Regulation of DnaA assembly and activity: Taking directions from the genome

Annual Review of Microbiology

Volumn 65, Issue , 2011, Pages 19-35

  Leonard, Alan C ^a   Grimwade, Julia E ^a  

^a Florida Institute of Technology   (United States)

Author keywords

Cell cycle; Chromosome replication; Initiator protein; oriC; Pre replicative complex

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; REPLICATION INITIATOR PROTEIN DNAA;

ACCURACY; BACILLUS SUBTILIS; BACTERIAL GENE; BACTERIAL GENOME; BINDING SITE; CELL CYCLE; CELL GROWTH; CHROMOSOME DUPLICATION; DNA REPLICATION; ESCHERICHIA COLI; EUKARYOTE; MOLECULAR RECOGNITION; NONHUMAN; ORIC GENE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW;

BACTERIA; BACTERIAL PROTEINS; DNA REPLICATION; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; REPLICATION ORIGIN;

EID: 80053266375     PISSN: 00664227     EISSN: 15453251     Source Type: Book Series    
DOI: 10.1146/annurev-micro-090110-102934     Document Type: Review

References (98)

1. Abe Y, Jo T, Matsuda Y, Matsunaga C, Katayama T, Ueda T. 2007. Structure and function of DnaA Nterminal domains: specific sites and mechanisms in inter-DnaA interaction and in DnaB helicase loading on oriC. J. Biol. Chem. 282:17816-27 (Pubitemid 47100271)
2. Atlung T, Clausen ES, Hansen FG. 1985. Autoregulation of the dnaA gene of Escherichia coli K12. Mol. Gen. Genet. 200:442-50 (Pubitemid 15024889)
3. Atlung T, L'ner-Olesen A, Hansen FG. 1987. Overproduction of DnaA protein stimulates initiation. Mol. Gen. Genet. 206:51-59
4. Baker TA, Kornberg A. 1988. Transcriptional activation of initiation of replication from the E. coli chromosomal origin: an RNA-DNA hybrid near oriC. Cell 55:113-23
5. Ball CA, Osuna R, Ferguson KC, Johnson RC. 1992. Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli. J. Bacteriol. 174:8043-56 (Pubitemid 23002939)
6. Boeneman K, Crooke E. 2005. Chromosomal replication and the cell membrane. Curr. Opin. Microbiol. 8:143-48 (Pubitemid 40417954)
7. Boeneman K, Fossum S, Yang Y, Fingland N, Skarstad K, Crooke E. 2009. Escherichia coli DnaA forms helical structures along the longitudinal cell axis distinct from MreB filaments. Mol. Microbiol. 72:645-57
8. Bramhill D, Kornberg A. 1988. Duplex opening by DnaA protein at novel sequences in initiation of replication at the origin of the E. coli chromosome. Cell 52:743-55
9. 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 Rep. 6:736-41 (Pubitemid 43108695)
10. Campbell JL, Kleckner N. 1990. E. coli oriC and the DnaA gene promoter are sequestered from DAM methyltransferase following the passage of the chromosomal replication fork. Cell 62:967-79
11. Cassler MR, Grimwade JE, Leonard AC. 1995. Cell cycle-specific changes in nucleoprotein complexes at a chromosomal replication origin. EMBO J. 14:5833-41
12. Chen Z, Speck C,Wendel P, Tang C, Stillman B, Li H. 2008. The architecture of the DNA replication origin recognition complex in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 105:10326-31
13. Cho E, Ogasawara N, Ishikawa S. 2008. The functional analysis of YabA, which interacts with DnaA and regulates initiation of chromosome replication in Bacillus subtilis. Genes Genet. Syst. 83:111-25 (Pubitemid 351872856)
14. Chodavarapu S, Felczak MM, Yaniv JR, Kaguni JM. 2008. Escherichia coli DnaA interacts with HU in initiation at the E. coli replication origin. Mol. Microbiol. 67:781-92 (Pubitemid 351143691)
15. Chodavarapu S, Gomez R, VicenteM, Kaguni JM. 2008. Escherichia coli Dps interacts with DnaA protein to impede initiation: a model of adaptive mutation. Mol. Microbiol. 67:1331-46 (Pubitemid 351316958)
16. Cooper S, Helmstetter CE. 1968. Chromosome replication and the division cycle of Escherichia coli. Br. J. Mol. Biol. 31:519-40
17. Costa S, Blow JJ. 2007. The elusive determinants of replication origins. EMBO Rep. 8:332-34 (Pubitemid 46511032)
18. Crooke E, Thresher R, Hwang DS, Griffith J, Kornberg A. 1993. Replicatively active complexes of DnaA protein and the Escherichia coli chromosomal origin observed in the electron microscope. J. Mol. Biol. 233:16-24 (Pubitemid 23288908)
19. Da-Silva LF, Duncker BP. 2007. ORC function in late G1: maintaining the license for DNA replication. Cell Cycle 6:128-30 (Pubitemid 46232488)
20. Diffley JF. 2004. Regulation of early events in chromosome replication. Curr. Biol. 14:R778-86 (Pubitemid 39239353)
21. Duderstadt KE, Mott ML, Crisona NJ, Chuang K, Yang H, Berger JM. 2010. Origin remodeling and opening in bacteria rely on distinct assembly states of the DnaA initiator. J. Biol. Chem. 285:28229-39
22. Erzberger JP, Mott ML, Berger JM. 2006. Structural basis for ATP-dependent DnaA assembly and replication-origin remodeling. Nat. Struct. Mol. Biol. 13:676-83 (Pubitemid 44175159)
23. Erzberger JP, Pirruccello MM, Berger JM. 2002. The structure of bacterial DnaA: implications for general mechanisms underlying DNA replication initiation. EMBO J. 21:4763-73
24. Felczak MM, Kaguni JM. 2004. The box VII motif of Escherichia coli DnaA protein is required for DnaA oligomerization at the E. coli replication origin. J. Biol. Chem. 279:51156-62 (Pubitemid 40017858)
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. 280:24627-33 (Pubitemid 40934551)
26. Finkel SE, Johnson RC. 1992. The Fis protein: It's not just for DNA inversion anymore. Mol. Microbiol. 6:3257-65
27. Flátten I,Morigen Skarstad K. 2009. DnaA protein interacts with RNA polymerase and partially protects it from the effect of rifampicin. Mol. Microbiol. 71:1018-30
28. Fujikawa N, KurumizakaH,NurekiO,TeradaT, ShirouzuM,KatayamaT,Yokoyama S. 2003. Structural basis of replication origin recognition by the DnaA protein. Nucleic Acids Res. 31:2077-86 (Pubitemid 37442075)
29. Fujimitsu K, Senriuchi T, Katayama T. 2009. Specific genomic sequences of E. coli promote replicational initiation by directly reactivating ADP-DnaA. Genes Dev. 23:1221-33
30. Fuller RS, Funnell BE, Kornberg A. 1984. The DnaA protein complex with the E. coli chromosomal replication origin (oriC) and other DNA sites. Cell 38:889-90
31. Garner J, Crooke E. 1996. Membrane regulation of the chromosomal replication activity of E. coli DnaA requires a discrete site on the protein. EMBO J. 15:3477-85 (Pubitemid 26231955)
32. Garner J, Durrer P, Kitchen J, Brunner J, Crooke E. 1998. Membrane-mediated release of nucleotide from an initiator of chromosomal replication, Escherichia coli DnaA, occurs with insertion of a distinct region of the protein into the lipid bilayer. J. Biol. Chem. 273:5167-73 (Pubitemid 28108678)
33. Gille H, Egan JB, Roth A, MesserW. 1991. The FIS protein binds and bends the origin of chromosomal DNA replication, oriC, of Escherichia coli. Nucleic Acids Res. 19:4167-72 (Pubitemid 21912789)
34. Goranov AI, Breier AM,Merrikh H, Grossman AD. 2009. YabA of Bacillus subtilis controls DnaA-mediated replication initiation but not the transcriptional response to replication stress. Mol. Microbiol. 74:454-66
35. Grimwade JE, Torgue JJ, McGarry KC, Rozgaja T, Enloe ST, Leonard AC. 2007. Mutational analysis reveals Escherichia coli oriC interacts with both DnaA-ATP and DnaA-ADP during pre-RC assembly. Mol. Microbiol. 66:428-39 (Pubitemid 47482384)
36. Hansen FG, Atlung T, Braun RE, Wright A, Hughes P, Kohiyama M. 1991. Initiator (DnaA) protein concentration as a function of growth rate in Escherichia coli and Salmonella typhimurium. J. Bacteriol. 173:5194-99
37. Hansen FG, Christensen BB, Atlung T. 1991. The initiator titration model: computer simulation of chromosome and minichromosome control. Res. Microbiol. 142:161-67
38. Hansen FG, Christensen BB, Atlung T. 2007. Sequence characteristics required for cooperative binding and efficient in vivo titration of the replication initiator protein DnaA in E. coli. J. Mol. Biol. 367:942-52 (Pubitemid 46386076)
39. Hansen FG, Koefoed S, Sorensen L, Atlung T. 1987. Titration of DnaA protein by oriC DnaA-boxes increases DnaA gene expression in Escherichia coli. EMBO J. 6:255-58
40. IshidaT, AkimitsuN,KashiokaT,HatanoM,KubotaT, et al. 2004. DiaA, a novel DnaA-binding protein, ensures the timely initiation of Escherichia coli chromosome replication. J. Biol. Chem. 279:45546-55 (Pubitemid 39491541)
41. Jacob F, Brenner S, Cuzin F. 1963. On the regulation of DNA replication in bacteria. Cold Spring Harbor Symp. Quant. Biol. 28:329-48
42. Kaguni JM. 2006. DnaA: controlling the initiation of bacterial DNA replication and more. Annu. Rev. Microbiol. 60:351-71 (Pubitemid 44627953)
43. Katayama T, Fujimitsu K, Ogawa T. 2001. Multiple pathways regulating DnaA function in Escherichia coli: distinct roles for DnaA titration by the datA locus and the regulatory inactivation of DnaA. Biochimie 83:13-17 (Pubitemid 32181518)
44. Katayama T, Sekimizu K. 1999. Inactivation of Escherichia coli DnaA protein by DNA polymerase III and negative regulations for initiation of chromosomal replication. Biochimie. 81:835-40 (Pubitemid 29520609)
45. Kato J, Katayama T. 2001. Hda, a novel DnaA-related protein, regulates the replication cycle in Escherichia coli. EMBO J. 20:4253-62 (Pubitemid 32751841)
46. Kawakami H, Keyamura K, Katayama T. 2005. Formation of an ATP-DnaA-specific initiation complex requires DnaA arginine 285, a conserved motif in the AAA + protein family. J. Biol. Chem. 280:27420-30 (Pubitemid 41040784)
47. Kawakami H, Su'etsugu M, Katayama T. 2006. An isolated Hda-clamp complex is functional in the regulatory inactivation of DnaA and DNA replication. J. Struct. Biol. 156:220-29 (Pubitemid 44486055)
48. Keyamura K, Abe Y, Higashi M, Ueda T, Katayama T. 2009. DiaA dynamics are coupled with changes in initial origin complexes leading to helicase loading. J. Biol. Chem. 284:25038-50
49. Kimura M, Miki T, Hiraga S, Nagata T, Yura T. 1979. Conditionally lethal amber mutations in the dnaA region of the Escherichia coli chromosome that affect chromosome duplication. J. Bacteriol. 140:825-34 (Pubitemid 10184855)
50. Kitagawa R, Mitsuki H, Okazaki T, Ogawa T. 1996. A novel DnaA protein-binding site at 94.7 min on the Escherichia coli chromosome. Mol. Microbiol. 19:1137-47
51. 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. 12:3032-43 (Pubitemid 28469305)
52. Kowalski D, Eddy MJ. 1989. The DNA unwinding element: a novel, cis-acting component that facilitates opening of the Escherichia coli replication origin. EMBO J. 8:4335-44 (Pubitemid 20066878)
53. Leonard AC, Grimwade JE. 2005. Building a bacterial orisome: emergence of new regulatory features for replication origin unwinding. Mol. Microbiol. 55:978-85 (Pubitemid 40299170)
54. Leonard AC, Grimwade JE. 2010. Chapter 4.4.1 Initiation of DNA replication. In EcoSal-Escherichia coli and Salmonella: Cellular and Molecular Biology, ed. A Bock, RCurtiss III, JB Kaper,PDKarp, FCNeidhardt, et al. Washington, DC: ASM
55. Leonard AC, Grimwade JE. 2010. Regulating DnaA complex assembly: It is time to fill the gaps. Curr. Opin. Microbiol. 13:766-72
56. Loner-Olesen A, Hansen FG, Rasmussen KV, Martin B, Kuempel PL. 1994. The initiation cascade for chromosome replication in wild-type and Dam methyltransferase deficient Escherichia coli cells. EMBO J. 13:1856-62 (Pubitemid 24124518)
57. Loner-Olesen A, Skarstad K, Hansen FG, von Meyenburg K, Boye E. 1989. The DnaA protein determines the initiation mass of Escherichia coli K-12. Cell. 57:881-89 (Pubitemid 19149826)
58. Loner-Olesen A, Skovgaard O, Marinus MG. 2005. Dam methylation: coordinating cellular processes. Curr. Opin. Microbiol. 8:154-60 (Pubitemid 40417956)
59. Madiraju MV, Moomey M, Neuenschwander PF, Muniruzzaman S, Yamamoto K, et al. 2006. The intrinsic ATPase activity of Mycobacterium tuberculosis DnaA promotes rapid oligomerization of DnaA on oriC. Mol. Microbiol. 59:1876-90
60. MarguliesC,Kaguni JM. 1996. Ordered and sequential binding ofDnaA protein to oriC, the chromosomal origin of Escherichia coli. J. Biol. Chem. 271:17035-40
61. Matsui M, OkaA,TakanamiM,Yasuda S, Hirota Y. 1985. Sites of DnaA protein-binding in the replication origin of the Escherichia coli K-12 chromosome. J. Mol. Biol. 184:529-33
62. McGarry KC, Ryan VT,Grimwade JE, Leonard AC. 2004. Two discriminatory binding sites in the Escherichia coli replication origin are required for DNA strand opening by initiator DnaA-ATP. Proc. Natl. Acad. Sci. USA 101:2811-16 (Pubitemid 38327693)
63. Miller DT, Grimwade JE, Betteridge T, Rozgaja T, Torgue JJ, Leonard AC. 2009. Bacterial origin recognition complexes direct assembly of higher-order DnaA oligomeric structures. Proc. Natl. Acad. Sci. USA 106:18479-84
64. Molt KL, Sutera VA, Moore KK, Lovett ST. 2009. A role for nonessential domain II of initiator protein, DnaA, in replication control. Genetics 183:39-49
65. Morigen Boye E, Skarstad K, Loner-Olesen A. 2001. Regulation of chromosomal replication by DnaA protein availability in Escherichia coli: effects of the datA region. Biochim. Biophys. Acta 1521:73-80 (Pubitemid 33020768)
66. Mott ML, Berger JM. 2007. DNA replication initiation: mechanisms and regulation in bacteria. Nat. Rev. Microbiol. 5:343-54 (Pubitemid 46605488)
67. Mott ML, Erzberger JP, Coons MM, Berger JM. 2008. Structural synergy and molecular crosstalk between bacterial helicase loaders and replication initiators. Cell. 135:623-34
68. Nakamura K, Katayama T. 2010. Novel essential residues of Hda for interaction with DnaA in the regulatory inactivation ofDnaA: unique roles for Hda AAA Box VI and VIImotifs. Mol. Microbiol. 76:302-17
69. Nievera C, Torgue JJ, Grimwade JE, Leonard AC. 2006. SeqA blocking of DnaA-oriC interactions ensures staged assembly of the E. coli pre-RC. Mol. Cell 24:581-92 (Pubitemid 44750768)
70. Nozaki S, Yamada Y, Ogawa T. 2009. Initiator titration complex formed at datA with the aid of IHF regulates replication timing in Escherichia coli. Genes Cells 14:329-41
71. Ogden GB, Pratt MJ, Schaechter M. 1988. The replicative origin of the E. coli chromosome binds to cell membranes only when hemimethylated. Cell 54:127-35
72. Oka A, Sugimoto K, Sasaki H, Takanami M. 1982. An in vitro method generating base substitutions in preselected regions of plasmid DNA: application to structural analysis of the replication origin of the Escherichia coli K-12 chromosome. Gene 19:59-69 (Pubitemid 13235742)
73. Pierucci O, Helmstetter CE, RickertM,WeinbergerM, Leonard AC. 1987. Overexpression of the dnaA gene in Escherichia coli B/r: chromosome and minichromosome replication in the presence of rifampin. J. Bacteriol. 169:1871-77 (Pubitemid 17081738)
74. Riber L, Fujimitsu K, Katayama T, Loner-Olesen A. 2009. Loss of Hda activity stimulates replication initiation from I-box, but not R4 mutant origins in Escherichia coli. Mol. Microbiol. 71:107-22
75. Riber L, Olsson JA, Jensen RB, Skovgaard O, Dasgupta S, et al. 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. 20:2121-34 (Pubitemid 44157462)
76. Rice PA. 1997. Making DNA do a U-turn: IHF and related proteins. Curr. Opin. Struct. Biol. 7:86-93 (Pubitemid 27092383)
77. Roth A, MesserW. 1998. High-affinity binding sites for the initiator protein DnaA on the chromosome of Escherichia coli. Mol. Microbiol. 28:395-401 (Pubitemid 28182261)
78. Roth A, Urmoneit B, Messer W. 1994. Functions of histone-like proteins in the initiation of DNA replication at oriC of Escherichia coli. Biochimie 76:917-23
79. 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. 51:1347-59 (Pubitemid 38338897)
80. Samitt CE, Hansen FG, Miller JF, Schaechter M. 1989. In vivo studies of DnaA binding to the origin of replication of Escherichia coli. EMBO J. 8:989-93 (Pubitemid 19273267)
81. Schaper S, Messer W. 1995. Interaction of the initiator protein DnaA of Escherichia coli with its DNA target. J. Biol. Chem. 270:17622-26
82. Sclafani RA, Holzen TM. 2007. Cell cycle regulation of DNA replication. Annu. Rev. Genet. 41:237-80
83. Sekimizu K, Bramhill D, Kornberg A. 1987. ATP activates DnaA protein in initiating replication of plasmids bearing the origin of the E. coli chromosome. Cell 50:259-65
84. Sekimizu K, Yung BY, Kornberg A. 1988. The DnaA protein of Escherichia coli. Abundance, improved purification, and membrane binding. J. Biol. Chem. 263:7136-40
85. Skarstad K, Baker TA, Kornberg A. 1990. Strand separation required for initiation of replication at the chromosomal origin of E. coli is facilitated by a distant RNA-DNA hybrid. EMBO J. 9:2341-48
86. Skarstad K, Boye E, Steen HB. 1986. Timing of initiation of chromosome replication in individual Escherichia coli cells. EMBO J. 5:1711-17
87. Slater S, Wold S, Lu M, Boye E, Skarstad K, Kleckner N. 1995. E. coli SeqA protein binds oriC in two different methyl-modulated reactions appropriate to its roles in DNA replication initiation and origin sequestration. Cell 82:927-36
88. Smits WK, Merrikh H, Bonilla CY, Grossman AD. 2011. Primosomal proteins DnaD and DnaB are recruited to chromosomal regions bound by DnaA in Bacillus subtilis. J. Bacteriol. 193:640-48
89. SoufoCD, SoufoHJ, Noirot-GrosMF, SteindorfA,NoirotP,GraumannPL. 2008. Cell-cycle-dependent spatial sequestration of the DnaA replication initiator protein in Bacillus subtilis. Dev. Cell 15:935-41
90. Speck C, MesserW. 2001. Mechanism of origin unwinding: sequential binding of DnaA to double- and single-stranded DNA. EMBO J. 20:1469-76 (Pubitemid 32233986)
91. Stepankiw N, Kaidow A, Boye E, Bates D. 2009. The right half of the Escherichia coli replication origin is not essential for viability, but facilitates multi-forked replication. Mol. Microbiol. 74:467-79
92. Su'etsugu M, Nakamura K, Keyamura K, Kudo Y, Katayama T. 2008. Hda monomerization by ADP binding promotes replicase clamp-mediated DnaA-ATP hydrolysis. J. Biol. Chem. 283:36118-31
93. Sutton MD, Carr KM, Vicente M, Kaguni JM. 1998. Escherichia coli DnaA protein. The N-terminal domain and loading of DnaB helicase at the E. coli chromosomal origin. J. Biol. Chem. 273:34255-62
94. Tabata S, Oka A, Sugimoto K, Takanami M, Yasuda S, Hirota Y. 1983. The 245 base-pair oriC sequence of the E. coli chromosome directs bidirectional replication at an adjacent region. Nucleic Acids Res. 11:2617-26
95. 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 (Pubitemid 29460485)
96. Yung BY, Crooke E, Kornberg A. 1990. Fate of the DnaA initiator protein in replication at the origin of the Escherichia coli chromosome in vitro. J. Biol. Chem. 265:1282-85
97. Zawilak-Pawlik A, Kois A, Majka J, Jakimowicz D, Smulczyk-Krawczyszyn A, et al. 2005. Architecture of bacterial replication initiation complexes: orisomes from four unrelated bacteria. Biochem. J. 389:471-81 (Pubitemid 41021151)
98. Zyskind JW, Cleary JM, BrusilowWS, Harding NE, Smith DW. 1983. Chromosomal replication origin from the marine bacterium Vibrio harveyi functions in Escherichia coli: oriC consensus sequence. Proc. Natl. Acad. Sci. USA 80:1164-68 (Pubitemid 13082776)