Regulatory interplay between pap operons in uropathogenic Escherichia coli

Molecular Microbiology

Volumn 67, Issue 5, 2008, Pages 996-1011

  Totsika, Makrina ^a   Beatson, Scott A ^b   Holden, Nicola ^a   Gally, David L ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; ARTICLE; BACTERIAL CELL; BINDING SITE; CELL ORGANELLE; CELL SURFACE; CONTROLLED STUDY; ESCHERICHIA COLI; FIMBRIA; GENE; NONHUMAN; OPERON; PAP GENE; PAPB GENE; PAPI GENE; PRIORITY JOURNAL; URINARY TRACT INFECTION;

ALLELES; AMINO ACID SEQUENCE; BASE SEQUENCE; CLONING, MOLECULAR; CONSERVED SEQUENCE; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; FRAMESHIFT MUTATION; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; OPERON; REGULATORY SEQUENCES, NUCLEIC ACID; REPRESSOR PROTEINS; SEQUENCE ALIGNMENT; TRANSCRIPTION FACTORS; URINARY TRACT INFECTIONS; VARIATION (GENETICS);

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 38849130677     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2007.06098.x     Document Type: Article

References (77)

1. Andersson, P., Engberg, I., Lidin-Janson, G., Lincoln, K., Hull, R., Hull, S. Svanborg, C. (1991) Persistence of Escherichia coli bacteriuria is not determined by bacterial adherence. Infect Immun 59 : 2915 2921.
2. Anisimova, M., Bielawski, J.P. Yang, Z. (2002) Accuracy and power of Bayes prediction of amino acid sites under positive selection. Mol Biol Evol 19 : 950 958.
3. Barnich, N., Boudeau, J., Claret, L. Darfeuille-Michaud, A. (2003) Regulatory and functional co-operation of flagella and type 1 pili in adhesive and invasive abilities of AIEC strain LF82 isolated from a patient with Crohn[apos]s disease. Mol Microbiol 48 : 781 794.
4. Berger, H., Hacker, J., Juarez, A., Hughes, C. Goebel, W. (1982) Cloning of the chromosomal determinants encoding hemolysin production and mannose-resistant hemagglutination in Escherichia coli. J Bacteriol 152 : 1241 1247.
5. Bergsten, G., Samuelsson, M., Wullt, B., Leijonhufvud, I., Fischer, H. Svanborg, C. (2004) PapG-dependent adherence breaks mucosal inertia and triggers the innate host response. J Infect Dis 189 : 1734 1742.
6. Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., et al. (2000) The Protein Data Bank. Nucleic Acids Res 28 : 235 242.
7. Berman, H., Henrick, K. Nakamura, H. (2003) Announcing the worldwide Protein Data Bank. Nat Struct Biol 10 : 980.
8. Blomfield, I.C. (2001) The regulation of Pap and type 1 fimbriation in Escherichia coli. Adv Microb Physiol 45 : 1 49.
9. Blomfield, I.C., Vaughn, V., Rest, R.F. Eisenstein, B.I. (1991) Allelic exchange in Escherichia coli using the Bacillus subtilis sacB gene and a temperature-sensitive pSC101 replicon. Mol Microbiol 5 : 1447 1457.
10. Blyn, L.B., Braaten, B.A., White-Ziegler, C.A., Rolfson, D.H. Low, D.A. (1989) Phase-variation of pyelonephritis-associated pili in Escherichia coli: evidence for transcriptional regulation. EMBO J 8 : 613 620.
11. Braaten, B.A., Platko, J.V., van der Woude, M.W., Simons, B.H., de Graaf, F.K., Calvo, J.M. Low, D.A. (1992) Leucine-responsive regulatory protein controls the expression of both the pap and fan pili operons in Escherichia coli. PNAS 89 : 4250 4254.
12. Braaten, B.A., Nou, X., Kaltenbach, L.S. Low, D.A. (1994) Methylation patterns in pap regulatory DNA control pyelonephritis-associated pili phase variation in E. coli. Cell 76 : 577 588.
13. Brzuszkiewicz, E., Bruggemann, H., Liesegang, H., Emmerth, M., Olschlager, T., Nagy, G., et al. (2006) How to become a uropathogen: comparative genomic analysis of extraintestinal pathogenic Escherichia coli strains. PNAS 103 : 12879 12884.
14. Chattopadhyay, S., Dykhuizen, D.E. Sokurenko, E.V.Z.P.S. (2007a) Visualization of recent adaptive evolution of proteins. BMC Bioinformatics 7 : 187.
15. Chattopadhyay, S., Feldgarden, M., Weissman, S.J., Dykhuizen, D.E., van Belle, G. Sokurenko, E.V. (2007b) Haplotype diversity in 'source-sink' dynamics of Escherichia coli urovirulence. J Mol Evol 64 : 204 214.
16. Chen, S.L., Hung, C.S., Xu, J., Reigstad, C.S., Magrini, V., Sabo, A., et al. (2006) Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli: a comparative genomics approach. PNAS 103 : 5977 5982.
17. DeLano, W.L. (2002) The PyMOL Molecular Graphics System. Palo Alto, CA : DeLano Scientific [WWW document]. URL http://pymol.sourceforge.net/.
18. Evans, D.G., Evans, D.J., Jr, and Tjoa, W. (1977) Hemagglutination of human group A erythrocytes by enterotoxigenic Escherichia coli isolated from adults with diarrhea: correlation with colonization factor. Infect Immun 18 : 330 337.
19. Forsman, K., Goransson, M. Uhlin, B.E. (1989) Autoregulation and multiple DNA interactions by a transcriptional regulatory protein in E. coli pili biogenesis. EMBO J 8 : 1271 1277.
20. Gally, D.L., Leathart, J. Blomfield, I.C. (1996) Interaction of FimB and FimE with the fim switch that controls the phase variation of type 1 fimbriae in Escherichia coli K-12. Mol Microbiol 21 : 725 738.
21. Goldman, N. Yang, Z. (1994) A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol 11 : 725 736.
22. Goransson, M., Forsman, K. Uhlin, B.E. (1988) Functional and structural homology among regulatory cistrons of pili-adhesin determinants in Escherichia coli. Mol Gen Genet 212 : 412 417.
23. Goransson, M., Forsman, P., Nilsson, P. Uhlin, B.E. (1989) Upstream activating sequences that are shared by two divergently transcribed operons mediate cAMP-CRP regulation of pilus-adhesin in Escherichia coli. Mol Microbiol 3 : 1557 1565.
24. Graham, J.C., Leathart, J.B., Keegan, S.J., Pearson, J., Bint, A. Gally, D.L. (2001) Analysis of Escherichia coli strains causing bacteriuria during pregnancy: selection for strains that do not express type 1 fimbriae. Infect Immun 69 : 794 799.
25. Guyer, M.S., Reed, R.R., Steitz, J.A. Low, K.B. (1981) Identification of a sex-factor-affinity site in E. coli as gamma delta. Cold Spring Harb Symp Quant Biol 45 (Part 1 135 140.
26. Hasman, H., Chakraborty, T. Klemm, P. (1999) Antigen-43-mediated autoaggregation of Escherichia coli is blocked by fimbriation. J Bacteriol 181 : 4834 4841.
27. Hayashi, T., Makino, K., Ohnishi, M., Kurokawa, K., Ishii, K., Yokoyama, K., et al. (2001) Complete genome sequence of enterohemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12. DNA Res 8 : 11 22.
28. Hernday, A.D., Braaten, B.A. Low, D.A. (2003) The mechanism by which DNA adenine methylase and PapI activate the pap epigenetic switch. Mol Cell 12 : 947 957.
29. Hernday, A.D., Braaten, B.A., Broitman-Maduro, G., Engelberts, P. Low, D.A. (2004) Regulation of the pap epigenetic switch by CpxAR: phosphorylated CpxR inhibits transition to the phase ON state by competition with Lrp. Mol Cell 16 : 537 547.
30. Holden, N., Totsika, M., Dixon, L., Catherwood, K. Gally, D.L. (2007) Regulation of P-fimbrial phase variation frequencies in Escherichia coli CFT073. Infect Immun 75 : 3325 3334.
31. Holden, N.J. Gally, D.L. (2004) Switches, cross-talk and memory in Escherichia coli adherence. J Med Microbiol 53 : 585 593.
32. Holden, N.J., Uhlin, B.E. Gally, D.L. (2001) PapB paralogues and their effect on the phase variation of type 1 fimbriae in Escherichia coli. Mol Microbiol 42 : 319 330.
33. Holden, N.J., Totsika, M., Mahler, E., Roe, A.J., Catherwood, K., Lindner, K., et al. (2006) Demonstration of regulatory cross-talk between P fimbriae and type 1 fimbriae in uropathogenic Escherichia coli. Microbiology 152 : 1143 1153.
34. Hommais, F., Gouriou, S., Amorin, C., Bui, H., Rahimy, M.C., Picard, B. Denamur, E. (2003) The FimH A27V mutation is pathoadaptive for urovirulence in Escherichia coli B2 phylogenetic group isolates. Infect Immun 71 : 3619 3622.
35. Hull, R.A., Rudy, D.C., Donovan, W.H., Wieser, I.E., Stewart, C. Darouiche, R.O. (1999) Virulence properties of Escherichia coli 83972, a prototype strain associated with asymptomatic bacteriuria. Infect Immun 67 : 429 432.
36. Huson, D.H. Bryant, D. (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23 : 254 267.
37. Kaltenbach, L., Braaten, B. Low, D. (1995) Specific binding of PapI to Lrp-pap DNA complexes. J Bacteriol 177 : 6449 6455.
38. Kaltenbach, L., Braaten, B., Tucker, J., Krabbe, M. 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. Kawamura, T., Le, L.U., Zhou, H. Dahlquist, F.W. (2007) Solution structure of Escherichia coli PapI, a key regulator of the pap pili phase variation. J Mol Biol 365 : 1130 1142.
40. Kearns, D.B., Chu, F., Rudner, R. Losick, R. (2004) Genes governing swarming in Bacillus subtilis and evidence for a phase variation mechanism controlling surface motility. Mol Microbiol 52 : 357 369.
41. Klemm, P., Roos, V., Ulett, G.C., Svanborg, C. Schembri, M.A. (2006) Molecular characterization of the Escherichia coli asymptomatic bacteriuria strain 83972: the taming of a pathogen. Infect Immun 74 : 781 785.
42. Korotkova, N., Chattopadhyay, S., Tabata, T.A., Beskhlebnaya, V., Vigdorovich, V., Kaiser, B.K., et al. (2007) Selection for functional diversity drives accumulation of point mutations in Dr adhesins of Escherichia coli. Mol Microbiol 64 : 180 194.
43. Li, X., Rasko, D.A., Lockatell, C.V., Johnson, D.E. Mobley, H.L. (2001) Repression of bacterial motility by a novel fimbrial gene product. EMBO J 20 : 4854 4862.
44. Martin, D.P., Williamson, C. Posada, D. (2005) RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21 : 260 262.
45. Minshew, B.H., Jorgensen, J., Counts, G.W. Falkow, S. (1978) Association of hemolysin production, hemagglutination of human erythrocytes, and virulence for chicken embryos of extraintestinal Escherichia coli isolates. Infect Immun 20 : 50 54.
46. Mobley, H.L., Green, D.M., Trifillis, A.L., Johnson, D.E., Chippendale, G.R., Lockatell, C.V., et al. (1990) Pyelonephritogenic Escherichia coli and killing of cultured human renal proximal tubular epithelial cells: role of hemolysin in some strains. Infect Immun 58 : 1281 1289.
47. Morschhauser, J., Vetter, V., Emody, L. Hacker, J. (1994) Adhesin regulatory genes within large, unstable DNA regions of pathogenic Escherichia coli: cross-talk between different adhesin gene clusters. Mol Microbiol 11 : 555 566.
48. Nielsen, R. Yang, Z. (1998) Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148 : 929 936.
49. Nou, X., Skinner, B., Braaten, B., Blyn, L., Hirsch, D. Low, D. (1993) Regulation of pyelonephritis-associated pili phase-variation in Escherichia coli: binding of the PapI and the Lrp regulatory proteins is controlled by DNA methylation. Mol Microbiol 7 : 545 553.
50. Nou, X., Braaten, B., Kaltenbach, L. Low, D.A. (1995) Differential binding of Lrp to two sets of pap DNA binding sites mediated by PapI regulates Pap phase variation in Escherichia coli. EMBO J 14 : 5785 5797.
51. Nowicki, B., Rhen, M., Vaisanen-Rhen, V., Pere, A. Korhonen, T.K. (1984) Immunofluorescence study of fimbrial phase variation in Escherichia coli KS71. J Bacteriol 160 : 691 695.
52. Nowicki, B., Rhen, M., Vaisanen-Rhen, V., Pere, A. Korhonen, T.K. (1985) Kinetics of phase variation between S and type-1 fimbriae of Escherichia coli. FEMS Microbiol Lett 28 : 237 242.
53. Perna, N.T., Plunkett, G., Burland, V., Mau, B., Glasner, J.D., Rose, D.J., et al. (2001) Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409 : 529 533.
54. Plos, K., Carter, T., Hull, S., Hull, R. Svanborg Eden, C. (1990) Frequency and organization of pap homologous DNA in relation to clinical origin of uropathogenic Escherichia coli. J Infect Dis 161 : 518 524.
55. Schembri, M.A. Klemm, P. (2001) Coordinate gene regulation by fimbriae-induced signal transduction. EMBO J 20 : 3074 3081.
56. Schembri, M.A., Dalsgaard, D. Klemm, P. (2004) Capsule shields the function of short bacterial adhesins. J Bacteriol 186 : 1249 1257.
57. Schembri, M.A., Blom, J., Krogfelt, K.A. Klemm, P. (2005) Capsule and fimbria interaction in Klebsiella pneumoniae. Infect Immun 73 : 4626 4633.
58. Schwan, W.R., Beck, M.T., Hultgren, S.J., Pinkner, J., Woolever, N.L. Larson, T. (2005) Down-regulation of the kps region 1 capsular assembly operon following attachment of Escherichia coli type 1 fimbriae to d-mannose receptors. Infect Immun 73 : 1226 1231.
59. Snyder, J.A., Haugen, B.J., Lockatell, C.V., Maroncle, N., Hagan, E.C., Johnson, D.E., et al. (2005) Coordinate expression of fimbriae in uropathogenic Escherichia coli. Infect Immun 73 : 7588 7596.
60. Sokurenko, E.V., Chesnokova, V., Dykhuizen, D.E., Ofek, I., Wu, X.-R., Krogfelt, K.A., et al. (1998) Pathogenic adaptation of Escherichia coli by natural variation of the FimH adhesin. PNAS 95 : 8922 8926.
61. Sokurenko, E.V., Feldgarden, M., Trintchina, E., Weissman, S.J., Avagyan, S., Chattopadhyay, S., et al. (2004) Selection footprint in the FimH adhesin shows pathoadaptive niche differentiation in Escherichia coli. Mol Biol Evol 21 : 1373 1383.
62. Ulett, G.C., Webb, R.I. Schembri, M.A. (2006) Antigen-43-mediated autoaggregation impairs motility in Escherichia coli. Microbiology 152 : 2101 2110.
63. Weissman, S.J., Chattopadhyay, S., Aprikian, P., Obata-Yasuoka, M., Yarova-Yarovaya, Y., Stapleton, A., et al. (2006) Clonal analysis reveals high rate of structural mutations in fimbrial adhesins of extraintestinal pathogenic Escherichia coli. Mol Microbiol 59 : 975 988.
64. Welch, R.A., Burland, V., Plunkett, G., 3rd, Redford, P., Roesch, P., Rasko, D., et al. (2002) Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. PNAS 99 : 17020 17024.
65. van der Woude, M.W. (2006) Re-examining the role and random nature of phase variation. FEMS Microbiol Lett 254 : 190 197.
66. van der Woude, M.W. Baumler, A.J. (2004) Phase and antigenic variation in bacteria. Clin Microbiol Rev 17 : 581 611.
67. van der Woude, M.W. Low, D.A. (1994) Leucine-responsive regulatory protein and deoxyadenosine methylase control the phase variation and expression of the sfa and daa pili operons in Escherichia coli. Mol Microbiol 11 : 605 618.
68. van der Woude, M.W., Braaten, B.A. Low, D.A. (1992) Evidence for global regulatory control of pilus expression in Escherichia coli by Lrp and DNA methylation: model building based on analysis of Pap. Mol Microbiol 6 : 2429 2435.
69. van der Woude, M.W., Kaltenbach, L.S. Low, D.A. (1995) Leucine-responsive regulatory protein plays dual roles as both an activator and a repressor of the Escherichia coli pap fimbrial operon. Mol Microbiol 17 : 303 312.
70. Wullt, B., Bergsten, G., Connell, H., Rollano, P., Gebretsadik, N., Hull, R. Svanborg, C. (2000) P fimbriae enhance the early establishment of Escherichia coli in the human urinary tract. Mol Microbiol 38 : 456 464.
71. Wullt, B., Bergsten, G., Connell, H., Rollano, P., Gebratsedik, N., Hang, L. Svanborg, C. (2001) P-fimbriae trigger mucosal responses to Escherichia coli in the human urinary tract. Cell Microbiol 3 : 255 264.
72. Xia, Y. Uhlin, B.E. (1999) Mutational analysis of the PapB transcriptional regulator in Escherichia coli. Regions important for DNA binding and oligomerization. J Biol Chem 274 : 19723 19730.
73. Xia, Y., Forsman, K., Jass, J. 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.
74. Xia, Y., Gally, D., Forsman-Semb, K. Uhlin, B.E. (2000) Regulatory cross-talk between adhesin operons in Escherichia coli: inhibition of type 1 fimbriae expression by the PapB protein. EMBO J 19 : 1450 1457.
75. Yang, Z. (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13 : 555 556.
76. Yang, Z., Nielsen, R. Hasegawa, M. (1998) Models of amino acid substitution and applications to mitochondrial protein evolution. Mol Biol Evol 15 : 1600 1611.
77. Yang, Z., Nielsen, R., Goldman, N. Pedersen, A.M. (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155 : 431 449.