Specific genomic sequences of E. coli promote replicational initiation by directly reactivating ADP-DnaA

Genes and Development

Volumn 23, Issue 10, 2009, Pages 1221-1233

  Fujimitsu, Kazuyuki ^a   Senriuchi, Takayuki ^a,b   Katayama, Tsutomu ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b OTSUKA PHARMACEUTICAL CO LTD   (Japan)

Author keywords

DnaA reactivation; Functional DNA sequence; Initiation regulation; Nucleotide exchange; Protein complex; Replication cycle

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; REPLICATION INITIATOR PROTEIN DNAA; ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; DEOXYRIBONUCLEASE; DNA BINDING PROTEIN; DNAA PROTEIN, BACTERIA; DROSOPHILA PROTEIN; ESCHERICHIA COLI PROTEIN; HDA PROTEIN, E COLI; HELICASE; METHYL DIRECTED MISMATCH REPAIR PROTEIN, E COLI; METHYL-DIRECTED MISMATCH REPAIR PROTEIN, E COLI; NUCLEOTIDE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; SPACER DNA; UVRB PROTEIN, E COLI;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BINDING SITE; CONTROLLED STUDY; DATA GENE; DNA REPLICATION; DNA SEQUENCE; DNAA REACTIVATING SEQUENCE 1; DNAA REACTIVATING SEQUENCE 2; ESCHERICHIA COLI; NONHUMAN; ORIC GENE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SEQA GENE; GENE DELETION; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE;

ESCHERICHIA COLI;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASES; BACTERIAL PROTEINS; DNA HELICASES; DNA REPAIR ENZYMES; DNA REPLICATION; DNA, INTERGENIC; DNA-BINDING PROTEINS; DROSOPHILA PROTEINS; ENDODEOXYRIBONUCLEASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENOME, BACTERIAL; NUCLEOTIDES; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE DELETION;

EID: 66149097454     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1775809     Document Type: Article

References (49)

1. Abe Y, Jo T, Matsuda Y, Matsunaga C, Katayama T, Ueda T. 2007. Structure and function of DnaA N-terminal domains: Specific sites and mechanisms in inter-DnaA interaction and in DnaB helicase loading on oriC. J Biol Chem 282: 17816-17827. (Pubitemid 47100271)
2. Blaesing F, Weigel C, Welzeck M, Messer W. 2000. Analysis of the DNA-binding domain of Escherichia coli DnaA protein. Mol Microbiol 36: 557-569. (Pubitemid 30258841)
3. Bochner BR, Ames BN. 1982. Complete analysis of cellular nucleotides by two-dimensional thin layer chromatography. J Biol Chem 257: 9759-9769. (Pubitemid 13205141)
4. Cooper S, Helmstetter CE. 1968. Chromosome replication and the division cycle of Escherichia coli B/r. J Mol Biol 31: 519-540.
5. Crooke E, Castuma CE, Kornberg A. 1992. The chromosome origin of Escherichia coli stabilizes DnaA protein during rejuvenation by phospholipids. J Biol Chem 267: 16779-16782.
6. + machines within the replisome. Nat Rev Mol Cell Biol 3: 826-835.
7. Enemark EJ, Joshua-Tor L. 2006. Mechanism of DNA translocation in a replicative hexameric helicase. Nature 442: 270-275. (Pubitemid 44114897)
8. 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. (Pubitemid 44175159)
9. 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: 51156-51162. (Pubitemid 40017858)
10. 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. (Pubitemid 40934551)
11. Fujikawa N, Kurumizaka H, Nureki O, Terada T, Shirouzu M, Katayama T, Yokoyama S. 2003. Structural basis of replication origin recognition by the DnaA protein. Nucleic Acids Res 31: 2077-2086. (Pubitemid 37442075)
12. Fujimitsu K, Katayama T. 2004. Reactivation of DnaA by DNA sequence-specific nucleotide exchange in vitro. Biochem Biophys Res Commun 322: 411-419. (Pubitemid 39490319)
13. Fujimitsu K, Su'etsugu M, Yamaguchi Y, Mazda K, Fu N, Kawakami H, Katayama T. 2008. Modes of overinitiation, dnaA gene expression, and inhibition of cell division in a novel cold-sensitive hda mutant of Escherichia coli. J Bacteriol 190: 5368-5381.
14. Gai D, Zhao R, Li D, Finkielstein CV, Chen XS. 2004. Mechanisms of conformational change for a replicative hexameric helicase of SV40 large tumor antigen. Cell 119: 47-60. (Pubitemid 39349319)
15. 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. (Pubitemid 43372126)
16. Hansen FG, Koefoed S, Atlung T. 1992. Cloning and nucleotide sequence determination of twelve mutant dnaA genes of Escherichia coli. Mol Gen Genet 234: 14-21.
17. Heacock PN, Dowhan W. 1989. Alteration of the phospholipid composition of Escherichia coli through genetic manipulation. J Biol Chem 264: 14972-14977. (Pubitemid 19237326)
18. Iyer LM, Leipe DD, Koonin EV, Aravind L. 2004. Evolutionary history and higher order classification of AAA+ ATPases. J Struct Biol 146: 11-31. (Pubitemid 38369015)
19. Kaguni JM. 2006. DnaA: Controlling the initiation of bacterial DNA replication and more. Annu Rev Microbiol 60: 351-375.
20. 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. (Pubitemid 28347470)
21. 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)
22. Kato J, Katayama T. 2001. Hda, a novel DnaA-related protein, regulates the replication cycle in Escherichia coli. EMBO J 20: 4253-4262. (Pubitemid 32751841)
23. 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: 27420-27430. (Pubitemid 41040784)
24. + sensor 1 motif. Mol Microbiol 62: 1310-1324.
25. Keyamura K, Fujikawa N, Ishida T, Ozaki S, Su'etsugu M, Fujimitsu K, Kagawa W, Yokoyama S, Kurumizaka H, Katayama T. 2007. The interaction of DiaA and DnaA regulates the replication cycle in E. coli by directly promoting ATP DnaA-specific initiation complexes. Genes & Dev 21: 2083-2099.
26. Kogoma T. 1997. Stable DNA replication: Interplay between DNA replication, homologous recombination, and transcription. Microbiol Mol Biol Rev 61: 212-238. (Pubitemid 27283801)
27. Kurokawa K, Nishida S, Emoto A, Sekimizu K, Katayama T. 1999. Replication cycle-coordinated change of the adenine nucleotide-bound forms of DnaA protein in Escherichia coli. EMBO J 18: 6642-6652.
28. 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 101: 2811-2816. (Pubitemid 38327693)
29. Messer W. 2002. The bacterial replication initiator DnaA. DnaA and oriC, the bacterial mode to initiate DNA replication. FEMS Microbiol Rev 26: 355-374.
30. Messer W, Weigel C. 1997. DnaA initiator - Also a transcription factor. Mol Microbiol 24: 1-6. (Pubitemid 27160833)
31. Neuwald AF, Aravind L, Spouge JL, Koonin EV. 1999. AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 9: 27-43. (Pubitemid 29095146)
32. Nishida S, Fujimitsu K, Sekimizu K, Ohmura T, Ueda T, Katayama T. 2002. A nucleotide switch in the Escherichia coli DnaA protein initiates chromosomal replication: Evidnece from a mutant DnaA protein defective in regulatory ATP hydrolysis in vitro and in vivo. J Biol Chem 277: 14986-14995.
33. Obita T, Iwura T, Su'etsugu M, Yoshida Y, Tanaka Y, Katayama T, Ueda T, Imoto T. 2002. Determination of secondary structure in solution of Escherichia coli DnaA DNA-binding domain. Biochem Biophys Res Commun 299: 42-48.
34. Ozaki S, Kawakami H, Nakamura K, Fujikawa N, Kagawa W, Park SY, Yokoyama S, Kurumizaka H, Katayama T. 2008. A common mechanism for the ATP-DnaA-dependent formation of open complexes at the replication origin. J Biol Chem 283: 8351-8362.
35. Rossman KL, Der CJ, Sondek J. 2005. GEF means go: Turning on RHO GTPases with guanine nucleotide-exchange factors. Nat Rev Mol Cell Biol 6: 167-180. (Pubitemid 40215811)
36. Roth A, Messer W. 1995. The DNA binding domain of the initiator protein DnaA. EMBO J 14: 2106-2111.
37. Schaper S, Messer W. 1995. Interaction of the initiator protein DnaA of Escherichia coli with its DNA target. J Biol Chem 270: 17622-17626.
38. Sekimizu K, Kornberg A. 1988. Cardiolipin activation of dnaA protein, the initiation protein of replication in Escherichia coli. J Biol Chem 263: 7131-7135. (Pubitemid 18155739)
39. 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: 259-265.
40. Shimuta T, Nakano K, Yamaguchi Y, Ozaki S, Fujimitsu K, Matsunaga C, Noguchi K, Emoto A, Katayama T. 2004. Novel heat shock protein HspQ stimulates the degradation of mutant DnaA protein in Escherichia coli. Genes Cells 9: 1151-1166. (Pubitemid 39618530)
41. Skarstad K, Lobner-Olesen A, Atlung T, von Meyenburg K, Boye E. 1989. Initiation of DNA replication in Escherichia coli after overproduction of the DnaA protein. Mol Gen Genet 218: 50-56.
42. Skarstad K, Bernander R, Boye E. 1995. Analysis of DNA replication in vivo by flow cytometry. Methods Enzymol 262: 604-613.
43. Speck C, Weigel C, Messer W. 1999. ATP- and ADP-dnaA protein, a molecular switch in gene regulation. EMBO J 18: 6169-6176. (Pubitemid 29515691)
44. Su'etsugu M, Shimuta T, Ishida T, Kawakami H, Katayama T. 2005. Protein associations in DnaA-ATP hydrolysis mediated by the Hda-replicase clamp complex. J Biol Chem 280: 6528-6536.
45. 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: 36118-36131.
46. Sutton MD, Kaguni JM. 1997. Threonine 435 of Escherichia coli DnaA protein confers sequence-specific DNA binding activity. J Biol Chem 272: 23017-23024. (Pubitemid 27392425)
47. Torheim KN, Boye E, Lobner-Olesen A, Stokke T, Skarstad K. 2000. The Escherichia coli SeqA protein destabilizes mutant DnaA204 protein. Mol Microbiol 37: 629-638. (Pubitemid 30611843)
48. 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)
49. Xia W, Dowhan W. 1995. In vivo evidence for the involvement of anionic phospholipids in initiation of DNA replication in Escherichia coli. Proc Natl Acad Sci 92: 783-787.