Caenorhabditis elegans as a model for intracellular pathogen infection

Cellular Microbiology

Volumn 15, Issue 8, 2013, Pages 1313-1322

  Balla, Keir M ^a   Troemel, Emily R ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; CAENORHABDITIS ELEGANS; CELLULAR IMMUNITY; ECOLOGY; ENDOCYTOSIS; EXOCYTOSIS; HOST RESISTANCE; HUMAN; IMMUNOCOMPETENT CELL; INTESTINE EPITHELIUM CELL; MICROSPORIDIA; NODAVIRUS; NONHUMAN; PATHOGENESIS; PHAGOCYTE; PHYLUM; PRIORITY JOURNAL; REVIEW; VIRUS CELL INTERACTION;

ANIMALS; CAENORHABDITIS ELEGANS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; HOST-PATHOGEN INTERACTIONS; INTESTINES; MICROSPORIDA; MICROSPORIDIOSIS; NODAVIRIDAE; RNA VIRUS INFECTIONS;

ANIMALIA; CAENORHABDITIS ELEGANS; MICROSPORIDIA; NEMATODA; NODAVIRIDAE;

EID: 84880329381     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12152     Document Type: Review

References (58)

1. Aballay, A., Yorgey, P., and Ausubel, F.M. (2000) Salmonella typhimurium proliferates and establishes a persistent infection in the intestine of Caenorhabditis elegans. Curr Biol 10: 1539-1542.
2. Andersen, E.C., Gerke, J.P., Shapiro, J.A., Crissman, J.R., Ghosh, R., Bloom, J.S., etal. (2012) Chromosome-scale selective sweeps shape Caenorhabditis elegans genomic diversity. Nat Genet 44: 285-290.
3. Brenner, S. (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
4. Burton, E.A., Pendergast, A.M., and Aballay, A. (2006) The Caenorhabditis elegans ABL-1 tyrosine kinase is required for Shigella flexneri pathogenesis. Appl Environ Microbiol 72: 5043-5051.
5. Casadevall, A. (2008) Evolution of intracellular pathogens. Annu Rev Microbiol 62: 19-33.
6. Chisholm, A.D., and Hardin, J. (2005) Epidermal morphogenesis. WormBook 1 December: 1-22.
7. Chiu, I.M., von Hehn, C.A., and Woolf, C.J. (2012) Neurogenic inflammation and the peripheral nervous system in host defense and immunopathology. Nat Neurosci 15: 1063-1067.
8. Cuomo, C.A., Desjardins, C.A., Bakowski, M.A., Goldberg, J., Ma, A.T., Becnel, J.J., etal. (2012) Microsporidian genome analysis reveals evolutionary strategies for obligate intracellular growth. Genome Res 22: 2478-2488.
9. Didier, E.S., and Weiss, L.M. (2011) Microsporidiosis: not just in AIDS patients. Curr Opin Infect Dis 24: 490-495.
10. Ding, S.W. (2010) RNA-based antiviral immunity. Nat Rev Immunol 10: 632-644.
11. Dunbar, T.L., Yan, Z., Balla, K.M., Smelkinson, M.G., and Troemel, E.R. (2012) C.elegans detects pathogen-induced translational inhibition to activate immune signaling. Cell Host Microbe 11: 375-386.
12. Elde, N.C., and Malik, H.S. (2009) The evolutionary conundrum of pathogen mimicry. Nat Rev Microbiol 7: 787-797.
13. Estes, K.A., Szumowski, S.C., and Troemel, E.R. (2011) Non-lytic, actin-based exit of intracellular parasites from C.elegans intestinal cells. PLoS Pathog 7: e1002227.
14. Félix, M.A., and Braendle, C. (2010) The natural history of Caenorhabditis elegans. Curr Biol 20: R965-R969.
15. Félix, M.A., and Duveau, F. (2012) Population dynamics and habitat sharing of natural populations of Caenorhabditis elegans and C.briggsae. BMC Biol 10: 59.
16. Félix, M.A., Ashe, A., Piffaretti, J., Wu, G., Nuez, I., Belicard, T., etal. (2011) Natural and experimental infection of Caenorhabditis nematodes by novel viruses related to nodaviruses. PLoS Biol 9: e1000586.
17. Fire, A., Xu, S., Montgomery, M.K., Kostas, S.A., Driver, S.E., and Mello, C.C. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806-811.
18. Forrester, S., Milillo, S.R., Hoose, W.A., Wiedmann, M., and Schwab, U. (2007) Evaluation of the pathogenicity of Listeria spp. in Caenorhabditis elegans. Foodborne Pathog Dis 4: 67-73.
19. Franz, C.J., Zhao, G., Félix, M.A., and Wang, D. (2012) Complete genome sequence of Le Blanc virus, a third Caenorhabditis nematode-infecting virus. J Virol 86: 11940.
20. Gallo, R.L., and Hooper, L.V. (2012) Epithelial antimicrobial defence of the skin and intestine. Nat Rev Immunol 12: 503-516.
21. Guha, S., Klees, M., Wang, X., Li, J., Dong, Y., and Cao, M. (2013) Influence of planktonic and sessile Listeria monocytogenes on Caenorhabditis elegans. Arch Microbiol 195: 19-26.
22. Irazoqui, J.E., Urbach, J.M., and Ausubel, F.M. (2010a) Evolution of host innate defence: insights from Caenorhabditis elegans and primitive invertebrates. Nat Rev 10: 47-58.
23. Irazoqui, J.E., Troemel, E.R., Feinbaum, R.L., Luhachack, L.G., Cezairliyan, B.O., and Ausubel, F.M. (2010b) Distinct pathogenesis and host responses during infection of C.elegans by P.aeruginosa and S.aureus. PLoS Pathog 6: e1000982.
24. Jia, K., Thomas, C., Akbar, M., Sun, Q., Adams-Huet, B., Gilpin, C., and Levine, B. (2009) Autophagy genes protect against Salmonella typhimurium infection and mediate insulin signaling-regulated pathogen resistance. Proc Natl Acad Sci USA 106: 14564-14569.
25. Katinka, M.D., Duprat, S., Cornillot, E., Metenier, G., Thomarat, F., Prensier, G., etal. (2001) Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414: 450-453.
26. Keeling, P.J., and Corradi, N. (2011) Shrink it or lose it: balancing loss of function with shrinking genomes in the microsporidia. Virulence 2: 67-70.
27. Kesika, P., and Balamurugan, K. (2012) Studies on Shigella boydii infection in Caenorhabditis elegans and bioinformatics analysis of immune regulatory protein interactions. Biochim Biophys Acta 1824: 1449-1456.
28. Labrousse, A., Chauvet, S., Couillault, C., Kurz, C.L., and Ewbank, J.J. (2000) Caenorhabditis elegans is a model host for Salmonella typhimurium. Curr Biol 10: 1543-1545.
29. Liu, W.H., Lin, Y.L., Wang, J.P., Liou, W., Hou, R.F., Wu, Y.C., and Liao, C.L. (2006) Restriction of vaccinia virus replication by a ced-3 and ced-4-dependent pathway in Caenorhabditis elegans. Proc Natl Acad Sci USA 103: 4174-4179.
30. Lu, R., Maduro, M., Li, F., Li, H.W., Broitman-Maduro, G., Li, W.X., and Ding, S.W. (2005) Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans. Nature 436: 1040-1043.
31. Lu, R., Yigit, E., Li, W.X., and Ding, S.W. (2009) An RIG-I-Like RNA helicase mediates antiviral RNAi downstream of viral siRNA biogenesis in Caenorhabditis elegans. PLoS Pathog 5: e1000286.
32. McEwan, D.L., Kirienko, N.V., and Ausubel, F.M. (2012) Host translational inhibition by Pseudomonas aeruginosa Exotoxin A Triggers an immune response in Caenorhabditis elegans. Cell Host Microbe 11: 364-374.
33. McGhee, J.D. (2007) The C.elegans intestine. WormBook 27 March: 1-36.
34. Marx, J. (2002) Nobel prize in physiology or medicine. Tiny worm takes a star turn. Science 298: 526.
35. Morran, L.T., Schmidt, O.G., Gelarden, I.A., Parrish, R.C., 2nd, and Lively, C.M. (2011) Running with the Red Queen: host-parasite coevolution selects for biparental sex. Science 333: 216-218.
36. Mylonakis, E., Ausubel, F.M., Perfect, J.R., Heitman, J., and Calderwood, S.B. (2002) Killing of Caenorhabditis elegans by Cryptococcus neoformans as a model of yeast pathogenesis. Proc Natl Acad Sci USA 99: 15675-15680.
37. Nikitas, G., Deschamps, C., Disson, O., Niault, T., Cossart, P., and Lecuit, M. (2011) Transcytosis of Listeria monocytogenes across the intestinal barrier upon specific targeting of goblet cell accessible E-cadherin. J Exp Med 208: 2263-2277.
38. Pentecost, M., Otto, G., Theriot, J.A., and Amieva, M.R. (2006) Listeria monocytogenes invades the epithelial junctions at sites of cell extrusion. PLoS Pathog 2: e3.
39. Pujol, N., Link, E.M., Liu, L.X., Kurz, C.L., Alloing, G., Tan, M.W., etal. (2001) A reverse genetic analysis of components of the Toll signaling pathway in Caenorhabditis elegans. Curr Biol 11: 809-821.
40. Pukkila-Worley, R., and Ausubel, F.M. (2012) Immune defense mechanisms in the Caenorhabditis elegans intestinal epithelium. Curr Opin Immunol 24: 3-9.
41. Rechavi, O., Minevich, G., and Hobert, O. (2011) Transgenerational inheritance of an acquired small RNA-based antiviral response in C.elegans. Cell 147: 1248-1256.
42. Schott, D.H., Cureton, D.K., Whelan, S.P., and Hunter, C.P. (2005) An antiviral role for the RNA interference machinery in Caenorhabditis elegans. Proc Natl Acad Sci USA 102: 18420-18424.
43. Shivers, R.P., Youngman, M.J., and Kim, D.H. (2008) Transcriptional responses to pathogens in Caenorhabditis elegans. Curr Opin Microbiol 11: 251-256.
44. Shu, X., Lev-Ram, V., Deerinck, T.J., Qi, Y., Ramko, E.B., Davidson, M.W., etal. (2011) A genetically encoded tag for correlated light and electron microscopy of intact cells, tissues, and organisms. PLoS Biol 9: e1001041.
45. Sifri, C.D., Begun, J., and Ausubel, F.M. (2005) The worm has turned - microbial virulence modeled in Caenorhabditis elegans. Trends Microbiol 13: 119-127.
46. Stuart, L.M., Paquette, N., and Boyer, L. (2013) Effector-triggered versus pattern-triggered immunity: how animals sense pathogens. Nature Reviews. Immunology 13: 199-206.
47. Suh, J., and Hutter, H. (2012) A survey of putative secreted and transmembrane proteins encoded in the C.elegans genome. BMC Genomics 13: 333.
48. Sulston, J.E., Schierenberg, E., White, J.G., and Thomson, J.N. (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100: 64-119.
49. Texier, C., Vidau, C., Vigues, B., El Alaoui, H., and Delbac, F. (2010) Microsporidia: a model for minimal parasite-host interactions. Curr Opin Microbiol 13: 443-449.
50. The C.elegans Sequencing Consortium (1998) Genome sequence of the nematode C.elegans: a platform for investigating biology. Science 282: 2012-2018.
51. Thomsen, L.E., Slutz, S.S., Tan, M.W., and Ingmer, H. (2006) Caenorhabditis elegans is a model host for Listeria monocytogenes. Appl Environ Microbiol 72: 1700-1701.
52. Tour, O., Meijer, R.M., Zacharias, D.A., Adams, S.R., and Tsien, R.Y. (2003) Genetically targeted chromophore-assisted light inactivation. Nat Biotechnol 21: 1505-1508.
53. Troemel, E.R. (2011) New models of microsporidiosis: infections in zebrafish, C. elegans, and honey bee. PLoS Pathog 7: e1001243.
54. Troemel, E.R., Félix, M.A., Whiteman, N.K., Barriere, A., and Ausubel, F.M. (2008) Microsporidia are natural intracellular parasites of the nematode Caenorhabditis elegans. PLoS Biol 6: 2736-2752.
55. Wilkins, C., Dishongh, R., Moore, S.C., Whitt, M.A., Chow, M., and Machaca, K. (2005) RNA interference is an antiviral defence mechanism in Caenorhabditis elegans. Nature 436: 1044-1047.
56. Woolhouse, M.E., Webster, J.P., Domingo, E., Charlesworth, B., and Levin, B.R. (2002) Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat Genet 32: 569-577.
57. Zhang, Y., Lu, H., and Bargmann, C.I. (2005) Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature 438: 179-184.
58. Zugasti, O., and Ewbank, J.J. (2009) Neuroimmune regulation of antimicrobial peptide expression by a noncanonical TGF-beta signaling pathway in Caenorhabditis elegans epidermis. Nat Immunol 10: 249-256.