Looking beneath the surface to determine what makes DNA damage deleterious

Current Opinion in Chemical Biology

Volumn 21, Issue , 2014, Pages 48-55

  Greenberg, Marc M ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC ANTIBIOTIC; DNA; DNA DIRECTED DNA POLYMERASE GAMMA; ELECTROPHILE; LYASE; SCHIFF BASE;

CHROMATIN ASSEMBLY AND DISASSEMBLY; CYTOTOXICITY; DNA CLEAVAGE; DNA CROSS LINKING; DNA DAMAGE; DNA REPAIR; DNA STRAND; ELECTROPHILICITY; ELIMINATION REACTION; ENZYME ACTIVITY; ENZYME INHIBITION; ESCHERICHIA COLI; EXCISION REPAIR; HUMAN; HYDROGEN BOND; LIMIT OF DETECTION; MAMMAL CELL; MOLECULAR MODEL; NONHUMAN; PROTEIN EXPRESSION; REVIEW; CHEMISTRY; GENETICS; METABOLISM; OXIDATION REDUCTION REACTION;

DNA; DNA DAMAGE; DNA REPAIR; HUMANS; LYASES; OXIDATION-REDUCTION;

EID: 84899084768     PISSN: 13675931     EISSN: 18790402     Source Type: Journal    
DOI: 10.1016/j.cbpa.2014.03.018     Document Type: Review

References (57)

1. Galm U., Hager M.H., Van Lanen S.G., Ju J., Thorson J.S., Shen B. Antitumor antibiotics: bleomycin, enediynes, and mitomycin. Chem Rev 2005, 105:739-758.
2. Pitié M., Pratviel G. Activation of DNA carbon, hydrogen bonds by metal complexes. Chem Rev 2010, 110:1018-1059.
3. Greenberg M.M. The formamidopyrimidines: purine lesions formed in competition with 8-oxopurines from oxidative stress. Acc Chem Res 2012, 45:588-597.
4. Delaney J.C., Essigmann J.M. Assays for determining lesion bypass efficiency and mutagenicity of site-specific DNA lesions in vivo. Methods Enzymol 2006, 408:1-15.
5. Bjelland S., Seeberg E. Mutagenicity, toxicity and repair of DNA base damage induced by oxidation. Mutation Res 2003, 531:37-80.
6. Yang W., Woodgate R. What a difference a decade makes: insights into translesion DNA synthesis. Proc Natl Acad Sci U S A 2007, 104:15591-15598.
7. Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., Ellenberger T. DNA Repair and Mutagenesis 2006, ASM Press, Washington, DC.
8. Weinfeld M., Mani R.S., Abdou I., Aceytuno R.D., Glover J.N.M. Tidying up loose ends: the role of polynucleotide kinase/phosphatase in DNA strand break repair. Trends Biochem Sci 2011, 36:262-271.
9. Guainazzi A., Scharer O.D. Using synthetic DNA interstrand crosslinks to elucidate repair pathways and identify new therapeutic targets for cancer chemotherapy. Cell Mol Life Sci 2010, 67:3683-3697.
10. Kuang Y., Balakrishnan K., Gandhi V., Peng X. Hydrogen peroxide inducible DNA cross-linking agents: targeted anticancer prodrugs. J Am Chem Soc 2011, 133:19278-19281.
11. Stone M.P., Cho Y.-J., Huang H., Kim H.-Y., Kozekov I.D., Kozekova A., Wang H., Minko I.G., Lloyd R.S., Harris T.M., Rizzo C.J. Interstrand DNA cross-links induced by α,β-unsaturated aldehydes derived from lipid peroxidation and environmental sources. Acc Chem Res 2008, 41:793-804.
12. Kozekov I.D., Turesky R.J., Alas G.R., Harris C.M., Harris T.M., Rizzo C.J. Formation of deoxyguanosine cross-links from calf thymus DNA treated with acrolein and 4-hydroxy-2-nonenal. Chem Res Toxicol 2010, 23:1701-1713.
13. Dutta S., Chowdhury G., Gates K.S. Interstrand cross-links generated by abasic sites in duplex DNA. J Am Chem Soc 2007, 129:1852-1853.
14. Johnson K.M., Price N.E., Wang J., Fekry M.I., Dutta S., Seiner D.R., Wang Y., Gates K.S. On the formation and properties of interstrand DNA, DNA cross-links forged by reaction of an abasic site with the opposing guanine residue of 5'-cap sequences in duplex DNA. J Am Chem Soc 2013, 135:1015-1025.
15. Regulus P., Duroux B., Bayle P.-A., Favier A., Cadet J., Ravanat J.-L. Oxidation of the sugar moiety of DNA by ionizing radiation or bleomycin could induce the formation of a cluster DNA lesion. Proc Natl Acad Sci U S A 2007, 104:14032-14037.
16. Balasubramanian B., Pogozelski W.K., Tullius T.D. DNA strand breaking by the hydroxyl radical is governed by the accessible surface areas of the hydrogen atoms of the DNA backbone. Proc Natl Acad Sci USA 1998, 95:9738-9743.
17. Sczepanski J.T., Jacobs A.C., Greenberg M.M. Self-promoted DNA interstrand cross-link formation by an abasic site. J Am Chem Soc 2008, 130:9646-9647.
18. Sczepanski J.T., Jacobs A.C., Majumdar A., Greenberg M.M. Scope and mechanism of interstrand cross-link formation by the C4'-oxidized abasic site. J Am Chem Soc 2009, 131:11132-11139.
19. Sczepanski J.T., Hiemstra C.N., Greenberg M.M. Probing DNA interstrand cross-link formation by an oxidized abasic site using nonnative nucleotides. Bioorg Med Chem 2011, 19:5788-5793.
20. Guan L., Greenberg M.M. DNA interstrand cross-link formation by the 1,4-dioxobutane abasic lesion. J Am Chem Soc 2009, 131:15225-15231.
21. -2]purin-10(3h)-one (M1dG). J Am Chem Soc 2004, 126:10571-10581.
22. Boger D.L., Garbaccio R.M. Shape-dependent catalysis: insights into the source of catalysis for the CC-1065 and duocarmycin DNA alkylation reaction. Acc Chem Res 1999, 32:1043-1052.
23. Sczepanski J.T., Jacobs A.C., Van Houten B., Greenberg M.M. Double strand break formation during nucleotide excision repair of a DNA interstrand cross-link. Biochemistry 2009, 48:7565-7567.
24. Peng X., Ghosh A.K., Van Houten B., Greenberg M.M. Nucleotide excision repair of a DNA interstrand cross-link produces single- and double-strand breaks. Biochemistry 2010, 49:11-19.
25. Weng M-w, Zheng Y., Jasti V.P., Champeil E., Tomasz M., Wang Y., Basu A.K., Tang M.-s. Repair of mitomycin C mono- and interstrand cross-linked DNA adducts by UvrABC: a new model. Nucleic Acids Res 2010, 38:6976-6984.
26. Matsumoto Y., Kim K. Excision of deoxyribose phosphate residues by DNA polymerase β during DNA repair. Science 1995, 269:699-702.
27. Wilson D.M.I., Barsky D. The major human abasic endonuclease: formation, consequences and repair of abasic lesions in DNA. Mutat Res 2001, 485:283-307.
28. Kow Y.W., Wallace S.S. Mechanism of action of Escherichia coli endonuclease III. Biochemistry 1987, 26:8200-8206.
29. Hashimoto M., Greenberg M.M., Kow Y.W., Hwang J.-T., Cunningham R.P. The 2-deoxyribonolactone lesion produced in DNA by neocarzinostatin and other DNA damaging agents forms cross-links with the base-excision repair enzyme endonuclease III. J Am Chem Soc 2001, 123:3161-3162.
30. Kroeger K.M., Hashimoto M., Kow Y.W., Greenberg M.M. Cross-linking of 2-deoxyribonolactone and its β-elimination product by base excision repair enzymes. Biochemistry 2003, 42:2449-2455.
31. DeMott M.S., Beyret E., Wong D., Bales B.C., Hwang J.-T., Greenberg M.M., Demple B. Covalent trapping of human DNA polymerase β by the oxidative DNA lesion 2-deoxyribonolactone. J Biol Chem 2002, 277:7637-7640.
32. Xu Y-j, DeMottt M.S., Hwang J.T., Greenberg M.M., Demple B. Action of human apurinic endonuclease (Ape1) on C1'-oxidized deoxyribose damage in DNA. DNA Repair 2003, 2:175-185.
33. Nakano T., Terato H., Asagoshi K., Masaoka A., Mukuta M., Ohyama Y., Suzuki T., Makino K., Ide H. DNA-protein cross-link formation mediated by oxanine. A novel genotoxic mechanism of nitric oxide-induced DNA damage. J Biol Chem 2003, 278:25264-25272.
34. Guan L., Greenberg M.M. Irreversible inhibition of DNA polymerase β by an oxidized abasic lesion. J Am Chem Soc 2010, 132:5004-5005.
35. Guan L., Bebenek K., Kunkel T.A., Greenberg M.M. Inhibition of short patch and long patch base excision repair by an oxidized abasic site. Biochemistry 2010, 49:9904-9910.
36. Jacobs A.C., Kreller C.R., Greenberg M.M. Long patch base excision repair compensates for DNA polymerase β inactivation by the C4'-oxidized abasic site. Biochemistry 2011, 50:136-143.
37. Usui K., Aso M., Fukuda M., Suemune H. Photochemical generation of oligodeoxynucleotide containing a C4'-oxidized abasic site and its efficient amine modification: dependence on structure and microenvironment. J Org Chem 2008, 73:241-248.
38. Aso M., Kondo M., Suemune H., Hecht S.M. Chemistry of the bleomycin-induced alkali-labile DNA lesion. J Am Chem Soc 1999, 121:9023-9033.
39. Garcia-Diaz M., Bebenek K., Kunkel T.A., Blanco L. Identification of an intrinsic 5'-deoxyribose-5-phosphate lyase activity in human DNA polymerase λ. J Biol Chem 2001, 276:34659-34663.
40. Braithwaite E.K., Prasad R., Shock D.D., Hou E.W., Beard W.A., Wilson S.H. DNA polymerase lambda mediates a back-up base excision repair activity in extracts of mouse embryonic fibroblasts. J Biol Chem 2005, 280:18469-18475.
41. Stevens A.J., Guan L., Bebenek K., Kunkel T.A., Greenberg M.M. DNA polymerase λ inactivation by oxidized abasic sites. Biochemistry 2013, 52:975-983.
42. Xi Z., Goldberg I.H. DNA-damaging enediyne compounds. Comprehensive Natural Products Chemistry 1999, vol 7:553-592. Elsevier, Amsterdam.
43. Luger K., Mader A.W., Richmond R.K., Sargent D.F., Richmond T.J. Crystal structure of the nucleosome core particle at 2.8Å resolution. Nature 1997, 389:251-260.
44. Bennett R.A.O., Swerdlow P.S., Povirk L.F. Spontaneous cleavage of bleomycin-induced abasic sites in chromatin and their mutagenicity in mammalian shuttle vectors. Biochemistry 1993, 32:3188-3195.
45. Sczepanski J.T., Wong R.S., McKnight J.N., Bowman G.D., Greenberg M.M. Rapid DNA-protein cross-linking and strand scission by an abasic site in a nucleosome core particle. Proc Natl Acad Sci U S A 2010, 107:22475-22480.
46. Zhou C., Greenberg M.M. Histone-catalyzed cleavage of nucleosomal DNA containing 2-deoxyribonolactone. J Am Chem Soc 2012, 134:8090-8093.
47. Zhou C., Sczepanski J.T., Greenberg M.M. Mechanistic studies on histone catalyzed cleavage of apyrimidinic/apurinic sites in nucleosome core particles. J Am Chem Soc 2012, 134:16734-16741.
48. Sczepanski J.T., Zhou C., Greenberg M.M. Nucleosome core particle-catalyzed strand scission at abasic sites. Biochemistry 2013, 52:2157-2164.
49. Zhou C., Sczepanski J.T., Greenberg M.M. Histone modification via rapid cleavage of C4'-oxidized abasic sites in nucleosome core particles. J Am Chem Soc 2013, 135:5274-5277.
50. Sage E., Harrison L. Clustered DNA lesion repair in eukaryotes: relevance to mutagenesis and cell survival. Mutat Res 2011, 711:123-133.
51. O'Neill P., Wardman P. Radiation chemistry comes before radiation biology. Int J Radiat Biol 2009, 85:9-25.
52. Jiang T., Zhou X., Taghizadeh K., Dong M., Dedon P.C. N-formylation of lysine in histone proteins as a secondary modification arising from oxidative DNA damage. Proc Natl Acad Sci U S A 2007, 104:60-65.
53. Edrissi B., Taghizadeh K., Dedon P.C. Quantitative analysis of histone modifications: formaldehyde is a source of pathological N-6-formyllysine that is refractory to histone deacetylases. PLoS Genet 2013, 9:12.
54. Roberts S.A., Strande N., Burkhalter M.D., Strom C., Havener J.M., Hasty P., Ramsden D.A. Ku is a 5'-dRp/AP lyase that excises nucleotide damage near broken ends. Nature 2010, 464:1214-1217.
55. Strande N., Roberts S.A., Oh S., Hendrickson E.A., Ramsden D.A. Specificity of the dRp/AP lyase of Ku promotes nonhomologous end joining (NHEJ) fidelity at damaged ends. J Biol Chem 2012, 287:13686-13693.
56. Muller T.A., Andrzejak M.M., Hausinger R.P. A covalent protein, DNA 5'-product adduct is generated following AP lyase activity of human AlkBH1 (AlkB homologue 1). Biochem J 2013, 452:509-518.
57. Muller T.A., Meek K., Hausinger R.P. Human AlkB homologue 1 (AbH1) exhibits DNA lyase activity at abasic sites. DNA Repair 2010, 9:58-65.