A novel mechanism of phase variation of virulence in Staphylococcus epidermidis: Evidence for control of the polysaccharide intercellular adhesin synthesis by alternating insertion and excision of the insertion sequence element IS256

Molecular Microbiology

Volumn 32, Issue 2, 1999, Pages 345-356

  Ziebuhr, Wilma ^a   Krimmer, Vanessa ^a   Rachid, Shwan ^a   Lößner, Isabel ^a   Götz, Friedrich ^b   Hacker, Jörg ^a  

^a Inst fur Molec Infektionsbiol   (Germany)

^b Mikrobielle Genetik   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN;

AGAR GEL ELECTROPHORESIS; ARTICLE; BACTERIAL VIRULENCE; BIOFILM; CELL ADHESION; DNA TRANSPOSITION; GENE CLUSTER; GENE INSERTION; GENE INSERTION SEQUENCE; MOLECULAR GENETICS; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; OPERON; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SEQUENCE ANALYSIS; SOUTHERN BLOTTING; STAPHYLOCOCCUS EPIDERMIDIS;

EID: 0032896896     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1999.01353.x     Document Type: Article

References (63)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
2. Arber, W. (1993) Evolution of prokaryotic genomes. Gene 135: 49-56.
3. Baddour, L.M., and Christensen, G.D. (1987) Prosthetic valve endocarditis due to small colony staphylococcal variants. Rev Infect Dis 9: 1168-1173.
4. Baddour, L.M., Barker, L.P., Christensen, G.D., Parisi, J.T., and Simpson, W.A. (1990) Phenotypic variation of Staphylococcus epidermidis in infection of transvenous endocardial pacemaker electrodes. J Clin Microbiol 28: 676-679.
5. Baselga, R., De Albizu, I., La Cruz, M., Del Cacho, E., Barberan, M., and Amorena, B. (1993) Phase variation of slime production in Staphylococcus aureus: Implications in colonization and virulence. Infect Immun 61: 4857-4862.
6. Berg, D.E. and Howe, M. M. (eds) (1989) Mobile DNA. Washington, DC: ASM.
7. Bonafede, M., Carias, L.L., and Rice, L.B. (1997) Enterococcal transposon Tn5384: Evolution of a composite transposon through cointegration of enterococcal and staphylococcal plasmids. Antimicrob Agents Chemother 41: 1854-1858.
8. Byrne, M.E., Rouch, D.A., and Skurray, R.A. (1989) Nucleotide sequence of IS256 from the Staphylococcus aureus gentamicin-tobramycin-kanamycin-resistance transposon Tn4001. Gene 81: 361-367.
9. Cheung, A.L., Eberhardt, K., and Fischetti, V.A. (1994) A method to isolate RNA from gram-positive bacteria and Mycobacteria. Anal Biochem 222: 511-514.
10. Christensen, G.D., Simson, W.A., Younger, J.J., Baddour, L.M., Barrett, F.F., Melton, D.M., and Beachy, E.H. (1985) Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. J Clin Microbiol 22: 996-1006.
11. Christensen, G.D., Baddour, L.M., and Simpson, W.A. (1987) Phenotypic variation of Staphylococcus epidermidis slime production in vitro and in vivo. Infect Immun 55: 2870- 2877.
12. Christensen, G.D., Baddour, L.M., Madison, B.M., Parisi, J.T., Abraham, S.N., Hasty, D.L., et al. (1990) Colonial Morphology of Staphylococci on Memphis agar: phase variation of slime production, resistance to β-lactam antibiotics, and virulence. J Infect Dis 161: 1153-1169.
13. Cleary, P.P., MCLandsborough, L., Ikeda, L., Cue, D., Krawczak, J., and Lam, H. (1998) High-frequency intracellular infection and erythrogenic toxin A expression undergo phase variation in M1 group A streptococci. Mol Microbiol 28: 157-167.
14. Coffey, T.J., Enright, M.C., Daniels, M., Morona, J.K., Morona, R., Hryniewicz, W., et al. (1998) Recombinational exchange at the capsular polysaccharide biosynthetic locus lead to frequent serotype changes among natural isolates of Streptococcus pneumoniae. Mol Microbiol 27: 73-83.
15. Deighton, M., Pearson, S., Capstick, J., Spelman, D., and Borland, R. (1992). Phenotypic variation of Staphylococcus epidermidis isolated from a patient with native valve endocarditis. J Clin Microbiol 30: 2385-2390.
16. Deighthon, M., Borland, R., and Capstick, J.A. (1996) Virulence of Staphylococcus epidermidis in a mouse model: significance of extracellular slime. Epidemiol Infect 117: 267-280.
17. Deplano, A., Vaneechoutte, M., Verschraegen, G., and Struelens, M.J. (1997) Typing of Staphylococcus aureus and Staphylococcus epidermidis strains by PCR analysis of inter-IS256 spacer length polymorphisms. J Clin Microbiol 35: 2580-2587.
18. Dyke, K.G.H., Aubert, S., and El Solh, N. (1992) Multiple copies of IS256 in Staphylococci. Plasmid 28: 235-246.
19. Eisen, J.A., Benito, M.-J., and Walbot, V. (1994) Sequence similarity of putative transposases links the Mutator autonomous element and a group of bacterial insertion sequences. Nucleic Acids Res 22: 2634-2636.
20. Freeman, D.J., Falkiner, F.R., and Keane, C.T. (1989) New method for detection slime production by coagulase negative Staphylococci. J Clin Pathol 42: 872-874.
21. Galas, D.J., and Chandler, M. (1989) Bacterial insertion sequences. In Berg, D.E., and Howe, M.M. (eds). Mobile DNA. Washington, DC: ASM, pp. 109-162.
22. Gally, L.G., Bognan, J.A., Eisenstein, B.I., and Blomfield, I.C. (1993) Environmental regulation of the fim switch controlling type 1 fimbrial phase variation in Escherichia coli K-12: effects of temperature and media. J Bacteriol 175: 6186-6193.
23. Gerke, C., Kraft, A., Süßmuth, R., Schweitzer, O., and Götz, F. (1998) Characterization of the N-acetylglucosaminyl- transferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin. J Biol Chem 273: 18586-18593.
24. Goering, R.V., and Winters, A. (1992) Rapid method for epidemiological evaluation of Gram-positive cocci by field inversion gel electrophoresis. J Clin Microbiol 30: 213-225.
25. Hacker, J. (1992) Role of fimbrial adhesins in the pathogenesis of Escherichia coli infections. Can J Microbiol 38: 720-727.
26. Hammerschmidt, S., Hilse, R., van Putten, J.P.M., Gerardy- Schahn, R., Unkenmeir, A., and Frosch, M. (1996) Modulation of cell surface sialic acid expression in Neisseria meningitidis via a transposable genetic element. EMBO J 15: 192-196.
27. Heilmann, C., Gerke, C., Perdreau-Remington, F., and Götz, F. (1996a) Characterization of Tn917 insertion mutants of Staphylococcus epidermidis affected in biofilm formation. Infect Immun 64: 277-282.
28. Heilmann, C., Schweitzer, O., Gerke, C., Vanittanakom, N., Mack, D., and Götz, F. (1996b) Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol Microbiol 20: 1083-1091.
29. Heilmann, C., Hussain, M., Peters, G., and Götz, F. (1997) Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol Microbiol 24: 1013-1024.
30. Heilmann, C., and Götz, F. (1998) Further characterization of Staphylococcus epidermidis transposon mutants deficient in primary attachment or intercellular adhesion. Zentralbl Bakteriol 287: 69-83.
31. Heinzelmann, M., Herzig, D.O., Swain, B., Mercer-Jones, M.A., Bergamini, T.M., and Polk, H.C. Jr. (1997) Phagocytosis and oxidative-burst response of planktonic Staphylococcus epidermidis RP62A and its non-slime-producing variant in human neutrophils. Clin Diagn Lab Immunol 4: 705-710.
32. Hodel-Christian, S.L., and Murray, B.E. (1991) Characterization of the gentamicin resistance transposon Tn5281 from Enterococcus faecalis and comparison to staphylococcal transposons Tn4001 and Tn4031. Antimicrob Agents Chemother 35: 1147-1152.
33. Kloos, W.E., and Bannerman, T.L. (1994) Update on clinical significance of coagulase-negative staphylococci. Clin Microbiol Rev 7: 117-140.
34. Linhardt, F., Ziebuhr, W., Meyer, P., Witte, W., and Hacker, J. (1992) Pulsed-field gel electrophoresis of genomic restriction fragments as a tool for the epidemiological analysis of Staphylococcus aureus and coagulase-negative staphylococci. FEMS Microbiol Lett 95: 181-186.
35. Lyon, B.R., May, J.W., and Skurray, R.A. (1984) Tn4001: a gentamicin and kanamycin resistance transposon in Staphylococcus aureus. Mol Gen Genet 193: 554-556.
36. Lyon, B.R., Gillespie, M.T., and Skurray, R.A. (1987) Detection and characterization of IS256, an insertion sequence in Staphylococcus aureus. J Gen Microbiol 133: 3031- 3038.
37. Mack, D., Nedelmann, M., Krokotsch, Schwarzkopf, A., Heesemann, J., and Laufs, R. (1994) Characterization of transposon mutants of biofilm-producing Staphylococcus epidermidis impaired in the accumulative phase of biofilm production: Genetic identification of a hexosamine-containing polysaccharide intercellular adhesin. Infect Immun 62: 3244-3253.
38. Mack, D., Fischer, W., Krokotsch, A., Leopold, K., Hartmann, R., Egge, H., and 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.
39. Mahillon, J., and Chandler, M. (1998) Insertion sequences. Microbiol Mol Biol Rev 62: 725-774.
40. Maki, H., and Murakami, K. (1997) Formation of potent hybrid promoters of the mutant llm gene by IS256 transposition in methicillin-resistant Staphylococcus aureus. J Bacteriol 179: 6944-6948.
41. Mempel, M., Feucht, H., Ziebuhr, W., Endres, M., Laufs, R., and Grüter, L. (1994) Lack of mecA transcription in slime- negative phase variants of methicillin resistant Staphylococcus epidermidis. Antimicrob Agents Chemother 38: 1251-1255.
42. Meyer, T.F., Pohlner, J., and van Putten, J.P. (1994) Biology of the pathogenic Neísseriae. Curr Top Microbiol Immunol 192: 283-317.
43. Mol, O., and Oudega, B. (1996) Molecular and structural aspects of fimbriae biosynthesis and assembly in Escherichia coli. FEMS Microbiol Rev 19: 25-52.
44. Monzon-Moreno, C., Aubert, S., Morvan, A., and El Solh, N. (1991) Usefulness of three probes in typing isolates of methicillin-resistant Staphylococcus aureus (MRSA). J Med Microbiol 34: 80-88.
45. Morvan, A., Aubert, S., Godard, S., and El Solh, N. (1997) Contribution of a typing method based on IS256 probing of Smal-digested cellular DNA to discrimination of European phage type 77 methicillin-resistant Staphylococcus aureus strains. J Clin Microbiol 35: 1415-1423.
46. Owen, P., de Meehan, M., Loughry-Doherty, H., and Henderson, I. (1996) Phase variable outer membrane proteins in Escherichia coli. FEMS Immunol Med Microbiol 16: 63-76.
47. Proctor, R.A., van Langevelde, P., Kristjanson, M., Maslow, J.N., and Arbeit, R.D. (1995) Persistent and relapsing infections associated with small-colony variants of Staphylococcus aureus. Clin Infect Dis 20: 95-102.
48. van Putten, J.P., and Robertson, B.D. (1995) Molecular mechanisms and implications for infection of lipopolysaccharide variation in Neisseria. Mol Microbiol 16: 847-853.
49. Rice, L.B., and Carias, L.L. (1998) Transfer of Tn5385, a composite, multiresistance chromosomal element from Enterococcus faecalis. J Bacteriol 180: 714-721.
50. Rice, L.B., and Marshall, S.H. (1994) Insertion of IS256-like element flanking the chromosomal β-lactamase gene of Enterococcus faecalis CX19. Antimicrob Agents Chemother 38: 693-701.
51. Rice, L.B., and Thorisdottir, A.S. (1994) The prevalence of sequences homologous to IS256 in clinical enterococcal isolates. Plasmid 32: 344-349.
52. Rice, L.B., Carias, L.L., and Marshall, S. (1995) Tn5384, a composite enterococcal mobile element conferring resistance to erythromycin and gentamicin whose ends are directly repeated copies of IS256. Antimicrob Agents Chemother 39: 1147-1153.
53. Roche, R.J., and Moxon, E.R. (1995) Phenotypic variation of carbohydrate surface antigens and the pathogenesis of Haemophilus influenzae infections. Trends Microbiol 3: 304-309.
54. Saluja, S.K., and Weiser, J.N. (1995) The genetic basis of colony opacity in Streptococcus pneumoniae: evidence for the effect of box elements on the frequency of phenotypic variation. Mol Microbiol 16: 215-227.
55. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning. A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor laboratory Press.
56. Sanger, F., Nicklen, S., and Coulson, A.R. (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463-5467.
57. Saunders, J.R., O'Sullivan, H., Wakeman, J., Sims, G., Hart, C.A., Virji, M., et al. (1993) Flagella and pili as antigenically variable structures on the bacterial surface. J Appl Bacteriol 74 (Suppl.): 33S-42S.
58. Seifert, H.S., and So, M. (1988) Genetic mechanisms of bacterial antigenic variation. Microbiol Rev 52: 327-336.
59. Thomas, W.D. Jr and Archer, G.L. (1989) Mobility of gentamicin resistance genes in the United States. Identification of Tn4031, a gentamicin resistance transposon from Staphylococcus epidermidis. Antimicrob Agents Chemother 33: 1335-1341.
60. Walcher-Salesse, S., Monzon-Moreno, C., Aubert, S., and El Solh, N. (1992) An epidemiological assessment of coagulase-negative staphylococci (CNS) from an intensive care unit. J Med Microbiol 36: 321-331.
61. Weiser, J.N., Chong, S.T.H., Greenberg, D., and Fong, W. (1995) Identification and characterization of a cell envelope protein of Haemophilus influenzae contributing to phase variation in colony opacity and nasopharyngeal colonization. Mol Microbiol 17: 555-564.
62. Weiser, J.N., Markiewicz, Z., Tuomanen, E.I., and Wani, J.H. (1996) Relationship between phase variation in colony morphology, intrastrain variation in cell wall physiology, and nasopharyngeal colonization by Streptococcus pneumoniae. Infect Immun 64: 2240-2245.
63. Ziebuhr, W., Heilmann, C., Götz, F., Meyer, P., Wilms, K., Straube, E., and Hacker, J. (1997) Detection of the intercellular adhesin gene cluster (ica) and phase variation in Staphylococcus epidermidis blood culture strains and mucosal isolates. Infect Immun 65: 890-896.