Crystal structure of the chi:psi subassembly of the Escherichia coli DNA polymerase clamp-loader complex

European Journal of Biochemistry

Volumn 271, Issue 2, 2004, Pages 439-449

  Gulbis, Jacqueline M ^a,d   Kazmirski, Steven L ^b,c   Finkelstein, Jeff ^a   Kelman, Zvi ^a,e   O'Donnell, Mike ^a   Kuriyan, John ^b,c  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^d WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^e UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

Author keywords

Clamp loader; DNA replication; Processivity factor; Sliding clamp

Indexed keywords

ADENOSINE TRIPHOSPHATE; BINDING PROTEIN; DINUCLEOTIDE; DNA POLYMERASE; NITROGEN; NUCLEOTIDE; PROTEIN SUBUNIT; SINGLE STRANDED DNA;

ARTICLE; BACTERIAL GENOME; COMPLEX FORMATION; CRYSTALLIZATION; ENZYME SUBUNIT; ESCHERICHIA COLI; GENE SEQUENCE; GENETIC CODE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STRUCTURE;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; DNA POLYMERASE III; DNA REPLICATION; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; ESCHERICHIA COLI; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN SUBUNITS; SEQUENCE HOMOLOGY, AMINO ACID;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 1642521025     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1033.2003.03944.x     Document Type: Article

References (52)

1. Kornberg, A. & Baker, T. (1992) DNA Replication, 2nd edn. W. H. Freeman, New York.
2. Jeruzalmi, D., O'Donnell, M. & Kuriyan, J. (2002) Clamp loaders and sliding clamps. Curr. Opin. Struct. Biol. 12, 217-224.
3. Stukenberg, P.T., Turner, J. & O'Donnell, M. (1994) An explanation for lagging strand replication: polymerase hopping among DNA sliding clamps. Cell 78, 877-887.
4. Onrust, R., Finkelstein, J., Naktinis, V., Turner, J., Fang, L. & O'Donnell, M. (1995) 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, 13348-13357.
5. Stewart, J., Hingorani, M.M., Kelman, Z. & O'Donnell, M. (2001) Mechanism of beta clamp opening by the δ subunit of Escherichia coli DNA polymerase III holoenzyme. J. Biol. Chem. 276, 19182-19189.
6. Pritchard, A.E., Dallmann, H.G., Glover, B.P. & McHenry, C.S. (2000) A novel assembly mechanism for the DNA polymerase III holoenzyme DnaX complex: association of δδ′ with DnaX (4) forms DnaX (3) δδ′. EMBO J. 19, 6536-6545.
7. Tsuchihashi, Z. & Kornberg, A. (1990) Translational frameshifting generates the γ subunit of DNA polymerase III holoenzyme. Proc. Natl. Acad. Sci. USA 87, 2516-2520.
8. Flower, A.M. & McHenry, C.S. (1990) The γ subunit of DNA polymerase III holoenzyme of Escherichia coli is produced by ribosomal frameshifting. Proc. Natl Acad. Sci. USA 87, 3713-3717.
9. Studwell-Vaughan, P.S. & O'Donnell, M. (1991) Constitution of the twin polymerase of DNA polymerase III holoenzyme. J. Biol. Chem. 266, 19833-19841.
10. Yuzhakov, A., Turner, J. & O'Donnell, M. (1996) Replisome assembly reveals the basis for asymmetric function in leading and lagging strand replication. Cell 86, 877-886.
11. Kim, S., Dallmann, H.G., McHenry, C.S. & Marians, K.J. (1996) τ Couples the leading- and lagging-strand polymerases at the Escherichia coli DNA replication fork. J. Biol. Chem. 271, 21406-21412.
12. Kim, S., Dallmann, H.G., McHenry, C.S. & Marians, K.J. (1996) Coupling of a replicative polymerase and helicase: a τ-DnaB interaction mediates rapid replication fork movement. Cell 84, 643-650.
13. Gao, D. & McHenry, C.S. (2001) 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 alpha binding domain. J. Biol. Chem. 276, 4433-4440.
14. Gao, D. & McHenry, C.S. (2001) 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, 4441-4446.
15. Guenther, B., Onrust, R., Sali, A., O'Donnell, M. & Kuriyan, J. (1997) Crystal structure of the δ-subunit of the clamp-loader complex of E. coli DNA polymerase III. Cell 91, 335-345.
16. Oyama, T., Ishino, Y., Cann, I.K., Ishino, S. & Morikawa, K. (2001) Atomic structure of the clamp loader small subunit from Pyrococcus furiosus. Mol. Cell. 8, 455-463.
17. Jeruzalmi, D., O'Donnell, M. & Kuriyan, J. (2001) Crystal structure of the processivity clamp loader γ (γ) complex of E. coli DNA polymerase III. Cell 106, 429-441.
18. Jeruzalmi, D., Yurieva, O., Zhao, Y., Young, M., Stewart, J., Hingorani, M., O'Donnell, M. & Kuriyan, J. (2001) Mechanism of processivity clamp opening by the 5 subunit wrench of the clamp loader complex of E. coli DNA polymerase III. Cell 106, 417-428.
19. 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.
20. O'Donnell, M. & Studwell, P.S. (1990) Total reconstitution of DNA polymerase III holoenzyme reveals dual accessory protein clamps. J. Biol. Chem. 265, 1179-1187.
21. Xiao, H., Dong, Z. & O'Donnell, M. (1993) DNA polymerase III accessory proteins. IV. Characterization of χ and ψ. J. Biol. Chem. 268, 11779-11784.
22. Gao, D. & McHenry, C.S. (2001) τ 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, 4447-4453.
23. Kelman, Z., Yuzhakov, A., Andjelkovic, J. & O'Donnell, M. (1998) Devoted to the lagging strand - the χ subunit of DNA polymerase III holoenzyme contacts SSB to promote processive elongation and sliding clamp assembly. EMBO J. 17, 2436-2449.
24. Glover, B.P. & McHenry, C.S. (1998) The χ ψ subunits of DNA polymerase. III holoenzyme bind to single-stranded DNA-binding protein (SSB) and facilitate replication of an SSB-coated template. J. Biol. Chem. 273, 23476-23484.
25. Olson, M.W., Dallmann, H.G. & McHenry, C.S. (1995) DnaX complex of Escherichia coli DNA polymerase III holoenzyme. The χ ψ complex functions by increasing the affinity of τ and γ for δ.δ′ to a physiologically relevant range. J. Biol. Chem. 270, 29570-29577.
26. Yuzhakov, A., Kelman, Z. & O'Donnell, M. (1999) Trading places on DNA - a three-point switch underlies primer handoff from primase to the replicative DNA polymerase. Cell 96, 153-163.
27. Xiao, H., Crombie, R., Dong, Z., Onrust, R. & O'Donnell, M. (1993) DNA polymerase III accessory proteins. III. holC and holD encoding χ and ψ. J. Biol. Chem. 268, 11773-11778.
28. Sheldrick, G.M. (1990) Phase annealing in SHELX-90: direct methods for larger structures. Acta Crystallogr. A 46, 467-473.
29. Otwinowski, Z. & Minor, W. (1997) HKL DENZO and SCALEPACK. University of Texas, Southwestern Medical Center at Dallas, Dallas.
30. CCP4 (Collaborative Computational Project, 4) (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760-763.
31. Zhang, K.Y.J. & Main, P. (1990) The use of Sayre's equation with solvent flattening and histogram matching for phase extension and refinement of protein structures. Acta Crystallogr. A 46, 377-381.
32. Jones, T.A., Zou, J.-Y., Cowan, S.W. & Kjeldgaard, M. (1991) Improved methods for the building of protein models in electron density maps and the locations of errors in these models. Acta Crystallogr. A 47, 110-119.
33. Navaza, J. (1994) AMoRe: an automated package for molecular replacement. Acta Crystallogr. A 50, 157-163.
34. Kleywegt, G.J. & Jones, T.A. (1994) Halloween ... masks and bones. In From First Map to Final Model (Bailey, S., Hubbard, R. & Waller, D., eds), pp. 59-66. SERC Daresbury Laboratory, Daresbury.
35. Brünger, A.T. (1992) XPLOR: a System for X-Ray Crystallography and NMR. Yale Academic Press, New Haven.
36. Brünger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S., Read, R.J., Rice, L.M., Simonson, T. & Warren, G.L. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921.
37. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
38. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882.
39. Henikoff, S. & Henikoff, J.G. (1992) Amino acid substitution matrices from protein blocks. Proc. Natl Acad. Sci. USA 89, 10915-10919.
40. Schulz, G.E. (1992) Binding of nucleotides by proteins. Curr. Opin. Struct. Biol. 2, 61-67.
41. Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N. & Bourne, P.W. (2000) The protein data bank. Nucleic Acids Res. 28, 235-242.
42. Holm, L. & Sander, C. (1993) Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233, 123-138.
43. Volz, K. & Matsumura, P. (1991) Crystal structure of Escherichia coli CheY refined at 1.7-A resolution. J. Biol. Chem. 266, 15511-15519.
44. Savva, R., McAuley-Hecht, K., Brown, T. & Pearl, L. (1995) The structural basis of specific base-excision repair by uracil-DNA glycosylase. Nature 373, 487-493.
45. Barrett, T.E., Savva, R., Panayotou, G., Barlow, T., Brown, T., Jiricny, J. & Pearl, L.H. (1998) Crystal structure of a G:T/U mismatch-specific DNA glycosylase: mismatch recognition by complementary-strand interactions. Cell 92, 117-129.
46. Subramanya, H.S., Bird, L.E., Brannigan, J.A. & Wigley, D.B. (1996) Crystal structure of a DExx box DNA helicase. Nature 384, 379-383.
47. Korolev, S., Hsieh, J., Gauss, G.H., Lohman, T.M. & Waksman, G. (1997) Major domain swiveling revealed by the crystal structures of complexes of E. coli Rep helicase bound to single-stranded DNA and ADP. Cell 90, 635-647.
48. Genschel, J., Curth, U. & Urbanke, C. (2000) Interaction of E. coli single-stranded DNA binding protein (SSB) with exonuclease I. The carboxy-terminus of SSB is the recognition site for the nuclease. Biol. Chem. 381, 183-192.
49. Witte, G., Urbanke, C. & Curth, U. (2003) DNA polymerase III χ subunit ties single-stranded DNA binding protein to the bacterial replication machinery. Nucleic Acids Res. 31, 4434-4440.
50. Webster, G., Genschel, J., Curth, U., Urbanke, C., Kang, C. & Hilgenfeld, R. (1997) A common core for binding single-stranded DNA: structural comparison of the single-stranded DNA-binding proteins (SSB) from E. coli and human mitochondria. FEBS Lett. 411, 313-316.
51. Yang, C., Curth, U., Urbanke, C. & Kang, C. (1997) Crystal structure of human mitochondrial single-stranded DNA binding protein at 2.4 A resolution. Nat. Struct. Biol. 4, 153-157.
52. Raghunathan, S., Ricard, C.S., Lohman, T.M. & Waksman, G. (1997) Crystal structure of the homo-tetrameric DNA binding domain of Escherichia coli single-stranded DNA-binding protein determined by multiwavelength x-ray diffraction on the selenomethionyl protein at 2.9-A resolution. Proc. Natl Acad. Sci. USA 94, 6652-6657.