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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.
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“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]
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Cited by
Sorted by citations
Legionella and Legionnaires' Disease: 25 Years of Investigation
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“These bacteria have been shown to multiply in 14 species of amoebae, two species of ciliated protozoa, and one species of slime mold, while growth of legionellae in the absence of protozoa has been documented only on laboratory media (91, 123, 254).”
BackgroundThe 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
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
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
“Models for testing virulence were developed by using Dictyostelium discoideum as a host (53, 105, 197, 221, 222).”
MethodResultAmoebae 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
“analysis of host-pathogen interactions (93, 94).”
BackgroundInfluential
Metadata
- 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
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