Molecular switches - The ON and OFF of bacterial phase variation

Molecular Microbiology

Volumn 33, Issue 5, 1999, Pages 919-932

  Henderson, Ian R ^a   Owen, Peter ^b   Nataro, James P ^a  

^a University of Maryland School of Medicine Center for Vaccine Development   (United States)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL GENE; BASE MISPAIRING; GENE EXPRESSION; GENETIC VARIABILITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; TRANSCRIPTION REGULATION;

ADAPTATION, PHYSIOLOGICAL; AMINO ACID SEQUENCE; BACTERIA; BASE SEQUENCE; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; PROTEIN BIOSYNTHESIS; RECOMBINATION, GENETIC; TRANSCRIPTION, GENETIC;

EID: 0032881595     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1999.01555.x     Document Type: Review

References (76)

1. Abeles, A., Brendler, T., and Austin, S. (1993) Evidence of two levels of control of P1 oriR and host oriC replication origins by DNA adenine methylation. J Bacteriol 175: 7801-7807.
2. Abraham, J.M., Freitag, C.S., Clements, J.R., and Eisenstein, B.I. (1985) An invertible element of DNA controls phase variation of type 1 fimbriae of Escherichia coli. Proc Natl Acad Sci USA 82: 5724-5727.
3. Adley, C.C., and Bukhari, A.I. (1984) Methylation dependent expression of the mom gene of bacteriophage Mu: deletions downstream from the methylation sites affect expression. Nucleic Acids Res 12: 3535-3550.
4. 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.
5. Andrewes, F.W. (1922) Studies in group agglutination I. J Path Bacteriol 25: 505.
6. Andrews, J.H. (1995) What if bacteria are modular organisms. Am Soc Microbiol News 61: 627-632.
7. Barbour, A.G. (1993) Linear DNA of Borrelia species and antigenic variation. Trends Microbiol 1: 236-239.
8. van Belkum, A., Scherer, S., van Alphen, L., and Verbrugh, H. (1998) Short-sequence DNA repeats in prokaryotic genomes. Microbiol Mol Biol Rev 62: 275-293.
9. Belland, R.J. (1991) H-DNA formation by the coding repeat elements of neisserial opa genes. Mol Microbiol 5: 2351-2360.
10. Blomfield, I.C., Calie, P.J., Eberhardt, K.J., McClain, M.S., and Eisenstein, B.I. (1993) Lrp stimulates phase variation of type 1 fimbriation in Escherichia coli K-12, J Bacteriol 175: 27-36.
11. Blomfield, I.C., Kulasekara, D.H., and Eisenstein, B.I. (1997) Integration host factor stimulates both FimB-and FimE-mediated site-specific DNA inversion that controls phase variation of type 1 fimbriae expression in Escherichia coli. Mol Microbiol 23: 705-717.
12. Blyn, L.B., Braaten, B.A., and Low, D.A. (1990) Regulation of pap pilin phase variation by a mechanism involving differential dam methylation states. EMBO J 9: 4045-4054.
13. Chandler, M., and Fayet, O. (1993) Translational frameshifting in the control of transposition in bacteria. Mol Microbiol 7: 497-503.
14. Connell, T.D., Shaffer, D., and Cannon, J.G. (1990) Characterization of the repertoire of hypervariable regions in the Protein II (opa) gene family of Neisseria gonorrhoeae. Mol Microbiol 4: 439-449.
15. Dehio, C., Gray-Owen, S.D., and Meyer, T.F. (1998) The role of neisserial Opa proteins in interactions with host cells. Trends Microbiol 6: 489-495.
16. Donelson, J.E. (1995) Mechanisms of antigenic variation in Borrelia hermsii and African trypanosornes. J Biol Chem 270: 7783-7786.
17. Dorman, C.J. (1994) Genetics of Bacterial Virulence. Oxford: Blackwell Scientific Publications.
18. Dorman, C.J., and Higgins, C.F. (1987) Fimbrial phase variation in Escherichia coli: dependence on integration host factor and homologies with other site-specific recombinases. J Bacteriol 169: 3840-3843.
19. Dorman, C.J., and Ní Bhriain, N. (1992) Global regulation of gene expression during environmental adaptation: implications for bacterial pathogens. In Molecular Biology of Bacterial Infection, Current Status and Future Perspectives. Hormaeche, C.E., Penn, C.W., and Smyth, C.J. (eds). Cambridge: Cambridge University Press, pp. 193-230.
20. Dove, S.L., Smith, S.G., and Dorman, C.J. (1997) Control of Escherichia coli type 1 fimbrial gene expression in stationary phase: a negative role for RpoS. Mol Gen Genet 254: 13-20.
21. Dybvig, K. (1993) DNA rearrangements and phenotypic switching in prokaryotes. Mol Microbiol 10: 465-471.
22. Dybvig, K., Sitaraman, R., and French, C.T. (1998) A family of phase-variable restriction enzymes with differing specificities generated by high-frequency gene rearrangements. Proc Natl Acad Sci USA 95: 13923-13928.
23. Foster, P.L., and Trimarchi, J.M. (1994) Adaptive reversion of a frameshift mutation in Escherichia coli by simple base deletions in homopolymeric runs. Science 265: 407-409.
24. Gally, D.L., Bogan, 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.
25. Glasgow, A.C., Hughes, K.T., and Simon, M.I. (1989) Bacterial DNA inversion systems. In Mobile DNA. Berg, D.E., and Howe, M.M. (eds). Washington, DC: American Society for Microbiology Press, pp. 637-659.
26. Gutierrez Fernandez, J., Rodriguez Fernandez, M., Nunez Murillo, F., and Maroto Vela, M.C. (1997) Antigenic and genetic structure of Borrelia burgdorferi. Microbios 91: 165-174.
27. 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.
28. Hale, W.B., van der Woude, M.W., and Low, D.A. (1994) Analysis of nonmethylated GATC sites in the Escherichia coli chromosome and identification of sites that are differentially methylated in response to environmental stimuli. J Bacteriol 176: 3438-3441.
29. Hale, W.B., van der Woude, M.W., Braaten, B.A., and Low, D.A. (1998) Regulation of uropathogenic Escherichia coli adhesin expression by DNA methylation. Mol Genet Metab 65: 191-196.
30. van Ham, S.M., van Alphen, L., Mooi, F.R., and van Putten, J.P. (1993) Phase variation of H. influenzae fimbriae: transcriptional control of two divergent genes through a variable combined promoter region. Cell 73: 1187-1196.
31. + cells can be attributed to its ability to bind hemimethylated Pmom promoter DNA. Nucleic Acids Res 25: 4385-4388.
32. Heichman, K.A., and Johnson, R.C. (1990) The Hin invertasome: protein-mediated joining of distant recombination sites at the enhancer. Science249: 511-517.
33. Henderson, I.R., Meehan, M., and Owen, P. (1997) A novel regulatory mechanism for a novel phase-variable outer membrane protein of Escherichia coli. Adv Exp Med Biol 412: 349-355.
34. Henderson, I.R., and Owen, P. (1999) The major phase-variable outer membrane protein of Escherichia coli structurally resembles the immunoglobulin A1 protease class of exported protein and is regulated by a novel mechanism involving Dam and OxyR. J Bacteriol 181: 2132-2141.
35. Johnson, R.C., and Simon, M.I. (1985) Hin-mediated site-specific recombination requires two 26 bp recombination sites and a 60 bp recornbinational enhancer. Cell 41: 781-791.
36. Johnson, B.C., Glasgow, A.C., and Simon, M.I. (1987) Spatial relationship of the Fis binding sites for Hin recombinational enhancer activity. Nature 329: 462-465.
37. Kattenbach, L.S., Braaten, B.A., and Low, D.A. (1995) Specific binding of Papl to Lrp-pap DNA complexes. J Bacteriol 177: 6449-6455.
38. Kaltenbach, L., Braaten, B., Tucker, J., Krabbe, M., and Low, D. (1998) Use of a two-color genetic screen to identify a domain of the global regulator Lrp that is specifically required for pap phase variation. J Bacteriol 180: 1224-1231.
39. Keith, B.R., Harris, S.L., Russell, P.W., and Orndorff, P.E. (1990) Effect of type 1 piliation on in vitro killing of Escherichia coli by mouse peritoneal macrophages. Infect Immun 58: 3448-3454.
40. Klemm, P. (1986) Two regulatory fim genes, fimB and fimE, control the phase variation of type 1 fimbriae in Escherichia coli. EMBO J 5: 1389-1393.
41. Koomey, M. (1997) Bacterial pathogenesis: a variation on variation in Lyme disease. Curr Biol 7: R538-R540.
42. Kroll, J.S. (1992) The genetics of encapsulation in Haemophilus influenzae. J Infect Dis 165 (Suppl. 1): S93-S96.
43. Kulasekara, H.D., and Blomfield, I.C. (1999) The molecular basis for the specificity of FimE in the phase variation of type 1 fimbriae of Escherichia coli K-12. Mol Microbiol 31: 1171-1182.
44. Lim, J.K., Gunther, N.W.T., Zhao, H., Johnson, D.E., Keay, S.K., and Mobley, H.L. (1998) In vivo phase variation of Escherichia coli type 1 fimbrial genes in women with urinary tract infection. Infect Immun 66: 3303-3310.
45. Lovett, S.T., and Feschenko, V.V. (1996) Stabilization of diverged tandem repeats by mismatch repair: evidence for deletion formation via a misaligned replication intermediate. Proc Natl Acad Sci USA 93: 7120-7124.
46. McClain, M.S., Blomfield, I.C., Eberhardt, K.J., and Eisenstein, B.I. (1993) Inversion-independent phase variation of type 1 fimbriae in Escherichia coli. J Bacteriol 175: 4335-4344.
47. Mehr, I.J., and Seifert, H.S. (1998) Differential roles of homologous recombination pathways in Neisseria gonorrhoeae pilin antigenic variation, DNA transformation and DNA repair. Mol Microbiol 30: 697-710.
48. Meyer, T.F., Gibbs, C.P., and Haas, R. (1990) Variation and control of protein expression in Neisseria. Annu Rev Microbiol 44: 451-477.
49. Mhlanga-Mutangadura, T., Morlin, G., Smith, A.L., Eisenstark, A., and Golomb, M. (1998) Evolution of the major pilus gene cluster of Haemophilus influenzae. J Bacteriol 180: 4693-4703.
50. Mornet, E., Chateau, C., Taillandier, A., Simon-Bouy, B., and Serre, J.L. (1996) Recurrent and unexpected segregation of the FMR1 CGG repeat in a family with fragile X syndrome. Hum Genet 97: 512-515.
51. 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.
52. Ofek, I., and Sharon, N. (1988) Lectinophagocytosis: a molecular mechanism of recognition between cell surface sugars and lectins in the phagocytosis of bacteria. Infect Immun 56: 539-547.
53. Parniewski, P., Bacolla, A., Jaworski, A., and Wells, R.D. (1999) Nucleotide excision repair affects the stability of long transcribed (CTG*CAG) tracts in an orientation-dependent manner in Escherichia coli. Nucleic Acids Res 27: 616-623.
54. Ringquist, S., and Smith, C.L. (1992) The Escherichia coli chromosome contains specific, unmethylated dam and dcm sites. Proc Natl Acad Sci USA 89: 4539-4543.
55. Robertson, B.D., and Meyer, T.F. (1992a) Antigenic variation in bacterial pathogens. In Molecular Biology of Bacterial Infection, Current Status and Future Perspectives. Hormaeche, C.E., Penn, C.W., and Smyth, C.J. (eds). Cambridge: Cambridge University Press, pp. 61-73.
56. Robertson, B.D., and Meyer, T.F. (1992b) Genetic variation in pathogenic bacteria. Trends Genet 8: 422-427.
57. Roche, A.J., and Owen, P. (1999) Some Escherichia coli strains possess multiple copies of agn43 - the gene encoding a major phase variable outer membrane protein. 142nd Ordinary Meeting of the Society for General Microbiology. Warwick: Society for General Microbiology Press.
58. Roesch, P.L., and Blomfield, I.C. (1998) Leucine alters the interaction of the leucine-responsive regulatory protein (Lrp) with the fim switch to stimulate site-specific recombination in Escherichia coli. Mol Microbiol 27: 751-761.
59. Rosenberg, S.M., Longerich, S., Gee, P., and Harris, R.S. (1994) Adaptive mutation by deletions in small mononucleotide repeats. Science 265: 405-407.
60. Sarkari, J., Pandit, N., Moxon, E.R., and Achtman, M. (1994) Variable expression of the Opc outer membrane protein in Neisseria meningitidis is caused by size variation of a promoter containing poly-cytidine. Mol Microbiol 13: 207-217.
61. Saunders, J.R. (1986) The genetic basis of phase and antigenic variation in bacteria. In Antigenic Variation in Infectious Diseases. Birkback, T.H., and Penn, C.W. (eds). Oxford: IRL Press, pp. 57-76.
62. Saunders, J.R. (1994) Population genetics of phase variable antigens. In Population Genetics of Bacteria. Baumberg, S., Young, J.P.W., Wellington, E.M.H., and Saunders, J.R. (eds). Cambridge: Cambridge University Press, pp. 247-268.
63. Saunders, N.J., Peden, J.F., Hood, D.W., and Moxon, E.R. (1998) Simple sequence repeats in the Helicobacter pylori genome. Mol Microbiol 27: 1091-1098.
64. Schembri, M.A., Olsen, P.B., and Klemm, P. (1998) Orientation-dependent enhancement by H-NS of the activity of the type 1 fimbrial phase switch promoter in Escherichia coli. Mol Gen Genet 259: 336-344.
65. Seifert, H.S. (1996) Questions about gonococcal pilus phase-and antigenic variation. Mol Microbiol 21: 433-440.
66. Sia, E.A., Kokoska, R.J., Dominska, M., Greenwell, P., and Petes, T.D. (1997) Microsatellite instability in yeast: dependence on repeat unit size and DNA mismatch repair genes. Mol Cell Biol 17: 2851-2858.
67. 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.
68. Stibitz, S., Aaronson, W., Monack, D., and Falkow, S. (1989) Phase variation in Bordetella pertussis by frameshift mutation in a gene for a novel two-component system. Nature 338: 266-269.
69. - changes in Neisseria gonorrhoeae. Cell 47: 267-276.
70. Virji, M., Kayhty, H., Ferguson, D.J., Alexandrescu, C., Heckels, J.E., and Moxon, E.R. (1991) The role of pili in the interactions of pathogenic Neisseria with cultured human endothelial cells. Mol Microbiol 5: 1831-1841.
71. Wells, R.D., Parniewski, P., Pluciennik, A., Bacolla, A., Gellibolian, R., and Jaworski, A. (1998) Small slipped register genetic instabilities in Escherichia coli in triplet repeat sequences associated with hereditary neurological diseases. J Biol Chem 273: 19532-19541.
72. White-Ziegler, C.A., Angus Hill, M.L., Braaten, B.A., van der Woude, M.W., and Low, D.A. (1998) Thermoregulation of Escherichia coli pap transcription: H-NS is a temperature-dependent DNA methylation blocking factor. Mol Microbiol 28: 1121-1137.
73. van der Woude, M., Braaten, B., and Low, D. (1996) Epigenetic phase variation of the pap operon in Escherichia coli. Trends Microbiol 4: 5-9.
74. Xia, Y., Forsman, K., Jass, J., and Uhlin, B.E. (1998) Oligomeric interaction of the PapB transcriptional regulator with the upstream activating region of pili adhesin gene promoters in Escherichia coli. Mol Microbiol 30: 513-523.
75. Zhao, H., Li, X., Johnson, D.E., Blomfield, I., and Mobley, H.L. (1997) In vivo phase variation of MR/P fimbrial gene expression in Proteus mirabilis infecting the urinary tract. Mol Microbiol 23: 1009-1019.
76. Zieg, J., Silverman, M., Hilmen, M., and Simon, M. (1977) Recombinational switch for gene expression. Science 196: 170-172.