Mutagenic potential of DNA-peptide crosslinks mediated by acrolein-derived DNA adducts

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 637, Issue 1-2, 2008, Pages 161-172

  Minko, Irina G ^a   Kozekov, Ivan D ^b   Kozekova, Albena ^b   Harris, Thomas M ^b   Rizzo, Carmelo J ^b   Lloyd, R Stephen ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Acrolein; DNA peptide crosslinks; DNA protein crosslinks; Hydroxypropano DNA adducts; Mutagenesis

Indexed keywords

ACROLEIN; DNA; GUANINE; PEPTIDE; THYMIDINE;

ANIMAL CELL; ARTICLE; CELL STRAIN COS7; CHEMICAL MUTAGENESIS; CONTROLLED STUDY; DNA ADDUCT; DNA CROSS LINKING; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; SHUTTLE VECTOR;

ACROLEIN; ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; CROSS-LINKING REAGENTS; DEOXYADENOSINES; DEOXYGUANOSINE; DNA ADDUCTS; DNA DAMAGE; MUTAGENESIS; PEPTIDES; TRANSFECTION;

MAMMALIA; SIMIAE;

EID: 37249015575     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2007.08.001     Document Type: Article

References (59)

1. Zhitkovich A., Voitkun V., and Costa M. Glutathione and free amino acids form stable complexes with DNA following exposure of intact mammalian cells to chromate. Carcinogenesis 16 (1995) 907-913
2. Voitkun V., Zhitkovich A., and Costa M. Cr(III)-mediated crosslinks of glutathione or amino acids to the DNA phosphate backbone are mutagenic in human cells. Nucleic Acids Res. 26 (1998) 2024-2030
3. Kuykendall J.R., and Bogdanffy M.S. Formation and stability of acetaldehyde-induced crosslinks between poly-lysine and poly-deoxyguanosine. Mutat. Res. 311 (1994) 49-56
4. Hawkins C.L., Pattison D.I., and Davies M.J. Reaction of protein chloramines with DNA and nucleosides: evidence for the formation of radicals, protein-DNA cross-links and DNA fragmentation. Biochem. J. 365 (2002) 605-615
5. Kurtz A.J., Dodson M.L., and Lloyd R.S. Evidence for multiple imino intermediates and identification of reactive nucleophiles in peptide-catalyzed beta-elimination at abasic sites. Biochemistry 41 (2002) 7054-7064
6. 2-deoxyguanosine adducts of acrolein, crotonaldehyde, and trans-4-hydroxynonenal cross-link to peptides via Schiff base linkage. J. Biol. Chem. 278 (2003) 5970-5976
7. Copeland K.D., Lueras A.M., Stemp E.D., and Barton J.K. DNA cross-linking with metallointercalator-peptide conjugates. Biochemistry 41 (2002) 12785-12797
8. Minko I.G., Kurtz A.J., Croteau D.L., Van Houten B., Harris T.M., and Lloyd R.S. Initiation of repair of DNA-polypeptide cross-links by the UvrABC nuclease. Biochemistry 44 (2005) 3000-3009
9. 2-propano-2′-deoxyguanosine DNA adduct. J. Am. Chem. Soc. 127 (2005) 17686-17696
10. Marchand C., Krajewski K., Lee H.F., Antony S., Johnson A.A., Amin R., Roller P., Kvaratskhelia M., and Pommier Y. Covalent binding of the natural antimicrobial peptide indolicidin to DNA abasic sites. Nucleic Acids Res. 34 (2006) 5157-5165
11. Quievryn G., and Zhitkovich A. Loss of DNA-protein crosslinks from formaldehyde-exposed cells occurs through spontaneous hydrolysis and an active repair process linked to proteosome function. Carcinogenesis 21 (2000) 1573-1580
12. Mao Y., Desai S.D., Ting C.Y., Hwang J., and Liu L.F. 26 S proteasome-mediated degradation of topoisomerase II cleavable complexes. J. Biol. Chem. 276 (2001) 40652-40658
13. Desai S.D., Zhang H., Rodriguez-Bauman A., Yang J.M., Wu X., Gounder M.K., Rubin E.H., and Liu L.F. Transcription-dependent degradation of topoisomerase I-DNA covalent complexes. Mol. Cell. Biol. 23 (2003) 2341-2350
14. Brun F., Toulme J.J., and Helene C. Interactions of aromatic residues of proteins with nucleic acids. Fluorescence studies of the binding of oligopeptides containing tryptophan and tyrosine residues to polynucleotides. Biochemistry 14 (1975) 558-563
15. Behmoaras T., Toulme J.J., and Helene C. A tryptophan-containing peptide recognizes and cleaves DNA at apurinic sites. Nature 292 (1981) 858-859
16. Behmoaras T., Toulme J.J., and Helene C. Specific recognition of apurinic sites in DNA by a tryptophan-containing peptide. Proc. Natl. Acad. Sci. U.S.A. 78 (1981) 926-930
17. Pierre J., and Laval J. Specific nicking of DNA at apurinic sites by peptides containing aromatic residues. J. Biol. Chem. 256 (1981) 10217-10220
18. 2-propanodeoxyguanosine adducts in DNA upon reaction with acrolein or crotonaldehyde. Cancer Res. 44 (1984) 990-995
19. Marnett L.J., Hurd H.K., Hollstein M.C., Levin D.E., Esterbauer H., and Ames B.N. Naturally occurring carbonyl compounds are mutagens in Salmonella tester strain TA104. Mutat. Res. 148 (1985) 25-34
20. Curren R.D., Yang L.L., Conklin P.M., Grafstrom R.C., and Harris C.C. Mutagenesis of xeroderma pigmentosum fibroblasts by acrolein. Mutat. Res. 209 (1988) 17-22
21. Smith R.A., Cohen S.M., and Lawson T.A. Acrolein mutagenicity in the V79 assay. Carcinogenesis 11 (1990) 497-498
22. Cohen S.M., Garland E.M., St John M., Okamura T., and Smith R.A. Acrolein initiates rat urinary bladder carcinogenesis. Cancer Res. 52 (1992) 3577-3581
23. Nechev L.V., Harris C.M., and Harris T.M. Synthesis of nucleosides and oligonucleotides containing adducts of acrolein and vinyl chloride. Chem. Res. Toxicol. 13 (2000) 421-429
24. Nechev L.V., Kozekov I.D., Brock A.K., Rizzo C.J., and Harris T.M. DNA adducts of acrolein: site-specific synthesis of an oligodeoxynucleotide containing 6-hydroxy-5,6,7,8-tetrahydropyrimido[1,2-a]purin-10(3H)-one, an acrolein adduct of guanine. Chem. Res. Toxicol. 15 (2002) 607-613
25. 2-propano-2′-deoxyguanosine. J. Biol. Chem. 276 (2001) 9077-9082
26. 2-propano-2′-deoxyguanosine. J. Am. Chem. Soc. 124 (2002) 9324-9325
27. 3 frameshift hotspot of Salmonella typhimurium hisD3052: Hoogsteen base-pairing at pH 5.8. Chem. Res. Toxicol. 6 (1993) 825-836
28. Yang I.Y., Hossain M., Miller H., Khullar S., Johnson F., Grollman A., and Moriya M. Responses to the major acrolein-derived deoxyguanosine adduct in Escherichia coli. J. Biol. Chem. 276 (2001) 9071-9076
29. Yang I.Y., Johnson F., Grollman A.P., and Moriya M. Genotoxic mechanism for the major acrolein-derived deoxyguanosine adduct in human cells. Chem. Res. Toxicol. 15 (2002) 160-164
30. Yang I.Y., Chan G., Miller H., Huang Y., Torres M.C., Johnson F., and Moriya M. Mutagenesis by acrolein-derived propanodeoxyguanosine adducts in human cells. Biochemistry 41 (2002) 13826-13832
31. Kanuri M., Minko I.G., Nechev L.V., Harris T.M., Harris C.M., and Lloyd R.S. Error prone translesion synthesis past gamma-hydroxypropano deoxyguanosine, the primary acrolein-derived adduct in mammalian cells. J. Biol. Chem. 277 (2002) 18257-18265
32. Minko I.G., Washington M.T., Kanuri M., Prakash L., Prakash S., and Lloyd R.S. Translesion synthesis past acrolein-derived DNA adduct, gamma-hydroxypropanodeoxyguanosine, by yeast and human DNA polymerase eta. J. Biol. Chem. 278 (2003) 784-790
33. Moriya M., Zhang W., Johnson F., and Grollman A.P. Mutagenic potency of exocyclic DNA adducts: marked differences between Escherichia coli and simian kidney cells. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 11899-11903
34. Kuykendall J.R., and Bogdanffy M.S. Efficiency of DNA-histone crosslinking induced by saturated and unsaturated aldehydes in vitro. Mutat. Res. 283 (1992) 131-136
35. Sanchez A.M., Minko I.G., Kurtz A.J., Kanuri M., Moriya M., and Lloyd R.S. Comparative evaluation of the bioreactivity and mutagenic spectra of acrolein-derived alpha-HOPdG and gamma-HOPdG regioisomeric deoxyguanosine adducts. Chem. Res. Toxicol. 16 (2003) 1019-1028
36. Bandaru V., Sunkara S., Wallace S.S., and Bond J.P. A novel human DNA glycosylase that removes oxidative DNA damage and is homologous to Escherichia coli endonuclease VIII. DNA Repair (Amst) 1 (2002) 517-529
37. Hazra T.K., Izumi T., Boldogh I., Imhoff B., Kow Y.W., Jaruga P., Dizdaroglu M., and Mitra S. Identification and characterization of a human DNA glycosylase for repair of modified bases in oxidatively damaged DNA. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 3523-3528
38. Moriya M. Single-stranded shuttle phagemid for mutagenesis studies in mammalian cells: 8-oxoguanine in DNA induces targeted G.C → T.A transversions in simian kidney cells. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 1122-1126
39. Hirt B. Selective extraction of polyoma DNA from infected mouse cell cultures. J. Mol. Biol. 26 (1967) 365-369
40. Kalam M.A., Haraguchi K., Chandani S., Loechler E.L., Moriya M., Greenberg M.M., and Basu A.K. Genetic effects of oxidative DNA damages: comparative mutagenesis of the imidazole ring-opened formamidopyrimidines (Fapy lesions) and 8-oxo-purines in simian kidney cells. Nucleic Acids Res. 34 (2006) 2305-2315
41. Pawlowicz A.J., Munter T., Zhao Y., and Kronberg L. Formation of acrolein adducts with 2′-deoxyadenosine in calf thymus DNA. Chem. Res. Toxicol. 19 (2006) 571-576
42. Fornace Jr. A.J., and Seres D.S. Repair of trans-Pt(II) diamminedichloride DNA-protein crosslinks in normal and excision-deficient human cells. Mutat. Res. 94 (1982) 277-284
43. Speit G., Schutz P., and Merk O. Induction and repair of formaldehyde-induced DNA-protein crosslinks in repair-deficient human cell lines. Mutagenesis 15 (2000) 85-90
44. Minko I.G., Zou Y., and Lloyd R.S. Incision of DNA-protein crosslinks by UvrABC nuclease suggests a potential repair pathway involving nucleotide excision repair. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 1905-1909
45. Reardon J.T., and Sancar A. Repair of DNA-polypeptide crosslinks by human excision nuclease. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 4056-4061
46. 2]. A concept for activation of the trans geometry in platinum antitumor complexes. Nucleic Acids Res. 31 (2003) 6450-6460
47. Shapiro R., Sodum R.S., Everett D.W., and Kundu S.K. Reactions of nucleosides with glyoxal and acrolein. IARC Sci. Publ. (1986) 165-173
48. 4-propanodeoxycytidine 5′-monophosphate formed by the reaction of acrolein with deoxycytidine 5′-monophosphate. Chem. Res. Toxicol. 2 (1989) 267-271
49. 32P postlabeling. Cancer Res. 50 (1990) 3005-3012
50. Kozekov I.D., Nechev L.V., Sanchez A., Harris C.M., Lloyd R.S., and Harris T.M. Interchain cross-linking of DNA mediated by the principal adduct of acrolein. Chem. Res. Toxicol. 14 (2001) 1482-1485
51. Kozekov I.D., Nechev L.V., Moseley M.S., Harris C.M., Rizzo C.J., Stone M.P., and Harris T.M. DNA interchain cross-links formed by acrolein and crotonaldehyde. J. Am. Chem. Soc. 125 (2003) 50-61
52. Washington M.T., Minko I.G., Johnson R.E., Wolfle W.T., Harris T.M., Lloyd R.S., Prakash S., and Prakash L. Efficient and error-free replication past a minor-groove DNA adduct by the sequential action of human DNA polymerases iota and kappa. Mol. Cell. Biol. 24 (2004) 5687-5693
53. Wolfle W.T., Johnson R.E., Minko I.G., Lloyd R.S., Prakash S., and Prakash L. Human DNA polymerase iota promotes replication through a ring-closed minor-groove adduct that adopts a syn conformation in DNA. Mol. Cell. Biol. 25 (2005) 8748-8754
54. Sanchez A.M., Kozekov I.D., Harris T.M., and Lloyd R.S. Formation of inter- and intrastrand imine type DNA-DNA cross-links through secondary reactions of aldehydic adducts. Chem. Res. Toxicol. 18 (2005) 1683-1690
55. Avkin S., Goldsmith M., Velasco-Miguel S., Geacintov N., Friedberg E.C., and Livneh Z. Quantitative analysis of translesion DNA synthesis across a benzo[a]pyrene-guanine adduct in mammalian cells: the role of DNA polymerase kappa. J. Biol. Chem. 279 (2004) 53298-53305
56. Bi X., Slater D.M., Ohmori H., and Vaziri C. DNA polymerase kappa is specifically required for recovery from the benzo[a]pyrene-dihydrodiol epoxide (BPDE)-induced S-phase checkpoint. J. Biol. Chem. 280 (2005) 22343-22355
57. 2-alkyl guanine DNA adducts by human DNA polymerase kappa. J. Biol. Chem. 281 (2006) 21062-21072
58. Kawai Y., Furuhata A., Toyokuni S., Aratani Y., and Uchida K. Formation of acrolein-derived 2′-deoxyadenosine adduct in an iron-induced carcinogenesis model. J. Biol. Chem. 278 (2003) 50346-50354
59. Rothwell P.J., and Waksman G. Structure and mechanism of DNA polymerases. Adv. Protein Chem. 71 (2005) 401-440