Processivity factor of DNA polymerase and its expanding role in normal and translesion DNA synthesis

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1804, Issue 5, 2010, Pages 1081-1093

  Zhuang, Zhihao ^a   Ai, Yongxing ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

Clamp loader; DNA polymerase; PCNA; Polymerase exchange; Translesion DNA synthesis

Indexed keywords

DNA POLYMERASE;

BACTERIOPHAGE; DNA REPAIR; DNA REPLICATION; DNA STRUCTURE; DNA SYNTHESIS; ESCHERICHIA COLI; EUKARYOTE; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ANIMALS; DNA; DNA REPAIR; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; HUMANS;

EID: 77949570096     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2009.06.018     Document Type: Review

References (135)

1. Yao N.Y., and O'Donnell M. Replisome dynamics and use of DNA trombone loops to bypass replication blocks. Mol. Biosyst. 4 (2008) 1075-1084
2. Benkovic S.J., Valentine A.M., and Salinas F. Replisome-mediated DNA replication. Annu. Rev. Biochem. 70 (2001) 181-208
3. Garg P., and Burgers P.M. DNA polymerases that propagate the eukaryotic DNA replication fork. Crit. Rev. Biochem. Mol. Biol. 40 (2005) 115-128
4. Frouin I., Montecucco A., Spadari S., and Maga G. DNA replication: a complex matter. EMBO Rep. 4 (2003) 666-670
5. Kunkel T.A., and Burgers P.M. Dividing the workload at a eukaryotic replication fork. Trends Cell Biol. 18 (2008) 521-527
6. Johnson A., and O'Donnell M. Cellular DNA replicases: components and dynamics at the replication fork. Annu. Rev. Biochem. 74 (2005) 283-315
7. McCulloch S.D., and Kunkel T.A. The fidelity of DNA synthesis by eukaryotic replicative and translesion synthesis polymerases. Cell Res. 18 (2008) 148-161
8. Joyce C.M., and Benkovic S.J. DNA polymerase fidelity: kinetics, structure, and checkpoints. Biochemistry 43 (2004) 14317-14324
9. Stukenberg P.T., Studwell-Vaughan P.S., and O'Donnell M. Mechanism of the sliding beta-clamp of DNA polymerase III holoenzyme. J. Biol. Chem. 266 17 (1991) 11328-11334
10. Capson T.L., Peliska J.A., Kaboord B.F., Frey M.W., Lively C., Dahlberg M., and Benkovic S.J. Kinetic characterization of the polymerase and exonuclease activities of the gene 43 protein of bacteriophage T4. Biochemistry 31 (1992) 10984-10994
11. Kamtekar S., Berman A.J., Wang J., Lazaro J.M., de Vega M., Blanco L., Salas M., and Steitz T.A. Insights into strand displacement and processivity from the crystal structure of the protein-primed DNA polymerase of bacteriophage phi29. Mol. Cell 16 (2004) 609-618
12. Mace D.C., and Alberts B.M. T4 DNA polymerase: rates and processivity on single-stranded DNA templates. J. Mol. Biol. 177 (1984) 295-311
13. Yang J., Zhuang Z., Roccasecca R.M., Trakselis M.A., and Benkovic S.J. The dynamic processivity of the T4 DNA polymerase during replication. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 8289-8294
14. Zhuang Z., Johnson R.E., Haracska L., Prakash L., Prakash S., and Benkovic S.J. Regulation of polymerase exchange between Poleta and Poldelta by monoubiquitination of PCNA and the movement of DNA polymerase holoenzyme. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 5361-5366
15. Langston L.D., and O'Donnell M. DNA polymerase delta is highly processive with proliferating cell nuclear antigen and undergoes collision release upon completing DNA. J. Biol. Chem. 283 (2008) 29522-29531
16. Burgers P.M. Saccharomyces cerevisiae replication factor C. II. Formation and activity of complexes with the proliferating cell nuclear antigen and with DNA polymerases delta and epsilon. J. Biol. Chem. 266 33 (1991) 22698-22706
17. Himawan J.S., and Richardson C.C. Amino acid residues critical for the interaction between bacteriophage T7 DNA polymerase and Escherichia coli thioredoxin. J. Biol. Chem. 271 (1996) 19999-20008
18. Ghosh S., Hamdan S.M., Cook T.E., and Richardson C.C. Interactions of Escherichia coli thioredoxin, the processivity factor, with bacteriophage T7 DNA polymerase and helicase. J. Biol. Chem. 283 (2008) 32077-32084
19. Kong X.P., Onrust R., O'Donnell M., and Kuriyan J. Three-dimensional structure of the beta subunit of E. coli DNA polymerase III holoenzyme: a sliding DNA clamp. Cell 69 (1992) 425-437
20. Moarefi I., Jeruzalmi D., Turner J., O'Donnell M., and Kuriyan J. Crystal structure of the DNA polymerase processivity factor of T4 bacteriophage. J. Mol. Biol. 296 (2000) 1215-1223
21. Shamoo Y., and Steitz T.A. 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
22. Argiriadi M.A., Goedken E.R., Bruck I., O'Donnell M., and Kuriyan J. Crystal structure of a DNA polymerase sliding clamp from a Gram-positive bacterium. BMC Struct. Biol. 6 (2006) 2
23. Krishna T.S., Kong X.P., Gary S., Burgers P.M., and Kuriyan J. Crystal structure of the eukaryotic DNA polymerase processivity factor PCNA. Cell 79 (1994) 1233-1243
24. Gulbis J.M., Kelman Z., Hurwitz J., O'Donnell M., and Kuriyan J. Structure of the C-terminal region of p21(WAF1/CIP1) complexed with human PCNA. Cell 87 (1996) 297-306
25. Matsumiya S., Ishino Y., and Morikawa K. Crystal structure of an archaeal DNA sliding clamp: proliferating cell nuclear antigen from Pyrococcus furiosus. Protein Sci. 10 (2001) 17-23
26. Williams G.J., Johnson K., Rudolf J., McMahon S.A., Carter L., Oke M., Liu H., Taylor G.L., White M.F., and Naismith J.H. Structure of the heterotrimeric PCNA from Sulfolobus solfataricus. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 62 (2006) 944-948
27. Appleton B.A., Brooks J., Loregian A., Filman D.J., Coen D.M., and Hogle J.M. Crystal structure of the cytomegalovirus DNA polymerase subunit UL44 in complex with the C terminus from the catalytic subunit. Differences in structure and function relative to unliganded UL44. J. Biol. Chem. 281 (2006) 5224-5232
28. Zuccola H.J., Filman D.J., Coen D.M., and Hogle J.M. The crystal structure of an unusual processivity factor, herpes simplex virus UL42, bound to the C terminus of its cognate polymerase. Mol. Cell 5 (2000) 267-278
29. Kuriyan J., and O'Donnell M. Sliding clamps of DNA polymerases. J. Mol. Biol. 234 (1993) 915-925
30. Yao N., Turner J., Kelman Z., Stukenberg P.T., Dean F., Shechter D., Pan Z.Q., Hurwitz J., and O'Donnell M. Clamp loading, unloading and intrinsic stability of the PCNA, beta and gp45 sliding clamps of human, E. coli and T4 replicases. Genes Cells 1 (1996) 101-113
31. Moldovan G.L., Pfander B., and Jentsch S. PCNA, the maestro of the replication fork. Cell 129 (2007) 665-679
32. Maga G., and Hubscher U. Proliferating cell nuclear antigen (PCNA): a dancer with many partners. J. Cell. Sci. 116 (2003) 3051-3060
33. Bruning J.B., and Shamoo Y. Structural and thermodynamic analysis of human PCNA with peptides derived from DNA polymerase-delta p66 subunit and flap endonuclease-1. Structure 12 (2004) 2209-2219
34. Venclovas C., and Thelen M.P. Structure-based predictions of Rad1, Rad9, Hus1 and Rad17 participation in sliding clamp and clamp-loading complexes. Nucleic Acids Res. 28 (2000) 2481-2493
35. Lindsey-Boltz L.A., Bermudez V.P., Hurwitz J., and Sancar A. Purification and characterization of human DNA damage checkpoint Rad complexes. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 11236-11241
36. Shiomi Y., Shinozaki A., Nakada D., Sugimoto K., Usukura J., Obuse C., and Tsurimoto T. Clamp and clamp loader structures of the human checkpoint protein complexes, Rad9-1-1 and Rad17-RFC. Genes Cells 7 (2002) 861-868
37. Griffith J.D., Lindsey-Boltz L.A., and Sancar A. Structures of the human Rad17-replication factor C and checkpoint Rad 9-1-1 complexes visualized by glycerol spray/low voltage microscopy. J. Biol. Chem. 277 (2002) 15233-15236
38. Kaur R., Kostrub C.F., and Enoch T. Structure-function analysis of fission yeast Hus1-Rad1-Rad9 checkpoint complex. Mol. Biol. Cell 12 (2001) 3744-3758
39. Majka J., and Burgers P.M. Yeast Rad17/Mec3/Ddc1: a sliding clamp for the DNA damage checkpoint. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 2249-2254
40. Dore A.S., Kilkenny M.L., Rzechorzek N.J., and Pearl L.H. Crystal structure of the Rad9-Rad1-Hus1 DNA damage checkpoint complex-implications for clamp loading and regulation. Mol. Cell 34 (2009) 735-745
41. Dionne I., Nookala R.K., Jackson S.P., Doherty A.J., and Bell S.D. A heterotrimeric PCNA in the hyperthermophilic archaeon Sulfolobus solfataricus. Mol. Cell 11 (2003) 275-282
42. Pascal J.M., Tsodikov O.V., Hura G.L., Song W., Cotner E.A., Classen S., Tomkinson A.E., Tainer J.A., and Ellenberger T. A flexible interface between DNA ligase and PCNA supports conformational switching and efficient ligation of DNA. Mol. Cell 24 (2006) 279-291
43. Hlinkova V., Xing G., Bauer J., Shin Y.J., Dionne I., Rajashankar K.R., Bell S.D., and Ling H. Structures of monomeric, dimeric and trimeric PCNA: PCNA-ring assembly and opening. Acta Crystallogr. D Biol. Crystallogr. 64 (2008) 941-949
44. Pages V., and Fuchs R.P. How DNA lesions are turned into mutations within cells?. Oncogene 21 (2002) 8957-8966
45. Chow C.S., and Coen D.M. Mutations that specifically impair the DNA binding activity of the herpes simplex virus protein UL42. J. Virol. 69 (1995) 6965-6971
46. Randell J.C., and Coen D.M. Linear diffusion on DNA despite high-affinity binding by a DNA polymerase processivity factor. Mol. Cell 8 (2001) 911-920
47. Loregian A., Appleton B.A., Hogle J.M., and Coen D.M. Specific residues in the connector loop of the human cytomegalovirus DNA polymerase accessory protein UL44 are crucial for interaction with the UL54 catalytic subunit. J. Virol. 78 (2004) 9084-9092
48. Appleton B.A., Loregian A., Filman D.J., Coen D.M., and Hogle J.M. The cytomegalovirus DNA polymerase subunit UL44 forms a C clamp-shaped dimer. Mol. Cell 15 (2004) 233-244
49. Franklin M.C., Wang J., and Steitz T.A. Structure of the replicating complex of a pol alpha family DNA polymerase. Cell 105 (2001) 657-667
50. Johansson E., Garg P., and Burgers P.M. The Pol32 subunit of DNA polymerase delta contains separable domains for processive replication and proliferating cell nuclear antigen (PCNA) binding. J. Biol. Chem. 279 (2004) 1907-1915
51. Furukohri A., Goodman M.F., and Maki H. A dynamic polymerase exchange with Escherichia coli DNA polymerase IV replacing DNA polymerase III on the sliding clamp. J. Biol. Chem. 283 (2008) 11260-11269
52. Indiani C., McInerney P., Georgescu R., Goodman M.F., and O'Donnell M. A sliding-clamp toolbelt binds high- and low-fidelity DNA polymerases simultaneously. Mol. Cell 19 (2005) 805-815
53. Prakash S., Johnson R.E., and Prakash L. Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu. Rev. Biochem. 74 (2005) 317-353
54. Haracska L., Kondratick C.M., Unk I., Prakash S., and Prakash L. Interaction with PCNA is essential for yeast DNA polymerase eta function. Mol. Cell 8 (2001) 407-415
55. Acharya N., Yoon J.H., Gali H., Unk I., Haracska L., Johnson R.E., Hurwitz J., Prakash L., and Prakash S. Roles of PCNA-binding and ubiquitin-binding domains in human DNA polymerase eta in translesion DNA synthesis. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 17724-17729
56. Hishiki A., Hashimoto H., Hanafusa T., Kamei K., Ohashi E., Shimizu T., Ohmori H., and Sato M. Structural basis for novel interactions between human translesion synthesis polymerases and PCNA. J. Biol. Chem. (2009)
57. Zhang H., Gibbs P.E., and Lawrence C.W. The Saccharomyces cerevisiae rev6-1 mutation, which inhibits both the lesion bypass and the recombination mode of DNA damage tolerance, is an allele of POL30, encoding proliferating cell nuclear antigen. Genetics 173 (2006) 1983-1989
58. Freudenthal B.D., Ramaswamy S., Hingorani M.M., and Washington M.T. Structure of a mutant form of proliferating cell nuclear antigen that blocks translesion DNA synthesis. Biochemistry 47 (2008) 13354-13361
59. Xing G., Kirouac K., Shin Y.J., Bell S.D., and Ling H. Structural insight into recruitment of translesion DNA polymerase Dpo4 to sliding clamp PCNA. Mol. Microbiol. 71 (2009) 678-691
60. Bunting K.A., Roe S.M., and Pearl L.H. Structural basis for recruitment of translesion DNA polymerase Pol IV/DinB to the beta-clamp. EMBO J. 22 (2003) 5883-5892
61. Georgescu R.E., Kim S.S., Yurieva O., Kuriyan J., Kong X.P., and O'Donnell M. Structure of a sliding clamp on DNA. Cell 132 (2008) 43-54
62. Laurence T.A., Kwon Y., Johnson A., Hollars C.W., O'Donnell M., Camarero J.A., and Barsky D. Motion of a DNA sliding clamp observed by single molecule fluorescence spectroscopy. J. Biol. Chem. 283 (2008) 22895-22906
63. Ivanov I., Chapados B.R., McCammon J.A., and Tainer J.A. Proliferating cell nuclear antigen loaded onto double-stranded DNA: dynamics, minor groove interactions and functional implications. Nucleic Acids Res. 34 (2006) 6023-6033
64. Mayanagi K., Kiyonari S., Saito M., Shirai T., Ishino Y., and Morikawa K. Mechanism of replication machinery assembly as revealed by the DNA ligase-PCNA-DNA complex architecture. Proc. Natl. Acad. Sci. U. S. A. (2009)
65. Neuwald A.F., Aravind L., Spouge J.L., and Koonin E.V. AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res. 9 (1999) 27-43
66. Smiley R.D., Zhuang Z., Benkovic S.J., and Hammes G.G. Single-molecule investigation of the T4 bacteriophage DNA polymerase holoenzyme: multiple pathways of holoenzyme formation. Biochemistry 45 (2006) 7990-7997
67. Zhuang Z., Berdis A.J., and Benkovic S.J. An alternative clamp loading pathway via the T4 clamp loader gp44/62-DNA complex. Biochemistry 45 (2006) 7976-7989
68. Millar D., Trakselis M.A., and Benkovic S.J. On the solution structure of the T4 sliding clamp (gp45). Biochemistry 43 (2004) 12723-12727
69. Trakselis M.A., Berdis A.J., and Benkovic S.J. Examination of the role of the clamp-loader and ATP hydrolysis in the formation of the bacteriophage T4 polymerase holoenzyme. J. Mol. Biol. 326 (2003) 435-451
70. Alley S.C., Abel-Santos E., and Benkovic S.J. Tracking sliding clamp opening and closing during bacteriophage T4 DNA polymerase holoenzyme assembly. Biochemistry 39 (2000) 3076-3090
71. Alley S.C., Shier V.K., Abel-Santos E., Sexton D.J., Soumillion P., and Benkovic S.J. Sliding clamp of the bacteriophage T4 polymerase has open and closed subunit interfaces in solution. Biochemistry 38 (1999) 7696-7709
72. Pietroni P., and von Hippel P.H. Multiple ATP binding is required to stabilize the "activated" (clamp open) clamp loader of the T4 DNA replication complex. J. Biol. Chem. 283 (2008) 28338-28353
73. Latham G.J., Dong F., Pietroni P., Dozono J.M., Bacheller D.J., and von Hippel P.H. Opening of a monomer-monomer interface of the trimeric bacteriophage T4-coded GP45 sliding clamp is required for clamp loading onto DNA. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 12448-12453
74. Latham G.J., Bacheller D.J., Pietroni P., and von Hippel P.H. Structural analyses of gp45 sliding clamp interactions during assembly of the bacteriophage T4 DNA polymerase holoenzyme. III. The Gp43 DNA polymerase binds to the same face of the sliding clamp as the clamp loader. J. Biol. Chem. 272 (1997) 31685-31692
75. Latham G.J., Bacheller D.J., Pietroni P., and von Hippel P.H. Structural analyses of gp45 sliding clamp interactions during assembly of the bacteriophage T4 DNA polymerase holoenzyme. II. The Gp44/62 clamp loader interacts with a single defined face of the sliding clamp ring. J. Biol. Chem. 272 (1997) 31677-31684
76. Pietroni P., Young M.C., Latham G.J., and von Hippel P.H. Structural analyses of gp45 sliding clamp interactions during assembly of the bacteriophage T4 DNA polymerase holoenzyme. I. Conformational changes within the gp44/62-gp45-ATP complex during clamp loading. J. Biol. Chem. 272 (1997) 31666-31676
77. Pietroni P., Young M.C., Latham G.J., and von Hippel P.H. Dissection of the ATP-driven reaction cycle of the bacteriophage T4 DNA replication processivity clamp loading system. J. Mol. Biol. 309 (2001) 869-891
78. Ason B., Handayani R., Williams C.R., Bertram J.G., Hingorani M.M., O'Donnell M., Goodman M.F., and Bloom L.B. 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
79. Anderson S.G., Williams C.R., O'Donnell M., and Bloom L.B. A function for the psi subunit in loading the Escherichia coli DNA polymerase sliding clamp. J. Biol. Chem. 282 (2007) 7035-7045
80. Bertram J.G., Bloom L.B., O'Donnell M., and Goodman M.F. Increased dNTP binding affinity reveals a nonprocessive role for Escherichia coli beta clamp with DNA polymerase IV. J. Biol. Chem. 279 (2004) 33047-33050
81. Snyder A.K., Williams C.R., Johnson A., O'Donnell M., and Bloom L.B. Mechanism of loading the Escherichia coli DNA polymerase III sliding clamp: II. Uncoupling the beta and DNA binding activities of the gamma complex. J. Biol. Chem. 279 (2004) 4386-4393
82. Williams C.R., Snyder A.K., Kuzmic P., O'Donnell M., and Bloom L.B. Mechanism of loading the Escherichia coli DNA polymerase III sliding clamp: I. Two distinct activities for individual ATP sites in the gamma complex. J. Biol. Chem. 279 (2004) 4376-4385
83. Bertram J.G., Bloom L.B., Hingorani M.M., Beechem J.M., O'Donnell M., and Goodman M.F. Molecular mechanism and energetics of clamp assembly in Escherichia coli. The role of ATP hydrolysis when gamma complex loads beta on DNA. J. Biol. Chem. 275 (2000) 28413-28420
84. Ason B., Bertram J.G., Hingorani M.M., Beechem J.M., O'Donnell M., Goodman M.F., and Bloom L.B. 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 (2000) 3006-3015
85. Chen S., Coman M.M., Sakato M., O'Donnell M., and Hingorani M.M. Conserved residues in the delta subunit help the E. coli clamp loader, gamma complex, target primer-template DNA for clamp assembly. Nucleic Acids Res. 36 (2008) 3274-3286
86. Magdalena Coman M., Jin M., Ceapa R., Finkelstein J., O'Donnell M., Chait B.T., and Hingorani M.M. Dual functions, clamp opening and primer-template recognition, define a key clamp loader subunit. J. Mol. Biol. 342 (2004) 1457-1469
87. Gomes X.V., and Burgers P.M. ATP utilization by yeast replication factor C. I. ATP-mediated interaction with DNA and with proliferating cell nuclear antigen. J. Biol. Chem. 276 (2001) 34768-34775
88. Gomes X.V., Schmidt S.L., and Burgers P.M. ATP utilization by yeast replication factor C. II. Multiple stepwise ATP binding events are required to load proliferating cell nuclear antigen onto primed DNA. J. Biol. Chem. 276 (2001) 34776-34783
89. Schmidt S.L., Gomes X.V., and Burgers P.M. ATP utilization by yeast replication factor C. III. The ATP-binding domains of Rfc2, Rfc3, and Rfc4 are essential for DNA recognition and clamp loading. J. Biol. Chem. 276 (2001) 34784-34791
90. Yao N., Coryell L., Zhang D., Georgescu R.E., Finkelstein J., Coman M.M., Hingorani M.M., and O'Donnell M. Replication factor C clamp loader subunit arrangement within the circular pentamer and its attachment points to proliferating cell nuclear antigen. J. Biol. Chem. 278 (2003) 50744-50753
91. Yao N.Y., Johnson A., Bowman G.D., Kuriyan J., and O'Donnell M. Mechanism of proliferating cell nuclear antigen clamp opening by replication factor C. J. Biol. Chem. 281 (2006) 17528-17539
92. Johnson A., Yao N.Y., Bowman G.D., Kuriyan J., and O'Donnell M. The replication factor C clamp loader requires arginine finger sensors to drive DNA binding and proliferating cell nuclear antigen loading. J. Biol. Chem. 281 (2006) 35531-35543
93. Zhuang Z., Yoder B.L., Burgers P.M., and Benkovic S.J. The structure of a ring-opened proliferating cell nuclear antigen-replication factor C complex revealed by fluorescence energy transfer. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 2546-2551
94. Uhlmann F., Cai J., Gibbs E., O'Donnell M., and Hurwitz J. Deletion analysis of the large subunit p140 in human replication factor C reveals regions required for complex formation and replication activities. J. Biol. Chem. 272 (1997) 10058-10064
95. Uhlmann F., Gibbs E., Cai J., O'Donnell M., and Hurwitz J. Identification of regions within the four small subunits of human replication factor C required for complex formation and DNA replication. J. Biol. Chem. 272 (1997) 10065-10071
96. Cai J., Gibbs E., Uhlmann F., Phillips B., Yao N., O'Donnell M., and Hurwitz J. A complex consisting of human replication factor C p40, p37, and p36 subunits is a DNA-dependent ATPase and an intermediate in the assembly of the holoenzyme. J. Biol. Chem. 272 (1997) 18974-18981
97. Zhang G., Gibbs E., Kelman Z., O'Donnell M., and Hurwitz J. Studies on the interactions between human replication factor C and human proliferating cell nuclear antigen. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 1869-1874
98. Seybert A., Singleton M.R., Cook N., Hall D.R., and Wigley D.B. Communication between subunits within an archaeal clamp-loader complex. EMBO J. 25 (2006) 2209-2218
99. Seybert A., and Wigley D.B. Distinct roles for ATP binding and hydrolysis at individual subunits of an archaeal clamp loader. EMBO J. 23 (2004) 1360-1371
100. Seybert A., Scott D.J., Scaife S., Singleton M.R., and Wigley D.B. Biochemical characterisation of the clamp/clamp loader proteins from the euryarchaeon Archaeoglobus fulgidus. Nucleic Acids Res. 30 (2002) 4329-4338
101. Pisani F.M., De Felice M., Carpentieri F., and Rossi M. Biochemical characterization of a clamp-loader complex homologous to eukaryotic replication factor C from the hyperthermophilic archaeon Sulfolobus solfataricus. J. Mol. Biol. 301 (2000) 61-73
102. Hingorani M.M., and O'Donnell M. 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
103. Trakselis M.A., Alley S.C., Abel-Santos E., and Benkovic S.J. Creating a dynamic picture of the sliding clamp during T4 DNA polymerase holoenzyme assembly by using fluorescence resonance energy transfer. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 8368-8375
104. Chen S., Levin M.K., Sakato M., Zhou Y., and Hingorani M.M. Mechanism of ATP-driven PCNA clamp loading by S. cerevisiae RFC. J. Mol. Biol. 388 (2009) 431-442
105. Davey M.J., Jeruzalmi D., Kuriyan J., and O'Donnell M. Motors and switches: AAA+ machines within the replisome. Nat. Rev. Mol. Cell Biol. 3 (2002) 826-835
106. Bowman G.D., O'Donnell M., and Kuriyan J. Structural analysis of a eukaryotic sliding DNA clamp-clamp loader complex. Nature 429 (2004) 724-730
107. Goedken E.R., Kazmirski S.L., Bowman G.D., O'Donnell M., and Kuriyan J. Mapping the interaction of DNA with the Escherichia coli DNA polymerase clamp loader complex. Nat. Struct. Mol. Biol. 12 (2005) 183-190
108. Simonetta K.R., Kazmirski S.L., Goedken E.R., Cantor A.J., Kelch B.A., McNally R., Seyedin S.N., Makino D.L., O'Donnell M., and Kuriyan J. The mechanism of ATP-dependent primer-template recognition by a clamp loader complex. Cell 137 (2009) 659-671
109. Jeruzalmi D., O'Donnell M., and Kuriyan J. Crystal structure of the processivity clamp loader gamma (gamma) complex of E. coli DNA polymerase III. Cell 106 (2001) 429-441
110. Kazmirski S.L., Podobnik M., Weitze T.F., O'Donnell M., and Kuriyan J. Structural analysis of the inactive state of the Escherichia coli DNA polymerase clamp-loader complex. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 16750-16755
111. Burgers P.M. Saccharomyces cerevisiae replication factor C. II. Formation and activity of complexes with the proliferating cell nuclear antigen and with DNA polymerases delta and epsilon. J. Biol. Chem. 266 (1991) 22698-22706
112. Tsurimoto T., and Stillman B. Replication factors required for SV40 DNA replication in vitro. I. DNA structure-specific recognition of a primer-template junction by eukaryotic DNA polymerases and their accessory proteins. J. Biol. Chem. 266 (1991) 1950-1960
113. Miyata T., Oyama T., Mayanagi K., Ishino S., Ishino Y., and Morikawa K. The clamp-loading complex for processive DNA replication. Nat. Struct. Mol. Biol. 11 (2004) 632-636
114. Miyata T., Suzuki H., Oyama T., Mayanagi K., Ishino Y., and Morikawa K. Open clamp structure in the clamp-loading complex visualized by electron microscopic image analysis. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 13795-13800
115. Kazmirski S.L., Zhao Y., Bowman G.D., O'Donnell M., and Kuriyan J. Out-of-plane motions in open sliding clamps: molecular dynamics simulations of eukaryotic and archaeal proliferating cell nuclear antigen. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 13801-13806
116. Dionne I., Brown N.J., Woodgate R., and Bell S.D. On the mechanism of loading the PCNA sliding clamp by RFC. Mol. Microbiol. 68 (2008) 216-222
117. Johnson D.E., Takahashi M., Hamdan S.M., Lee S.J., and Richardson C.C. Exchange of DNA polymerases at the replication fork of bacteriophage T7. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 5312-5317
118. Hoege C., Pfander B., Moldovan G.L., Pyrowolakis G., and Jentsch S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419 (2002) 135-141
119. Stelter P., and Ulrich H.D. Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature 425 (2003) 188-191
120. Pfander B., Moldovan G.L., Sacher M., Hoege C., and Jentsch S. SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 436 (2005) 428-433
121. Papouli E., Chen S., Davies A.A., Huttner D., Krejci L., Sung P., and Ulrich H.D. Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. Mol. Cell 19 (2005) 123-133
122. Krejci L., Damborsky J., Thomsen B., Duno M., and Bendixen C. Molecular dissection of interactions between Rad51 and members of the recombination-repair group. Mol. Cell. Biol. 21 (2001) 966-976
123. Veaute X., Jeusset J., Soustelle C., Kowalczykowski S.C., Le Cam E., and Fabre F. The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423 (2003) 309-312
124. Watanabe K., Tateishi S., Kawasuji M., Tsurimoto T., Inoue H., and Yamaizumi M. Rad18 guides poleta to replication stalling sites through physical interaction and PCNA monoubiquitination. EMBO J. 23 (2004) 3886-3896
125. Kannouche P.L., Wing J., and Lehmann A.R. Interaction of human DNA polymerase eta with monoubiquitinated PCNA: a possible mechanism for the polymerase switch in response to DNA damage. Mol. Cell 14 (2004) 491-500
126. Plosky B.S., Vidal A.E., Fernandez de Henestrosa A.R., McLenigan M.P., McDonald J.P., Mead S., and Woodgate R. Controlling the subcellular localization of DNA polymerases iota and eta via interactions with ubiquitin. EMBO J. 25 (2006) 2847-2855
127. Parker J.L., Bielen A.B., Dikic I., and Ulrich H.D. Contributions of ubiquitin- and PCNA-binding domains to the activity of Polymerase eta in Saccharomyces cerevisiae. Nucleic Acids Res. 35 (2007) 881-889
128. Guo C., Sonoda E., Tang T.S., Parker J.L., Bielen A.B., Takeda S., Ulrich H.D., and Friedberg E.C. REV1 protein interacts with PCNA: significance of the REV1 BRCT domain in vitro and in vivo. Mol. Cell 23 (2006) 265-271
129. Wood A., Garg P., and Burgers P.M. A ubiquitin-binding motif in the translesion DNA polymerase Rev1 mediates its essential functional interaction with ubiquitinated proliferating cell nuclear antigen in response to DNA damage. J. Biol. Chem. 282 (2007) 20256-20263
130. Guo C., Tang T.S., Bienko M., Dikic I., and Friedberg E.C. Requirements for the interaction of mouse Polkappa with ubiquitin and its biological significance. J. Biol. Chem. 283 (2008) 4658-4664
131. Prakash S., and Prakash L. Translesion DNA synthesis in eukaryotes: a one- or two-polymerase affair. Genes Dev. 16 (2002) 1872-1883
132. Waters L.S., Minesinger B.K., Wiltrout M.E., D'Souza S., Woodruff R.V., and Walker G.C. Eukaryotic translesion polymerases and their roles and regulation in DNA damage tolerance. Microbiol. Mol. Biol. Rev. 73 (2009) 134-154
133. Huang T.T., Nijman S.M., Mirchandani K.D., Galardy P.J., Cohn M.A., Haas W., Gygi S.P., Ploegh H.L., Bernards R., and D'Andrea A.D. Regulation of monoubiquitinated PCNA by DUB autocleavage. Nat. Cell Biol. 8 (2006) 339-347
134. Cohn M.A., Kowal P., Yang K., Haas W., Huang T.T., Gygi S.P., and D'Andrea A.D. A UAF1-containing multisubunit protein complex regulates the Fanconi anemia pathway. Mol Cell 28 (2007) 786-797
135. Niimi A., Brown S., Sabbioneda S., Kannouche P.L., Scott A., Yasui A., Green C.M., and Lehmann A.R. Regulation of proliferating cell nuclear antigen ubiquitination in mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 16125-16130