Transformation competence and type-4 pilus biogenesis in Neisseria gonorrhoeae - A review

Gene

Volumn 192, Issue 1, 1997, Pages 125-134

  Fussenegger, Martin ^a,b   Rudel, Thomas ^c,d   Barten, Roland ^a   Ryll, Roland ^a   Meyer, Thomas F ^a,c  

^a MAX PLANCK INST FÜR BIOLOGIE   (Germany)

^b ETH ZURICH   (Switzerland)

^c MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Antigenic variation; DNA processing; DNA uptake; Horizontal exchange; Peptidoglycan; Population structure

Indexed keywords

MEMBRANE PROTEIN; PEPTIDOGLYCAN; PROTEIN SUBUNIT;

BACTERIUM PILUS; BACTERIUM TRANSFORMATION; BIOGENESIS; CHROMOSOME; CONFERENCE PAPER; DNA TRANSFER; EPITHELIUM CELL; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENE POOL; NEISSERIA GONORRHOEAE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY;

BACTERIA (MICROORGANISMS); NEISSERIA; NEISSERIA GONORRHOEA; NEISSERIA GONORRHOEAE;

EID: 0030920498     PISSN: 03781119     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0378-1119(97)00038-3     Document Type: Conference Paper

References (93)

1. Achtman, M. (1994) Clonal spread of serogroup A meningococci. A paradigm for the analysis of microevolution in bacteria. Mol. Microbiol. 11, 15-22.
2. Achtman, M. (1997) Microevolution and epidemic spread of sero-group A Neisseria meningitidis - a review. Gene 192, 135-140.
3. Alm, R.A. and Mattick, J.S. (1997) Genes involved in the biogenesis of type-4 fimbriae in Pseudomonas aeruginosa. Gene 192, 89-98.
4. Bautsch, W. (1993) A NheI macrorestriction map of the Neisseria meningitidis B1940 genome. FEMS Microbiol. Lett. 107, 191-197.
5. Bihlmaier, A., Römling, U., Meyer, T.F., Tümmler, B. and Gibbs, C.P. (1991) Physical and genetic map of the Neisseria gonorrhoeae strain MS11-N178 chromosome. Mol. Microbiol. 5, 2529-2539.
6. Biswas, G.D., Sox, T. Blackman, E. and Sparling, P.F (1977) Factors affecting genetic transformation of Neisseria gonorrhoeae. J. Bacteriol. 129, 983-992.
7. Biswas, G.D., Burnstein K.L. and Sparling, P.F. (1986) Linearization of Donor DNA during plasmid transformation in Neisseria gonorrhoeae. J. Bacteriol. 168, 756-761.
8. Breitling, R. and Dubnau, D. (1990) A pilin-like membrane protein is essential for DNA binding by competent Bacillus subtilis. J. Bacteriol. 172, 1499-1508.
9. Broome-Smith, J.K., Edelman, A., Yousif, S. and Spratt, B.G. (1985) The nucleotide sequences of the ponA and ponB genes encoding penicillin-binding proteins 1A and 1B of Escherichia coli. Eur. J. Biochem. 147, 437-446.
10. Catlin, B.W. and Cunningham, L.S. (1961) Transforming activities and base contents of deoxyribonucleate preparations from various Neisseriae. J. Gen. Microbiol. 26, 303-312.
11. Clifton, S.W., McCarthy, D. and Roe, B.A. (1994) Sequence of the rec-2 locus of Haemophilus influenzae: homolgies to comE-ORF3 of Bacillus subtilis and msbA of Escherichia coli. Gene 146, 95-100.
12. d'Enfert, C. and Pugsley, A.P. (1989) Klebsialla pneumoniae pulS gene encodes an outer membrane lipoprotein required for pullulanase secretion. J. Bacteriol. 171, 3673-3679.
13. Drake, S.L. and Koomey, M. (1995) The product of the pilQ gene is essential for the biogenesis of type IV pili in Neisseria gonorrhoeae. Mol. Microbiol. 18, 975-986.
14. Dubnau, D. (1991) Genetic competence of Bacillus subtilis. Microbiol. Rev. 55, 395-424.
15. Facius, D. and Meyer, T.F. (1993) A novel determinant (comA) essential for natural transformation competence in Neisseria gonorrhoeae and the effect of a comA mutant on pilin variation. Mol. Microbiol. 10, 699-712.
16. Facius, D., Fussenegger, M., and Meyer, T.F. (1996) Sequential function of factors involved in natural competence for transformation of Neisseria gonorrhoeae. FEMS Lett. 137, 159-164.
17. Feavers, I.M, Heath, A.B., Bygraves, J.A. and Maiden, M.C.J. (1992) Role of horizontal genetic exchange in the antigenic variation of the class 1 outer membrane protein of Neisseria meningitidis. Mol. Microbiol. 6, 489-495.
18. Forest, K.T. and Tainer, J.A. (1997) Type-4 pilus structure: outside to inside and top to bottom - a minireview. Gene 192, 165-169.
19. Freitag, N.E., Seifert, H.S. and Koomey, M. (1995) Characterzation of the pilF-pilD pilus-assembly locus of Neisseria gonorrrhoeae. Mol. Microbiol. 16, 575-586.
20. Frosch, M. and Meyer, T.F. (1992) Transformation-mediated exchange of virulence determinants by co-cultivation of pathogenic Neisseriae. FEMS Microbiol. Lett. 100, 3435-3439.
21. Frosch, M., Weiseberger, C. and Meyer, T.F. (1989) Molecular characterization and expression in Escherichia coli of the gene complex encoding the polysaccaride capsule of Neisseria meningitidis group B. Proc. Natl. Acad. Sci. USA 86, 1669-1673.
22. Fussenegger, M., Facius, D., Meier, J. and Meyer, T.F. (1996a) A novel peptidoglycan-linked lipoprotein (ComL) that functions in natural transformation competence of Neisseria gonorrhoeae. Mol. Microbiol. 19, 1095-1105.
23. Fussenegger, M., Kahrs, A.F., Facius, D. and Meyer, T.F. (1996b) Tetrapac (tpc), a novel genotype of Neisseria gonorrhoeae affecting cell invasion, natural transformation competence and cell separation. Mol. Microbiol. 19, 1357-1372.
24. Gibbs, C.P. and Meyer, T.F. (1996) Genome plasticity in Neisseria gonorrhoeae. FEMS Microbiol. Lett. 145, 173-179.
25. Gibbs, C.P., Reinmann, B.-Y., Schultz, F., Kaufmann, A., Haas, R. and Meyer T.F. (1989) Reassortment of pilin genes in Neisseria gonorrhoeae occurs by two distinct mechanisms. Nature 338, 651-652.
26. Goodman, S.D. and Scocca, J.J. (1988) Identification and arrangement of the DNA sequence recognized in specific transformation of Neisseria gonorrhoeae. Proc. Natl. Acad. Sci. USA 85, 6982-6986.
27. Haas, R. and Meyer, T.F. (1986) The repertoire of silent pilus genes in Neisseria gonorrhoeae: evidence for gene conversion. Cell 44, 107-115.
28. Haas, R. and Meyer, T.F. (1992) Silent pilin genes of Neisseria gonorrhoeae MS11 and the occurrence of related hypervaraint sequences among gonococcal isolates. Mol. Microbiol. 6, 197-208.
29. Haas, R., Schwarz, H. and Meyer, T.F. (1987) Release of soluble pilin antigen coupled with gene conversion in Neisseria gonorrhoeae. Proc. Natl. Acad. Sci. USA 84, 9079-9083.
30. Hagblom, P., Segal, E., Billyard, E. and So, M. (1985) Intragenic recombination leads to pilus antigenic variation in Neisseria gonorrhoeae. Nature 315, 156-158.
31. Hahn, J., Inamine, G., Kozlov, Y. and Dubnau, D. (1993) Characterization of comE, a late competence operon of Bacillus subtilis required for the binding and uptake of transforming DNA. Mol. Microbiol. 10, 99-111.
32. Halter, R., Pohlner, J. and Meyer, T.F. (1989) Mosaic-like organisation of IgA protease genes in Neisseria gonorrhoeae generated by horizontal genetic exchange in vivo. EMBO J. 8, 2737-2744.
33. Hill, S.A. (1996) Limited variation and maintenance of tight genetic linkage characterize heteroallelic pilE recombination following DNA transformation of Neisseria gonorrhoeae. Mol. Microbiol. 20, 507-518.
34. Hill, S.A., Morrison, S.G. and Swanson, J. (1990) The role of direct oligonucleotide repeats in gonococcal pilin gene variation. Mol. Microbiol. 4, 1341-1352.
35. Hobbs, M. and Mattick, J.S. (1993) Common components in the assembly of type-4 fimbriae, DNA transfer systems, filamentous phage and protein-secretion apparatus: a general system for the formation of surface-associated protein complexes. Mol. Microbiol. 10, 233-243.
36. Hobbs, M.M., Seiler, A., Achtmann, M., and Cannon, J.G. (1994) Microevolution within a clonal population of pathogenic bacteria: recombination, gene duplication and horizontal genetic exchange in the opa gene family of Neisseria meningitidis. Mol. Microbiol. 12, 171-180.
37. Hoyne, P.A., Haas, R., Meyer, T.F., Davies, J. and Elleman, T.C. (1992) Production of Neisseria gonorrhoeae pili (fimbriae) in Pseudomonas aeruginosa. J. Bact. 174, 7321-7327.
38. Höltje, J.-V. (1993) Three for one - a simple growth mechanism that guarantees a precise copy of the thin, rodshaped murein sacculus of Escherichia coli. In: de Pedro, M.A, Höltje, J.-V. and Löffelhardt, W. (Eds.), Bacterial Growth and Lysis Metabolism and Structure of the Bacterial Sacculus. Plenum, New York, pp. 419-426.
39. Inamine, G.S. and Dubnau, D. (1995) ComEA, a Bacillus subtilis integral inner membrane protein required for genetic transformation, is needed for both DNA binding and transport. J. Bacteriol. 177, 3045-3051.
40. Iredell, J.R. and Manning, P.A. (1994) The toxin-co-regulated pilus of Vibrio cholerae O1: a model for type-4 pilus biogenesis? Trends Microbiol. 2, 187-192.
41. Jonsson, A.-B., Nyberg, G. and Normark, S. (1991) Phase variation of gonococcal pili by frame shift mutation in pilC, a novel gene for pilus assembly. EMBO J. 10, 477-488.
42. Jonsson, A.-B., Pfeifer, J. and Normark, S. (1992) Neisseria gonorrhoeae PilC expression provides a selective mechanism for structural diversity of pili. Proc. Natl. Acad. Sci. USA 89, 3204-3208.
43. Jonsson, A.-B., Ilver, D. Falk, P., Pepose, J. and Normark, S. (1994) Sequence changes in the pilus subunit lead to tropism variation of Neisseria gonorrhoeae to human tissue. Mol. Microbiol. 12, 403-416.
44. Koomey, J.M., Gotschlich, E.C., Robbins, K., Bergström, S. and Swanson, J. (1987) Effects of recA mutation on pilus antigenic variation and phase transition in Neisseria gonorrhoeae. Genetics 117, 391-398.
45. Kupsch, E.-M., Knepper, B., Kuroki, T., Heuer, I. and Meyer, T.F. (1993) Variable opacity (Opa) outer membrane proteins account for the cell tropisms displayed by Neisseria gonorrhoeae for human leukocytes and epithelial cells. EMBO J. 12, 641-650.
46. Lacks, S., Greenberg, B. and Neuberger, M. (1974) Role of a deoxyribonuclease in the transformation of Diplococcus pneumonieae. Proc. Natl. Acad. Sci. USA 71, 2305-2309.
47. Larson, T.G. and Goodgal, S.H. (1991) Donor DNA processing is blocked by a mutation in the comlOlA locus of Haemophilus influenzae. J. Bacteriol. 174, 3392-3394.
48. Lawson, F.S., Billowes, F.M., and Dillon, J.-A.R. (1995) Organization of carbamoyl-phosphate synthetase genes in Neisseria gonorrhoeae includes a large, variable intergeneic sequence which is also present in other Neisseria species. Microbiology 141, 1183-1191.
49. Lauer, P., Albertson, N.H. and Koomey, M. (1993) Conservation of genes encoding components of a type IV pilus assembly/two-step export pathway in Neisseria gonorrhoeae. Mol. Microbiol. 8, 357-368.
50. Lorenz, M.G. and Wackernagel W. (1994) Bacterial gene transfer by natural genetic transformation in the environment. Microbiol. Rev. 58, 563-602.
51. Manning, P.A., Kaufmann, A., Roll, U., Pohlner, J., Meyer, T.F. and Haas, R. (1991) L-pilin variants of Neisseria gonorrhoeae MS11. Mol. Microbiol. 5, 917-926.
52. Martin, P.R., Hobbs, M., Free, P.D., Jeske, Y. and Mattick, J.S. (1993) Charactersation of pilQ, a new gene required for the biogenesis of type-4 fimbriae in Pseudomonas aeruginosa. Mol. Microbiol. 9, 857-868.
53. Maynard Smith, J., Dawson, C.G. and Spratt, B.G. (1991) Localized sex in bacteria. Nature 349, 29-31.
54. Maynard Smith, J., Smith, N.H., O'Rourke, M. and Spratt, B.G. (1993) How clonal are bacteria? Proc. Natl. Acad. Sci. USA 90, 4384-4388.
55. Meyer, T.F. (1990) Variation of pilin and opacity-associated protein in pathogenic Neisseria species. In: B. Iglewski and V. Clark. (Eds.) The Bacteria 43 - Molecular Basis of Bacterial Pathogenesis. Academic Press, New York, pp. 137-159.
56. Meyer, T.F., Billyard, E., Haas, R., Störzbach, S. and So, M. (1984) Pilus gene of Neisseria gonorrhoeae: chromosomal organization and DNA sequence. Proc. Natl. Acad. Sci. USA 81, 6110-6114.
57. Meyer, T.F., Pohlner, J. and Van Putten, J.P.M. (1994) Biology of the pathogenic Neisseriae. Curr. Top. Microbiol. 192, 283-317.
58. Nassif, X., Lowy, J., Stenberg, P., O'Gaora, P., Ganji, A. and So, M. (1993) Antigenic variation of pilin regulates adhesion of Neisseria meningitidis to human epithelial cells. Mol. Microbiol. 8, 719-725.
59. Ogierman, M.A., Zabihi, S., Mourtziol, L. and Manning, P.A. (1993) Genetic organization and sequence of the promoter-distal region of the tcp gene cluster of Vibrio choloerae. Gene 126, 51-60.
60. Parge, H.E., Forest, K.T., Hickey, M.J., Christensen, D.A., Getzoff, E.D. and Tainer, J.A. (1995) Structure of the fibre-forming protein pilin at 2.6 Å resolution. Nature 378, 32-38.
61. Pifer, M.L. and Smith, O. (1985) Processing of donor DNA during Haemophilus influenzae transformation: analysis using a model plasmid system. Proc. Natl. Acad. Sci. USA 82, 3731-3735.
62. Pugsley, A.P., Francetic, O., Possot, O.M., Sauvonnet, N. and Hardie, K.R. (1997) Recent progress and future directions in studies of the main terminal branch of the general secretory pathway in Gramnegative bacteria - a review. Gene 192, 13-19.
63. Robertson, B.D.R., Frosch, M. and van Putten, J.P.M. (1993) The role of galE in the biosynthesis and function of gonococcal lipopolysaccharide. Mol. Microbiol. 8, 891-901.
64. Rudel, T., van Putten, J.P.M., Gibbs, C.P., Haas, R. and Meyer, T.F. (1992) Interaction of two variable proteins (PilE and PilC) required for pilus-mediated adherence of Neisseria gonorrhoeae to human epithelial cells. Mol. Microbiol. 22, 3439-3450.
65. Rudel, T., Facius, D., Barten, R., Nonnenbacher, E. and Meyer, T.F. (1995a) Dissecting the process of natural transformation competence in Neisseria gonorrhoeae and the role of phase variable proteins. Proc. Natl. Acad. Sci. USA 92, 7986-7990.
66. Rudel, T., Scheuerpflug, I. and Meyer, T.F. (1995b) Neisseria PilC protein identified as type-4 pilus tip-located adhesin. Nature 373, 357-359.
67. Rudel, T., Boxberger, H.-J. and Meyer, T.F. (1995c) Pilus biogenesis and epithelial cell adherence of Neisseria gonorrhoeae pilC double knock-out mutants. Mol. Microbiol. 17, 1057-1071.
68. Russel, M. (1991) Filamentous phage assembly. Mol. Microbiol. 5, 1607-1613.
69. Russel, M., Linderoth, N.A. and Sali, A. (1997) Filamentous phage assembly: variation on a protein export theme. Gene 192, 23-32.
70. Sansonetti, P. (1992) Pathogenesis of Shigellosis. Curr. Top. Microbiol. Immunol. 180, 1-143.
71. Schwarz, U., Asmus, A. and Frank, H. (1969) Autolytic enzymes and cell division in Escherichia coli. J. Mol. Biol. 41, 419-429.
72. Seifert, H.S., Ajioka, R.S., Marchal, C., Sparling, P.F. and So, M. (1988) DNA transformation leads to pili antigenic variation in Neisseria gonorrhoeae. Nature 336, 392-395.
73. Sparling, P.F. (1966) Genetic transformation of Neisseria gonorrhoeae to streptomycin resistance. J. Bacteriol. 92, 1364-1369.
74. Spratt, B.G., Bowler, L.D., Zhang, Q.-Y., Zhon, J. and Smith J.M (1992) Role of interspecies transfer of chromosomal genes in the evolution of penicillin resistance in pathogenic and commensal Neisseria species. J. Mol. Evol. 34, 115-125.
75. Stein, C.D., Chien, R. and Seifert, H.S. (1992) Construction of a Neisseria gonorrhoeae MS11 derivative deficient in NgoMI restriction and modification. J. Bacteriol. 174, 4899-4906.
76. Stern, A., Brown, M., Nickel, P. and Meyer, T.F. (1986) Opacity genes in Neisseria gonorrhoeae: control of phase and antigenic variation. Cell 47, 61-71.
77. Strahley, S., Skrzypek, E., Plano, G. and Bliska, J.G. (1993) The Yops of the human-pathogenic Yersinia. Infect. Immun. 61, 3105-3110.
78. Strom, M.S. and Lory, S. (1986) Cloning and expression of the pilin gene of Pseudomonas aeruginosa PAK in Escherichia coli. J. Bacteriol. 165, 367-372.
79. Strom, M.S. and Lory, S. (1993) Structure-function and biogenesis of the type IV pili. Annu. Rev. Microbiol. 47, 565-596.
80. Swanson, J. (1973) Studies on gonococcus infection. Pili: their role in attachment of gonococci to tissue culture cells. J. Exp. Med. 173, 571-589.
81. Swanson, J., Berström, S., Robbins, K., Barrera, O. and Koomey, M.J. (1986) Gene conversion involving the pilin structural gene correlates with the pilus+ to pilus- changes in Neisseria gonorrhoeae. Cell 47, 267-276.
82. Tomb, J.-F., El-Hajj, H. and Smith, H.O. (1991) Nucleotide sequence of a cluster of genes involved in transformation of Haemophilus influenzae Rd. Gene 104, 1-10.
83. Tønjum, T. and Koomey, M. (1997) The pilus colonization factor of pathogenic neisserial species: organelle biogenesis and structure/function relationships - a review. Gene 192, 155-163.
84. Tønjum, T., Freitag, N.E., Namork, E. and Koomey, M. (1995) Identification and characterization of pilG, a highly conderved pilus-assembly gene in pathognic Neisseria. Mol. Microbiol. 16, 451-464.
85. Tsai, W.-M., Larsen, S.H. and Wilde, C.E. (1989) Cloning and DNA sequence of the omc gene encoding the outer membrane protein-macromolecular complex from Neisseria gonorrhoeae. Infect. Immun. 57, 2653-2659.
86. Virji, M. and Heckels, J.E. (1984) The role of common and type-specific antigenic domains in adhesion and rivulence of gonoccci for human epithelial cells. J. Gen. Microbiol. 130, 1089-1095.
87. Virji, M., Alexandrescu, C., Ferguson, D.J.P., Saunders, J. and Moxon, E.R. (1992) Variations in the expression of pili: the effect on adherence of Neisseria meningitidis to human epithelial and endothelial cells. Mol. Microbiol. 6, 1271-1279.
88. Virji, M. (1997) Post-translational modifications of meningococcal pili. Identification of common substituents: glycans and α-glycerophosphate - a review. Gene 192, 141-147.
89. Walderich, B. and Höltje, J.-V. (1991) Subcellular distribution of the soluble lytic transglycosylase in Escherichia coli. J. Bacteriol. 173, 5668-5676.
90. Ward, M.E., Watt, P.J. and Robertson, J.N. (1974) The human fallopian tube: a model for gonococcal infection. J. Inf. Dis. 129, 650-659.
91. Young, F.E. and Spizizen, J. (1963) Biochemical aspects of competence in the Bacillus subtilis transformation system. J. Biol. Chem. 238, 3126-3130.
92. Zhang, Q.Y, DeRyckere, D., Lauer, P. and Koomey J.M. (1992) Gene conversion in Neisseria gonorrhoeae: evidence for its role in pilus antigenic variation. Proc. Natl. Acad. Sci. USA 89, 5366-5370.
93. Zhou, J. and Spratt, B.G. (1992) Sequence diversity within the argF, fbp and recA genes of natural isolates of Neisseria meningitidis -interspecies recombination within the argF gene. Mol. Microbiol. 6, 2135-2146.