Abstract
The β subunit of E. coli DNA polymerase III holoenzyme (pol III holoenzyme) anchors this multiprotein chromosomal replicase to DNA for fast and highly processive replication (Kornberg and Baker 1991; Stukenberg et al. 1991). Its ring shape (Fig. 1) allows it to completely encircle DNA while freely diffusing along the duplex (Stukenberg et al. 1991; Kong et al. 1992). The β “sliding clamp” confers onto pol III holoenzyme a high degree of processivity (50kb; Fay et al. 1981) and a rapid speed of synthesis (750 nucleotides/s; O’Donnell and Kornberg 1985) which results from the continual proximity of the polymerase and DNA through their mutual association with β (Stukenberg et al. 1991).
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Arai N, Kornberg A (1981) Rep protein as a helicase in an active, isolatable replication fork of duplex Φχ174 DNA. J Biol Chem 256:5294–5298
Blinkowa AL, Walker JL (1990) Programmed ribosomal frameshifiting generates the Escherichia coli DNA polymerase III γ subunit from within the τ subunit reading frame. Nucleic Acids Res 18:1725–1729
Bonner CA, Stukenberg PT, Rajagopalan M, Eritja R, O’Donnell M, McEntee K, Echols H, Goodman MF (1992) Processive DNA synthesis by DNA polymerase II mediated by DNA polymerase III accessory proteins. J Biol Chem 267:11431–11438
Bravo R, Frank R, Blundell PA, Macdonald-Bravo H (1987) Cyclin/PCNA is the auxiliary protein of DNA polymerase delta. Nature 326:515–517
Burgers PMJ (1991) Saccharomyces cerevisiae replication factor C. II. Formation and activity of complexes with proliferating cell nuclear antigen and with DNA polymerases δ and ε. J Biol Chem 266:22698–22706
Burgers PMJ, Kornberg A (1982a) ATP activation of DNA polymerase III holoenzyme from Escherichia coli. I. ATP dependent formation of an initiation complex with a primed template. J Biol Chem 257:11468–11473
Burgers PMJ, Kornberg A (1982b) ATP activation of DNA polymerase III holoenzyme from Escherichia coli. II. Initiation complex: stoichiometry and reactivity. J Biol Chem 257:11474–11478
Burgers PMJ, Kornberg A (1983) The cycling of Escherichia coli DNA polymerase III holoenzyme in replication. J Biol Chem 258:7669–7675
Burgers PMJ, Kornberg A, Sakakibara Y (1981) The dnaN gene codes for the β subunit of DNA polymerase III holoenzyme. Proc Natl Acad Sci USA 78:5391–5395
Carter JR, Franden MA, Aebersold R, McHenry CS (1992) Molecular cloning sequencing and overexpression of the structural gene encoding the delta subunit of Escherichia coli DNA polymerase III holoenzyme. J Bacteriol 174:7013–7025
Dong Z, Onrust R, Skangalis M, O’Donnell M (1993) DNA polymerase III accessory proteins. I. holA and holB encoding δ and δ′. J Biol Chem 268:11758–11765
Fay PJ, Johanson KO, McHenry CS, Bambara RA (1981) Size classes of products synthesized processively by DNA polymerase III and DNA polymerase III holoenzyme of Escherichia coli. J Biol Chem 256:976–983
Flower AM, McHenry CS (1990) The γ subunit of DNA polymerase III holoenzyme of Esherichia coli is produced by ribosomal frameshifting. Proc Natl Acad Sci USA 87:3713–3717
Gogol EP, Young MC, Kubasek WL, Jarvis TC, von Hippel PH (1992) Cryoelectron microscopic visualization of functional subassemblies of the bacteriophage T4 DNA replication complex. J Mol Biol 224:395–412
Herendeen DR, Kassavetis GA, Barry J, Alberts BM, Geiduschek EP (1989) Enhancement of bacteriophage T4 late transcription by components of the T4 DNA replication apparatus. Science 245:952–958
Herendeen DR, Williams KP, Kassavetis GA, Geiduschek EP (1990) An RNA polymerase-binding protein that is required for communication between an enhancer and a promoter. Science 248:573–578
Herendeen DR, Kassavetis GA, Geiduschek EP (1992) A transcriptional enhancer whose function imposes a requirement that proteins track along DNA. Science 256:1298–1303
Huang C-C, Hearst JE, Alberts BM (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
Hughes JA Jr, Bryan SK, Chen H, Moses RE, McHenry CS (1991) Escherichia coli DNA polymerase II is stimulated by DNA polymerase III holoenzyme auxiliary subunits. J Biol Chem 266:4568–4573
Jarvis TC, Paul LS, von Hippel PH (1989) Structural and enzymatic studies of the T4 DNA replication system. I. Physical characterization of the polymerase accessory protein complex. J Biol Chem 264:12709–12716
Jarvis TC, Newport JW, von Hippel PH (1991) Stimulation of the processivity of the DNA polymerase of bacteriophage T4 by the polymerase accessory proteins. J Biol Chem 266:1820–1840
Johanson KO, McHenry CS (1982) The β subunit of the DNA polymerase III holoenzyme becomes inaccessible to antibody after formation of an initiation complex with primed DNA. J Biol Chem 257:12310–12315
Kissinger CR, Liu B, Martin-Blanco E, Kornberg TB, Pabo CO (1990) Crystal structure of an engrailed homeodomain-DNA complex at 2.8 angstrom resolution: a framework for understanding homeodomain-DNA interactions. Cell 63:579–590
Kong X-P, Onrust R, O’Donnell M, Kuriyan J (1992) Three dimensional structure of the β subunit of Escherichia coli DNA polymerase III holoenzyme: a sliding DNA clamp. Cell 69:425–437
Kornberg A (1988) DNA replication. J Biol Chem 263:1–4
Kornberg A, Baker TA (1991) DNA replication. WH Freeman, New York, pp 165–207
Kwon-Shin O, Bodner JB, McHenry CS, Bambara RA (1987) Properties of initiation complexes formed between Escherichia coli DNA polymerase III holoenzyme and primed DNA in the absence of ATP. J Biol Chem 262:2121–2130
LaDuca RJ, Crute JJ, McHenry CS, Bambara RA (1986) The β subunit of the Escherichia coli DNA polymerase III holoenzyme interacts functionally with the catalytic core in the absence of other subunits. J Biol Chem 261:7550–7557
Lee S-H, Kwong AD, Pan Z-H, Hurwitz J (1991) Studies on the activator 1 protein complex, and accessory factor for proliferating cell nuclear antigen-dependent DNA polymerase δ. J Biol Chem 266:594–602
Mace DC, Alberts BM (1984) Characterization of the stimulatory effect of T4 gene 45 protein and the gene 44/62 protein complex on DNA synthesis by T4 DNA polymerase. J Mol Biol 177:313–327
Maki H, Kornberg A (1985) The polymerase subunit of DNA polymerase III of Escherichia coli. J Biol Chem 260:12987–12992
Maki S, Kornberg A (1988) DNA polymerase III holoenzyme of Escherichia coli. II. A novel complex including the y subunit essential for processive synthesis. J Biol Chem 263:6555–6560
McHenry CS (1982) Purification and characterization of DNA polymerase III. Identification of τ as a subunit of the DNA polymerase III holoenzyme. J Biol Chem 257:2657–2663
McHenry CS (1991) DNA polymerase III holoenzyme. J Biol Chem 266:19127–19130
McHenry CS, Crow W (1979) DNA polymerase III of Escherichia coli. J Biol Chem 254:1748–1753
Mok M, Marians KJ (1987) The Escherichia coli preprimosome and DNA B helicase can form replication forks that move at the same rate. J Biol Chem 262:16644–16654
Munn MM, Alberts BM (1991a) The T4 DNA polymerase accessory proteins form an ATP-dependent complex on a primer-template junction. J Biol Chem 266:20024–20033
Munn MM, Alberts BM (1991b) DNA footprinting studies of the complex formed by the T4 DNA polymerase holoenzyme at a primer-template junction. J Biol Chem 266:20034–20044
Nicholls A, Sharp KA, Honig B (1991) Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins: Struct Funct Genet 11:281–296
Nossal NG, Alberts BM (1983) Mechanism of DNA replication catalyzed by purified T4 replication proteins. In: Mathews CK, Kutter EM, Mosig G, Berget PB (eds) Bacteriophage T4. American Society for Microbiology, Washington, DC, pp 71–81
O’Donnell M (1987) Accessory proteins bind a primed template and mediate rapid cycling of DNA polymerase III holoenzyme from Escherichia coli. J Biol Chem 262:16558–16565
O’Donnell M (1992) Accessory protein function in the DNA polymerase III holoenzyme from E. coli. BioEssays 14:105–111
O’Donnell M, Kornberg A (1985) Dynamics of DNA polymerase III holoenzyme of Escherichia coli in replication of a multiprimed template. J Biol Chem 260:12875–12883
O’Donnell M, Studwell PS (1990) Total reconstitution of DNA polymerase III holoenzyme reveals dual accessory protein clamps. J Biol Chem 265:1179–1187
O’Donnell M, Onrust R, Dean FB, Chen M, Hurwitz J (1993) Homology in accessory proteins of replicative polymerases — E. coli to humans. Nucleic Acids Res 21:1–3
Onrust R (1993) The structure and function of the accessory proteins of the E. coli DNA polymerase III holoenzyme. PhD Thesis, Cornell University Medical Center, New York
Onrust R, O’Donnell M (1993) DNA polymerase III accessory proteins. II. Characterization of δ and δ′. J Biol Chem 268:11766–11772
Onrust R, Stukenberg PT, O’Donnell M (1991) Analysis of the ATPase subassembly which initiates processive DNA synthesis by DNA polymerase III holoenzyme. J Biol Chem 266:21681–21686
O’Reilly DR, Crawford AM, Miller LK (1989) Viral proliferating cell nuclear antigen. Nature 337:606
Prelich G, Tan C-K, Kostura M, Mathews MB, So AG, Downey KM, Stillman B (1987) Functional identity of proliferating cell nuclear antigen and a DNA polymerase auxiliary protein. Nature 326:517–520
Roth AC, Nossal NG, Englund PT (1982) Rapid hydrolysis of deoxynucleoside triphosphates accompanies DNA synthesis by T4 DNA polymerase and T4 accessory protein 44/62 and 45. J Biol Chem 257:1267–1273
Sancar A, Hearst JE (1993) Molecular matchmakers. Science 259:1415–1420
Scheuermann RH, Echols H (1985) A separate editing exonuclease for DNA replication: the ε subunit of Escherichia coli DNA polymerase III holoenzyme. Proc Natl Acad Sci USA 81:7747–7751
Sinha NK, Morris CF, Alberts BM (1980) Efficient in vitro replication of double-stranded DNA templates by a purified T4 bacteriophage replication system. J Biol Chem 225:4290–4303
Studwell PS, Stukenberg PT, Onrust R, Skangalis M, O’Donnell M (1990) Replication of the lagging strand by DNA polymerase III holoenzyme. UCLA Symp Mol Cell Biol New Ser 127:153–164
Studwell-Vaughan PS, O’Donnell M (1991) Constitution of the twin polymerase of DNA polymerase III holoenzyme. J Biol Chem 266:19833–19841
Studwell-Vaughan PS, O’Donnell M (1993) DNA polymerase III accessory proteins. V. θ encoded by holE. J Biol Chem 268:11785–11791
Stukenberg PT (1993) The dynamics of E. coli DNA polymerase III holoenzyme in an in vitro lagging strand model system. PhD Thesis, Cornell University Medical College, New York
Stukenberg PT, Studwell-Vaughan PS, O’Donnell M (1991) Mechanism of the sliding β-clamp of DNA polymerase III holoenzyme. J Biol Chem 266:11328–11334
Tsuchihashi Z, Kornberg A (1989) ATP interactions of the τ and γ subunits of DNA polymerase III holoenzyme of Escherichia coli. J Biol Chem 264:17790–17795
Tsuchihashi Z, Kornberg A (1990) Translational frameshifting generates the γ subunit of DNA polymerase III holoenzyme. Proc Natl Acad Sci USA 87:2516–2520
Tsurimoto T, 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
Wickner S (1976) Mechanism of DNA elongation catalyzed by Escherichia coli DNA polymerase III, dnaZ protein, and DNA elongation factors I and III. Proc Natl Acad Sci USA 73:3511–3515
Wickner S, Hurwitz J (1974) Conversion of ΦX174 viral DNA to double-stranded form by purified Escherichia coli proteins. Proc Natl Acad Sci USA 71:4120–4124
Wu YH, Franden MA, Hawker JR, McHenry CS (1984) Monoclonal antibodies specific for the a subunit of the Escherichia coli DNA polymerase III holoenzyme. J Biol Chem 259:12117–12122
Xiao H, Crombie R, Dong Z, Onrust R, O’Donnell M (1993a) DNA polymerase III accessory proteins. III. holC and holD encoding χ and ψ. J Biol Chem 268:11773–11778
Xiao H, Dong Z, O’Donnell M (1993b) DNA polymerase III accessory proteins. IV. Characterization of χ and ψ. J Biol Chem 268:11779–11784
Xiong Y, Zhang H, Beach D (1993) D type cyclins associate with multiple protein kinases and the DNA replication and repair factor PCNA. Cell 71:505–514
Yoder BL, Burgers PMJ (1991) Saccharomyces cerevisiae replication factor C. I. Purification and characterization of its ATPase activity. J Biol Chem 266:22689–22697
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1994 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
O’donnell, M., Kuriyan, J., Kong, XP., Stukenberg, P.T., Onrust, R., Yao, N. (1994). The β Sliding Clamp of E. coli DNA Polymerase III Holoenzyme Balances Opposing Functions. In: Eckstein, F., Lilley, D.M.J. (eds) Nucleic Acids and Molecular Biology. Nucleic Acids and Molecular Biology, vol 8. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-78666-2_11
Download citation
DOI: https://doi.org/10.1007/978-3-642-78666-2_11
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-78668-6
Online ISBN: 978-3-642-78666-2
eBook Packages: Springer Book Archive