Auto, a surface associated autolysin of Listeria monocytogenes required for entry into eukaryotic cells and virulence

Molecular Microbiology

Volumn 51, Issue 6, 2004, Pages 1601-1614

  Cabanes, Didier ^a   Dussurget, Olivier ^a   Dehoux, Pierre ^a   Cossart, Pascale ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOLYSIN; BACTERIAL PROTEIN; GENE PRODUCT;

AMINO ACID SEQUENCE; ANIMAL MODEL; ARTICLE; BACTERIAL CELL WALL; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERIUM MUTANT; DELETION MUTANT; DNA SEQUENCE; GENE EXPRESSION; GENOMICS; GUINEA PIG; LISTERIA; LISTERIA MONOCYTOGENES; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL ADHESION; BACTERIAL PROTEINS; BRAIN; CELL LINE; EUKARYOTIC CELLS; FEMALE; GUINEA PIGS; HUMANS; INTESTINES; LISTERIA INFECTIONS; LISTERIA MONOCYTOGENES; LIVER; LYMPH NODES; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; N-ACETYLMURAMOYL-L-ALANINE AMIDASE; SPLEEN; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); CAVIA; CAVIA PORCELLUS; EUKARYOTA; LISTERIA INNOCUA; LISTERIA MONOCYTOGENES; NEGIBACTERIA; SUS SCROFA;

EID: 1642442774     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2003.03945.x     Document Type: Article

References (58)

1. Allignet, J., Aubert, S., Dyke, K.G., and El Solh, N. (2001) Staphylococcus caprae strains carry determinants known to be involved in pathogenicity: a gene encoding an autolysin-binding fibronectin and the ica operon involved in biofilm formation. Infect Immun 69: 712-718.
2. 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.
3. Blackman, S.A., Smith, T.J., and Foster, S.J. (1998) The role of autolysins during vegetative growth of Bacillus subtilis 168. Microbiology 144: 73-82.
4. Bockmann, R., Dickneite, C., Goebel, W., and Bohne, J. (2000) PrfA mediates specific binding of RNA polymerase of Listeria monocytogenes to PrfA-dependent virulence gene promoters resulting in a transcriptionally active complex. Mol Microbiol 36: 487-497.
5. Borezee, E., Pellegrini, E., Beretti, J.L., and Berche, P. (2001) SvpA, a novel surface virulence-associated protein required for intracellular survival of Listeria monocytogenes. Microbiology 147: 2913-2923.
6. Braun, L., Dramsi, S., Dehoux, P., Bierne, H., Lindahl, G., and Cossart, P. (1997) InlB: an invasion protein of Listeria monocytogenes with a novel type of surface association. Mol Microbio 25: 285-294.
7. Braun, L., Ohayon, H., and Cossart, P. (1998) The InlB protein of Listeria monocytogenes is sufficient to promote entry into mammalian cells. Mol Microbiol 27: 1077-1087.
8. Braun, L., Nato, F., Payrastre, B., Mazie, J.C., and Cossart, P. (1999) The 213-amino-acid leucine-rich repeat region of the Listeria monocytogenes InlB protein is sufficient for entry into mammalian cells, stimulation of PI 3-kinase and membrane ruffling. Mol Microbiol 34: 10-23.
9. Braun, L., Ghebrehiwet, B., and Cossart, P. (2000) gC1q-R/p32, a C1q-binding protein, is a receptor for the InlB invasion protein of Listeria monocytogenes. EMBO J 19: 1458-1466.
10. Cabanes, D., Dehoux, P., Dussurget, O., Frangeul, L., and Cossart, P. (2002) Surface proteins and the pathogenic potential of Listeria monocytogenes. Trends Microbiol 10: 238-245.
11. Cossart, P. (2000) Actin-based motility of pathogens: the Arp2/3 complex is a central player. Cell Microbiol 2: 195-205.
12. Cossart, P., and Bierne, H. (2001) The use of host cell machinery in the pathogenesis of Listeria monocytogenes. Curr Opin Immunol 13: 96-103.
13. 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.
14. Doumith, M., Cazalet, C., Simoes, N., Frangeul, L., Jacquet, C., Kunst, F., et al. (2004) New aspects regarding evolution and virulence of Listeria monocytogenes revealed by comparative genomics. Infect Immun 72:
15. Dramsi, S., Biswas, I., Maguin, E., Braun, L., Mastroeni, P., and Cossart, P. (1995) Entry of Listeria monocytogenes into hepatocytes requires expression of inlB, a surface protein of the internalin multigene family. Mol Microbiol 16: 251-261.
16. Dussurget, O., Cabanes, D., Dehoux, P., Lecuit, M., Buchrieser, C., Glaser, P., and Cossart, P. (2002) 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.
17. Gaillard, J.L., Berche, P., Frehel, C., Gouin, E., and Cossart, P. (1991) Entry of Listeria monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from Gram-positive cocci. Cell 65: 1127-1141.
18. Gaillard, J.L., Dramsi, S., Berche, P., and Cossart, P. (1994) Molecular cloning and expression of internalin in Listeria. Methods Enzymol 236: 551-565.
19. Girardin, S.E., Boneca, I.G., Carneiro, L.A., Antignac, A., Jehanno, M., Viala, J., et al. (2003a) Nod1 detects a unique muropeptide from Gram-negative bacterial peptidoglycan. Science 300: 1584-1587.
20. Girardin, S.E., Boneca, I.G., Viala, J., Chamaillard, M., Labigne, A., Thomas, G., et al. (2003b) Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem 278: 8869-8872.
21. Girardin, E., Sansonetti, P., and Philpott, D. (2002) Intracellular vs extracellular recognition of pathogens-common concepts in mammals and flies. Trends Microbiol 10: 193-199.
22. Glaser, P., Frangeul, L., Burchrieser, C., Rusniock, C., Amend, A., Baquero, F., et al. (2001) Comparative genomics of Listeria species. Science 294: 849-852.
23. Gouin, E., Dehoux, P., Mengaud, J., Kocks, C., and Cossart, P. (1995) iactA of Listeria ivanovii, although distantly related to Listeria monocytogenes actA, restores actin tail formation in an L. monocytogenes actA mutant. Infect Immun 63: 2729-2737.
24. Heilmann, C., Hussain, M., Peters, G., and Gotz, F. (1997) Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol Microbiol 24: 1013-1024.
25. Hell, W., Meyer, H.G., and Gatermann, S.G. (1998) Cloning of aas, a gene encoding a Staphylococcus saprophyticus surface protein with adhesive and autolytic properties. Mol Microbiol 29: 871-881.
26. Hof, H. (1984) Virulence of different strains of Listeria monocytogenes serovar 1/2a. Med Microbiol Immunol 173: 207-218.
27. 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. Science 274: 780-782.
28. Jonquieres, R., Bierne, H., Fiedler, F., Gounon, P., and Cossart, P. (1999) Interaction between the protein InlB of Listeria monocytogenes and lipoteichoic acid: a novel mechanism of protein association at the surface of Gram-positive bacteria. Mol Microbio 34: 902-914.
29. Joris, B., Englebert, S., Chu, C.P., Kariyama, R., Daneo-Moore, L., Shockman, G.D., and Ghuysen, J.M. (1992) Modular design of the Enterococcus hirae muramidase-2 and Streptococcus faecalis autolysin. FEMS Microbiol Lett 70: 257-264.
30. Kohler, S., Bubert, A., Vogel, M., and Goebel, W. (1991) Expression of the iap gene coding for protein p60 of Listeria monocytogenes is controlled on the posttranscriptional level. J Bacteriol 173: 4668-4674.
31. Lecuit, M., and Cossart, P. (2002) Genetically-modified-animal models for human infections: the Listeria paradigm. Trends Mol Med 8: 537-542.
32. Lecuit, M., Vandormael-Pournin, S., Lefort, J., Huerre, M., Gounon, P., Dupuy, C., et al. (2001) A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier. Science 292: 1722-1725.
33. Lingnau, A., Domann, E., Hudel, M., Bock, M., Nichterlein, T., Wehland, J., and Chakraborty, T. (1995) Expression of the Listeria monocytogenes EGD inIA and inlB genes, whose products mediate bacterial entry into tissue culture cell lines, by PrfA-dependent and - independent mechanisms. Infect Immun 63: 3896-3903.
34. McLaughlan, A.M., and Foster, S.J. (1997) Characterisation of the peptidoglycan hydrolases of Listeria monocytogenes EGD. FEMS Microbiol Lett 152: 149-154.
35. McLaughlan, A.M., and Foster, S.J. (1998) Molecular characterization of an autolytic amidase of Listeria monocytogenes EGD. Microbiology 144: 1359-1367.
36. Marino, M., Banerjee, M., Jonquieres, R., Cossart, P., and Ghosh, P. (2002) GW domains of the Listeria monocytogenes invasion protein lnlB are SH3-like and mediate binding to host ligands. EMBO J 21: 5623-5634.
37. Mengaud, J., Ohayon, H., Gounon, P., Mege, 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.
38. Mengaud, J., Lecuit, M., Lebrun, M., Nato, F., Mazie, 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.
39. Milohanic, E., Pron, B., Berche, P., and Gaillard, J.L. (2000) Identification of new loci involved in adhesion of Listeria monocytogenes to eukaryotic cells. Microbiology 146: 731-739.
40. Milohanic, E., Jonquieres, R., Cossart, P., Berche, P., and Gaillard, J.L. (2001) The autolysin Ami contributes to the adhesion of Listeria monocytogenes to eukaryotic cells via its cell wall anchor. Mol Microbiol 39: 1212-1224.
41. Milohanic, E., Glaser, P., Coppee, J.Y., Frangeul, L., Vega, Y., Vazquez-Boland, J.A., et al. (2003) Transcriptome analysis of Listeria monocytogenes identifies three groups of genes differently regulated by PrfA. Mol Microbiol 47: 1613-1625.
42. Nato, F., Reich, K., Lhopital, S., Rouyre, S., Geoffroy, C., Mazie, J.C., and Cossart, P. (1991) Production and characterization of neutralizing and nonneutralizing monoclonal antibodies against listeriolysin O. Infect Immun 59: 4641-4646.
43. 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.
44. Oshida, T., Sugai, M., Komatsuzawa, H., Hong, Y.M., Suginaka, H., and Tomasz, A. (1995) A Staphylococcus aureus autolysin that has an N-acetylmuramoyl-L-alanine amidase domain and an endo-beta-N- acetylglucosaminidase domain, cloning, sequence analysis, and characterization. Proc Natl Acad Sci USA 92: 285-289.
45. Peerschke, E.I., and Ghebrehiwet, B. (2001) Human blood platelet gC1qR/p33. Immunol Rev 180: 56-64.
46. Pilgrim, S., Kolb-Maurer, A., Gentschev, I., Goebel, W., and Kuhn, M. (2003) Deletion of the gene encoding p60 in Listeria monocytogenes leads to abnormal cell division and loss of actin-based motility. Infect Immun 71: 3473-3484.
47. Reglier-Poupet, H., Pellegrini, E., Charbit, A., and Berche, P. (2003) Identification of LpeA, a PsaA-like membrane protein that promotes cell entry by Listeria monocytogenes. Infect Immun 71: 474-482.
48. Sambrook, J.E., Fritsch, E.K., and Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual. 2nd edn. Cold Spring Harbor, N.Y: Cold Spring Harbor Laboratory.
49. Schubert, K., Bichlmaier, A.M., Mager, E., Wolff, K., Ruhland, G., and Fiedler, F. (2000) P45, an extracellular 45 kDa protein of Listeria monocytogenes with similarity to protein p60 and exhibiting peptidoglycan lytic activity. Arch Microbiol 173: 21-28.
50. Sheehan, B., Klarsfeld, A., Msadek, T., and Cossart, P. (1995) Differential activation of virulence gene expression by PrfA, the Listeria monocytogenes virulence regulator. J Bacteriol 177: 6469-6476.
51. Shen, Y., Naujokas, M., Park, M., and Ireton, K. (2000) InlB-dependent internalization of Listeria is mediated by the Met receptor tyrosine kinase. Cell 103: 501-510.
52. Smith, K., and Youngman, P. (1992) Use of a new integrational vector to investigate compartment-specific expression of the Bacillus subtilis spollM gene. Biochimie 74: 705-711.
53. Steffen, P., Schafer, D.A., David, V., Gouin, E., Cooper, J.A., and Cossart, P. (2000) Listeria monocytogenes ActA protein interacts with phosphatidylinositol 4,5-bisphosphate in vitro. Cell Motil Cytoskeleton 45: 58-66.
54. Sugai, M., Akiyama, T., Komatsuzawa, H., Miyake, Y., and Suginaka, H. (1990) Characterization of sodium dodecyl sulfate-stable Staphylococcus aureus bacteriolytic enzymes by polyacrylamide gel electrophoresis. J Bacteriol 172: 6494-6498.
55. Sun, A.N., Camilli, A., and Portnoy, D.A. (1990) Isolation of Listeria monocytogenes small-plaque mutants defective for intracellular growth and cell-to-cell spread. Infect Immun 58: 3770-3778.
56. Trieu-Cuot, P., Carlier, C., Poyart-Salmeron, C., and Courvalin, P. (1991) Shuttle vectors containing a multiple cloning site and a lacZ alpha gene for conjugal transfer of DNA from Escherichia coli to Gram-positive bacteria. Gene 102: 99-104.
57. Vazquez-Boland, J.A., Kuhn, M., Berche, P., Chakraborty, T., Dominguez-Bernal, G., Goebel, W., et al. (2001) Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14: 584-640.
58. Wuenscher, M.D., Kohler, S., Bubert, A., Gerike, U., and Goebel, W. (1993) The iap gene of Listeria monocytogenes is essential for cell viability, and its gene product, p60, has bacteriolytic activity. J Bacteriol 175: 3491-3501.