A Single Subunit Directs the Assembly of the Escherichia coli DNA Sliding Clamp Loader

Structure

Volumn 18, Issue 3, 2010, Pages 285-292

  Park, Ah Young ^a,b   Jergic, Slobodan ^c   Politis, Argyris ^a,b   Ruotolo, Brandon T ^b,d   Hirshberg, Daniel ^b   Jessop, Linda L ^c   Beck, Jennifer L ^c   Barsky, Daniel ^b,e   O'Donnell, Mike ^f   Dixon, Nicholas E ^c   Robinson, Carol V ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF WOLLONGONG   (Australia)

^d UNIVERSITY OF MICHIGAN   (United States)

^e LAWRENCE LIVERMORE NATIONAL LABORATORY   (United States)

^f ROCKEFELLER UNIVERSITY   (United States)

Author keywords

DNA

Indexed keywords

DIMER; DNA; DNA DIRECTED DNA POLYMERASE GAMMA; HOLOENZYME; MONOMER; MULTIPROTEIN COMPLEX; OLIGOMER; PROTEIN; PROTEIN DNAX; PROTEIN SUBUNIT; TETRAMER; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ESCHERICHIA COLI; IN VIVO STUDY; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN STABILITY;

BACTERIAL PROTEINS; BINDING SITES; DNA POLYMERASE III; DNA, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MODELS, BIOLOGICAL; PROTEIN SUBUNITS;

ESCHERICHIA COLI;

EID: 77649103357     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2010.01.009     Document Type: Article

References (44)

1. Blinkova A., Hervas C., Stukenberg P.T., Onrust R., O'Donnell M.E., and Walker J.R. The Escherichia coli DNA polymerase III holoenzyme contains both products of the dnaX gene, τ and γ, but only τ is essential. J. Bacteriol. 175 (1993) 6018-6027
2. Blinkowa A.L., and Walker J.R. Programmed ribosomal frameshifting generates the Escherichia coli DNA polymerase III γ subunit from within the τ subunit reading frame. Nucleic Acids Res. 18 (1990) 1725-1729
3. Bloom L.B. Loading clamps for DNA replication and repair. DNA Repair (Amst.) 8 (2009) 570-578
4. Cann I.K., and Ishino Y. Archaeal DNA replication: identifying the pieces to solve a puzzle. Genetics 152 (1999) 1249-1267
5. Chernushevich I.V., and Thomson B.A. Collisional cooling of large ions in electrospray mass spectrometry. Anal. Chem. 76 (2004) 1754-1760
6. Cullmann G., Fien K., Kobayashi R., and Stillman B. Characterization of the five replication factor C genes of Saccharomyces cerevisiae. Mol. Cell. Biol. 15 (1995) 4661-4671
7. Dallmann H.G., and McHenry C.S. DnaX complex of Escherichia coli DNA polymerase III holoenzyme. Physical characterization of the DnaX subunits and complexes. J. Biol. Chem. 270 (1995) 29563-29569
8. Flower A.M., and McHenry C.S. The γ subunit of DNA polymerase III holoenzyme of Escherichia coli is produced by ribosomal frameshifting. Proc. Natl. Acad. Sci. USA 87 (1990) 3713-3717
9. Gao D., and McHenry C.S. τ binds and organizes Escherichia coli replication through distinct domains. Partial proteolysis of terminally tagged τ to determine candidate domains and to assign domain V as the α binding domain. J. Biol. Chem. 276 (2001) 4433-4440
10. Gao D., and McHenry C.S. τ binds and organizes Escherichia coli replication proteins through distinct domains. Domain IV, located within the unique C terminus of τ, binds the replication fork, helicase, DnaB. J. Biol. Chem. 276 (2001) 4441-4446
11. Gao D., and McHenry C.S. tau binds and organizes Escherichia coli replication proteins through distinct domains. Domain III, shared by γ and τ, binds δ δ ′ and χ ψ. J. Biol. Chem. 276 (2001) 4447-4453
12. Gulbis J.M., Kazmirski S.L., Finkelstein J., Kelman Z., O'Donnell M., and Kuriyan J. Crystal structure of the chi:psi sub-assembly of the Escherichia coli DNA polymerase clamp-loader complex. Eur. J. Biochem. 271 (2004) 439-449
13. Hernández H., and Robinson C.V. Dynamic protein complexes: insights from mass spectrometry. J. Biol. Chem. 276 (2001) 46685-46688
14. Hernández H., and Robinson C.V. Determining the stoichiometry and interactions of macromolecular assemblies from mass spectrometry. Nat. Protoc. 2 (2007) 715-726
15. Jergic S., Ozawa K., Su X.-C., Scott D.D., Williams N.K., Hamdan S.M., Crowther J.A., Otting G., and Dixon N.E. The unstructured C-terminus of the τ subunit of Escherichia coli DNA polymerase III holoenzyme is the site of interaction with the α subunit. Nucleic Acids Res. 35 (2007) 2813-2824
16. Jeruzalmi D., O'Donnell M., and Kuriyan J. Crystal structure of the processivity clamp loader gamma (γ) complex of E. coli DNA polymerase III. Cell 106 (2001) 429-441
17. Jeruzalmi D., O'Donnell M., and Kuriyan J. Clamp loaders and sliding clamps. Curr. Opin. Struct. Biol. 12 (2002) 217-224
18. Johnson A., and O'Donnell M. Cellular DNA replicases: components and dynamics at the replication fork. Annu. Rev. Biochem. 74 (2005) 283-315
19. Kornberg A., and Baker T.A. DNA Replication. Second Edition (1992), W.H. Freeman, New York
20. Loo J.A. Studying noncovalent protein complexes by electrospray ionization mass spectrometry. Mass Spectrom. Rev. 16 (1997) 1-23
21. Lopez de Saro F.J., Georgescu R.E., and O'Donnell M. A peptide switch regulates DNA polymerase processivity. Proc. Natl. Acad. Sci. USA 100 (2003) 14689-14694
22. McHenry C.S. Chromosomal replicases as asymmetric dimers: studies of subunit arrangement and functional consequences. Mol. Microbiol. 49 (2003) 1157-1165
23. McInerney P., Johnson A., Katz F., and O'Donnell M. Characterization of triple DNA polymerase replisome. Mol. Cell. 27 (2007) 527-538
24. McKay A.R., Ruotolo B.T., Ilag L.L., and Robinson C.V. Mass measurements of increased accuracy resolve heterogeneous populations of intact ribosomes. J. Am. Chem. Soc. 128 (2006) 11433-11442
25. Naktinis V., Onrust R., Fang L., and O'Donnell M. Assembly of a chromosomal replication machine: two DNA polymerases, a clamp loader, and sliding clamps in one holoenzyme particle. II. Intermediate complex between the clamp loader and its clamp. J. Biol. Chem. 270 (1995) 13358-13365
26. 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
27. O'Donnell M., and Kuriyan J. Clamp loaders and replication initiation. Curr. Opin. Struct. Biol. 16 (2006) 35-41
28. O'Donnell M., Onrust R., Dean F.B., Chen M., and Hurwitz J. Homology in accessory proteins of replicative polymerases-E. coli to humans. Nucleic Acids Res. 21 (1993) 1-3
29. Onrust R., Finkelstein J., Naktinis V., Turner J., Fang L., and O'Donnell M. Assembly of a chromosomal replication machine: two DNA polymerases, a clamp loader, and sliding clamps in one holoenzyme particle. I. Organization of the clamp loader. J. Biol. Chem. 270 (1995) 13348-13357
30. Onrust R., Finkelstein J., Turner J., Naktinis Y., and O'Donnell M. 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 (1995) 13366-13377
31. Ozawa K., Jergic S., Crowther J.A., Thompson P.R., Wijffels G., Otting G., and Dixon N.E. Cell-free protein synthesis in an autoinduction system for NMR studies of protein-protein interactions. J. Biomol. NMR 32 (2005) 235-241
32. Pritchard A.E., Dallmann H.G., Glover B.P., and McHenry C.S. A novel assembly mechanism for the DNA polymerase III holoenzyme DnaX complex: association of deltadelta' with DnaX(4) forms DnaX(3)deltadelta'. EMBO J. 19 (2000) 6536-6545
33. Pritchard A.E., and McHenry C.S. Assemby of DNA polymerase III holoenzyme: co-assembly of gamma and tau is inhibited by DnaX complex accessory proteins but stimulated by DNA polymerase III core. J. Biol. Chem. 276 (2001) 35217-35222
34. Schaeffer P.M., Headlam M.J., and Dixon N.E. Protein-protein interactions in the eubacterial replisome. IUBMB Life 57 (2005) 5-12
35. Sharon M., and Robinson C.V. The role of mass spectrometry in structure elucidation of dynamic protein complexes. Annu. Rev. Biochem. 76 (2007) 167-193
36. 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
37. Sobott F., Hernández H., McCammon M.G., Tito M.A., and Robinson C.V. A tandem mass spectrometer for improved transmission and analysis of large macromolecular assemblies. Anal. Chem. 74 (2002) 1402-1407
38. Tanner N.A., Hamdan S.M., Jergic S., Loscha K.V., Schaeffer P.M., Dixon N.E., and van Oijen A.M. Single-molecule studies of fork dynamics in Escherichia coli DNA replication. Nat. Struct. Mol. Biol. 15 (2008) 170-176
39. Tsuchihashi Z., and Kornberg A. Translational frameshifting generates the γ subunit of DNA polymerase III holoenzyme. Proc. Natl. Acad. Sci. USA 87 (1990) 2516-2520
40. van den Heuvel R.H., and Heck A.J. Native protein mass spectrometry: from intact oligomers to functional machineries. Curr. Opin. Chem. Biol. 8 (2004) 519-526
41. Wijffels G., Dalrymple B.P., Prosselkov P., Kongsuwan K., Epa V.C., Lilley P.E., Jergic S., Buchardt J., Brown S.E., Alewood P.F., et al. Inhibition of protein interactions with the beta 2 sliding clamp of Escherichia coli DNA polymerase III by peptides from beta 2-binding proteins. Biochemistry 43 (2004) 5661-5671
42. Xiao H., Crombie R., Dong Z., Onrust R., and O'Donnell M. DNA polymerase III accessory proteins. III. holC and holD encoding chi and psi. J. Biol. Chem. 268 (1993) 11773-11778
43. Xiao H., Dong Z., and O'Donnell M. DNA polymerase III accessory proteins. IV. Characterization of chi and psi. J. Biol. Chem. 268 (1993) 11779-11784
44. Yuzhakov A., Kelman Z., and O'Donnell M. Trading places on DNA-a three-point switch underlies primer handoff from primase to the replicative DNA polymerase. Cell 96 (1999) 153-163