Structure of the SSB-DNA polymerase III interface and its role in DNA replication

EMBO Journal

Volumn 30, Issue 20, 2011, Pages 4236-4247

  Marceau, Aimee H ^a   Bahng, Soon ^b   Massoni, Shawn C ^c   George, Nicholas P ^a   Sandler, Steven J ^c   Marians, Kenneth J ^b   Keck, James L ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

DNA replication; genome maintenance; protein interaction; X ray crystal structure

Indexed keywords

DNA POLYMERASE; REPLISOME; SINGLE STRANDED DNA BINDING PROTEIN;

ARTICLE; BIOCHEMISTRY; CELL CYCLE; CRYSTALLOGRAPHY; DNA REPLICATION; DNA STRUCTURE; DNA SYNTHESIS; ESCHERICHIA COLI; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; TEMPERATURE DEPENDENCE; UTILIZATION REVIEW;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASE SEQUENCE; DNA POLYMERASE III; DNA REPLICATION; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HOLOENZYMES; MOLECULAR SEQUENCE DATA;

ESCHERICHIA COLI;

EID: 80054954986     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.305     Document Type: Article

References (52)

1. Alberts BM, Barry J, Bedinger P, Formosa T, Jongeneel CV, Kreuzer KN (1983) Studies on DNA replication in the bacteriophage T4 in vitro system. Cold Spring Harb Symp Quant Biol 47 (Part 2): 655-668
2. Arai K, Kornberg A (1979) A general priming system employing only dnaB protein and primase for DNA replication. Proc Natl Acad Sci USA 76: 4308-4312 (Pubitemid 9256551)
3. Bloom LB (2006) Dynamics of loading theEscherichia coli DNA polymerase processivity clamp. Crit Rev Biochem Mol Biol 41: 179-208
4. Courcelle CT, Courcelle J (2006) Monitoring DNA replication following UV-induced damage in Escherichia coli. Methods Enzymol 409: 425-441
5. Datsenko KA (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci 97: 6640-6645 (Pubitemid 30412767)
6. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645 (Pubitemid 30412767)
7. Downey CD, McHenry CS (2010) Chaperoning of a replicative polymerase onto a newly assembled DNA-bound sliding clamp by the clamp loader. Mol Cell 37: 481-491
8. Dri AM, Rouviere-Yaniv J, Moreau PL (1991) Inhibition of cell division in hupA hupB mutant bacteria lacking HU protein. J Bact 173: 2852-2863
9. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132 (Pubitemid 41742764)
10. Flores MJ, Bierne H, Ehrlich SD, Michel B (2001) Impairment of lagging strand synthesis triggers the formation of a RuvABC substrate at replication forks. EMBO J 20: 619-629 (Pubitemid 32126997)
11. Flores MJ, Ehrlich SD, Michel B (2002) Primosome assembly requirement for replication restart in the Escherichia coli holDG10 replication mutant. Mol Microbiol 44: 783-792 (Pubitemid 34526588)
12. Glover BP, McHenry CS (1998) The chi psi 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 (Pubitemid 28417539)
13. Glover BP, McHenry CS (2001) The DNA polymerase III holoen-zyme: an asymmetric dimeric replicative complex with leading and lagging strand polymerases. Cell 105: 925-934 (Pubitemid 32635093)
14. Greenberg J, Donch J (1974) Sensitivity to elevated temperatures in exrB strains of Escherichia coli. Mutat Res 25: 403-405
15. Gulbis JM, Kazmirski SL, Finkelstein J, Kelman Z, O'Donnell M, Kuriyan J (2004) Crystal structure of the chi:psi subassembly of the Escherichia coli DNA polymerase clamp-loader complex. Eur J Biochem 271: 439-449 (Pubitemid 38130471)
16. Heller RC, Marians KJ (2006) Replication fork reactivation downstream of a blocked nascent leading strand. Nature 439: 557-562 (Pubitemid 43185374)
17. Hiasa H, DiGate RJ, Marians KJ (1994) Decatenating activity of Escherichia coli DNA gyrase and topoisomerases I and III during oriC and pBR322 DNA replication in vitro. J Biol Chem 269: 2093-2099 (Pubitemid 24035419)
18. Johnson A, O'Donnell M (2005) Cellular DNA replicases: components and dynamics at the replication fork. Annu Rev Biochem 74: 283-315 (Pubitemid 40995509)
19. Kelman Z, O'Donnell M (1995) DNA polymerase III holoenzyme: structure and function of a chromosomal replicating machine. Annu Rev Biochem 64: 171-200
20. Kelman Z, Yuzhakov A, Andjelkovic J, O'Donnell M (1998) Devoted to the lagging strand-the subunit of DNA polymerase III holoen-zyme contacts SSB to promote processive elongation and sliding clamp assembly. EMBO J 17: 2436-2449 (Pubitemid 28171927)
21. Kozlov AG, Cox MM, Lohman TM (2010a) Regulation of single-stranded DNA binding by the C termini of Escherichia coli single-stranded DNA-binding (SSB) protein. J Biol Chem 285: 17246-17252
22. Kozlov AG, Jezewska MJ, Bujalowski W, Lohman TM (2010b) Binding specificity of Escherichia coli single-stranded DNA binding protein for the w subunit of DNA pol III holoenzyme and PriA helicase. Biochemistry 49: 3555-3566
23. Lohman TM, Green JM, Beyer RS (1986) Large-scale overproduction and rapid purification of the Escherichia coli ssb gene product. Expression of the ssb gene under lambda PL control. Biochemistry 25: 21-25 (Pubitemid 16053074)
24. Lu D, Keck JL (2008) Structural basis of Escherichia coli single-stranded DNA-binding protein stimulation of exonuclease I. Proc Natl Acad Sci USA 105: 9169-9174
25. McCool JD, Long E, Petrosino JF, Sandler HA, Rosenberg SM, Sandler SJ (2004) Measurement of SOS expression in individual Escherichia coli K-12 cells using fluorescence microscopy. Mol Microbiol 53: 1343-1357 (Pubitemid 39209109)
26. McCool JD, Sandler SJ (2001) Effects of mutations involving cell division, recombination, and chromosome dimer resolution on a priA2Hkan mutant. Proc Natl Acad Sci USA 98: 8203-8210 (Pubitemid 32678014)
27. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674 (Pubitemid 47080256)
28. Meyer RR, Glassberg J, Kornberg A (1979) An Escherichia coli mutant defective in single-strand binding protein is defective in DNA replication. Proc Natl Acad Sci USA 76: 1702-1705 (Pubitemid 9175383)
29. Murli S, Opperman T, Smith BT, Walker GC (2000) A role for the umuDC gene products of Escherichia coli in increasing resistance to DNA damage in stationary phase by inhibiting the transition to exponential growth. J Bacteriol 182: 1127-1135 (Pubitemid 30075037)
30. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macro-molecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255 (Pubitemid 27235885)
31. Naue N, Fedorov R, Pich A, Manstein DJ, Curth U (2011) Site-directed mutagenesis of the {chi} subunit of DNA polymerase III and single-stranded DNA-binding protein of E. coli reveals key residues for their interaction. Nucleic Acids Res 39: 1398-1407
32. Nordman J, Skovgaard O, Wright A (2007) A novel class of mutations that affect DNA replication in E. coli. Mol Microbiol 64: 125-138 (Pubitemid 46435043)
33. Oakley GG, Patrick SM (2010) Replication protein A: directing traffic at the intersection of replication and repair. Front Biosci 15: 883-900
34. Olson MW, Dallmann HG, McHenry CS (1995) DnaX complex of Escherichia coli DNA polymerase III holoenzyme. The chi psi complex functions by increasing the affinity of tau and gamma for delta.delta0 to a physiologically relevant range. J Biol Chem 270: 29570-29577
35. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326 (Pubitemid 27085611)
36. Saveson CJ, Lovett ST (1997) Enhanced deletion formation by aberrant DNA replication in Escherichia coli. Genetics 146: 457-470 (Pubitemid 27251385)
37. Shereda RD, Kozlov AG, Lohman TM, Cox MM, Keck JL (2008) SSB as an organizer/mobilizer of genome maintenance complexes. Crit Rev Biochem Mol Biol 43: 289-318
38. Shereda RD, Reiter NJ, Butcher SE, Keck JL (2009) Identification of the SSB binding site on E. coli RecQ reveals a conserved surface for binding SSB's C terminus. J Mol Biol 386: 612-625
39. Simonetta KR, Kazmirski SL, Goedken ER, Cantor AJ, Kelch BA, McNally R, Seyedin SN, Makino DL, O'Donnell M, Kuriyan J (2009) The mechanism of ATP-dependent primer-template recognition by a clamp loader complex. Cell 137: 659-671
40. Stukenberg PT, Studwell-Vaughan PS, O'Donnell M (1991) Mechanism of the sliding beta-clamp of DNA polymerase III holoenzyme. J Biol Chem 266: 11328-11334 (Pubitemid 21906950)
41. Tougu K, Peng H, Marians KJ (1994) Identification of a domain of Escherichia coli primase required for functional interaction with the DnaB helicase at the replication fork. J Biol Chem 269: 4675-4682 (Pubitemid 24237842)
42. Van Oijen AM, Loparo JJ (2010) Single-molecule studies of the replisome. Annu Rev Biophys 39: 429-448
43. Viguera E, Petranovic M, Zahradka D, Germain K, Ehrlich DS, Michel B (2003) Lethality of bypass polymerases in Escherichia coli cells with a defective clamp loader complex of DNA poly-merase III. Mol Microbiol 50: 193-204 (Pubitemid 37222797)
44. Wery M, Woldringh CL, Rouviere-Yaniv J (2001) HU-GFP and DAPI co-localize on the Escherichia coli nucleoid. Biochimie 83: 193-200 (Pubitemid 32243564)
45. Wickner W, Schekman R, Geider K, Kornberg A (1973) A new form of DNA polymerase 3 and a copolymerase replicate a long, single-stranded primer-template. Proc Natl Acad Sci USA 70: 1764-1767
46. Wu CA, Zechner EL, Marians KJ (1992a) Coordinated leading-and lagging-strand synthesis at the Escherichia coli DNA replication fork. I. Multiple effectors act to modulate Okazaki fragment size. J Biol Chem 267: 4030-4044
47. Wu CA, Zechner EL, Reems JA, McHenry CS, Marians KJ (1992b) Coordinated leading-and lagging-strand synthesis at the Escherichia coli DNA replication fork. V. Primase action regulates the cycle of Okazaki fragment synthesis. J Biol Chem 267: 4074-4083
48. Xiao H, Crombie R, Dong Z, Onrust R, O'Donnell M (1993) DNA polymerase III accessory proteins. III. holC and holD encoding chi and psi. J Biol Chem 268: 11773-11778 (Pubitemid 23168129)
49. Xu L, Marians KJ (2000) Purification and characterization of DnaC810, a primosomal protein capable of bypassing PriA function. J Biol Chem 275: 8196-8205 (Pubitemid 30159736)
50. Yuan Q, McHenry CS (2009) Strand displacement by DNA poly-merase III occurs through a tau-psi-chi link to single-stranded DNA-binding protein coating the lagging strand template. J Biol Chem 284: 31672-31679
51. Yuzhakov A, Kelman Z, O'Donnell M (1999) Trading places on DNA-a three-point switch underlies primer handoff from pri-mase to the replicative DNA polymerase. Cell 96: 153-163
52. Zechner EL, Wu CA, Marians KJ (1992) Coordinated leading-and lagging-strand synthesis at the Escherichia coli DNA replication fork. II. Frequency of primer synthesis and efficiency of primer utilization control Okazaki fragment size. J Biol Chem 267: 4045-4053