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DNA Repair pp 103–123Cite as

Functional Domains of the E. coli UvrABC Proteins in Nucleotide Excision Repair

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Part of the book series: Nucleic Acids and Molecular Biology ((NUCLEIC,volume 12))

Abstract

Different classes of DNA repair systems exist to counteract the effect of the many forms of DNA damage that are generated by exposure of living cells to ultraviolet or ionising radiation and a variety of chemicals. Of these repair systems the nucleotide excision repair pathway is unique in its ability to recognise and repair a vast array of structurally unrelated DNA lesions (see Van Houten 1990 for review). The principles of nucleotide excision repair are the same in prokaryotic and eukaryotic organisms. After recognition of a DNA lesion, incisions are made in the damaged strand on both sides of the lesion, the oligonucleotide containing the lesion is removed, and the resulting gap is filled by DNA synthesis followed by ligation of the remaining nick. The proteins involved in the prokaryotic system, however, differ from those of the eukaryotic system, indicating that the two repair processes are not evolutionaryly related. Whereas eukaryotic nucleotide excision repair requires about 30 polypeptides (Sancar 1996), just 6 proteins (UvrA, UvrB, UvrC, UvrD, DNA polymerase (Pol) I and ligase) are sufficient for carrying out the repair process in E. coli.

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References

  • Belguise-Valladier P, Fuchs RPP (1991) Strong sequence dependent polymorphism in adduct-induced DNA structure. Analysis of single N-2-acetylaminofluorene residues bound within the NarI mutation hotspot. Biochemistry 30: 10091–10100

    Article  PubMed  CAS  Google Scholar 

  • Berg JM (1990) Zinc fingers and other metal-binding domain-elements for interactions between macromolecules. J Biol Chem 265: 6513–6515

    PubMed  CAS  Google Scholar 

  • Bertrand-Burggraf E, Selby CP, Hearst JE, Sancar A (1991) Identification of the different intermediates in the interaction of (A)BC excinuclease with its substrates by DNase I footprinting on two uniquely modified oligonucleoties. J Mol Biol 219: 27–36.

    Article  PubMed  CAS  Google Scholar 

  • Dean M, Allikmets R (1995) Evolution of ATP-binding cassette transporter genes. Curr Opin Gen Dev 5: 779–785

    Article  CAS  Google Scholar 

  • Delagoutte E, Bertrand-Burggraf E, Dunand J, Fuchs RPP (1997) Sequencedependent modulation of nucleotide excision repair: the efficiency of the incision reaction is inversely correlated with the stability of the preincision UvrB-DNA complex. J Mol Biol 266: 703–710

    Article  PubMed  CAS  Google Scholar 

  • Doherty AJ, Serpell LC, Ponting CP (1996) The helix-hairpin-helix DNA-binding motif. A structural basis for non-sequence-specific recognition of DNA. Nucleic Acids Res 24: 2488–2497

    Article  PubMed  CAS  Google Scholar 

  • Doolittle RF, Johnson MS, Husain I, van Houten B, Thomas DC, Sancar A (1986) Domainal evolution of a prokaryotic DNA-repair protein and its relationship to active-transport proteins. Nature 323: 451–453.

    Article  PubMed  CAS  Google Scholar 

  • Gorbalenya AE, Koonin EV (1990) Superfamily of UvrA-related NTP-binding proteins. Implications for rational classification of recombination repair systems. J Mol Biol 213: 583–591

    Article  PubMed  CAS  Google Scholar 

  • Gorbalenya AE, Koonin EV (1993) Helicases. Amino acid sequence comparisons and structure-function relationships. Curr Opin Struct Biol 3: 419–429

    Article  CAS  Google Scholar 

  • Gorbalenya AE, Koonin EV, Donchenko AP, Blinov VM (1989) Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes. Nucleic Acids Res 17: 4713–4730

    Article  PubMed  CAS  Google Scholar 

  • Gordienko I, Rupp WD (1997) The limited strand-separating activity of the UvrAB complex and its role in the recognition of DNA damage. EMBO J 16: 889–895

    Article  PubMed  CAS  Google Scholar 

  • Hsu DS, Kim ST, Sun Q, Sancar A (1995) Structure and function of the UvrB protein. J Biol Chem 270: 8319–8327

    Article  PubMed  CAS  Google Scholar 

  • Hyde SC, Emsley P, Hartshorn MJ, Mimmack MM, Gileadi U, Pearce SR, Gallagher MP, Gill DP, Hubbard RE, Higgins CF (1990) Structural model of ATP-binding proteins associated with cystic fibrosis, multidrug resistance and bacterial transport. Nature 346: 362–365

    Article  PubMed  CAS  Google Scholar 

  • Kim Y, Eom SH, Wang J, Lee DS, Suh SW, Steitz TA (1995) Crystal structure of Thermus aquaticus DNA polymerase. Nature 376: 612–616

    Article  PubMed  CAS  Google Scholar 

  • Koo HS, Claassen L, Grossman L, Liu LF (1991) ATP-dependent partitioning of the DNA-template into supercoiled domains by Escherichia coli UvrAB. Proc Natl Acad Sci USA 88: 1212–1216

    Article  PubMed  CAS  Google Scholar 

  • Kovalsky OI, Grossman L (1994) The use of monoclonal antibodies for studying intermediates in DNA repair by the Escherichia coli Uvr(A)BC endonuclease. J Biol Chem 269: 27421–27426

    PubMed  CAS  Google Scholar 

  • Labahn J, Schrarer OD, Long A, Ezaz-Nikpay K, Verdine GL, Ellenberger TE (1996) Structural basis for the excision repair of alkylation-damaged DNA. Cell 86: 321–329

    Article  CAS  Google Scholar 

  • Lin JJ, Sancar A (1990) Reconstitution of nucleotide excision nuclease with UvrA and UvrB proteins from Escherichia coli and UvrC protein from Bacillus subtilis. J Biol Chem 265: 21337–21341

    CAS  Google Scholar 

  • Lin JJ, Sancar A (1992) Active site of (A)BC excinuclease. 1. Evidence for 5′ incision by UvrC through a catalytic site involving Asp399, Asp438, Asp466 and His538 residues. J Biol Chem 267: 17688–17692

    CAS  Google Scholar 

  • Lin JJ, Phillips AM, Hearst JE, Sancar A (1992) Active site of (A)BC excinuclease. 2. Binding, bending and catalysis mutants of UvrB reveal a direct role in 3′ and an indirect role in 5′ incision. J Biol Chem 267: 17693–17700

    PubMed  CAS  Google Scholar 

  • Lomovskaya N, Hong SK, Kim SU, Fonstein L, Furuya K, Hutchinson CR (1996) The Streptomyces peucetius DrrC gene encodes a UvrA-like protein involved in daunorubicin resistance and production. J Bacteriol 178: 3238–3245

    CAS  Google Scholar 

  • Lupas A, van Dijke M, Stock J (1991) Predicting coiled coils from protein sequences. Science 252: 1162–1164

    Article  CAS  Google Scholar 

  • Mazur SJ, Grossman L (1991) Dimerization of Escherichia coli UvrA and its binding to undamaged and ultraviolet-light damaged DNA. Biochemistry 30: 4432–4443

    Article  PubMed  CAS  Google Scholar 

  • Moolenaar GF, Visse R, Ortiz-Buysse M, Goosen N, van de Putte P (1994) Helicase motif V and motif VI of the Escherichia coli UvrB protein of the UvrABC endonuclease are essential for the formation of the preincision complex. J Mol Biol 240: 294–307

    Article  PubMed  CAS  Google Scholar 

  • Moolenaar GF, Franken KLMC, Dijkstra DM, Thomas-Oates JE, Visse R, van de Putte P, Goosen N (1995) The C-terminal region of the UvrB protein of Escherichia coli contains an important determinant for UvrC binding to the preincision complex but not the catalytic site for 3′-incision. J Biol Chem 270: 30508–30515

    Article  PubMed  CAS  Google Scholar 

  • Moolenaar GF, Franken KLMC, van de Putte P, Goosen N (1998a) Function of the homologous regions of the Escherichia coli DNA excision repair proteins UvrB and UvrC in stabilization of the UvrBC-DNA complex in 3′-incision. Mutat Res 385: 195–203

    Google Scholar 

  • Moolenaar GF, Schoot Uiterkamp R, Zwijnenburg DA, Goosen N (1998b) The C-terminal region of the Escherichia coli UvrC protein, which is homologous to the C-terminal region of the human ERCC1 protein, is involved in DNA binding and 5′-incision. Nucleic Acids Res 26: 462–468

    Article  PubMed  CAS  Google Scholar 

  • Munn MM, Rupp WD (1992) Interaction of the UvrABC endonuclease with DNA containing a psoralen monoadduct or cross-link. Differential effects of superhelical density and comparison of preincision complexes. J Biol Chem 266: 24748–24756

    Google Scholar 

  • Myles GM, Sancar A (1991) Isolation and characterization of functional domains of UvrA. Biochemistry 30: 3834–3840

    Article  PubMed  CAS  Google Scholar 

  • Navaratnam S, Myles GM, Strange RW, Sancar A (1989) Evidence from extended X-ray absorption fine-structure and site-specific mutagenesis for zinc fingers in UvrA protein of Escherichia coli. J Biol Chem 264: 16067–16071

    PubMed  CAS  Google Scholar 

  • Oh EY, Grossman L (1986) The effect of Escherichia coli Uvr protein-binding on the topology of supercoiled DNA. Nucleic Acids Res 14: 8557–8571

    Article  PubMed  CAS  Google Scholar 

  • Oh EY, Grossman L (1987) Helicase properties of the Escherichia coli UvrAB protein complex. Proc Natl Acad Sci USA 84: 3638–3642

    Article  PubMed  CAS  Google Scholar 

  • Oh EY, Claassen L, Thiagalingam S, Mazur S, Grossman L (1989) ATPase activity of the UvrA and UvrB protein complexes of the Escherichia coli UvrABC endonuclease. Nucleic Acids Res 17: 4145–4159

    Article  PubMed  CAS  Google Scholar 

  • Oleykowski CA, Mayernik JA, Lim SE, Groopman JD, Grossman L, Wogan GN, Yeung AT (1993) Repair of aflatoxin-B1 DNA adducts by the UvrABC endonuclease of Escherichia coli. J Biol Chem 268: 7990–8002

    PubMed  CAS  Google Scholar 

  • Orren DK, Sancar A (1989) The (A)BC excinuclease of Escherichia coli has only the UvrB and UvrC subunits in the incision complex. Proc Natl Acad Sci USA 86: 5237–5241

    Article  PubMed  CAS  Google Scholar 

  • Orren DK, Sancar A (1990) Formation and enzymatic properties of the UvrB-DNA complex. J Biol Chem 265: 15796–15803

    PubMed  CAS  Google Scholar 

  • Orren DK, Selby CP, Hearst JE, Sancar A (1992) Post-incision steps of nucleotide excision repair in Escherichia coli. Disassembly of the UvrBC-DNA complex by helicase II and DNA polymerase I. J Biol Chem 267: 780–788

    PubMed  CAS  Google Scholar 

  • Pu WT, Kahn R, Munn MM, Rupp WD (1989) UvrABC incision of normalmethylmitomycin-A-DNA monoadducts and cross-links. J Biol Chem 264: 20697–20704

    PubMed  CAS  Google Scholar 

  • Sancar A (1996) DNA excision-repair. Annu Rev Biochem 65: 43–63

    Article  PubMed  CAS  Google Scholar 

  • Sancar A, Hearst JE (1993) Molecular matchmakers. Science 259: 1415–1420

    Article  PubMed  CAS  Google Scholar 

  • Sancar A, Rupp WD (1983) A novel repair enzyme: UvrABC excision nuclease of Escherichia coli cuts a DNA strand on both sides of the damaged region. Cell 33: 249–260

    Article  PubMed  CAS  Google Scholar 

  • Sancar A, Tang M (1993) Nucleotide excision repair. Photochem Photobiol 57: 905–921

    Article  PubMed  CAS  Google Scholar 

  • Seeberg E (1978) Reconstitution of an Escherichia coli repair endonuclease activity from the separated uvrA and uvrB/uvrC gene products. Proc Natl Acad Sci USA 75: 2569–2573

    Article  PubMed  CAS  Google Scholar 

  • Seeberg E, Steinum A (1982) Purification and properties of the UvrA protein from Escherichia coli. Proc Natl Acad Sci USA 79: 988–992

    Article  PubMed  CAS  Google Scholar 

  • Seeberg E, Nissen-Meyer J, Strike P (1976) Incision of ultraviolet-irradiated DNA by extracts of E. coli requires three different gene products. Nature 263: 524–526

    Article  PubMed  CAS  Google Scholar 

  • Seeley TW, Grossman L (1989) Mutations in the Escherichia coli UvrB ATPase motif compromise excision repair capacity. Proc Natl Acad Sci USA 86: 6577–6581

    Article  PubMed  CAS  Google Scholar 

  • Selby CP, Sancar A (1988) ABC excinuclease incises both 5′ and 3′ to the CC-1065-DNA adduct and its incision activity is stimulated by helicase II and DNA polymerase I. Biochemistry 27: 7184–7188

    Article  PubMed  CAS  Google Scholar 

  • Selby CP, Sancar A (1993) Molecular mechanism of transcription-repair coupling. Science 260: 53–58

    Article  PubMed  CAS  Google Scholar 

  • Shi Q, Thresher R, Sancar A, Griffith J (1992) Electron-microscopic study of (A)BC excinuclease. DNA is sharply bent in the UvrB-DNA complex. J Mol Biol 226: 425–432

    Article  PubMed  CAS  Google Scholar 

  • Sijbers AM, van der Spek PJ, Odijk H, van den Berg J, van Duin M, Westerveld A, Jaspers NGJ, Bootsma D, Hoeijmakers JHJ (1996) Mutational analysis of the human nucleotide excision repair gene ERCC1. Nucleic Acids Res 24: 3370–3380

    Article  PubMed  CAS  Google Scholar 

  • Snowden A, van Houten B (1991) Initiation of the UvrABC nuclease activity reaction. Efficiency of incision is not correlated with UvrA binding affinity. J Mol Biol 220: 19–33

    Article  PubMed  CAS  Google Scholar 

  • Subramanya H, Bird LE, Brannigan JA, Wigley DB (1996) Crystal structure of a DEXX box DNA helicase. Nature 384: 379–383

    Article  PubMed  CAS  Google Scholar 

  • Swenson DH, Li LH, Hurley LH, Rokem JS, Petzgold GL, Dayton BD, Wallace TL, Lin AH, Kruger WC (1982) Mechanism of interaction of CC-1065 (NSC-298223) with DNA. Cancer Res 42: 2821–2828

    CAS  Google Scholar 

  • Takahashi M, Bertrand-Burggraf E, Fuchs RPP, Norden B (1992) Structure of UvrABC excinuclease UV-damaged DNA complexes studied by flow linear dichroism. DNA curved by UvrB and UvrC. FEBS Lett 314: 10–12

    Article  PubMed  CAS  Google Scholar 

  • Tand M, Lee CS, Doisy R, Ross L, Needham-VanDevanter DR, Hurley LH (1988) Recognition and repair of the CC-1065-(N3-adenine)-DNA adduct by the UvrABC nucleases. Biochemistry 27: 893–909

    Article  Google Scholar 

  • Thiagalingam S, Grossman L (1993) The multiple roles for ATP in Escherichia coli UvrABC endonuclease-catalyzed incision reaction. J Biol Chem 268: 18382–18389

    PubMed  CAS  Google Scholar 

  • Tomer G, Cohen-Fix O, O’Donnell M, Goodman M, Livneh Z (1996) Reconstitution of repair-gap UV mutagenesis with purified proteins from Escherichia coli. A role for DNA polymerase III and polymerase II. Proc Natl Acad Sci USA 93: 1376–1380

    Article  PubMed  CAS  Google Scholar 

  • Van Houten B (1990) Nucleotide excision repair in Escherichia coli. Microbiol Rev 54: 18–51

    PubMed  Google Scholar 

  • Van Houten B, Gamper H, Sancar A, Hearst JE (1987) DNase I footprinting of ABC excinuclease. J Biol Chem 262: 13180–13187

    PubMed  Google Scholar 

  • Visse R, De Ruijter M, Brouwer J, Brandsma JA, van de Putte P (1991) Uvr excision repair protein complex of Escherichia coli binds to the convex side of a cisplatininduced kink in the DNA. J Biol Chem 266: 7609–7617

    PubMed  CAS  Google Scholar 

  • Visse R, de Ruijter M, Moolenaar GF, van de Putte P (1992) Analysis of UvrABC endonuclease reaction intermediates on cisplatin-damaged DNA using mobility shift gel electrophoresis. J Biol Chem 267: 6736–6742

    PubMed  CAS  Google Scholar 

  • Visse R, de Ruijter M, Ubbink M, Brandsma JA, van de Putte P (1993) The first zincbinding domain of UvrA is not essential for UvrABC-mediated DNA excision repair. Mutat Res 294: 263–274

    PubMed  CAS  Google Scholar 

  • Visse R, van Gool AJ, Moolenaar GF, de Ruijter M, van de Putte P (1994a) The actual incision determines the efficiency of repair of cisplatin-damaged DNA by the Escherichia coli UvrABC endonuclease. Biochemistry 33: 1804–1811

    Article  PubMed  CAS  Google Scholar 

  • Visse R, King A, Moolenaar GF, Goosen N, van de Putte P (1994b) Protein-DNA interactions and alterations in the DNA structure upon UvrB-DNA preincision complex formation during nucleotide excision repair in Escherichia coli. Biochemistry 33: 9881–9888

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Mueller KL, Grossman L (1994) A mutational study of the C-terminal zinc-finger motif of the Escherichia coli UvrA protein. J Biol Chem 269: 10771–10775

    PubMed  CAS  Google Scholar 

  • Yamagata Y, Kato M, Odawara K, Tokuno Y, Nakashima Y, Matsushima N, Yasumura K, Tomita K, Ihara K, Fujii Y, Nakabeppu Y, Sekiguchi M, Fujii S (1996) Three-dimensional structure of a DNA repair enzyme, 3-methyl-adenine-DNA glycosylase II, from Escherichia coli. Cell 86: 311–319

    Article  PubMed  CAS  Google Scholar 

  • Yeung AT, Mattes WB, Oh EY, Yoakum GH, Grossman L (1983) Enzymatic properties of purified Escherichia coli UvrABC proteins. Proc Natl Acad Sci USA 80: 6157–6161

    Article  PubMed  CAS  Google Scholar 

  • Zou Y, Liu TM, Geacintov NE, Van Houten B (1995) Interaction of the UvrABC nuclease system with a DNA duplex containing a single stereoisomer of DG-( + )-anti-BPDE or D G-(—)-anti-BPDE. Biochemistry 34: 13582–13593

    Article  PubMed  CAS  Google Scholar 

  • Zou Y, Walker A, Bassett H, Geacintov NE, Van Houten B (1997) Formation of DNA repair intermediates and incision by the ATP-dependent UvrB-UvrC endonuclease. J Biol Chem 272: 4820–4827

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Laboratory of Molecular Genetics, Leiden Institue of Chemistry, Gorlaeus Laboratories, Leiden University, Einsteinweg 55, 2300 RA, Leiden, The Netherlands

    N. Goosen, G. F. Moolenaar, R. Visse & P. van de Putte

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  1. N. Goosen
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  2. G. F. Moolenaar
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  3. R. Visse
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  4. P. van de Putte
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Editors and Affiliations

  1. Max-Planck-Institut für Experimentelle Medizin, Hermann-Rein-Straße 3, 37075, Göttingen, Germany

    Fritz Eckstein

  2. Biochemistry Department, University of Dundee, Dundee, DD1 4HN, UK

    David M. J. Lilley

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© 1998 Springer-Verlag Berlin Heidelberg

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Goosen, N., Moolenaar, G.F., Visse, R., van de Putte, P. (1998). Functional Domains of the E. coli UvrABC Proteins in Nucleotide Excision Repair. In: Eckstein, F., Lilley, D.M.J. (eds) DNA Repair. Nucleic Acids and Molecular Biology, vol 12. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-48770-5_5

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  • DOI: https://doi.org/10.1007/978-3-642-48770-5_5

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