Chapter 8 : Mechanisms of Pilus Antigenic Variation in Neisseria gonorrhoeae

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Mechanisms of Pilus Antigenic Variation in Neisseria gonorrhoeae, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818340/9781555810825_Chap08-1.gif /docserver/preview/fulltext/10.1128/9781555818340/9781555810825_Chap08-2.gif


The alteration of gene expression by DNA rearrangement appears to be an essential part of most biological systems. When an extremely high level of diversification for a set of gene products with a common function is advantageous, these rearrangements are achieved by the reassortment and recombination of repeated gene segments. The generation of the variable domains in avian immunoglobulins, antigenic variation of surface proteins in African trypanosomes and , and pilus antigenic variation in each results from the transfer of genetic information from nonexpressed donor alleles or pseudogenes to an active expression locus, a process likened to gene conversion occurring in spore-forming fungi. In this chapter, the author concentrates primarily on recent studies that have influenced understanding of variable pilus expression in gonococci. The vast majority of recombination events between double-stranded DNA forms of the filamentous bacteriophage f1 appear to be a consequence of gene conversion, and the mechanism appears to be the formation of asymmetric heteroduplex molecules. It may also seem that reciprocal exchange and gene conversion demand fundamentally distinct recombination reactions, but mechanistically, these two outcomes may simply be alternative resolutions of the same basic event. The identification of equivalent gonococcal genes by interspecies complementation or by virtue of their DNA homologies and the construction of mutants altered in their expression should make it possible to define their role in the chemistry of the exchange reaction.

Citation: Koomey M. 1994. Mechanisms of Pilus Antigenic Variation in Neisseria gonorrhoeae, p 113-126. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch8
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
Figure 1

Pilin variation occurring in the absence of transformation. Pilin amino acid sequences (derived from DNA sequencing of pilE-containing plasmid clones) are of P+ revertants arising from the nonpiliated strain NN99 - ClaI during propagation in the presence of DNase I ( ). The arrow indicates the location of the ClaI restriction site encompassing a frameshift mutation in pilE used to demonstrate the nonreciprocal character of the recombination events responsible for reversion. See the text and reference 62 for details. Amino acids are noted by single-letter code. Boxed residues indicate conserved pilin domains. Numbers on the left refer to revertant strain designations, while the numbering of the residues is based on those found in mature pilin. Revertants are ordered to emphasize the use of identical (or highly related) partial pilin gene copies as donors in productive recombination events. Revertants 73, 79, and 83 represent the use of one donor allele, 74 and 85 represent the use of another donor allele, and 78, 86, and 89 represent the use of a third donor allele. Solid underlining denotes the corresponding minimal nucleotide stretches introduced by recombination.

Citation: Koomey M. 1994. Mechanisms of Pilus Antigenic Variation in Neisseria gonorrhoeae, p 113-126. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch8
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Barbour, A., 1989. Antigenic variation in relapsing fever Borrelia species: genetic aspects, p. 783 789. In D. E. Berg, and M. M. Howe (ed.), Mobile DNA. American Society for Microbiology, Washington, D.C.
2. Bergstrom, S.,, K. Rabbins,, J. M. Koomey,, and J. Swanson. 1986. Piliation control mechanisms in Neisseria gonorrhoeae. Proc. Natl. Acad. Sci. USA 83: 3890 3894.
3. Biswas, G. D.,, S. A. Lacks,, and P. F. Sparling. 1989. Transformation-deficient mutants of piliated Neisseria gonorrhoeae. J. Bacteriol. 171: 657 664.
4. Boon, T.,, and N. D. Zinder. 1971. Genotypes produced by individual recombination events involving bacteriophage fl. J. Mol. Biol. 58: 133 151.
5. Borst, P.,, and D. R. Greaves. 1987. Programmed gene rearrangements altering gene expression. Science 235: 658 667.
6. Buchanan, T. M. 1975. Antigenic heterogeneity of gonococcal pili. J. Exp. Med. 141: 1470 1475.
7. Donelson, J. E.,, and A. C. Rice-Ficht. 1985. Molecular biology of trypanosome antigenic variation. Microbiol. Rev. 49: 107 125.
8. Elleman, T. C, and P. A. Hoyne. 1984. Nucleotide sequence of the gene encoding pilin of Bacteroides nodosus, the causal organism of ovine footrot. J. Bacteriol. 160: 1184 1187.
9. Enea, V.,, G. F. Vovis,, and N. D. Zinder. 1975. Genetic studies of heteroduplex DNA of bacteriophage fl. Asymmetric segregation, base correction and implications for the mechanism of genetic recombination. J. Mol. Biol. 96: 495 509.
10. Gibbs, C. P.,, B. Y. Reimann,, E. Schultz,, A. Kaufman,, R. Haas,, and T. F. Meyer. 1989. Reassortment of pilin genes in Neisseria gonorrhoeae occurs by two distinct mechanisms. Nature (London) 338: 651 652.
11. Giron, J. A.,, A. S. Y. Ho,, and G. K. Schoolnik. 1991. An inducible bundle-forming pilus of enteropathogenic Escherichia coli. Science 254: 710 713.
12. Haas, R.,, and T. F. Meyer. 1986. The repertoire of silent pilus genes in Neisseria gonorrhoeae: evidence for gene conversion. Cell 44: 107 115.
13. Haas, R.,, H. Schwarz,, and T. F. Meyer. 1987. Release of soluble pilin antigen coupled with gene conversion in Neisseria gonorrhoeae. Proc. Natl. Acad. Sci. USA 84: 9079 9083.
14. Hagblom, P.,, E. Segal,, E. Billyard,, and M. So. 1985. Intragenic recombination leads to pilus antigenic variation in Neisseria gonorrhoeae. Nature (London) 315: 156 158.
15. Hartman, N.,, and N. D. Zinder. 1974. The effect of B specific restriction and modification of DNA on linkage relationships in fl bacteriophage. II. Evidence for a heteroduplex intermediate in f1 recombination. J. Mol. Biol. 85: 357 369.
16. Hastings, P. J., 1988. Conversion events in fungi, p. 397 428 In R. Kucharlapati, and G. R. Smith (ed.), Genetic Recombination. American Society for Microbiology, Washington, D.C.
17. Hebeler, B. H.,, and F. E. Young. 1975. Autolysis of Neisseria gonorrhoeae. J. Bacteriol. 122: 385 392.
18. Helling, R. B. 1967. The effect of arabinose-specific enzyme synthesis on recombination in the arabinose genes of Escherichia coli. Genetics 57: 665 675.
19. Henrichsen, J. 1983. Twitching motility. Annu. Rev. Microbiol. 37: 81 93.
20. Hermodson, M. A.,, K. C. Chen,, and T. M. Buchanan. 1978. Neisseria pili proteins: amino-terminal amino acid sequences and identification of an unusual amino acid. Biochemistry 17: 442 445.
21. Hill, S. A.,, S. G. Morrison,, and J. Swanson. 1990. The role of direct oligonucleotide repeats in gonococcal pilin gene variation. Mol. Microbiol. 4: 1341 1352.
22. Jonsson, A. B.,, G. Nyberg,, and S. Normark. 1991. Phase variation of gonococcal pili by frameshift mutation in pilC, a novel gene for pilus assembly. EMBO J. 10: 477 488.
23. Jonsson, A. B.,, J. Pfeifer,, and S. Normark. 1992. Neisseria gonorrhoeae PilC expression provides a selective mechanism for structural diversity of pili. Proc. Natl. Acad. Sci. USA 89: 3204 3208.
24. Kellog, D. S.,, I. R. Cohen,, L. C. Norins,, A. L. Schroeter,, and G. Reising. 1968. Neisseria gonorrhoeae. II. Colonial variation and pathogenicity during 35 months in vitro. J. Bacteriol. 96: 596 605.
25. Koomey, M.,, E. C. Gotschlich,, K. Robbins,, S. Bergstrom,, and J. Swanson. 1987. Effects of recA mutations on pilus antigenic variation and phase transitions in Neisseria gonorrhoeae. Genetics 117: 391 398.
26. Koomey, M.,, and Q. Y. Z. Zhang. Unpublished data.
27. Kostriken, R.,, N. Strathern,, A. J. Sklar,, J. B. Hicks,, and F. Heffron. 1983. A site-specific endonuclease essential for mating-type switching in Saccharomyces cerevisiae. Cell 35: 167 174.
28. Marrs, C. F.,, G. Schoolnik,, J. M. Koomey,, J. Hardy,, J. Rothbard,, and S. Falkow. 1985. Cloning and sequencing of a Moraxella bovis pilin gene. J. Bacteriol. 163: 132 139.
29. Meyer, T. F.,, E. Billyard,, R. Haas,, S. Storzbach,, and M. So. 1984. Pilus genes of Neisseria gonorrheae: chromosomal organization and DNA sequence. Proc. Natl. Acad. Sci. USA 81: 6110 6114.
30. Meyer, T. F.,, C. P. Gibbs,, and R. Haas. 1990. Variation and control of protein expression in Neisseria. Annu. Rev. Microbiol. 44: 451 477.
31. Meyer, T. F.,, N. Mlawer,, and M. So. 1982. Pilus expression in Neisseria gonorrhoeae involves chromosomal rearrangement. Cell 30: 45 52.
32. Murphy, G. L.,, T. D. Connell,, D. S. Barrit,, M. Koomey,, and J. G. Cannon. 1989. Phase variation of gonococcal protein. II. Regulation of gene expression by slipped-strand mispairing of a repetitive DNA sequence. Cell 56: 539 547.
33. Norlander, L.,, J. Davies,, A. Norqvist,, and S. Normark. 1979. Genetic basis for colonial variation in Neisseria gonorrhoeae. J. Bacteriol. 138: 762 769.
34. Pasloske, B. L.,, B. B. Finlay,, and W. Paranchych. 1985. Cloning and sequencing of the Pseudomonas aeruginosa PAK pilin gene. FEBS Lett. 183: 408 412.
35. Plasterk, R. H. A.,, M. I. Simon,, and A. G. Barbour. 1985. Transposition of structural genes to an expression sequence on a linear plasmid causes antigenic variation in the bacterium Borrelia hermsii. Nature (London) 318: 257 263.
36. Pugsley, A. P. 1993. The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 57: 50 108.
37. Reynaud, C.-A.,, V. Anquez,, H. Grimal,, and J.-C. Weill. 1987. A hyperconversion mechanism generates the chicken light chain gene preimmune repertoire. Cell 48: 379 388.
38. Rudel, T.,, J. P. M. van Putten,, C. P. Gibbs,, R. Hass,, and T. F. Meyer. 1992. Interaction of two variable proteins (PilE and PilC) required for pilus-mediated adherence of Neisseria gonorrhoeae to human epithelial cells. Mol. Microbiol. 6: 3439 3450.
39. Scocca, J. J. 1990. The role of transformation in the variability of the Neisseria gonorrhoeae cell surface. Mol. Microbiol. 4: 321 327.
40. 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.
41. Segall, A. M.,, and J. R. Roth. 1989. Recombination between homologies in direct and inverse orientation in the chromosome of Salmonella: intervals which are nonpermissive for inversion formation. Genetics 122: 737 747.
42. Seifert, H. S.,, R. Ajioka,, and M. So. 1988. Alternative model for Neisseria gonorrhoeae pilin variation. Vaccine 6: 107 109.
43. 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 (London) 336: 392 395.
44. Shaw, C. E.,, and R. K. Taylor. 1990. Vibrio cholerae 0395 tcpA pilin gene sequence and comparison of the predicted protein structural features to those of type IV pilins. Infect. Immun. 58: 3042 3049.
45. Simon, M.,, and I. Herskowitz,. 1985. Introduction, p. xv xix. In M. Simon, and I. Herskowitz (ed.), Genome Rearrangement. Alan R. Liss, Inc., New York.
46. Smith, G. R. 1988. Homologous recombination in prokaryotes. Microbiol. Rev. 52: 1 28.
47. Sparling, P. F. 1966. Genetic transformation of Neisseria gonorrhoeae to streptomycin resistance. J. Bacteriol. 92: 1364 1371.
48. Swanson, J.,, and O. Barrera. 1983. Gonococcal pilus subunit size heterogeneity correlates with transitions in colony piliation phenotype, not with changes in colony opacity. J. Exp. Med. 158: 1459 1472.
49. Swanson, J.,, S. Bergstrom,, O. Barrera,, K. Robbins,, and D. Corwin. 1985. Pilus~ gonococcal variants. Evidence for multiple forms of piliation control. J. Exp. Med. 162: 729 744.
50. Swanson, J.,, S. Bergstrom,, K. Robbins,, O. Barrera,, D. Corwin,, and J. M. Koomey. 1986. Gene conversion involving the pilin structural gene correlates with pilus + pilus - changes in Neisseria gonorrhoeae. Cell 47: 267 276.
51. Swanson, J.,, and J. M. Koomey,. 1989. Mechanisms for variation of pili and outer membrane protein II in Neisseria gonorrhoeae, p. 743 761 In D. E. Berg, and M. M. Howe (ed.), Mobile DNA. American Society for Microbiology, Washington, D.C.
52. Swanson, J.,, S. J. Kraus,, and E. C. Gotschlich. 1971. Studies on gonococcus infection. I. Pili and zones of adhesion: their relation to gonococcal growth patterns. J. Exp. Med. 134: 886 906.
53. Swanson, J.,, S. Morrison,, O. Barrera,, and S. Hill. 1990. Piliation changes in tranformation-defective Neisseria gonorrhoeae. J. Exp. Med. 171: 2131 2139.
54. Swanson, J.,, K. Robbins,, O. Barrera,, D. Corwin,, J. Boslego,, J. Ciak,, M. Blake,, and J. M. Koomey. 1987. Gonococcal pilin variants in experimental gonorrhea. J. Exp. Med. 165: 1344 1357.
55. Swanson, J.,, K. Robbins,, O. Barrera,, and J. M. Koomey. 1987. Gene conversion variations generate structurally distinct pilin polypeptides in Neisseria gonorrhoeae. J. Exp. Med. 165: 1016 1025.
56. Thompson, C. B. 1992. Creation of immunoglobulin diversity by intrachromosomal gene conversion. Trends Genet. 8: 416 422.
57. Thompson, C. B.,, and P. E. Neiman. 1987. Somatic diversification of the chicken immunoglobulin light chain gene is limited to the rearranged variable gene segment. Cell 48: 369 378.
58. Tenjum, T.,, C. Marrs,, F. Rozsa,, and K. B0vre. 1991. The type IV pilin of Moraxella nonliquefaciens exhibits unique similarities with pilins of Neisseria gonorrhoeae and Bacteroides nodosus. J. Gen. Microbiol. 137: 2483 2490.
59. Vickerman, K. 1978. Antigenic variation in trypanosomes. Nature (London) 273: 613 617,
60. Virji, M.,, J. E. Heckels,, and P. J. Watt. 1983. Monoclonal antibodies to gonococcal pili: studies on antigenic determinants on pili variants of strain P9. J. Gen. Microbiol. 129: 1965 1973.
61. Zak, K.,, J.-L. Diaz,, D. Jackson,, and J. E. Heckels. 1984. Antigenic variation during infection with Neisseria gonorrhoeae: detection of antibodies to surface proteins in sera of patients with gonorrhea. J. Infect. Dis. 149: 166 173.
62. 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.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error