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The Caenorhabditis elegans Model of Legionella Infection

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Legionella

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1921))

Abstract

Caenorhabditis elegans can serve as a simple genetic host to study interactions between Legionellaceae and their hosts and to examine the contribution of specific gene products to virulence and immunity. C. elegans nematodes have several appealing attributes as a host organism; they are inexpensive, have robust genetic analysis tools, have a simple anatomy yet display a wide range of complex behaviors, and, as invertebrates, do not require animal ethics protocols. Use of C. elegans as a host model complements cell-based models, providing additional support and consistency of the experimental data obtained from multiple models. The C. elegans innate immune system functions similarly to that of the alveolar macrophage including the apoptosis [a.k.a. programmed cell death (PCD)] pathway located within the germline. The digestive tract of C. elegans is a primary interface between the innate immune system and bacterial pathogens. Thus, the C. elegans host model provides an alternative approach to investigate L. pneumophila immunopathogenesis, particularly in the view of the recent discovery of Legionella-containing vacuoles within the gonadal tissues of Legionella-colonized nematodes supporting the plausible evolutionary origin of the strategies employed by L. pneumophila to counteract macrophage cellular responses.

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References

  1. Sifri CD, Begun J, Ausubel FM (2005) The worm has turned—microbial virulence modeled in Caenorhabditis elegans. Trends Microbiol 13:119–127

    Article  CAS  PubMed  Google Scholar 

  2. Hilbi H, Weber SS, Ragaz C et al (2007) Environmental predators as models for bacterial pathogenesis. Environ Microbiol 9:563–575

    Article  CAS  PubMed  Google Scholar 

  3. Mellies JL, Lawrence-Pine ER (2010) Interkingdom signaling between pathogenic bacteria and Caenorhabditis elegans. Trends Microbiol 18:448–454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Irazoqui JE, Urbach JM, Ausubel FM (2010) Evolution of host innate defence: insights from Caenorhabditis elegans and primitive invertebrates. Nat Rev Immunol 10:47–58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71–94

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Hope IA (ed) (1999) C. elegans: a practical approach. Oxford University Press, Oxford

    Google Scholar 

  7. Millet AC, Ewbank JJ (2004) Immunity in Caenorhabditis elegans. Curr Opin Immunol 16:4–9

    Article  CAS  PubMed  Google Scholar 

  8. Nicholas HR, Hodgkin J (2004) Responses to infection and possible recognition strategies in the innate immune system of Caenorhabditis elegans. Mol Immunol 41:479–493

    Article  CAS  PubMed  Google Scholar 

  9. Pujol N, Link EM, Liu LX et al (2001) A reverse genetic analysis of components of the Toll signaling pathway in Caenorhabditis elegans. Curr Biol 11:809–821

    Article  CAS  PubMed  Google Scholar 

  10. Troemel ER, Chu SW, Reinke V et al (2006) p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genet 2:e183. https://doi.org/10.1371/journal.pgen.0020183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Schulenburg H, Ewbank JJ (2007) The genetics of pathogen avoidance in Caenorhabditis elegans. Mol Microbiol 66:563–570

    Article  CAS  PubMed  Google Scholar 

  12. Pradel E, Zhang Y, Pujol N et al (2007) Detection and avoidance of a natural product from the pathogenic bacterium Serratia marcescens by Caenorhabditis elegans. Proc Natl Acad Sci U S A 104:2295–2300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Tenor JL, Aballay A (2008) A conserved Toll-like receptor is required for Caenorhabditis elegans innate immunity. EMBO Rep 9:103–109

    Article  CAS  PubMed  Google Scholar 

  14. Kim DH, Feinbaum R, Alloing G et al (2002) A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 297:623–626

    Article  CAS  PubMed  Google Scholar 

  15. Garsin DA, Villanueva JM, Begun J et al (2003) Long-lived C. elegans daf-2 mutants are resistant to bacterial pathogens. Science 300:1921

    Article  CAS  PubMed  Google Scholar 

  16. Aballay A, Yorgey P, Ausubel FM (2000) Salmonella typhimurium proliferates and establishes a persistent infection in the intestine of Caenorhabditis elegans. Curr Biol 10:1539–1542

    Article  CAS  PubMed  Google Scholar 

  17. Kinchen JM, Hengartner MO (2005) Tales of cannibalism, suicide, and murder: Programmed cell death in C. elegans. Curr Top Dev Biol 65:1–45

    CAS  PubMed  Google Scholar 

  18. Mizuno T, Hisamoto N, Terada T et al (2004) The Caenorhabditis elegans MAPK phosphatase VHP-1 mediates a novel JNK-like signaling pathway in stress response. EMBO J 23:2226–2234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Darby C (2005) Interactions with microbial pathogens. In: WormBook (ed) The C. elegans research community, WormBook, https://doi.org/10.1895/wormbook.1.21.1., http://www.wormbook.org

  20. Caffrey DR, O’Neill LA, Shields DC (1999) The evolution of the MAP kinase pathways: coduplication of interacting proteins leads to new signaling cascades. J Mol Evol 49:567–582

    Article  CAS  PubMed  Google Scholar 

  21. Plowman GD, Sudarsanam S, Bingham J et al (1999) The protein kinases of Caenorhabditis elegans: a model for signal transduction in the multicellular organisms. Proc Natl Acad Sci U S A 96:13603–13610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Kim DH, Liberati NT, Mizuno T et al (2004) Integration of Caenorhabditis elegans MAPK pathways mediating immunity and stress resistance by MEK-1 MAPK kinase and VHP-1 MAPK phosphatase. Proc Natl Acad Sci U S A 101:10990–10994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Brassinga AKC, Kinchen JM, Cupp ME et al (2010) Caenorhabditis is a metazoan host for Legionella. Cell Microbiol 12:343–361

    Article  CAS  PubMed  Google Scholar 

  24. Welsh CT, Summersgill JT, Miller RD (2004) Increases in c-Jun N-Terminal kinase/stress-activated protein kinase and p38 activity in monocyte-derived macrophages following the uptake of Legionella pneumophila. Infect Immun 72:1512–1518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Abu-Zant A, Santic M, Molmeret M et al (2005) Incomplete activation of macrophage apoptosis during intracellular replication of Legionella pneumophila. Infect Immun 73:5339–5349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Alper S, Laws R, Lackford B et al (2008) Identification of innate immunity genes and pathways using a comparative genomics approach. Mol Cell Biol 27:5544–5553

    Article  Google Scholar 

  27. Hellinga JR, Garduño RA, Kormish JD, Tanner JR, Khan D, Buchko K, Jimenez C, Pinette MM, Brassinga AKC (2015) Identification of vacuoles containing extraintestinal differentiated forms of Legionella pneumophila in colonized Caenorhabditis elegans soil nematodes. Microbiologyopen 4:660–681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Abnave P, Mottola G, Gimenez G, Boucherit N, Trouplin V, Torre C, Conti F, Amara AB, Lepolard C, Djian B, Hamaoui D, Mettouchi A, Kumar A, Pagnotta S, Bonatti S, Lepidi H, Salvetti A, Abi-Rached L, Lemichez E, Mege J-L, Ghigo E (2014) Screening in planarians identifies MORN2 as a key component in LC3-associated phagocytosis and resistance to bacterial infection. Cell Host Microbe 16:338–350

    Article  CAS  PubMed  Google Scholar 

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Acknowledgment

We thank Mathieu Pinette, Jacqueline Hellinga, Alexander Diamandas, and Dr. Jay Kormish for their contributions. This work was supported by a Howard Hughes Medical Institute Early Career Award to C.D.S., and a National Science and Engineering Council Discovery Grant, a Canadian Foundation for Innovation, a Manitoba Medical Service Foundation Award and a Manitoba Health Research Council Establishment Grant to A.K.C.B.

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Authors and Affiliations

  1. Department of Microbiology, University of Manitoba, Winnipeg, MB, Canada

    Ann Karen C. Brassinga

  2. Division of Infectious Diseases and International Health, Department of Medicine, University of Virginia Health System, Charlottesville, VA, USA

    Costi D. Sifri

Authors
  1. Ann Karen C. Brassinga
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  2. Costi D. Sifri
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Corresponding author

Correspondence to Ann Karen C. Brassinga .

Editor information

Editors and Affiliations

  1. Institut Pasteur, Biologie des Bactéries Intracellulaires, Paris, France

    Carmen Buchrieser

  2. Institute of Medical Microbiology, University of Zürich, Zürich, Switzerland

    Hubert Hilbi

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Brassinga, A.K.C., Sifri, C.D. (2019). The Caenorhabditis elegans Model of Legionella Infection. In: Buchrieser, C., Hilbi, H. (eds) Legionella. Methods in Molecular Biology, vol 1921. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-9048-1_24

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  • DOI: https://doi.org/10.1007/978-1-4939-9048-1_24

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  • Publisher Name: Humana Press, New York, NY

  • Print ISBN: 978-1-4939-9047-4

  • Online ISBN: 978-1-4939-9048-1

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