Evolutionary clues to eukaryotic DNA clamp-loading mechanisms: Analysis of the functional constraints imposed on replication factor C AAA+ ATPases

Nucleic Acids Research

Volumn 33, Issue 11, 2005, Pages 3614-3628

  Neuwald, Andrew F ^a  

^a Simons Center for Quantitative Biology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ARGININE; CHAPERONE; DNA; DNA POLYMERASE; REPLICATION FACTOR C; CYCLINE; DNA BINDING PROTEIN; REPLICATION PROTEIN A;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; DNA BINDING; DNA CONFORMATION; DNA REPLICATION; EUKARYOTE EVOLUTION; HUMAN; HYDROLYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; CHEMICAL STRUCTURE; CHEMISTRY; EUKARYOTIC CELL; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; SEQUENCE ALIGNMENT; STATISTICAL ANALYSIS;

EUKARYOTA;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; DATA INTERPRETATION, STATISTICAL; DNA REPLICATION; DNA-BINDING PROTEINS; EUKARYOTIC CELLS; EVOLUTION, MOLECULAR; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROLIFERATING CELL NUCLEAR ANTIGEN; REPLICATION PROTEIN A; REPLICATION PROTEIN C; SEQUENCE ALIGNMENT;

EID: 23344439328     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gki674     Document Type: Article

References (61)

1. Huang,C.C., Hearst,J.E. and Alberts,B.M. (1981) Two types of replication proteins increase the rate at which T4 DNA polymerase traverses the helical regions in a single-stranded DNA template. J. Biol. Chem., 256, 4087-4094.
2. Prelich,G., Kostura,M., Marshak,D.R., Mathews,M.B. and Stillman,B. (1987) The cell-cycle regulated proliferating cell nuclear antigen is required for SV40 DNA replication in vitro. Nature, 326, 471-475.
3. Kong,X.P., Onrust,R., O'Donnell,M. and Kuriyan,J. (1992) Three-dimensional structure of the beta subunit of E. coli DNA polymerise III holoenzyme: A sliding DNA clamp. Cell, 69, 425-437.
4. 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.
5. Stukenberg,P.T., Studwell-Vaughan,P.S. and O'Donnell,M. (1991) Mechanism of the sliding beta-clamp of DNA polymerase III holoenzyme. J. Biol. Chem., 266, 11328-11334.
6. Kelman,Z. and O'Donnell,M. (1995) DNA polymemse III holoenzyme: structure and function of a chromosomal replicating machine. Annu. Rev. Biochem., 64, 171-200.
7. Waga,S. and Stillman,B. (1998) The DNA replication fork in eukaryotic cells. Annu. Rev. Biochem., 67, 721-751.
8. Majka,J. and Burgers,P.M. (2004) The PCNA-RFC families of DNA clamps and clamp loaders. Prog. Nucleic Acid Res. Mol. Biol., 78, 227-260.
9. Majka,J. and Burgers,P.M. (2003) Yeast Rad17/Mec3/Ddc1: A sliding clamp for the DNA damage checkpoint. Proc. Natl Acad. Sci. USA, 100 2249-2254.
10. Longhese,M.P., Foiani,M., Muzi-Falconi,M., Lucchini,G. and Plevani,P. (1998) DNA damage checkpoint in budding yeast. EMBO J., 17, 5525-5528.
11. Melo,J. and Toczyski,D. (2002) A unified view of the DNA-damage checkpoint. Curr. Opin. Cell Biol., 14, 237-245.
12. Huberman,J.A. (1999) DNA damage and replication checkpoints in the fission yeast, Schizosaccharomyces pombe. Prog. Nucleic Acid Res. Mol. Biol., 62, 369-395.
13. Tsurimoto,T. and Stillman,B. (1989) Purification of a cellular replication factor, RF-C, that is required for coordinated synthesis of leading and lagging strands during simian virus 40 DNA replication in vitro. Mol. Cell. Biol., 9, 609-619.
14. Tsurimoto,T. and Stillman,B. (1990) Functions of replication factor C and proliferating-cell nuclear antigen: Functional similarity of DNA polymerase accessory proteins from human cells and bacteriophage T4. Proc. Natl Acad. Sci. USA, 87, 1023-1027.
15. Lee,S.H., Kwong,A.D., Pan,Z.Q. and Hurwitz,J. (1991) Studies on the activator 1 protein complex, an accessory factor for proliferating cell nuclear antigen-dependent DNA polymerase delta. J. Biol. Chem., 266, 594-602.
16. Gomes,X.V. and Burgers,P.M. (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.
17. Bowman,G.D., O'Donnell,M. and Kuriyan,J. (2004) Structural analysis of a eukaryotic sliding DNA clamp-clamp loader complex. Nature, 429 724-730.
18. Tsurimoto,T. and Stillman,B. (1991) 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, 1950-1960.
19. Miyata,T., Oyama,T., Mayanagi,K., Ishino,S., Ishino,Y. and Morikawa,K (2004) The clamp-loading complex for processive DNA replication. Nature Struct. Mol. Biol., 11, 632-636.
20. Oyama,T., Ishino,Y., Cann,I.K., Ishino,S. and Morikawa,K. (2001) Atomic structure of the clamp loader small subunit from Pyrococcus furiosus. Mol. Cell, 8, 455-463.
21. Naiki,T., Kondo,T., Nakada,D., Matsumoto,K. and Sugimoto,K. (2001) Chl12 (Ctf18) forms a novel replication factor C-related complex and functions redundantly with Rad24 in the DNA replication checkpoint pathway. Mol. Cell. Biol., 21, 5838-5845.
22. Bermudez,V.P., Maniwa,Y., Tappin,I., Ozato,K., Yokomori,K. and Hurwitz,J. (2003) The alternative Ctf18-Dcc1-Ctf8-replication factor C complex required for sister chromatid cohesion loads proliferating cell nuclear antigen onto DNA. Proc. Natl Acad. Sci. USA, 100, 10237-10242.
23. Parrilla-Castellar,E.R., Arlander,S.J. and Karnitz,L. (2004) Dial 9-1-1 for DNA damage: The Rad9-Hus1-Rad1 (9-1-1) clamp complex. DNA Repair (Amst.), 3, 1009-1014.
24. Ellison,V. and Stillman,B. (2003) Biochemical characterization of DNA damage checkpoint complexes: Clamp loader and clamp complexes with specificity for 5′ recessed DNA. PLoS Biol., 1, E33.
25. Guenther,B., Onrust,R., Sali,A., O'Donnell,M. and Kuriyan,J. (1997) Crystal structure of the delta' subunit of the clamp-loader complex of E.coli DNA polymerase III. Cell, 91, 335-345.
26. Neuwald,A.F., Aravind,L., Spouge,J.L. and Koonin,E.V. (1999) AAA+:a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res., 9, 27-43.
27. Ogura,T. and Wilkinson,A.J. (2001) AAA+ superfamily ATPases: Common structure - diverse function. Genes Cells, 6, 575-597.
28. Lupas,A.N. and Martin,J. (2002) AAA proteins. Curr. Opin. Struct. Biol., 12, 746-753.
29. Ahmadian,M.R., Stege,P., Scheffzek,K. and Wittinghofer,A. (1997) Confirmation of the arginine-finger hypothesis for the GAP-stimulated GTP-hydrolysis reaction of Ras. Nature Struct. Biol., 4, 686-689.
30. Neuwald,A.F., Kannan,N., Poleksic,A., Hata,N. and Liu,J.S. (2003) Ran's C-terminal, basic patch and nucleotide exchange mechanisms in light of a canonical structure for Rab, Rho, Ras and Ran GTPases. Genome Res. 13, 673-692.
31. Wilbur,W.J. and Neuwald,A.F. (2000) A theory of information with special application to search problems. Comput. Chem., 24, 33-42.
32. Neuwald,A.F. and Liu,J.S. (2004) Gapped alignment of protein sequence motifs through Monte Carlo optimization of a hidden Markov model. BMC Bioinformatics, 5, 157.
33. Altschul,S.F., Madden,T.L., Schaffer,A.A., Zhang,J., Zhang,Z., Miller,W. and Lipman,D.J. (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res., 25, 3389-3402.
34. Liu,J.S. (2001) Monte Carlo Strategies in Scientific Computing. Springer-Verlag, New York.
35. Neuwald,A.F. and Liu,J.S. (2005) Measuring evolutionary constraints as protein properties reflecting underlying mechanisms. In: Jorde,L.B., Little,P.R.R., Dunn,M.J. and Subramaniam.S. Encyclopedia of Genetics, Genomics, Proteomics and Bioinformatics. John Wiley & Sons, Hoboken, NJ.
36. Shindyalov,I.N. and Bourne,P.E. (1998) Protein structure alignment by incremental combinatorial extension (CE) of the optimal path. Protein Eng., 11, 739-747.
37. Neuwald,A.F. (2003) Evolutionary clues to DNA polymerase III beta clamp structural mechanisms. Nucleic Acids Res., 31, 4503-4516.
38. Word,J.M., Lovell,S.C., LaBean,T.H., Taylor,H.C., Zalis,M.E., Presley,B.K., Richardson,T.S. and Richardson,D.C. (1999) Visualizing and quantifying molecular goodness-of-fit: Small-probe contact dots with explicit hydrogen atoms. J. Mol. Biol., 285, 1711-1733.
39. Kabsch,W. and Sander,C. (1983) Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22, 2577-2637.
40. Sayle,R.A. and Milner-White,E.J. (1995) RASMOL: Biomolecular graphics for all. Trends Biochem. Sci., 20, 374.
41. Walker,J.E., Saraste,M., Runswick,M.J. and Gay,N.J. (1982) Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J., 1, 945-951.
42. 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.
43. DeLaBarre,B. and Brunger,A.T. (2003) Complete structure of p97/ valosin-containing protein reveals communication between nucleotide domains. Nature Struct. Biol., 10, 856-863.
44. Delabarre,B. and Brunger,A.T. (2005) Nucleotide dependent motion and mechanism of action of p97/VCP. J. Mol. Biol., 347, 437-452.
45. Dittrich,M., Hayashi,S. and Schulten,K. (2003) On the mechanism of ATP hydrolysis in F1-ATPase. Biophys. J., 85, 2253-2266.
46. Jeruzalmi,D., O'Donnell,M. and Kuriyan,J. (2001) Crystal structure of the processivity clamp loader gamma (γ) complex of E.coli DNA polymerase III. Cell, 106, 429-441.
47. Richardson,J.S. and Richardson,D.C. (1988) Amino acid preferences for specific locations at the ends of alpha helices. Science, 240 1648-1652.
48. Presta,L.G. and Rose,G.D. (1988) Helix signals in proteins. Science 240, 1632-1641.
49. Lee,S.Y., De La Torre,A., Yan,D., Kustu,S., Nixon,B.T. and Wemmer,D.E. (2003) Regulation of the transcriptional activator NtrC1: Structural studies of the regulatory and AAA+ ATPase domains. Genes Dev., 17, 2552-2563.
50. Wyman,C., Rombel,I., North,A.K., Bustamante,C. and Kustu,S. (1997) Unusual oligomerization required for activity of NtrC, a bacterial enhancer-binding protein. Science, 275, 1658-1661.
51. Cropp,T.A. and Schultz,P.G. (2004) An expanding genetic code. Trends Genet., 20, 625-630.
52. England,P.M. (2004) Unnatural amino acid mutagenesis: A precise tool for probing protein structure and function. Biochemistry, 43, 11623-11629.
53. Jantz,D. and Berg,J.M. (2003) Expanding the DNA-recognition repertoire for zinc finger proteins beyond 20 amino acids. J. Am. Chem. Soc., 125, 4960-4961.
54. Deiters,A., Geierstanger,B.H. and Schultz,P.G. (2005) Site-specific in vivo labeling of proteins for NMR studies. Chembiochem., 6, 55-58.
55. Fernandez,C. and Wider,G. (2003) TROSY in NMR studies of the structure and function of large biological macromolecules. Curr. Opin. Struct. Biol., 13, 570-580.
56. Johnson,A. and O'Donnell,M. (2003) Ordered ATP hydrolysis in the gamma complex clamp loader AAA+ machine. J. Biol. Chem., 278, 14406-14413.
57. Eyles,S.J. and Kaltashov,I.A. (2004) Methods to study protein dynamics and folding by mass spectrometry. Methods, 34, 88-99.
58. Busenlehner,L.S. and Armstrong,R.N. (2005) Insights into enzyme structure and dynamics elucidated by amide H/D exchange mass spectrometry. Arch. Biochem. Biophys., 433, 34-46.
59. Hoofnagle,A.N., Resing,K.A. and Ahn,N.G. (2003) Protein analysis by hydrogen exchange mass spectrometry. Annu. Rev. Biophys. Biomol. Struct., 32, 1-25.
60. Hoofnagle,A.N., Resing,K.A., Goldsmith,E.J. and Ahn,N.G. (2001) Changes in protein conformational mobility upon activation of extracellular regulated protein kinase-2 as detected by hydrogen exchange. Proc. Natl Acad. Sci. USA, 98, 956-961.
61. Lee,T., Hoofnagle,A.N., Kabuyama,Y., Stroud,J., Min,X., Goldsmith,E.J., Chen,L., Resing,K.A. and Ahn,N.G. (2004) Docking motif interactions in MAP kinases revealed by hydrogen exchange mass spectrometry. Mol. Cell, 14, 43-55.