Mechanism of polymerase collision release from sliding clamps on the lagging strand

EMBO Journal

Volumn 28, Issue 19, 2009, Pages 2981-2991

  Georgescu, Roxana E ^a   Kurth, Isabel ^a   Yao, Nina Y ^a   Stewart, Jelena ^a   Yurieva, Olga ^a   O'Donnell, Mike ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Lagging strand; Okazaki fragment; Replication fork; Replisome; Sliding clamp

Indexed keywords

DNA BINDING PROTEIN; DNA DIRECTED DNA POLYMERASE GAMMA; ESCHERICHIA COLI PROTEIN; OKAZAKI FRAGMENT; PROTEIN SUBUNIT; REPLISOME; SINGLE STRANDED DNA; SINGLE STRANDED DNA BINDING PROTEIN;

ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; DNA BINDING; DNA CONFORMATION; DNA REPLICATION; DNA STRAND; DNA TEMPLATE; ENZYME BINDING; ENZYME MECHANISM; ENZYME RELEASE; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN;

BINDING SITES; DNA POLYMERASE III; DNA, BACTERIAL; DNA, SINGLE-STRANDED; ESCHERICHIA COLI; MUTATION; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

ESCHERICHIA COLI;

EID: 70350564160     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.233     Document Type: Article

References (51)

1. Bailey S, Wing RA, Steitz TA (2006) The structure of T. aquaticus DNA polymerase III is distinct from eukaryotic replicative DNA polymerases. Cell 126: 893-904
2. Baranovskiy AG, Babayeva ND, Liston VG, Rogozin IB, Koonin EV, Pavlov YI, Vassylyev DG, Tahirov TH (2008) X-ray structure of the complex of regulatory subunits of human DNA polymerase delta. Cell Cycle (Georgetown, TX) 7: 3026-3036
3. Benkovic SJ, Valentine AM, Salinas F (2001) Replisome-mediated DNA replication. Ann Rev Biochem 70: 181-208
4. Bochkarev A, Barwell JA, Pfuetzner RA, Bochkareva E, Frappier L, Edwards AM (1996) Crystal structure of the DNA-binding domain of the Epstein-Barr virus origin-binding protein, EBNA1, bound to DNA. Cell 84: 791-800
5. Bowman GD, O'Donnell M, Kuriyan J (2004) Structural analysis of a eukaryotic sliding DNA clamp-clamp loader complex. Nature 429:724-730
6. Breier AM, Weier HU, Cozzarelli NR (2005) Independence of replisomes in Escherichia coli chromosomal replication. Proc Natl Acad Sci USA 102: 3942-3947
7. Chilkova O, Stenlund P, Isoz I, Stith CM, Grabowski P, Lundstrom EB, Burgers PM, Johansson E (2007) The eukaryotic leading and lagging strand DNA polymerases are loaded onto primer-ends via separate mechanisms but have comparable processivity in the presence of PCNA. Nucleic Acids Res 35: 6588-6597
8. Dallmann HG, Kim S, Pritchard AE, Marians KJ, McHenry CS (2000) Characterization of the unique C terminus of the Escherichia coli tau DnaX protein. Monomeric C-tau binds alpha AND DnaB and can partially replace tau in reconstituted replication forks. J Biol Chem 275: 15512-15519
9. Dohrmann PR, McHenry CS (2005) A bipartite polymerase-proces-sivity factor interaction: only the internal beta binding site of the alpha subunit is required for processive replication by the DNA polymerase III holoenzyme. J Mol Biol 350: 228-239
10. Evans RJ, Davies DR, Bullard JM, Christensen J, Green LS, Guiles JW, Pata JD, Ribble WK, Janjic N, Jarvis TC (2008) Structure of PolC reveals unique DNA binding and fidelity determinants. Proc Natl Acad Sci USA 105: 20695-20700
11. Gao D, McHenry CS (2001) tau binds and organizes Escherichia coli replication through distinct domains. Partial proteolysis of terminally tagged tau to determine candidate domains and to assign domain V as the alpha binding domain. J Biol Chem 276: 4433-4440
12. Hacker KJ, Alberts BM (1994) The rapid dissociation of the T4 DNA polymerase holoenzyme when stopped by a DNA hairpin helix. A model for polymerase release following the termination of each Okazaki fragment. J Biol Chem 269: 24221-24228
13. Hamdan SM, Loparo JJ, Takahashi M, Richardson CC, van Oijen AM (2009) Dynamics of DNA replication loops reveal temporal control of lagging-strand synthesis. Nature 457: 336-339
14. Johnson A, O'Donnell M (2005) Cellular DNA replicases: components and dynamics at the replication fork. Ann Rev Biochem 74: 283-315
15. Johnson DE, Takahashi M, Hamdan SM, Lee SJ, Richardson CC (2007) Exchange of DNA polymerases at the replication fork of bacteriophage T7. Proc Natl Acad Sci USA 104: 5312-5317
16. Kim DR, McHenry CS (1996) Biotin tagging deletion analysis of domain limits involved in protein-macromolecular interactions. Mapping the tau binding domain of the DNA polymerase III alpha subunit. J Biol Chem 271: 20690-20698
17. Kong XP, Onrust R, O'Donnell M, Kuriyan J (1992) Three-dimensional structure of the beta subunit of E. coli DNA polymerase III holoenzyme: a sliding DNA clamp. Cell 69: 425-437
18. Kornberg A, Baker TA (1992) DNA Replication, 2nd edn., New York: W.H. Freeman
19. Lamers MH, Georgescu RE, Lee SG, O'Donnell M, Kuriyan J (2006) Crystal structure of the catalytic alpha subunit of E. coli replica-tive DNA polymerase III. Cell 126: 881-892
20. Langston L, O'Donnell M (2008) DNA Polymerase delta is highly processive with PCNA and undergoes collision release upon completing DNA. J Biol Chem 283: 29522-29531
21. Lee JB, Hite RK, Hamdan SM, Xie XS, Richardson CC, van Oijen AM (2006) DNA primase acts as a molecular brake in DNA replication. Nature 439: 621-624
22. Lei M, Podell ER, Baumann P, Cech TR (2003) DNA self-recognition in the structure of Pot1 bound to telomeric single-stranded DNA. Nature 426: 198-203
23. Leu FP, Georgescu R, O'Donnell M (2003) Mechanism of the E. coli tau processivity switch during lagging-strand synthesis. Mol Cell 11: 315-327
24. Li X, Marians KJ (2000) Two distinct triggers for cycling of the lagging strand polymerase at the replication fork. J Biol Chem 275: 34757-34765
25. Lopez de Saro FJ, Georgescu RE, O'Donnell M (2003) A peptide switch regulates DNA polymerase processivity. Proc Natl Acad Sci USA 100: 14689-14694
26. Maga G, Hubscher U (2003) Proliferating cell nuclear antigen (PCNA): a dancer with many partners. J Cell Sci 1 1 6 (Pt 15): 3051-3060
27. McCauley MJ, Shokri L, Sefcikova J, Venclovas C, Beuning PJ, Williams MC (2008) Distinct double-and single-stranded DNA binding of E. coli replicative DNA polymerase III alpha subunit. ACS Chem Biol 3: 577-587
28. McHenry CS (2003) Chromosomal replicases as asymmetric dimers: studies of subunit arrangement and functional consequences. Mol Microbiol 49: 1157-1165
29. McInerney P, O'Donnell M (2004) Functional uncoupling of twin polymerases: mechanism of polymerase dissociation from a lagging-strand block. J Biol Chem 279: 21543-21551
30. McInerney P, O'Donnell M (2007) Replisome fate upon encountering a leading strand block and clearance from DNA by recombination proteins. J Biol Chem 282: 25903-25916
31. Mok M, Marians KJ (1987) The Escherichia coli preprimosome and DNA B helicase can form replication forks that move at the same rate. J Biol Chem 262: 16644-16654
32. O'Donnell M (2006) Replisome architecture and dynamics in Escherichia coli. J Biol Chem 281: 10653-10656
33. O'Donnell ME (1987) Accessory proteins bind a primed template and mediate rapid cycling of DNA polymerase III holoenzyme from Escherichia coli. J Biol Chem 262: 16558-16565
34. O'Donnell ME, Kornberg A (1985) Dynamics of DNA polymerase III holoenzyme of Escherichia coli in replication of a multiprimed template. J Biol Chem 260: 12875-12883 (Pubitemid 16230586)
35. Onrust R, Finkelstein J, Turner J, Naktinis V, O'Donnell M (1995) Assembly of a chromosomal replication machine: two DNA polymerases, a clamp loader, and sliding clamps in one holo-enzyme particle. III. Interface between two polymerases and the clamp loader. J Biol Chem 270: 13366-13377
36. Podust VN, Podust LM, Muller F, Hubscher U (1995) DNA poly-merase delta holoenzyme: action on single-stranded DNA and on double-stranded DNA in the presence of replicative DNA heli-cases. Biochemistry 34: 5003-5010
37. Pomerantz RT, O'Donnell M (2008) The replisome uses mRNA as a primer after colliding with RNA polymerase. Nature 456: 762-766
38. Rowen L, Kornberg A (1978) Primase, the dnaG protein of Escherichia coli. An enzyme which starts DNA chains. J Biol Chem 253: 758-764
39. Stillman B (2008) DNA polymerases at the replication fork in eukaryotes. Mol Cell 30: 259-260
40. Stukenberg PT, O'Donnell M (1995) Assembly of a chromosomal replication machine: two DNA polymerases, a clamp loader, and sliding clamps in one holoenzyme particle. V. Four different polymerase-clamp complexes on DNA. J Biol Chem 270: 13384-13391
41. Stukenberg PT, Turner J, O'Donnell M (1994) An explanation for lagging strand replication: polymerase hopping among DNA sliding clamps. Cell 78: 877-887
42. Sugimoto K, Sakamoto Y, Takahashi O, Matsumoto K (1995) HYS2, an essential gene required for DNA replication in Saccharomyces cerevisiae. Nucleic Acids Res 23: 3493-3500
43. Turner J, O'Donnell M (1995) Cycling of Escherichia coli DNA polymerase III from one sliding clamp to another: model for lagging strand. Methods Enzymol 262: 442-449
44. Wang F, Podell ER, Zaug AJ, Yang Y, Baciu P, Cech TR, Lei M (2007) The POT1-TPP1 telomere complex is a telomerase processivity factor. Nature 445: 506-510
45. Wing RA, Bailey S, Steitz TA (2008) Insights into the replisome from the structure of a ternary complex of the DNA polymerase III alpha-subunit. J Mol Biol 382: 859-869
46. Wu CA, Zechner EL, Reems JA, McHenry CS, Marians KJ (1992) Coordinated leading-and lagging-strand synthesis at the Escherichia coli DNA replication fork. V. Primase action regulates the cycle of Okazaki fragment synthesis. J Biol Chem 267: 4074-4083
47. Xi J, Zhang Z, Zhuang Z, Yang J, Spiering MM, Hammes GG, Benkovic SJ (2005) Interaction between the T4 helicase loading protein (gp59) and the DNA polymerase (gp43): unlocking of the gp59-gp43-DNA complex to initiate assembly of a fully functional replisome. Biochemistry 44: 7747-7756 (Pubitemid 40740758)
48. Yang J, Nelson SW, Benkovic SJ (2006) The control mechanism for lagging strand polymerase recycling during bacteriophage T4 DNA replication. Mol Cell 21: 153-164
49. Yao N, Hurwitz J, O'Donnell M (2000) Dynamics of beta and proliferating cell nuclear antigen sliding clamps in traversing DNA secondary structure. J Biol Chem 275: 1421-1432
50. Yuzhakov A, Turner J, O'Donnell M (1996) Replisome assembly reveals the basis for asymmetric function in leading and lagging strand replication. Cell 86: 877-886
51. Zhao XQ, Hu JF, Yu J (2006) Comparative analysis of eubacterial DNA polymerase III alpha subunits. Genomics Proteomics Bioinformatics 4: 203-211