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Enterococcus infection biology: Lessons from invertebrate host models

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Abstract

The enterococci are commensals of the gastrointestinal tract of many metazoans, from insects to humans. While they normally do not cause disease in the intestine, they can become pathogenic when they infect sites outside of the gut. Recently, the enterococci have become important nosocomial pathogens, with the majority of human enterococcal infections caused by two species, Enterococcus faecalis and Enterococcus faecium. Studies using invertebrate infection models have revealed insights into the biology of enterococcal infections, as well as general principles underlying host innate immune defense. This review highlights recent findings on Enterococcus infection biology from two invertebrate infection models, the greater wax moth Galleria mellonella and the free-living bacteriovorous nematode Caenorhabditis elegans.

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References

  • Abranches, J., Martinez, A.R., Kajfasz, J.K., Chavez, V., Garsin, D.A., and Lemos, J.A. 2009. The molecular alarmone (p)ppGpp mediates stress responses, vancomycin tolerance, and virulence in Enterococcus faecalis. J. Bacteriol. 191, 2248–2256.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Apidianakis, Y. and Rahme, L.G. 2011. Drosophila melanogaster as a model for human intestinal infection and pathology. Dis. Model Mech. 4, 21–30.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Arias, C.A. and Murray, B.E. 2012. The rise of the Enterococcus: beyond vancomycin resistance. Nat. Rev. Microbiol. 10, 266–278.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Beale, E., Li, G., Tan, M.W., and Rumbaugh, K.P. 2006. Caenorhabditis elegans senses bacterial autoinducers. Appl. Environ. Microbiol. 72, 5135–5137.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bourgogne, A., Garsin, D.A., Qin, X., Singh, K.V., Sillanpaa, J., Yerrapragada, S., Ding, Y., Dugan-Rocha, S., Buhay, C., Shen, H., and et al. 2008. Large scale variation in Enterococcus faecalis illustrated by the genome analysis of strain OG1RF. Genome Biol. 9, R110.

    PubMed Central  PubMed  Google Scholar 

  • Bucher, G.E. and Williams, R. 1967. The microbial flora of laboratory culture of the greater wax moth and its effects on rearing parasites. J. Invert. Pathol. 9, 467–473.

    Google Scholar 

  • Carniol, K. and Gilmore, M.S. 2004. Signal transduction, quorum-sensing, and extracellular protease activity in Enterococcus faecalis biofilm formation. J. Bacteriol. 186, 8161–8163.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Casadevall, A. 2005. Host as the variable: model hosts approach the immunological asymptote. Infect. Immun. 73, 3829–3832.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chavez, V., Mohri-Shiomi, A., Maadani, A., Vega, L.A., and Garsin, D.A. 2007. Oxidative stress enzymes are required for DAF-16-ediated immunity due to generation of reactive oxygen species by Caenorhabditis elegans. Genetics 176, 1567–1577.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Coburn, P.S. and Gilmore, M.S. 2003. The Enterococcus faecalis cytolysin: a novel toxin active against eukaryotic and prokaryotic cells. Cell. Microbiol. 5, 661–669.

    CAS  PubMed  Google Scholar 

  • Cook, L.C. and Federle, M.J. 2013. Peptide pheromone signaling in Streptococcus and Enterococcus. FEMS Microbiol. Rev. doi: 10.1111/1574-6976.12046.

    Google Scholar 

  • Cox, C.R., Coburn, P.S., and Gilmore, M.S. 2005. Enterococcal cytolysin: a novel two component peptide system that serves as a bacterial defense against eukaryotic and prokaryotic cells. Curr. Protein Pept. Sci. 6, 77–84.

    CAS  PubMed  Google Scholar 

  • Cox, C.R. and Gilmore, M.S. 2007. Native microbial colonization of Drosophila melanogaster and its use as a model of Enterococcus faecalis pathogenesis. Infect. Immun. 75, 1565–1576.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Creti, R., Fabretti, F., Koch, S., Huebner, J., Garsin, D.A., Baldassarri, L., Montanaro, L., and Arciola, C.R. 2009. Surface protein EF3314 contributes to virulence properties of Enterococcus faecalis. Int. J. Artif. Organs 32, 611–620.

    CAS  PubMed  Google Scholar 

  • de Oliveira, N.E., Abranches, J., Gaca, A.O., Laport, M.S., Damaso, C.R., Bastos Mdo, C., Lemos, J.A., and Giambiagi-de Marval, M. 2011. clpB, a class III heat-shock gene regulated by CtsR, is involved in thermotolerance and virulence of Enterococcus faecalis. Microbiology 157, 656–665.

    PubMed  Google Scholar 

  • Deibel, R.H. 1964a. The Group D Streptococci. Bacteriol. Reviews 28, 330–366.

    CAS  Google Scholar 

  • Deibel, R.H. 1964b. Utilization of arginine as an energy source for the growth of Streptococcus faecalis. J. Bacteriol. 87, 988–992.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Devriese, L.A., Pot, B., and Collins, M.D. 1993. Phenotypic identification of the genus Enterococcus and differentiation of phylogenetically distinct enterococcal species and species groups. J. Appl. Bacteriol. 75, 399–408.

    CAS  PubMed  Google Scholar 

  • Donlan, R.M. and Costerton, J.W. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15, 167–193.

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dunn, P.E., Bohnert, T.J., and Russell, V. 1994. Midgut antibacterial defenses of Manduca sexta following infection and during metamorphosis. In Hoffmann, J.A., Janeway, C.A.Jr., and Natori, S. (eds.), Phylogenetic Perspectives in Immunity: The Insect Host Defense, pp. 105–113. Landes, Austin, Texas, USA.

    Google Scholar 

  • Farrow, J.A., Jones, D., Phillips, B.A., and Collins, M.D. 1983. Taxonomic studies on some group D Streptococci. J. Gen. Microbiol. 129, 1423–1432.

    CAS  PubMed  Google Scholar 

  • Felix, M.A. and Braendle, C. 2010. The natural history of Caenorhabditis elegans. Curr. Biol. 20, R965–969.

    CAS  PubMed  Google Scholar 

  • Fischetti, V.A. and American Society for Microbiology. 2006. Gram-positive pathogens. ASM Press, Washington, D.C., USA.

    Google Scholar 

  • Fisher, K. and Phillips, C. 2009. The ecology, epidemiology and virulence of Enterococcus. Microbiology 155, 1749–1757.

    CAS  PubMed  Google Scholar 

  • Gaca, A.O., Abranches, J., Kajfasz, J.K., and Lemos, J.A. 2012. Global transcriptional analysis of the stringent response in Enterococcus faecalis. Microbiology 158, 1994–2004.

    CAS  PubMed  Google Scholar 

  • Garsin, D.A., Sifri, C.D., Mylonakis, E., Qin, X., Singh, K.V., Murray, B.E., Calderwood, S.B., and Ausubel, F.M. 2001. A simple model host for identifying Gram-positive virulence factors. Proc. Natl. Acad. Sci. USA 98, 10892–10897.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Garsin, D.A., Villanueva, J.M., Begun, J., Kim, D.H., Sifri, C.D., Calderwood, S.B., Ruvkun, G., and Ausubel, F.M. 2003. Long-lived C. elegans daf-2 mutants are resistant to bacterial pathogens. Science 300, 1921.

    CAS  PubMed  Google Scholar 

  • Gaspar, F., Teixeira, N., Rigottier-Gois, L., Marujo, P., Nielsen-LeRoux, C., Crespo, M.T., Lopes Mde, F., and Serror, P. 2009. Virulence of Enterococcus faecalis dairy strains in an insect model: the role of fsrB and gelE. Microbiology 155, 3564–3571.

    CAS  PubMed  Google Scholar 

  • Giard, J.C., Laplace, J.M., Rince, A., Pichereau, V., Benachour, A., Leboeuf, C., Flahaut, S., Auffray, Y., and Hartke, A. 2001. The stress proteome of Enterococcus faecalis. Electrophoresis 22, 2947–2954.

    CAS  PubMed  Google Scholar 

  • Gilmore, M.S. 2002. The enterococci: pathogenesis, molecular biology, and antibiotic resistance. ASM Press, Washington, D.C., USA.

    Google Scholar 

  • Glavis-Bloom, J., Muhammed, M., and Mylonakis, E. 2012. Of model hosts and man: using Caenorhabditis elegans, Drosophila melanogaster and Galleria mellonella as model hosts for infectious disease research. Adv. Exp. Med. Biol. 710, 11–17.

    CAS  PubMed  Google Scholar 

  • Goldsmith, M.R. and Marec, F. 2010. Molecular biology and genetics of the Lepidoptera. CRC Press/Taylor & Francis, Boca Raton, FL, USA.

    Google Scholar 

  • Gospodarek, E., Bogiel, T., and Zalas-Wiecek, P. 2009. Communication between microorganisms as a basis for production of virulence factors. Pol. J. Microbiol. 58, 191–198.

    CAS  PubMed  Google Scholar 

  • Hancock, L.E. and Perego, M. 2004. The Enterococcus faecalis fsr two-component system controls biofilm development through production of gelatinase. J. Bacteriol. 186, 5629–5639.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Heikens, E., Singh, K.V., Jacques-Palaz, K.D., van Luit-Asbroek, M., Oostdijk, E.A., Bonten, M.J., Murray, B.E., and Willems, R.J. 2011. Contribution of the enterococcal surface protein Esp to pathogenesis of Enterococcus faecium endocarditis. Microbes Infect. 13, 1185–1190.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Heim, S., Lleo, M., Bonato, B., Guzman, C.A., and Canepari, P. 2002. The viable but nonculturable state and starvation are different stress responses of Enterococcus faecalis, as determined by proteome analysis. J. Bacteriol. 184, 6739–6745.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hoeven, R., McCallum, K.C., Cruz, M.R., and Garsin, D.A. 2011. Ce-Duox1/BLI-3 generated reactive oxygen species trigger protective SKN-1 activity via p38 MAPK signaling during infection in C. elegans. PLoS Pathog. 7, e1002453.

    PubMed Central  PubMed  Google Scholar 

  • Huycke, M.M., Spiegel, C.A., and Gilmore, M.S. 1991. Bacteremia caused by hemolytic, high-level gentamicin-resistant Enterococcus faecalis. Antimicrob. Agents Chemother. 35, 1626–1634.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hynes, W.L. and Walton, S.L. 2000. Hyaluronidases of Gram-positive bacteria. FEMS Microbiol. Lett. 183, 201–207.

    CAS  PubMed  Google Scholar 

  • Irazoqui, J.E., Urbach, J.M., and Ausubel, F.M. 2010. Evolution of host innate defence: insights from Caenorhabditis elegans and primitive invertebrates. Nat. Rev. Immunol. 10, 47–58.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jander, G., Rahme, L.G., and Ausubel, F.M. 2000. Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J. Bacteriol. 182, 3843–3845.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jarosz, J. 1975. Lysozyme-like lytic enzyme of Streptococcus faecalis and its role in larval development of wax moth, Galleria mellonella. J. Invert. Pathol. 26, 275–281.

    CAS  Google Scholar 

  • Jarosz, J. 1979. Gut flora of Galleria mellonella suppressing ingested bacteria. J. Invert. Pathol. 34, 192–198.

    CAS  Google Scholar 

  • Jett, B.D., Huycke, M.M., and Gilmore, M.S. 1994. Virulence of enterococci. Clin. Microbiol. Rev. 7, 462–478.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Johnson, A.P. 1994. The pathogenicity of enterococci. J. Antimicrob. Chemother. 33, 1083–1089.

    CAS  PubMed  Google Scholar 

  • Kamath, R.S. and Ahringer, J. 2003. Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30, 313–321.

    CAS  PubMed  Google Scholar 

  • Kamath, R.S., Martinez-Campos, M., Zipperlen, P., Fraser, A.G., and Ahringer, J. 2001. Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol. 2, RESEARCH0002.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Karaolis, D.K., Means, T.K., Yang, D., Takahashi, M., Yoshimura, T., Muraille, E., Philpott, D., Schroeder, J.T., Hyodo, M., Hayakawa, Y., and et al. 2007. Bacterial c-di-GMP is an immunostimulatory molecule. J. Immunol. 178, 2171–2181.

    CAS  PubMed  Google Scholar 

  • Kayaoglu, G. and Orstavik, D. 2004. Virulence factors of Enterococcus faecalis: relationship to endodontic disease. Crit. Rev. Oral. Biol. Med. 15, 308–320.

    PubMed  Google Scholar 

  • Kong, K.F., Vuong, C., and Otto, M. 2006. Staphylococcus quorum sensing in biofilm formation and infection. Int. J. Med. Microbiol. 296, 133–139.

    CAS  PubMed  Google Scholar 

  • Lantz, M.S. 1997. Are bacterial proteases important virulence factors? J. Periodontal Res. 32, 126–132.

    CAS  PubMed  Google Scholar 

  • Lebreton, F., Riboulet-Bisson, E., Serror, P., Sanguinetti, M., Posteraro, B., Torelli, R., Hartke, A., Auffray, Y., and Giard, J.C. 2009. ace, which encodes an adhesin in Enterococcus faecalis, is regulated by Ers and is involved in virulence. Infect. Immun. 77, 2832–2839.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lebreton, F., van Schaik, W., Sanguinetti, M., Posteraro, B., Torelli, R., Le Bras, F., Verneuil, N., Zhang, X., Giard, J.C., Dhalluin, A., and et al. 2012. AsrR is an oxidative stress sensing regulator modulating Enterococcus faecium opportunistic traits, antimicrobial resistance, and pathogenicity. PLoS Pathog. 8, e1002834.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lemaitre, B., Nicolas, E., Michaut, L., Reichhart, J.M., and Hoffmann, J.A. 2012. Pillars article: the dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell. 1996. 86: 973–983. J. Immunol. 188, 5210–5220.

    Google Scholar 

  • Lewis, K. 2001. Riddle of biofilm resistance. Antimicrob. Agents Chemother. 45, 999–1007.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lleo, M.M., Tafi, M.C., and Canepari, P. 1998. Nonculturable Enterococcus faecalis cells are metabolically active and capable of resuming active growth. System. Appl. Microbiol. 21, 333–339.

    CAS  Google Scholar 

  • Lyon, G.J. and Novick, R.P. 2004. Peptide signaling in Staphylococcus aureus and other Gram-positive bacteria. Peptides 25, 1389–1403.

    CAS  PubMed  Google Scholar 

  • Maadani, A., Fox, K.A., Mylonakis, E., and Garsin, D.A. 2007. Enterococcus faecalis mutations affecting virulence in the Caenorhabditis elegans model host. Infect. Immun. 75, 2634–2637.

    CAS  PubMed Central  PubMed  Google Scholar 

  • MacCallum, W.G. and Hastings, T.W. 1899. A case of acute endocarditis caused by Micrococcus zymogenes (nov. spec.), with a description of the microorganism. J. Exp. Med. 4, 521–534.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Makinen, P.L., Clewell, D.B., An, F., and Makinen, K.K. 1989. Purification and substrate specificity of a strongly hydrophobic extracellular metalloendopeptidase (“gelatinase”) from Streptococcus faecalis (strain 0G1-10). J. Biol. Chem. 264, 3325–3334.

    CAS  PubMed  Google Scholar 

  • Makinen, P.L. and Makinen, K.K. 1994. The Enterococcus faecalis extracellular metalloendopeptidase (EC 3.4.24.30; coccolysin) inactivates human endothelin at bonds involving hydrophobic amino acid residues. Biochem. Biophys. Res. Commun. 200, 981–985.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed Central  PubMed  Google Scholar 

  • McWhirter, S.M., Barbalat, R., Monroe, K.M., Fontana, M.F., Hyodo, M., Joncker, N.T., Ishii, K.J., Akira, S., Colonna, M., Chen, Z.J., and et al. 2009. A host type I interferon response is induced by cytosolic sensing of the bacterial second messenger cyclic-di-GMP. J. Exp. Med. 206, 1899–1911.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Medzhitov, R. 2001. Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1, 135–145.

    CAS  PubMed  Google Scholar 

  • Melo, J.A. and Ruvkun, G. 2012. Inactivation of conserved C. elegans genes engages pathogen- and xenobiotic-associated defenses. Cell 149, 452–466.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Michaux, C., Sanguinetti, M., Reffuveille, F., Auffray, Y., Posteraro, B., Gilmore, M.S., Hartke, A., and Giard, J.C. 2011. SlyA is a transcriptional regulator involved in the virulence of Enterococcus faecalis. Infect. Immun. 79, 2638–2645.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Moy, T.I., Ball, A.R., Anklesaria, Z., Casadei, G., Lewis, K., and Ausubel, F.M. 2006. Identification of novel antimicrobials using a live-animal infection model. Proc. Natl. Acad. Sci. USA 103, 10414–10419.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Moy, T.I., Conery, A.L., Larkins-Ford, J., Wu, G., Mazitschek, R., Casadei, G., Lewis, K., Carpenter, A.E., and Ausubel, F.M. 2009. High-throughput screen for novel antimicrobials using a whole animal infection model. ACS Chem. Biol. 4, 527–533.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Moy, T.I., Mylonakis, E., Calderwood, S.B., and Ausubel, F.M. 2004. Cytotoxicity of hydrogen peroxide produced by Enterococcus faecium. Infect. Immun. 72, 4512–4520.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Murphy, C.T., McCarroll, S.A., Bargmann, C.I., Fraser, A., Kamath, R.S., Ahringer, J., Li, H., and Kenyon, C. 2003. Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424, 277–283.

    CAS  PubMed  Google Scholar 

  • Murray, B.E., Singh, K.V., Ross, R.P., Heath, J.D., Dunny, G.M., and Weinstock, G.M. 1993. Generation of restriction map of Enterococcus faecalis OG1 and investigation of growth requirements and regions encoding biosynthetic function. J. Bacteriol. 175, 5216–5223.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Murray, P.R., Rosenthal, K.S., and Pfaller, M.A. 2013. Medical microbiology. Elsevier/Saunders, Philadelphia, USA.

    Google Scholar 

  • Nakayama, J., Cao, Y., Horii, T., Sakuda, S., Akkermans, A.D., de Vos, W.M., and Nagasawa, H. 2001. Gelatinase biosynthesis-activating pheromone: a peptide lactone that mediates a quorum sensing in Enterococcus faecalis. Mol. Microbiol. 41, 145–154.

    CAS  PubMed  Google Scholar 

  • Nakayama, J., Chen, S., Oyama, N., Nishiguchi, K., Azab, E.A., Tanaka, E., Kariyama, R., and Sonomoto, K. 2006. Revised model for Enterococcus faecalis fsr quorum-sensing system: the small open reading frame fsrD encodes the gelatinase biosynthesis-activating pheromone propeptide corresponding to Staphylococcal AgrD. J. Bacteriol. 188, 8321–8326.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nallapareddy, S.R., Singh, K.V., Duh, R.W., Weinstock, G.M., and Murray, B.E. 2000. Diversity of ace, a gene encoding a microbial surface component recognizing adhesive matrix molecules, from different strains of Enterococcus faecalis and evidence for production of Ace during human infections. Infect. Immun. 68, 5210–5217.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Noble, C.J. 1978. Carriage of group D streptococci in the human bowel. J. Clin. Pathol. 31, 1182–1186.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Novick, R.P. and Geisinger, E. 2008. Quorum sensing in staphylococci. Ann. Review Genet. 42, 541–564.

    CAS  Google Scholar 

  • Papp, D., Csermely, P., and Soti, C. 2012. A role for SKN-1/Nrf in pathogen resistance and immunosenescence in Caenorhabditis elegans. PLoS Pathog. 8, e1002673.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Park, S.Y., Kim, K.M., Lee, J.H., Seo, S.J., and Lee, I.H. 2007. Extracellular gelatinase of Enterococcus faecalis destroys a defense system in insect hemolymph and human serum. Infect. Immun. 75, 1861–1869.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Paulsen, I.T., Banerjei, L., Myers, G.S., Nelson, K.E., Seshadri, R., Read, T.D., Fouts, D.E., Eisen, J.A., Gill, S.R., Heidelberg, J.F., and et al. 2003. Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science 299, 2071–2074.

    CAS  PubMed  Google Scholar 

  • Pillai, S.K., Sakoulas, G., Eliopoulos, G.M., Moellering, R.C. Jr., Murray, B.E., and Inouye, R.T. 2004. Effects of glucose on fsr-mediated biofilm formation in Enterococcus faecalis. J. Infect. Dis. 190, 967–970.

    CAS  PubMed  Google Scholar 

  • Podbielski, A. and Kreikemeyer, B. 2004. Cell density-dependent regulation: basic principles and effects on the virulence of Gram-positive cocci. Int. J. Infect. Dis. 8, 81–95.

    CAS  PubMed  Google Scholar 

  • Pukkila-Worley, R., Feinbaum, R., Kirienko, N.V., Larkins-Ford, J., Conery, A.L., and Ausubel, F.M. 2012. Stimulation of host immune defenses by a small molecule protects C. elegans from bacterial infection. PLoS Genet. 8, e1002733.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rakita, R.M., Vanek, N.N., Jacques-Palaz, K., Mee, M., Mariscalco, M.M., Dunny, G.M., Snuggs, M., Van Winkle, W.B., and Simon, S.I. 1999. Enterococcus faecalis bearing aggregation substance is resistant to killing by human neutrophils despite phagocytosis and neutrophil activation. Infect. Immun. 67, 6067–6075.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ran, F.A., Hsu, P.D., Lin, C.Y., Gootenberg, J.S., Konermann, S., Trevino, A.E., Scott, D.A., Inoue, A., Matoba, S., Zhang, Y., and Zhang, F. 2013a. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154, 1380–1389.

    CAS  PubMed  Google Scholar 

  • Ran, F.A., Hsu, P.D., Wright, J., Agarwala, V., Scott, D.A., and Zhang, F. 2013b. Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8, 2281–2308.

    CAS  PubMed  Google Scholar 

  • Reid, G., Denstedt, J.D., Kang, Y.S., Lam, D., and Nause, C. 1992. Microbial adhesion and biofilm formation on ureteral stents in vitro and in vivo. J. Urol. 148, 1592–1594.

    CAS  PubMed  Google Scholar 

  • Roon, R.J. and Barker, H.A. 1972. Fermentation of agmatine in Streptococcus faecalis: occurrence of putrescine transcarbamoylase. J. Bacteriol. 109, 44–50.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sabbuba, N., Hughes, G., and Stickler, D.J. 2002. The migration of Proteus mirabilis and other urinary tract pathogens over Foley catheters. BJU Int. 89, 55–60.

    CAS  PubMed  Google Scholar 

  • Sava, I.G., Heikens, E., and Huebner, J. 2010. Pathogenesis and immunity in enterococcal infections. Clin. Microbiol. Infect. 16, 533–540.

    CAS  PubMed  Google Scholar 

  • Schmidtchen, A., Frick, I.M., Andersson, E., Tapper, H., and Bjorck, L. 2002. Proteinases of common pathogenic bacteria degrade and inactivate the antibacterial peptide LL-37. Mol. Microbiol. 46, 157–168.

    CAS  PubMed  Google Scholar 

  • Shankar, N., Baghdayan, A.S., and Gilmore, M.S. 2002. Modulation of virulence within a pathogenicity island in vancomycin-resistant Enterococcus faecalis. Nature 417, 746–750.

    CAS  PubMed  Google Scholar 

  • Shankar, N., Baghdayan, A.S., Willems, R., Hammerum, A.M., and Jensen, L.B. 2006. Presence of pathogenicity island genes in Enterococcus faecalis isolates from pigs in Denmark. J. Clin. Microbiol. 44, 4200–4203.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sifri, C.D., Mylonakis, E., Singh, K.V., Qin, X., Garsin, D.A., Murray, B.E., Ausubel, F.M., and Calderwood, S.B. 2002. Virulence effect of Enterococcus faecalis protease genes and the quorum-sensing locus fsr in Caenorhabditis elegans and mice. Infect. Immun. 70, 5647–5650.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Singh, K.V., Nallapareddy, S.R., Nannini, E.C., and Murray, B.E. 2005. Fsr-independent production of protease(s) may explain the lack of attenuation of an Enterococcus faecalis fsr mutant versus a gelE-sprE mutant in induction of endocarditis. Infect. Immun. 73, 4888–4894.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sorsa, T., Ingman, T., Suomalainen, K., Haapasalo, M., Konttinen, Y.T., Lindy, O., Saari, H., and Uitto, V.J. 1992. Identification of proteases from periodontopathogenic bacteria as activators of latent human neutrophil and fibroblast-type interstitial collagenases. Infect. Immun. 60, 4491–4495.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Takao, A., Nagashima, H., Usui, H., Sasaki, F., Maeda, N., Ishibashi, K., and Fujita, H. 1997. Hyaluronidase activity in human pus from which Streptococcus intermedius was isolated. Microb. Immunol. 41, 795–798.

    CAS  Google Scholar 

  • Tang, H. 2009. Regulation and function of the melanization reaction in Drosophila. Fly 3, 105–111.

    CAS  PubMed  Google Scholar 

  • Teixeira, N., Varahan, S., Gorman, M.J., Palmer, K.L., Zaidman-Remy, A., Yokohata, R., Nakayama, J., Hancock, L.E., Jacinto, A., Gilmore, M.S., and de Fatima Silva Lopes, M. 2013. Drosophila host model reveals new Enterococcus faecalis quorum-sensing associated virulence factors. PloS One 8, e64740.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Thomas, V.C., Hiromasa, Y., Harms, N., Thurlow, L., Tomich, J., and Hancock, L.E. 2009. A fratricidal mechanism is responsible for eDNA release and contributes to biofilm development of Enterococcus faecalis. Mol. Microbiol. 72, 1022–1036.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Toto, P.D., Santangelo, M.V., and Madonia, J.V. 1968. Use of hyaluronic acid and chondroitin sulfate by bacterial isolates from carious dentin. J. Dental Res. 47, 1056–1061.

    CAS  Google Scholar 

  • Tunney, M.M. and Gorman, S.P. 2002. Evaluation of a poly(vinyl pyrollidone)-coated biomaterial for urological use. Biomaterials 23, 4601–4608.

    CAS  PubMed  Google Scholar 

  • van Opijnen, T. and Camilli, A. 2010. Genome-wide fitness and genetic interactions determined by Tn-seq, a high-throughput massively parallel sequencing method for microorganisms. Curr. Protoc. Microbiol. Chapter 1, Unit1E 3.

    Google Scholar 

  • Van Tyne, D., Martin, M.J., and Gilmore, M.S. 2013. Structure, function, and biology of the Enterococcus faecalis cytolysin. Toxins 5, 895–911.

    PubMed Central  PubMed  Google Scholar 

  • Vance, R.E., Isberg, R.R., and Portnoy, D.A. 2009. Patterns of pathogenesis: discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe 6, 10–21.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vanek, N.N., Simon, S.I., Jacques-Palaz, K., Mariscalco, M.M., Dunny, G.M., and Rakita, R.M. 1999. Enterococcus faecalis aggregation substance promotes opsonin-independent binding to human neutrophils via a complement receptor type 3-mediated mechanism. FEMS Immunol. Med. Microbiol. 26, 49–60.

    CAS  PubMed  Google Scholar 

  • Vebo, H.C., Solheim, M., Snipen, L., Nes, I.F., and Brede, D.A. 2010. Comparative genomic analysis of pathogenic and probiotic Enterococcus faecalis isolates, and their transcriptional responses to growth in human urine. PLoS One 5, e12489.

    PubMed Central  PubMed  Google Scholar 

  • Vogel, S.N. 2012. How discovery of Toll-mediated innate immunity in Drosophila impacted our understanding of TLR signaling (and vice versa). J. Immunol. 188, 5207–5209.

    CAS  PubMed  Google Scholar 

  • Walhout, A.J.M. and Boulton, S.J. 2006. Biochemistry and molecular biology, The online review of C. elegans biology. In Walhout, A.J.M. and Boulton, S.J. (eds.), WormBook.

    Google Scholar 

  • Waterfield, N.R., Wren, B.W., and Ffrench-Constant, R.H. 2004. Invertebrates as a source of emerging human pathogens. Nat. Rev. Microbiol. 2, 833–841.

    CAS  PubMed  Google Scholar 

  • Waters, C.M., Antiporta, M.H., Murray, B.E., and Dunny, G.M. 2003. Role of the Enterococcus faecalis GelE protease in determination of cellular chain length, supernatant pheromone levels, and degradation of fibrin and misfolded surface proteins. J. Bacteriol. 185, 3613–3623.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yin, Q., Tian, Y., Kabaleeswaran, V., Jiang, X., Tu, D., Eck, M.J., Chen, Z.J., and Wu, H. 2012. Cyclic di-GMP sensing via the innate immune signaling protein STING. Mol. Cell 46, 735–745.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhao, C., Hartke, A., La Sorda, M., Posteraro, B., Laplace, J.M., Auffray, Y., and Sanguinetti, M. 2010. Role of methionine sulfoxide reductases A and B of Enterococcus faecalis in oxidative stress and virulence. Infect. Immun. 78, 3889–3897.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zimmermann, S., Wagner, C., Muller, W., Brenner-Weiss, G., Hug, F., Prior, B., Obst, U., and Hansch, G.M. 2006. Induction of neutrophil chemotaxis by the quorum-sensing molecule N-(3-oxododecanoyl)-L-homoserine lactone. Infect. Immun. 74, 5687–5692.

    CAS  PubMed Central  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Molecular Biology, Massachusetts General Hospital, Boston, MA, 02114, USA

    Grace J. Yuen & Frederick M. Ausubel

  2. Program in Immunology, Harvard Medical School, Boston, MA, 02115, USA

    Grace J. Yuen

  3. Department of Genetics, Harvard Medical School, Boston, MA, 02115, USA

    Frederick M. Ausubel

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  1. Grace J. Yuen
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  2. Frederick M. Ausubel
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Correspondence to Frederick M. Ausubel.

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Yuen, G.J., Ausubel, F.M. Enterococcus infection biology: Lessons from invertebrate host models. J Microbiol. 52, 200–210 (2014). https://doi.org/10.1007/s12275-014-4011-6

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