Proximal recognition sites facilitate intrasite hopping by DNA adenine methyltransferase: Mechanistic exploration of epigenetic gene regulation

Journal of Biological Chemistry

Volumn 287, Issue 27, 2012, Pages 22873-22881

  Pollak, Adam J ^a   Reich, Norbert O ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONTEXT DEPENDENT; DNA SUBSTRATES; EPIGENETIC REGULATION; HOPPING MECHANISM; HUMAN PATHOGENS; IN-VIVO; METHYLTRANSFERASES; PALINDROMIC; PROCESSIVITY; RECOGNITION SITE; VIRULENCE GENE;

ALKYLATION; DAMS; ESCHERICHIA COLI; GENES; METHYLATION;

DNA;

DNA ADENINE METHYLTRANSFERASE;

ARTICLE; DNA FLANKING REGION; DNA METHYLATION; ENZYME ACTIVITY; EPIGENETICS; ESCHERICHIA COLI; GENE CONTROL; GENE SEQUENCE; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RESTRICTION MAPPING;

BINDING SITES; DEOXYRIBONUCLEASES, TYPE II SITE-SPECIFIC; DNA METHYLATION; EPIGENESIS, GENETIC; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; METHYLTRANSFERASES; MUTAGENESIS; OPERON; SUBSTRATE SPECIFICITY; VIRULENCE;

ESCHERICHIA COLI;

EID: 84863319342     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.332502     Document Type: Article

References (34)

1. Herman, G. E., and Modrich, P. (1982) Escherichia coli dam methylase: physical and catalytic properties of the homogeneous enzyme. J. Biol. Chem. 257, 2605-2612 (Pubitemid 12158143)
2. 6-methyl-adenine: an epigenetic signal for DNA-protein interactions. Nat. Rev. Microbiol. 4, 183-192
3. Marinus, M. G., and Casadesus, J. (2009) Roles of DNA adenine methylation in host-pathogen interactions: mismatch repair, transcriptional regulation, and more. FEMS Microbiol. Rev. 33, 488-503
4. Touzain, F., Petit, M. A., Schbath, S., and El Karoui, M. (2011) DNA motifs that sculpt the bacterial chromosome. Nat. Rev. Microbiol. 9, 15-26
5. Broadbent, S. E., Davies, M. R., and van der Woude, M. W. (2010) Phase variation controls expression of Salmonella lipopolysaccharide modification genes by a DNA methylation-dependent mechanism. Mol. Microbiol. 77, 337-353
6. Casadesuαs, J., and Low, D. (2006) Epigenetic gene regulation in the bacterial world. Microbiol. Mol. Biol. Rev. 70, 830-856
7. Løbner-Olesen, A., Skovgaard, O., and Marinus, M. G. (2005) Dam methylation: coordinating cellular processes. Curr. Opin. Microbiol. 8, 154-160 (Pubitemid 40417956)
8. Ringquist, S., and Smith, C. L. (1992) The Escherichia coli chromosome contains specific, unmethylated dam and dcm sites. Proc. Natl. Acad. Sci. U.S.A. 89, 4539-4543
9. Tavazoie, S., and Church, G. M. (1998) Quantitative whole-genome analysis of DNA-protein interactions by in vivo methylase protection in E. coli. Nat. Biotechnol. 16, 566-571 (Pubitemid 28269816)
10. Hernday, A. D., Braaten, B. A., and Low, D. A. (2003) The mechanism by which DNA adenine methylase and PapI activate the pap epigenetic switch. Mol. Cell 12, 947-957 (Pubitemid 37352787)
11. Kaminska, R., and van der Woude, M. W. (2010) Establishing and maintaining sequestration of Dam target sites for phase variation of agn43 in Escherichia coli. J. Bacteriol. 192, 1937-1945
12. Coffin, S. R., and Reich, N. O. (2008) Modulation of Escherichia coli DNA methyltransferase activity by biologically derived GATC-flanking sequences. J. Biol. Chem. 283, 20106-20116
13. Peterson, S. N., and Reich, N. O. (2006)GATCflanking sequences regulate Dam activity: evidence for how Dam specificity may influence pap expression. J. Mol. Biol. 355, 459-472 (Pubitemid 41785750)
14. van der Woude, M. W. (2011) Phase variation: how to create and coordinate population diversity. Curr. Opin. Microbiol. 14, 205-211
15. Coffin, S. R., and Reich, N. O. (2009) Escherichia coli DNA adenine methyltransferase: intrasite processivity and substrate-induced dimerization and activation. Biochemistry 48, 7399-7410
16. Sasnauskas, G., Zakrys, L., Zaremba, M., Cosstick, R., Gaynor, J. W., Halford, S. E., and Siksnys, V. (2010) A novel mechanism for the scission of double-stranded DNA: BfiI cuts both 3′-5′ and 5′-3′ strands by rotating a single active site. Nucleic Acids Res. 38, 2399-2410
17. Sasnauskas, G., Kostiuk, G., Tamulaitis, G., and Siksnys, V. (2011) Target site cleavage by the monomeric restriction enzyme BcnI requires translocation to a random DNA sequence and a switch in enzyme orientation. Nucleic Acids Res. 39, 8844-8856
18. Halford, S. E., and Marko, J. F. (2004) How do site-specific DNA-binding proteins find their targets? Nucleic Acids Res. 32, 3040-3052 (Pubitemid 39022995)
19. Stanford, N. P., Szczelkun, M. D., Marko, J. F., and Halford, S. E. (2000) One- and three-dimensional pathways for proteins to reach specific DNA sites. EMBO J. 19, 6546-6557
20. Tafvizi, A., Mirny, L. A., and van Oijen, A. M. (2011) Dancing on DNA: kinetic aspects of search processes on DNA. Chem. Phys. Chem. 12, 1481-1489
21. Vuzman, D., Azia, A., and Levy, Y. (2010) Searching DNA via a "Monkey Bar" mechanism: the significance of disordered tails. J. Mol. Biol. 396, 674-684
22. Zhou, H. X. (2011) Rapid search for specific sites on DNA through conformational switch of nonspecifically bound proteins. Proc. Natl. Acad. Sci. U.S.A. 108, 8651-8656
23. Zinoviev, V. V., Evdokimov, A. A., Malygin, E. G., Sclavi, B., Buckle, M., and Hattman, S. (2007) Differential methylation kinetics of individual target site strands by T4 Dam DNA methyltransferase. Biol. Chem. 388, 1199-1207 (Pubitemid 350059622)
24. Porecha, R. H., and Stivers, J. T. (2008) Uracil DNA glycosylase uses DNA hopping and short-range sliding to trap extrahelical uracils. Proc. Natl. Acad. Sci. U.S.A. 105, 10791-10796
25. Hedglin, M., and O'Brien, P. J. (2010) Hopping enables a DNA repair glycosylase to search both strands and bypass a bound protein. ACS Chem. Biol. 5, 427-436
26. Gowers, D. M., Wilson, G. G., Halford, S. E. (2005) Measurement of the contributions of one-dimensional and three-dimensional pathways to the translocation of a protein along DNA. Proc. Natl. Acad. Sci. U.S.A. 102, 15883-15888 (Pubitemid 41552837)
27. Mashhoon, N., Carroll, M., Pruss, C., Eberhard, J., Ishikawa, S., Estabrook, R. A., and Reich, N. (2004) Functional characterization of Escherichia coli DNA adenine methyltransferase, a novel target for antibiotics. J. Biol. Chem. 279, 52075-52081 (Pubitemid 39656579)
28. Fersht, A. (1998) Structure and Mechanism in Protein Science, pp. 143-145, W. H. Freeman, New York
29. Coffin, S. R., and Reich, N. O. (2009) Escherichia coli DNA adenine methyltransferase: the structural basis of processive catalysis and indirect readout. J. Biol. Chem. 284, 18390-18400
30. Boye, E., Marinus, M. G., and Løbner-Olesen, A., (1992) Quantitation of Dam methyltransferase in Escherichia coli. J. Bacteriol. 174, 1682-1685
31. Handa, V., and Jeltsch, A. (2005) Profound flanking sequence preference of Dnmt3a and Dnmt3b mammalian DNA methyltransferases shape the human epigenome. J. Mol. Biol. 348, 1103-1112 (Pubitemid 40602369)
32. Wienholz, B. L., Kareta, M. S., Moarefi, A. H., Gordon, C. A., Ginno, P. A., and Chédin, F. (2010) DNMT3L modulates significant and distinct flanking sequence preference for DNA methylation by DNMT3A and DNMT3B in vivo. PLoS Genet. 6, e101106
33. Halford, S. E. (2009) An end to 40 years of mistakes in DNA-protein association kinetics? Biochem. Soc. Trans. 37, 343-348
34. Rau, D. C., and Sidorova, N. Y. (2010) Diffusion of the restriction nuclease EcoRI along DNA. J. Mol. Biol. 395, 408-416