Site-directed mutagenesis of the χ subunit of DNA polymerase III and single-stranded DNA-binding protein of E. coli reveals key residues for their interaction

Nucleic Acids Research

Volumn 39, Issue 4, 2011, Pages 1398-1407

  Naue, Natalie ^a   Fedorov, Roman ^a   Pich, Andreas ^a   Manstein, Dietmar J ^a   Curth, Ute ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE GAMMA; EXONUCLEASE; GLYCINE; PHENYLALANINE; RECQ HELICASE; SINGLE STRANDED DNA BINDING PROTEIN; TYROSINE;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME SUBUNIT; GENETIC CONSERVATION; HYDROPHOBICITY; MASS SPECTROMETRY; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN INTERACTION; SITE DIRECTED MUTAGENESIS; ULTRACENTRIFUGATION;

BINDING SITES; DNA POLYMERASE III; DNA-BINDING PROTEINS; ESCHERICHIA COLI PROTEINS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LYSINE; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PHENYLALANINE; PROTEIN BINDING; TYROSINE;

ESCHERICHIA COLI;

EID: 79952323279     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq988     Document Type: Article

References (51)

1. Lohman, T.M. and Ferrari, M.E. (1994) Escherichia coli single-stranded DNA-binding protein: multiple DNA-binding modes and cooperativities. Annu. Rev. Biochem., 63, 527-570.
2. Mushegian, A.R. and Koonin, E.V. (1996) A minimal gene set for cellular life derived by comparison of complete bacterial genomes. Proc. Natl Acad. Sci. USA, 93, 10268-10273. (Pubitemid 26314611)
3. Sigal, N., Delius, H., Kornberg, T., Gefter, M.L. and Alberts, B. (1972) A DNA-unwinding protein isolated from Escherichia coli: its interaction with DNA and with DNA polymerases. Proc. Natl Acad. Sci. USA, 69, 3537-3541.
4. Molineux, I.J., Pauli, A. and Gefter, M.L. (1975) Physical studies of the interaction between the Escherichia coli DNA binding protein and nucleic acids. Nucleic Acids Res., 2, 1821-1837.
5. Kuzminov, A. (1995) A mechanism for induction of the SOS response in E. coli: insights into the regulation of reversible protein polymerization in vivo. J. Theor. Biol., 177, 29-43.
6. Meyer, R.R. and Laine, P.S. (1990) The single-stranded DNA-binding protein of Escherichia coli. Microbiol. Rev., 54, 342-380. (Pubitemid 120004379)
7. Kowalczykowski, S.C., Dixon, D.A., Eggleston, A.K., Lauder, S.D. and Rehrauer, W.M. (1994) Biochemistry of homologous recombination in Escherichia coli. Microbiol. Rev., 58, 401-465.
8. Kuzminov, A. (1999) Recombinational repair of DNA damage in Escherichia coli and bacteriophage lambda. Microbiol. Mol. Biol. Rev., 63, 751-813.
9. Kuzminov, A. (2001) DNA replication meets genetic exchange: chromosomal damage and its repair by homologous recombination. Proc. Natl Acad. Sci. USA, 98, 8461-8468. (Pubitemid 32678050)
10. Williams, K.R., Spicer, E.K., LoPresti, M.B., Guggenheimer, R.A. and Chase, J.W. (1983) Limited proteolysis studies on the Escherichia coli single-stranded DNA binding protein. Evidence for a functionally homologous domain in both the Escherichia coli and T4 DNA binding proteins. J. Biol. Chem., 258, 3346-3355. (Pubitemid 13130245)
11. Casas-Finet, J.R., Khamis, M.I., Maki, A.H. and Chase, J.W. (1987) Tryptophan 54 and phenylalanine 60 are involved synergistically in the binding of E. coli SSB protein to single-stranded polynucleotides. FEBS Lett., 220, 347-352.
12. Raghunathan, S., Kozlov, A.G., Lohman, T.M. and Waksman, G. (2000) Structure of the DNA binding domain of E. coli SSB bound to ssDNA. Nat. Struct. Biol., 7, 648-652. (Pubitemid 30636675)
13. Yuzhakov, A., Kelman, Z. and 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.
14. Kelman, Z., Yuzhakov, A., Andjelkovic, J. and O'Donnell, M. (1998) Devoted to the lagging strand-the w subunit of DNA polymerase III holoenzyme contacts SSB to promote processive elongation and sliding clamp assembly. EMBO J., 17, 2436-2449. (Pubitemid 28171927)
15. Sandigursky, M., Mendez, F., Bases, R.E., Matsumoto, T. and Franklin, W.A. (1996) Protein-protein interactions between the Escherichia coli single-stranded DNA-binding protein and exonuclease I. Radiat. Res., 145, 619-623. (Pubitemid 26127862)
16. Genschel, J., Curth, U. and 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. (Pubitemid 30179552)
17. Shereda, R.D., Bernstein, D.A. and Keck, J.L. (2007) A central role for SSB in Escherichia coli RecQ DNA helicase function. J. Biol. Chem., 282, 19247-19258. (Pubitemid 47100133)
18. Shereda, R.D., Kozlov, A.G., Lohman, T.M., Cox, M.M. and Keck, J.L. (2008) SSB as an organizer/mobilizer of genome maintenance complexes. Crit. Rev. Biochem. Mol. Biol., 43, 289-318.
19. Curth, U., Urbanke, C., Greipel, J., Gerberding, H., Tiranti, V. and Zeviani, M. (1994) Single-stranded-DNA-binding proteins from human mitochondria and Escherichia coli have analogous physicochemical properties. Eur. J. Biochem., 221, 435-443. (Pubitemid 24120589)
20. Curth, U., Genschel, J., Urbanke, C. and Greipel, J. (1996) In vitro and in vivo function of the C-terminus of Escherichia coli single-stranded DNA binding protein. Nucleic Acids Res., 24, 2706-2711. (Pubitemid 26239738)
21. Wang, T.C. and Smith, K.C. (1982) Effects of the ssb-1 and ssb-113 mutations on survival and DNA repair in UV-irradiated delta uvrB strains of Escherichia coli K-12. J. Bacteriol., 151, 186-192. (Pubitemid 12022322)
22. Chase, J.W., L'Italien, J.J., Murphy, J.B., Spicer, E.K. and Williams, K.R. (1984) Characterization of the Escherichia coli SSB-113 mutant single-stranded DNA-binding protein. Cloning of the gene, DNA and protein sequence analysis, high pressure liquid chromatography peptide mapping, and DNA-binding studies. J. Biol. Chem., 259, 805-814. (Pubitemid 14192144)
23. Greenberg, J., Berends, L.J., Donch, J. and Green, M.H. (1974) exrB: a malB-linked gene in Escherichia coli B involved in sensitivity to radiation and filament formation. Genet. Res., 23, 175-184.
24. Johnson, B.F. (1984) Two-dimensional electrophoretic analysis of the regulation of SOS proteins in three ssb mutants. Arch. Microbiol., 138, 106-112. (Pubitemid 14078370)
25. Witte, G., Urbanke, C. and Curth, U. (2003) DNA polymerase III chi subunit ties single-stranded DNA binding protein to the bacterial replication machinery. Nucleic Acids Res., 31, 4434-4440. (Pubitemid 37441804)
26. Glover, B.P. and McHenry, C.S. (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)
27. Fedorov, R., Witte, G., Urbanke, C., Manstein, D.J. and Curth, U. (2006) 3D structure of Thermus aquaticus single-stranded DNA-binding protein gives insight into the functioning of SSB proteins. Nucleic Acids Res., 34, 6708-6717. (Pubitemid 46019402)
28. Gulbis, J.M., Kazmirski, S.L., Finkelstein, J., Kelman, Z., O'Donnell, M. and Kuriyan, J. (2004) Crystal structure of the chi:psi sub-assembly of the Escherichia coli DNA polymerase clamp-loader complex. Eur. J. Biochem., 271, 439-449. (Pubitemid 38130471)
29. Lu, D. and Keck, J.L. (2008) Structural basis of Escherichia coli single-stranded DNA-binding protein stimulation of exonuclease I. Proc. Natl Acad. Sci. USA, 105, 9169-9174.
30. Shereda, R.D., Reiter, N.J., Butcher, S.E. and Keck, J.L. (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.
31. Laue, T., Shah, B., Ridgeway, T. and Pelletier, S. (1992) Computer-aided interpretation of analytical sedimentation data for proteins. In Harding, S., Rowe, A. and Horton, J. (eds), The Royal Society of Chemistry, Cambridge, UK, pp. 378-387.
32. Pace, C.N., Vajdos, F., Fee, L., Grimsley, G. and Gray, T. (1995) How to measure and predict the molar absorption coefficient of a protein. Protein Sci., 4, 2411-2423.
33. Lohman, T.M. and Overman, L.B. (1985) Two binding modes in Escherichia coli single strand binding protein-single stranded DNA complexes. Modulation by NaCl concentration. J. Biol. Chem., 260, 3594-3603. (Pubitemid 15114361)
34. Bayer, I., Fliess, A., Greipel, J., Urbanke, C. and Maass, G. (1989) Modulation of the affinity of the single-stranded DNA-binding protein of Escherichia coli (E. coli SSB) to poly(dT) by site-directed mutagenesis. Eur. J. Biochem., 179, 399-404. (Pubitemid 19051582)
35. Landwehr, M., Curth, U. and Urbanke, C. (2002) A dimeric mutant of the homotetrameric single-stranded DNA binding protein from Escherichia coli. Biol. Chem., 383, 1325-1333. (Pubitemid 35282950)
36. Lohman, T.M., Green, J.M. and Beyer, R.S. (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)
37. Xiao, H., Crombie, R., Dong, Z., Onrust, R. and 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)
38. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J., 78, 1606-1619. (Pubitemid 30141584)
39. Dam, J. and Schuck, P. (2005) Sedimentation velocity analysis of heterogeneous protein-protein interactions: sedimentation coefficient distributions c(s) and asymptotic boundary profiles from Gilbert-Jenkins theory. Biophys. J., 89, 651-666. (Pubitemid 41098316)
40. Witte, G., Fedorov, R. and Curth, U. (2008) Biophysical analysis of Thermus aquaticus single-stranded DNA binding protein. Biophys. J., 94, 2269-2279.
41. Porter, R.D., Black, S., Pannuri, S. and Carlson, A. (1990) Use of the Escherichia coli SSB gene to prevent bioreactor takeover by plasmidless cells. Biotechnology, 8, 47-51. (Pubitemid 20028200)
42. de Vries, J. and Wackernagel, W. (1992) Recombination and UV resistance of Escherichia coli with the cloned recA and recBCD genes of Serratia marcescens and Proteus mirabilis: evidence for an advantage of intraspecies combination of P. mirabilis RecA protein and RecBCD enzyme. J. Gen. Microbiol., 138, 31-38.
43. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, NY.
44. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
45. Muetzelburg, M.V., Hofmann, F., Just, I. and Pich, A. (2009) Identification of biomarkers indicating cellular changes after treatment of neuronal cells with the C3 exoenzyme from Clostridium botulinum using the iTRAQ protocol and LC-MS/MS analysis. J. Chromatogr. B. Analyt Technol. Biomed. Life Sci., 877, 1344-1351.
46. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr., 60, 2126-2132. (Pubitemid 41742764)
47. Krissinel, E. and Henrick, K. (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D Biol. Crystallogr., 60, 2256-2268. (Pubitemid 41742778)
48. Brunger, 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. et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr., 54, 905-921.
49. Dam, J., Velikovsky, C.A., Mariuzza, R.A., Urbanke, C. and Schuck, P. (2005) Sedimentation velocity analysis of heterogeneous protein-protein interactions: Lamm equation modeling and sedimentation coefficient distributions c(s). Biophys. J., 89, 619-634. (Pubitemid 41098314)
50. Kozlov, A.G., Jezewska, M.J., Bujalowski, W. and Lohman, T.M. (2010) Binding specificity of Escherichia coli single-stranded DNA binding protein for the chi subunit of DNA pol III holoenzyme and PriA helicase. Biochemistry, 49, 3555-3566.
51. Landau, M., Mayrose, I., Rosenberg, Y., Glaser, F., Martz, E., Pupko, T. and Ben-Tal, N. (2005) ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res., 33, W299-W302. (Pubitemid 44529930)