Regulation of the initiation of chromosomal replication in bacteria

FEMS Microbiology Reviews

Volumn 31, Issue 4, 2007, Pages 378-387

  Zakrzewska Czerwińska, Jolanta ^a   Jakimowicz, Dagmara ^a   Zawilak Pawlik, Anna ^a   Messer, Walter ^b  

^a INSTITUTE OF IMMUNOLOGY AND EXPERIMENTAL THERAPY   (Poland)

^b MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

Author keywords

DnaA; oriC; Orisome; Regulatory protein; Two component signal transduction system

Indexed keywords

DNA A; GENE PRODUCT; ORIC PROTEIN; UNCLASSIFIED DRUG;

BACTERIAL CHROMOSOME; BACTERIUM; CHROMOSOME REPLICATION; DNA SYNTHESIS; ENDOSYMBIONT; ESCHERICHIA COLI; GENE CONTROL; NONHUMAN; PATHOGENESIS; REVIEW;

BACTERIA; BACTERIAL PROTEINS; CHROMOSOMES, BACTERIAL; DNA REPLICATION; DNA, BACTERIAL; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; ORIGIN RECOGNITION COMPLEX; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA; PROKARYOTA;

EID: 34250324310     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1111/j.1574-6976.2007.00070.x     Document Type: Review

References (108)

1. Akman L, Yamashita A, Watanabe H, Oshima K, Shiba T, Hattori M Aksoy S (2002) Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat Genet 32: 402 407.
2. Baldus JM, Green BD, Youngman P Moran CP Jr. (1994) Phosphorylation of Bacillus subtilis transcription factor Spo0A stimulates transcription from the spoIIG promoter by enhancing binding to weak 0A boxes. J Bacteriol 176: 296 306.
3. Boye E, Lobner-Olesen A Skarstad K (2000) Limiting DNA replication to once & only once. EMBO Rep 1: 479 483.
4. Brazhnik P Tyson JJ (2006) Cell cycle control in bacteria and yeast: a case of convergent evolution? Cell Cycle 5: 522 529.
5. Bruand C, Velten M, McGovern S, Marsin S, Serena C, Ehrlich D Polard P (2005) Functional interplay between the Bacillus subtilis DnaD and DnaB proteins essential for initiation and re-initiation of DNA replication. Mol Microbiol 55: 1138 1150.
6. Burkholder WF, Kurtser I Grossman AD (2001) Replication initiation proteins regulate a developmental checkpoint in Bacillus subtilis. Cell 104: 269 279.
7. Camara JE, Breier AM, Brendler T, Austin S, Cozzarelli NR Crooke E (2005) Hda inactivation of DnaA is the predominant mechanism preventing hyperinitiation of Escherichia coli DNA replication. EMBO Reports 6: 1 6.
8. Carneiro MJV, Zhang W, Ioannou C, Scott DJ, Allen S, Roberts CJ Soultanas P (2006) The DNA-remodelling activity of DnaD is the sum of oligomerization and DNA-binding activities on separate domains. Mol Microbiol 60: 917 924.
9. Cassler MR, Grimwade JE Leonard AC (1995) Cell cycle-specific changes in nucleoprotein complexes at a chromosomal replication origin. EMBO J 14: 5833 5841.
10. Castilla-Liorente V, Munoz-Espin D, Villar L, Salas M Meijer WJJ (2006) Spo0A, the key transcriptional regulator for entrance into sporulation, is an inhibitor of DNA replication. EMBO J 25: 3890 3899.
11. Clarey MG, Erzberger JP, Grob P, Leschziner AE, Berger JM, Nogales E Botchan M (2006) Nucleotide-dependent conformational changes in the DnaA-like core of the origin recognition complex. Nat Struct Mol Biol 13: 684 690.
12. Collier J, Murray SR Shapiro L (2006) DnaA couples DNA replication and the expression of two cell cycle master regulators. EMBO J 25: 346 356.
13. Crosson S, McAdams H Shapiro L (2004) A genetic oscillator and the regulation of cell cycle progression in Caulobacter crescentus. Cell Cycle 10: 1252 1254.
14. Cunningham EL Berger JM (2005) Unraveling the early steps of prokaryotic replication. Curr Opin Struct Biol 15: 68 76.
15. Davey MJ, Jeruzalmi D, Kuriyan J O'Donnell M (2002) Motors and switches: AAA+machines within the replisome. Nat Rev Mol Cell Biol 3: 826 835.
16. Degnan PH, Lazarus AB Wernegreen JJ (2005) Genome sequence of Blochmannia pennsylvanicus indicates parallel evolutionary trends among bacterial mutualists of insects. Genome Res 8: 1023 1033.
17. Domain IJ, Reisenauer A Shapiro L (1999) Feedback control of a master bacterial cell-cycle regulator. Proc Natl Acad Sci USA 96: 6648 6653.
18. Duigou S, Knudsen KG, Skovgaard O, Egan ES, Løbner-Olesen A Waldor MK (2006) Independent control of replication initiation of the two Vibrio cholerae chromosomes by DnaA and RctB. J Bacteriol 188: 6419 6424.
19. Egan ES, Fogel MA Waldor MK (2005) Divided genomes: negotiating the cell cycle in prokaryotes with multiple chromosomes. Mol Microbiol 56: 1129 1138.
20. Egan ES Waldor MK (2003) Distinct replication requirements for the two Vibrio cholerae chromosomes. Cell 114: 521 530.
21. Egan ES, Løbner-Olesen A Waldor MK (2004) Synchronous replication initiation of the two Vibrio cholerae chromosomes. Curr Biol 14: R501 R502.
22. Errington J, Murray H Wu LJ (2005) Diversity and redundancy in bacterial chromosome segregation mechanisms. Phil Trans R Soc B 360: 497 505.
23. Erzberger JP, Pirruccello MM Berger JM (2002) The structure of bacterial DnaA: implications for general mechanisms underlying DNA replication initiation. EMBO J 21: 4763 4773.
24. Erzberger JP, Mott ML Berger JM (2006) Structural basis for ATP-dependent DnaA assembly and replication-origin remodeling. Nat Struct Mol Biol 13: 676 683.
25. Felczak MM, Simmons LA Kaguni JM (2005) An essential tryptophan of Escherichia coli DnaA protein functions in oligomerization at the E. coli replication origin. J Biol Chem 280: 24627 24633.
26. Fol M, Chauhan A, Nair NK, Malone E, Moomey M, Jagannath C, Madiraju MV Rajagopalan M (2006) Modulation of Mycobacterium tuberculosis proliferation by MtrA, an essential two-component response regulator. Mol Microbiol 60: 643 657.
27. Foster J, Ganatra M, Kamal I et al 2005) The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol 3 e121: 599 612.
28. Fukuoka T, Moriya S, Yoshikawa H Ogasawara N (1990) Purification and characterization of an initiation protein for chromosomal replication, DnaA, in Bacillus subtilis. J Biochem 107: 732 739.
29. Gil R, Silva FJ, Zientz E et al 2003) The genome sequence of Blochmannia floridanus: comparative analysis of reduced genomes. Proc Natl Acad Sci USA 100: 9388 9393.
30. Gon S, Camara JE, Klungsoyr HK, Crooke E, Skarstad K Beckwith J (2006) A novel regulatory mechanism couples deoxyribonucleotide synthesis and DNA replication in Escherichia coli. EMBO J 25: 1137 1147.
31. Goranov AI, Katz L, Breier AM, Burge ChB Grossman AD (2005) A transcriptional response to replication status mediated by the conserved bacterial replication protein DnaA. Proc Natl Acad Sci USA 102: 12932 12937.
32. Gorbatyuk B Marczynski GT (2005) Regulated degradation of chromosome replication proteins DnaA and CtrA in Caulobacter crescentus. Mol Microbiol 55: 1233 1245.
33. Han JS, Park JY, Lee YS, Thony B Hwang DS (1999) PhoB-dependent transcriptional activation of the iciA gene during starvation for phosphate in Escherichia coli. Mol Gen Genet 262: 448 452.
34. Hayashi M, Ogura Y, Harry EJ, Ogasawara N Moriya S (2005) Bacillus subtilis YabA is involved in determining the timing and synchrony of replication initiation. FEMS Microbiol Lett 247: 73 79.
35. Heidelberg JF, Eisen JA, Nelson WC et al 2000) DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406: 469 470.
36. Holtzendorff J, Hung D, Brende P, Reisenauer A, Viollier PH, McAdams HH Shapiro L (2004) Oscillating global regulators control the genetic circuit driving a bacterial cell cycle. Science 304: 983 987.
37. Holtzendorff J, Reinhardt J Viollier PH (2006) Cell cycle control by oscillating regulatory proteins in Caulobacter crescentus. BioEssays 28: 355 361.
38. Hoskisson PA Hutchings MI (2006) MtrAB-LpqB: a conserved three-component system in actinobacteria? Trends Microbiol 14: 444 449.
39. Hottes AK, Shapiro L McAdams HH (2005) DnaA coordinates replication initiation and cell cycle transcription in Caulobacter crescentus. Mol Microbiol 58: 1340 1353.
40. Hung DY Shapiro L (2002) A signal transduction protein cues proteolytic events critical to Caulobacter cell cycle progression. Proc Natl Acad Sci USA 99: 13160 13165.
41. Hwang DS Kornberg A (1992) Opening of the replication origin of Escherichia coli by DnaA protein with protein HU or IHF. J Biol Chem 267: 23083 23086.
42. Ishida T, Akimitsu N, Kashioka T, Hatano M, Kubota T, Ogata Y, Sekimizu K Katayama T (2004) DiaA, a novel DnaA-binding protein, ensures the timely initiation of Escherichia coli chromosome replication. J Biol Chem 279: 45546 45555.
43. Iuchi S Weiner L (1996) Cellular and molecular physiology of Escherichia coli in the adaptation to aerobic environments. J Biochem 120: 1055 1063.
44. Jakimowicz D, Chater K Zakrzewska-Czerwińska J (2002) 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: 1365 1377.
45. Jakimowicz D, Gust B, Zakrzewska-Czerwińska J Chater C (2005) Developmental-stage-specific assembly of ParB complexes in Streptomyces coelicolor hyphae. J Bacteriol 187: 3572 3580.
46. Jenal U Fuchs T (1998) An essential protease involved in bacterial cell-cycle control. EMBO J 17: 5658 5669.
47. Jensen RB (2006) Coordination between chromosome replication, segregation, and cell division in Caulobacter crescentus. J Bacteriol 188: 2244 2253.
48. Kaguni JM (2006) DnaA: controlling the initiation of bacterial DNA replication and more. Annu Rev Microbiol 60: 351 371.
49. Kahng LS Shapiro L (2001) The CcrM DNA methyltransferase of Agrobacterium tumefaciens is essential, and its activity is cell cycle regulated. J Bacteriol 181: 3065 3075.
50. Katayama T (2001) Feedback controls restrain the initiation of Escherichia coli chromosomal replication. Mol Microbiol 41: 9 17.
51. Katayama T, Kubota T, Kurokawa K, Crooke E Sekimizu K (1998) The initiator function of DnaA protein is negatively regulated by the sliding clamp of the E. coli chromosomal replicase. Cell 94: 61 71.
52. Kato J (2005) Regulatory network of the initiation of chromosomal replication in Escherichia coli. Critical Rev Biochem Mol Biol 40: 331 342.
53. Kato J Katayama T. (2001) Hda, a novel DnaA-related protein, regulates the replication cycle in Escherichia coli. EMBO J 20: 4253 4262.
54. Kim MS, Bae SH, Yun SH et al 2005) Cnu, a novel oriC-binding protein of Escherichia coli. J Bacteriol 187: 6998 7008.
55. Kim S, Dallmann HG, McHenry CS Marians KJ (1996) Coupling of a replicative polymerase and helicase: a tau-DnaB interaction mediates rapid replication fork movement. Cell 84: 643 650.
56. Kitagawa R, Ozaki T, Moriya S Ogawa T (1998) Negative control of replication initiation by a novel chromosomal locus exhibiting exceptional affinity for Escherichia coli DnaA protein. Genes Dev 12: 3032 3043.
57. Konieczny I. (2003) Strategies for helicase recruitment and loading in bacteria. EMBO Rep 4: 37 41.
58. Lee DG Bell SP (2000) ATPase switches controlling DNA replication initiation. Curr Opin Cell Biol 3: 280 285.
59. Lee PS Grossman AD (2006) The chromosome partitioning proteins Soj (ParA) and Spo0J (ParB) contribute to accurate chromosome partitioning, separation of replicated sister origins, and regulation of replication initiation in Bacillus subtilis. Mol Microbiol 60: 853 869.
60. Lee PS, Lin DCH, Shigeki MS Grossman AD (2003) Effects of the chromosome partitioning protein Spo0J (ParB) on oriC positioning and replication initiation in Bacillus subtilis. J Bacteriol 185: 1326 1337.
61. Lee YS, Han JS, Jeon Y Hwang DS (2001) The Arc two-component signal transduction system inhibits in vitro Escherichia coli chromosomal initiation. J Biol Chem 276: 9917 9923.
62. Leonard AC Grimwade JE (2005) Building a bacterial orisome: emergence of new regulatory features for replication origin unwinding. Mol Microbiol 55: 978 985.
63. Lobner-Olesen A, Skovgaard O Marinus MG (2005) Dam methylation: coordinating cellular processes. Curr Opin Microbiol 8: 154 160.
64. Lu Y-B, Ratnakar PVAL, Mohanty B. Bastia D (1996) Direct physical interaction between DnaG primase and DnaB helicase of Escherichia coli is necessary for optimal synthesis of primer RNA. Pro. Natl Aca Sci USA 93: 12902 12907.
65. Maaloe O Kjeldgaard NO (1966) Control of Macromolecular Synthesis. W.A. Benjamin, Inc., New York, NY.
66. Mackiewicz P, Zakrzewska-Czerwiñska J, Zawilak A, Dudek MR Cebrat S (2004) Where does bacterial replication start? Rules for predicting the oriC region. Nucl Acids Res 32: 3781 3791.
67. Madiraju MVV, Moomey M, Neuenschwander PF, Muniruzzaman S, Yamamoto K, Grimwade JE Rajagopalan M (2006) The intrinsic ATPase activity of Mycobacterium tuberculosis DnaA promotes its rapid oliogmerization on oriC. Mol Microbiol 59: 1876 1890.
68. Majka J, Messer W, Schrempf H Zakrzewska-Czerwińska J (1997) Purification and characterization of the Streptomyces lividans initiator protein DnaA. J Bacteriol 179: 2426 2432.
69. Marczynski GT Shapiro L (2002) Control of chromosome replication in Caulobacter crescentus. Annu Rev Microbiol 56: 625 656.
70. Margolin W Bernander R (2004) How do prokaryotic cells cycle? Curr Biol 14: R768 R770.
71. McAdams HH Shapiro L (2003) A bacterial cell-cycle regulatory network operating in time and space. Science 301: 1874 1877.
72. McGrath PT, Viollier P McAdams HH (2004) Setting the pace: mechanisms tying Caulobacter cell-cycle progression to macroscopic cellular events. Curr Opin Microbiol 7: 192 197.
73. Mergaert P, Uchiumi T, Alunni B et al 2006) Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. Proc Natl Acad Sci USA 103: 5230 5235.
74. Messer W Weigel C (1997) DnaA initiator-also a transcription factor. Mol Microbiol 24: 1 6.
75. Messer W (2002) The bacterial replication initiator DnaA. DnaA & oriC, the bacterial mode to initiate DNA replication. FEMS Microbiol Rev 26: 355 374.
76. Moran NA (2002) Microbial minimalism: genome reduction in bacterial pathogens. Cell 108: 583 586.
77. Moriya S, Ima Y, Hassan AK Ogasawara N (1999) Regulation of initiation of Bacillus subtilis chromosome replication. Plasmid 41: 17 29.
78. Mukhopadhyay S Chattoraj DK (2000) Replication-induced transcription of an autorepressed gene: the replication initiator gene of plasmid P1. Proc Natl Acad Sci USA 97: 7142 7147.
79. Murray H, Ferreira H Errington J (2006) The bacterial chromosome segregation protein Spo0J spreads along DNA from parS nucleation sites. Mol Microbiol 61: 1352 1361.
80. Noirot-Gros MF, Dervyn E, Wu LJ, Mervelet P, Errington J, Ehrlich SD Noirot P (2002) An expanded view of bacterial DNA replication. Proc Natl Acad Sci USA 99: 8342 8347.
81. Noirot-Gros MF, Velten M, Yoshimura M, McGovern S, Morimoto T, Ehrlich SD, Ogasawara N, Polard P Noirot P (2006) Functional dissection of YabA, a negative regulator of DNA replication initiation in Bacillus subtilis. Proc Natl Acad Sci USA 103: 2368 2373.
82. Ogura Y, Imai Y, Ogasawara N Moriya S (2001) Autoregulation of the dnaA-dnaN operon and effects of DnaA protein levels on replication initiation in Bacillus subtilis. J Bacteriol 183: 3833 3841.
83. Ozaki S, Fujimitsu K, Kurumizaka H Katayama T (2006) 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: 425 438.
84. Park K, Han E, Paulsson J Chattoraj DK (2001) Origin pairing ('handcuffing') as a mode of negative control of P1 plasmid copy number. EMBO J 20: 7323 7332.
85. Paulsson J Chattoraj DK (2006) Origin inactivation in bacterial DNA replication control. Mol Microbiol 61: 9 15.
86. Quon KC, Yang B, Domian IJ, Shapiro L Marczynski GT (1998) Negative control of bacterial DNA replication by a cell cycle regulatory protein that binds at the chromosome origin. Proc Natl Acad Sci USA 95: 120 125.
87. Riber L, Olsson JA, Jensen RB, Skovgaard O, Dasgupta S, Marinus MG Lobner-Olesen A (2006) Hda mediated inactivation of the DnaA protein and dnaA gene autoregulation act in concert to ensure homeostatic maintenance of the Escherichia coli chromosome. Genes Dev 20: 2121 2134.
88. Robinson NP Bell SD (2005) Origins of DNA replication in the three domains of life. FEBS J 272: 3757 3766.
89. Ruban-Osmialowska B, Jakimowicz D, Smulczyk-Krawczyszyn A, Chater KF Zakrzewska-Czerwińska J (2006) Replisome localization in vegetative and aerial hyphae of Streptomyces coelicolor. J Bacteriol 188: 7311 7316.
90. Ryan VT, Grimwade JE, Camara JE, Crooke E Leonard AC (2004) Escherichia coli prereplication complex assembly is regulated by dynamic interplay among Fis, IHF and DnaA. Mol Microbiol 51: 1347 1359.
91. Schaeffer PM, Headlam MJ Dixon NE (2005) Protein-protein interactions in the eubacterial replisome. IUBMB Life 57: 5 12.
92. Schaper S, Nardmann J, Lüder G, Lurz R, Speck C Messer W (2000) Identification of the chromosomal replication origin from Thermus thermophilus and its interaction with the replication initiator DnaA. J Mol Biol 299: 655 665.
93. Siam R Marczynski GT (2000) Cell cycle regulator phosphorylation stimulates two distinct modes of binding at a chromosome replication origin. EMBO J 19: 1138 1147.
94. Smulczyk-Krawczyszyn A, Jakimowicz D, Ruban-Ośmiałowska B, Zawilak-Pawlik A, Majka J, Chater K Zakrzewska-Czerwińska J (2006) Cluster of DnaA boxes involved in the regulation of Streptomyces chromosome replication: from in silico to in vivo studies. J Bacteriol 188: 6184 6194.
95. Speck C Messer W (2001) Mechanism of origin unwinding: sequential binding of DnaA initiator protein to double-stranded and single-stranded DNA in the AT-rich region of the replication origin. EMBO J 20: 1469 1476.
96. Speck C, Chen Z, Li H Stillman B (2005) ATPase-dependent cooperative binding of ORC and Cdc6 to origin DNA. Nat Struct Mol Biol 12: 965 971.
97. Stephens C, Reisenauer A, Wright R Shapiro L (1996) A cell cycle-regulated bacterial DNA methyltransferase is essential for viability. Proc Natl Acad Sci USA 93: 1210 1214.
98. Stephens CM, Zweiger G Shapiro L (1995) Coordinate cell cycle control of a Caulobacter DNA methyltransferase and the flagellar genetic hierarchy. J Bacteriol 177: 1662 1669.
99. Tougu K Marians KJ (1996) The extreme C terminus of primase is required for interaction with DnaB at the replication fork. J Biol Chem 271: 21391 21397.
100. Weigel C, Schmidt A, Ruckert B, Lurz R Messer W (1997) DnaA protein binding to individual DnaA boxes in the Escherichia coli replication origin, oriC. EMBO J 16: 6574 6583.
101. Weigel C, Schmidt A, Seitz H, Tungler D, Welzeck M Messer W (1999) The N-terminus promotes oligomerization of the Escherichia coli initiator protein DnaA. Mol Microbiol 34: 53 66.
102. Wortinger M, Sackett MJ Brun YV (2000) CtrA mediates a DNA replication checkpoint that prevents cell division in Caulobacter crescentus. EMBO J 19: 4503 4512.
103. Wu D, Daugherty SC, Aken SE et al 2006) Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol 6 e188: 1079 1092.
104. Yamamoto K, Muniruzzaman S, Rajagopalan M Madiraju MV (2002) Modulation of Mycobacterium tuberculosis DnaA protein-adenine-nucleotide interactions by acidic phospholipids. Biochem J 363: 305 311.
105. Zakrzewska-Czerwińska J Schrempf H (1992) Characterization of an autonomously replicating region from the Streptomyces lividans chromosome. J Bacteriol 174: 2688 2693.
106. Zawilak-Pawlik A, Kois A, Majka J, Jakimowicz D, Smulczyk-Krawczyszyn A, Messer W Zakrzewska-Czerwinska J (2005) Architecture of bacterial replication initiation complexes: orisomes from four unrelated bacteria. Biochem J 389: 471 481.
107. Zhang W, Allen S, Roberts CJ Soultanas P (2006) The Bacillus subtilis primosomal protein DnaD untwists supercoiled DNA. J Bacteriol 188: 5487 5493.
108. Zhang W, Carneiro MJVM, Turner IJ, Allen S, Roberts CJ Soultanas P (2005) The Bacillus subtilis DnaD and DnaB proteins exhibit different DNA remodeling activities. J Mol Biol 351: 66 75.