Wall teichoic acids are dispensable for anchoring the PNAG exopolysaccharide to the Staphylococcus aureus cell surface

Microbiology

Volumn 154, Issue 3, 2008, Pages 865-877

  Vergara Irigaray, Marta ^a   Maira Litrán, Tomas ^b   Merino, Nekane ^a   Pier, Gerald B ^b   Penadés, José R ^c   Lasa, Iñigo ^a  

^a PUBLIC UNIVERSITY OF NAVARRE   (Spain)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c INSTITUTO VALENCIANO DE INVESTIGACIONES AGRARIAS IVIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; EXOPOLYSACCHARIDE; POLY N ACETYLGLUCOSAMINE; POLYANION; PROTEIN ICAADBC; PROTEIN TAGO; TEICHOIC ACID; BETA GLUCAN; POLY N ACETYL 1 6 GLUCOSAMINE; POLY-N-ACETYL-1-6-GLUCOSAMINE;

ARTICLE; BACTERIAL CELL; BACTERIAL CELL WALL; BACTERIAL STRAIN; BACTERIUM MUTANT; BIOFILM; CARBOHYDRATE ANALYSIS; CARBOHYDRATE SYNTHESIS; CELL ACTIVITY; CELL ADHESION; CELL AGGREGATION; CELL INTERACTION; CELL SURFACE; CONTROLLED STUDY; GENE DELETION; GRAM POSITIVE BACTERIUM; HIGH TEMPERATURE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; STEADY STATE; TEMPERATURE SENSITIVITY; THERMOSTABILITY; WILD TYPE; BACTERIOLYSIS; BACTERIUM ADHERENCE; BIOSYNTHESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEAT; IMMUNOELECTRON MICROSCOPY; METABOLISM; PHYSIOLOGY; SCANNING ELECTRON MICROSCOPY; ULTRASTRUCTURE;

BACTERIA (MICROORGANISMS); POSIBACTERIA; STAPHYLOCOCCUS AUREUS;

BACTERIAL ADHESION; BACTERIOLYSIS; BETA-GLUCANS; BIOFILMS; BIOSYNTHETIC PATHWAYS; GENE DELETION; HEAT; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, IMMUNOELECTRON; STAPHYLOCOCCUS AUREUS; TEICHOIC ACIDS;

EID: 42949109357     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.2007/013292-0     Document Type: Article

References (49)

1. Aly, R, Shinefield, H. R., Litz, C. & Maibach, H I. (1980). Role of teichoic acid in the binding of Staphylococcus aureus to nasal epithelial cells. J Infect Dis 141, 463-465.
2. Arnaud, M, Chastanet, A. & Débarbouillé, M. (2004). A new vector for efficient allelic replacement in naturally non transformable low GC% Gram-positive bacteria. Appl Environ Microbiol 70, 6887-6891.
3. Augustin, J., Rosenstein, R., Wieland, B, Schneider, U., Schnell, N., Engelke, G., Entian, K. D. & Gotz, F. (1992). Genetic analysis of epidermin biosynthetic genes and epidermin-negative mutants of Staphylococcus epidermidis. Eur J Biochem 204, 1149-1154.
4. Baddiley, J. (2000). Teichoic acids in bacterial coaggregation. Microbiology 146, 1257-1258.
5. Baddiley, J, Buchanan, J. G., Hardy, F. E. Martin, R. O., Rajbhandary, U. L. & Sanderson, A. R. (1961). The structure of the ribitol teichoic acid of Staphylococcus aureus H. Biochim Biophys Acta 52, 406-407.
6. Bera, A. Biswas, R., Herbert S., Kulauzovic, E., Weidenmaier, C., Paschel, A. & Gotz, F. (2007). Influence of wall teichoic acid on lysozyme resistance in Staphylococcus aureus. J Bacteriol 189, 280-283.
7. Cerca, N., Jefferson, K. K., Maira-Litrán, T., Pier, D. B., Kelly-Quintos, C., Goldmann, D. A., Azeredo, J. & Pier, G. B. (2001). Molecular basis for preferential protective efficacy of antibodies directed to the poorly acetylated form of staphylococcal poly-N-acetyi-β-(1-6)-glucosamine. Infect Immun 75, 3406-3413.
8. Cobb, B. A. & Kasper, D. L. (2005). Zwitterionic capsular polysaccharides: the new MHCII-dependent antigens. Cell Microbiol 7, 1398-1403.
9. Cobb, B. A., Wang, O, Tzianabos, A. O. & Kasper, D. L. (2004). Polysaccharide processing and presentation by the MHCH pathway. Cell 117, 677-687.
10. Cramton, S. E., Gerke, C., Schnell, N. F., Nichols, W. W. & Gotz, F. (1999). The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect Immun 67, 5427-5433.
11. Cucarella, C., Solano, C, Valle, J, Amorena, B, Lasa, I. I. & Penades, J. R. (2001). Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J Bacteriol 183, 2888-2896.
12. D'Elia, M. A., Millar, K E., Beveridge, T. J. & Brown, E. D. (2006a). Wall teichoic acid polymers are dispensable for cell viability in Bacillus subtilis. J Bacteriol 188, 8313-8316.
13. D'Elia, M. AL, Pereira, M. P., Chung, Y. S., Zhao, W., Chau, A., Kenney, T. J., Sulavik M. C., Black T. A. & Brown, E. D. (2006b). Lesions in teichoic acid biosynthesis in Staphylococcus aureus lead to a lethal gain of function in the otherwise dispensable pathway. J Bacteriol 188, 4183-4189.
14. Doyle, R. J., Chatterjee, A. N, Streips, U. N. & Young, F. E. (1975). Soluble macromolecular complexes involving bacterial teichoic acids. J Bacteriol 124, 341-347.
15. Endl, J., Seidl, H. P., Fiedler, F. & Schleifer, K H. (1983). Chemical composition and structure of cell wall teichoic acids of staphylococci. Arch Microbiol 135, 215-223.
16. Fischer, W. (1994). Lipoteichoic acid and lipids in the membrane of Staphylococcus aureus. Med Microbiol Immunol 183, 61-76.
17. Gotz, F. (2002). Staphylococcus and biofilms. Mol Microbiol 43, 1367-1378.
18. Gross, M., Cramton, S. E., Gotz, F. & Peschel, A. (2001). Key role of teichoic acid net charge in Staphylococcus aureus colconization of artificial surfaces. Infect Immun 69, 3423-34261.
19. Grundling, A. & Schneewind, O. (2007). Synthesis of glycerol phosphate lipoteichoic acid in Staphylococcus aureus. Proc Natl Acad Sci U S A 104, 8478-8483.
20. Heilmann, C., Gerke, C., Perdreau-Remington, F. & Gotz, F. (1996a). Characterization of Tn917 insertion mutants of Staphylococcus epidermidis affected in biofilm formation. Infect Immun 64, 277-282.
21. Heilmann, C, Schweitzer, O., Gerke, C., Vanittanakom, N., Mack D. & Gotz, F. (1996b). Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol Microbiol 20, 1083-1091.
22. Herbert, S., Bera, A., Nerz, C, Kraus, D., Peschel, A, Goerke, C., Meehl, M., Cheung, A. & Gotz, F. (2007). Molecular basis of resistance to muramidase and cationic antimicrobial peptide activity of lysozyme in staphylococci. PLoS Pathogens 3, e102.
23. Ingavale, S. S., Van Wamel, W. & Cheung, A. L. (2003). Characterization of RAT, an autolysis regulator in Staphylococcus aureus. Mol Microbiol 48, 1451-1466.
24. Jefferson, K. K. Cramton, S. E, Gotz, F. & Pier, G. B. (2003). Identification of a 5-nucleotide sequence that controls expression of the ica locus in Staphylococcus aureus and characterization of the DNA-binding properties of IcaR. Mol Microbiol 48, 889-899.
25. Joyce, J. G., Abeygunawardana, C., Xu, O., Cook J. C., Hepler, R., Przysiecki, C. T., Grimm, K. M., Roper, K., Ip, C. C. & other authors (2003). Isolation, structural characterization, and immunological evaluation of a high-molecular-weight exopolysaccharide from Staphylococcus aureus. Carbohydr Res 338, 903-922.
26. Kaplan, J. B., Ragunath, C, Velliyagounder, K. Fine, D. H. & Ramasubbu, N. (2004a). Enzymatic detachment of Staphylococcus epidermidis biofilms. Antimicrob Agents Chemother 48, 2633-2636.
27. Kaplan, J. B., Velliyagounder, K., Ragunath, C., Rohde, H., Mack D., Knobloch, J. K. & Ramasubbu, N. (2004b). Genes involved in the synthesis and degradation of matrix polysaccharide in Actinobacillus actinomycetemcomitans and Actinobacillus pleuropneumoniae biofilms. J Bacteriol 186, 8213-8220.
28. Mack D., Fischer, W., Krokotsch, A., Leopold, K, Hartmann, R., Egge, H. & Laufs, R. (1996). The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear β-1,6-linked glucosaminoglycan: purification and structural analysis. J Bacteriol 178, 175-183.
29. Mack, D., Becker, P, Chatterjee, I., Dobinsky, S,, Knobloch, J. K., Peters, G., Rohde, H. & Herrmann, M. (2004). Mechanisms of biofilm formation in Staphylococcus epidermidis and Staphylococcus aureus: functional molecules, regulatory circuits, and adaptive responses. Int J Med Microbiol 294, 203-212.
30. Maira-Litrán, T., Kropec, A, Abeygunawardana, C., Joyce, J., Mark, G., III, Goldmann, D. A. & Pier, G. B. (2002). Immunochemical properties of the staphylococcal poly-N-acetylglucosamine surface polysaccharide. Infect Immun 70, 4433-4440.
31. Maira Litrán, T., Kroper, A., Góldmann, D. A. & Pier, G. B. (2005). Comparative opsonic and protective activities of Staphylococcus aureus conjugate vaccines containing native or deacetylated staphylococcal poly-N-acetyl-β-(1-6)-glucosamine. Infect Immun 73, 6752-6762.
32. Maki, H., Yamaguchi, T. & Murakami, K. (1994). Cloning and characterization of a gene affecting the methicillin resistance level and the autolysis rate in Staphylococcus aureus. J Bacteriol 176, 4993-5000.
33. McKenney, D., Hubner, J., Muller, E., Wang, Y., Goldmann, D. A. & Pier, G. B. (1998). The ica locus of Staphylococcus epidermidis encodes production of the capsular polysaccharide/ adhesin. Infect Immun 66, 4711-4720.
34. Mckenney, D., Pouliot, K., Wang, V., Murthy, V., Ulrich, M., Döring, G., Lee, J. C., Goldmann, D. A. & Pier, G. B. (1999). Broadly protective vaccine for Staphylococcus aureus based on an in vivo-expressed antigen. Science 284, 1523-1527.
35. Neuhaus, F. C. & Baddiley, J. (2003). A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in Gram-positive bacteria. Microbiol Mol Biol Rev 67, 686-723.
36. Novick R. P. (1990). The Staphylococcus as a molecular genetic system. In Molecular Biology of the Staphylococcus, pp. 1-40. Edited by R. P. Novick. New York: VCH Publishers.
37. Peschel, A., Otto, M., Jack R. W., Kalbacher, H., Jung, G. & Gotz, F. (1999). Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J Biol Chem 274, 8405-8410.
38. Prigent-Combaret C., Prensier, G, Le Thi, T. T., Vidal, O., Lejeune, P. & Dorel, C. (2000). Developmental pathway for biofilm formation in curli-producing Escherichia coli strains: role of flagella, curli and colanic acid. Environ Microbiol 2, 450-464.
39. Rice, K. C., Mann, E. E., Endres, J. L., Weiss, E. C., Cassat J. E., Smeltzer, M. S. & Bayles, K. W. (2007). The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc Natl Acad Sci U S A 104, 8113-8118.
40. Soldo, B., Lazarevic, V. & Karamata, D. (2002a). tagO is involved in the synthesis of all anionic cell-wall polymers in Bacillus subtilis 168. Microbiology 148, 2079-2087.
41. Soldo, B., Lazarevic, V. Pooley, H. M. & Karamata, D. (2002b). Characterization of a Bacillus subtilis thermosensitive teichoic acid-deficient mutant: gene mnaA (yvyH) encodes the UDP-N-acetylglucosamine 2-epimerase. J. Bacteriol 184, 4316-4320.
42. Toledo-Arana, A., Merino, N., Vergara-Irigaray, M., Debarbouille, M., Penades, J. R. & Lasa, I. (2005). Staphylococcus aureus develops an alternative, ica-independent biofilm in the absence of the arlRS two-component system. J Bacteriol 187, 5318-5329.
43. B is essential for biofilm development by Staphylococcus aureus. Mol Microbiol 48, 1075-1087.
44. Vinogradov, E., Sadovskaya, I., Li, J. & Jabbouri, S. (2006). Structural elucidation of the extracellular and cell-wall teichoic acids of Staphylococcus aureus MN8m, a biofilm forming strain. Carbohydr Res 341, 738-743.
45. Vuong, C., Kocianova, S., Voyich, J. M., Yao, Y., Fischer, E. R., DeLeo, F. R. & Otto, M. (2004). A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J Biol Chem 279, 54881-54886.
46. Wing, X., Preston, J. F., III & Romeo, T. (2004). The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adbesin required for biofilm formation. J. Bacteriol 186, 2724-2734.
47. Ward, J. B. (1981). Teichoic and teichuronic acids: biosynthesis, assembly, and location. Microbiol Rev 45, 211-243.
48. Weidenmaier, C., Kokai-Kun, J. F., Kristian, S. A., Chanturiya, T., Kalbacher, H., Gross, M., Nicholson, G., Neumeister, B., Mond, J. J. & Peschel, A. (2004). Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat Med 10, 243-245.
49. Weidenmaier, C., Paschal, A., Xiong, Y. Q., Kristian, S. A., Dietz, K., Yeaman, M. R. & Bayer, A. S. (2005). Lack of wall teichoic acids in Staphylocaccus aureus leads to reduced interactions with endothelial cells and to attenuated virulence in a rabbit model of endocarditis. J Infect Dis 191, 1771-1777.