Beyond DnaA: The role of DNA topology and DNA methylation in bacterial replication initiation

Journal of Molecular Biology

Volumn 426, Issue 12, 2014, Pages 2269-2282

  Zawilak Pawlik, Anna ^a   Donczew, Rafał ^a   Zakrzewska Czerwińska, Jolanta ^a,b  

^a INSTITUTE OF IMMUNOLOGY AND EXPERIMENTAL THERAPY   (Poland)

^b UNIVERSITY OF WROC AW   (Poland)

Author keywords

DNA replication; DNA tertiary structure; nucleoid associated proteins; oriC methylation; orisome formation

Indexed keywords

BACTERIAL DNA; DNA TOPOISOMERASE; NUCLEOID ASSOCIATED PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

BACTERIAL CHROMOSOME; BACTERIAL REPRODUCTION; CHROMOSOME REPLICATION; CONFORMATIONAL TRANSITION; DNA CONFORMATION; DNA DENATURATION; DNA HELIX; DNA METHYLATION; DNA REPLICATION; DNA REPLICATION ORIGIN; DNA STRUCTURE; DNA SUPERCOILING; ESCHERICHIA COLI; GENETIC TRANSCRIPTION; NONHUMAN; NUTRIENT AVAILABILITY; OLIGOMERIZATION; OSMOLARITY; PRIORITY JOURNAL; REVIEW; TEMPERATURE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

DNA REPLICATION; DNA TERTIARY STRUCTURE; NUCLEOID-ASSOCIATED PROTEINS; ORIC METHYLATION; ORISOME FORMATION;

BACTERIA; BACTERIAL PROTEINS; DNA METHYLATION; DNA REPLICATION; DNA-BINDING PROTEINS; NUCLEIC ACID CONFORMATION; ORIGIN RECOGNITION COMPLEX; PROTEIN BINDING;

EID: 84901197793     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2014.04.009     Document Type: Review

References (164)

1. S.J. Aves DNA replication initiation Methods Mol Biol 521 2009 3 17
2. O. Nielsen, and A. Løbner-Olesen Once in a lifetime: strategies for preventing re-replication in prokaryotic and eukaryotic cells EMBO Rep 9 2008 151 156
3. H. Kawakami, and T. Katayama DnaA, ORC, and Cdc6: similarity beyond the domains of life and diversity Biochem Cell Biol 88 2010 49 62
4. Z Chen, C Speck, P Wendel, C Tang, B Stillman, and H Li The architecture of the DNA replication origin recognition complex in Saccharomyces cerevisiae Proc Natl Acad Sci USA 105 2008 10326 10331
5. A.C. Leonard, and J.E. Grimwade Regulation of DnaA assembly and activity: taking directions from the genome Annu Rev Microbiol 65 2011 19 35
6. D.B. Wigley ORC proteins: marking the start Curr Opin Struct Biol 19 2009 72 78
7. C. Cayrou, P. Coulombe, and M. Méchali Programming DNA replication origins and chromosome organization Chromosome Res 18 2010 137 145
8. M. Su'etsugu, A. Emoto, K. Fujimitsu, K. Keyamura, and T. Katayama Transcriptional control for initiation of chromosomal replication in Escherichia coli: fluctuation of the level of origin transcription ensures timely initiation Genes Cells 8 2003 731 745
9. M. Méchali Eukaryotic DNA replication origins: many choices for appropriate answers Nat Rev Mol Cell Biol 11 2010 728 738
10. D. Remus, E.L. Beall, and M.R. Botchan DNA topology, not DNA sequence, is a critical determinant for Drosophila ORC-DNA binding EMBO J 23 2004 897 907
11. H. Masai, S. Matsumoto, Z. You, N. Yoshizawa-Sugata, and M. Oda Eukaryotic chromosome DNA replication: where, when, and how? Annu Rev Biochem 79 2010 89 130
12. E.C. Dueber, A. Costa, J.E. Corn, S.D. Bell, and J.M. Berger Molecular determinants of origin discrimination by Orc1 initiators in archaea Nucleic Acids Res 39 2011 3621 3631
13. C Cayrou, P Coulombe, A Puy, S Rialle, N Kaplan, and E Segal et al. New insights into replication origin characteristics in metazoans Cell Cycle 11 2012 658 667
14. M. Méchali, K. Yoshida, P. Coulombe, and P. Pasero Genetic and epigenetic determinants of DNA replication origins, position and activation Curr Opin Genet Dev 23 2013 124 131
15. J. Collier Epigenetic regulation of the bacterial cell cycle Curr Opin Microbiol 12 2009 722 729
16. J. Casadesús, and D.A. Low Programmed heterogeneity: epigenetic mechanisms in bacteria J Biol Chem 288 2013 13929 13935
17. R. Donczew, R. Lurz, J. Zakrzewska-Czerwinska, and A. Zawilak-Pawlik Helicobacter pylori oriC - the first bipartite origin of chromosome replication in Gram-negative bacteria Nucleic Acids Res 40 2012 9647 9660
18. V.T. Ryan, J.E. Grimwade, J.E. Camara, E. Crooke, and A.C. Leonard Escherichia coli prereplication complex assembly is regulated by dynamic interplay among Fis, IHF and DnaA Mol Microbiol 51 2004 1347 1359
19. S. Ozaki, and T. Katayama Highly organized DnaA-oriC complexes recruit the single-stranded DNA for replication initiation Nucleic Acids Res 40 2012 1648 1665
20. G Kaur, MP Vora, CA Czerwonka, TA Rozgaja, JE Grimwade, and AC Leonard Building the bacterial orisome: high affinity DnaA recognition plays a role in setting the conformation of oriC DNA Mol Microbiol 2014 10.1111/mmi.12525
21. K.E. Duderstadt, and J.M. Berger A structural framework for replication origin opening by AAA + initiation factors Curr Opin Struct Biol 23 2013 144 153
22. C. Weigel, A. Schmidt, B. Rückert, R. Lurz, and W. Messer DnaA protein binding to individual DnaA boxes in the Escherichia coli replication origin, oriC EMBO J 16 1997 6574 6583
23. A.C. Leonard, and J.E. Grimwade Regulating DnaA complex assembly: it is time to fill the gaps Curr Opin Microbiol 13 2010 766 772
24. J.P. Erzberger, M.L. Mott, and J.M. Berger Structural basis for ATP-dependent DnaA assembly and replication-origin remodeling Nat Struct Mol Biol 13 2006 676 683
25. S. Zorman, H. Seitz, B. Sclavi, and T.R. Strick Topological characterization of the DnaA-oriC complex using single-molecule nanomanipulation Nucleic Acids Res 40 2012 7375 7383
26. S. Schaper, and W. Messer Interaction of the initiator protein DnaA of Escherichia coli with its DNA target J Biol Chem 270 1995 17622 17626
27. N Fujikawa, H Kurumizaka, O Nureki, T Terada, M Shirouzu, and T Katayama et al. Structural basis of replication origin recognition by the DnaA protein Nucleic Acids Res 31 2003 2077 2086
28. MG Clarey, JP Erzberger, P Grob, AE Leschziner, JM Berger, and E Nogales et al. Nucleotide-dependent conformational changes in the DnaA-like core of the origin recognition complex Nat Struct Mol Biol 13 2006 684 690
29. L. Saiz, and J.M.G. Vilar DNA looping: the consequences and its control Curr Opin Struct Biol 16 2006 344 350
30. S. Ozaki, Y. Noguchi, Y. Hayashi, E. Miyazaki, and T. Katayama Differentiation of the DnaA-oriC subcomplex for DNA unwinding in a replication initiation complex J Biol Chem 287 2012 37458 37471
31. M. Krause, B. Rückert, R. Lurz, and W. Messer Complexes at the replication origin of Bacillus subtilis with homologous and heterologous DnaA protein J Mol Biol 274 1997 365 380
32. G. Scholefield, J. Errington, and H. Murray Soj/ParA stalls DNA replication by inhibiting helix formation of the initiator protein DnaA EMBO J 31 2012 1542 1555
33. S.C. Dillon, and C.J. Dorman Bacterial nucleoid-associated proteins, nucleoid structure and gene expression Nat Rev Microbiol 8 2010 185 195
34. S. Rimsky, and A. Travers Pervasive regulation of nucleoid structure and function by nucleoid-associated proteins Curr Opin Microbiol 14 2011 136 141
35. K.K. Swinger, and P.A. Rice IHF and HU: flexible architects of bent DNA Curr Opin Struct Biol 14 2004 28 35
36. N.A. Becker, J.D. Kahn, and L.J. Maher Effects of nucleoid proteins on DNA repression loop formation in Escherichia coli Nucleic Acids Res 35 2007 3988 4000
37. P.A. Rice, S. Yang, K. Mizuuchi, and H.A. Nash Crystal structure of an IHF-DNA complex: a protein-induced DNA U-turn Cell 87 1996 1295 1306
38. CQ Pan, JA Feng, SE Finkel, R Landgraf, D Sigman, and RC Johnson Structure of the Escherichia coli Fis-DNA complex probed by protein conjugated with 1,10-phenanthroline copper(I) complex Proc Natl Acad Sci USA 91 1994 1721 1725
39. D Skoko, D Yoo, H Bai, B Schnurr, J Yan, and SM McLeod Mechanism of chromosome compaction and looping by the Escherichia coli nucleoid protein Fis J Mol Biol 364 2006 777 798
40. A. Bahloul, F. Boubrik, and J. Rouviere-Yaniv Roles of Escherichia coli histone-like protein HU in DNA replication: HU-beta suppresses the thermosensitivity of dnaA46ts Biochimie 83 2001 219 229
41. S. Chodavarapu, M.M. Felczak, J.R. Yaniv, and J.M. Kaguni Escherichia coli DnaA interacts with HU in initiation at the E coli replication origin Mol Microbiol 67 2008 781 792
42. D.S. Hwang, and A. Kornberg Opening of the replication origin of Escherichia coli by DnaA protein with protein HU or IHF J Biol Chem 267 1992 23083 23086
43. S. Ozaki, K. Fujimitsu, H. Kurumizaka, and T. Katayama The DnaA homolog of the hyperthermophilic eubacterium Thermotoga maritima forms an open complex with a minimal 149-bp origin region in an ATP-dependent manner Genes Cells 11 2006 425 438
44. P. Polaczek Bending of the origin of replication of E coli by binding of IHF at a specific site New Biol 2 1990 265 271
45. M. Filutowicz, W. Ross, J. Wild, and R.L. Gourse Involvement of Fis protein in replication of the Escherichia coli chromosome J Bacteriol 174 1992 398 407
46. H. Gille, J.B. Egan, A. Roth, and W. Messer The FIS protein binds and bends the origin of chromosomal DNA replication, oriC, of Escherichia coli Nucleic Acids Res 19 1991 4167 4172
47. S. Wold, E. Crooke, and K. Skarstad The Escherichia coli Fis protein prevents initiation of DNA replication from oriC in vitro Nucleic Acids Res 24 1996 3527 3532
48. C. Margulies, and J.M. Kaguni The FIS protein fails to block the binding of DnaA protein to oriC, the Escherichia coli chromosomal origin Nucleic Acids Res 26 1998 5170 5175
49. I. Flåtten, and K. Skarstad The Fis protein has a stimulating role in initiation of replication in Escherichia coli in vivo PLoS One 8 2013 e83562
50. M.R. Cassler, J.E. Grimwade, and A.C. Leonard Cell cycle-specific changes in nucleoprotein complexes at a chromosomal replication origin EMBO J 14 1995 5833 5841
51. V.T. Ryan, J.E. Grimwade, C.J. Nievera, and A.C. Leonard IHF and HU stimulate assembly of pre-replication complexes at Escherichia coli oriC by two different mechanisms Mol Microbiol 46 2002 113 124
52. J.E. Grimwade, V.T. Ryan, and A.C. Leonard IHF redistributes bound initiator protein, DnaA, on supercoiled oriC of Escherichia coli Mol Microbiol 35 2000 835 844
53. Y-H Yang, E Song, J Willemse, S-H Park, W-S Kim, and E-J Kim et al. A novel function of Streptomyces integration host factor (sIHF) in the control of antibiotic production and sporulation in Streptomyces coelicolor Antonie Van Leeuwenhoek 101 2012 479 492
54. R. Siam, A.K.C. Brassinga, and G.T. Marczynski A dual binding site for integration host factor and the response regulator CtrA inside the Caulobacter crescentus replication origin J Bacteriol 185 2003 5563 5572
55. V. Castilla-Llorente, D. Munoz-Espin, L. Villar, M. Salas, and W.J.J. Meijer Spo0A, the key transcriptional regulator for entrance into sporulation, is an inhibitor of DNA replication EMBO J 25 2006 3890 3899
56. M Boonstra, IG de Jong, G Scholefield, H Murray, OP Kuipers, and J-W. Veening Spo0A regulates chromosome copy number during sporulation by directly binding to the origin of replication in Bacillus subtilis Mol Microbiol 87 2013 925 938
57. G.S. Briggs, W.K. Smits, and P. Soultanas Chromosomal replication initiation machinery of low-G + C-content Firmicutes J Bacteriol 194 2012 5162 5170
58. W Zhang, MJVM Carneiro, IJ Turner, S Allen, CJ Roberts, and P. Soultanas The Bacillus subtilis DnaD and DnaB proteins exhibit different DNA remodelling activities J Mol Biol 351 2005 66 75
59. W.H. Grainger, C. Machón, D.J. Scott, and P. Soultanas DnaB proteolysis in vivo regulates oligomerization and its localization at oriC in Bacillus subtilis Nucleic Acids Res 38 2010 2851 2864
60. W. Zhang, S. Allen, C.J. Roberts, and P. Soultanas The Bacillus subtilis primosomal protein DnaD untwists supercoiled DNA J Bacteriol 188 2006 5487 5493
61. W Zhang, C Machón, A Orta, N Phillips, CJ Roberts, and S Allen et al. Single-molecule atomic force spectroscopy reveals that DnaD forms scaffolds and enhances duplex melting J Mol Biol 377 2008 706 714
62. S. Marsin, S. McGovern, S.D. Ehrlich, C. Bruand, and P. Polard Early steps of Bacillus subtilis primosome assembly J Biol Chem 276 2001 45818 45825
63. M Velten, S McGovern, S Marsin, SD Ehrlich, P Noirot, and P Polard A two-protein strategy for the functional loading of a cellular replicative DNA helicase Mol Cell 11 2003 1009 1020
64. C Bruand, M Velten, S McGovern, S Marsin, C Sérèna, and SD Ehrlich et al. Functional interplay between the Bacillus subtilis DnaD and DnaB proteins essential for initiation and re-initiation of DNA replication Mol Microbiol 55 2005 1138 1150
65. C. Ioannou, P.M. Schaeffer, N.E. Dixon, and P. Soultanas Helicase binding to DnaI exposes a cryptic DNA-binding site during helicase loading in Bacillus subtilis Nucleic Acids Res 34 2006 5247 5258
66. C. Nievera, J.J.-C. Torgue, J.E. Grimwade, and A.C. Leonard SeqA blocking of DnaA-oriC interactions ensures staged assembly of the E coli pre-RC Mol Cell 24 2006 581 592
67. S Slater, S Wold, M Lu, E Boye, K Skarstad, and N Kleckner E coli SeqA protein binds oriC in two different methyl-modulated reactions appropriate to its roles in DNA replication initiation and origin sequestration Cell 82 1995 927 936
68. T. Bach, Morigen, and K. Skarstad The initiator protein DnaA contributes to keeping new origins inactivated by promoting the presence of hemimethylated DNA J Mol Biol 384 2008 1076 1085
69. H.K. Klungsøyr, and K. Skarstad Positive supercoiling is generated in the presence of Escherichia coli SeqA protein Mol Microbiol 54 2004 123 131
70. A Guarné, T Brendler, Q Zhao, R Ghirlando, S Austin, and W Yang Crystal structure of a SeqA-N filament: implications for DNA replication and chromosome organization EMBO J 24 2005 1502 1511
71. I. Odsbu, H.K. Klungsøyr, S. Fossum, and K. Skarstad Specific N-terminal interactions of the Escherichia coli SeqA protein are required to form multimers that restrain negative supercoils and form foci Genes Cells 10 2005 1039 1049
72. K. Skarstad, G. Lueder, R. Lurz, C. Speck, and W. Messer The Escherichia coli SeqA protein binds specifically and co-operatively to two sites in hemimethylated and fully methylated oriC Mol Microbiol 36 2000 1319 1326
73. T. Weitao, K. Nordström, and S. Dasgupta Escherichia coli cell cycle control genes affect chromosome superhelicity EMBO Rep 1 2000 494 499
74. F. Molina, and K. Skarstad Replication fork and SeqA focus distributions in Escherichia coli suggest a replication hyperstructure dependent on nucleotide metabolism Mol Microbiol 52 2004 1597 1612
75. R.E. Bird, J. Louarn, J. Martuscelli, and L. Caro Origin and sequence of chromosome replication in Escherichia coli J Mol Biol 70 1972 549 566
76. L.F. Liu, and J.C. Wang Supercoiling of the DNA template during transcription Proc Natl Acad Sci USA 84 1987 7024 7027
77. M. Rajewska, K. Wegrzyn, and I. Konieczny AT-rich region and repeated sequences - the essential elements of replication origins of bacterial replicons FEMS Microbiol Rev 36 2012 408 434
78. M.A. Schauzu, C. Kücherer, R. Kölling, W. Messer, and H. Lother Transcripts within the replication origin, oriC, of Escherichia coli Nucleic Acids Res 15 1987 2479 2497
79. J. Zakrzewska-Czerwińska, J. Majka, and H. Schrempf Minimal requirements of the Streptomyces lividans 66 oriC region and its transcriptional and translational activities J Bacteriol 177 1995 4765 4771
80. T.A. Baker, and A. Kornberg Transcriptional activation of initiation of replication from the E coli chromosomal origin: an RNA-DNA hybrid near oriC Cell 55 1988 113 123
81. K. Skarstad, T.A. Baker, and A. Kornberg Strand separation required for initiation of replication at the chromosomal origin of E coli is facilitated by a distant RNA-DNA hybrid EMBO J 9 1990 2341 2348
82. M. Tanaka, and S. Hiraga Negative control of oriC plasmid replication by transcription of the oriC region Mol Gen Genet 200 1985 21 26
83. T. Ogawa, and T. Okazaki Cell cycle-dependent transcription from the gid and mioC promoters of Escherichia coli J Bacteriol 176 1994 1609 1615
84. I. Flåtten, Morigen, and K. Skarstad DnaA protein interacts with RNA polymerase and partially protects it from the effect of rifampicin Mol Microbiol 71 2009 1018 1030
85. A. Szambowska, M. Pierechod, G. Wegrzyn, and M. Glinkowska Coupling of transcription and replication machineries in λ DNA replication initiation: evidence for direct interaction of Escherichia coli RNA polymerase and the λO protein Nucleic Acids Res 39 2011 168 177
86. L. Salazar Inhibition of chromosome replication in Mycobacterium smegmatis: effect of the rpmH-dnaA promoter region Microbiology 146 2000 2199 2207
87. L. Salazar, E. Guerrero, Y. Casart, L. Turcios, and F. Bartoli Transcription analysis of the dnaA gene and oriC region of the chromosome of Mycobacterium smegmatis and Mycobacterium bovis BCG, and its regulation by the DnaA protein Microbiology 149 2003 773 784
88. S. Chauhan, and J.S. Tyagi Analysis of transcription at the oriC locus in Mycobacterium tuberculosis Microbiol Res 166 2011 508 514
89. D.B. Bates, E. Boye, T. Asai, and T. Kogoma The absence of effect of gid or mioC transcription on the initiation of chromosomal replication in Escherichia coli Proc Natl Acad Sci USA 94 1997 12497 12502
90. T. Hase, M. Nakai, and Y. Masamune Transcription of a region downstream from lambda ori is required for replication of plasmids derived from coliphage lambda Mol Gen Genet 216 1989 120 125
91. A. Szalewska, G. Wegrzyn, and K. Taylor Neither absence nor excess of lambda O initiator-digesting ClpXP protease affects lambda plasmid or phage replication in Escherichia coli Mol Microbiol 13 1994 469 474
92. G. Wȩgrzyn, K. Licznerska, and A. Wȩgrzyn Phage λ - new insights into regulatory circuits Adv Virus Res 82 2012 155 178
93. A. Løbner-Olesen, and E. Boye Different effects of mioC transcription on initiation of chromosomal and minichromosomal replication in Escherichia coli Nucleic Acids Res 20 1992 3029 3036
94. W.G. Miller, and R.W. Simons Chromosomal supercoiling in Escherichia coli Mol Microbiol 10 1993 675 684
95. A. Travers, and G. Muskhelishvili A common topology for bacterial and eukaryotic transcription initiation? EMBO Rep 8 2007 147 151
96. R. Kanaar, and N.R. Cozzarelli Roles of supercoiled DNA structure in DNA transactions Curr Opin Struct Biol 2 1992 369 379
97. K. Drlica Control of bacterial DNA supercoiling Mol Microbiol 6 1992 425 433
98. V.L. Balke, and J.D. Gralla Changes in the linking number of supercoiled DNA accompany growth transitions in Escherichia coli J Bacteriol 169 1987 4499 4506
99. C.J. Dorman, G.C. Barr, N. Ni Bhriain, and C.F. Higgins DNA supercoiling and the anaerobic and growth phase regulation of tonB gene expression J Bacteriol 170 1988 2816 2826
100. J.B. Schvartzman, and A. Stasiak A topological view of the replicon EMBO Rep 5 2004 256 261
101. E. Crooke, D.S. Hwang, K. Skarstad, B. Thöny, and A. Kornberg E coli minichromosome replication: regulation of initiation at oriC Res Microbiol 142 1991 127 130
102. U. Von Freiesleben, and K.V. Rasmussen The level of supercoiling affects the regulation of DNA replication in Escherichia coli Res Microbiol 143 1992 655 663
103. B.E. Funnell, T.A. Baker, and A. Kornberg in vitro assembly of a prepriming complex at the origin of the Escherichia coli chromosome J Biol Chem 262 1987 10327 10334
104. E. Goldstein, and K. Drlica Regulation of bacterial DNA supercoiling: plasmid linking numbers vary with growth temperature Proc Natl Acad Sci USA 81 1984 4046 4050
105. R. González-Soltero, E. Botello, and A. Jiménez- Sánchez Initiation of heat-induced replication requires DnaA and the L-13-mer of oriC J Bacteriol 188 2006 8294 8298
106. EL Zechiedrich, AB Khodursky, S Bachellier, R Schneider, D Chen, and DM Lilley Roles of topoisomerases in maintaining steady-state DNA supercoiling in Escherichia coli J Biol Chem 275 2000 8103 8113
107. J.J. Champoux DNA topoisomerases: structure, function, and mechanism Annu Rev Biochem 70 2001 369 413
108. J.L. Snoep, C.C. van der Weijden, H.W. Andersen, H.V. Westerhoff, and P.R. Jensen DNA supercoiling in Escherichia coli is under tight and subtle homeostatic control, involving gene-expression and metabolic regulation of both topoisomerase I and DNA gyrase Eur J Biochem 269 2002 1662 1669
109. M. Gellert, M.H. O'Dea, T. Itoh, and J. Tomizawa Novobiocin and coumermycin inhibit DNA supercoiling catalyzed by DNA gyrase Proc Natl Acad Sci USA 73 1976 4474 4478
110. M. Gellert, K. Mizuuchi, M.H. O'Dea, and H.A. Nash DNA gyrase: an enzyme that introduces superhelical turns into DNA Proc Natl Acad Sci USA 73 1976 3872 3876
111. N. Ogasawara, M. Seiki, and H. Yoshikawa Effect of novobiocin on initiation of DNA replication in Bacillus subtilis Nature 281 1979 702 704
112. J. Louarn, J.P. Bouché, J. Patte, and J.M. Louarn Genetic inactivation of topoisomerase I suppresses a defect in initiation of chromosome replication in Escherichia coli Mol Gen Genet 195 1984 170 174
113. D.P. Biek, and S.N. Cohen Propagation of pSC101 plasmids defective in binding of integration host factor J Bacteriol 174 1992 785 792
114. T.A. Azam, and A. Ishihama Twelve species of the nucleoid-associated protein from Escherichia coli. Sequence recognition specificity and DNA binding affinity J Biol Chem 274 1999 33105 33113
115. R Mercier, M-G Petit, S Schbath, S Robin, M El Karoui, and F Boccard et al. The MatP/matS site-specific system organizes the terminus region of the E coli chromosome into a macrodomain Cell 135 2008 475 485
116. J. Teramoto, S.H. Yoshimura, K. Takeyasu, and A. Ishihama A novel nucleoid protein of Escherichia coli induced under anaerobiotic growth conditions Nucleic Acids Res 38 2010 3605 3618
117. S.S. Broyles, and D.E. Pettijohn Interaction of the Escherichia coli HU protein with DNA. Evidence for formation of nucleosome-like structures with altered DNA helical pitch J Mol Biol 187 1986 47 60
118. A. Bensaid, A. Almeida, K. Drlica, and J. Rouviere-Yaniv Cross-talk between topoisomerase I and HU in Escherichia coli J Mol Biol 256 1996 292 300
119. M. Malik, A. Bensaid, J. Rouviere-Yaniv, and K. Drlica Histone-like protein HU and bacterial DNA topology: suppression of an HU deficiency by gyrase mutations J Mol Biol 256 1996 66 76
120. O Huisman, M Faelen, D Girard, A Jaffé, A Toussaint, and J Rouvière-Yaniv Multiple defects in Escherichia coli mutants lacking HU protein J Bacteriol 171 1989 3704 3712
121. F. Bartels, S. Fernández, A. Holtel, K.N. Timmis, and V. de Lorenzo The essential HupB and HupN proteins of Pseudomonas putida provide redundant and nonspecific DNA-bending functions J Biol Chem 276 2001 16641 16648
122. B. Micka, and M.A. Marahiel The DNA-binding protein HBsu is essential for normal growth and development in Bacillus subtilis Biochimie 74 1992 641 650
123. S. Nozaki, Y. Yamada, and T. Ogawa Initiator titration complex formed at datA with the aid of IHF regulates replication timing in Escherichia coli Genes Cells 14 2009 329 341
124. J. Zakrzewska-Czerwińska, D. Jakimowicz, A. Zawilak-Pawlik, and W. Messer Regulation of the initiation of chromosomal replication in bacteria FEMS Microbiol Rev 31 2007 378 387
125. K. Kasho, and T. Katayama DnaA binding locus datA promotes DnaA-ATP hydrolysis to enable cell cycle-coordinated replication initiation Proc Natl Acad Sci USA 110 2013 936 941
126. J.P. Swiercz, T. Nanji, M. Gloyd, A. Guarné, and M.A. Elliot A novel nucleoid-associated protein specific to the actinobacteria Nucleic Acids Res 41 2013 4171 4184
127. B.-K. Cho, E.M. Knight, C.L. Barrett, and B.∅. Palsson Genome-wide analysis of Fis binding in Escherichia coli indicates a causative role for A-/AT-tracts Genome Res 18 2008 900 910
128. A. Travers, R. Schneider, and G. Muskhelishvili DNA supercoiling and transcription in Escherichia coli: the FIS connection Biochimie 83 2001 213 217
129. R. Schneider, A. Travers, T. Kutateladze, and G. Muskhelishvili A DNA architectural protein couples cellular physiology and DNA topology in Escherichia coli Mol Microbiol 34 1999 953 964
130. D. Weinstein-Fischer, and S. Altuvia Differential regulation of Escherichia coli topoisomerase I by Fis Mol Microbiol 63 2007 1131 1144
131. A. Jeltsch Beyond Watson and Crick: DNA methylation and molecular enzymology of DNA methyltransferases ChemBioChem 3 2002 274 293
132. J. Casadesús, and D. Low Epigenetic gene regulation in the bacterial world Microbiol Mol Biol Rev 70 2006 830 856
133. A. Løbner-Olesen, O. Skovgaard, and M.G. Marinus Dam methylation: coordinating cellular processes Curr Opin Microbiol 8 2005 154 160
134. V.G. Kossykh, and R.S. Lloyd A DNA adenine methyltransferase of Escherichia coli that is cell cycle regulated and essential for viability J Bacteriol 186 2004 2061 2067
135. T. Barbeyron, K. Kean, and P. Forterre DNA adenine methylation of GATC sequences appeared recently in the Escherichia coli lineage J Bacteriol 160 1984 586 590
136. F. Barras, and M.G. Marinus The great GATC: DNA methylation in E coli Trends Genet 5 1989 139 143
137. M.G. Marinus, and N.R. Morris Pleiotropic effects of a DNA adenine methylation mutation (dam-3) in Escherichia coli K12 Mutat Res 28 1975 15 26
138. W. Messer, and M. Noyer-Weidner Timing and targeting: the biological functions of Dam methylation in E coli Cell 54 1988 735 737
139. W. Messer, U. Bellekes, and H. Lother Effect of dam methylation on the activity of the E coli replication origin, oriC EMBO J 4 1985 1327 1332
140. DW Smith, AM Garland, G Herman, RE Enns, TA Baker, and JW Zyskind Importance of state of methylation of oriC GATC sites in initiation of DNA replication in Escherichia coli EMBO J 4 1985 1319 1326
141. E. Boye, and A. Løbner-Olesen The role of dam methyltransferase in the control of DNA replication in E coli Cell 62 1990 981 989
142. P. Polaczek, K. Kwan, D.A. Liberies, and J.L. Campbell Role of architectural elements in combinatorial regulation of initiation of DNA replication in Escherichia coli Mol Microbiol 26 1997 261 275
143. P. Polaczek, K. Kwan, and J.L. Campbell GATC motifs may alter the conformation of DNA depending on sequence context and N6-adenine methylation status: possible implications for DNA-protein recognition Mol Gen Genet 258 1998 488 493
144. SM Julio, DM Heithoff, D Provenzano, KE Klose, RL Sinsheimer, and DA Low et al. DNA adenine methylase is essential for viability and plays a role in the pathogenesis of Yersinia pseudotuberculosis and Vibrio cholerae Infect Immun 69 2001 7610 7615
145. D. Saint-Dic, J. Kehrl, B. Frushour, and L.S. Kahng Excess SeqA leads to replication arrest and a cell division defect in Vibrio cholerae J Bacteriol 190 2008 5870 5878
146. A. Aloui, A. Chatty, A. El May, and A. Landoulsi The effect of methylation on DNA replication in Salmonella enterica serovar typhimurium C R Biol 330 2007 576 580
147. G. Demarre, and D.K. Chattoraj DNA adenine methylation is required to replicate both Vibrio cholerae chromosomes once per cell cycle PLoS Genet 6 2010 e1000939
148. B. Koch, X. Ma, and A. Løbner-Olesen Replication of Vibrio cholerae chromosome I in Escherichia coli: dependence on dam methylation J Bacteriol 192 2010 3903 3914
149. R. Wright, C. Stephens, and L. Shapiro The CcrM DNA methyltransferase is widespread in the alpha subdivision of proteobacteria, and its essential functions are conserved in Rhizobium meliloti and Caulobacter crescentus J Bacteriol 179 1997 5869 5877
150. G. Zweiger, G. Marczynski, and L. Shapiro A Caulobacter DNA methyltransferase that functions only in the predivisional cell J Mol Biol 235 1994 472 485
151. C. Stephens, A. Reisenauer, R. Wright, and L. Shapiro A cell cycle-regulated bacterial DNA methyltransferase is essential for viability Proc Natl Acad Sci USA 93 1996 1210 1214
152. J. Collier, H.H. McAdams, and L. Shapiro A DNA methylation ratchet governs progression through a bacterial cell cycle Proc Natl Acad Sci USA 104 2007 17111 17116
153. A. Reisenauer, and L. Shapiro DNA methylation affects the cell cycle transcription of the CtrA global regulator in Caulobacter EMBO J 21 2002 4969 4977
154. R. Kumar, and D.N. Rao Role of DNA methyltransferases in epigenetic regulation in bacteria Subcell Biochem 61 2012 81 102
155. RA Alm, LS Ling, DT Moir, BL King, ED Brown, and PC Doig et al. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori Nature 397 1999 176 180
156. J Krebes, RD Morgan, B Bunk, C Spröer, K Luong, and R Parusel et al. The complex methylome of the human gastric pathogen Helicobacter pylori Nucleic Acids Res 42 2014 2415 2432
157. R. Reyes-Lamothe, E. Nicolas, and D.J. Sherratt Chromosome replication and segregation in bacteria Annu Rev Genet 46 2012 121 143
158. D. Jakimowicz, K. Chater, and J. Zakrzewska-Czerwínska The ParB protein of Streptomyces coelicolor A3(2) recognizes a cluster of parS sequences within the origin-proximal region of the linear chromosome Mol Microbiol 45 2002 1365 1377
159. A. Robinson, and A.M. van Oijen Bacterial replication, transcription and translation: mechanistic insights from single-molecule biochemical studies Nat Rev Microbiol 11 2013 303 315
160. R.T. Dame, M.C. Noom, and G.J.L. Wuite Bacterial chromatin organization by H-NS protein unravelled using dual DNA manipulation Nature 444 2006 387 390
161. H. Yardimci, A.B. Loveland, A.M. van Oijen, and J.C. Walter Single-molecule analysis of DNA replication in Xenopus egg extracts Methods 57 2012 179 186
162. A.H. Hardin, S.H. Sarkar, Y. Seol, G.F. Liou, N. Osheroff, and K.C. Neuman Direct measurement of DNA bending by type IIA topoisomerases: implications for non-equilibrium topology simplification Nucleic Acids Res 39 2011 5729 5743
163. I. Lee, K.C. Dong, and J.M. Berger The role of DNA bending in type IIA topoisomerase function Nucleic Acids Res 41 2013 5444 5456
164. A. Gahlmann, and W.E. Moerner Exploring bacterial cell biology with single-molecule tracking and super-resolution imaging Nat Rev Microbiol 12 2014 9 22