Soj/ParA stalls DNA replication by inhibiting helix formation of the initiator protein DnaA

EMBO Journal

Volumn 31, Issue 6, 2012, Pages 1542-1555

  Scholefield, Graham ^a   Errington, Jeff ^a   Murray, Heath ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

AAA +; DnaA; helix; ParA; Soj

Indexed keywords

ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; PROTEIN PARA; PROTEIN SOJ; REPLICATION INITIATOR PROTEIN DNAA; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; DNA BINDING; DNA HELIX; DNA REPLICATION; DNA STRUCTURE; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; REGULATORY MECHANISM;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; BACILLUS SUBTILIS; BACTERIAL PROTEINS; DNA REPLICATION; DNA, BACTERIAL; DNA-BINDING PROTEINS; HYDROLYSIS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; POINT MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; REPLICATION ORIGIN;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS);

EID: 84858794276     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.6     Document Type: Article

References (46)

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. Bowers JL, Randell JC, Chen S, Bell SP (2004) ATP hydrolysis by ORC catalyzes reiterative Mcm2-7 assembly at a defined origin of replication. Mol Cell 16: 967-978 (Pubitemid 40018406)
3. Carr KM, Kaguni JM (2001) Stoichiometry of DnaA and DnaB protein in initiation at the Escherichia coli chromosomal origin. J Biol Chem 276: 44919-44925
4. Cassler MR, Grimwade JE, Leonard AC (1995) Cell cycle-specific changes in nucleoprotein complexes at a chromosomal replication origin. EMBO J 14: 5833-5841
5. Chen LL, Rosa JJ, Turner S, Pepinsky RB (1991) Production of multimeric forms of CD4 through a sugar-based crosslinking strategy. J Biol Chem 266: 18237-18243 (Pubitemid 21908071)
6. 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 (Pubitemid 44175160)
7. Duderstadt KE, Chuang K, Berger JM (2011) DNA stretching by bacterial initiators promotes replication origin opening. Nature 478: 209-213
8. Duderstadt KE, Mott ML, Crisona NJ, Chuang K, Yang H, Berger JM (2010) Origin remodeling and opening in bacteria relies on distinct assembly states of the DnaA initiator. J Biol Chem 285: 28229-28239
9. Erzberger JP, Mott ML, Berger JM (2006) Structural basis for ATPdependent DnaA assembly and replication-origin remodeling. Nat Struct Mol Biol 13: 676-683 (Pubitemid 44175159)
10. 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
11. 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)
12. 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)
13. Funnell BE, Baker TA, Kornberg A (1987) In vitro assembly of a prepriming complex at the origin of the Escherichia coli chromosome. J Biol Chem 262: 10327-10334
14. Gerdes K, Howard M, Szardenings F (2010) Pushing and pulling in prokaryotic DNA segregation. Cell 141: 927-942
15. Gorbatyuk B, Marczynski GT (2005) Regulated degradation of chromosome replication proteins DnaA and CtrA in Caulobacter crescentus. Mol Microbiol 55: 1233-1245 (Pubitemid 40299190)
16. Gruber S, Errington J (2009) Recruitment of condensin to replication origin regions by ParB/SpoOJ promotes chromosome segregation in B. subtilis. Cell 137: 685-696
17. Hassan AK, Moriya S, Ogura M, Tanaka T, Kawamura F, Ogasawara N (1997) Suppression of initiation defects of chromosome replication in Bacillus subtilis dnaA and oriC-deleted mutants by integration of a plasmid replicon into the chromosomes. J Bacteriol 179: 2494-2502 (Pubitemid 27164545)
18. Hester CM, Lutkenhaus J (2007) Soj (ParA) DNA binding is mediated by conserved arginines and is essential for plasmid segregation. Proc Natl Acad Sci USA 104: 20326-20331
19. Ireton K, Gunther NWt, Grossman AD (1994) spo0J is required for normal chromosome segregation as well as the initiation of sporulation in Bacillus subtilis. J Bacteriol 176: 5320-5329
20. Katayama T, Ozaki S, Keyamura K, Fujimitsu K (2010) Regulation of the replication cycle: conserved and diverse regulatory systems for DnaA and oriC. Nat Rev Microbiol 8: 163-170
21. Kawakami H, Katayama T (2010) DnaA, ORC, and Cdc6: similarity beyond the domains of life and diversity. Biochem Cell Biol 88: 49-62
22. Kurokawa K, Nishida S, Emoto A, Sekimizu K, Katayama T (1999) Replication cycle-coordinated change of the adenine nucleotidebound forms of DnaA protein in Escherichia coli. EMBO J 18: 6642-6652
23. 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
24. Leonard AC, Grimwade JE (2005) Building a bacterial orisome: emergence of new regulatory features for replication origin unwinding. Mol Microbiol 55: 978-985 (Pubitemid 40299170)
25. Leonard AC, Grimwade JE (2010) Regulating DnaA complex assembly: it is time to fill the gaps. Curr Opin Microbiol 13: 766-772
26. Leonard TA, Butler PJ, Lowe J (2005) Bacterial chromosome segregation: structure and DNA binding of the Soj dimer-a conserved biological switch. EMBO J 24: 270-282 (Pubitemid 40216132)
27. Livny J, Yamaichi Y, Waldor MK (2007) Distribution of centromerelike parS sites in bacteria: insights from comparative genomics. J Bacteriol 189: 8693-8703 (Pubitemid 350210040)
28. 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: 18479-18484
29. Molt KL, Sutera Jr VA, Moore KK, Lovett ST (2009) A role for nonessential domain II of initiator protein, DnaA, in replication control. Genetics 183: 39-49
30. Mott ML, Berger JM (2007) DNA replication initiation: mechanisms and regulation in bacteria. Nat Rev Microbiol 5: 343-354 (Pubitemid 46605488)
31. Murray H, Errington J (2008) Dynamic control of the DNA replication initiation protein DnaA by Soj/ParA. Cell 135: 74-84
32. Ozaki S, Katayama T (2009) DnaA structure, function, and dynamics in the initiation at the chromosomal origin. Plasmid 62: 71-82
33. Ozaki S, Katayama T (2011) Highly organized DnaA-oriC complexes recruit the single-stranded DNA for replication initiation. Nucleic Acids Res (advance online publication 3 November 2011; doi:10.1093/nar/gkr832)
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. Ptacin JL, Lee SF, Garner EC, Toro E, Eckart M, Comolli LR, Moerner WE, Shapiro L (2010) A spindle-like apparatus guides bacterial chromosome segregation. Nat Cell Biol 12: 791-798
36. Rozgaja TA, Grimwade JE, Iqbal M, Czerwonka C, Vora M, Leonard AC (2011) Two oppositely-oriented arrays of low affinity recognition sites in oriC guide progressive binding of DnaA during E. coli pre-RC assembly. Mol Microbiol 82: 475-488
37. Schepers A, Diffley JF (2001) Mutational analysis of conserved sequence motifs in the budding yeast Cdc6 protein. J Mol Biol 308: 597-608 (Pubitemid 32568464)
38. Scholefield G, Veening JW, Murray H (2010) DnaA and ORC: more than DNA replication initiators. Trends Cell Biol 21: 188-194
39. Scholefield G, Whiting R, Errington J, Murray H (2011) Spo0J regulates the oligomeric state of Soj to trigger its switch from an activator to an inhibitor of DNA replication initiation. Mol Microbiol 79: 1089-1100
40. Simmons LA, Felczak M, Kaguni JM (2003) DnaA Protein of Escherichia coli: oligomerization at the E. coli chromosomal origin is required for initiation and involves specific N-terminal amino acids. Mol Microbiol 49: 849-858 (Pubitemid 36918701)
41. Speck C, Messer W (2001) Mechanism of origin unwinding: sequential binding of DnaA to double-and single-stranded DNA. EMBO J 20: 1469-1476 (Pubitemid 32233986)
42. Sullivan NL, Marquis KA, Rudner DZ (2009) Recruitment of SMC by ParB-parS organizes the origin region and promotes efficient chromosome segregation. Cell 137: 697-707
43. 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: 34255-34262
44. Tucker PA, Sallai L (2007) The AAA+ superfamily-a myriad of motions. Curr Opin Struct Biol 17: 641-652
45. 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)
46. Wigley DB (2009) ORC proteins: marking the start. Curr Opin Struct Biol 19: 72-78