Hypothesis: Bacterial clamp loader ATPase activation through DNA-dependent repositioning of the catalytic base and of a trans-acting catalytic threonine

Nucleic Acids Research

Volumn 34, Issue 18, 2006, Pages 5280-5290

  Neuwald, Andrew F ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; DNA; HISTIDINE; LYSINE; THREONINE;

ARCHAEBACTERIUM; ARTICLE; BAYES THEOREM; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SUBUNIT; EUBACTERIUM; HYPOTHESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DNA INTERACTION;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; ARGININE; BACTERIAL PROTEINS; BAYES THEOREM; BINDING SITES; CATALYSIS; DNA, BACTERIAL; DNA-BINDING PROTEINS; ENZYME ACTIVATION; HISTIDINE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN SUBUNITS; SEQUENCE ALIGNMENT; THREONINE;

ARCHAEA; BACTERIA (MICROORGANISMS); EUKARYOTA; PROKARYOTA;

EID: 33750971457     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkl519     Document Type: Article

References (59)

1. Waga,S. and Stillman,B. (1998) The DNA replication fork in eukaryotic cells. Annu. Rev. Biochem., 67, 721-751.
2. Jeruzalmi,D., O'Donnell,M. and Kuriyan,J. (2002) Clamp loaders and sliding clamps. Curr. Opin. Struct. Biol., 12, 217-224.
3. 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.
4. 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.
5. Kong,X.P., Onrust,R., O'Donnell,M. and Kuriyan,J. (1992) Three-dimensional structure of the beta subunit of E.coli DNA polymerase III holoenzyme: A sliding DNA clamp. Cell, 69, 425-437.
6. Yao,N., Turner,J., Kelman,Z., Stukenberg,P.T., Dean,F., Shechter,D., Pan,Z.Q., Hurwitz,J. and O'Donnell,M. (1996) Clamp loading, unloading and intrinsic stability of the PCNA, beta and gp45 sliding clamps of human, E.coli and T4 replicases. Genes Cells, 1, 101-113.
7. Leu,F.P., Hingorani,M.M., Turner,J. and O'Donnell,M. (2000) The delta subunit of DNA polymerase III holoenzyme serves as a sliding clamp unloader in Escherichia coli. J. Biol. Chem., 275, 34609-34618.
8. Marians,K.J. (1992) Prokaryotic DNA replication. Annu. Rev. Biochem., 61, 673-719.
9. Bowman,G.D., Goedken,E.R., Kazmirski,S.L., O'Donnell,M. and Kuriyan,J. (2005) DNA polymerase clamp loaders and DNA recognition. FEBS Lett., 579, 863-867.
10. Onrust,R., Finkelstein,J., Turner,J., Naktinis,V. and O'Donnell,M. (1995) Assembly of a chromosomal replication machine: Two DNA polymerases, a clamp loader, and sliding clamps in one holoenzyme particle III. Interface between two polymerases and the clamp loader. J. Biol. Chem., 270, 13366-13377.
11. Jeruzalmi,D., O'Donnell,M. and Kuriyan,J. (2001) Crystal structure of the processivity clamp loader gamma (gamma) complex of E.coli DNA polymerase III. Cell, 106, 429-441.
12. 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.
13. Hanson,P.I. and Whiteheart,S.W. (2005) AAA+ proteins: Have engine, will work. Nature Rev. Mol. Cell. Biol., 6, 519-529.
14. 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.
15. Studwell-Vaughan,P.S. and O'Donnell,M. (1991) Constitution of the twin polymerase of DNA polymerase III holoenzyme. J. Biol. Chem., 266, 19833-19841.
16. 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.
17. Guenther,B., Onrust,R., Sali,A., O'Donnell,M. and Kuriyan,J. (1997) Crystal structure of the δ′ subunit of the clamp-loader complex of E.coli DNA polymerase III. Cell, 91, 335-345.
18. Podobnik,M., Weitze,T.F., O'Donnell,M. and Kuriyan,J. (2003) Nucleotide-Induced conformational changes in an isolated Escherichia coli DNA polymerase III clamp loader subunit. Structure (Camb.), 11, 253-263.
19. Kazmirski,S.L., Podobnik,M., Weitze,T.F., O'Donnell,M. and Kuriyan,J. (2004) Structural analysis of the inactive state of the Escherichia coli DNA polymerase clamp-loader complex. Proc. Natl Acad. Sci. USA, 101, 16750-16755.
20. 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.
21. 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.
22. 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.
23. Stewart,J., Hingorani,M.M., Kelman,Z. and O'Donnell,M. (2001) Mechanism of beta clamp opening by the delta subunit of Escherichia coli DNA polymerase III holoenzyme. J. Biol. Chem., 276, 19182-19189.
24. Bloom,L.B., Turner,J., Kelman,Z., Beechem,J.M., O'Donnell,M. and Goodman,M.F. (1996) Dynamics of loading the beta sliding clamp of DNA polymerase III onto DNA. J. Biol. Chem., 271, 30699-30708.
25. Ason,B., Bertram,J.G., Hingorani,M.M., Beechem,J.M., O'Donnell,M., Goodman,M.F. and Bloom,L.B. (2000) 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, 3006-3015.
26. Goedken,E.R., Kazmirski,S.L., Bowman,G.D., O'Donnell,M. and Kuriyan,J. (2005) Mapping the interaction of DNA with the Escherichia coli DNA polymerase clamp loader complex. Nature Struct. Mol. Biol., 12, 183-190.
27. Ason,B., Handayani,R., Williams,C.R., Bertram,J.G., Hingorani,M.M., O'Donnell,M., Goodman,M.F. and Bloom,L.B. (2003) 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, 10033-10040.
28. O'Donnell,M., Jeruzalmi,D. and Kuriyan,J. (2001) Clamp loader structure predicts the architecture of DNA polymerase III holoenzyme and RFC. Curr. Biol., 11, R935-946.
29. Davey,M.J., Jeruzalmi,D., Kuriyan,J. and O'Donnell,M. (2002) Motors and switches: AAA+ machines within the replisome. Nature Rev. Mol. Cell Biol., 3, 826-835.
30. 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.
31. 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.
32. Neuwald,A.F. (2006) Bayesian shadows of molecular mechanisms cast in the light of evolution. Trends Biochem. Sci., 31, 374-382.
33. Neuwald,A.F. (2005) Evolutionary clues to eukaryotic DNA clamp-loading mechanisms: Analysis of the functional constraints imposed on replication factor C AAA+ ATPases. Nucleic Acids Res., 33, 3614-3628.
34. Saraste,M., Sibbald,P.R. and Wittinghofer,A. (1990) The P-loop - a common motif in ATP- and GTP-binding proteins. Trends Biochem. Sci., 15, 430-434.
35. Koonin,E.V. (1993) A common set of conserved motifs in a vast variety of putative nucleic acid-dependent ATPases including MCM proteins involved in the initiation of eukaryotic DNA replication. Nucleic Acids Res., 21, 2541-2547.
36. Lenzen,C.U., Steinmann,D., Whiteheart,S.W. and Weis,W.I. (1998) Crystal structure of the hexamerization domain of N-ethylmaleimide-sensitive fusion protein. Cell, 94, 525-536.
37. Yu,R.C., Hanson,P.I., Jahn,R. and Brunger,A.T. (1998) Structure of the ATP-dependent oligomerization domain of N-ethylmaleimide sensitive factor complexed with ATP. Nature Struct. Biol., 5, 803-811.
38. Hattendorf,D.A. and Lindquist,S.L. (2002) Cooperative kinetics of both Hsp104 ATPase domains and interdomain communication revealed by AAA sensor-1 mutants. EMBO J., 21, 12-21.
39. 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.
40. Johnson,A. and O'Donnell,M. (2003) Ordered ATP hydrolysis in the gamma complex clamp loader AAA+ machine. J. Biol. Chem., 278, 14406-14413.
41. Snyder,A.K., Williams,C.R., Johnson,A., O'Donnell,M. and Bloom,L.B. (2004) 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, 4386-4393.
42. Orelle,C., Dalmas,O., Gros,P., Di Pietro,A. and Jault,J.M. (2003) The conserved glutamate residue adjacent to the Walker-B motif is the catalytic base for ATP hydrolysis in the ATP-binding cassette transporter BmrA. J. Biol. Chem., 278, 47002-47008.
43. Richardson,D.C.R. and Richardson,J.S. (1989) In Fasman,G.D. (ed.), Prediction of Protein Structure and The Principles of Protein Conformation. Plenum, NY, pp. 1-98.
44. Pauling,L., Corey,R.B. and Branson,H.R. (1951) The structure of proteins; two hydrogen-bonded helical configurations of the polypeptide chain. Proc. Natl Acad. Sci. USA, 37, 205-211.
45. Pal,D. and Chakrabarti,P. (2001) Non-hydrogen bond interactions involving the methionine sulfur atom. J. Biomol. Struct. Dyn., 19, 115-128.
46. Wang,J., Song,J.J., Franklin,M.C., Kamtekar,S., Im,Y.J., Rho,S.H., Seong,I.S., Lee,C.S., Chung,C.H. and Eom,S.H. (2001) Crystal structures of the HslVU peptidase-ATPase complex reveal an ATP-dependent proteolysis mechanism. Structure, 9, 177-184.
47. Cremo,C.R., Grammer,J.C. and Yount,R.G. (1989) Direct chemical evidence that serine 180 in the glycine-rich loop of myosin binds to ATP. J. Biol. Chem., 264, 6608-6611.
48. Cremo,C.R., Loo,J.A., Edmonds,C.G. and Hatlelid,K.M. (1992) Vanadate catalyzes photocleavage of adenylate kinase at proline-17 in the phosphate-binding loop. Biochemistry, 31, 491-497.
49. Ko,Y.H., Bianchet,M., Amzel,L.M. and Pedersen,P.L. (1997) Novel insights into the chemical mechanism of ATP synthase. Evidence that in the transition state the gamma-phosphate of ATP is near the conserved alanine within the P-loop of the beta-subunit. J. Biol. Chem., 272, 18875-18881.
50. Ko,Y.H., Hong,S. and Pedersen,P.L. (1999) Chemical mechanism of ATP synthase. Magnesium plays a pivotal role in formation of the transition state where ATP is synthesized from ADP and inorganic phosphate. J. Biol. Chem., 274, 28853-28856.
51. Armstrong,G.A., Alberti,M., Leach,F. and Hearst,J.E. (1989) Nucleotide sequence, organization, and nature of the protein products of the carotenoid biosynthesis gene cluster of Rhodobacter capsulatus. Mol. Gen. Genet., 216, 254-268.
52. Petruzzella,V., Tiranti,V., Fernandez,P., Ianna,P., Carrozzo,R. and Zeviani,M. (1998) Identification and characterization of human cDNAs specific to BCS1, PET112, SCO1, COX15, and COX11, five genes involved in the formation and function of the mitochondrial respiratory chain. Genomics, 54, 494-504.
53. Johnson,A. and O'Donnell,M. (2005) Cellular DNA replicases: Components and dynamics at the replication fork. Annu. Rev. Biochem., 74, 283-315.
54. O'Donnell,M. and Kuriyan,J. (2006) Clamp loaders and replication initiation. Curr. Opin. Struct. Biol., 16, 35-41.
55. Sayle,R.A. and Milner-White,E.J. (1995) RASMOL: Biomolecular graphics for all. Trends Biochem. Sci., 20, 374.
56. 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.
57. 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.
58. Neuwald,A.F. (2003) Evolutionary clues to DNA polymerase III beta clamp structural mechanisms. Nucleic Acids Res., 31, 4503-4516.
59. Word,J.M., Lovell,S.C., LaBean,T.H., Taylor,H.C., Zalis,M.E., Presley,B.K., Richardson,J.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.