Genetic diversity and mosaicism at the por locus of Neisseria gonorrhoeae

Journal of Bacteriology

Volumn 181, Issue 18, 1999, Pages 5591-5599

  Fudyk, Trevor C ^a   Maclean, Ian W ^a   Simonsen, J Neil ^a   Njagi, Ephantus N ^b   Kimani, Joshua ^b   Brunham, Robert C ^a   Plummer, Francis A ^a,b  

^a UNIVERSITY OF MANITOBA   (Canada)

^b UNIVERSITY OF NAIROBI   (Kenya)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; PORIN;

ARTICLE; BACTERIUM ISOLATE; CONTROLLED STUDY; DNA SEQUENCE; GENE LOCUS; GENETIC VARIABILITY; KENYA; MOSAICISM; NEISSERIA GONORRHOEAE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEQUENCE HOMOLOGY;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; NEISSERIA GONORRHOEAE; PROKARYOTA;

EID: 0032862321     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.181.18.5591-5599.1999     Document Type: Article

References (56)

1. Bauer, F. J., T. Rudel, M. Stein, and T. F. Meyer. 1999. Mutagenesis of the Neisseria gonorrhoeae porin reduces invasion in epithelial cells and enhances phagocyte responsiveness. Mol. Microbiol. 31:903-913.
2. Bhat, K. S., C. P. Gibbs, O. Barrera, S. G. Morrison, F. Jahnig, A. Stern, E. M. Kupsch, T. F. Meyer, and J. Swanson. 1991. The opacity proteins of Neisseria gonorrhoeae strain MS11 are encoded by a family of 11 complete genes. Mol Microbiol. 5:1889-1901. Erratum, 6:1073-1076, 1992.)
3. Bjerknes, R., H. K. Guttormsen, C. O. Solberg, and L. M. Wetzler. 1995. Neisserial porins inhibit human neutrophil actin polymerization, degranulation, opsonin receptor expression, and phagocytosis but prime the neutrophils to increase their oxidative burst. Infect. Immun. 63:160-167.
4. Blake, M. S., and E. C. Gotschlich. 1982. Purification and partial characterization of the major outer membrane protein of Neisseria gonorrhoeae. Infect. Immun. 36:277-283.
5. Brooks, G. F., L. Olinger, C. J. Lammel, K. S. Bhat, C. A. Calvello, M. L. Palmer, J. S. Knapp, and R. S. Stephens. 1991. Prevalence of gene sequences coding for hypervariable regions of Opa (protein II) in Neisseria gonorrhoeae. Mol. Microbiol. 5:3063-3072.
6. Brunham, R., C. Yang, I. Maclean, J. Kimani, G. Maitha, and F. Plummer. 1994. Chlamydia trachomatis from individuals in a sexually transmitted disease core group exhibit frequent sequence variation in the major outer membrane protein (omp1) gene. J. Clin. Investig. 94:458-463.
7. Brunham, R. C., J. Kimani, J. Bwayo, G. Maitha, I. W. Maclean, C. Yang, C. Shen, S. Roman, N. J. Nagelkerke, M. Cheang, F. A. Plummer. 1996. The epidemiology of Chlamyida trachomatis within a sexually transmitted disease core group. J. Infect. Dis. 17:950-956.
8. Brunham, R. C., F. Plummer, L. Slaney, F. Rand, and W. DeWitt. 1985. Correlation of auxotype and protein I type with expression of disease due to Neisseria gonorrhoeae. J. Infect. Dis. 152:339-343.
9. Buchanan, T. M., D. A. Eschenbach, J. S. Knapp, and K. K. Holmes. 1980. Gonococcal salpingitis is less likely to recur with Neisseria gonorrhoeae of the same principal outer membrane protein antigenic type. Am. J. Obstet. Gynecol. 138:978-980.
10. Butt, N. J., P. R. Lambden, and J. E. Heckels. 1990. The nucleotide sequence of the por gene from Neisseria gonorrhoeae strain P9 encoding outer membrane protein PIB. Nucleic Acids Res. 18:4258.
11. Butt, N. J., M. Virji, F. Vayreda, P. R. Lambden, and J. E. Heckels. 1990. Gonococcal outer-membrane protein PIB: comparative sequence analysis and localization of epitopes which are recognized by type-specific and cross-reacting monoclonal antibodies. J. Gen. Microbiol. 136:2165-2172.
12. Bygdeman, S. M., P. A. Mardh, and E. G. Sandstrom. 1984. Susceptibility of Neisseria gonorrhoeae to rifampicin and thiamphenicol: correlation with protein I antigenic determinants. Sex. Transm. Dis. 11:366-370.
13. Cannon, J. G., T. M. Buchanan, and P. F. Sparling. 1983. Confirmation of association of protein I serotype of Neisseria gonorrhoeae with ability to cause disseminated infection. Infect. Immun. 40:816-819.
14. Carbonetti, N., V. Simnad, C. Elkins, and P. F. Sparling. 1990. Construction of isogenic gonococci with variable porin structure: effects on susceptibility to human serum and antibiotics. Mol. Microbiol. 4:1009-1018.
15. Carbonetti, N. H., V. I. Simnad, H. S. Seifert, M. So, and P. F. Sparling. 1988. Genetics of protein I of Neisseria gonorrhoeae: construction of hybrid porins. Proc. Natl. Acad. Sci. USA 85:6841-6845. (Erratum, 86:1317, 1989.)
16. Connell, T. D., W. J. Black, T. H. Kawula, D. S. Barritt, J. A. Dempsey, K. Kverneland, Jr., A. Stephenson, B. S. Schepart, G. L. Murphy, and J. G. Cannon. 1988. Recombination among protein II genes of Neisseria gonorrhoeae generates new coding sequences and increases structural variability in the protein II family. Mol. Microbiol. 2:227-236.
17. Cooke, S. J., H. de la Paz, C. La Poh, C. A. Ison, and J. E. Heckels. 1997. Variation within serovars of Neisseria gonorrhoeae detected by structural analysis of outer-membrane protein PIB and by pulsed-field gel electrophoresis. Microbiology 143:1415-1422.
18. Cooke, S. J., K. Jolley, C. A. Ison, H. Young, and J. E. Heckels. 1998. Naturally occurring isolates of Neisseria gonorrhoeae, which display anomalous serovar properties, express PIA/PIB hybrid porins, deletions in PIB or novel PIA molecules. FEMS Microbiol Lett. 162:75-82.
19. Cowan, S. W., T. Schirmer, G. Rummel, M. Steiert, R. Ghosh, R. A. Pauptit, J. N. Jansonius, and J. P. Rosenbusch. 1992. Crystal structures explain functional properties of two E. coli porins. Nature 358:727-733.
20. Ebert, D. 1998. Experimental evolution of parasites. Science 282:1432-1435.
21. Elkins, C., N. H. Carbonetti, V. A. Varela, D. Stirewalt, D. G. Klapper, and P. F. Sparling. 1992. Antibodies to N-terminal peptides of gonococcal porin are bactericidal when gonococcal lipopolysaccharide is not sialylated. Mol. Microbiol. 6:2617-2628.
22. Gibbs, C. P., B. Y. Reimann, E. Schultz, A. Kaufmann, R. Haas, and T. F. Meyer. 1989. Reassortment of pilin genes in Neisseria gonorrhoeae occurs by two distinct mechanisms. Nature 338:651-652.
23. Gotschlich, E. C., M. E. Seiff, M. S. Blake, and M. Koomey. 1987. Porin protein of Neisseria gonorrhoeae: cloning and gene structure. Proc. Natl. Acad. Sci. USA 84:8135-8139.
24. Haas, R., and T. F. Meyer. 1986. The repertoire of silent pilus genes in Neisseria gonorrhoeae: evidence for gene conversion. Cell 44:107-115.
25. Higgins, D. G., and PM. Sharp. 1988. CLUSTAL: a package for performing multiple sequence alignments on a microcomputer. Gene 73:237-244.
26. Hobbs, M. M., T. M. Alcorn, R. H. Davis, W. Fischer, J. C. Thomas, I. Martin, C. Ison, P. F. Sparling, and M. S. Cohen. 1999. Molecular typing of Neisseria gonorrhoeae causing repeated infections: evolution of porin during passage within a community. J. Infect. Dis. 179:371-381.
27. Jeanteur, D., J. H. Lakey, and F. Pattus. 1991. The bacterial porin super-family: sequence alignment and structure prediction. Mol. Microbiol. 5:2153-2164.
28. Johnston, K. H., K. K. Holmes, and E. C. Gotschlich. 1976. The serological classification of Neisseria gonorrhoeae. I. Isolation of the outer membrane complex responsible for serotypic specificity. J. Exp. Med. 143:741-758.
29. Knapp, J. S., M. R. Tam, R. C. Nowinski, and K. K. Holmes. 1984. Serological classification of Neisseria gonorrhoeae with use of monoclonal antibodies to gonococcal outer membrane I. J. Infect. Dis. 150:44-48.
30. Kohl, P. K., D. A. Olsen, and T. M. Buchanan. 1989. Monoclonal antibodies to protein I for serotyping of Neisseria gonrrhoeae: correlation of serotype with bactericidal activity. Zentbl. Bakteriol. Mikrobiol. Hyg. A 270:517-526.
31. Kumar, S., K. Tamura, and M. Nei. 1994. MEGA: Molecular Evolutionary Genetics Analysis software for microcomputers. Comput. Appl. Biosci. 10: 189-191.
32. Mauro, A., M. Blake, and P. Labarca. 1988. Voltage gating of conductance in lipid bilayers induced by porin from outer membrane of Neisseria gonorrhoeae. Proc. Natl. Acad. Sci. USA 85:1071-1075.
33. Mee, B. J., H. Thomas, S. J. Cooke, P. R. Lambden, and J. E. Heckels. 1993. Structural comparison and epitope analysis of outer-membrane protein PIA from strains of Neisseria gonorrhoeae with differing serovar specificities. J. Gen. Microbiol. 139:2613-2620.
34. Meyer, T. F. 1991. Evasion mechanisms of pathogenic Neisseriae. Behring Inst. Mitt. 88:194-199.
35. Meyer, T. F., N. Mlawer, and M. So. 1982. Pilus expression in Neisseria gonorrhoeae involves chromosomal rearrangement. Cell 30:45-52.
36. Molecular Biology Group, University of Sussex. 30 July 1999, revision date. MAXCHI program [Online.] http://epunix.biols.susx.ac.uk/ [30 July 1999, last date accessed.]
37. Mosleh, I. M., L. A. Huber, P. Steinlein, C. Pasquali, D. Gunther, and T. F. Meyer. 1998. Neisseria gonorrhoeae porin modulates phagosome maturation. J. Biol. Chem. 273:35332-35338.
38. Muller, A., D. Gunther, F. Dux, M. Naumann, T. F. Meyer, and T. Rudel. 1999. Neisserial porin (PorB) causes rapid calcium influx in target cells and induces apoptosis by the activation of cysteine proteases. EMBO J. 18:339-352.
39. Murphy, T. F. 1994. Antigenic variation of surface proteins as a survival strategy for bacterial pathogens. Trends Microbiol. 2:427-428.
40. Nei, M., and T. Gojobori. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3:418-426.
41. Plummer, F. A., J. N. Simonsen, H. Chubb, L. Slaney, J. Kimata, M. Bosire, J. O. Ndinja-Achola, and E. N. Ngugi. 1989. Epidemiologic evidence for the development of serovar-specific immunity after gonococcal infection. J. Clin. Investig. 83:1472-1476.
42. Ram, S., D, P. McQuillen, S. Gulati, C. Elkins, M. K. Pangburn, and P. A. Rice. 1998. Binding of complement factor H to loop S of porin protein 1A: a molecular mechanism of serum resistance of nonsialylated Neisseria gonorrhoeae. J. Exp. Med. 188:671-680.
43. Segal, E., E. Billyard, M. So, S. Storzbach, and T. F. Meyer. 1985. Role of chromosomal rearrangement in N. gonorrhoeae pilus phase variation. Cell 40:293-300.
44. Segal, E., P. Hagblom, H. S. Seifert, and M. So. 1986. Antigenic variation of gonococcal pilus involves assembly of separated silent gene segments. Proc. Natl. Acad. Sci. USA 83:2177-2181.
45. Seifert, H. S., R. S. Ajioka, C. Marchal, P. F. Sparling, and M. So. 1988. DNA transformation leads to pilin antigenic variation in Neisseria gonorrhoeae. Nature 336:392-395.
46. Smith, J. M. 1992. Analyzing the mosaic structure of genes. J. Mol. Evol. 34:126-129.
47. Smith, J, M., C. G. Dowson, and B. G. Spratt. 1991. Localized sex in bacteria. Nature 349:29-31.
48. Smith, N. H., J. Maynard Smith, and B. G. Spratt. 1995. Sequence evolution of the porB gene of Neisseria gonorrhoeae and Neisseria meningitidis: evidence of positive Darwinian selection. Mol. Biol. Evol. 12:363-370.
49. Tam, M. R., T. M. Buchanan, E. G. Sandstrom, K. K. Holmes, J. S. Knapp, A. W. Siadak, and R. C. Nowinski. 1982. Serological classification of Neisseria gonorrhoeae with monoclonal antibodies. Infect. Immun. 36:1042-1053.
50. van der Ley, P., H. J. E., M. Virji, P. Hoogerhout, and J. T. Poolman. 1991. Topology of outer membrane porins in pathogenic Neisseria spp. Infect. Immun. 59:2963-2971.
51. van Putten, J. P., T. D. Duensing, and J. Carlson. 1998. Gonococcal invasion of epithelial cells driven by P.IA, a bacterial ion channel with GTP binding properties. J. Exp. Med. 188:941-952.
52. Virji, M., J. N. Fletcher, K. Zak, and J. E. Heckels. 1987. The potential protective effect of monoclonal antibodies to gonococcal outer membrane protein IA. J. Gen. Microbiol. 133:2639-2646.
53. Virji, M., K. Zak, and J. E. Heckels. 1986. Monoclonal antibodies to gonococcal outer membrane protein IB: use in the investigation of the potential protective effect of antibodies directed against conserved and type-specific epitopes. J. Gen. Microbiol. 133:1621-1629.
54. Weiss, M. S., U. Abele, J. Weckesser, W. Welte, E. Schiltz, and G. E. Schulz. 1991. Molecular architecture and electrostatic properties of a bacterial porin. Science 254:1627-1630.
55. Yorke, J. A., H. W. Hethcote, and A. Nold. 1978. Dynamics and control of the transmission of gonorrhea. Sex. Transm. Dis. 5:51-56.
56. Zhang, Q. Y., D. DeRyckere, P. Lauer, and M. Koomey. 1992. Gene conversion in Neisseria gonorrhoeae: evidence for its role in pilus antigenic variation. Proc. Natl. Acad. Sci. USA 89:5366-5370.