A Structural Basis for the Regulatory Inactivation of DnaA

Journal of Molecular Biology

Volumn 385, Issue 2, 2009, Pages 368-380

  Xu, Qingping ^a   McMullan, Daniel ^b   Abdubek, Polat ^b   Astakhova, Tamara ^c   Carlton, Dennis ^d   Chen, Connie ^b   Chiu, Hsiu Ju ^a   Clayton, Thomas ^d   Das, Debanu ^a   Deller, Marc C ^d   Duan, Lian ^c   Elsliger, Marc Andre ^d   Feuerhelm, Julie ^b   Hale, Joanna ^b   Han, Gye Won ^d   Jaroszewski, Lukasz ^c,e   Jin, Kevin K ^a   Johnson, Hope A ^d   Klock, Heath E ^b   Knuth, Mark W ^b   Kozbial, Piotr ^e   Sri Krishna, S ^c,e   Kumar, Abhinav ^a   Marciano, David ^d   Miller, Mitchell D ^a   Morse, Andrew T ^c   Nigoghossian, Edward ^b   Nopakun, Amanda ^d   Okach, Linda ^b   Oommachen, Silvya ^a   Paulsen, Jessica ^b   Puckett, Christina ^b   Reyes, Ron ^a   Rife, Christopher L ^a   Sefcovic, Natasha ^e   Trame, Christine ^a   van den Bedem, Henry ^a   Weekes, Dana ^e   Hodgson, Keith O ^f   Wooley, John ^c   Deacon, Ashley M ^a   Godzik, Adam ^c,e   Lesley, Scott A ^b,d   Wilson, Ian A ^d   more..

^a SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

^b GENOMICS INSTITUTE OF THE NOVARTIS RESEARCH FOUNDATION   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e BURNHAM INSTITUTE   (United States)

^f SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

Author keywords

AAA+ ATPase; DnaA; Hda; RIDA; Structural Genomics

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; ARGININE; DIMER; DNA A; MONOMER; OLIGOMER;

AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; COMPLEX FORMATION; CRYSTAL STRUCTURE; DIMERIZATION; DNA STRUCTURE; GENE CONTROL; GENE INACTIVATION; HYDROLYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN MOTIF; SEQUENCE HOMOLOGY; SHEWANELLA; SHEWANELLA AMAZONENSIS; SIMULATION;

SHEWANELLA AMAZONENSIS;

EID: 58149100731     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.10.059     Document Type: Article

References (56)

1. Sekimizu K., Bramhill D., and Kornberg A. ATP activates dnaA protein in initiating replication of plasmids bearing the origin of the E. coli chromosome. Cell 50 (1987) 259-265
2. Messer W. The bacterial replication initiator DnaA. DnaA and oriC, the bacterial mode to initiate DNA replication. FEMS Microbiol. Rev. 26 (2002) 355-374
3. Crooke E., Thresher R., Hwang D.S., Griffith J., and Kornberg A. Replicatively active complexes of DnaA protein and the Escherichia coli chromosomal origin observed in the electron microscope. J. Mol. Biol. 233 (1993) 16-24
4. Mott M.L., and Berger J.M. DNA replication initiation: mechanisms and regulation in bacteria. Nat. Rev. Microbiol. 5 (2007) 343-354
5. Kaguni J.M. DnaA: controlling the initiation of bacterial DNA replication and more. Annu. Rev. Microbiol. 60 (2006) 351-375
6. Katayama T., Kubota T., Kurokawa K., Crooke E., and Sekimizu K. The initiator function of DnaA protein is negatively regulated by the sliding clamp of the E. coli chromosomal replicase. Cell 94 (1998) 61-71
7. Katayama T. Feedback controls restrain the initiation of Escherichia coli chromosomal replication. Mol. Microbiol. 41 (2001) 9-17
8. Kurokawa K., Nishida S., Emoto A., Sekimizu K., and Katayama T. Replication cycle-coordinated change of the adenine nucleotide-bound forms of DnaA protein in Escherichia coli. EMBO J. 18 (1999) 6642-6652
9. Kato J., and Katayama T. Hda, a novel DnaA-related protein, regulates the replication cycle in Escherichia coli. EMBO J. 20 (2001) 4253-4262
10. Kim P.D., Banack T., Lerman D.M., Tracy J.C., Camara J.E., Crooke E., et al. Identification of a novel membrane-associated gene product that suppresses toxicity of a TrfA peptide from plasmid RK2 and its relationship to the DnaA host initiation protein. J. Bacteriol. 185 (2003) 1817-1824
11. Su'etsugu M., Takata M., Kubota T., Matsuda Y., and Katayama T. Molecular mechanism of DNA replication-coupled inactivation of the initiator protein in Escherichia coli: interaction of DnaA with the sliding clamp-loaded DNA and the sliding clamp-Hda complex. Genes Cells 9 (2004) 509-522
12. Kawakami H., Su'etsugu M., and Katayama T. An isolated Hda-clamp complex is functional in the regulatory inactivation of DnaA and DNA replication. J. Struct. Biol. 156 (2006) 220-229
13. Su'etsugu M., Shimuta T.R., Ishida T., Kawakami H., and Katayama T. Protein associations in DnaA-ATP hydrolysis mediated by the Hda-replicase clamp complex. J. Biol. Chem. 280 (2005) 6528-6536
14. Camara J.E., Breier A.M., Brendler T., Austin S., Cozzarelli N.R., and Crooke E. Hda inactivation of DnaA is the predominant mechanism preventing hyperinitiation of Escherichia coli DNA replication. EMBO Rep. 6 (2005) 736-741
15. Riber L., Olsson J.A., Jensen R.B., Skovgaard O., Dasgupta S., Marinus M.G., and Lobner-Olesen A. 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 (2006) 2121-2134
16. Camara J.E., Skarstad K., and Crooke E. Controlled initiation of chromosomal replication in Escherichia coli requires functional Hda protein. J. Bacteriol. 185 (2003) 3244-3248
17. Kurz M., Dalrymple B., Wijffels G., and Kongsuwan K. Interaction of the sliding clamp beta-subunit and Hda, a DnaA-related protein. J. Bacteriol. 186 (2004) 3508-3515
18. Kongsuwan K., Josh P., Picault M.J., Wijffels G., and Dalrymple B. The plasmid RK2 replication initiator protein (TrfA) binds to the sliding clamp beta subunit of DNA polymerase III: implication for the toxicity of a peptide derived from the amino-terminal portion of 33-kilodalton TrfA. J. Bacteriol. 188 (2006) 5501-5509
19. Erzberger J.P., Mott M.L., and Berger J.M. Structural basis for ATP-dependent DnaA assembly and replication-origin remodeling. Nat. Struct. Mol. Biol. 13 (2006) 676-683
20. Neuwald A.F., Aravind L., Spouge J.L., and Koonin E.V. AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res. 9 (1999) 27-43
21. Iyer L.M., Leipe D.D., Koonin E.V., and Aravind L. Evolutionary history and higher order classification of AAA+ ATPases. J. Struct. Biol. 146 (2004) 11-31
22. Erzberger J.P., and Berger J.M. Evolutionary relationships and structural mechanisms of AAA+ proteins. Annu. Rev. Biophys. Biomol. Struct. 35 (2006) 93-114
23. Hanson P.I., and Whiteheart S.W. AAA+ proteins: have engine, will work. Nat. Rev. Mol. Cell Biol. 6 (2005) 519-529
24. Tucker P.A., and Sallai L. The AAA+ superfamily-a myriad of motions. Curr. Opin. Struct. Biol. 17 (2007) 641-652
25. Davey M.J., Jeruzalmi D., Kuriyan J., and O'Donnell M. Motors and switches: AAA+ machines within the replisome. Nat. Rev. Mol. Cell Biol. 3 (2002) 826-835
26. Erzberger J.P., Pirruccello M.M., and Berger J.M. The structure of bacterial DnaA: implications for general mechanisms underlying DNA replication initiation. EMBO J. 21 (2002) 4763-4773
27. Ozaki S., Kawakami H., Nakamura K., Fujikawa N., Kagawa W., Park S.Y., et al. A common mechanism for the ATP-DnaA-dependent formation of open complexes at the replication origin. J. Biol. Chem. 283 (2008) 8351-8362
28. Fujikawa N., Kurumizaka H., Nureki O., Terada T., Shirouzu M., Katayama T., and Yokoyama S. Structural basis of replication origin recognition by the DnaA protein. Nucleic Acids Res. 31 (2003) 2077-2086
29. Gaudier M., Schuwirth B.S., Westcott S.L., and Wigley D.B. Structural basis of DNA replication origin recognition by an ORC protein. Science 317 (2007) 1213-1216
30. Dueber E.L., Corn J.E., Bell S.D., and Berger J.M. Replication origin recognition and deformation by a heterodimeric archaeal Orc1 complex. Science 317 (2007) 1210-1213
31. Gao F., and Zhang C.T. DoriC: a database of oriC regions in bacterial genomes. Bioinformatics 23 (2007) 1866-1867
32. Davis I.W., Leaver-Fay A., Chen V.B., Block J.N., Kapral G.J., Wang X., et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35 (2007) W375-W383
33. Jeruzalmi D., Yurieva O., Zhao Y., Young M., Stewart J., Hingorani M., et al. Mechanism of processivity clamp opening by the delta subunit wrench of the clamp loader complex of E. coli DNA polymerase III. Cell 106 (2001) 417-428
34. Lee S.Y., De La Torre A., Yan D., Kustu S., Nixon B.T., and Wemmer D.E. Regulation of the transcriptional activator NtrC1: structural studies of the regulatory and AAA+ ATPase domains. Genes Dev. 17 (2003) 2552-2563
35. Bramhill D., and Kornberg A. Duplex opening by dnaA protein at novel sequences in initiation of replication at the origin of the E. coli chromosome. Cell 52 (1988) 743-755
36. Putnam C.D., Clancy S.B., Tsuruta H., Gonzalez S., Wetmur J.G., and Tainer J.A. Structure and mechanism of the RuvB Holliday junction branch migration motor. J. Mol. Biol. 311 (2001) 297-310
37. Hishida T., Iwasaki H., Yagi T., and Shinagawa H. Role of Walker motif A of RuvB protein in promoting branch migration of Holliday junctions. Walker motif A mutations affect ATP binding, ATP hydrolyzing, and DNA binding activities of RuvB. J. Biol. Chem. 274 (1999) 25335-25342
38. Davey M.J., Fang L., McInerney P., Georgescu R.E., and O'Donnell M. The DnaC helicase loader is a dual ATP/ADP switch protein. EMBO J. 21 (2002) 3148-3159
39. Finn R.D., Mistry J., Schuster-Bockler B., Griffiths-Jones S., Hollich V., Lassmann T., et al. Pfam: clans, web tools and services. Nucleic Acids Res. 34 (2006) D247-D251
40. Wijffels G., Dalrymple B., Kongsuwan K., and Dixon N.E. Conservation of eubacterial replicases. IUBMB Life 57 (2005) 413-419
41. Bunting K.A., Roe S.M., and Pearl L.H. Structural basis for recruitment of translesion DNA polymerase Pol IV/DinB to the beta-clamp. EMBO J. 22 (2003) 5883-5892
42. Dalrymple B.P., Kongsuwan K., Wijffels G., Dixon N.E., and Jennings P.A. A universal protein-protein interaction motif in the eubacterial DNA replication and repair systems. Proc. Natl Acad. Sci. USA 98 (2001) 11627-11632
43. Wijffels G., Dalrymple B.P., Prosselkov P., Kongsuwan K., Epa V.C., Lilley P.E., et al. Inhibition of protein interactions with the beta 2 sliding clamp of Escherichia coli DNA polymerase III by peptides from beta 2-binding proteins. Biochemistry 43 (2004) 5661-5671
44. Boeneman K., and Crooke E. Chromosomal replication and the cell membrane. Curr. Opin. Microbiol. 8 (2005) 143-148
45. Makise M., Mima S., Koterasawa M., Tsuchiya T., and Mizushima T. Biochemical analysis of DnaA protein with mutations in both Arg328 and Lys372. Biochem. J. 362 (2002) 453-458
46. Santarsiero B.D., Yegian D.T., Lee C.C., Spraggon G., Gu J., Scheibe D., et al. An approach to rapid protein crystallization using nanodroplets. J. Appl. Crystallogr. 35 (2002) 278-281
47. Lesley S.A., Kuhn P., Godzik A., Deacon A.M., Mathews I., Kreusch A., et al. Structural genomics of the Thermotoga maritima proteome implemented in a high-throughput structure determination pipeline. Proc. Natl Acad. Sci. USA 99 (2002) 11664-11669
48. Cohen A.E., Ellis P.J., Miller M.D., Deacon A.M., and Phizackerley R.P. An automated system to mount cryo-cooled protein crystals on a synchrotron beamline, using compact sample cassettes and a small-scale robot. J. Appl. Crystallogr. 35 (2002) 720-726
49. Leslie A.G.W. Recent changes to the MOSFLM package for processing film and image plate data. Jnt. CCP4 + ESF-EAMCB Newsl. Protein Crystallogr. 26 (1992)
50. Evans P. Scaling and assessment of data quality. Acta Crystallogr., Sect. D: Biol. Crystallogr. 62 (2006) 72-82
51. CCP4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 (1994) 760-763
52. Schneider T.R., and Sheldrick G.M. Substructure solution with SHELXD. Acta Crystallogr., Sect. D: Biol. Crystallogr. 58 (2002) 1772-1779
53. Vonrhein C., Blanc E., Roversi P., and Bricogne G. Automated structure solution with autoSHARP. Methods Mol. Biol. 364 (2007) 215-230
54. Cohen S.X., Morris R.J., Fernandez F.J., Ben Jelloul M., Kakaris M., Parthasarathy V., et al. Towards complete validated models in the next generation of ARP/wARP. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 2222-2229
55. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr., Sect. D: Biol. Crystallogr. 53 (1997) 240-255
56. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 2126-2132