Multiple point mutations in virulence genes explain the low virulence of Listeria monocytogenes field strains

Microbiology

Volumn 154, Issue 3, 2008, Pages 939-948

  Temoin S ^a   Roche, Sylvie M ^a   Grepinet O ^a   Fardini, Y ^a   Velge, P ^a  

^a UR1282   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; BACTERIAL PROTEIN; INTERNALIN A; INTERNALIN B; LEUCINE; PHOSPHATIDYLINOSITOL DIACYLGLYCEROL LYASE; SCATTER FACTOR RECEPTOR; THREONINE; BACTERIAL DNA; INLB PROTEIN, LISTERIA MONOCYTOGENES; INTERNALIN PROTEIN, BACTERIA; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE PHOSPHODIESTERASE; VIRULENCE FACTOR;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELL INVASION; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME DEGRADATION; EPITHELIUM CELL; FIBROBLAST; GENETIC COMPLEMENTATION; GENETIC CONSERVATION; HUMAN; HUMAN CELL; IN VIVO STUDY; LISTERIA MONOCYTOGENES; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; STOP CODON; ANIMAL; BACTERIAL COUNT; CELL LINE; CERCOPITHECUS; CHEMISTRY; DNA SEQUENCE; GENETICS; ISOLATION AND PURIFICATION; LISTERIOSIS; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PATHOGENICITY; SPLEEN; VIRULENCE;

LISTERIA MONOCYTOGENES;

AMINO ACID SUBSTITUTION; ANIMALS; BACTERIAL PROTEINS; CELL LINE; CERCOPITHECUS AETHIOPS; CODON, NONSENSE; COLONY COUNT, MICROBIAL; DNA, BACTERIAL; EPITHELIAL CELLS; FIBROBLASTS; GENETIC COMPLEMENTATION TEST; HUMANS; LISTERIA INFECTIONS; LISTERIA MONOCYTOGENES; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; PHOSPHOINOSITIDE PHOSPHOLIPASE C; POINT MUTATION; SEQUENCE ANALYSIS, DNA; SPLEEN; VIRULENCE; VIRULENCE FACTORS;

EID: 42949111248     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.2007/011106-0     Document Type: Article

References (38)

1. Alberti-Segui, C., Goeden, K. R. & Higgins, D. E. (2007). Differential function of Listeria monocytogenes listeriolysin O and phospholipases C in vacuolar dissolution following cell-to-cell spread. Cell Microbiol 9, 179-195.
2. Arnaud, M., Chastanet, A. & Debarbouille, M. (2004). New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, Gram-positive bacteria. Appl Environ Microbiol 70, 6887-6891.
3. Autret, N., Raynaud, C., Dubail, I., Berche, P. & Charbit, A. (2003). Identification of the agr locus of Listeria monocytogenes: role in bacterial virulence. Infect Immun 71, 4463-4471.
4. Bannam, T. & Goldfine, H. (1999). Mutagenesis of active-site histidines of Listeria monocytogenes phosphatidylinositol-specific phospholipase C: effects on enzyme activity and biological function. Infect Immun 67, 182-186.
5. Braun, L., Nato, F., Payrastre, B., Mazie, J. C. & 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.
6. Braun, L., Ghebrehiwet, B. & Cossart, P. (2000). gClq-R/p32, a Clq-binding protein, is a receptor for the InlB invasion protein of Listeria monocytogenes. EMBO J 19, 1458-1466.
7. Cossart, P., Vicente, M. F., Mengaud, J., Baquero, F., Perez-Diaz, J. C. & Berche, P. (1989). Listeriolysin O is essential for virulence of Listeria monocytogenes: direct evidence obtained by gene complementation. Infect Immun 57, 3629-3636.
8. Doumith, M., Cazalet, C., Simoes, N., Frangeul, L., Jacquet, C., Kunst, F., Martin, P., Cossart, P., Glaser, P. & Buchrieser, C. (2004). New aspects regarding evolution and virulence of Listeria monocytogenes revealed by comparative genomics and DNA arrays. Infect Immun 72, 1072-1083.
9. Dramsi, S., Biswas, I., Maguid, E., Braun, L., Mastroeni, P. & 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.
10. Felicio, M. T., Hogg, T., Gibbs, P., Teixeira, P. & Wiedmann, M. (2007). Recurrent and sporadic Listeria monocytogenes contamination in alheiras represents considerable diversity, including virulence-attenuated isolates. Appl Environ Microbiol 73, 3887-3895.
11. Gaillard, J. L., Berche, P. & Sansonetti, P. (1986). Transposon mutagenesis as a tool to study the role of hemolysin in the virulence of Listeria monocytogenes. Infect Immun 52, 50-55.
12. Gaillard, J. L., Berche, P., Frehel, C, Gouin, E. & 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.
13. Gracieux, P., Roche, S. M., Pardon, P. & Velge, P. (2003). Hypovirulent Listeria monocytogenes strains are less frequently recovered than virulent strains on PALCAM and Rapid L. mono media. Int J Food Microbiol 83, 133-145.
14. Handa-Miya, S., Kimura, B., Takahashi, H., Sato, M., Ishikawa, T., Igarashi, K. & Fujii, T. (2007). Nonsense-mutated inlA and prfA not widely distributed in Listeria monocytogenes isolates from ready-to-eat seafood products in Japan. Int J Food Microbiol 117, 312-318.
15. Jacquet, C., Dournith, M, Gordon, J. I., Martin, P. M., Cossart, P. & Lecuit, M. (2004). A molecular marker for evaluating the pathogenic potential of foodborne Listeria monocytogenes. J Infect Dis 189, 2094-2100.
16. Jonquieres, R., Bierne, H., Mengaud, J. & Cossart, P. (1998). The inlA gene of Listeria monocytogenes LO28 harbors a nonsense mutation resulting in release of internalin. Infect Immun 66, 3420-3422.
17. Jonquieres, R., Pizarro-Cerda, J. & Cossart, P. (2001). Synergy between the N- and C-terminal domains of InlB for efficient invasion of non-phagocytic cells by Listeria monocytogenes. Mol Microbiol 42, 955-965.
18. Kathariou, S., Metz, P., Hof, H. & Goebel, W. (1987). Tn916-induced mutations in the hemolysin determinant affecting virulence of Listeria monocytogenes. J Bacteriol 169, 1291-1297.
19. Lecuit, M., Ohayon, H., Braun, L., Mengaud, J. & Cossart, P. (1997). Internalin of Listeria monocytogenes with an intact leucine-rich repeat region is sufficient to promote internalization. Infect Immun 65, 5309-5319.
20. Lecuit, M., Dramsi, S., Gottardi, C., Fedor-Chaiken, M., Gumbiner, B. & Cossart, P. (1999). A single amino acid in E-cadberin responsible for host specificity towards the human pathogen Listeria monocytogenes. EMBO J 118, 3956-3963.
21. Lereclus, D. & Arantes, O. (1992). spbA locus ensures the segregational stability of pTH1030, a novel type of Gram-positive replicon. Mol Microbiol 6, 35-46.
22. Moser, J., Gerstel, B., Meyer, J. E., Chakraborty, T., Wehland, J. & Heinz, D. W. (1997). Crystal structure of the phosphatidylinositol-specific phospholipase C from the human pathogen Listeria monocytogenes. J Mol Biol 273, 269-282.
23. Nightingale, K. K., Windham, K., Martin, K. E., Yeung, M. & Wiedmann, M. (2005). Select Listeria monocytogenes subtypes commonly found in foods carry distinct nonsense mutations in inlA, leading to expression of truncated and secreted internalin A, and are associated with a reduced invasion phenotype for human intestinal epithelial cells. Appl Environ Microbiol 71, 8764-8772.
24. Norrung, B. & Andersen, J. K. (2000). Variations in virulence between different electrophoretic types of Listeria monocytogenes. Lett Appl Microbiol 30, 228-232.
25. Notermans, S. H., Dufrenne, J., Leimeister-Wachter, M., Domann, E. & Chakraborty, T. (1991). Phosphatidylinositol-specific phospholipase C activity as a marker to distinguish between pathogenic and nonpathogenic Listeria species. Appl Environ Microbiol 57, 2666-2670.
26. Olier, M., Pierre, F., Rousseaux, S., Lemaitre, J. P., Rousset, A., Piveteau, P. & Guzzo, J. (2003). Expression of truncated internalin A is involved in impaired internalization of some Listeria monocytogenes isolates carried asymptomatically by humans. Infect Immun 71, 1217-1224.
27. Oiler, M., Garmyn, D., Rousseaux, S., Lemaitre, J. P., Piveteau, P. & Guzzo, J. (2005). Truncated internalin A and asymptomatic Listeria monocytogenes carriage: in vivo investigation by allelic exchange. Infect Immun 73, 644-648.
28. Park S. F. & Stewart, G. S. (1990). High-efficiency transformation of Listeria monocytogenes by electroporation of penicillin-treated cells. Gene 94, 129-132.
29. Roche, S. M., Velge, P., Bottreau, E., Durier, C., Marquet-van der Mee, N. & Pardon, P. (2001). Assessment of the virulence of Listeria monocytogenes: agreement between a plaque-forming assay with HT-29 cells and infection of immunocompetent mice. Int J Food Microbiol 68, 33-44.
30. Roche, S. M., Gracieux, P., Albert I., Gouali, M., Jacquet, C., Martin, P. M. & Velge, P. (2003). Experimental validation of low virulence in field strains of Listeria monocytogenes. Infect Immun 71, 3429-3436.
31. Roche, S. M., Gracieux, P., Milohanic, E., Albert I., Virlogeuz-Payant, I., Témoin, S., Grépinet, O., Kerouanton, A., Jacquet C. & other authors (2005). Investigation of specific substitutions in virulence genes characterizing phenotypic groups of low-virulence field strains of Listeria monocytogenes. Appl Environ Microbiol 71, 6039-6048.
32. Sabet, C., Lecuit, M., Cabanas, D., Cossart, P. & Bierne, H. (2005). LPXTG protein InlJ, a newly identified internalin involved in Listeria monocytogenes virulence. Infect Immun 73, 6912-6922.
33. Shen, Y., Naujokas, M., Park M. & Ireton, K. (2000). InlB-dependent internalization of Listeria is mediated by the Met receptor tyrosine kinase. Cell 103, 501-510.
34. Tabouret, M., De Rycke, J., Audurier, A. & Poutrel, B. (1991). Pathogenicity of Listefia monocytogenes isolates in immunocompromised mice in relation to listeriolysin production. J Med Microbiol 34, 13-18.
35. Van Langendonck, N., Bottreau, E., Bailly, S., Tabouret, M., Marty, J., Pardon, P. & Velge, P. (1998). Tissue culture assays using Caco-2 cell line differentiate virulent from non-virulent Listeria monocytogenes strains. J Appl Microbiol 85, 337-346.
36. Vazquez-Boland, J. A., Kocks, C., Dramsi, S., Ohayon, H., Geoffroy, C., Mengaud, J. & Cossart, P. (1992). Nucleotide sequence of the lecithinase operon of Listeria monocytogenes and possible role of lecithinase in cell-to-cell spread. Infect Immun 60, 219-230.
37. Velge, P., Bottreau, E., Van-Langendonck, N. & Kaeffer, B. (1997). Cell proliferation enhances entry of Listeria monocytogenes into intestinal epithelial cells by two proliferation-dependent entry pathways. J Med Microbiol 46, 681-692.
38. Velge, P., Herler, M., Johansson, J., Roche, S, M., Témoin, S., Fedorov, A. A., Gracieux, P., Almo, S. C., Goebel, W. & Cossart, P. (2007). A naturally occurring mutation K220T in the pleiotropic activator PrfA of Listeria monocytogenes results in a loss of virulence due to decreasing DNA-binding affinity. Microbiology 153, 995-1005.