Differential DNA recognition and cleavage by EcoRI dependent on the dynamic equilibrium between the two forms of the malondialdehyde-deoxyguanosine adduct

Biochemistry

Volumn 44, Issue 13, 2005, Pages 5024-5033

  VanderVeen, Laurie A ^a   Druckova, Alexandra ^a   Riggins, James N ^a   Sorrells, Jennifer L ^b   Guengerich, F Peter ^a   Marnett, Lawrence J ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDES; CRYSTAL STRUCTURE; ENZYMES; NUCLEIC ACIDS; PROTEINS; STRUCTURE (COMPOSITION); SUBSTRATES;

CLEAVAGE; COMPLEMENTARY STRAND; DNA PROCESSING ENZYMES; PROTEIN-NUCLEIC ACIDS;

DNA;

3 (2' DEOXY BETA DEXTRO ERYTHRO PENTOFURANOSYL)PYRIMIDO[1,2 A]PURIN 10(3H) ONE; DEOXYGUANOSINE DERIVATIVE; DNA; DNA BINDING PROTEIN; DNA POLYMERASE; DOUBLE STRANDED DNA; MALONALDEHYDE; N2 (3 OXO 1 PROPENYL)DEOXYGUANOSINE; RESTRICTION ENDONUCLEASE; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; DNA ADDUCT; DNA CLEAVAGE; DNA DAMAGE; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN NUCLEIC ACID INTERACTION; RING OPENING;

BASE SEQUENCE; CATALYTIC DOMAIN; DEOXYGUANOSINE; DEOXYRIBONUCLEASE ECORI; DNA; DNA ADDUCTS; DNA DAMAGE; DNA-BINDING PROTEINS; KINETICS; MODELS, MOLECULAR; MOLECULAR STRUCTURE; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OLIGODEOXYRIBONUCLEOTIDES; SUBSTRATE SPECIFICITY;

EID: 16344379034     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0472898     Document Type: Article

References (51)

1. 6-ethenoadenine repair by interacting with the human 3-methyladenine DNA glycosylase, Biochemistry 39, 8032-8038.
2. Rechkoblit, O., Krzeminsky, J., Amin, S., Jernstrom, B., Louneva, N., and Geacintov, N. E. (2001) Influence of bulky polynuclear carcinogen lesions in a TATA promoter sequence on TATA binding protein-DNA complex formation, Biochemistry 40, 5622-5632.
3. Siddik, Z. H. (2003) Cisplatin: mode of cytotoxic action and molecular basis of resistance, Oncogene 22, 7265-7279.
4. 32P-postlabelling determination of DNA adducts of malonaldehyde in humans: total white blood cells and breast tissue, Carcinogenesis 16, 1847-1851.
5. Fang, J. L., Vaca, C. E., Valsta, L. M., and Mutanen, M. (1996) Determination of DNA adducts of malonaldehyde in humans: effects of dietary fatty acid composition, Carcinogenesis 17, 1035-1040.
6. Rouzer, C. A., Chaudhary, A. K., Nokubo, M., Ferguson, D. M., Reddy, G. R., Blair, I. A., and Marnett, L. J. (1997) Analysis of the malondialdehyde- 2′-deoxyguanosine adduct pyrimidopurinone in human leukocyte DNA by gas chromatography/electron capture/negative chemical ionization/mass spectrometry, Chem. Res. Toxicol. 10, 181-188.
7. Everett, S. M., Singh, R., Leuratti, C., White, K. L., Neville, P., Greenwood; D., Marnett, L. J., Schorah, C. J., Formen, D., Shuker, D., and Axon, A. T. (2001) Levels of malondialdehyde-deoxyguanosine in the gastric mucosa: relationship with lipid peroxidation, ascorbic acid, and Helicobacter pylori, Cancer Epidemiol., Biomarkers Prev. 10, 369-376.
8. Leuratti, C., Watson, M. A., Deag, E. J., Welch, A., Singh, R., Gottschalg, E., Marnett, L. J., Atkin, W., Day, N. E., Shuker, D. E., and Bingham, S. A. (2002) Detection of malondialdehyde DNA adducts in human colorectal mucosa: relationship with diet and the presence of adenomas, Cancer Epidemiol., Biomarkers Prev. 11, 267-273.
9. Fink, S. P., Reddy, G. R., and Marnett, L. J. (1997) Mutagenicity in Escherichia coli of the major DNA adduct derived from the endogenous mutagen malondialdehyde, Proc. Natl. Acad. Sci. U.S.A. 94, 8652-8657.
10. VanderVeen, L. A., Hashim, M. F., Shyr, Y., and Marnett, L. J. (2003) Induction of frameshift and base pair substitution mutations by the major DNA adduct of the endogenous carcinogen malondialdehyde, Proc. Natl. Acad. Sci. U.S.A. 100, 14247-14252.
11. 1G) positioned in a (CpG)s frameshift hotspot of the Salmonella typhimurium hisD3052 gene, Biochemistry 38, 13491-13501.
12. Mao, H., Schnetz-Boutaud, N. C., Weisenseel, J. P., Marnett, L. J., and Stone, M. P. (1999) Duplex DNA catalyzes the chemical rearrangement of a malondialdehyde deoxyguanosine adduct, Proc. Natl. Acad. Sci. U.S.A. 96, 6615-6620.
13. Hashim, M. F., Riggins, J. N., Schnetz-Boutaud, N., Voehler, M., Stone, M. P., and Marnett, L. J. (2004) In vitro bypass of malondialdehyde- deoxyguanosine adducts: differential base selection during extension by the klenow fragment of DNA polymerase I is the critical determinant of replication outcome, Biochemistry 43, 11828-11835.
14. Thielking, V., Alves, J., Fliess, A., Maass, G., and Pingoud, A. (1990) Accuracy of the EcoRI restriction endonuclease: binding and cleavage studies with oligodeoxynucleotide substrates containing degenerate recognition sequences, Biochemistry 29, 4682-4691.
15. Brennan, C. A., Van Cleve, M. D., and Gumport, R. I. (1986) The effects of base analogue substitutions on the cleavage by the EcoRI restriction endonuclease of octadeoxyribonucleotides containing modified EcoRI recognition sequences, J. Biol. Chem. 261, 7270-7278.
16. McLaughlin, L. W., Benseler, F., Graeser, E., Piel, N., and Scholtissek, S. (1987) Effects of functional group changes in the EcoRI recognition site on the cleavage reaction catalyzed by the endonuclease, Biochemistry 26, 7238-7245.
17. Lesser, D. R., Kurpiewski, M. R., and Jen-Jacobson, L. (1990) The energetic basis of specificity in the Eco RI endonuclease-DNA interaction, Science 250, 776-786.
18. Zebala, J. A., Choi, J., Trainor, G. L., and Barany, F. (1992) DNA recognition of base analogue and chemically modified substrates by the Taq1 restriction endonuclease, J. Biol. Chem. 267, 8106-8116.
19. Parry, D., Moon, S. A., Liu, H. H., Heslop, P., and Connolly, B. A. (2003) DNA recognition by the EcoRV restriction endonuclease probed using base analogues, J. Mol. Biol. 331, 1005-1016.
20. Gill, R. D., Min, Z., Cortez, C., Harvey, R. G., Loechler, E. L., and DiGiovanni, J. (1993) Construction of Escherichia coli vectors containing deoxyadenosine and deoxyguanosine adducts from (+)-anti-dibenz[a,j]anthracene diol epoxide at a defined site, Chem. Res. Toxicol. 6, 681-689.
21. Turk, P. W., and Weitzman, S. A. (1995) Free radical DNA adduct 8-OH-deoxyguanosine affects activity of Hpa II and Msp I restriction endonucleases, Free Radical Res. 23, 255-258.
22. Denissenko, M. F., Venkatachalam, S., Ma, Y. H., and Wani, A. A. (1996) Site-specific induction and repair of benzo[a]pyrene diol epoxide DNA damage in human H-ras protooncogene as revealed by restriction cleavage inhibition, Mutat. Res. 363, 27-42.
23. Kim, Y. C., Grable, J. C., Love, R., Greene, P. J., and Rosenberg, J. M. (1990) Refinement of Eco RI endonuclease crystal structure: a revised protein chain tracing, Science 249, 1307-1309.
24. Robinson, C. R., and Sligar, S. G. (1998) Changes in solvation during DNA binding and cleavage are critical to altered specificity of the EcoRI endonuclease, Proc. Natl. Acad. Sci. U.S.A. 95, 2186-2191.
25. Wright, D. J., Jack, W. E., and Modrich, P. (1999) The kinetic mechanism of EcoRI endonuclease, J. Biol. Chem. 274, 31896-31902.
26. 2+ cofactor, Biochemistry 40, 683-692.
27. 1G, Chem. Res. Toxicol. 13, 90-95.
28. 2-(1,3-propano)-2′-deoxyguanosine and incorporation into oligodeoxynucleotides: a model for exocyclic acrolein-DNA adducts, Chem. Res. Toxicol. 3, 49-58.
29. -, human immunodeficiency virus-1 reverse transcriptase, and rat polymerase β, Biochemistry 36, 6069-6079.
30. Minko, I. G., Washington, M. T., Kanuri, M., Prakash, L., Prakash, S., and Lloyd, R. S. (2003) Translesion synthesis past acrolein-derived DNA adduct, γ-hydroxypropanodeoxyguanosine, by yeast and human DNA polymerase ζ, J. Biol. Chem. 278, 784-790.
31. 3 frameshift hotspot of Salmonella typhimurium hisD3052: Hoogsteen base-pairing at pH 5.8, Chem. Res. Toxicol. 6, 825-836.
32. Riggs, A. D., Suzuki, H., and Bourgeois, S. (1970) Lac repressor-operator interaction. I. Equilibrium studies, J. Mol. Biol. 48, 67-83.
33. Terry, B. J., Jack, W. E., Rubin, R. A., and Modrich, P. (1983) Thermodynamic parameters governing interaction of EcoRI endonuclease with specific and nonspecific DNA sequences, J. Biol. Chem. 258, 9820-9825.
34. Jen-Jacobson, L., Kurpiewski, M., Lesser, D., Grable, J., Boyer, H. W., Rosenberg, J. M., and Greene, P. J. (1983) Coordinate ion pair formation between EcoRI endonuclease and DNA, J. Biol. Chem. 258, 14638-14646.
35. Scicchitano, D. A., Olesnicky, E. C., and Dimitri, A. (2004) Transcription and DNA adducts: what happens when the message gets cut off?, DNA Repair 3, 1537-1548.
36. Viswanathan, A., You, H. J., and Doetsch, P. W. (1999) Phenotypic change caused by transcriptional bypass of uracil in nondividing cells, Science 284, 159-162.
37. Ghosh, R., and Mitchell, D. L. (1999) Effect of oxidative DNA damage in promoter elements on transcription factor binding, Nucleic Acids Res. 27, 3213-3218.
38. Pil, P. M., and Lippard, S. J. (1992) Specific binding of chromosomal protein HMG1 to DNA damaged by the anticancer drug cisplatin, Science 256, 234-237.
39. Cline, S. D., Riggins, J. N., Tornaletti, S., Marnett, L. J., and Hanawalt, P. C. (2004) Malondialdehyde adducts in DNA arrest transcription by T7 RNA polymerase and mammalian RNA polymerase II, Proc. Natl. Acad. Sci. U.S.A. 101, 7275-7280.
40. Needels, M. C., Fried, S. R., Love, R., Rosenberg, J. M., Boyer, H. W., and Greene, P. J. (1989) Determinants of EcoRI endonuclease sequence discrimination, Proc. Natl. Acad. Sci. U.S.A. 86, 3579-3583.
41. Van Cleve, M. D., and Gumport, R. I. (1992) Influence of enzyme-substrate contacts located outside the EcoRI recognition site on cleavage of duplex oligodeoxyribonucleotide substrates by EcoRI endonuclease, Biochemistry 31, 334-339.
42. McClarin, J. A., Frederick, C. A., Wang, B. C., Greene, P., Boyer, H. W., Grable, J., and Rosenberg, J. M. (1986) Structure of the DNA-Eco RI endonuclease recognition complex at 3 Å resolution, Science 234, 1526-1541.
43. Lesser, D. R., Kurpiewski, M. R., Waters, T., Connolly, B. A., and Jen-Jacobson, L. (1993) Facilitated distortion of the DNA site enhances EcoRI endonuclease-DNA recognition. Proc. Natl. Acad. Sci. U.S.A. 90, 7548-7552.
44. 2- propanodeoxyguanosine adducts (X) opposite purines in DNA duplexes: protonated X(syn)·A(anti) pairing (acidic pH) and X(syn)·G(anti) pairing (neutral pH) at the lesion site, Biochemistry 28, 5647-5657.
45. 2- propanodeoxyguanosine adduct (X) located opposite deoxyadenosine (A) in DNA duplexes at basic pH: simultaneous partial intercalation of X and A between stacked bases, Biochemistry 29, 4456-4465.
46. Kouchakdjian, M., Eisenberg, M., Johnson, F., Grollman, A. P., and Patel, D. J. (1991) Structural features of an exocyclic adduct positioned opposite an abasic site in a DNA duplex, Biochemistry 30, 3262-3270.
47. 2- propanodeoxyguanosine opposite deoxyadenosine. Restrained molecular dynamics and NOE-based refinement calculations, Biochemistry 31, 6518-6532.
48. 2-propanodeoxyguanosine adduct opposite deoxyadenosine in a DNA nonamer duplex at pH 8.9: Model of pH-dependent conformational transition, Biochemistry 32, 3852-3866.
49. 2- propanodeoxyguanosine adduct positioned in a palindrome derived from the Salmonella typhimurium hisD3052 gene: Hoogsteen pairing at pH 5.2, Chem. Res. Toxicol. 15, 127-139.
50. Riggins, J. N., Daniels, J. S., Rouzer, C. A., and Marnett, L. J. (2004) Kinetic and thermodynamic analysis of the hydrolytic ring-opening of the malondialdehyde-deoxyguanosine adduct, 3-(2′-deoxy-β-D-erythro- pentofuranosyl)-pyrimido[1,2-α]purin-10-(3H)-one, J. Am. Chem. Soc. 126, 8237-8243.
51. 1dG), J. Am. Chem. Soc. 126, 10571-10581.