Structural basis for recruitment of translesion DNA polymerase Pol IV/DinB to the β-clamp

EMBO Journal

Volumn 22, Issue 21, 2003, Pages 5883-5892

  Bunting, Karen A ^a   Roe, S Mark ^a   Pearl, Laurence H ^b  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^b NONE

Author keywords

clamp processivity factor; DNA polymerase IV; Y family

Indexed keywords

BETA CLAMP PROCESSIVITY FACTOR; CYCLINE; DNA POLYMERASE; PEPTIDE; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DNA REPLICATION; DNA STRAND; DNA SYNTHESIS; DNA TEMPLATE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME REGULATION; ENZYME STRUCTURE; ESCHERICHIA COLI; GENE MUTATION; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; STRUCTURE ANALYSIS;

BACTERIAL PROTEINS; BINDING SITES; DNA POLYMERASE BETA; DNA POLYMERASE III; DNA REPLICATION; DNA, BACTERIAL; ESCHERICHIA COLI PROTEINS; HUMANS; MACROMOLECULAR SUBSTANCES; MODELS, MOLECULAR; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN SUBUNITS; RECOMBINANT PROTEINS;

ESCHERICHIA COLI; NEGIBACTERIA;

EID: 0242389787     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg568     Document Type: Article

References (57)

1. Boudsocq, F., Ling, H., Yang, W. and Woodgate, R. (2002) Structure-based interpretation of missense mutations in Y-family DNA polymerases and their implications for polymerase function and lesion bypass. DNA Repair, 1, 343-358.
2. Brünger, A.T. et al. (1998) Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D, 54, 905-921.
3. CCP4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D, 50, 760-763.
4. Cordonnier, A.M. and Fuchs, R.P. (1999) Replication of damaged DNA: molecular defect in xeroderma pigmentosum variant cells. Mutat. Res., 435, 111-119.
5. 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.
6. Friedberg, E.C., Fischhaber, P.L. and Kisker, C. (2001) Error-prone DNA polymerases: novel structures and the benefits of infidelity. Cell, 107, 9-12.
7. Friedberg, E.C., Wagner, R. and Radman, M. (2002) Specialized DNA polymerases, cellular survival and the genesis of mutations. Science, 296, 1627-1630.
8. Gerlach, V.L., Aravind, L., Gotway, G., Schultz, R.A., Koonin, E.V. and Friedberg, E.C. (1999) Human and mouse homologs of Escherichia coli DinB (DNA polymerase IV), members of the UmuC/DinB superfamily. Proc. Natl Acad. Sci. USA, 96, 11922-11927.
9. Gibbs, P.E., Wang, X.D., Li, Z., McManus, T.P., McGregor, W.G., Lawrence, C.W. and Maher, V.M. (2000) The function of the human homolog of Saccharomyces cerevisiae REV1 is required for mutagenesis induced by UV light. Proc. Natl Acad. Sci. USA, 97, 4186-4191.
10. Goodman, M.F. (1997) Hydrogen bonding revisited: geometric selection as a principal determinant of DNA replication fidelity. Proc. Natl Acad. Sci. USA, 94, 10493-10495.
11. Gulbis, J.M., Kelman, Z., Hurwitz, J., O'Donnell, M. and Kuriyan, J. (1996) Structure of the C-terminal region of p21(WAF1/CIP1) complexed with human PCNA. Cell, 87, 297-306.
12. Haracska, L., Prakash, S. and Prakash, L. (2000) Replication past O(6)-methylguanine by yeast and human DNA polymerase η. Mol. Cell. Biol., 20, 8001-8007.
13. Haracska, L., Johnson, R.E., Unk, I., Phillips, B., Hurwitz, J., Prakash, L. and Prakash, S. (2001a) Physical and functional interactions of human DNA polymerase η with PCNA. Mol. Cell. Biol., 21, 7199-7206.
14. Haracska, L., Washington, M.T., Prakash, S. and Prakash, L. (2001b) Inefficient bypass of an abasic site by DNA polymerase η. J. Biol. Chem., 276, 6861-6866.
15. Haracska, L., Unk, I., Johnson, R.E., Phillips, B.B., Hurwitz, J., Prakash, L. and Prakash, S. (2002) Stimulation of DNA synthesis activity of human DNA polymerase κ by PCNA. Mol. Cell. Biol., 22, 784-791.
16. Hingorani, M.M. and O'Donnell, M. (2000) Sliding clamps: a (tail)ored fit. Curr. Biol., 10, R25-R29.
17. Hosfield, D.J., Mol, C.D., Shen, B.H. and Tainer, J.A. (1998) Structure of the DNA repair and replication endonuclease and exonuclease FEN-1: coupling DNA and PCNA binding to FEN-1 activity. Cell, 95, 135-146.
18. Hughes, A.J., Jr, 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.
19. 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 δ subunit wrench of the clamp loader complex of E.coli DNA polymerase III. Cell, 106, 417-428.
20. Johnson, R.E., Washington, M.T., Haracska, L., Prakash, S. and Prakash, L. (2000) Eukaryotic polymerases ι and ζ act sequentially to bypass DNA lesions. Nature, 406, 1015-1019.
21. Jones, T.A., Zou, J.-Y., Cowan, S.W. and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A, 47, 110-119.
22. Kelman, Z. and O'Donnell, M. (1995) Structural and functional similarities of prokaryotic and eukaryotic DNA polymerase sliding clamps. Nucleic Acids Res., 23, 3613-3620.
23. 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.
24. Kong, X.P., Onrust, R., O'Donnell, M. and Kuriyan, J. (1992) Three-dimensional structure of the β subunit of E.coli DNA polymerase III holoenzyme: a sliding DNA clamp. Cell, 69, 425-437.
25. Krishna, T.S., Kong, X.P., Gary, S., Burgers, P.M. and Kuriyan, J. (1994) Crystal structure of the eukaryotic DNA polymerase processivity factor PCNA. Cell, 79, 1233-1243.
26. Kunkel, T.A., Oavlov, Y.I. and Bebenek, K. (2003) Functions of human DNA polymerases η, κ and ι suggested by their properties, including fidelity with undamaged DNA templates. DNA Repair, 2, 135-149.
27. Lenne-Samuel, N., Wagner, J., Etienne, H. and Fuchs, R.P. (2002) The processivity factor β controls DNA polymerase IV traffic during spontaneous mutagenesis and translesion synthesis in vivo. EMBO Rep., 3, 45-49.
28. Leslie, A.G.W. (1995) MOSFLM Users Guide. MRC Laboratory of Molecular Biology, Cambridge, UK.
29. Lin, W., Xin, H., Zhang, Y., Wu, X., Yuan, F. and Wang, Z. (1999) The human REV1 gene codes for a DNA template-dependent dCMP transferase. Nucleic Acids Res., 27, 4468-4475.
30. Ling, H., Boudsocq, F., Woodgate, R. and Yang, W. (2001) Crystal structure of a Y-family DNA polymerase in action: a mechanism for error-prone and lesion-bypass replication. Cell, 107, 91-102.
31. Lopez 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.
32. Masutani, C. et al. (1999) The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase η. Nature, 399, 700-704.
33. Matsumiya, S., Ishino, Y. and Morikawa, K. (2001) Crystal structure of an archaeal DNA sliding clamp: proliferating cell nuclear antigen from Pyrococcus furiosus. Protein Sci., 10, 17-23.
34. Matsumiya, S., Ishino, S., Ishino, Y. and Morikawa, K. (2002) Physical interaction between proliferating cell nuclear antigen and replication factor C from Pyrococcus furiosus. Genes Cells, 7, 911-922.
35. McDonald, J.P., Rapic-Otrin, V., Epstein, J.A., Broughton, B.C., Wang, X., Lehmann, A.R., Wolgemuth, D.J. and Woodgate, R. (1999) Novel human and mouse homologs of Saccharomyces cerevisiae DNA polymerase η. Genomics, 60, 20-30.
36. McKenzie, G.J., Lee, P.L., Lombardo, M.J., Hastings, P.J. and Rosenberg, S.M. (2001) SOS mutator DNA polymerase IV functions in adaptive mutation and not adaptive amplification. Mol. Cell, 7, 571-579.
37. Moarefi, I., Jeruzalmi, D., Turner, J., O'Donnell, M. and Kuriyan, J. (2000) Crystal structure of the DNA polymerase processivity factor of T4 bacteriophage. J. Mol. Biol., 296, 1215-1223.
38. Murshudov, G.N., Vagin, A.A. and Dodson, E.J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D, 53, 240-255.
39. Naktinis, V., Onrust, R., Fang, L. and O'Donnell, M. (1995) Assembly of a chromosomal replication machine: two DNA polymerases, a clamp loader and sliding clamps in one holoenzyme particle. II. Intermediate complex between the clamp loader and its clamp. J. Biol. Chem., 270, 13358-13365.
40. 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.
41. Napolitano, R., Janel-Bintz, R., Wagner, J. and Fuchs, R.P. (2000) All three SOS-inducible DNA polymerases (Pol II, Pol IV and Pol V) are involved in induced mutagenesis. EMBO J., 19, 6259-6265.
42. Navaza, J. (1994) AMoRE-an automated package for molecular replacement. Acta Crystallogr. D, 50, 157-163.
43. Ohashi, E., Bebenek, K., Matsuda, T., Feaver, W.J., Gerlach, V.L., Friedberg, E.C., Ohmori, H. and Kunkel, T.A. (2000) Fidelity and processivity of DNA synthesis by DNA polymerase κ, the product of the human DINB1 gene. J. Biol. Chem., 275, 39678-39684.
44. Ohmori, H. et al. (2001) The Y-family of DNA polymerases. Mol. Cell, 8, 7-8.
45. O-Wang, Z., Kawamura, K., Tada, Y., Ohmori, H., Kimura, H., Sakiyama, S. and Tagawa, M. (2001) DNA polymerase κ, implicated in spontaneous and DNA damage-induced mutagenesis, is overexpressed in lung cancer. Cancer Res., 61, 5366-5369.
46. Pages, V. and Fuchs, R.P. (2002) How are DNA lesions turned into mutations within cells? Oncogene, 21, 8957-8966.
47. 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.
48. Silvian, L.F., Toth, E.A., Pham, P., Goodman, M.F. and Ellenberger, T. (2001) Crystal structure of a DinB family error-prone DNA polymerase from Sulfolobus solfataricus. Nat. Struct. Biol., 8, 984-989.
49. Sutton, M.D., Kim, M. and Walker, G.C. (2001) Genetic and biochemical characterization of a novel umuD mutation: insights into a mechanism for UmuD self-cleavage. J. Bacteriol., 183, 347-357.
50. Tang, M., Shen, X., Frank, E.G., O'Donnell, M., Woodgate, R. and Goodman, M.F. (1999) UmuD′(2)C is an error-prone DNA polymerase, Escherichia coli pol V. Proc. Natl Acad. Sci. USA, 96, 8919-8924.
51. 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 SOS mutagenesis. Nature, 404, 1014-1018.
52. Trincao, J., Johnson, R.E., Escalante, C.R., Prakash, S., Prakash, L. and Aggarwal, A.K. (2001) Structure of the catalytic core of S. cerevisiae DNA polymerase η: implications for translesion DNA synthesis. Mol. Cell, 8, 417-426.
53. van Steeg, H. and Kraemer, K.H. (1999) Xeroderma pigmentosum and the role of UV-induced DNA damage in skin cancer. Mol. Med. Today, 5, 86-94.
54. Wagner, J., Gruz, P., Kim, S.R., Yamada, M., Matsui, K., Fuchs, R.P. and Nohmi, T. (1999) The dinB gene encodes a novel E.coli DNA polymerase, DNA pol IV, involved in mutagenesis. Mol. Cell, 4, 281-286.
55. Wagner, J., Fujii, S., Gruz, P., Nohmi, T. and Fuchs, R.P. (2000) The β clamp targets DNA polymerase IV to DNA and strongly increases its processivity. EMBO Rep., 1, 484-488.
56. Woodgate, R., Singh, M., Kulaeva, O.I., Frank, E.G., Levine, A.S. and Koch, W.H. (1994) Isolation and characterization of novel plasmid-encoded umuC mutants. J. Bacteriol., 176, 5011-5021.
57. Zhang, Y., Yuan, F., Wu, X., Wang, M., Rechkoblit, O., Taylor, J.S., Geacintov, N.E. and Wang, Z. (2000) Error-free and error-prone lesion bypass by human DNA polymerase κ in vitro. Nucleic Acids Res., 28, 4138-4146.