DNA stretching by bacterial initiators promotes replication origin opening

Nature

Volumn 478, Issue 7368, 2011, Pages 209-213

  Duderstadt, Karl E ^a   Chuang, Kevin ^b   Berger, James M ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; OLIGOMER; RECA PROTEIN; REPLICATION INITIATOR PROTEIN DNAA; SINGLE STRANDED DNA;

BACTERIUM; COMPARATIVE STUDY; CRYSTALLOGRAPHY; DNA; ENZYME ACTIVITY; GENETIC ANALYSIS; HOMOLOGY; MELTING; NUCLEIC ACID; PROTEIN; RECOMBINATION;

AQUIFEX AEOLICUS; ARTICLE; CATALYSIS; CELL ACTIVITY; CONFORMATION; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DNA BINDING; DNA REPLICATION; DNA STRETCHING; DNA STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DNA INTERACTION;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; AT RICH SEQUENCE; BACTERIA; BACTERIAL PROTEINS; BIOCATALYSIS; CRYSTALLOGRAPHY, X-RAY; DNA REPLICATION; DNA, BACTERIAL; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; DNA-DIRECTED DNA POLYMERASE; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MULTIENZYME COMPLEXES; NUCLEIC ACID CONFORMATION; NUCLEIC ACID DENATURATION; REC A RECOMBINASES; REPLICATION ORIGIN; SUBSTRATE SPECIFICITY;

AQUIFEX AEOLICUS; BACTERIA (MICROORGANISMS);

EID: 80054029342     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature10455     Document Type: Article

References (60)

1. Kornberg, A.&Baker, T. A. inDNAReplication (W. H. FreemanandCompany,1992).
2. Stillman, B. Origin recognition and the chromosome cycle. FEBS Lett. 579, 877-884 (2005). (Pubitemid 40361858)
3. Duderstadt, K. E. & Berger, J. M. AAA1ATPases in the initiation of DNAreplication. Crit. Rev. Biochem. Mol. Biol. 43, 163-187 (2008).
4. Lee, D. G. & Bell, S. P. ATPase switches controlling DNA replication initiation. Curr. Opin. Cell Biol. 12, 280-285 (2000). (Pubitemid 30265055)
5. Leipe, D. D., Koonin, E. V.&Aravind, L. Evolution and classification of P-loop kinases and related proteins. J. Mol. Biol. 333, 781-815 (2003). (Pubitemid 37268019)
6. Katayama, T., Ozaki, S., Keyamura, K. & Fujimitsu, K. Regulation of the replication cycle: conserved and diverse regulatory systems for DnaA and oriC. Nature Rev. Microbiol. 8, 163-170 (2010).
7. Kaguni, J. M.DnaA: controlling the initiation of bacterialDNAreplication andmore. Annu. Rev. Microbiol. 60, 351-371 (2006). (Pubitemid 44627953)
8. Leonard, A. C.&Grimwade, J. E.RegulatingDnaAcomplex assembly: it is timeto fill the gaps. Curr. Opin. Microbiol. 13, 766-772 (2010).
9. Fuller, R. S., Funnell, B. E. & Kornberg, A. The dnaA protein complex with the E. coli chromosomal replication origin (oriC) and other DNA sites. Cell 38, 889-900 (1984). (Pubitemid 15176118)
10. Funnell, B. E., Baker, T. A.& Kornberg, A. In vitro assembly of a prepriming complex at the origin of the Escherichia coli chromosome. J. Biol. Chem. 262, 10327-10334 (1987).
11. Crooke, E., Thresher, R., Hwang, D. S., Griffith, J. & Kornberg, A. Replicatively active complexes of DnaA protein and the Escherichia coli chromosomal origin observed in the electron microscope. J. Mol. Biol. 233, 16-24 (1993). (Pubitemid 23288908)
12. Bramhill, D. & Kornberg, A. Duplex opening by dnaA protein at novel sequences in initiation of replication at the origin of the E. coli chromosome. Cell 52, 743-755 (1988).
13. Kowalski, D. & Eddy, M. J. The DNA unwinding element: a novel, cis-acting component that facilitates opening of the Escherichia coli replication origin. EMBO J. 8, 4335-4344 (1989). (Pubitemid 20066878)
14. Erzberger, J. P., Mott, M. L.&Berger, J. M. Structural basis for ATP-dependentDnaA assembly and replication-origin remodeling. Nature Struct. Mol. Biol. 13, 676-683 (2006). (Pubitemid 44175159)
15. Ozaki, S. et al. A common mechanism for the ATP-DnaA-dependent formation of open complexes at the replication origin. J. Biol. Chem. 283, 8351-8362 (2008).
16. Speck, C. & Messer, W. Mechanism of origin unwinding: sequential binding of DnaA to double-and single-stranded DNA. EMBO J. 20, 1469-1476 (2001). (Pubitemid 32233986)
17. Sutton, M. D., Carr, K. M., Vicente, M. & Kaguni, J. M. 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 (1998).
18. Fang, L., Davey, M. J. & O'Donnell, M. Replisome assembly at oriC, the replication origin of E. coli, reveals an explanation for initiation sites outside an origin. Mol. Cell 4, 541-553 (1999). (Pubitemid 29531134)
19. Mott, M. L., Erzberger, J. P., Coons, M. M. & Berger, J. M. Structural synergy and molecular crosstalk between bacterial helicase loaders and replication initiators. Cell 135, 623-634 (2008).
20. Neuwald, A. F., Aravind, L., Spouge, J. L.& Koonin, E. V. AAA1: A class of chaperonelike ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res. 9, 27-43 (1999). (Pubitemid 29095146)
21. Ogura, T. & Wilkinson, A. J. AAA1 superfamily ATPases: common structure-diverse function. Genes Cells 6, 575-597 (2001). (Pubitemid 32747198)
22. Jeruzalmi, D., O'Donnell,M.& Kuriyan, J. Crystal structure of the processivity clamp loader gamma (c) complex of E. coliDNA polymerase III.Cell 106, 429-441(2001). (Pubitemid 32786987)
23. Speck, C., Chen, Z., Li, H. & Stillman, B. ATPase-dependent cooperative binding of ORC and Cdc6 to origin DNA. Nature Struct. Mol. Biol. 12, 965-971 (2005).
24. Clarey, M. G. et al. Nucleotide-dependent conformational changes in the DnaA-like core of the origin recognition complex. Nature Struct. Mol. Biol. 13, 684-690 (2006). (Pubitemid 44175160)
25. Duderstadt, K. E. et al. Origin remodeling and opening in bacteria rely on distinct assembly states of the DnaA initiator. J. Biol. Chem. 285, 28229-28239 (2010).
26. Dueber, E. L., Corn, J. E., Bell, S. D.& Berger, J. M. Replication origin recognition and deformation by a heterodimeric archaeal Orc1 complex. Science317,1210-1213 (2007).
27. Iyer, L. M., Leipe, D. D., Koonin, E. V. & Aravind, L. Evolutionary history and higher order classification of AAA1 ATPases. J. Struct. Biol. 146, 11-31 (2004). (Pubitemid 38369015)
28. Story, R. M., Weber, I. T. & Steitz, T. A. The structure of the E. coli recA protein monomer and polymer. Nature 355, 318-325 (1992).
29. Kowalczykowski, S. C. Initiation of genetic recombination and recombinationdependent replication. Trends Biochem. Sci. 25, 156-165 (2000). (Pubitemid 30195831)
30. Cox, M. M. Motoring along with the bacterial RecA protein.Nature Rev.Mol. Cell Biol. 8, 127-138 (2007). (Pubitemid 46432527)
31. Egelman, E. A common structural core in proteins active in DNA recombination and replication. Trends Biochem. Sci. 25, 179-182 (2000). (Pubitemid 30196949)
32. Conway, A. B. et al. Crystal structure of a Rad51filament.Nature Struct.Mol. Biol.11, 791-796 (2004).
33. Chen, Z., Yang, H. & Pavletich, N. P. Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature 453, 489-494 (2008). (Pubitemid 351733325)
34. Stasiak, A.&DiCapua, E.The helicity ofDNAin complexes with recAprotein.Nature 299, 185-186 (1982).
35. Galletto, R., Amitani, I., Baskin, R. J. & Kowalczykowski, S. C. Direct observation of individual RecA filaments assembling on single DNA molecules. Nature 443, 875-878 (2006). (Pubitemid 44622700)
36. Nishinaka, T., Ito, Y., Yokoyama, S. & Shibata, T. An extended DNA structure through deoxyribose-base stacking induced by RecA protein. Proc. Natl Acad. Sci. USA 94, 6623-6628 (1997). (Pubitemid 27281914)
37. Joo, C. et al. Real-time observation of RecA filament dynamics with single monomer resolution. Cell 126, 515-527 (2006). (Pubitemid 44163610)
38. Bianchi, M., Riboli, B.&Magni, G. E. coli recA protein possesses a strand separating activity on short duplex DNAs. EMBO J. 4, 3025-3030 (1985).
39. Thomsen, N. D. & Berger, J. M. Running in reverse: the structural basis for translocation polarity in hexameric helicases. Cell 139, 523-534 (2009).
40. Enemark, E. J. & Joshua-Tor, L. Mechanism of DNA translocation in a replicative hexameric helicase. Nature 442, 270-275 (2006). (Pubitemid 44114897)
41. Simonetta, K. R. et al. The mechanism of ATP-dependent primer-template recognition by a clamp loader complex. Cell 137, 659-671 (2009).
42. Gaudier, M., Schuwirth, B. S., Westcott, S. L. & Wigley, D. B. Structural basis of DNA replication origin recognition byanORCprotein. Science 317, 1213-1216(2007).
43. Liu, X., Schuck, S. & Stenlund, A. Adjacent residues in the E1 initiator b-hairpin define different roles of the beta-hairpin in Ori melting, helicase loading, and helicase activity. Mol. Cell 25, 825-837 (2007). (Pubitemid 46436527)
44. MacDowell, A. A. et al. Suite of three protein crystallography beamlines with single superconducting bend magnet as the source. J. Synchrotron Radiat. 11, 447-455 (2004). (Pubitemid 40087583)
45. Otwinowski, Z. & Minor, W. in Methods in Enzymology 307-326 (Academic Press, 1997).
46. Adams, P. D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D 58, 1948-1954 (2002). (Pubitemid 35337293)
47. Terwilliger, T. C. Maximum-likelihood density modification. Acta Crystallogr. D 56, 965-972 (2000). (Pubitemid 30622779)
48. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004). (Pubitemid 41742764)
49. Brünger, A. T. et al. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905-921 (1998).
50. DeLano, W. L. The PyMOL Molecular Graphics System (DeLano Scientific, 2002).
51. Ennifar, E., Carpentier, P., Ferrer, J. L., Walter, P. & Dumas, P. X-ray-induced debromination of nucleic acids at the Br K absorption edge and implications for MAD phasing. Acta Crystallogr. D 58, 1262-1268 (2002). (Pubitemid 34877907)
52. Felczak, M. M. & Kaguni, J. M. 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 (2004). (Pubitemid 40017858)
53. Mujumdar, R. B., Ernst, L. A., Mujumdar, S. R., Lewis, C. J.&Waggoner, A. S. Cyanine dye labeling reagents: sulfoindocyanine succinimidyl esters. Bioconjug. Chem. 4, 105-111 (1993).
54. Cantor, C. R. & Schimmel, P. R. in Biophysical Chemistry: Part II: Techniques for the study of biological structure and function 846 (W. H. Freeman and Company, 1980).
55. Magde, D., Wong, R. & Seybold, P. G. Fluorescence quantum yields and their relation to lifetimes of rhodamine 6G and fluorescein in nine solvents: improved absolute standards for quantum yields. Photochem. Photobiol. 75, 327-334 (2002).
56. Lakowicz, J. R. in Principles of Fluorescence Spectroscopy 2nd edn. (Kluwer/Plenum, 1999).
57. Clegg, R. M. Fluorescence resonance energy transfer and nucleic acids. Methods Enzymol. 211, 353-388 (1992).
58. Petsko, G. A. Chemistry and biology. Proc. Natl Acad. Sci. USA 97, 538-540 (2000). (Pubitemid 30070344)
59. Crisona, N. J. & Cozzarelli, N. R. Alteration of Escherichia coli topoisomerase IV conformation upon enzyme binding to positively supercoiled DNA. J. Biol. Chem. 281, 18927-18932 (2006). (Pubitemid 44035395)
60. Weber, K. & Osborn, M. The reliability of molecular weight determinations by dodecyl sulfate-polyacrylamide gel electrophoresis. J. Biol. Chem. 244, 4406-4412 (1969).