Abstract
Listeria monocytogenes is a food borne pathogen which has the very unique property of crossing three barriers during infection eliciting meningitis, meningo-encephalitis and abortions with a mortality rate of about 30%. Indeed, after crossing the intestinal barrier,Listeria disseminatesvia the lymph and the blood, to the brain and/or the placenta after crossing the brain-blood barrier and/or the placental barrier. During disease, this organism infects a variety of tissues and cell types in which it is mostly intracellular due to its capacity to induce its own phagocytosis into cells which are normally nonphagocytic. The strategies used byListeria to enter cells are different from those used by other well known invasive pathogens.Listeria thus appears as a fine model to study the molecular and cellular basis of bacterial invasion. In addition, not only during entry into cells but also during intra-and intercellular movement,Listeria exploits mammalian cell functions and is thus a novel tool for elucidating some unsolved fundamental aspects of cell biology, such as ligand receptor signaling and actin cytoskeleton rearrangements. In this review, the molecular and cellular basis of entry ofListeria into cells and of its intracellular motility will be discussed.
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Braun L., Dramsi S., Dehoux P., Bierne H., Lindahl G., Cossart P.: InlB: an invasion protein ofListeria monocytogenes with a novel type of surface association.Mol. Microbiol. 25, 285–294 (1997).
Braun L., Ohayon H., Cossart P.: The InlB protein ofListeria monocytogenes is sufficient to promote entry into mammalian cells.Mol. Microbiol.,27, 1077–1088 (1998).
Chakraborty T., Ebel F., Dommann E., Niebuhr K., Gerstel B., Pistor S., Temm-Grove C.J., Jockusch B.M., Reinhard M., Walter U., Wehland J.: A focal adhesion factor directly linking intracellularly motileListeria monocytogenes andListeria ivanovii to the actin-based cytoskeleton of mammalian cells.EMBO J. 14, 1314–1321 (1995).
Cossart P.: Bacterial actin based motility.Curr. Opin. Cell. Biol.,7, 94–101 (1995).
Cossart P.: Subversion of the mammalian cell cytoskeleton by invasive bacteria.J. Clin. Invest. 99, 2307–2311 (1997).
Cossart P., Kocks C.: The actin based motility of the intracellular pathogenListeria monocytogenes.Mol. Microbiol.,13, 395–402 (1994).
Dold F.G., Sanger J.M., Sanger J.W.: Intact alpha-actinin molecules are needed for both the assembly of actin into tails and the locomotion ofListeria monocytogenes inside infected cells.Cell Mot. Cytoskel. 28, 97–107 (1994).
Dramsi S., Kocks C., Forestier C., Cossart P.: Internalin-mediated invasion of epithelial cells byListeria monocytogenes is regulated by the bacterial growth state temperature and the pleiotropic, activator, prfA.Mol. Microbiol. 9, 931–941 (1993).
Dramsi S., Biswas I., Maguin E., Braun L., Mastroeni P., Cossart P.: Entry ofL. monocytogenes into hepatocytes requires expression of InlB, a surface protein of the internalin multigenefamily.Mol. Microbiol. 16, 251–261 (1995).
Finlay B.B., Cossart P.: Exploitation of mammalian host cell functions by bacterial pathogens.Science 276, 718–725 (1997).
Finlay B.B., Falkow S.: Common themes in microbial pathogenicity. II.Microbiol. Mol. Biol. Rev. 61, 136–169 (1997).
Friederich E., Gouin E., Hellio R., Kocks C., Cossart P., Louvard D.: Targeting ofListeria monocytogenes ActA protein to the plasma membrane as a tool to dissect both actin-based cell morphogenesis and ActA function.EMBO J. 14, 2731–2744 (1995).
Gaillard J.L., Berche P., Mounier J., Richard S., Sansonetti P.J.:In vitro model of penetration and intracellular growth ofL. monocytogenes in the human enterocyle-like cell line Caco-2.Infect. Immun. 55, 2822–2829 (1987).
Gaillard J.-L., Berche P., Frehel C., Gouin, E., Cossart P.: Entry ofL. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent, of surface antigens from gram-positive cocci.Cell 65, 1127–1141 (1991).
Gaillard J.L., Finlay B.B.: Effect of cell polarization and differentiation on entry ofListeria monocytogenes into enterocyte-like Caco-2 cell line.Infect. Immun.,64, 1299–1308 (1996).
Golsteyn R.M., Beckerle M., Koay T., Friederich E.: Structural and functional similarities between the human cytoskeletal protein zyxin and the ActA protein ofListeria monocytogenes.J. Cell Sci. 110, 1893–1906 (1997).
Ireton K., Cossart P.: Host pathogen interactions during entry and actin-based movement ofListeria monocytogenes.Ann. Rev. Genet. 31, 113–138 (1997).
Ireton K., Payrastre B., Chap H., Ogawa W., Sakaue H., Kasuga M., Cossart P.: A role for phosphoinositide 3-kinase in bacterial invasion.Science 274, 780–782 (1996).
Kocks C., Gouin E., Tabouret M., Berche P., Ohayon H., Cossart P.:Listeria monocytogenes-induced actin assembly requires theactA gene product, a surface protein.Cell 68, 521–531 (1992).
Kocks C., Hellio R., Gounon P., Ohayon H., Cossart P.: Polarized distribution ofListeria monocytogenes surface protein ActA at the site of directional actin assembly.J. Cell Sci.,105, 699–710 (1993).
Kocks C., Marchand J.B., Gouin E., D'Hauteville H., Sansonetti P.J., Carlier M.F., Cossart P.: The unrelated surface proteins ActA ofListeria monocytogenes and IcsA ofShigella flexneri are sufficient to confer actin-based motility toL. innocua andE. coli, respectively.Mol. Microbiol.,18, 413–423 (1995).
Lasa I., Cossart P.: Actin-based motility: towards a definition of the minimal requirements.Trends Cell Biol. 6, 109–114 (1996).
Lasa I., David V., Gouin E., Marchand J., Cossart P.: The amino-terminal part of ActA is critical for the actin based motility ofListeria monocytogenes; the central proline-rich region acts as a stimulator.Mol. Microbiol. 18, 425–436 (1995).
Lasa I., Gouin E., Goethals M., Vancompernolle K., David V., Vandekerckhove J., Cossart C.: Identification of two regions in the amino-terminal domain of ActA involved in the actin comet tail formation byListeria monocytogenes.EMBO J. 16, 1531–1540 (1997).
Lasa I., Dehoux P., Cossart P.: Bacterial actin-based motility.Biochim. Biophys. Acta, in press (1997).
Lebrun M., Mengaud J., Ohayon H., Nato F., Cossart P.: Internalin must be on the bacterial surface to mediate entry ofListeria monocytogenes into epithelial cells.Mol. Microbiol. 21, 579–592 (1996).
Lecuit M., Ohayon H., Braun L., Mengaud C.P.: Internalin ofListeria monocytogenes with an intact leucine-rich repeat region is sufficient to promote internalization.Infect. Immun. 65, 5309–5319 (1997).
Marchand J.B., Moreau P., Paoletti A., Cossart P., Carlier M.F., Pantaloni D.: Actin-based movement ofListeria monocytogenes inXenopus egg extracts is due to local uncapping of the barbed ends of actin filaments at the bacterial surface and resulting shift in steady state of actin assembly.J. Cell Biol. 130, 331–343 (1995).
Mengaud J., Lecuit M., Lebrun M., Nato F., Mazié J.C., Cossart P.: Antibodies to the leucine-rich repeat region of internalin block entry ofListeria monocytogenes into cells expressing E-cadherin.Infect. Immun. 64, 5430–5433 (1996).
Mengaud J., Ohayon H., Gounon P., Mége R.M., Cossart P.: E-cadherin is the receptor for internalin, a surface protein required for entry ofListeria monocytogenes into epithelial cells.Cell 84, 923–932 (1996).
Mourrain P., Lasa L., Gautreau A., Gouin E., Pugsley A., Cossart P.: ActA is a dimer.Proc. Nat. Acad. Sci. USA 94, 10034–10039 (1997).
Niebuhr K., Ebel F., Frank R., Reinhard M., Domann E. D. C.U., Walter U., Gertler F.B., Wehland J., Chakraborty T.: A novel proline-rich motif present in ActA ofListeria monocytogenes and cytoskeletal proteins is the ligand for the EVHl domain, a protein module present in the Ena/VASP family.EMBO J. 16, 5433–5444 (1997).
Pistor S., Chakraborty T., Niebuhr K., Domann E., Wehland J.: The ActA protein ofL. monocytogenes acts as a nucleator inducing reorganization of the actin cytoskeleton.EMBO J. 13, 758–763 (1994).
Renzoni A., Klarsfeld A., Dramsi S., Cossart P.: Evidence that PrfA, the pleiotropic activator of virulence genes inListeria monocytogenes, can be present but inactive.Infect. Immun. 65, 1515–1518 (1997).
Tang P., Rosenshine I., Finlay B.B.:Listeria monocytogenes, an invasive bacterium, stimulates MAP kinase upon attachment to epithelials cells.Mol. Biol. Cell. 5, 455–464 (1994).
Theriot J.A., Rosenblatt J., Portnoy D.A., Goldschmidt-Clermont P.J., Mitchison T.J.: Involvement of profilin in the actin-based motility ofL. monocytogenes in cells and in cell-free extracts.Cell 76, 505–517 (1994).
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).
Tran Van Nhieu G., Isberg R.: Bacterial internalization mediated by β1, chain integrins is determined by ligand affinity and receptor density.EMBO J. 12, 1887–1895 (1993).
Velge P., Bottreau E., Kaeffer B., Yurdusev N., Pardon P., Van Langendonck N.: Protein tyrosine kinase inhibitors block the entries ofListeria monocytogenes andListeria ivanovii into epithelial cells.Microbial Path.,17, 37–50 (1994).
Welch M.D., Iwamatsu A., Mitchison T.J.: Actin polymerization is induced by Arp2/3 protein complex at the surface ofListeria monocytogenes.Nature 385, 265–269 (1997).
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Cossart, P. Interactions of the bacterial pathogenListeria monocytogenes with mammalian cells: Bacterial factors, cellular ligands, and signaling. Folia Microbiol 43, 291–303 (1998). https://doi.org/10.1007/BF02818615
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DOI: https://doi.org/10.1007/BF02818615