The RFC clamp loader: Structure and Function

Subcellular Biochemistry

Volumn 62, Issue , 2012, Pages 259-279

  Yao, Nina Y ^a   O’Donnell, Mike ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

AAA+ machine; Clamp loader; DNA polymerase; PCNA; Replisome; RFC; Sliding clamp

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; CYCLINE; DNA BINDING PROTEIN;

ANIMAL; CHEMISTRY; GENETICS; HUMAN; HYDROLYSIS; METABOLISM; PROTEIN TERTIARY STRUCTURE; REVIEW;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ANIMALS; DNA-BINDING PROTEINS; HUMANS; HYDROLYSIS; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN STRUCTURE, TERTIARY;

EID: 84873118328     PISSN: 03060225     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-94-007-4572-8_14     Document Type: Article

References (81)

1. Ason B, Handayani R, Williams CR, Bertram JG, Hingorani MM, O'Donnell M, Goodman MF, Bloom LB (2003) Mechanism of loading the Escherichia coli DNA polymerase III DDsliding clamp on DNA. Bonafide primer/templates preferentially trigger the//complex to hydrolyze ATP and load the clamp. J Biol Chem 278: 10033-10040.
2. Ayyagari R, Impellizzeri KJ, Yoder BL, Gary SL, Burgers PM (1995) A mutational analysis of the yeast proliferating cell nuclear antigen indicates distinct roles in DNA replication and DNA repair. Mol Cell Biol 15: 4420-4429.
3. Ayyagari R, Gomes XV, Gordenin DA, Burgers PM (2003) Okazaki fragment maturation in yeast. I. Distribution of functions between FEN1 AND DNA2. J Biol Chem 278: 1618-1625.
4. Bellaoui M, Chang M, Ou J, Xu H, Boone C, Brown GW (2003) Elg1 forms an alternative RFC complex important for DNA replication and genome integrity. EMBO J 22: 4304-4313.
5. Ben-Aroya S, Koren A, Liefshitz B, Steinlauf R, Kupiec M (2003) ELG1, a yeast gene required for genome stability, forms a complex related to replication factor C. Proc Natl Acad Sci U S A 100: 9906-9911.
6. Benkovic SJ, Valentine AM, Salinas F (2001) Replisome-mediated DNA replication. Annu Rev Biochem 70: 181-208.
7. Bertram JG, Bloom LB, Hingorani MM, Beechem JM, O'Donnell M, Goodman MF (2000) Molecular mechanism and energetics of clamp assembly in Escherichia coli. The role of ATP hydrolysis when hhcomplex loads ccon DNA. J Biol Chem 275: 28413-28420.
8. Bowman GD, O'Donnell M, Kuriyan J (2004) Structural analysis of a eukaryotic sliding DNA clamp-clamp loader complex. Nature 429: 724-730.
9. Bowman GD, Goedken ER, Kazmirski SL, O'Donnell M, Kuriyan J (2005) DNA polymerase clamp loaders and DNA recognition. FEBS Lett 579: 863-867.
10. Bunting KA, Roe SM, Pearl LH (2003) Structural basis for recruitment of translesion DNA polymerase Pol IV/DinB to the//-clamp. EMBO J 22: 5883-5892.
11. Bunz F, Kobayashi R, Stillman B (1993) cDNAs encoding the large subunit of human replication factor C. Proc Natl Acad Sci U S A 90: 11014-11018.
12. Bylund GO, Burgers PM (2005) Replication protein A-directed unloading of PCNA by the Ctf18 cohesion establishment complex. Mol Cell Biol 25: 5445-5455.
13. Cai J, Yao N, Gibbs E, Finkelstein J, Phillips B, O'Donnell M, Hurwitz J (1998) ATP hydrolysis catalyzed by human replication factor C requires participation of multiple subunits. Proc Natl Acad Sci U S A 95: 11607-11612.
14. Cullmann G, Fien K, Kobayashi R, Stillman B (1995) Characterization of thefive replication factor C genes of Saccharomyces cerevisiae. Mol Cell Biol 15: 4661-4671.
15. Dalrymple BP, Kongsuwan K, Wijffels G, Dixon NE, Jennings PA (2001) A universal proteinprotein interaction motif in the eubacterial DNA replication and repair systems. Proc Natl Acad Sci U S A 98: 11627-11632.
16. Davey MJ, Jeruzalmi D, Kuriyan J, O'Donnell M (2002) Motors and switches: AAA+ machines within the replisome. Nat Rev Mol Cell Biol 3: 826-835.
17. Dore AS, Kilkenny ML, Jones SA, Oliver AW, Roe SM, Bell SD, Pearl LH (2006) Structure of an archaeal PCNA1-PCNA2-FEN1 complex: elucidating PCNA subunit and client enzyme specificity. Nucleic Acids Res 34: 4515-4526.
18. Eissenberg JC, Ayyagari R, Gomes XV, Burgers PM (1997) Mutations in yeast proliferating cell nuclear antigen define distinct sites for interaction with DNA polymerase nnand DNA polymerase aa. Mol Cell Biol 17: 6367-6378.
19. Ellison V, Stillman B (2003) Biochemical characterization of DNA damage checkpoint complexes: clamp loader and clamp complexes with specificity for 5 ccrecessed DNA. PLoS Biol 1: E33.
20. Erzberger JP, Berger JM (2006) Evolutionary relationships and structural mechanisms of AAA+ proteins. Annu Rev Biophys Biomol Struct 35: 93-114.
21. Fairman M, Prelich G, Tsurimoto T, Stillman B (1988) Identification of cellular components required for SV40 DNA replication in vitro. Biochim Biophys Acta 951: 382-387.
22. Georgescu RE, Kim SS, Yurieva O, Kuriyan J, Kong XP, O'Donnell M (2008) Structure of a sliding clamp on DNA. Cell 132: 43-54.
23. Goedken ER, Kazmirski SL, Bowman GD, O'Donnell M, Kuriyan J (2005) Mapping the interaction of DNA with the Escherichia coli DNA polymerase clamp loader complex. Nat Struct Mol Biol 12: 183-190.
24. Gomes XV, Burgers PM (2000) Two modes of FEN1 binding to PCNA regulated by DNA. EMBO J 19: 3811-3821.
25. Gomes XV, Burgers PM (2001) ATP utilization by yeast replication factor C. I. ATP-mediated interaction with DNA and with proliferating cell nuclear antigen. J Biol Chem 276: 34768-34775.
26. Gomes XV, Gary SL, Burgers PM (2000) Overproduction in Escherichia coli and characterization of yeast replication factor C lacking the ligase homology domain. J Biol Chem 275: 14541-14549.
27. Gomes XV, Schmidt SL, Burgers PM (2001) 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: 34776-34783.
28. Grabowski B, Kelman Z (2003) Archaeal DNA replication: eukaryal proteins in a bacterial context. Annu Rev Microbiol 57: 487-516.
29. Green CM, Erdjument-Bromage H, Tempst P, Lowndes NF (2000) A novel Rad24 checkpoint protein complex closely related to replication factor C. Curr Biol 10: 39-42.
30. Guenther B, Onrust R, Sali A, O'Donnell M, Kuriyan J (1997) Crystal structure of the GGGGsubunit of the clamp-loader complex of E. coli DNA polymerase III. Cell 91: 335-345.
31. WAF1/CIP1 complexed with human PCNA. Cell 87: 297-306.
32. Jeruzalmi D, O'Donnell M, Kuriyan J (2001a) Crystal structure of the processivity clamp loader c complex of E. coli DNA polymerase III. Cell 106: 429-441.
33. Jeruzalmi D, Yurieva O, Zhao Y, Young M, Stewart J, Hingorani M, O'Donnell M, Kuriyan J (2001b) Mechanism of processivity clamp opening by the subunit wrench of the clamp loader complex of E. coli DNA polymerase III. Cell 106: 417-428.
34. Johansson E, Garg P, Burgers PM (2004) The Pol32 subunit of DNA polymerase JJcontains separable domains for processive replication and proliferating cell nuclear antigen (PCNA) binding. J Biol Chem 279: 1907-1915.
35. Johnson A, O'Donnell M (2003) Ordered ATP hydrolysis in the JJcomplex clamp loader AAA+ machine. J Biol Chem 278: 14406-14413.
36. Johnson A, O'Donnell M (2005) Cellular DNA replicases: components and dynamics at the replication fork. Annu Rev Biochem 74: 283-315.
37. Johnson A, Yao NY, Bowman GD, Kuriyan J, O'Donnell M (2006) The replication factor C clamp loader requires argininefinger sensors to drive DNA binding and proliferating cell nuclear antigen loading. J Biol Chem 281: 35531-35543.
38. Jonsson ZO, Hindges R, Hubscher U (1998) Regulation of DNA replication and repair proteins through interaction with the front side of proliferating cell nuclear antigen. EMBO J 17: 2412-2425.
39. Kanellis P, Agyei R, Durocher D (2003) Elg1 forms an alternative PCNA-interacting RFC complex required to maintain genome stability. Curr Biol 13: 1583-1595.
40. Kao HI, Bambara RA (2003) The protein components and mechanism of eukaryotic Okazaki fragment maturation. Crit Rev Biochem Mol Biol 38: 433-452.
41. Kazmirski SL, Zhao Y, Bowman GD, O'Donnell M, Kuriyan J (2005) 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: 13801-13806.
42. Kobayashi M, Ab E, Bonvin AM, Siegal G (2010) Structure of the DNA-bound BRCA1 C-terminal region from human replication factor C p140 and model of the protein-DNA complex. J Biol Chem 285: 10087-10097.
43. Kong XP, Onrust R, O'Donnell M, Kuriyan J (1992) Three-dimensional structure of the KKsubunit of E. coli DNA polymerase III holoenzyme: a sliding DNA clamp. Cell 69: 425-437.
44. Kornberg A, Baker TA (1992) DNA replication. W. H. Freeman, New York.
45. Krishna TS, Kong XP, Gary S, Burgers PM, Kuriyan J (1994) Crystal structure of the eukaryotic DNA polymerase processivity factor PCNA. Cell 79: 1233-1243.
46. Langston LD, O'Donnell M (2008) DNA polymerase LLis highly processive with proliferating cell nuclear antigen and undergoes collision release upon completing DNA. J Biol Chem 283: 29522-29531.
47. Laurence TA, Kwon Y, Johnson A, Hollars CW, O'Donnell M, Camarero JA, Barsky D (2008) Motion of a DNA sliding clamp observed by single moleculefluorescence spectroscopy. J Biol Chem 283: 22895-22906.
48. Lee SH, Eki T, Hurwitz J (1989) Synthesis of DNA containing the simian virus 40 origin of replication by the combined action of DNA polymerases bband aa. Proc Natl Acad Sci U S A 86: 7361-7365.
49. Leu FP, Hingorani MM, Turner J, O'Donnell M (2000) The LLsubunit of DNA polymerase III holoenzyme serves as a sliding clamp unloader in Escherichia coli. J Biol Chem 275: 34609-34618.
50. Lindsey-Boltz LA, Bermudez VP, Hurwitz J, Sancar A (2001) Purification and characterization of human DNA damage checkpoint Rad complexes. Proc Natl Acad Sci U S A 98: 11236-11241.
51. Majka J, Binz SK, Wold MS, Burgers PM (2006a) Replication protein A directs loading of the DNA damage checkpoint clamp to 5-DNA junctions. J Biol Chem 281: 27855-27861.
52. Majka J, Niedziela-Majka A, Burgers PM (2006b) The checkpoint clamp activates Mec1 kinase during initiation of the DNA damage checkpoint. Mol Cell 24: 891-901.
53. Matsumiya S, Ishino Y, Morikawa K (2001) Crystal structure of an archaeal DNA sliding clamp: proliferating cell nuclear antigen from Pyrococcus furiosus. Protein Sci 10: 17-23.
54. Ctf18p, Ctf8p, Dcc1p : an alternative RFC complex required for sister chromatid cohesion in S. cerevisiae. Mol Cell 7: 959-970.
55. McNally R, Bowman GD, Goedken ER, O'Donnell M, Kuriyan J (2010) Analysis of the role of PCNA-DNA contacts during clamp loading. BMC Struct Biol 10: 3.
56. Miyata T, Suzuki H, Oyama T, Mayanagi K, Ishino Y, Morikawa K (2005) Open clamp structure in the clamp-loading complex visualized by electron microscopic image analysis. Proc Natl Acad Sci U S A 102: 13795-13800.
57. Moare fi I, Jeruzalmi D, Turner J, O'Donnell M, Kuriyan J (2000) Crystal structure of the DNA polymerase processivity factor of T4 bacteriophage. J Mol Biol 296: 1215-1223.
58. Naktinis V, Turner J, O'Donnell M (1996) A molecular switch in a replication machine defined by an internal competition for protein rings. Cell 84: 137-145.
59. Neuwald AF, Aravind L, Spouge JL, Koonin EV (1999) AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 9: 27-43.
60. O'Donnell M, Kuriyan J (2006) Clamp loaders and replication initiation. Curr Opin Struct Biol 16: 35-41.
61. O'Donnell M, Onrust R, Dean FB, Chen M, Hurwitz J (1993) Homology in accessory proteins of replicative polymerases: E. coli to humans. Nucleic Acids Res 21: 1-3.
62. Podust VN, Tiwari N, Ott R, Fanning E (1998) Functional interactions among the subunits of replication factor C potentiate and modulate its ATPase activity. J Biol Chem 273: 12935-12942.
63. Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S (2004) Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 73: 39-85.
64. Schmidt SL, Gomes XV, Burgers PM (2001) 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: 34784-34791.
65. Shamoo Y, Steitz TA (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.
66. Simonetta KR, Kazmirski SL, Goedken ER, Cantor AJ, Kelch BA, McNally R, Seyedin SN, Makino DL, O'Donnell M, Kuriyan J (2009) The mechanism of ATP-dependent primer-template recognition by a clamp loader complex. Cell 137: 659-671.
67. Sinha NK, Morris CF, Alberts BM (1980) Efficient in vitro replication of double-stranded DNA templates by a purified T4 bacteriophage replication system. J Biol Chem 255: 4290-4293.
68. Snyder AK, Williams CR, Johnson A, O'Donnell M, Bloom LB (2004) Mechanism of loading the Escherichia coli DNA polymerase III sliding clamp: II. Uncoupling the beta and DNA binding activities of the aacomplex. J Biol Chem 279: 4386-4393.
69. Song W, Pascal JM, Ellenberger T, Tomkinson AE (2009) The DNA binding domain of human DNA ligase I interacts with both nicked DNA and the DNA sliding clamps, PCNA and hRad9-hRad1-hHus1. DNA Repair 8: 912-919.
70. Stewart J, Hingorani MM, Kelman Z, O'Donnell M (2001) Mechanism of HHclamp opening by the ccsubunit of Escherichia coli DNA polymerase III holoenzyme. J Biol Chem 276: 19182-19189.
71. Stukenberg PT, Studwell-Vaughan PS, O'Donnell M (1991) Mechanism of the sliding SS-clamp of DNA polymerase III holoenzyme. J Biol Chem 266: 11328-11334.
72. Turner J, Hingorani MM, Kelman Z, O'Donnell M (1999) The internal workings of a DNA polymerase clamp-loading machine. EMBO J 18: 771-783.
73. Uhlmann F, Cai J, Gibbs E, O'Donnell M, Hurwitz J (1997) 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: 10058-10064.
74. Waga S, Stillman B (1994) Anatomy of a DNA replication fork revealed by reconstitution of SV40 DNA replication in vitro. Nature 369: 207-212.
75. Warbrick E (2000) The puzzle of PCNA's many partners. Bioessays 22: 997-1006.
76. 2 -binding proteins. Biochemistry 43: 5661-5671.
77. Williams CR, Snyder AK, Kuzmic P, O'Donnell M, Bloom LB (2004) Mechanism of loading the Escherichia coli DNA polymerase III sliding clamp: I. Two distinct activities for individual ATP sites in the AAcomplex. J Biol Chem 279: 4376-4385.
78. Yao N, Turner J, Kelman Z, Stukenberg PT, Dean F, Shechter D, Pan ZQ, Hurwitz J, O'Donnell M (1996) Clamp loading, unloading and intrinsic stability of the PCNA, and gp45 sliding clamps of human, E. coli and T4 replicases. Genes Cells 1: 101-113.
79. Yao N, Coryell L, Zhang D, Georgescu RE, Finkelstein J, Coman MM, Hingorani MM, O'Donnell M (2003) Replication factor C clamp loader subunit arrangement within the circular pentamer and its attachment points to proliferating cell nuclear antigen. J Biol Chem 278: 50744-50753.
80. Yao NY, Johnson A, Bowman GD, Kuriyan J, O'Donnell M (2006) Mechanism of proliferating cell nuclear antigen clamp opening by replication factor C. J Biol Chem 281: 17528-17539.
81. Zhuang Z, Yoder BL, Burgers PM, Benkovic SJ (2006) The structure of a ring-opened proliferating cell nuclear antigen-replication factor C complex revealed byfluorescence energy transfer. Proc Natl Acad Sci U S A 103: 2546-2551.