1146/annurev.micro.56.012302.161110 · Cited by 42 · see citing works
Dictyostelium discoideum as a non‐mammalian biomedical model
Martín‐González, J., Montero‐Bullón, J., & Lacal, J. (2020) · Microbial Biotechnology · doi:10.1111/1751-7915.13692 · Cited by 41 · see citing works
Goy, G., Thomas, V., Herrera-Rimann, K., Jaton, K., Prod’hom, G., & Greub, G. (2007) · Research in Microbiology · doi:10.1016/j.resmic.2007.01.003 · Cited by 40 · see citing works
Manifestations of multicellularity: Dictyostelium reports in
Williams, J. G., Noegel, A. A., & Eichinger, L. (2005) · Trends in Genetics · doi:10.1016/j.tig.2005.05.002 · Cited by 39 · see citing works
Amaro, F., & Martín‐González, A. (2021) · International Microbiology · doi:10.1007/s10123-021-00192-y · Cited by 38 · see citing works
The Amoebal MAP Kinase Response to Legionella pneumophila Is Regulated by DupA
Li, Z., Dugan, A. S., Bloomfield, G., Skelton, J., Ivens, A. C., Losick, V. P., & Isberg, R. R. (2009) · Cell Host & Microbe · doi:10.1016/j.chom.2009.08.005 · Cited by 38 · see citing works
Setting Up and Monitoring an Infection of Dictyostelium discoideum with Mycobacteria
Arafah, S., Kicka, S., Trofimov, V., Hagedorn, M., Andreu, N., Wiles, S., Robertson, B. D., & Soldati, T. (2013) · Methods in molecular biology · doi:10.1007/978-1-62703-302-2_22 · Cited by 37 · see citing works
Surrogate hosts: protozoa and invertebrates as models for studying pathogen-host interactions
Steinert, M., Leippe, M., & Roeder, T. (2003) · International Journal of Medical Microbiology · doi:10.1078/1438-4221-00275 · Cited by 37 · see citing works
Self-citationIntra-Amoeba Multiplication Induces Chemotaxis and Biofilm Colonization and Formation for Legionella
Bigot, R., Bertaux, J., Frère, J., & Berjeaud, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077875 · Cited by 36 · see citing works
Rashidi, G., & Ostrowski, E. A. (2019) · Biology Letters · doi:10.1098/rsbl.2018.0607 · Cited by 36 · see citing works
Salmonella typhimurium is pathogenic for Dictyostelium cells and subverts the starvation response
Sillo, A., Matthias, J., Konertz, R., Bozzaro, S., & Eichinger, L. (2011) · Cellular Microbiology · doi:10.1111/j.1462-5822.2011.01662.x · Cited by 36 · see citing works
Buracco, S., Peracino, B., Andreini, C., Bracco, E., & Bozzaro, S. (2018) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00536 · Cited by 36 · see citing works
Type II Secretion and Legionella Virulence
Cianciotto, N. P. (2013) · Current topics in microbiology and immunology · doi:10.1007/82_2013_339 · Cited by 34 · see citing works
Experimental Models of Cryptococcosis
Sabiiti, W., May, R. C., & Pursall, E. R. (2011) · International Journal of Microbiology · doi:10.1155/2012/626745 · Cited by 34 · see citing works
Riyahi, T. Y., Frese, F., Steinert, M., Omosigho, N. N., Glöckner, G., Eichinger, L., Orabi, B., Williams, R. S. B., & Noegel, A. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027311 · Cited by 32 · see citing works
Self-citationQuantitative Analysis of Phagocytosis and Phagosome Maturation
Sattler, N., Monroy, R., & Soldati, T. (2013) · Methods in molecular biology · doi:10.1007/978-1-62703-302-2_21 · Cited by 31 · see citing works
- Authors
- Hagele, S., Kohler, R., Merkert, H., Schleicher, M., Hacker, J., & Steinert, M.
- Affiliations
- University of Würzburg (DE)
- Ludwig-Maximilians-Universität München (DE)
- Corresponding author
- Steinert, Michael
- ORCID
- Steinert, Michael
- Venue
- Cellular Microbiology
- Publisher
- Hindawi Limited
- Published
- 2000-04
- Volume
- 2
- Issue
- 2
- Pages
- 165-171
- ISSN
- 1462-5814 (ISSN-L)
- 1462-5822
- OpenAlex
- W2035842134
- Cited by
- 198
- References
- 35
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 1 · 2023: 3 · 2022: 2 · 2021: 5 · 2020: 5 · 2019: 7 · 2018: 13 · 2017: 11 · 2016: 1 · 2015: 5 · 2014: 16 · 2013: 15 · 2012: 6
- FWCI
- 5.25
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cellular Microbiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Legionella and Acanthamoeba research
- Physical Sciences › Engineering › Biomedical Engineering › Slime Mold and Myxomycetes Research
- Health Sciences › Medicine › Infectious Diseases › Amoebic Infections and Treatments
- Keywords
- Dictyostelium discoideum, Legionella, intracellular pathogens, host-pathogen interaction, profilin, Acanthamoeba castellanii, intracellular bacterial growth
- MeSH terms
- Acanthamoeba, Animals, Dictyostelium, Disease Models, Animal, Flow Cytometry, Humans, Legionella, Legionellosis, In Situ Hybridization, Microscopy, Confocal
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