The interaction of DiaA and DnaA regulates the replication cycle in E. coli by directly promoting ATP-DnaA-specific initiation complexes

Genes and Development

Volumn 21, Issue 16, 2007, Pages 2083-2099

  Keyamura, Kenji ^a   Fujikawa, Norie ^b   Ishida, Takuma ^a   Ozaki, Shogo ^a   Su'etsugu, Masayuki ^a   Fujimitsu, Kazuyuki ^a   Kagawa, Wataru ^b   Yokoyama, Shigeyuki ^b,c   Kurumizaka, Hitoshi ^b,d   Katayama, Tsutomu ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b RIKEN YOKOHAMA INSTITUTE   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d WASEDA UNIVERSITY   (Japan)

Author keywords

Cell cycle regulation; Complex structure; DNA dynamics; Initiation of replication; Initiator regulation; Protein complex

Indexed keywords

ADENOSINE TRIPHOSPHATE; BINDING PROTEIN; DOUBLE STRANDED DNA; PROTEIN DIAA; REPLICATION INITIATOR PROTEIN DNAA; SUGAR PHOSPHATE; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CELL CYCLE; CELL CYCLE REGULATION; CHROMOSOME REPLICATION; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA DENATURATION; DNA REPLICATION; DNA REPLICATION ORIGIN; ESCHERICHIA COLI; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; BASE SEQUENCE; CARRIER PROTEINS; CELL CYCLE; DNA REPLICATION; DNA, BACTERIAL; DNA-BINDING PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MACROMOLECULAR SUBSTANCES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; ORIGIN RECOGNITION COMPLEX; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION FACTORS, GENERAL;

ESCHERICHIA COLI;

EID: 34547941118     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1561207     Document Type: Article

References (37)

1. Abe, Y., Jo, T., Matsuda, Y., Matsunaga, C., Katayama, T., and 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.
2. Arunkumar, A.I., Stauffer, M.E., Bochkareva, E., Bochkarev, A., and Chazin, W.J. 2003. Independent and coordinated functions of replication protein A tandem high-affinity single-stranded DNA binding domains. J. Biol. Chem. 278: 41077-41082.
3. Bateman, A. 1999. The SIS domain; a phosphosugar-binding domain. Trends Biochem. Sci. 24: 94-95.
4. Bleasing, F., Weigel, C., Welzeck, M., and Messer, W. 2000. Analysis of the DNA-binding domain of Escherichia coli DnaA protein. Mol. Microbiol. 36: 557-569.
5. Botchan, M. 2007. A switch for S phase. Nature 445: 272-274.
6. Brooke, J.S. and Valvano, M.A. 1996. Molecular cloning of the Haemophilus influenzae gmhA (lcpA) gene encoding a phosphoheptose isomerase required for lipooligosaccharide biosynthesis. J. Bacteriol. 178: 3339-3341.
7. Burz, D.S., Beckett, D., Benson, N., and Ackers, G.K. 1994. Self-assembly of bacteriophage λ cI repressor: Effects of single-site mutations on the monomer-dimer equilibrium. Biochemistry 33: 8399-8405.
8. Erzberger, J.P., Pirruccello, M.M., and Berger, J.M. 2002. The structure of bacterial DnaA: Implications for general mechanisms underlying DNA replication initiation. EMBO J. 21: 4763-4773.
9. Erzberger, J.P., Mott, M.L., and Berger, J.M. 2006. Structural basis for ATP-dependent DnaA assembly and replication-origin remodeling. Nat. Struct. Mol. Biol. 13: 676-683.
10. Fujikawa, N., Kurumizaka, H., Nureki, O., Terada, T., Shirouzu, M., Katayama, T., and Yokoyama, S. 2003. Structural basis of replication origin recognition by the DnaA protein. Nucleic Acids Res. 31: 2077-2086.
11. Guo, L., Katayama, T., Seyama, Y., Sekimizu, K., and Miki, T. 1999. Isolation and characterization of novel cold-sensitive dnaA mutants of Escherichia coli. FEMS Microbiol. Lett. 176: 357-366.
12. Hanson, C.J., Bootman, M.D., and Roderick, H.L. 2004. Cell signalling: IP3 receptors channel calcium into cell death. Curr. Biol. 14: R933-R935.
13. Ishida, T., Akimitsu, N., Kashioka, T., Hatano, M., Kubota, T., Ogata, Y., Sekimizu, K., and Katayama, T. 2004. DiaA, a novel DnaA-binding protein, ensures the timely initiation of Escherichia coli chromosome replication. J. Biol. Chem. 279: 45546-45555.
14. Kaguni, J.M. 2006. DnaA: Controlling the initiation of bacterial DNA replication and more. Annu. Rev. Microbiol. 60: 351-375.
15. Katayama, T. and Crooke, E. 1995. DnaA protein is sensitive to a soluble factor and is specifically inactivated for initiation of in vitro replication of the Escherichia coli minichromosome. J. Biol. Chem. 270: 9265-9271.
16. Katayama, T., Kubota, T., Kurokawa, K., Crooke, E., and 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.
17. Kato, J. and Katayama, T. 2001. Hda, a novel DnaA-related protein, regulates the replication cycle in Escherichia coli. EMBO J. 20: 4253-4262.
18. Kawakami, H., Keyamura, K., and 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.
19. Kawakami, H., Ozaki, S., Suzuki, S., Nakamura, K., Senriuchi, T., Su'etsugu, M., Fujimitsu, K., and Katayama, T. 2006. The exceptionally tight affinity of DnaA for ATP/ADP requires a unique aspartic acid residue in the AAA+ sensor 1 motif. Mol. Microbiol. 62: 1310-1324.
20. Kim, Y.K., Lee, K.J., Jeon, H., and Yu, Y.G. 2006. Protein kinase CK2 is inhibited by human nucleolar phosphoprotein p140 in an inositol hexakisphosphate-dependent manner. J. Biol. Chem. 281: 36752-36757.
21. Kurokawa, K., Nishida, S., Emoto, A., Sekimizu, K., and Katayama, T. 1999. Replication cycle-coordinated change of the adenine nucleotide-bound forms of DnaA protein in Escherichia coli. EMBO J. 18: 6642-6652.
22. Margulies, C. and Kaguni, J.M. 1996. Ordered and sequential binding of DnaA protein to oriC, the chromosomal origin of Escherichia coli. J. Biol. Chem. 271: 17035-17040.
23. McGarry, K.C., Ryan, V.T., Grimwade, J.E., and Leonard, A.C. 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.
24. Messer, W. 2002. The bacterial replication initiator DnaA. DnaA and oriC, the bacterial mode to initiate DNA replication. FEMS Microbiol. Rev. 26: 355-374.
25. Nishida, S., Fujimitsu, K., Sekimizu, K., Ohmura, T., Ueda, T., and Katayama, T. 2002. A nucleotide switch in the Escherichia coli DnaA protein initiates chromosomal replication: Evidence from a mutant DnaA protein defective in regulatory ATP hydrolysis in vitro and in vivo. J. Biol. Chem. 277: 14986-14995.
26. Nordström, K. 2006. Plasmid R1-replication and its control. Plasmid 55: 1-26.
27. O'Donnell, M. 2006. Replisome architecture and dynamics in Escherichia coli. J. Biol. Chem. 281: 10653-10656.
28. Ozaki, S., Fujimitsu, K., Kurumizaka, H., and 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.
29. Slater, S., Wold, S., Lu, M., Boye, E., Skarstad, K., and 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: 927-936.
30. Speck, C. and Messer, W. 2001. Mechanism of origin unwinding: Sequential binding of DnaA to double- and single-stranded DNA. EMBO J. 20: 1469-1476.
31. Stauffer, M.E. and Chazin, W.J. 2004. Structural mechanisms of DNA replication, repair, and recombination. J. Biol. Chem. 279: 30915-30918.
32. Stillman, B. 2005. Origin recognition and the chromosome cycle. FEBS Lett. 579: 877-884.
33. Sutton, M.D. and Kaguni, J.M. 1997. Threonine 435 of Escherichia coli DnaA protein confers sequence-specific DNA binding activity. J. Biol. Chem. 272: 23017-23024.
34. Tan, L. and Darby, C. 2006. Yersinia pestis YrbH is a multifunctional protein required for both 3-deoxy-D-manno-oct-2-ulosonic acid biosynthesis and biofilm formation. Mol. Microbiol. 61: 861-870.
35. Weigel, C., Schmidt, A., Rückert, B., Lurz, R., and Messer, W. 1997. DnaA protein binding to individual DnaA boxes in the Escherichia coli replication origin, oriC. EMBO J. 16: 6574-6583.
36. Zhou, H.X. 2001. Single-chain versus dimeric protein folding: Thermodynamic and kinetic consequences of covalent linkage. J. Am. Chem. Soc. 123: 6730-6731.
37. Zyskind, J.W. and Smith, D.W. 1992. DNA replication, the bacterial cell cycle, and cell growth. Cell 69: 5-8.