Interaction between the protein InlB of Listeria monocytogenes and lipoteichoic acid: A novel mechanism of protein association at the surface of Gram-positive bacteria

Molecular Microbiology

Volumn 34, Issue 5, 1999, Pages 902-914

  Jonquières, Renaud ^a   Bierne, Hélène ^a   Fiedler, Franz ^b   Gounon, Pierre ^a   Cossart, Pascale ^a  

^a INSTITUT PASTEUR   (France)

^b Inst fur Genetik und Mikrobiologie   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; LIPOTEICHOIC ACID; POLYPEPTIDE;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL INFECTION; BACTERIAL MEMBRANE; CELL ADHESION; CELL WALL; CONTROLLED STUDY; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HOST CELL; IMMUNOFLUORESCENCE; LISTERIA MONOCYTOGENES; MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION;

BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES; MAMMALIA; NEGIBACTERIA; POSIBACTERIA;

EID: 0033404562     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1999.01652.x     Document Type: Article

References (57)

1. Alvarez-Dominguez, C., Vasquez-Boland, J.A., Carrasco-Marin, E., Lopez-Mato, P., and Leyva-Cobain, F. (1997) Host cell heparan sulfate proteoglycans mediate attachment and entry of Listeria monocytogenes, and the listerial surface protein ActA is involved in heparan sulfate receptor recognition. Infect Immun 65: 78-88.
2. Baba, T., and Schneewind, O. (1996) Target cell specificity of a bacteriocin molecule: a C-terminal signal directs lysostaphin to the cell wall of Staphylococcus aureus. EMBO J 15: 4789-4797.
3. Baba, T., and Schneewind, O. (1998) Targeting of muralytic enzymes to the cell division site of Gram-positive bacteria: repeat domains direct autolysin to the equatorial surface ring of Staphylococcus aureus. EMBO J 17: 4639-4646.
4. Barreau, C., Bimet, F., Kiredjian, M., Rouillon, N., and Bizet, C. (1993) Comparative chemotaxonomic studies of mycolic acid-free coryneform bacteria of human origin. J Clin Microbiol 31: 2085-2090.
5. Braun, L, Dramsi, S., Dehoux, P., Bierne, H., Lindahl, G., and Cossart, P. (1997) InIB: an invasion protein of Listeria monocytogenes with a novel type of surface association. Mol Microbiol 25: 285-294.
6. Braun, L., Ohayon, H., and Cossart, P. (1998) The InIB protein of Listeria monocytogenes is sufficient to promote entry into mammalian cells. Mol Microbiol 27: 1077-1087.
7. Braun, L., Nato, F., Payrastre, B., Mazié, J.-C., and Cossart, P. (1999) The 213-amino acid LRR region of Listeria monocytogenes InIB protein is sufficient for entry into mammalian cells, stimulation of PI-3 kinase, and membrane ruffling. Mol Microbiol 34: 10-23.
8. Briese, T., and Hakenbeck, R. (1985) Interaction of the pneumococcal amidase with lipoteichoic acid and choline. Eur J Biochem 146: 417-427.
9. Cossart, P., and Lecuit, M. (1998) Interactions of Listeria monocytogenes with mammalian cells during entry and actin-based movement: bacterial factors, cellular ligands and signaling. EMBO J 17: 3797-3806.
10. Courtney, H.S., Simpson, W.A., and Beachey, E.H. (1983) Binding of streptococcal lipoteichoic acid to fatty acid-binding sites on human plasma fibronectin. J Bacteriol 153: 763-770.
11. De Jonge, B.L., Chang, Y.S., Gage, D., and Tomasz, A. (1992) Peptidoglycan composition of a highly methicillin-resistant Staphylococcus aureus strain. The role of penicillin binding protein 2A. J Biol Chem 267: 11248-11254.
12. Domann, E., Wehland, J., Rohde, M., Pistor, S., Hartl, M., Goebel, W., et al. (1992) A novel bacterial gene in Listeria monocytogenes required for host cell microfilament inter-action with homology to the proline-rich region of vinculin. EMBO J 11: 1981-1990.
13. Dramsi, S., Biswas, I., Maguin, E., Braun, L., Mastroeni, P., and Cossart, P. (1995) Entry of L. monocytogenes into hepatocytes requires expression of InIB, a surface protein of the internalin multigene family. Mol Microbiol 16: 251-261.
14. Dramsi, S., Dehoux, P., Lebrun, M., Goossens, P.L., and Cossart, P. (1997) Identification of four new members of the internalin multigene family of Listeria monocytogenes EGD. Infect Immun 65: 1615-1625.
15. Dunne, D.W., Resnick, D., Greenberg, J., Krieger, M., and Joiner, K.A. (1994) The type I macrophage scavenger receptor binds to Gram-positive bacteria and recognizes lipoteichoic acid. Proc Natl Acad Sci USA 91: 1863-1867.
16. Fiedler, F. (1988) Biochemistry of the cell surface of Listeria strains: a locating general view. Infection 16: 92-97.
17. Finlay, B.B., and Cossart, P. (1997) Exploitation of mammalian host cell functions by bacterial pathogens. Science 276: 718-725.
18. Fischer, W., Rosel, P., and Koch, H.U. (1981) Effect of alanine ester substitution and other structural features of lipoteichoic acids on their inhibitory activity against autolysins of Staphylococcus aureus. J Bacteriol 146: 467-475.
19. Fischetti, V.A., Pancholi, V., and Schneewind, O. (1990) Conservation of a hexapeptide sequence in the anchor region of surface proteins from Gram-positive cocci. Mol Microbiol 4: 1603-1605.
20. Gaillard, J.-L., Berche, P., Frehel, C., Gouin, E., and Cossart, P. (1991) Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from Gram-positive cocci. Cell 65: 1127-1141.
21. Garcia, J.L., Sanchez-Beato, A.R., Medrano, F.J., and Lopez, R. (1998) Versatility of choline-binding domain. Microb Drug Res 4: 25-36.
22. Gray, M.L., and Killinger, A.H. (1966) Listeria monocytogenes and listeric infections. Bact Rev 30: 309-382.
23. Grossman, A.D., and Losick, R. (1988) Extracellular control of spore formation in Bacillus Subtilis. Proc Natl Acad Sci USA 85: 4369-4373.
24. Guyer, M.S., Reed, R.R., Steitz, J.A., and Low, K.B. (1981) Identification of a sex-factor-affinity site in E. Coli as γδ. Cold Spring Harbor Symp Quant Biol45: 135-140.
25. Harwood, C.R., Cutting, S.M. et al. (1990) In Molecular Biological Methods for Bacillus. Harwood, C.R., and Cutting, S.M. (eds). John Wiley and Sons Ltd, p. 378.
26. Hauf, N., Goebel, W., Fiedler, F., Sokolovic, Z., and Kuhn, M. (1997) Listeria monocytogenes infection of P388D1 macrophages results in a biphasic NF-kappaB (RelA/ p50) activation induced by lipoteichoic acid and bacterial phospholipases and mediated by IkappaBα and IkappaBβ degradation. Proc Natl Acad Sci USA 94: 9394-9399.
27. Hess, J., Dreher, A., Gentschev, I., Goebel, W., Ladel, C., Miko, D., and Kaufmann, S.H. (1996) Protein p60 participates in intestinal host invasion by Listeria monocytogenes. Zentralbl Bakteriol 284: 263-272.
28. Höltje, J.V., and Tomasz, A. (1975) Lipoteichoic acid: a specific inhibitor of autolysin activity in Pneumococcus. Proc Natl Acad Sci USA 72: 1690-1694.
29. Horne, D., and Tomasz, A. (1985) Pneumococcal Forssman antigen: enrichment in mesosomal membranes and specific binding to the autolytic enzyme of Streptococcus pneumoniae. J Bacteriol 161: 18-24.
30. Ireton, K., and Cossart, P. (1997) Host pathogen interactions during entry and actin-based movement of Listeria monocytogenes. Annu Rev Genet 31: 113-138.
31. Ireton, K., Payrastre, B., Chap, H., Ogawa, W., Sakaue, H., Kasuga, M., and Cossart, P. (1996) A role for phosphoinositide 3-kinase in bacterial invasion [published erratum appears in Science 1997 Jan 24; 275 (5299): 464]. Science 274: 780-782.
32. Ireton, K., Payrastre, B., and Cossart, P. (1999) The Listeria monocytogenes protein InIB is an agonist of mammalian phosphoinositide 3-kinase. J Biol Chem 274:17025-17032.
33. Jonquières, R., Bierne, H., Mengaud, J., and Cossart, P. (1998) The inIA gene of Listeria monocytogenes LO28 harbors a nonsense mutation resulting in release of internalin. Infect Immun 66: 3420-3422.
34. Kocks, C., Gouin, E., Tabouret, M., Berche, P., Ohayon, H., and Cossart, P. (1992) Listeria monocyfogenes-induced actin assembly requires the actA gene product, a surface protein. Cell 68: 521-531.
35. Lebrun, M., Mengaud, J., Ohayon, H., Nato, F., and Cossart, P. (1996) Internalin must be on the bacterial surface to mediate entry of Listeria monocytogenes into epithelial cells. Mol Microbiol 21: 579-592.
36. Lecuit, M., Ohayon, H., Braun, L., Mengaud, J., and Cossart, P. (1997) Internalin of Listeria monocytogenes with an intact leucine-rich repeat region is sufficient to promote internalization. Infect Immun 65: 5309-5319.
37. Lecuit, M., Dramsi, S., Gottardi, C., Fredor-Chaiken, M., Gumbiner, B., and Cossart, P. (1999) A single amino acid in E-cadherin responsible for host specificity toward human pathogen Listeria monocytogenes. EMBO J 18: 3956-3963.
38. Lingnau, A., Domann, E., Hudel, M., Bock, M., Nichterlein, T., Wehland, J., and Chakraborty, T. (1995) Expression of the Listeria monocytogenes EGD inIA and inIB genes, whose products mediate bacterial entry into tissue culture cell lines, by PrfA-dependent and independent mechanisms. Infect Immun 63: 3896-3903.
39. Loos, M., Clas, F., and Fischer, W. (1986) Interaction of purified lipoteichoic acid with the classical complement pathway. Infect Immun 53: 595-599.
40. Mackaness, G.B. (1962) Cellular resistance to infection. J Exp Med 116: 381-406.
41. McLaughlan, A.M., and Foster, S.J. (1998) Molecular characterization of an autolytic amidase of Listeria monocytogenes EGD. Microbiology 144: 1359-1367.
42. Mengaud, J., Ohayon, H., Gounon, P., Mège, R.M., and Cossart, P. (1996a) E-cadherin is the receptor for internalin, a surface protein required for entry of Listeria monocytogenes into epithelial cells. Cell 84: 923-932.
43. Mengaud, J., Lecuit, M., Lebrun, M., Nato, F., Mazié, J.C., and Cossart, P. (1996b) Antibodies to the Leucine-Rich Repeat region of Internalin block entry of Listeria monocytogenes into cells expressing E-Cadherin. Infect Immun 64: 5430-5433.
44. Mesnage, S., Tosi-Couture, E., and Fouet, A. (1999) Production and cell surface anchoring of functional fusions between the SLH motifs of the Bacillus anthracis S-layer proteins and the Bacillus subtilis levansucrase. Mol Microbiol 31: 927-936.
45. Müller, S., Hain, T., Pashalidis, P., Lingnau, A., Domann, E., Chakraborty, T., and Wehland, J. (1998) Purification of the inIB gene product of Listeria monocytogenes and demonstration of its biological activity. Infect Immun 66: 3128-3133.
46. Navarre, W.W., and Schneewind, O. (1994) Proteolytic cleavage and cell wall anchoring at the LPXTGX motif of surface proteins in Gram-positive bacteria. Mol Microbiol 14: 115-121.
47. Navarre, W.W., and Schneewind, O. (1999) Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 63: 174-229.
48. Piard, J.C., Hautefort, I., Fischetti, V.A., Ehrlich, S.D., Fons, M., and Gruss, A. (1997) Cell wall anchoring of the Streptococcus pyogenes M6 protein in various lactic acid bacteria. J Bacteriol 179: 3068-3072.
49. Raffelsbauer, D., Bubert, A., Engelbrecht, F., Scheinpflug, J., Simm, A., Hess, J., et al. (1998) The gene cluster inIC2DE of Listeria monocytogenes contains additional new internalin genes and is important for virulence in mice. Mol Gen Genet 260: 144-158.
50. Rosenow, C., Ryan, P., Weiser, J.N., Johnson, S., Fontan, P., Ortqvist, A., and Masure, H.R. (1997) Contribution of novel choline-binding proteins to adherence, colonization and immunogenicity of Streptococcus pneumoniae. Mol Microbiol 25: 819-829.
51. Ruhland, G.J., and Fiedler, F. (1987) Occurrence and biochemistry of lipoteichoic acids in the genus Listeria. System Appl Microbiol 9: 40-46.
52. Schneewind, O., Model, P., and Fischetti, V.A. (1992) Sorting of protein A to the staphylococcal cell wall. Cell 70: 267-281.
53. Schneewind, O., Mihaylova-Petkov, D., and Model, P. (1993) Cell wall sorting signals in surface proteins of Gram positive bacteria. EMBO J 12: 4803-4811.
54. Tan, P., Chapot-Chartier, M.-P., Pos, K.M., Rousseau, M., Boquien, C.-Y., Gripon, J.-C., and Konings, W.N. (1992) Localisation of peptidase in Lactococci. Appl Environ Microbiol 58: 285-290.
55. Thumm, G., and Gotz, F. (1997) Studies on prolysostaphin processing and characterization of the lysostaphin immunity factor (Lif) of Staphylococcus simulans biovar staphylolyticus. Mol Microbiol 23: 1251-1265.
56. Van Driel, D., Wicken, A.J., Dickson, M.R., and Knox, K.W. (1973) Cellular location of the lipoteichoic acids of Lactobacillus fermenti NCTC 6991 and Lactobacillus casei NCTC 6375. J Ultrastruct Res 43: 483-497.
57. Yother, J., and White, J. (1994) Novel Surface Attachment Mechanism of the Streptococcus pneumoniae Protein PspA. J Bacteriol 176: 2976-2985.