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Listeria monocytogenes: a multifaceted model

Key Points

  • Listeria monocytogenes has evolved sophisticated mimicries to exploit the host cell. L. monocytogenes subverts host-cell receptors and signalling to trigger entry, and it harnesses the actin machinery to enable intracellular and intercellular spread.

  • A combination of molecular studies and in vivo work has yielded appropriate and useful model organisms to study the pathology of L. monocytogenes infection.

  • L. monocytogenes makes use of well-known, as well as previously uncharacterized, mechanisms to regulate the expression of virulence factors.

  • L. monocytogenes is a model of bacterial adaptation to the cytoplasm of the host cell. Specific growth mechanisms and a large proportion of its genome are called into action for survival in this compartment.

  • Comparative genomics is a powerful method that has allowed the identification of several new virulence factors.

Abstract

The opportunistic intracellular pathogen Listeria monocytogenes has become a paradigm for the study of host–pathogen interactions and bacterial adaptation to mammalian hosts. Analysis of L. monocytogenes infection has provided considerable insight into how bacteria invade cells, move intracellularly, and disseminate in tissues, as well as tools to address fundamental processes in cell biology. Moreover, the vast amount of knowledge that has been gathered through in-depth comparative genomic analyses and in vivo studies makes L. monocytogenes one of the most well-studied bacterial pathogens.

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Figure 1: Schematic representation and electron micrographs of the Listeria monocytogenes life cycle.
Figure 2: Met signalling induced by hepatocyte growth factor (HGF) and internalin B (InlB).
Figure 3: Adherens junction and internalin A (InlA)-induced bacterial entry.
Figure 4: Host specificity of Listeria monocytogenes proteins internalin A (InlA) and InlB.
Figure 5: The PrfA regulator.
Figure 6: Listeriolysin O (LLO) pore-forming mechanism.
Figure 7: The internalin family of proteins.

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References

  1. Khelef, N. et al. The Prokaryotes: An Evolving Electronic Resource for the Microbiological Community [online] (eds Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.-H. & Stackebrandt, E.) (Springer, New York, 2005).

    Google Scholar 

  2. Pamer, E. G. Immune responses to Listeria monocytogenes. Nature Rev. Immunol. 4, 812–823 (2004).

    CAS  Google Scholar 

  3. Mackaness, G. B. Cellular resistance to infection. J. Exp. Med. 116, 381–406 (1962). First in-depth analysis of the interaction between L. monocytogenes and its host, both in mice and in cultured mouse macrophages.

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Racz, P., Tenner, K. & Mero, E. Experimental Listeria enteritis. I. An electron microscopic study of the epithelial phase in experimental Listeria infection. Lab. Invest. 26, 694–700 (1972).

    CAS  PubMed  Google Scholar 

  5. McCaffrey, R. L. et al. A specific gene expression program triggered by Gram-positive bacteria in the cytosol. Proc. Natl Acad. Sci. USA 101, 11386–11391 (2004).

    CAS  PubMed  Google Scholar 

  6. Cohen, P. et al. Monitoring cellular responses to Listeria monocytogenes with oligonucleotide arrays. J. Biol. Chem. 275, 11181–11190 (2000).

    CAS  PubMed  Google Scholar 

  7. Shen, Y., Naujokas, M., Park, M. & Ireton, K. InIB-dependent internalization of Listeria is mediated by the Met receptor tyrosine kinase. Cell 103, 501–510 (2000). Identifies the cellular receptor for InlB and illustrates the exploitation of a receptor-tyrosine-kinase pathway for bacterial entry.

    CAS  PubMed  Google Scholar 

  8. Tang, P., Sutherland, C. L., Gold, M. R. & Finlay, B. B. Listeria monocytogenes invasion of epithelial cells requires the MEK-1/ERK-2 mitogen-activated protein kinase pathway. Infect. Immun. 66, 1106–1112 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Ireton, K. et al. A role for phosphoinositide 3-kinase in bacterial invasion. Science 274, 780–782 (1996).

    CAS  PubMed  Google Scholar 

  10. Copp, J., Marino, M., Banerjee, M., Ghosh, P. & van der Geer, P. Multiple regions of internalin B contribute to its ability to turn on the Ras–mitogen-activated protein kinase pathway. J. Biol. Chem. 278, 7783–7789 (2003).

    CAS  PubMed  Google Scholar 

  11. Braun, L., Ghebrehiwet, B. & Cossart, P. gC1q-R/p32, a C1q-binding protein, is a receptor for the InlB invasion protein of Listeria monocytogenes. EMBO J. 19, 1458–1466 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Bierne, H. et al. WASP-related proteins, Abi1 and Ena/VASP are required for Listeria invasion induced by the Met receptor. J. Cell Sci. 118, 1537–1547 (2005).

    CAS  PubMed  Google Scholar 

  13. Bierne, H. et al. A role for cofilin and LIM kinase in Listeria-induced phagocytosis. J. Cell Biol. 155, 101–112 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Veiga, E. & Cossart, P. Listeria hijacks the clathrin-dependent endocytic machinery to invade mammalian cells. Nature Cell Biol. 7, 894–900 (2005). Shows that the endocytic machinery is subverted for L. monocytogenes entry and therefore proposes that clathrin can help engulf large particles such as bacteria.

    CAS  PubMed  Google Scholar 

  15. Harvey, H. A., Jennings, M. P., Campbell, C. A., Williams, R. & Apicella, M. A. Receptor-mediated endocytosis of Neisseria gonorrhoeae into primary human urethral epithelial cells: the role of the asialoglycoprotein receptor. Mol. Microbiol. 42, 659–672 (2001).

    CAS  PubMed  Google Scholar 

  16. Van Nhieu, G. T., Krukonis, E. S., Reszka, A. A., Horwitz, A. F. & Isberg, R. R. Mutations in the cytoplasmic domain of the integrin β1 chain indicate a role for endocytosis factors in bacterial internalization. J. Biol. Chem. 271, 7665–7672 (1996).

    CAS  PubMed  Google Scholar 

  17. Wyrick, P. B. et al. Entry of genital Chlamydia trachomatis into polarized human epithelial cells. Infect. Immun. 57, 2378–2389 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Seveau, S., Bierne, H., Giroux, S., Prevost, M. C. & Cossart, P. Role of lipid rafts in E-cadherin- and HGF-R/Met-mediated entry of Listeria monocytogenes into host cells. J. Cell Biol. 166, 743–753 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Mengaud, J., Ohayon, H., Gounon, P., Mege, R. M. & Cossart, P. E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 84, 923–932 (1996). Identifies E-cadherin as the first cellular receptor for L. monocytogenes and reveals a novel heterophilic interaction with E-cadherin.

    CAS  PubMed  Google Scholar 

  20. Perez-Moreno, M., Jamora, C. & Fuchs, E. Sticky business: orchestrating cellular signals at adherens junctions. Cell 112, 535–548 (2003).

    CAS  PubMed  Google Scholar 

  21. Lecuit, M. et al. A role for α- and β-catenins in bacterial uptake. Proc. Natl Acad. Sci. USA 97, 10008–10013 (2000).

    CAS  PubMed  Google Scholar 

  22. Drees, F., Pokutta, S., Yamada, S., Nelson, W. J. & Weis, W. I. α-Catenin is a molecular switch that binds E-cadherin–β-catenin and regulates actin-filament assembly. Cell 123, 903–915 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Yamada, S., Pokutta, S., Drees, F., Weis, W. I. & Nelson, W. J. Deconstructing the cadherin–catenin–actin complex. Cell 123, 889–901 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Sousa, S. et al. ARHGAP10 is necessary for α-catenin recruitment at adherens junctions and for Listeria invasion. Nature Cell Biol. 7, 954–960 (2005).

    CAS  PubMed  Google Scholar 

  25. Kussel-Andermann, P. et al. Vezatin, a novel transmembrane protein, bridges myosin VIIA to the cadherin–catenins complex. EMBO J. 19, 6020–6029 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Sousa, S. et al. Unconventional myosin VIIa and vezatin, two proteins crucial for Listeria entry into epithelial cells. J. Cell Sci. 117, 2121–2130 (2004).

    CAS  PubMed  Google Scholar 

  27. Takemura, R., Stenberg, P. E., Bainton, D. F. & Werb, Z. Rapid redistribution of clathrin onto macrophage plasma membranes in response to Fc receptor–ligand interaction during frustrated phagocytosis. J. Cell Biol. 102, 55–69 (1986).

    CAS  PubMed  Google Scholar 

  28. Tilney, L. G. & Portnoy, D. A. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J. Cell Biol. 109, 1597–1608 (1989). First characterization of actin nucleation by L. monocytogenes and its importance for cell–cell spread during infection.

    CAS  PubMed  Google Scholar 

  29. Dabiri, G. A., Sanger, J. M., Portnoy, D. A. & Southwick, F. S. Listeria monocytogenes moves rapidly through the host-cell cytoplasm by inducing directional actin assembly. Proc. Natl Acad. Sci. USA 87, 6068–6072 (1990).

    CAS  PubMed  Google Scholar 

  30. Kocks, C. et al. L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell 68, 521–531 (1992).

    CAS  PubMed  Google Scholar 

  31. Domann, E. et al. A novel bacterial virulence gene in Listeria monocytogenes required for host cell microfilament interaction with homology to the proline-rich region of vinculin. EMBO J. 11, 1981–1990 (1992). References 30 and 31 identify ActA as the bacterial protein that is required for actin polymerization by L. monocytogenes.

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Welch, M. D., Iwamatsu, A. & Mitchison, T. J. Actin polymerization is induced by Arp2/3 protein complex at the surface of Listeria monocytogenes. Nature 385, 265–269 (1997). Shows that the Arp2/3 actin-nucleation complex initiates ActA-dependent polymerization.

    CAS  PubMed  Google Scholar 

  33. Machesky, L. M. et al. Scar, a WASp-related protein, activates nucleation of actin filaments by the Arp2/3 complex. Proc. Natl Acad. Sci. USA 96, 3739–3744 (1999).

    CAS  PubMed  Google Scholar 

  34. Lasa, I., David, V., Gouin, E., Marchand, J. B. & Cossart, P. The amino-terminal part of ActA is critical for the actin-based motility of Listeria monocytogenes; the central proline-rich region acts as a stimulator. Mol. Microbiol. 18, 425–436 (1995).

    CAS  PubMed  Google Scholar 

  35. May, R. C. et al. The Arp2/3 complex is essential for the actin-based motility of Listeria monocytogenes. Curr. Biol. 9, 759–762 (1999).

    CAS  PubMed  Google Scholar 

  36. Smith, G. A., Theriot, J. A. & Portnoy, D. A. The tandem repeat domain in the Listeria monocytogenes ActA protein controls the rate of actin-based motility, the percentage of moving bacteria, and the localization of vasodilator-stimulated phosphoprotein and profilin. J. Cell Biol. 135, 647–660 (1996).

    CAS  PubMed  Google Scholar 

  37. Niebuhr, K. et al. A novel proline-rich motif present in ActA of Listeria monocytogenes and cytoskeletal proteins is the ligand for the EVH1 domain, a protein module present in the Ena/VASP family. EMBO J. 16, 5433–5444 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Loisel, T. P., Boujemaa, R., Pantaloni, D. & Carlier, M. F. Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature 401, 613–616 (1999).

    CAS  PubMed  Google Scholar 

  39. Geese, M. et al. Contribution of Ena/VASP proteins to intracellular motility of Listeria requires phosphorylation and proline-rich core but not F-actin binding or multimerization. Mol. Biol. Cell 13, 2383–2396 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Samarin, S. et al. How VASP enhances actin-based motility. J. Cell Biol. 163, 131–142 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Plastino, J., Olivier, S. & Sykes, C. Actin filaments align into hollow comets for rapid VASP-mediated propulsion. Curr. Biol. 14, 1766–1771 (2004).

    CAS  PubMed  Google Scholar 

  42. Krause, M., Bear, J. E., Loureiro, J. J. & Gertler, F. B. The Ena/VASP enigma. J. Cell Sci. 115, 4721–4726 (2002).

    CAS  PubMed  Google Scholar 

  43. Gouin, E., Welch, M. D. & Cossart, P. Actin-based motility of intracellular pathogens. Curr. Opin. Microbiol. 8, 35–45 (2005).

    CAS  PubMed  Google Scholar 

  44. Stevens, J. M., Galyov, E. E. & Stevens, M. P. Actin-dependent movement of bacterial pathogens. Nature Rev. Microbiol. 4, 91–101 (2006).

    CAS  Google Scholar 

  45. Lecuit, M. et al. A single amino acid in E-cadherin responsible for host specificity towards the human pathogen Listeria monocytogenes. EMBO J. 18, 3956–3963 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Lecuit, M. et al. A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier. Science 292, 1722–1725 (2001).

    CAS  PubMed  Google Scholar 

  47. Pentecost, M., Otto, G., Theriot, J. A. & Amieva, M. R. Listeria monocytogenes invades the epithelial junctions at sites of cell extrusion. PLoS Pathog. 2, e3 (2006).

    PubMed  PubMed Central  Google Scholar 

  48. Khelef, N., Lecuit, M., Bierne, H. & Cossart, P. Species specificity of the Listeria monocytogenes InlB protein. Cell. Microbiol. 8, 457–470 (2006). Shows host specificity for InlB, thereby challenging the validity of some of the animal models that are used to study listerial infection and emphasizing the need to develop new models.

    CAS  PubMed  Google Scholar 

  49. Lecuit, M. et al. Targeting and crossing of the human maternofetal barrier by Listeria monocytogenes: role of internalin interaction with trophoblast E-cadherin. Proc. Natl Acad. Sci. USA 101, 6152–6157 (2004).

    CAS  PubMed  Google Scholar 

  50. Bakardjiev, A. I., Stacy, B. A., Fisher, S. J. & Portnoy, D. A. Listeriosis in the pregnant guinea pig: a model of vertical transmission. Infect. Immun. 72, 489–497 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Mansfield, B. E., Dionne, M. S., Schneider, D. S. & Freitag, N. E. Exploration of host–pathogen interactions using Listeria monocytogenes and Drosophila melanogaster. Cell. Microbiol. 5, 901–911 (2003).

    CAS  PubMed  Google Scholar 

  52. Cheng, L. W. et al. Use of RNA interference in Drosophila S2 cells to identify host pathways controlling compartmentalization of an intracellular pathogen. Proc. Natl Acad. Sci. USA 102, 13646–13651 (2005).

    CAS  PubMed  Google Scholar 

  53. Agaisse, H. et al. Genome-wide RNAi screen for host factors required for intracellular bacterial infection. Science 309, 1248–1251 (2005). References 52 and 53 use a novel system to identify, on a large scale, host factors that are important for supporting a listerial infection.

    CAS  PubMed  Google Scholar 

  54. Thomsen, L. E., Slutz, S. S., Tan, M. W. & Ingmer, H. Caenorhabditis elegans is a model host for Listeria monocytogenes. Appl. Environ. Microbiol. 72, 1700–1701 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Mengaud, J. et al. Pleiotropic control of Listeria monocytogenes virulence factors by a gene that is autoregulated. Mol. Microbiol. 5, 2273–2283 (1991).

    CAS  PubMed  Google Scholar 

  56. Freitag, N. E., Rong, L. & Portnoy, D. A. Regulation of the prfA transcriptional activator of Listeria monocytogenes: multiple promoter elements contribute to intracellular growth and cell-to-cell spread. Infect. Immun. 61, 2537–2544 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Leimeister-Wachter, M., Haffner, C., Domann, E., Goebel, W. & Chakraborty, T. Identification of a gene that positively regulates expression of listeriolysin, the major virulence factor of Listeria monocytogenes. Proc. Natl Acad. Sci. USA 87, 8336–8340 (1990).

    CAS  PubMed  Google Scholar 

  58. Johansson, J. et al. An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell 110, 551–561 (2002). Characterizes a novel regulatory mechanism that is encoded by the upstream untranslated region of prfA mRNA and that controls the expression of this important virulence transcription factor according to the temperature.

    PubMed  Google Scholar 

  59. Hoe, N. P. & Goguen, J. D. Temperature sensing in Yersinia pestis: translation of the LcrF activator protein is thermally regulated. J. Bacteriol. 175, 7901–7909 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Schwab, U., Bowen, B., Nadon, C., Wiedmann, M. & Boor, K. J. The Listeria monocytogenes prfAP2 promoter is regulated by σB in a growth phase dependent manner. FEMS Microbiol. Lett. 245, 329–336 (2005).

    CAS  PubMed  Google Scholar 

  61. Kreft, J. & Vazquez-Boland, J. A. Regulation of virulence genes in Listeria. Int. J. Med. Microbiol. 291, 145–157 (2001).

    CAS  PubMed  Google Scholar 

  62. Ripio, M. T., Dominguez-Bernal, G., Lara, M., Suarez, M. & Vazquez-Boland, J. A. A Gly145Ser substitution in the transcriptional activator PrfA causes constitutive overexpression of virulence factors in Listeria monocytogenes. J. Bacteriol. 179, 1533–1540 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Eiting, M., Hageluken, G., Schubert, W. D. & Heinz, D. W. The mutation G145S in PrfA, a key virulence regulator of Listeria monocytogenes, increases DNA-binding affinity by stabilizing the HTH motif. Mol. Microbiol. 56, 433–446 (2005).

    CAS  PubMed  Google Scholar 

  64. Jones, S. & Portnoy, D. A. Characterization of Listeria monocytogenes pathogenesis in a strain expressing perfringolysin O in place of listeriolysin O. Infect. Immun. 62, 5608–5613 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Schuerch, D. W., Wilson-Kubalek, E. M. & Tweten, R. K. Molecular basis of listeriolysin O pH dependence. Proc. Natl Acad. Sci. USA 102, 12537–12542 (2005). Structural studies of the L. monocytogenes toxin LLO reveal the molecular mechanism that controls the optimal pH for its activity.

    CAS  PubMed  Google Scholar 

  66. Shatursky, O. et al. The mechanism of membrane insertion for a cholesterol-dependent cytolysin: a novel paradigm for pore-forming toxins. Cell 99, 293–299 (1999).

    CAS  PubMed  Google Scholar 

  67. Kayal, S. et al. Listeriolysin O-dependent activation of endothelial cells during infection with Listeria monocytogenes: activation of NF-κB and upregulation of adhesion molecules and chemokines. Mol. Microbiol. 31, 1709–1722 (1999).

    CAS  PubMed  Google Scholar 

  68. Tang, P., Rosenshine, I., Cossart, P. & Finlay, B. B. Listeriolysin O activates mitogen-activated protein kinase in eucaryotic cells. Infect. Immun. 64, 2359–2361 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Sibelius, U. et al. Listeriolysin is a potent inducer of the phosphatidylinositol response and lipid mediator generation in human endothelial cells. Infect. Immun. 64, 674–676 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Sibelius, U. et al. The listerial exotoxins listeriolysin and phosphatidylinositol-specific phospholipase C synergize to elicit endothelial cell phosphoinositide metabolism. J. Immunol. 157, 4055–4060 (1996).

    CAS  PubMed  Google Scholar 

  71. Dramsi, S. & Cossart, P. Listeriolysin O-mediated calcium influx potentiates entry of Listeria monocytogenes into the human Hep-2 epithelial cell line. Infect. Immun. 71, 3614–3618 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Tsuchiya, K. et al. Listeriolysin O-induced membrane permeation mediates persistent interleukin-6 production in Caco-2 cells during Listeria monocytogenes infection in vitro. Infect. Immun. 73, 3869–3877 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Wadsworth, S. J. & Goldfine, H. Listeria monocytogenes phospholipase C-dependent calcium signaling modulates bacterial entry into J774 macrophage-like cells. Infect. Immun. 67, 1770–1778 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Wadsworth, S. J. & Goldfine, H. Mobilization of protein kinase C in macrophages induced by Listeria monocytogenes affects its internalization and escape from the phagosome. Infect. Immun. 70, 4650–4660 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Giddings, K. S., Zhao, J., Sims, P. J. & Tweten, R. K. Human CD59 is a receptor for the cholesterol-dependent cytolysin intermedilysin. Nature Struct. Mol. Biol. 11, 1173–1178 (2004).

    CAS  Google Scholar 

  76. Glaser, P. et al. Comparative genomics of Listeria species. Science 294, 849–852 (2001). Comparative analysis of the genome sequences of L. monocytogenes (which is pathogenic) and L. innocua (which is non-pathogenic), greatly advancing the understanding of Listeria species pathogenicity.

    CAS  PubMed  Google Scholar 

  77. Williams, T., Bauer, S., Beier, D. & Kuhn, M. Construction and characterization of Listeria monocytogenes mutants with in-frame deletions in the response regulator genes identified in the genome sequence. Infect. Immun. 73, 3152–3159 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Autret, N., Raynaud, C., Dubail, I., Berche, P. & Charbit, A. Identification of the agr locus of Listeria monocytogenes: role in bacterial virulence. Infect. Immun. 71, 4463–4471 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Mandin, P. et al. VirR, a response regulator critical for Listeria monocytogenes virulence. Mol. Microbiol. 57, 1367–1380 (2005).

    CAS  PubMed  Google Scholar 

  80. Cotter, P. D., Emerson, N., Gahan, C. G. & Hill, C. Identification and disruption of lisRK, a genetic locus encoding a two-component signal transduction system involved in stress tolerance and virulence in Listeria monocytogenes. J. Bacteriol. 181, 6840–6843 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Dons, L. et al. Role of flagellin and the two-component CheA/CheY system of Listeria monocytogenes in host cell invasion and virulence. Infect. Immun. 72, 3237–3244 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Christiansen, J. K., Larsen, M. H., Ingmer, H., Sogaard-Andersen, L. & Kallipolitis, B. H. The RNA-binding protein Hfq of Listeria monocytogenes: role in stress tolerance and virulence. J. Bacteriol. 186, 3355–3362 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Archambaud, C., Gouin, E., Pizarro-Cerda, J., Cossart, P. & Dussurget, O. Translation elongation factor EF-Tu is a target for Stp, a serine–threonine phosphatase involved in virulence of Listeria monocytogenes. Mol. Microbiol. 56, 383–396 (2005).

    CAS  PubMed  Google Scholar 

  84. Annous, B. A., Becker, L. A., Bayles, D. O., Labeda, D. P. & Wilkinson, B. J. Critical role of anteiso-C15:0 fatty acid in the growth of Listeria monocytogenes at low temperatures. Appl. Environ. Microbiol. 63, 3887–3894 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Angelidis, A. S. & Smith, G. M. Role of the glycine betaine and carnitine transporters in adaptation of Listeria monocytogenes to chill stress in defined medium. Appl. Environ. Microbiol. 69, 7492–7498 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Ko, R., Smith, L. T. & Smith, G. M. Glycine betaine confers enhanced osmotolerance and cryotolerance on Listeria monocytogenes. J. Bacteriol. 176, 426–431 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Junttila, J. R., Niemela, S. I. & Hirn, J. Minimum growth temperatures of Listeria monocytogenes and non-haemolytic Listeria. J. Appl. Bacteriol. 65, 321–327 (1988).

    CAS  PubMed  Google Scholar 

  88. Cotter, P. D., Gahan, C. G. & Hill, C. Analysis of the role of the Listeria monocytogenes F0F1-ATPase operon in the acid tolerance response. Int. J. Food Microbiol. 60, 137–146 (2000).

    CAS  PubMed  Google Scholar 

  89. Cotter, P. D., Gahan, C. G. & Hill, C. A glutamate decarboxylase system protects Listeria monocytogenes in gastric fluid. Mol. Microbiol. 40, 465–475 (2001).

    CAS  PubMed  Google Scholar 

  90. Dussurget, O. et al. Listeria monocytogenes bile salt hydrolase is a PrfA-regulated virulence factor involved in the intestinal and hepatic phases of listeriosis. Mol. Microbiol. 45, 1095–1106 (2002).

    CAS  PubMed  Google Scholar 

  91. Begley, M., Sleator, R. D., Gahan, C. G. & Hill, C. Contribution of three bile-associated loci, bsh, pva, and btlB, to gastrointestinal persistence and bile tolerance of Listeria monocytogenes. Infect. Immun. 73, 894–904 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Sleator, R. D., Wemekamp-Kamphuis, H. H., Gahan, C. G., Abee, T. & Hill, C. A PrfA-regulated bile exclusion system (BilE) is a novel virulence factor in Listeria monocytogenes. Mol. Microbiol. 55, 1183–1195 (2005).

    CAS  PubMed  Google Scholar 

  93. Hardy, J. et al. Extracellular replication of Listeria monocytogenes in the murine gall bladder. Science 303, 851–853 (2004).

    CAS  PubMed  Google Scholar 

  94. Goetz, M. et al. Microinjection and growth of bacteria in the cytosol of mammalian host cells. Proc. Natl Acad. Sci. USA 98, 12221–12226 (2001).

    CAS  PubMed  Google Scholar 

  95. Chico-Calero, I. et al. Hpt, a bacterial homolog of the microsomal glucose-6-phosphate translocase, mediates rapid intracellular proliferation in Listeria. Proc. Natl Acad. Sci. USA 99, 431–436 (2002).

    CAS  PubMed  Google Scholar 

  96. O'Riordan, M., Moors, M. A. & Portnoy, D. A. Listeria intracellular growth and virulence require host-derived lipoic acid. Science 302, 462–464 (2003).

    CAS  PubMed  Google Scholar 

  97. Klarsfeld, A. D., Goossens, P. L. & Cossart, P. Five Listeria monocytogenes genes preferentially expressed in infected mammalian cells: plcA, purH, purD, pyrE and an arginine ABC transporter gene, arpJ. Mol. Microbiol. 13, 585–597 (1994).

    CAS  PubMed  Google Scholar 

  98. Chatterjee, S. S. et al. Intracellular gene expression profile of Listeria monocytogenes. Infect. Immun. 74, 1323–1338 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Joseph, B. et al. Identification of Listeria monocytogenes genes contributing to intracellular replication by expression profiling and mutant screening. J. Bacteriol. 188, 556–568 (2006). An important study that identifies the listerial genes that are required to sustain growth in the cytoplasm of the host cell.

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Doumith, M. et al. New aspects regarding evolution and virulence of Listeria monocytogenes revealed by comparative genomics and DNA arrays. Infect. Immun. 72, 1072–1083 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Cabanes, D., Dehoux, P., Dussurget, O., Frangeul, L. & Cossart, P. Surface proteins and the pathogenic potential of Listeria monocytogenes. Trends Microbiol. 10, 238–245 (2002).

    CAS  PubMed  Google Scholar 

  102. Dhar, G., Faull, K. F. & Schneewind, O. Anchor structure of cell wall surface proteins in Listeria monocytogenes. Biochemistry 39, 3725–3733 (2000).

    CAS  PubMed  Google Scholar 

  103. Bierne, H. et al. Inactivation of the srtA gene in Listeria monocytogenes inhibits anchoring of surface proteins and affects virulence. Mol. Microbiol. 43, 869–881 (2002).

    CAS  PubMed  Google Scholar 

  104. Pucciarelli, M. G. et al. Identification of substrates of the Listeria monocytogenes sortases A and B by a non-gel proteomic analysis. Proteomics 5, 4808–4817 (2005).

    CAS  PubMed  Google Scholar 

  105. Sabet, C., Lecuit, M., Cabanes, D., Cossart, P. & Bierne, H. LPXTG protein InlJ, a newly identified internalin involved in Listeria monocytogenes virulence. Infect. Immun. 73, 6912–6922 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  106. Reglier-Poupet, H. et al. Maturation of lipoproteins by type II signal peptidase is required for phagosomal escape of Listeria monocytogenes. J. Biol. Chem. 278, 49469–49477 (2003).

    CAS  PubMed  Google Scholar 

  107. Braun, L. et al. InlB: an invasion protein of Listeria monocytogenes with a novel type of surface association. Mol. Microbiol. 25, 285–294 (1997).

    CAS  PubMed  Google Scholar 

  108. Lenz, L. L., Mohammadi, S., Geissler, A. & Portnoy, D. A. SecA2-dependent secretion of autolytic enzymes promotes Listeria monocytogenes pathogenesis. Proc. Natl Acad. Sci. USA 100, 12432–12437 (2003).

    CAS  PubMed  Google Scholar 

  109. Cabanes, D., Dussurget, O., Dehoux, P. & Cossart, P. Auto, a surface associated autolysin of Listeria monocytogenes required for entry into eukaryotic cells and virulence. Mol. Microbiol. 51, 1601–1614 (2004).

    CAS  PubMed  Google Scholar 

  110. Cabanes, D. et al. Gp96 is a receptor for a novel Listeria monocytogenes virulence factor, Vip, a surface protein. EMBO J. 24, 2827–2838 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  111. Li, Z., Dai, J., Zheng, H., Liu, B. & Caudill, M. An integrated view of the roles and mechanisms of heat shock protein gp96–peptide complex in eliciting immune response. Front. Biosci. 7, d731–d751 (2002).

    CAS  PubMed  Google Scholar 

  112. Nelson, K. E. et al. Whole genome comparisons of serotype 4b and 1/2a strains of the food-borne pathogen Listeria monocytogenes reveal new insights into the core genome components of this species. Nucleic Acids Res. 32, 2386–2395 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  113. Cossart, P. & Lecuit, M. Interactions of Listeria monocytogenes with mammalian cells during entry and actin-based movement: bacterial factors, cellular ligands and signaling. EMBO J. 17, 3797–3806 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  114. Schubert, W. D. et al. Structure of internalin, a major invasion protein of Listeria monocytogenes, in complex with its human receptor E-cadherin. Cell 111, 825–836 (2002).

    CAS  PubMed  Google Scholar 

  115. Tweten, R. K. Cholesterol-dependent cytolysins, a family of versatile pore-forming toxins. Infect. Immun. 73, 6199–6209 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

Our sincere apologies to colleagues whose work has not been cited in this manuscript because of space constraints and because of the focus of this Review, which does not claim to be comprehensive. We thank E. Gouin for critical assessment of the manuscript and E. Veiga for help with Fig. 2. Work in the laboratory of P.C. is supported by the Institut National de la Recherche Agronomique, the Institut Pasteur, the Institut National de la Santé et de la Recherche Médicale, the Ministère de l'Education Nationale et de la Recherche Scientifique et Technique, and the Association par la Recherche sur le Cancer. M.H. is supported by a Pasteur Foundation fellowship. P.C. is an international research scholar of the Howard Hughes Medical Institute.

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Correspondence to Pascale Cossart.

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DATABASES

Entrez Genome Project

Bacillus subtilis

Burkholderia pseudomallei

Chlamydia trachomatis

Escherichia coli

Listeria innocua

Listeria ivanovii

Listeria monocytogenes

Listeria welshimeri

Shigella flexneri

Yersinia pestis

FURTHER INFORMATION

Bacteria–Cells Interactions Unit, Institut Pasteur

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Microbiology in Motion

The Prokaryotes: An Evolving Electronic Resource for the Microbiological Community

Glossary

Adherens junctions

Together with tight junctions and desmosomes, these are specialized structures that allow epithelial cells to adhere to each other, and they have epithelial cadherin (E-cadherin) as a major component.

Filopodia

Rod-like cell-surface projections that are composed of actin filaments. They are found on various cell types and have sensory or exploratory functions.

Lamellipodia

Thin actin-rich structures that form protrusions at the edge of the cell and are essential for cellular motility.

Two-component regulatory system

A two-protein signal-transduction system that is important for the bacterial response to environmental changes. It consists of a membrane-bound sensor protein kinase and a transcriptional-response regulator.

Elongation factor

A protein that allows tRNAs to bind the ribosome and is essential for elongation of the polypeptide chain.

Chaperone

A protein that assists other proteins to fold correctly.

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Hamon, M., Bierne, H. & Cossart, P. Listeria monocytogenes: a multifaceted model. Nat Rev Microbiol 4, 423–434 (2006). https://doi.org/10.1038/nrmicro1413

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