Hypermutation in pathogenic bacteria: Frequent phase variation in meningococci is a phenotypic trait of a specialized mutator biotype

Molecular Cell

Volumn 3, Issue 4, 1999, Pages 435-445

  Bucci, Cecilia ^a   Lavitola, Alfredo ^a   Salvatore, Paola ^a,b   Giudice, Luigi Del ^c   Massardo, Domenica Rita ^c   Bruni, Carmelo B ^a   Alifano, Pietro ^a,d  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b SECOND UNIVERSITY OF NAPLES   (Italy)

^c CNR   (Italy)

^d UNIVERSITY OF SALENTO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL POLYSACCHARIDE; DNA ADENINE METHYLTRANSFERASE; RESTRICTION ENDONUCLEASE;

ARTICLE; BACTERIAL MUTATION; DNA RESTRICTION; DNA SEQUENCE; ENZYME ACTIVITY; FRAMESHIFT MUTATION; NEISSERIA MENINGITIDIS; NONHUMAN; NUCLEOTIDE REPEAT; PROTEIN EXPRESSION;

BACTERIA (MICROORGANISMS); NEISSERIA MENINGITIDIS;

EID: 0033120547     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(00)80471-2     Document Type: Article

References (39)

1. Aho, E.L., Dempsey, J.A., Hobbs, M.M., Klapper, D.G., and Cannon, J.G. (1991). Characterization of the opa (class 5) gene family of Neisseria meningitidis. Mol. Microbiol. 5, 1429-1437.
2. Black, C.G., Fyfe, J.a.m., and Davies, J.K. (1995). A promoter associated with the neisserial repeat can be used to transcribe the uvrB gene from Neisseria gonorrhoeae. J. Bacteriol. 177, 1952-1958.
3. Brooks, J.E., Blumenthal, R.M., and Gingeras, T.R. (1983). Isolation and characterization of the Escherichia coli DNA adenine methylase (dam) gene. Nucleic Acids Res. 11, 837-851.
4. Campbell, L.A., and Yasbin, R.E. (1984). Mutagenesis of Neisseria gonorrhoeae: Absence of error-prone repair. J. Bacteriol. 160, 288-293.
5. Carlomagno, M.S., Chiariotti, L., Alifano, P., Nappo, A.G., and Bruni, C.B. (1988). Structure and expression of the histidine operons of Salmonella typhimurium and Escherichia coli. J. Mol. Biol. 203, 585-606.
6. Chapalain, J.C., Dusseau, J.Y., Perrier-Gros-Claude, J.D., Rouby, Y., and Bartoli, M. (1994). Effect of rifampicin chemoprophylaxis on the aerobic bacterial flora of the oropharynx. J. Antimicrob. Chemother. 33, 151-155.
7. Correia, F.F., Inouye, S., and Inouye, M. (1988). A family of small repeated elements with some transposon-like properties in the genome of Neisseria gonorrhoeae. J. Biol. Chem. 263, 12194-12198.
8. Craig, R.J., Arraj, J.A., and Marinus, M.G. (1984). Induction of damage inducible (SOS) repair in dam mutants of Escherichia coli exposed to 2-aminopurine. Mol. Gen. Genet. 194, 539-540.
9. Craven, D.E., Peppler, M.S., Frasch, C.E., Mocca, L.F., McGrath, P.P., and Washington, G. (1980). Adherence of isolates of Neisseria meningitidis from patients and carriers to human buccal epithelial cells. J. Infect. Dis. 142, 556-568.
10. Davies, J.K. (1989). DNA restriction and modification systems in Neisseria gonorrhoeae. Clin. Microbiol. Rev. 2, S78-S82.
11. Dente, L., Cesareni, G., and Cortese, R. (1983). pEMBL: A new family of single stranded plasmids. Nucleic Acids Res. 11, 1645-1655.
12. de Vries, F.P., van der Ende, A., van Putten, J.P.M., and Dankert, J. (1996). Invasion of primary nasopharyngeal cells by Neisseria meningitidis is controlled by phase variation of multiple surface antigens. Infect. Immun. 64, 2998-3006.
13. de Vries, F.P., Cole, R., Dankert, J., Frosch, M., and van Putten, J.P.M. (1998). Neisseria meningitidis producing the Opc adhesin binds epithelial cell proteoglycan receptors. Mol. Microbiol. 27, 1203-1212.
14. Edwards, U., Müller, A., Hammerschmidt, S., Gerardy-Schahn, R., and Frosch, M. (1994). Molecular analysis of the biosynthesis pathway of the α-2,8 polysialic acid capsule by Neisseria meningitidis serogroup B. Mol. Microbiol. 14, 141-149.
15. Frosch, M., Schultz, E., Glenn-Calvo, E., and Meyer, T.F. (1990). Generation of capsule-deficient Neisseria meningitidis strains by homologous recombination. Mol. Microbiol. 4, 1215-1218.
16. Grisolia, V., Carlomagno, M.S., and Bruni, C.B. (1982). Cloning and expression of the distal portion of the histidine operon of Escherichia coli K-12. J. Bacteriol. 151, 692-700.
17. Hammerschmidt, S., Birkholz, C., Zahringer, U., Robertson, B.D., van Putten, J., Ebeling, O., and Frosch, M. (1994). Contribution of genes from the capsule gene complex (cps) to lipooligosaccharide biosynthesis and serum resistance in Neisseria meningitidis. Mol. Microbiol. 11, 885-896.
18. Hammerschmidt, S., Hilse, R., van Putten, J., Gerardy-Schahn, R., Unkmeir, A., and Frosch, M. (1996a). Modulation of cell surface sialic acid expression in Neisseria meningitidis via a transposable genetic element. EMBO J. 115, 192-198.
19. Hammerschmidt, S., Müller, A., Sillmann, H., Mühlenhoff, M., Borrow, R., Fox, A., van Putten, J., Zollinger, W.D., Gerardy-Schahn, R., and Frosch, M. (1996b). Capsule phase variation in Neisseria meningitidis serogroup B by slipped-strand mispairing in the polysialyltransferase gene (siaD): Correlation with bacterial invasion and the outbreak of meningococcal disease. Mol. Microbiol. 20, 1211- 1220.
20. Jones, D.M., Borrow, R., Fox, A.J., Gray, S., Cartwright, K.A., and Poolman, J.T. (1992). The lipooligosaccharide immunotype as a virulence determinant in Neisseria meningitidis. Microb. Pathogen. 13, 219-224.
21. Jonsson, A.-B., Nyberg, G., and Normark, S. (1991). Phase variation of gonococcal pili by frameshift mutation in pilC, a novel gene for pilus assembly. EMBO J., 10, 477-488.
22. Kawula, T.H., Aho, E.L., Barritt, D.S., Klapper, D.G., and Cannon, J.G. (1988). Reversible phase variation of expression of Neisseria meningitidis class 5 outer membrane proteins and their relationship to gonococcal proteins II. Infect. Immun. 56, 380-386.
23. LeClerc, J.E., Pyne, W.L., and Cebula, T.A. (1996). High mutation frequencies among Escherichia coli and Salmonella pathogens. Science 274, 1208-1211.
24. Longerich, S., Galloway, A.M., Harris, R.S., Wong, C., and Rosenberg, S.M. (1995). Adaptive mutation sequences reproduced by mismatch repair deficiency. Proc. Natl. Acad. Sci. USA 92, 12017-12020.
25. Marinus, M.G. (1984). Methylation of prokaryotic DNA. In DNA MethYlation, Biochemistry and Biological Significance, A. Razin, H. Cedar, and A.D. Riggs, eds. (New York: Springer-Verlag), pp. 81-109.
26. Modrich, P. (1991). Mechanisms and biological effects of mismatch repair. Annu. Rev. Genet. 25, 229-253.
27. Monod, M., Denoya, C., and Dubnau, C. (1986). Sequence and properties of pIM13, a macrolide-lincosamide-streptogramin B resistance plasmid from Bacillus subtilis. J. Bacteriol. 167, 138-147.
28. Murphy, G.L., Connell, T.D., Barritt, D.S., Koomey, M., and Cannon, J.G. (1989). Phase variation of gonococcal protein II: Regulation of gene expression by slipped-strand mispairing of a repetitive DNA sequence. Cell 56, 539-547.
29. Olyhoek, A.J.M., Sarkari, J., Boop, M., Morelli, G., and Achtman, M. (1991). Cloning and expression in Escherichia coli of opc, the gene for an unusual class 5 outer membrane protein from Neisseria meningitidis. Microb. Pathogen. 11, 249-257.
30. Robertson, B.D., and Meyer, T.F. (1992). Genetic variation in pathogenic bacteria. Trends Genet. 8, 422-427.
31. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, Second Edition (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory).
32. Sarkari, J.F., Pandit, N., Moxon, E.R., and Achtman, M. (1994). Variable expression of outer membrane protein Opc in Neisseria meningitidis is caused by size variation of a promoter containing polycytidine. Mol. Microbiol. 13, 207-217.
33. Stephens, D.S., Spellman, P.A., and Swartley, J.S. (1993). Effect of the (α2→8)-linked polysialic acid capsule on adherence of Neisseria meningitidis to human mucosal cells. J. Infect. Dis. 167, 475-479.
34. Stern, A., and Meyer, T.F. (1987). Common mechanism controlling phase and antigenic variation in pathogenic neisseriae. Mol. MicroBiol. 1, 5-12.
35. Taddei, F., Matic, I., Godelle, B., and Radmen, M. (1997). To be a mutator, or how pathogenic and commensal bacteria can evolve rapidly. Trends Microbiol. 5, 427-428.
36. Troy, F.A. (1992). Polysialylation: From bacteria to brains. Glycobiol. 2, 5-23.
37. Van der Ende, A., Hopman, C.T.P., Zaat, S., Oude Essink, B.B., Berkhout, B., and Dankert, J. (1995). Variable expression of class I outer membrane protein in Neisseria meningitidis is caused by variation in the spacing between the -10 and -35 regions of the promoter. J. Bacteriol. 177, 2475-2480.
38. Virji, M., Makepeace, K., Ferguson, D.J., Achtman, M., and Moxon, E.R. (1993). Meningococcal Opa and Opc proteins: Their role in colonization and invasion of human epithelial and endothelial cells. Mol. Microbiol. 10, 499-510.
39. Vogel, U., Hammerschmidt, S., and Frosch, M. (1996). Sialic acids of both capsule and the sialylated lipooligosaccharide of Neisseria meningitidis serogroup B are prerequisite for virulence of meningococci in the infant rat. Med. Microbiol. Immunol. 185, 81-87.