Competitive processivity-clamp usage by DNA polymerases during DNA replication and repair

EMBO Journal

Volumn 22, Issue 23, 2003, Pages 6408-6418

  López De Saro, Francisco J ^a   Georgescu, Roxana E ^a   Goodman, Myron F ^b   O'Donnell, Mike ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

clamp; Clamp loader; DNA polymerase; DNA repair; PCNA; RFC

Indexed keywords

BACTERIAL DNA; DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE BETA; DNA DIRECTED DNA POLYMERASE GAMMA; DNA POLYMERASE; DNA POLYMERASE 4; DNA POLYMERASE 5; POL PROTEIN; PROTEIN; PROTEIN BETA CLAMP; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPETITIVE ABILITY; CONTROLLED STUDY; DELTA SUBUNIT; DNA REPAIR; DNA REPLICATION; ENZYME BINDING; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM;

AMINO ACID SEQUENCE; DNA POLYMERASE III; DNA REPAIR; DNA REPLICATION; DNA, BACTERIAL; ESCHERICHIA COLI; KINETICS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN SUBUNITS; RECOMBINANT PROTEINS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 0348134870     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg603     Document Type: Article

References (48)

1. Ason, B., Hingorani M.M., Beechem, J.M., O'Donnell, M., Goodman, M.F. and Bloom, L.B. (2000) A model for Escherichia coli DNA polymerase III holoenzyme assembly at primer/template ends. DNA triggers a change in binding specificity of the gamma complex clamp loader. J. Biol. Chem., 275, 3006-3015.
2. Ason, B., Handayani, R., Williams, C.R., Bertram, J.G., Hingorani, M.M., O'Donnell, M., Goodman, M.F. and Bloom, L.B. (2003) Mechanism of loading the Escherichia coli DNA polymerase III β sliding clamp on DNA. Bona fide primer/template preferentially trigger the γ complex to hydrolyze ATP and load the clamp. J. Biol. Chem., 278, 10033-10040.
3. Baker, T. and Komberg, A. (1992) DNA Replication. Second edition. W.H. Freeman and Co, New York.
4. Becherel, O.J., Fuchs, R.P.P. and Wagner, J. (2002) Pivotal role of the β-clamp in translesion DNA synthesis and mutagenesis in E. coli cells. DNA Repair, 1, 703-708.
5. Berdis, A.J., Soumillion, P. and Benkovic, S.J. (1996) The carboxyl terminus of the bacteriophage T4 DNA polymerase is required for holoenzyme complex formation. Proc. Natl Acad. Sci. USA, 93, 12822-12827.
6. Bonner, C.A., Stukenberg, P.T., Rajagopalan, M., Eritja, R., O'Donnell, M., McEntee, K., Echols, H. and Goodman, M.F. (1992) Processive DNA synthesis by DNA polymerase II mediated by DNA polymerase III accessory subunits. J. Biol. Chem., 267, 11431-11438.
7. Braithwaite, D.K. and Ito, J. (1993) Compilation, alignment and phylogenetic relationships of DNA polymerases. Nucleic Acids Res., 21, 787-820.
8. Bruck I., Woodgate, R., McEntee, K. Goodman, M.F. (1996) Purification of a soluble UmuD'C complex from Escherichia coli. J. Biol. Chem., 271, 10767-10774.
9. Dalrymple, B.P., Kongsuwan, K., Wijffels, G., Dixon, N.E. and Jennings, P.A. (2001) A universal protein-protein interaction motif in the eubacterial DNA replication and repair systems. Proc. Natl Acad. Sci. USA, 98, 11627-11632.
10. Filée, J., Forterre, P., Sen-Lin, T. and Laurent, J. (2002) Evolution of DNA polymerase families: evidences for multiple gene exchange between cellular and viral proteins. J. Mol. Evol., 54, 763-773.
11. Goodman, M. (2002) Error-prone repair DNA polymerases in prokaryotes and eukaryotes. Annu. Rev. Biochem., 71, 17-50.
12. Goodman, M. and Tippin, B. (2000) Slopier copier DNA polymerases involved in DNA repair. Curr. Opin. Genet. Dev., 10, 162-168.
13. 2+. Biochemistry, 27, 5210-5215.
14. WAF1/CIP1 complexed with human PCNA. Cell, 87, 297-306.
15. Hughes, A.J., Bryan, S.K., Chen, H., Moses, R.E. and McHenry, C.S. (1991) Escherichia coli DNA polymerase II is stimulated by DNA polymerase III holoenzyme auxiliary subunits. J. Biol. Chem., 266, 4568-4573.
16. Jeruzalmi, D., Yurieva, O., Zhao, Y., Young, M., Stewart, J., Hingorani, M., O'Donnell, M. and Kuriyan, J. (2001) Mechanism of processivity clamp opening by the delta subunit wrench of the clamp loader complex of E.coli DNA polymerase III. Cell, 106, 417-428.
17. Kelman, Z., Naktinis, V. and O'Donnell, M. (1995) Radiolabeling of proteins for biochemical studies. Methods Enzymol., 262, 430-442.
18. Kelman, Z., Zuo, S., Arroyo, M.P., Wang, T.S.-F. and Hurwitz, J. (1999) The C-terminal region of Schizosaccharomyces pombe proliferating cell nuclear antigen is essential for DNA polymerase activity. Proc. Natl Acad. Sci. USA, 96, 9515-9520.
19. Kim, D.R. and McHenry, C.S. (1996) Identification of the β-binding domain of the α subunit of Escherichia coli Polymerase III holoenzyme. J. Biol. Chem., 271, 20699-20704.
20. Kobayashi, S., Valentine, M.R., Pham, P., O'Donnell, M. and Goodman, M.F. (2002) Fidelity of Escherichia coli DNA Polymerase IV. Preferential generation of small deletion mutations by dNTP-stabilized misalignment. J. Biol. Chem., 277, 34198-34207.
21. Kong, X.-P., Onrust, R., O'Donnell, M. and Kuriyan, J. (1992) Three dimensional structure of the β subunit of Escherichia coli DNA polymerase III Holoenzyme: a sliding DNA-clamp. Cell, 69, 425-437.
22. Lenne-Samuel, N., Wagner, J., Etienne, H. and Fuchs, R.P.P. (2002) The processivity factor β controls DNA polymerase IV traffic during spontaneous mutagenesis and translesion synthesis in vivo. EMBO Rep., 3, 45-49.
23. Leu, F., Georgescu, R. and O'Donnell, M. (2003) Mechanism of the E.coli τ processivity switch during lagging-strand synthesis. Mol. Cell, 11, 315-327.
24. López de Saro, F.J. and O'Donnell, M. (2001) Interaction of the β sliding clamp with MutS, ligase and DNA polymerase I. Proc. Natl Acad. Sci. USA, 98, 8376-8380.
25. López de Saro, F.J., Georgescu, R.E. and O'Donnell, M. (2003) A peptide switch regulates DNA polymerase processivity. Proc. Natl Acad. Sci. USA, in press.
26. Naktinis, V., Turner, J. and O'Donnell, M. (1996) A molecular switch in a replication machine defined by an internal competition for protein rings. Cell, 84, 137-145.
27. O'Donnell, M.E. (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.
28. O'Donnell, M., Jeruzalmi, D. and Kuriyan, J. (2001) Clamp loader structure predicts the architecture of DNA polymerase III holoenzyme and RFC. Curr. Biol., 11, R935-R946.
29. Ohmori, H. et al. (2001) The Y-family of DNA polymerases. Mol. Cell, 8, 7-8.
30. Pham, P., Bertram, J.G., O'Donnell, M., Woodgate, R. and Goodman, M.F. (2001) A model for SOS-lesion-targeted mutations in Escherichia coli. Nature, 409, 366-370.
31. Pham, P., Seitz, E.M., Saveliev, S., Shen, X., Woodgate, R., Cox, M.M. and Goodman, M.F. (2002) Two distinct modes of RecA action are required for DNA polymerase V-catalyzed translesion synthesis. Proc. Natl Acad. Sci. USA., 99, 11061-11066.
32. Shamoo, Y. and Steitz, T.A. (1999) Building a replisome from interacting pieces: sliding clamp complexed to a peptide from DNA polymerase and a polymerase editing complex. Cell, 99, 155-166.
33. Stucki, M., Stagljar, I., Jónsson, Z.O. and Hübscher, U. (2001) A coordinated interplay: proteins with multiple functions in DNA replication, DNA repair, cell cyle/checkpoint control and transcription. Prog. Nucleic Acids Res., 65, 261.
34. Stuckenberg, P.T., Studwell-Vaughan, P.S. and O'Donnell, M. (1991) Mechanism of the sliding β-clamp of DNA polymerase III holoenzyme. J. Biol. Chem., 266, 11328-11334.
35. Stuckenberg, P.T., Turner, J. and O'Donnell, M. (1994) An explanation for lagging strand replication: polymerase hopping among DNA sliding clamps. Cell, 78, 877-887.
36. Studwell, P.S. and O'Donnell, M. (1990) Processive replication is contingent on the exonuclease subunit of DNA polymerase III holoenzyme. J. Biol. Chem., 265, 1171-1178.
37. Studwell, P.S. and O'Donnell, M. (1991) Constitution of the twin polymerase of DNA polymerase III holoenzyme. J. Biol. Chem., 266, 19833-19841.
38. Studwell-Vaughan, P.S. and O'Donnell, M. (1991) Constitution of the twin polymerase of DNA polymerase III holoenzyme. J. Biol. Chem., 266, 19833-19841.
39. Sutton, M.D. and Walker, G.C. (2001) Managing DNA polymerases: coordinating DNA replication, DNA repair and DNA recombination. Proc. Natl Acad. Sci. USA, 98, 8342-8349.
40. Sutton, M.D., Opperman, T. and Walker, G.C. (1999) The Escherichia coli SOS mutagenesis proteins UmuD and UmuD' interact physically with the replicative DNA polymerase. Proc. Natl Acad. Sci. USA, 96, 12373-12378.
41. Tang, M., Pham, P., Shen, X., Taylor, J.-S., O'Donnell, M., Woodgate, R. and Goodman, M.F. (2000) Roles of E.coli DNA polymerases IV and V in lesion-targeted and untargeted mutagenesis. Nature, 404, 1014-1018.
42. Turner, J., Hingorani, M.M., Kelman, Z. and O'Donnell, M. (1999). The internal workings of a DNA polymerase clamp-loading machine. EMBO J., 18, 771-783.
43. Wagner, J., Fujii, S., Gruz, P., Nohmi, T. and Fuchs, R.P.P. (2000) The β clamp targets DNA polymerase IV to DNA and strongly increases its processivity. EMBO Rep., 1, 484-488.
44. Wagner, J., Etienne, H., Janel-Bintz, R. and Fuchs, R.P.P. (2002) Genetics of mutagenesis in E.coli: various combinations of translesion polymerases (PolII, IV and V) deal with lesion/sequence context diversity. DNA Repair, 1, 159-167.
45. Warbrick, E. (2000) The puzzle of PCNA's many partners. BioEssays, 22, 997-1006.
46. Woodgate, R. and Ennis, D.G. (1991) Levels of chromosomally encoded Umu proteins and requirements for in vivo UmuD cleavage. Mol. Gen. Genet., 229, 10-16.
47. Woodgate, R., Rajagopalan, M., Lu, C. and Echols, H. (1989) UmuC mutagenesis protein of Escherichia coli: purification and interaction with UmuD and UmuD'. Proc. Natl Acad. Sci. USA, 86, 7301-7305.
48. Yuzhakov, A., Kelman, Z. and O'Donnell, M. (1999) Trading places on DNA: a three point switch underlies primer handoff from primase to the replicative DNA polymerase. Cell, 96, 153-163.