Differential modes of DNA binding by mismatch uracil DNA glycosylase from Escherichia coli: Implications for abasic lesion processing and enzyme communication in the base excision repair pathway

Nucleic Acids Research

Volumn 39, Issue 7, 2011, Pages 2593-2603

  Grippon, Seden ^a   Zhao, Qiyuan ^a   Robinson, Tom ^b   Marshall, Jacqueline J T ^b   O'Neill, Rory J ^d   Manning, Hugh ^b   Kennedy, Gordon ^b   Dunsby, Christopher ^b   Neil, Mark ^b   Halford, Stephen E ^c   French, Paul M W ^c   Baldwin, Geoff S ^a  

^a Division of Molecular Biosciences   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

^d 16 the Edge Business Centre   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; SODIUM CHLORIDE; URACIL DNA GLYCOSIDASE;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SUBSTRATE; ESCHERICHIA COLI; EXCISION REPAIR; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING;

BINDING, COMPETITIVE; DNA; DNA DAMAGE; DNA REPAIR; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLUORESCENCE POLARIZATION; PROTEIN BINDING; SODIUM CHLORIDE; THYMINE DNA GLYCOSYLASE; URACIL-DNA GLYCOSIDASE;

ESCHERICHIA COLI;

EID: 79954576012     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq913     Document Type: Article

References (38)

1. Seeberg, E., Eide, L. and Bjoras, M. (1995) The base excision repair pathway. Trends Biochem. Sci., 20, 391-397.
2. Gallinari, P. and Jiricny, J. (1996) A new class of uracil-DNA glycosylases related to human thymine-DNA glycosylase. Nature, 383, 735-738. (Pubitemid 26360653)
3. Barrett, T.E., Savva, R., Panayotou, G., Barlow, T., Brown, T., Jiricny, J. and 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. (Pubitemid 28053303)
4. Saparbaev, M. and Laval, J. (1998) 3, N(4)-ethenocytosine, a highly mutagenic adduct, is a primary substrate for Escherichia coli double-stranded uracil-DNA glycosylase and human mismatch-specific thymine-DNA glycosylase. Proc Natl Acad. Sci. USA, 95, 8508-8513. (Pubitemid 28350518)
5. O'Neill, R.J., Vorob'eva, O.V., Shahbakhti, H., Zmuda, E., BhagwatA.S. and Baldwin, GS. (2003) Mismatch uracil glycosylase from Escherichia coli: a general mismatch or a specific DNA glycosylase? J. Biol. Chem., 278, 20526-20532. (Pubitemid 36806349)
6. Baker D., Liu P., Burdzy A., Sowers L.C. (2002) Characterization of the substrate specificity of a human 5-hydroxymethyluracil glycosylase activity. Chem. Res. Toxicol., 15; 33-39. (Pubitemid 34106088)
7. Saparbaev, M., Langouet, S., Privezentzev, C.V., Guengerich, F.P., Cai, H., Elder, R.H. and Laval, J. (2002) 1, N(2)-ethenoguanine, a mutagenic DNA adduct, is a primary substrate of Escherichia coli mismatch-specific uracil-DNA glycosylase and human alkylpurine-DNA-N-glycosylase. J. Biol. Chem., 277, 26987-26993. (Pubitemid 34951710)
8. Hang, B., Downing, G., GuliaevA.B. and Singer, B. (2002) Novel activity of Escherichia coli mismatch uracil-DNA glycosylase (Mug) excising 8-(hydroxymethyl)-3, N4-ethenocytosine, a potential product resulting from glycidaldehyde reaction. Biochemistry, 41, 2158-2165. (Pubitemid 34160875)
9. GuliaevA.B., Singer, B. and Hang, B. (2004) Chloroethylnitrosourea- derived ethano cytosine and adenine adducts are substrates for Escherichia coli glycosylases excising analogous etheno adducts. DNA Repair, 3, 1311-1321. (Pubitemid 39164594)
10. Mokkapati, S.K., Fernandez de HenestrosaA.R. and BhagwatA.S. (2001) Escherichia coli DNA glycosylase Mug: a growth-regulated enzyme required for mutation avoidance in stationary-phase cells. Mol. Microbiol., 41, 1101-1111. (Pubitemid 36124706)
11. Waters, T.R. and Swann, P.F. (1998) Kinetics of the action of thymine DNA glycosylase. J. Biol. Chem., 273, 20007-20014. (Pubitemid 28377551)
12. Farez-Vidal, M.E., Gallego, C., Ruiz-Perez, L.M. and Gonzalez-Pacanowska, D. (2001) Characterization of uracil-DNA glycosylase activity from Trypanosoma cruzi and its stimulation by AP endonuclease. Nucleic Acids Res., 29, 1549-1555. (Pubitemid 32288503)
13. Hill, J.W., Hazra, T.K., Izumi, T. and Mitra, S. (2001) Stimulation of human 8-oxoguanine-DNA glycosylase by AP-endonuclease: potential coordination of the initial steps in base excision repair. Nucleic Acids Res., 29, 430-438. (Pubitemid 32060930)
14. Parikh, S.S., Mol, C.D., Slupphaug, G., Bharati, S., Krokan, H.E. and Tainer, JA. (1998) Base excision repair initiation revealed by crystal structures and binding kinetics of human uracil-DNA glycosylase with DNA. EMBO J., 17, 5214-5226. (Pubitemid 28408487)
15. Pope, MA., Porello, S.L. and David, S.S. (2002) Escherichia coli apurinic-apyrimidinic endonucleases enhance the turnover of the adenine glycosylase MutY with G: A substrates. J. Biol. Chem., 277, 22605-22615. (Pubitemid 34967238)
16. Cortazar, D., Kunz, C., Saito, Y., Steinacher, R. and Schar, P. (2007) The enigmatic thymine DNA glycosylase. DNA Repair, 6, 489-504. (Pubitemid 46357052)
17. Zharkov, D.O., Rosenquist, TA., Gerchman, S.E. and Grollman, A.P. (2000) Substrate specificity and reaction mechanism of murine 8-oxoguanine-DNA glycosylase. J. Biol. Chem., 275, 28607-28617.
18. Sung, J.S. and Mosbaugh, D.W. (2000) Escherichia coli double-strand uracil-DNA glycosylase: involvement in uracil-mediated DNA base excision repair and stimulation of activity by endonuclease IV. Biochemistry, 39, 10224-10235. (Pubitemid 30663045)
19. Vidal, A.E., Hickson, I.D., Boiteux, S. and Radicella, J.P. (2001) Mechanism of stimulation of the DNA glycosylase activity of hOGG1 by the major human AP endonuclease: bypass of the AP lyase activity step. Nucleic Acids Res., 29, 1285-1292. (Pubitemid 32229455)
20. Waters, T.R., Gallinari, P., Jiricny, J. and Swann, P.F. (1999) Human thymine DNA glycosylase binds to apurinic sites in DNA but is displaced by human apurinic endonuclease 1. J. Biol. Chem., 274, 67-74. (Pubitemid 29035031)
21. Fitzgerald, M.E. and Drohat, A.C. (2008) Coordinating the initial steps of base excision repair apurinic/apyrimidinic endonuclease 1 actively stimulates thymine DNA glycosylase by disrupting the product complex. J. Biol. Chem., 283, 32680-32690.
22. Fried, M.G, Kanugula, S., Bromberg, J.L. and Pegg, A.E. (1996) DNA binding mechanism of O6-alkylguanine-DNA alkyltransferase: stoichiometry and effects of DNA base composition and secondary structure on complex stability. Biochemistry, 35, 15295-15301. (Pubitemid 26408864)
23. Rasimas, J.J., Kar, S.R., Pegg, A.E. and Fried, M.G (2007) Interactions of human O6-alkylguanine-DNA alkyltransferase (AGT) with short single-stranded DNAs. J. Biol. Chem., 282, 3357-3366. (Pubitemid 47084307)
24. Maiti, A., Morgan, M.T., Pozharski, E. and Drohat, A.C. (2008) Crystal structure of human thymine DNA glycosylase bound to DNA elucidates sequence-specific mismatch recognition. Proc Natl Acad. Sci. USA, 105, 8890-8895.
25. Baldwin, GS., Vipond, I.B. and Halford, S.E. (1995) Rapid reaction analysis of the catalytic cycle of the EcoRV restriction endonuclease. Biochemistry, 34, 705-714.
26. Bellamy, S.R. and Baldwin, GS. (2001) A kinetic analysis of substrate recognition by uracil-DNA glycosylase from herpes simplex virus type 1. Nucleic Acids Res., 29, 3857-3863. (Pubitemid 32910525)
27. Manning, H.B., Kennedy, GT., Owen, D.M., Grant, D.M., Magee, A.I., Neil, M.A., Itoh, Y., Dunsby, C. and French, P.M. (2008) A compact, multidimensional spectrofluorometer exploiting supercontinuum generation. J. Biophotonics, 1, 494-505.
28. Crutzen, M., Ameloot, M., Boens, N., Negri, R.M. and Deschryver, F.C. (1993) Global analysis of unmatched polarized fluorescence decay curves. J. Phys. Chem., 97, 8133-8145.
29. Sidorova, NY., Muradymov, S. and Rau, D.C. (2005) Trapping DNA-protein binding reactions with neutral osmolytes for the analysis by gel mobility shift and self-cleavage assays. Nucleic Acids Res., 33, 5145-5155. (Pubitemid 41487823)
30. Krusong, K., Carpenter, E.P., Bellamy, S.R., Savva, R. and Baldwin, GS. (2006) A comparative study of uracil-DNA glycosylases from human and herpes simplex virus type 1. J. Biol. Chem., 281, 4983-4992. (Pubitemid 43847761)
31. Powell, L.M., Connolly, BA. and Dryden, D.T.F. (1998) The DNA binding characteristics of the trimeric EcoKI methyltransferase and its partially assembled dimeric form determined by fluorescence polarisation and DNA footprinting. J. Mol. Biol., 283, 947-961. (Pubitemid 28515325)
32. Lakowicz, R.J. (1999) Principles of Fluorescence Spectroscopy, 2nd edn. Kluwer Academic/Plenum Publishers, New York.
33. Cornish-Bowden, A. (1995) Fundamentals of Enzyme Kinetics. Portland Press, London.
34. Barrett, T.E., Scharer, O.D., Savva, R., Brown, T., Jiricny, J., Verdine, GL. and Pearl, L.H. (1999) Crystal structure of a thwarted mismatch glycosylase DNA repair complex. EMBO J., 18, 6599-6609.
35. Hardeland, U., Bentele, M., Jiricny, J. and Schar, P. (2000) Separating substrate recognition from base hydrolysis in human thymine DNA glycosylase by mutational analysis. J. Biol. Chem., 275, 33449-33456.
36. Pearl, L.H. (2000) Structure and function in the uracil-DNA glycosylase superfamily. Mutat. Res., 460, 165-181. (Pubitemid 30628589)
37. Wong, I., Bernards, A.S., Miller, J.K. and Wirz, JA. (2003) A dimeric mechanism for contextual target recognition by MutY glycosylase. J. Biol. Chem., 278, 2411-2418. (Pubitemid 36801315)
38. Stivers, J.T., Pankiewicz, K.W. and Watanabe, KA. (1999) Kinetic mechanism of damage site recognition and uracil flipping by Escherichia coli uracil DNA glycosylase. Biochemistry, 38, 952-963.