The mechanism by which DNA adenine methylase and PapI activate the Pap epigenetic switch

Molecular Cell

Volumn 12, Issue 4, 2003, Pages 947-957

  Hernday, Aaron D ^a   Braaten, Bruce A ^a   Low, David A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA ADENINE METHYLTRANSFERASE; PILIN;

ARTICLE; BINDING SITE; DNA METHYLATION; DNA REPLICATION; ESCHERICHIA COLI; GENE MUTATION; GENE SEQUENCE; GENE SWITCHING; MUTATIONAL ANALYSIS; NONHUMAN; PROMOTER REGION; PROTEIN DNA BINDING; REGULATORY MECHANISM;

ESCHERICHIA COLI;

EID: 0242266619     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(03)00383-6     Document Type: Article

References (41)

1. Bartlett M.S., Thomm M., Geiduschek E.P. The orientation of DNA in an archaeal transcription initiation complex. Nat. Struct. Biol. 7:2000;782-785.
2. Bickle T.A., Kruger D.H. Biology of DNA restriction. Microbiol. Rev. 57:1993;434-450.
3. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 16:2002;6-21.
4. Blyn L.B., Braaten B.A., White-Ziegler C.A., Rolfson D.H., Low D.A. Phase-variation of pyelonephritis-associated pili in Escherichia coli. evidence for transcriptional regulation EMBO J. 8:1989;613-620.
5. Blyn L.B., Braaten B.A., Low D.A. Regulation of pap pilin phase variation by a mechanism involving differential dam methylation states. EMBO J. 9:1990;4045-4054.
6. Braaten B.A., Blyn L.B., Skinner B.S., Low D.A. Evidence for a methylation-blocking factor (mbf) locus involved in pap pilus expression and phase variation in Escherichia coli. J. Bacteriol. 173:1991;1789-1800.
7. Braaten B.A., Nou X., Kaltenbach L.S., Low D.A. Methylation patterns in pap regulatory DNA control pyelonephritis-associated pili phase variation in E. coli. Cell. 76:1994;577-588.
8. Brunelle A., Schleif R.F. Missing contact probing of DNA-protein interactions. Proc. Natl. Acad. Sci. USA. 84:1987;6673-6676.
9. Casadesus J., D'Ari R. Memory in bacteria and phage. Bioessays. 24:2002;512-518.
10. Cui Y., Wang Q., Stormo G.D., Calvo J.M. A consensus sequence for binding of Lrp to DNA. J. Bacteriol. 177:1995;4872-4880.
11. Forsman K., Goransson M., Uhlin B.E. Autoregulation and multiple DNA interactions by a transcriptional regulatory protein in E. coli pili biogenesis. EMBO J. 8:1989;1271-1277.
12. Friedhoff P., Thomas E., Pingoud A. Tyr212. a key residue involved in strand discrimination by the DNA mismatch repair endonuclease MutH J. Mol. Biol. 325:2003;285-297.
13. Goransson M., Forsman P., Nilsson P., Uhlin B.E. Upstream activating sequences that are shared by two divergently transcribed operons mediate cAMP-CRP regulation of pilus-adhesin in Escherichia coli. Mol. Microbiol. 3:1989;1557-1565.
14. Heithoff D.M., Sinsheimer R.L., Low D.A., Mahan M.J. An essential role for DNA adenine methylation in bacterial virulence. Science. 284:1999;967-970.
15. Hernday A., Krabbe M., Braaten B., Low D. Self-perpetuating epigenetic pili switches in bacteria. Proc. Natl. Acad. Sci. USA. 99:2002;16470-16476.
16. Huisman T.T., de Graaf F.K. Negative control of fae (K88) expression by the 'global' regulator Lrp is modulated by the "local" regulator FaeA and affected by DNA methylation. Mol. Microbiol. 16:1995;943-953.
17. Kaack M.B., Martin L.N., Svenson S.B., Baskin G., Steele R.H., Roberts J.A. Protective anti-idiotype antibodies in the primate model of pyelonephritis. Infect. Immun. 61:1993;2289-2295.
18. Kaltenbach L.S., Braaten B.A., Low D.A. Specific binding of PapI to Lrp-pap DNA complexes. J. Bacteriol. 177:1995;6449-6455.
19. Kim T., Lagrange T., Naryshkin N., Reinberg D., Ebright R. Site specific protein-DNA photocrosslinking. Travers A., Buckle M. Protein-Dna Interactions. A Practical Approach:1999;IRL Press, Oxford.
20. Low D.A., Weyand N.J., Mahan M.J. Roles of DNA adenine methylation in regulating bacterial gene expression and virulence. Infect. Immun. 69:2001;7197-7204.
21. Lu M., Campbell J.L., Boye E., Kleckner N. SeqA. a negative modulator of replication initiation in E. coli Cell. 77:1994;413-426.
22. Lund B., Lindberg F., Marklund B.I., Normark S. Tip proteins of pili associated with pyelonephritis. new candidates for vaccine development Vaccine. 6:1988;110-112.
23. Modrich P. Methyl-directed DNA mismatch correction. J. Biol. Chem. 264:1989;6597-6600.
24. Ng H.H., Jeppesen P., Bird A. Active repression of methylated genes by the chromosomal protein MBD1. Mol. Cell. Biol. 20:2000;1394-1406.
25. Nou X., Skinner B., Braaten B., Blyn L., Hirsch D., Low D. 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. 7:1993;545-553.
26. Nou X., Braaten B., Kaltenbach L., Low D.A. Differential binding of Lrp to two sets of pap DNA binding sites mediated by Pap I regulates Pap phase variation in Escherichia coli. EMBO J. 14:1995;5785-5797.
27. Papp P.P., Chattoraj D.K. Missing-base and ethylation interference footprinting of P1 plasmid replication initiator. Nucleic Acids Res. 22:1994;152-157.
28. Parker B., Marinus M.G. A simple and rapid method to obtain substitution mutations in Escherichia coli. isolation of a dam deletion/insertion mutation Gene. 73:1988;531-535.
29. Reisenauer A., Shapiro L. DNA methylation affects the cell cycle transcription of the CtrA global regulator in Caulobacter. EMBO J. 21:2002;4969-4977.
30. Roberts D., Hoopes B.C., McClure W.R., Kleckner N. IS10 transposition is regulated by DNA adenine methylation. Cell. 43:1985;117-130.
31. Simons R.W., Houman F., Kleckner N. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene. 53:1987;85-96.
32. Slominska M., Wahl A., Wegrzyn G., Skarstad K. Degradation of mutant initiator protein DnaA204 by proteases ClpP, ClpQ and Lon is prevented when DNA is SeqA-free. Biochem. J. 370:2003;867-871.
33. Taghbalout A., Landoulsi A., Kern R., Yamazoe M., Hiraga S., Holland B., Kohiyama M., Malki A. Competition between the replication initiator DnaA and the sequestration factor SeqA for binding to the hemimethylated chromosomal origin of E. coli in vitro. Genes Cells. 5:2000;873-884.
34. van der Woude M.W., Kaltenbach L.S., Low D.A. Leucine-responsive regulatory protein plays dual roles as both an activator and a repressor of the Escherichia coli pap fimbrial operon. Mol. Microbiol. 17:1995;303-312.
35. van der Woude M., Braaten B., Low D. Epigenetic phase variation of the pap operon in Escherichia coli. Trends Microbiol. 4:1996;5-9.
36. van der Woude M., Hale W.B., Low D.A. Formation of DNA methylation patterns. nonmethylated GATC sequences in gut and pap operons J. Bacteriol. 180:1998;5913-5920.
37. Wang Q., Calvo J.M. Lrp, a global regulatory protein of Escherichia coli, binds co-operatively to multiple sites and activates transcription of ilvIH. J. Mol. Biol. 229:1993;306-318. a.
38. Wang Q., Calvo J.M. Lrp, a major regulatory protein in Escherichia coli, bends DNA and can organize the assembly of a higher-order nucleoprotein structure. EMBO J. 12:1993;2495-2501. b.
39. Weyand N.J., Low D.A. Regulation of Pap phase variation. Lrp is sufficient for the establishment of the phase off pap DNA methylation pattern and repression of pap transcription in vitro. J. Biol. Chem. 275:2000;3192-3200.
40. Weyand N.J., Braaten B.A., van der Woude M., Tucker J., Low D.A. The essential role of the promoter proximal subunit of CAP in Pap phase variation. Lrp- and helical phase-dependent activation of papBA transcription by CAP from -215 Mol. Microbiol. 39:2001;1504-1522.
41. Xia Y., Forsman K., Jass J., Uhlin B.E. Oligomeric interaction of the PapB transcriptional regulator with the upstream activating region of pili adhesin gene promoters in Escherichia coli. Mol. Microbiol. 30:1998;513-523.