Characterization of DNA glycosylase activity by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry

Analytical Biochemistry

Volumn 394, Issue 1, 2009, Pages 13-23

  Darwanto, Agus ^a   Farrel, Alvin ^a   Rogstad, Daniel K ^a   Sowers, Lawrence C ^a  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

DNA glycosylase; MALDI TOF MS; Oxidative damage; Substrate specificity

Indexed keywords

DESORPTION; DNA; INDUCTIVELY COUPLED PLASMA; OLIGONUCLEOTIDES; SUBSTRATES;

BASE EXCISION REPAIRS; CHEMICAL IDENTITY; DNA GLYCOSYLASE; MALDI TOF MS; MATRIX-ASSISTED LASER DESORPTION/IONIZATION-TIME-OF-FLIGHT MASS SPECTROMETRY; NEW MECHANISMS; OXIDATIVE DAMAGE; SUBSTRATE SPECIFICITY;

MASS SPECTROMETRY;

DNA GLYCOSYLTRANSFERASE; OLIGONUCLEOTIDE; OXYGEN 18; RECOMBINANT ENZYME;

ARTICLE; CHEMICAL STRUCTURE; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVITY; ENZYME MECHANISM; EXCISION REPAIR; GEL ELECTROPHORESIS; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PRIORITY JOURNAL;

EID: 69249212168     PISSN: 00032697     EISSN: 10960309     Source Type: Journal    
DOI: 10.1016/j.ab.2009.07.015     Document Type: Article

References (57)

1. Mullart E., Lohman P.H.M., Berends F., and Vijg J. DNA damage metabolism and aging. Mutat. Res. 237 (1990) 189-210
2. Lindhal T. Instability and decay of the primary structure of DNA. Nature 362 (1993) 709-715
3. Slupphaug G., Eftedal I., Kavli B., Bharati S., Helle N.M., Haug T., Levine D.W., and Krokan H.E. Properties of a recombinant human uracil-DNA glycosylase from the UNG gene and evidence that UNG encodes the major uracil-DNA glycosylase. Biochemistry 34 (1995) 128-138
4. Jaiswal M., Lipinski L.J., Bohr V.A., and Mazur S.J. Efficient in vitro repair of 7-hydro-8-oxodeoxyguanosine by human cell extracts: Involvement of multiple pathways. Nucleic Acids Res. 26 (1998) 2184-2191
5. Pearl L.H. Structure and function in the uracil-DNA glycosylase superfamily. Mutat. Res. 460 (2000) 165-181
6. Krokan H.E., Nilsen H., Skorpen F., Otterlei M., and Slupphaug G. Base excision repair of DNA in mammalian cells. FEBS Lett. 476 (2000) 73-77
7. Ide H., and Kotera M. Human DNA glycosylases involved in the repair of oxidatively damaged DNA. Biol. Pharm. Bull. 27 (2004) 480-485
8. Prasad R., Beard W.A., Strauss P.R., and Wilson S.H. Human DNA polymerase β-deoxyribose phosphate lyase. J. Biol. Chem. 273 (1998) 15263-15270
9. Mosbaugh D.W., and Linn S. Further characterization of human fibroblast apurinic/apyrimidinic DNA endonucleases. J. Biol. Chem. 255 (1980) 11743-11752
10. Franklin W.A., and Lindahl T. DNA deoxyribophosphodiesterase. EMBO J. 7 (1988) 3617-3622
11. Pascucci B., Maga G., Hubscher U., Bjoras M., Seeberg E., Hickson I.D., Villani G., Giordano C., Cellai L., and Dogliotti E. Reconstitution of the base excision repair pathway for 7,8-dihydro-8-oxoguanine with purified human proteins. Nucleic Acids Res. 30 (2002) 2124-2130
12. Vidal A.E., Hickson I.D., Boiteux S., and Radicella J.P. 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 (2001) 1285-1292
13. McCullough A.K., Dodson M.L., and Lloyd R.S. Initiation of base excision repair: glycosylase mechanisms and structures. Annu. Rev. Biochem. 68 (1999) 255-285
14. Singer B., and Hang B. What structural features determine repair enzyme specificity and mechanism in chemically modified DNA?. Chem. Res. Toxicol. 10 (1997) 713-732
15. Liu P., Burdzy A., and Sowers L.C. Substrate recognition by a family of uracil-DNA glycosylases: UNG, MUG, TDG. Chem. Res. Toxicol. 15 (2002) 1001-1009
16. Liu P., Burdzy A., and Sowers L.C. Repair of the mutagenic DNA oxidation product, 5-formyluracil. DNA Repair 2 (2003) 199-210
17. Liu P., Theruvathu J.A., Darwanto A., Lao V.V., Pascal T., Goddard III W., and Sowers L.C. Mechanisms of base selection by the E. coli mispaired uracil glycosylase. J. Biol. Chem. 283 (2008) 8829-8836
18. Bennett M.T., Rodgers M.T., Hebert A.S., Ruslander L.E., Eisele L., and Drohat A.C. Specificity of human thymine DNA glycosylase depends on N-glycosidic bond stability. J. Am. Chem. Soc. 128 (2006) 12510-12519
19. Liu Y., Prasad R., Beard W.A., Kedar P.A., Hou E.W., Shock D.D., and Wilson S.H. Coordination of steps in single-nucleotide base excision repair medicated by apurinic/apyrimidinic endonuclease 2 and DNA polymerase β. J. Biol. Chem. 282 (2007) 13532-13541
20. Ischenko A.A., and Saparbaev M.K. Alternative nucleotide incision repair pathway for oxidative DNA damage. Nature 415 (2002) 183-187
21. Wiederhold L., Leppard J.B., Kedar P., Karimi-Busheri F., Rasouli-Nia A., Weinfeld M., Tomkinson A.E., Izumi T., Prasad R., Wilson S.H., Mitra S., and Hazra T.K. AP endonuclease-independent DNA base excision repair in human cells. Mol. Cell 15 (2004) 209-220
22. Sung J.-K., and Demple B. Roles of base excision repair subpathways in correcting oxidized abasic sites in DNA. FEBS J. 273 (2006) 1620-1629
23. -/- double-knockout mice. J. Immunol. 177 (2006) 5386-5392
24. Pettersen H.S., Sundheim O., Gilljam K.M., Slupphaug G., Krokan H.E., and Kavli B. Uracil-DNA glycosylases SMUG1 and UNG2 coordinate the initial steps of base excision repair by distinct mechanisms. Nucleic Acids Res. 35 (2007) 3879-3892
25. Di Noia J.M., Williams G.T., Chan D.T.Y., Buerstedde J.-M., Baldwin G.S., and Neuberger M.S. Dependence of antibody gene diversification on uracil excision. J. Exp. Med. 204 (2007) 3209-3219
26. Gait M.J. Oligonucleotide Synthesis: A Practical Approach (1984), IRL Press, Washington, DC
27. Brandon M.L., Mi L.-J., Chaung W., Teebor G., and Boorstein R.J. 5-Chloro-2′-deoxyuridine cytotoxicity results from base excision repair of uracil subsequent to thymidylate synthase inhibition. Mutat. Res. 459 (2000) 161-169
28. Sowers L.C., and Beardsley G.P. Synthesis of oligonucleotides containing 5-(hydroxymethyl)-2′-deoxyuridine at defined sites. J. Org. Chem. 58 (1993) 1664-1665
29. Berthod T., Petillot Y., Guy A., Cadet J., Forest E., and Molko D. Synthesis and mass spectrometry analysis of oligonucleotides bearing 5-formyl-2′-deoxyuridine in their structure. Nucleosides Nucleotides 15 (1996) 1287-1305
30. Kuijpers W.H.A., Kuyl-Yeheskiely E., van Boom J.H., and van Boeckel C.A.A. The application of the AMB protective group in the solid-phase synthesis of methylphosphonate DNA analogues. Nucleic Acids Res. 21 (1993) 3493-3500
31. Dizdaroglu M. Facts about the artifacts in the measurement of oxidative DNA base damage by gas chromatography-mass spectrometry. Free Radic. Res. 29 (1998) 551-563
32. LaFrancois C.J., Yu K., and Sowers L.C. Quantification of 5-(hydroxymethyl)uracil in DNA by gas chromatography/mass spectrometry: problems and solutions. Chem. Res. Toxicol. 11 (1998) 786-793
33. Pan C., Xu S., Houjiang Z., Fu Y., Ye M., and Zou H. Recent developments in methods and technology for analysis of biological samples by MALDI-TOF-MS. Anal. Bioanal. Chem. 387 (2007) 193-204
34. Cui Z., Theruvathu J.A., Farrel A., Burdzy A., and Sowers L.C. Characterization of synthetic oligonucleotides containing biologically important modified bases by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Anal. Biochem. 379 (2008) 196-207
35. Haushalter K.A., Stukenber P.T., Kirschner M.W., and Verdine G.L. Identification of a new uracil-DNA glycosylase family by expression cloning using synthetic inhibitors. Curr. Biol. 9 (1999) 174-185
36. Wong E., and Demple B. Modulation of the 5′-deoxyribose-5-phosphate lyase and DNA synthesis activities of mammalian DNA polymerase β by apurinic/apyrimidinic endonuclease 1. J. Biol. Chem. 279 (2004) 25268-25275
37. Hill J.W., Hazra T.K., Izumi T., and Mitra S. Stimulation of human 8-oxoguanine-DNA glycosylase by AP endonuclease: potential coordination of the initial steps in base excision repair. Nucleic Acids Res. 29 (2001) 430-438
38. Marenstein D.R., Chan M.K., Altamirano A., Basu A.K., Boorstein R.J., Cunningham R.P., and Teebor G.W. Substrate specificity of human endonuclease III (hNTH1): effect of human APE1 on hNTH1 activity. J. Biol. Chem. 278 (2003) 9005-9012
39. Zharkov D.O., Rieger R.A., Iden C.R., and Grollman A.P. NH2-terminal proline acts as a nucleophile in the glycosylase/AP-lyase reaction catalyzed by E. coli formamidopyrimidine-DNA glycosylase (Fpg) protein. J. Biol. Chem. 272 (1997) 5335-5341
40. Bhagwat M., and Gerlt J.A. 3′- and 5′-strand cleavage catalyzed by the Fpg protein from E. coli occur via successive β- and δ-elimination mechanisms, respectively. Biochemistry 35 (1996) 659-665
41. Kim J., and Linn S. The mechanisms of action of E. coli endonuclease III and T4 UV endonuclease (endonuclease V) at AP sites. Nucleic Acids Res. 16 (1988) 1135-1141
42. Bricteux-Gregoire S., and Verly W.G. The use of the thioglycolate to distinguish between 3′ AP (apurinic/apyrimidinic) endonucleases and AP lyases. Nucleic Acids Res. 17 (1989) 6269-6282
43. Bailly V., and Verly W.G. E. coli endonuclease III is not an endonuclease but a β-elimination catalyst. Biochem. J. 242 (1987) 565-572
44. Mazumder A., and Gerlt J.A. Stereochemical studies of the β-elimination reactions at aldehydic abasic sites in DNA: Endonuclease III from E. coli, sodium hydroxide, and Lys-Trp-Lys. Biochemistry 30 (1991) 1119-1126
45. van der Kemp P.A., Thomas D., Barbey R., de Oliveira R., and Boiteux S. Cloning and expression in E. coli of the OGG1 gene of Saccharomyces cerevisiae, which codes for a DNA glycosylase that excises 7,8-dihydro-8-oxoguanine and 2,6-diamino-4-hydroxy-5-N-methylformamidopyrimidine. Proc. Natl. Acad. Sci. USA 93 (1996) 5197-5202
46. Bjoras M., Luna L., Johnsen B., Hoff E., Haug T., Rognes T., and Seeberg E. Opposite base-dependent reactions of a human base excision repair enzyme on DNA containing 7,8-dihydro-8-oxoguanine and abasic sites. EMBO J. 16 (1997) 6314-6322
47. Warner H.R., Demple B.F., Deutsch W.A., Kane C.M., and Linn S. Apurinic/apyrimidinic endonucleases in repair of pyrimidine dimers and other lesions in DNA. Proc. Natl. Acad. Sci. USA 77 (1980) 4602-4606
48. Piersen C.E., McCullough A.M., and Lloyd R.S. AP lyases and dRPases: commonality of mechanism. Mutat. Res. 459 (2000) 43-53
49. Ikeda S., Biswas T., Roy R., Izumi T., Boldogh I., Kurosky A., Sarker A.H., and Mitra S. Purification and characterization of human NTH1, a homolog of E. coli endonuclease III. J. Biol. Chem. 273 (1998) 21585-21593
50. D'Ham C., Romieu A., Jaquinod M., Gasparutto D., and Cadet J. Excision of 5,6-dihydroxy-5,6-dihydrothymine, 5,6-dihydrothymine, and 5-hydroxycytosine from defined sequence oligonucleotides by E. coli endonuclease III and Fpg proteins: kinetic and mechanistic aspects. Biochemistry 38 (1999) 3335-3344
51. Duarte V., Gasparutto D., Jaquinod M., and Cadet J. In vitro DNA synthesis opposite oxazolone and repair of this DNA damage using modified oligonucleotides. Nucleic Acids Res. 28 (2000) 1555-1563
52. Hegde M.L., Hazra T., and Mitra S. Early steps in the DNA base excision/single-strand interruption repair pathway in mammalian cells. Cell Res. 18 (2008) 27-47
53. Sobol R.W., Prasad R., Evenski A., Baker A., Yang X.-P., Horton J.K., and Wilson S.H. The lyase activity of the DNA repair protein β-polymerase protects from DNA-damage-induced cytotoxicity. Nature 405 (2000) 807-810
54. Fortini P., Pascucci B., Parlanti E., Sobol R.W., Wilson S.H., and Doglitti E. Different DNA polymerases are involved in the short- and long-patch base excision repair in mammalian cells. Biochemistry 37 (1998) 3575-3580
55. Ali M.M., Hazra T.K., Hong D., and Kow Y.W. Action of human endonucleases III and VIII upon DNA-containing tandem dihydrouracil. DNA Repair 4 (2005) 679-686
56. Wibley J.E.A., Waters T.R., Haushalter K., Verdine G.L., and Pearl L.H. Structure and specificity of the vertebrate anti-mutator uracil-DNA glycosylase SMUG1. Mol. Cell 11 (2003) 1647-1659
57. Hardeland U., Steinacher R., Jiricny J., and Schar P. Modification of the human thymine-DNA glycosylase by ubiquitin-like proteins facilitates enzymatic turnover. EMBO J. 21 (2002) 1456-1464