A central swivel point in the RFC clamp loader controls PCNA opening and loading on DNA

Journal of Molecular Biology

Volumn 416, Issue 2, 2012, Pages 163-175

  Sakato, Miho ^a   O'Donnell, Mike ^b   Hingorani, Manju M ^a  

^a WESLEYAN UNIVERSITY   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

arginine finger; ATPase kinetic mechanism; DNA replication; PCNA clamp; RFC clamp loader

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; ARGININE; CYCLINE; MUTANT PROTEIN; PRIMER DNA; REPLICATION FACTOR C;

ARTICLE; BINDING AFFINITY; BIOCATALYSIS; CONTROLLED STUDY; DISSOCIATION; DNA BINDING; DNA TEMPLATE; ESCHERICHIA COLI; MICROBIAL KINETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN INDUCTION; PROTEIN SUBUNIT; SACCHAROMYCES CEREVISIAE; STEADY STATE;

ESCHERICHIA COLI; SACCHAROMYCES CEREVISIAE;

EID: 84856447919     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.12.017     Document Type: Article

References (36)

1. Johnson A., and O'Donnell M. Cellular DNA replicases: components and dynamics at the replication fork Annu. Rev. Biochem. 74 2005 283 315 (Pubitemid 40995509)
2. Moldovan G.L., Pfander B., and Jentsch S. PCNA, the maestro of the replication fork Cell 129 2007 665 679 (Pubitemid 46802385)
3. 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 (Pubitemid 26359007)
4. 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
5. 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 (Pubitemid 38833117)
6. Tainer J.A., McCammon J.A., and Ivanov I. Recognition of the ring-opened state of proliferating cell nuclear antigen by replication factor C promotes eukaryotic clamp-loading J. Am. Chem. Soc. 132 2010 7372 7378
7. 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
8. + proteins Annu. Rev. Biophys. Biomol. Struct. 35 2006 93 114 (Pubitemid 43877371)
9. + proteins: have engine, will work Nat. Rev. Mol. Cell Biol. 6 2005 519 529 (Pubitemid 40943043)
10. + ATPases J. Struct. Biol. 146 2004 11 31 (Pubitemid 38369015)
11. Simonetta K.R., Kazmirski S.L., Goedken E.R., Cantor A.J., Kelch B.A., and McNally R. The mechanism of ATP-dependent primer-template recognition by a clamp loader complex Cell 137 2009 659 671
12. 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 (Pubitemid 32786987)
13. O'Donnell M., and Kuriyan J. Clamp loaders and replication initiation Curr. Opin. Struct. Biol. 16 2006 35 41 (Pubitemid 43221869)
14. Scheffzek K., Ahmadian M.R., Kabsch W., Wiesmuller L., Lautwein A., Schmitz F., and Wittinghofer A. The Ras-RasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants Science 277 1997 333 338 (Pubitemid 27450699)
15. + ATPase for remodeling bacterial RNA polymerase Structure 18 2010 1420 1430
16. 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 (Pubitemid 46036588)
17. + machine J. Biol. Chem. 278 2003 14406 14413 (Pubitemid 36799993)
18. 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 (Pubitemid 38199027)
19. 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 (Pubitemid 38525007)
20. Schmidt S.L., Pautz A.L., and Burgers P.M. ATP utilization by yeast replication factor C: IV. RFC ATP-binding mutants show defects in DNA replication, DNA repair, and checkpoint regulation J. Biol. Chem. 276 2001 34792 34800
21. Sakato M., Zhou Y., and Hingorani M.M. ATP binding and hydrolysis-driven rate-determining events in the RFC-catalyzed PCNA clamp loading reaction J. Mol. Biol. 416 2012 176 191
22. 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. USA 103 2006 2546 2551
23. 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 (Pubitemid 30159414)
24. Brune M., Hunter J.L., Howell S.A., Martin S.R., Hazlett T.L., Corrie J.E., and Webb M.R. Mechanism of inorganic phosphate interaction with phosphate binding protein from Escherichia coli Biochemistry 37 1998 10370 10380 (Pubitemid 28357558)
25. 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 (Pubitemid 28454951)
26. Hingorani M.M., and Coman M.M. On the specificity of interaction between the Saccharomyces cerevisiae clamp loader replication factor C and primed DNA templates during DNA replication J. Biol. Chem. 277 2002 47213 47224 (Pubitemid 36159232)
27. 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 (Pubitemid 37384476)
28. 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. USA 102 2005 13795 13800 (Pubitemid 41377658)
29. Anderson S.G., Thompson J.A., Paschall C.O., O'Donnell M., and Bloom L.B. Temporal correlation of DNA binding, ATP hydrolysis, and clamp release in the clamp loading reaction catalyzed by the Escherichia coli gamma complex Biochemistry 48 2009 8516 8527
30. Ason B., Handayani R., Williams C.R., Bertram J.G., Hingorani M.M., and O'Donnell M. 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 (Pubitemid 36800257)
31. Turner J., Hingorani M.M., Kelman Z., and O'Donnell M. The internal workings of a DNA polymerase clamp-loading machine EMBO J. 18 1999 771 783 (Pubitemid 29057262)
32. 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
33. 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
34. 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
35. Paschall C.O., Thompson J.A., Marzahn M.R., Chiraniya A., Hayner J.N., and O'Donnell M. The E. coli clamp loader can actively pry open the β-sliding clamp J. Biol. Chem. 286 2011 42704 42714
36. Finkelstein J., Antony E., Hingorani M.M., and O'Donnell M. Overproduction and analysis of eukaryotic multiprotein complexes in Escherichia coli using a dual-vector strategy Anal. Biochem. 319 2003 78 87 (Pubitemid 36802145)