A sliding-clamp toolbelt binds high- and low-fidelity DNA polymerases simultaneously

Molecular Cell

Volumn 19, Issue 6, 2005, Pages 805-815

  Indiani, Chiara ^a   McInerney, Peter ^a   Georgescu, Roxana ^a   Goodman, Myron F ^b   O'Donnell, Mike ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE GAMMA;

ARTICLE; BINDING KINETICS; CHROMOSOME REPLICATION; DNA TEMPLATE; ENZYME BINDING; ENZYME KINETICS; ESCHERICHIA COLI; NONHUMAN; PROTEIN DNA BINDING; PROTEIN FAMILY; STRUCTURAL GENE;

DNA POLYMERASE BETA; DNA POLYMERASE III; DNA REPLICATION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MACROMOLECULAR SUBSTANCES; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 24944543952     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2005.08.011     Document Type: Article

References (56)

1. B. Ason, R. Handayani, C.R. Williams, J.G. Bertram, M.M. Hingorani, M. O'Donnell, M.F. Goodman, and L.B. Bloom Mechanism of loading the Escherichia coli DNA polymerase III beta sliding clamp on DNA. Bona fide primer/templates preferentially trigger the gamma complex to hydrolyze ATP and load the clamp J. Biol. Chem. 278 2003 10033 10040
2. J.G. Bertram, L.B. Bloom, M. O'Donnell, and M.F. Goodman Increased dNTP binding affinity reveals a nonprocessive role for Escherichia coli beta clamp with DNA polymerase IV J. Biol. Chem. 279 2004 33047 33050
3. C.A. Bonner, P.T. Stukenberg, M. Rajagopalan, R. Eritja, M. O'Donnell, K. McEntee, H. Echols, and M.F. Goodman Processive DNA synthesis by DNA polymerase II mediated by DNA polymerase III accessory proteins J. Biol. Chem. 267 1992 11431 11438
4. I. Bruck, and M. O'Donnell Reconstitution of the DNA replication apparatus of Streptococcus pyogenes, a gram positive organism J. Biol. Chem. 275 2000 28971 28983
5. I. Bruck, R.E. Georgescu, and M. O'Donnell Conserved interactions in the Staphylococcus aureus DNA POLC chromosome replication machine J. Biol. Chem. 280 2005 18152 18162
6. H.J. Bull, M.J. Lombardo, and S.M. Rosenberg Stationary-phase mutation in the bacterial chromosome: recombination protein and DNA polymerase IV dependence Proc. Natl. Acad. Sci. USA 98 2001 8334 8341
7. K.A. Bunting, S.M. Roe, and L.H. Pearl Structural basis for recruitment of translesion DNA polymerase Pol IV/DinB to the beta-clamp EMBO J. 22 2003 5883 5892
8. D.Y. Burnouf, V. Olieric, J. Wagner, S. Fujii, J. Reinbolt, R.P. Fuchs, and P. Dumas Structural and biochemical analysis of sliding clamp/ligand interactions suggest a competition between replicative and translesion DNA polymerases J. Mol. Biol. 335 2004 1187 1197
9. B.P. Dalrymple, K. Kongsuwan, G. Wijffels, N.E. Dixon, and P.A. Jennings A universal protein-protein interaction motif in the eubacterial DNA replication and repair systems Proc. Natl. Acad. Sci. USA 98 2001 11627 11632
10. I. Dionne, R.K. Nookala, S.P. Jackson, A.J. Doherty, and S.D. Bell A heterotrimeric PCNA in the hyperthermophilic archaeon Sulfolobus solfataricus Mol. Cell 11 2003 275 282
11. S. Fujii, and R.P. Fuchs Defining the position of the switches between replicative and bypass DNA polymerases EMBO J. 23 2004 4342 4352
12. M.F. Goodman Error-prone repair DNA polymerases in prokaryotes and eukaryotes Annu. Rev. Biochem. 71 2002 17 50
13. J.M. Gulbis, Z. Kelman, J. Hurwitz, M. O'Donnell, and J. Kuriyan Structure of the C-terminal region of p21(WAF1/CIP1) complexed with human PCNA Cell 87 1996 297 306
14. L. Haracska, I. Unk, R.E. Johnson, B.B. Phillips, J. Hurwitz, L. Prakash, and S. Prakash Stimulation of DNA synthesis activity of human DNA polymerase kappa by PCNA Mol. Cell. Biol. 22 2002 784 791
15. K. Higuchi, T. Katayama, S. Iwai, M. Hidaka, T. Horiuchi, and H. Maki Fate of DNA replication fork encountering a single DNA lesion during oriC plasmid DNA replication in vitro Genes Cells 8 2003 437 449
16. M. Hingorani, and M. O'Donnell ATP binding to the Escherichia coli clamp loader powers opening of the ring-shaped clamp of DNA polymerase III holoenzyme J. Biol. Chem. 273 1998 24550 24563
17. A.J. Hughes Jr., S.K. Bryan, H. Chen, R.E. Moses, and C.S. McHenry Escherichia coli DNA polymerase II is stimulated by DNA polymerase III holoenzyme auxiliary subunits J. Biol. Chem. 266 1991 4568 4573
18. D. Jeruzalmi, O. Yurieva, Y. Zhao, M. Young, J. Stewart, M. Hingorani, M. O'Donnell, and J. Kuriyan 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
19. A. Johnson, and M. O'Donnell Cellular DNA replicases: components and dynamics at the replication fork Annu. Rev. Biochem. 74 2005 283 315
20. A. Johnson, and M. O'Donnell DNA ligase: getting a grip to seal the deal Curr. Biol. 15 2005 R90 R92
21. D.R. Kim, and C.S. McHenry Identification of the beta-binding domain of the alpha subunit of Escherichia coli polymerase III holoenzyme J. Biol. Chem. 271 1996 20699 20704
22. S.R. Kim, G. Maenhaut-Michel, M. Yamada, Y. Yamamoto, K. Matsui, T. Sofuni, T. Nohmi, and H. Ohmori Multiple pathways for SOS-induced mutagenesis in Escherichia coli: an overexpression of dinB/dinP results in strongly enhancing mutagenesis in the absence of any exogenous treatment to damage DNA Proc. Natl. Acad. Sci. USA 94 1997 13792 13797
23. N. Klemperer, D. Zhang, M. Skangalis, and M. O'Donnell Cross-utilization of the beta sliding clamp by replicative polymerases of evolutionary divergent organisms J. Biol. Chem. 275 2000 26136 26143
24. S. Kobayashi, M.R. Valentine, P. Pham, M. O'Donnell, and M.F. Goodman Fidelity of Escherichia coli DNA polymerase IV. Preferential generation of small deletion mutations by dNTP-stabilized misalignment J. Biol. Chem. 277 2002 34198 34207
25. X.P. Kong, R. Onrust, M. O'Donnell, and J. Kuriyan Three-dimensional structure of the beta subunit of E. coli DNA polymerase III holoenzyme: a sliding DNA clamp Cell 69 1992 425 437
26. W. Kuban, P. Jonczyk, D. Gawel, K. Malanowska, R.M. Schaaper, and I.J. Fijalkowska Role of Escherichia coli DNA polymerase IV in in vivo replication fidelity J. Bacteriol. 186 2004 4802 4807
27. N. Lenne-Samuel, J. Wagner, H. Etienne, and R.P. Fuchs The processivity factor beta controls DNA polymerase IV traffic during spontaneous mutagenesis and translesion synthesis in vivo EMBO Rep. 3 2002 45 49
28. F.P. Leu, and M. O'Donnell Interplay of clamp loader subunits in opening the beta sliding clamp of Escherichia coli DNA polymerase III holoenzyme J. Biol. Chem. 276 2001 47185 47194
29. H. Ling, F. Boudsocq, R. Woodgate, and W. Yang Crystal structure of a Y-family DNA polymerase in action: A mechanism for error-prone and lesion-bypass replication Cell 107 2001 91 102
30. F.J. Lopez de Saro, and M. O'Donnell Interaction of the beta sliding clamp with MutS, ligase, and DNA polymerase I Proc. Natl. Acad. Sci. USA 98 2001 8376 8380
31. F.J. Lopez de Saro, R.E. Georgescu, M.F. Goodman, and M. O'Donnell Competitive processivity-clamp usage by DNA polymerases during DNA replication and repair EMBO J. 22 2003 6408 6418
32. F.J. Lopez de Saro, R.E. Georgescu, and M. O'Donnell A peptide switch regulates DNA polymerase processivity Proc. Natl. Acad. Sci. USA 100 2003 14689 14694
33. A. Maor-Shoshani, K. Hayashi, H. Ohmori, and Z. Livneh Analysis of translesion replication across an abasic site by DNA polymerase IV of Escherichia coli DNA Repair (Amst.) 2 2003 1227 1238
34. M.A. Marti-Renom, A.C. Stuart, A. Fiser, R. Sanchez, F. Melo, and A. Sali Comparative protein structure modeling of genes and genomes Annu. Rev. Biophys. Biomol. Struct. 29 2000 291 325
35. P. McInerney, and M. O'Donnell Functional uncoupling of twin polymerases: Mechanism of polymerase dissociation from a lagging strand block J. Biol. Chem. 279 2004 21543 21551
36. V. Naktinis, J. Turner, and M. O'Donnell A molecular switch in a replication machine defined by an internal competition for protein rings Cell 84 1996 137 145
37. R. Napolitano, R. Janel-Bintz, J. Wagner, and R.P. Fuchs All three SOS-inducible DNA polymerases (Pol II, Pol IV and Pol V) are involved in induced mutagenesis EMBO J. 19 2000 6259 6265
38. M.E. O'Donnell Accessory proteins bind a primed template and mediate rapid cycling of DNA polymerase III holoenzyme from Escherichia coli J. Biol. Chem. 262 1987 16558 16565
39. R. Onrust, J. Finkelstein, V. Naktinis, J. Turner, L. Fang, and M. O'Donnell Assembly of a chromosomal replication machine: two DNA polymerases, a clamp loader, and sliding clamps in one holoenzyme particle. I. Organization of the clamp loader J. Biol. Chem. 270 1995 13348 13357
40. A.E. Pritchard, H.G. Dallmann, B.P. Glover, and C.S. McHenry A novel assembly mechanism for the DNA polymerase III holoenzyme DnaX complex: association of deltadelta' with DnaX(4) forms DnaX(3)deltadelta' EMBO J. 19 2000 6536 6545
41. Y. Shamoo, and T.A. Steitz Building a replisome from interacting pieces: sliding clamp complexed to a peptide from DNA polymerase and a polymerase editing complex Cell 99 1999 155 166
42. H. Shwartz, and Z. Livneh Dynamics of termination during in vitro replication of ultraviolet-irradiated DNA with DNA polymerase III holoenzyme of Escherichia coli J. Biol. Chem. 262 1987 10518 10523
43. J. Stewart, M.M. Hingorani, Z. Kelman, and M. O'Donnell Mechanism of beta clamp opening by the delta subunit of Escherichia coli DNA polymerase III holoenzyme J. Biol. Chem. 276 2001 19182 19189
44. P.T. Stukenberg, P.S. Studwell-Vaughan, and M. O'Donnell Mechanism of the sliding beta-clamp of DNA polymerase III holoenzyme J. Biol. Chem. 266 1991 11328 11334
45. P.T. Stukenberg, J. Turner, and M. O'Donnell An explanation for lagging strand replication: polymerase hopping among DNA sliding clamps Cell 78 1994 877 887
46. M. Tang, P. Pham, X. Shen, J.S. Taylor, M. O'Donnell, R. Woodgate, and M.F. Goodman Roles of E. coli DNA polymerases IV and V in lesion-targeted and untargeted SOS mutagenesis Nature 404 2000 1014 1018
47. B. Tippin, P. Pham, and M.F. Goodman Error-prone replication for better or worse Trends Microbiol. 12 2004 288 295
48. J. Turner, M. Hingorani, Z. Kelman, and M. O'Donnell The internal workings of a DNA polymerase clamp-loading machine EMBO J. 18 1999 771 783
49. S.N. Uljon, R.E. Johnson, T.A. Edwards, S. Prakash, L. Prakash, and A.K. Aggarwal Crystal structure of the catalytic core of human DNA polymerase kappa Structure 12 2004 1395 1404
50. I. Unk, L. Haracska, X.V. Gomes, P.M. Burgers, L. Prakash, and S. Prakash Stimulation of 3′→5′ exonuclease and 3′- phosphodiesterase activities of yeast apn2 by proliferating cell nuclear antigen Mol. Cell. Biol. 22 2002 6480 6486
51. J. Wagner, and T. Nohmi Escherichia coli DNA polymerase IV mutator activity: genetic requirements and mutational specificity J. Bacteriol. 182 2000 4587 4595
52. J. Wagner, S. Fujii, P. Gruz, T. Nohmi, and R.P. Fuchs The beta clamp targets DNA polymerase IV to DNA and strongly increases its processivity EMBO Rep. 1 2000 484 488
53. E. Warbrick The puzzle of PCNA's many partners Bioessays 22 2000 997 1006
54. E. Wolff, M. Kim, K. Hu, H. Yang, and J.H. Miller Polymerases leave fingerprints: analysis of the mutational spectrum in Escherichia coli rpoB to assess the role of polymerase IV in spontaneous mutation J. Bacteriol. 186 2004 2900 2905
55. J. Yang, Z. Zhuang, R.M. Roccasecca, M.A. Trakselis, and S.J. Benkovic The dynamic processivity of the T4 DNA polymerase during replication Proc. Natl. Acad. Sci. USA 101 2004 8289 8294
56. B. Yeiser, E.D. Pepper, M.F. Goodman, and S.E. Finkel SOS-induced DNA polymerases enhance long-term survival and evolutionary fitness Proc. Natl. Acad. Sci. USA 99 2002 8737 8741