Dynamic opening of DNA during the enzymatic search for a damaged base

Nature Structural and Molecular Biology

Volumn 11, Issue 12, 2004, Pages 1230-1236

  Cao, Chunyang ^a   Jiang, Yu Lin ^a   Stivers, James T ^a   Song, Fenhong ^b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF STANDARDS AND TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA GLYCOSYLTRANSFERASE; PROTON; URACIL DNA GLYCOSIDASE; WATER;

ARTICLE; CATALYSIS; CHEMISTRY; CONFORMATION; DNA DAMAGE; DNA REPAIR; ENZYME SPECIFICITY; GENETICS; MAGNETISM; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE SEQUENCE; PH; THERMODYNAMICS;

BASE SEQUENCE; CATALYSIS; DNA; DNA DAMAGE; DNA GLYCOSYLASES; DNA REPAIR; HYDROGEN-ION CONCENTRATION; MAGNETIC RESONANCE SPECTROSCOPY; MAGNETICS; NUCLEIC ACID CONFORMATION; PROTONS; SUBSTRATE SPECIFICITY; THERMODYNAMICS; URACIL-DNA GLYCOSIDASE; WATER;

EID: 16544386633     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb864     Document Type: Article

References (35)

1. Stivers, J.T. & Jiang, Y.L. A mechanistic perspective on the chemistry of DNA repair glycosylases. Chem. Rev. 103, 2729-2759 (2003).
2. Stivers, J.T. Site-specific DNA damage recognition by enzyme-induced base flipping. Prog. Nucleic Acid Res. Moi. Biol. 77, 37-65 (2004).
3. Parikh, S.S. et al. Base excision repair initiation revealed by crystal structures and binding kinetics of human uracil-DNA glycosylase with DNA. EMBO J. 17, 5214-5226 (1998).
4. Parikh, S.S. et al. Uracil-DNA glycosylase-DNA substrate and product structures: con- formational strain promotes catalytic efficiency by coupled stereoelectronic effects. Proc. Natl. Acad. Sci. USA 97, 5083-5088 (2000).
5. Werner, R.M. et al. Stressing-out DNA? The contribution of serine-phosphodiester interactions in catalysis by uracil DNA glycosylase. Biochemistry 39, 12585-12594 (2000).
6. a for uracil bound to uracil DNA glycosylase: Implications for catalysis. J. Am. Chem. Soc. 122, 1840-1841 (2000).
7. Kwon, K., Jiang, Y. & Stivers, J. Rational engineering of a DNA glycosylase specific for an unnatural cytosine:pyrene base pair. Chem. Biol. 10, 1-20 (2003).
8. Cao, C., Kwon, K., Jiang, Y.L., Drohat, A.C. & Stivers, J.T. Solution structure and base perturbation studies reveal a novel mode of alkylated base recognition by 3-methylad- enine DNA glycosylase I. J. Biol. Chem. 48012-48021 (2003).
9. Slupphaug, G. et al. A nucleotide-flipping mechanism from the structure of human uracil-DNA glycosylase bound to DNA [see comments]. Nature 384, 87-92 (1996).
10. Lau, A.Y., Scharer, O.D., Samson, L., Verdine, G.L. & Ellenberger, T. Crystal structure of a human alkylbase-DNA repair enzyme complexed to DNA: mechanisms for nucleotide flipping and base excision. Cell 95, 249-258 (1998).
11. Lau, A.Y., Wyatt, M.D., Glassner, B.J., Samson, L.D. & Ellenberger, T. Molecular basis for discriminating between normal and damaged bases by the human alkyladenine glycosylase, AAG. Proc. Natl. Acad. Sci. USA 97, 13573-13578 (2000).
12. Jiang, Y.L. & Stivers, J.T. Mutational analysis of the base flipping mechanism of uracil DNA glycosylase. Biochemistry 41, 11236-11247 (2002).
13. Stivers, J.T., Pankiewicz, K.W. & Watanabe, K.A. Kinetic mechanism of damage site recognition and uracil flipping by Escherichia coli uracil DNA glycosylase. Biochemistry 38, 952-963 (1999).
14. Roberts, R.J. On base flipping. Cell 82, 9-12 (1995).
15. Krosky, D.J., Schwarz, F.P. & Stivers, J.T. Linear free energy correlations for enzymatic base flipping: how do damaged base pairs facilitate specific recognition? Biochemistry 43, 4188-4195 (2004).
16. Jencks, W.P. When is an intermediate not an intermediate—enforced mechanisms of general acid-base catalyzed, carbocation, carbanion, and ligand-exchange reactions. Acc. Chem. Res. 13, 161-169 (1980).
17. Chen, L., Haushalter, K.A., Lieber, C.M. & Verdine, G.L. Direct visualization of a DNA glycosylase searching for damage. Chem. Biol. 9, 345-350 (2002).
18. Verdine, G.L. & Bruner, S.D. How do DNA repair proteins locate damaged bases in the genome? Chem. Biol. 4, 329-334 (1997).
19. Seibert, E., Ross, J.B. & Osman, R. Role of DNA flexibility in sequence-dependent activity of uracil DNA glycosylase. Biochemistry 41, 10976-10984 (2002).
20. Banavali, N.K. & MacKerell, A.D. Jr. Free energy and structural pathways of base flipping in a DNA GCGC containing sequence. J. Mol. Biol. 319, 141-160 (2002).
21. Gueron, M. & Leroy, J.-L. Studies of Base Pair Kinetics by NMR Measurement of Proton Exchange. Methods Enzymol. 261, 383-413 (1995).
22. Gueron, M. et al. Applications to imino proton exchange to nucleic acid kinetics and structure. In Structure and Methods (eds. Sarma, R.H. & Sarma, M.H.) 113-137 (Adenine Press, Guilderland, New York, 1990).
23. Kavli, B. et al. Excision of cytosine and thymine from DNA by mutants of human uracil- DNA glycosylase. EMBO J. 15, 3442-3447 (1996).
24. Gueron, M., Kochoyan, M. & Leroy, J.L. A single mode of DNA base-pair opening drives imino proton exchange. Nature 328, 89-92 (1987).
25. Warmlander, S., Sen, A. & Leijon, M. Imino proton exchange in DNA catalyzed by ammonia and trimethylamine: evidence for a secondary long-lived open state of the base pair. Biochemistry 39, 607-615 (2000).
26. Handa, P., Acharya, N. & Varshney, U. Effects of mutations at tyrosine 66 and aspara- gine 123 in the active site pocket of Escherichia coli uracil DNA glycosylase on uracil excision from synthetic DNA oligomers: evidence for the occurrence of long-range interactions between the enzyme and substrate. Nucleic Acids Res. 30, 3086-3095 (2002).
27. Jiang, Y.L., Song, F. & Stivers, J.T. Base flipping mutations of uracil DNA glycosylase: substrate rescue using a pyrene nucleotide wedge. Biochemistry 41, 11248-11254 (2002).
28. Bommarito, S., Peyret, N. & SantaLucia, J. Jr. Thermodynamic parameters for DNA sequences with dangling ends. Nucleic Acids Res. 28, 1929-1934 (2000).
29. Stivers, J.T., Jagadeesh, G.J., Nawrot, B., Stec, W.J. & Shuman, S. Stereochemical outcome and kinetic effects of Rp- and Sp- phosphorothioate substitutions at the cleavage site of vaccinia type I DNA topoisomerase. Biochemistry 39, 5561-5572 (2000).
30. Drohat, A.C., Jagadeesh, J., Ferguson, E. & Stivers, J.T. Role of electrophilic and general base catalysis in the mechanism of Escherichia coli uracil DNA glycosylase. Biochemistry 38, 11866-11875 (1999).
31. Jiang, Y.L., Kwon, K. & Stivers, J.T. Turning on uracil-DNA glycosylase using a pyrene nucleotide switch. J. Biol. Chem. 276, 42347-42354 (2001).
32. Jiang, Y.L., Ichikawa, Y. & Stivers, J.T. Inhibition of uracil DNA glycosylase by an oxacarbenium ion mimic. Biochemistry 41, 7116-7124 (2002).
33. Delaglio, F. et al. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293 (1995).
34. Snoussi, K. & Leroy, J.L. Imino proton exchange and base-pair kinetics in RNA duplexes. Biochemistry 40, 8898-9904 (2001).
35. Benight, A.S., Schurr, J.M., Flynn, P.F., Reid, B.R. & Wemmer, D.E. Melting of a self- complementary DNA minicircle. Comparison of optical melting theory with exchange broadening of the nuclear magnetic resonance spectrum. J. Mol. Biol. 200, 377-399 (1988).