A novel cell wall-anchored peptidoglycan hydrolase (autolysin), IspC, essential for Listeria monocytogenes virulence: Genetic and proteomic analysis

Microbiology

Volumn 154, Issue 7, 2008, Pages 1900-1913

  Wang, Linru ^a,b   Lin, Min ^a,b  

^a CANADIAN FOOD INSPECTION AGENCY   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADHESIN; AUTOLYSIN; BACTERIAL PROTEIN; FLAGELLIN; HYDROLASE; MEMBRANE PROTEIN; PEPTIDOGLYCAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL CELL WALL; BACTERIAL CHROMOSOME; BACTERIAL COUNT; BACTERIAL GENETICS; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERIUM COLONY; BACTERIUM MUTANT; BIOCHEMISTRY; BLOOD CEREBROSPINAL FLUID BARRIER; BRAIN BLOOD VESSEL; BRAIN TISSUE; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CELL CULTURE; CELL DIVISION; CELL INVASION; CELL STRAIN CACO 2; CELL STRAIN HEPG2; CELL TYPE; CHOROID PLEXUS; CONTROLLED STUDY; ENDOTHELIUM CELL; EPITHELIUM CELL; EUKARYOTIC CELL; FIBROBLAST; GENE DELETION; GENE EXPRESSION; GENETIC ANALYSIS; GLYCOPROTEIN SYNTHESIS; HELA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LISTERIA MONOCYTOGENES; LIVER PARENCHYMA; MACROPHAGE; MASS SPECTROMETRY; MICROSCOPY; MICROVASCULATURE; MORPHOLOGY; MORTALITY; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEOMICS; SHEEP; VASCULAR ENDOTHELIUM; VERO CELL; WESTERN BLOTTING; WILD TYPE;

ANIMALS; BACTERIAL ADHESION; BACTERIAL PROTEINS; CELL LINE, TUMOR; CELL WALL; CERCOPITHECUS AETHIOPS; CHOROID PLEXUS; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; LISTERIA INFECTIONS; LISTERIA MONOCYTOGENES; MICE; MICE, INBRED BALB C; N-ACETYLMURAMOYL-L-ALANINE AMIDASE; PHENOTYPE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEOMICS; SEQUENCE DELETION; SHEEP; SPECIES SPECIFICITY; VERO CELLS; VIRULENCE; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); EUKARYOTA; LISTERIA MONOCYTOGENES; MUS; OVIS ARIES;

EID: 51149092565     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.2007/015172-0     Document Type: Article

References (47)

1. Allignet J., England, P., Old, I. & El Solh, N. (2002). Several regions of the repeat domain of the Staphylococcus caprae autolysin, AtlC, are involved in fibronectin binding. FEMS Microbiol Lett 213, 193-197.
2. Alvarez-Dominguez, C., Vazquez-Boland, J. A., Carrasco-Marin, E., Lopez-Mato, P. & Leyva-Cobian, 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.
3. Bergmann, B, Raffelsbauer, D., Kuhn, M, Goetz, M., Horn, S. & Goebel, W. (2002). InlA- but not InlB-mediated internalization of Listeria monocytogenes by non-phagocytic mammalian cells needs the support of other internalins. Mol Microbiol 43, 557-570.
4. Berry, A. M. & Paton, J. C. (2000). Additive attenuation of virulence of Streptococcus pneumoniae by mutation of the genes encoding pneumolysin and other putative pneumococcal virulence proteins. Infect Immun 68, 133-140.
5. Berry, A. M., Lock R. A., Hansman, D. & Paton, J. C. (1989). Contribution of autolysin to virulence of Streptococcus pneumoniae. Infect Immun 57, 2324-2330.
6. Biarne, H. & Cossart, P. (2007). Listeria monocytogenes surface proteins: from genome predictions to function. Microbiol Mol Biol Rev 71, 377-397.
7. Braun, L., Dramsi, S., Dehoux, P., Bierne, H., Lindahl, G. & Cossart, P. (1997). InlB: an invasion protein of Listeria monocytogenes with a novel type of surface association. Mol Microbiol 25, 285-294.
8. Brouwer, M. C., van de Beek D., Heckenberg, S. G., Spanjaard, L. & de Gans, J. (2006). Community-acquired Listeria monocytogenes meningitis in adults. Clin Infect Dis 43, 1233-1238.
9. Cabanes, D, Dehoux, P., Dussurget, O., Frangeul, L. & Cossart, P. (2002). Surface proteins and the pathogenic potential of Listeria monocytogenes. Trends Microbiol 10, 238-245.
10. Cabanes, D., Dussurget, O., Dehoux, P. & Cossark P. (2004). Auto, a surface associated autolysin of Listeria monocytogenes required for entry into eukaryotic cells and virulence. Mol Microbiol 51, 1601-1614.
11. Canvin, J. R., Marvin, A. P., Sivakumaran, M., Paton, J. C., Boulnois, G. J., Andrew, P. W. & Mitchell, T. J. (1995). The role of pneumolysin and autolysin in the pathology of pneumonia and septicemia in mice infected with a type 2 pneumococcus. J Infect Dis 172, 119-123.
12. Carroll, S. A., Hain, T., Technow, U., Darji, A., Pashalidis, P., Joseph, S. W. & Chakraborty, T. (2003). Identification and characterization of a peptidoglycan hydrolase, MurA, of Listeria monocytogenes, a muramidase needed for cell separation. J Bacteriol 185, 6801-6808.
13. Dons, L, Eriksson, E., Jin, Y., Rottenberg, M. E., Kristensson, K., Larsen, C. N., Bresciani, J. & Olsen, J. E. (2004). Role of flagellin and the two-component CheA/CheY system of Listeria monocytogenes in host cell invasion and virulence. Infect Immun 72, 3237-3244.
14. Dramsi, S., Dehoux, P, Lebrun, M, Goossens, P. L. & Cossart, P. (1997). Identification of four new members of the internalin multigene family of Listeria monocytogenes EGD. Infect Immun 65, 1615-1625.
15. Greiffenberg, L., Goebel, W., Kim, K. S., Welglein, I., Bubert, A., Engelbrecht, F., Stins, M. & Kuhn, M. (1998). Interaction of Listeria monocytogenes with human brain microvascular endothelial cells: In1B-dependent invasion, long-term intracellular growth, and spread from macrophages to endothelial cells. Infect Immun 66, 5260-5267.
16. Heilmann, C., Hussain, M., Peters, G. & Gotz, F. (1997). Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol Microbiol 24, 1013-1024.
17. Hell, W., Meyer, H. G. & 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.
18. Jedrzejas, M. J. (2001). Pneumococcal virulence factors: structure and function. Microbiol Mol Biol Rev 65, 187-207.
19. B regulates stress response and virulence functions. J Bacteriol 185, 5722-5734.
20. Lenz, L. L., Mohammadi, S., Geissler, A. & Portnoy, D. A. (2003). SecA2-dependent secretion of autolytic enzymes promotes Listeria monocytogenes pathogenesis. Proc Natl Acad Sci U S A 100, 12432-12437.
21. Lock, R. A., Hansman, D. & Paton, J. C. (1992). Comparative efficacy of autolysin and pneumolysin as immunogens protecting mice against infectioh by Streptococcus pneumoniae. Microb Pathog 12, 137-143.
22. MacFaddin, J. F. (2000). Biochemical Tests for Identification of Medical Bacteria, 3rd edn. New York: Lippincott Williams & Wilkins.
23. Machata, S., Hain, T., Rohde, M. & Chakraborty, T. (2005). Simultaneous deficiency of both MurA and p60 proteins generates a rough phenotype in Listeria monocytogenes. J Bacteriol 187, 8385-8394.
24. Mani, N., Baddour, L. M., Offutt, D. O., Vijaranakul, U., Nadakavukaren, M. J. & Jayaswal, R. K. (1994). Autolysis-defective mutant of Staphylococcus aureus: pathological considerations, genetic mapping, and electron microscopic studies. Infect Immun 62, 1406-1409.
25. Milohanic, E., Jonquieres, R., Cossart, P., Berche, P. & 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.
26. O'Neil, H. S. & Marquis, H. (2006). Listeria monocytogenes flagella are used for motility, not as adhesins, to increase host cell invasion. Infect Immun 74, 6675-6681.
27. Park, S. F. & Stewart, G. S. (1990). High-efficiency transformation of Listeria monocytogenes by electroporation of penicillin-treated cells. Gene 94, 129-132.
28. Pilgrim, S., Kolb-Maurer, A., Gentschev, I., Goebel, W. & 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.
29. Popowska, M. (2004). Analysis of the peptidoglycan hydrolases of Listeria monocytogenes: multiple enzymes with multiple functions. Pol J Microbiol 53 (suppl.), 29-34.
30. Popowska, M. & Markiewicz, Z. (2004). Murein-hydrolyzing activity of flagellin FlaA of Listeria monocytogenes. Pol J Microbiol 53, 237-241.
31. Prats, N., Briones, V., Blanco, M. M., Altimira, J., Ramos, J. A., Dominguez, L. & Marco, A. (1992). Choroiditis and meningitis in experimental murine infection with Listeria monocytogenes. Eur J Clin Microbiol Infect Dis 11, 744-747.
32. Rowan, N. J., Candlish, A. A., Bubert, A., Anderson, J. G., Kramer, K. & McLauchlin, J. (2000). Virulent rough filaments of Listeria monocytogenes from clinical and food samples secreting wild-type levels of cell-free p6O protein. J Clin Microbiol 38, 2643-2648.
33. Rupp, M. E., Ulphani, J. S., Fey, P. D., Bartscht, K. & Mack, D. (1999). Characterization of the importance of polysaccharide intercellular adhesin/hemagglutinin of Staphylococcus epidermidis in the pathogenesis of biomaterial-based infection in a mouse foreign body infection model. Infect Immun 67, 2627-2632.
34. Rupp, M. E., Fey, P. D., Heilmann, C. & Gotz, F. (2001). Characterization of the importance of Staphylococcus epidermidis autolysin and polysaccharide intercellular adhesin in the pathogenesis of intravascular catheter-associated infection in a rat model. J Infect Dis 183, 1038-1042.
35. Schaferkordt, S., Domann, E. & Chakraborty, T. (1998). Molecular approaches for the study of Listeria. In Bacterial Pathogenesis (Methods in Microbiology no. 27) pp. 421-431. Edited by P. Williams, J. Ketley & G. Salmond. San Diego, CA: Academic Press.
36. Schluter, D., Chahoud, S., Lassmann, H., Schumann, A., Hof, H. & Deckert-Schluter, M. (1996). Intracerebral targets and immunomodulation of murine Listeria monocytogenes meningoencephalitis. J Neuropathol Exp Neurol 55, 14-24.
37. Shockman, G. D. & Holtje, J.-V. (1994). Microbial peptidoglycan (murein) hydrolases. In Bacterial Cell Wall, pp. 131-166. Edited by J.-M. Ghuysen & R. Hakenbeck. Amsterdam: Elsevier.
38. Smith, T. J., Blackman, S. A. & Foster, S. J. (2000). Autolysins of Bacillus subtilis: multiple enzymes with multiple functions. Microbiology 146, 249-262.
39. Takahashi, J., Komatsuzawa, H., Yamada, S., Nishida, T., Labischinski, H., Fujiwara, T., Ohara, M., Yamagishi, J. & Sugal, M. (2002). Molecular characterization of an atl null mutant of Staphylococcus aureus. Microbiol Immunol 46, 601-612.
40. Tuomanen, E. (1996). Entry of pathogens into the central nervous system. FEMS Microbiol Rev 18, 289-299.
41. Tuomanen, E. I. (2000). Pathogenesis o bf pneumococcal inflammation: otitis media. Vaccine 19 (suppl. 1), S38-S40.
42. Vandegraaff, R., Borland, N. A. & Browning, J. W. (1981). An outbreak of listerial meningo-encephalitis in sheep. Aust Vet J 157, 94-96.
43. Vasilescu, J., Smith, J. C., Ethier, M. & Figeys, D. (2005). Proteomic analysis of ubiquitinated proteins from human MCF-7 breast cancer cells by immunoaffinity purification and mass spectrometry. J Proteome Res 4, 2192-2200.
44. Vazquez-Boland, J. A., Kuhn, M., Berche, P., Chakraborty, T., Dominguez-Bernal, G., Goebel, W., Gonzalez-Zorn, B., Wehland, J. & Kreft, J. (2001). Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14, 584-640.
45. Wang, L. & Lin, M. (2007). Identification of IspC, an 86-kilodalton protein target of humoral immune response to infection with Listeria monocytogenes serotype 4b, as a novel surface autolysin. J Bacteriol 189, 2046-2054.
46. Wang, L., Walrond, L., Cyr, T. D. & Lin, M. (2007). A novel surface autolysin of Listeria monocytogenes serotype 4b, IspC, contains a 23-residue N-terminal signal peptide being processed in E. coli. Biochem Biophys Res Commun 354, 403-408.
47. Yu, W. L., Dan, H. & Lin, M. (2007). Novel protein targets of humoral immune response to Listeria monocytogenes infection in rabbits. J Med Microbiol 56, 888-895.