Lessons learned from structural results on uracil-DNA glycosylase

Mutation Research - DNA Repair

Volumn 460, Issue 3-4, 2000, Pages 183-199

  Parikh, Sudip S ^a   Putnam, Christopher D ^a   Tainer, John A ^a  

^a Department of Cell and Molecular Biology   (United States)

Author keywords

DNA base excision repair; Enzyme mechanism; Protein structure; Uracil DNA glycosylase

Indexed keywords

URACIL DNA GLYCOSYLTRANSFERASE;

DNA REPAIR; ENZYME ANALYSIS; ENZYME MECHANISM; ENZYME SUBSTRATE; EXCISION REPAIR; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; REVIEW;

ZIZIPHUS MAURITIANA;

EID: 0034734380     PISSN: 09218777     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0921-8777(00)00026-4     Document Type: Article

References (79)

1. El-Hajj H.H., Wang L., Weiss B. Multiple mutant of Escherichia coli synthesizing virtually thymineless DNA during limited growth. J. Bacteriol. 174:1992;4450-4456.
2. Lindahl T. Instability and decay of the primary structure of DNA. Nature. 362:1993;709-715.
3. Dube D.K., Kunkel T.A., Seal G., Loeb L. Distinctive properties of mammalian DNA polymerases. Biochim. Biophys. Acta. 561:1979;369-382.
4. Cunningham R.P. DNA glycosylases. Mutat. Res. 383:1997;189-196.
5. Lindahl T., Wood R.D. Quality control in DNA repair. Science. 286:1999;1897-1905.
6. Wilson S.H. Mammalian base excision repair and DNA polymerase β Mutat. Res. 407:1998;203-215.
7. Parikh S.S., Mol C.D., Tainer J.A. Base excision repair enzyme family portrait: integrating the structure and chemistry of an entire DNA repair pathway. Structure. 5:1997;1543-1550.
8. Parikh S.S., Mol C.D., Hosfield D.J., Tainer J.A. Envisioning the molecular choreography of DNA base excision repair. Curr. Opin. Struct. Biol. 9:1999;37-47.
9. Lloyd R.S. Initiation of base excision repair: glycosylase mechanisms and structures. Annu. Rev. Biochem. 68:1999;255-285.
10. Krokan H.E., Standal R., Slupphaug G. DNA glycosylases in the base excision repair of DNA. Biochem. J. 325:1997;1-16.
11. Friedberg E.C., Walker G.C., Siede W. DNA Repair and Mutagenesis. 1995;ASM Press, Washington, DC.
12. Matsumoto Y., Kim K. Excision of deoxyribose phosphate residues by DNA polymerase beta during repair. Science. 269:1995;699-702.
13. 2-damaged Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 83:1986;7731-7735.
14. Loeb L.A. Apurinic sites as mutagenic intermediates. Cell. 40:1985;483-484.
15. Kingma P.S., Corbett A.H., Burcham P.C., Marnett L.J., Osheroff N. Abasic sites stimulate double-stranded DNA cleavage mediated by topoisomerase II. J. Biol. Chem. 270:1995;21441-21444.
16. Prasad R., Singhal R.K., Srivastava D.K., Molina J.T., Tomkinson A.E., Wilson S.H. Specific interaction of DNA polymerase β and DNA ligase I in a multiprotein base excision repair complex from bovine testis. J. Biol. Chem. 271:1996;16000-16007.
17. Kubota Y., Nash R.A., Klungland A., Schär P., Barnes D.E., Lindahl T. Reconstitution of DNA base excision-repair with purified human proteins: interaction between DNA polymerase β and the XRCC1 protein. EMBO J. 15:1996;6662-6670.
18. Caldecott K.W., Tucker J.D., Stanker L.H., Thompson L.H. Characterization of the XRCC1-DNA ligase III complex in vitro and its absence from mutant hamster cells. Nucleic Acids Res. 23:1995;4836-4843.
19. Rice P. Holding damaged DNA together. Nat. Struct. Biol. 6:1999;805-806.
20. Lindahl T. An N-glycosidase from Escherichia coli that releases free uracil from DNA containing deaminated cytosine residues. Proc. Natl. Acad. Sci. U. S. A. 71:1974;3649-3653.
21. Slupphaug G., Eftedal I., Kavli B., Bharati S., Helle N.M., Haug T., Levine D.W., Krokan H.E. Properties of a recombinant human uracil-DNA glycosylase from the UNG-gene and evidence that the UNG-gene encodes the major uracil-DNA glycosylase. Biochemistry. 34:1995;128-138.
22. Koistinen P., Vilpo J.A. Uracil-DNA glycosylase activity in human blood cells. Mutat. Res. 159:1986;99-102.
23. Koistinen P., Vilpo J.A. Uracil-DNA glycosylase in benign and malignant maturing human hematopoietic cells. Mutat. Res. 175:1986;115-120.
24. Vilpo J.A. The DNA-repair enzyme uracil-DNA glycosylase in the human hematopoietic system. Mutat. Res. 193:1988;207-217.
25. Gupta P.K., Sirover M.A. Stimulation of the nuclear uracil DNA glycosylase in proliferating fibroblasts. Cancer Res. 41:1981;3133-3136.
26. Slupphaug G., Olsen L.C., Helland D., Aasland R., Krokan H.E. Cell cycle regulation and in vitro hybrid arrest analysis of the major human uracil-DNA glycosylase. Nucleic Acids Res. 19:1991;5131-5137.
27. Otterlei M., Warbrick E., Nagelhus T.A., Haug T., Slupphaug G., Akbari M., Aas P.A., Steinsbekk K., Bakke O., Krokan H.E. Post-replicative base excision repair in replication foci. EMBO J. 18:1999;3834-3844.
28. Nilsen H., Otterlei M., Haug T., Solum K., Nagelus T.A., Skorpen F., Krokan H.E. Nuclear and mitochondrial uracil-DNA glycosylases are generated by alternative splicing and transcription from different positions in the ung gene. Nucleic Acids Res. 25:1997;750-755.
29. Otterlei M., Haug T., Nagelhus T.A., Slupphaug G., Lindmo T., Krokan H.E. Nuclear and mitochondrial splice forms of human uracil-DNA glycosylase contain a complex nuclear localisation signal and a strong classical mitochondrial localisation signal, respectively. Nucleic Acids Res. 26:1998;4611-4617.
30. Bharati S., Krokan H.E., Kristiansen L., Otterlei M., Slupphaug G. Human mitochondrial uracil-DNA glycosylase preform (UNG1) is processed to two forms one of which is resistant to inhibition by AP-sites. Nucleic Acids Res. 26:1998;4953-4959.
31. Takao M., Aburatani H., Kobayashi K., Yasui A. Mitochondrial targeting of human DNA glycosylases for DNA repair of oxidative DNA damage. Nucleic Acids Res. 26:1998;2917-2922.
32. Takao M., Zhang Q.M., Yonei S., Yasui A. Differential subcellular localization of human MutY homolog (hMYH) and the functional activity of adenine: 8-oxoguanine DNA glycosylase. Nucleic Acids Res. 27:1999;3638-3644.
33. Nishioka K., Ohtsubo T., Oda H., Fujiwara T., Kang D., Sugimachi K., Nakabeppu Y. Expression and differential intracellular localization of two major forms of human 8-oxoguanine DNA glycosylase encoded by alternatively spliced OGG1 mRNAs. Mol. Biol. Cell. 10:1999;1637-1652.
34. Ladner R.D., Caradonna S.J. The human dUTPase gene encodes both nuclear and mitochondrial isoforms. Differential expression of the isoforms and characterization of a cDNA encoding the mitochondrial species. J. Biol. Chem. 272:1997;19072-19080.
35. Huennekens F.M. The methotrexate story: a paradigm for development of cancer chemotherapeutic agents. Adv. Enzyme Regul. 34:1994;397-419.
36. Pogribny I.P., Muskhelishvili L., Miller B.J., James S.J. Presence and consequence of uracil in preneoplastic DNA from folate/methyl deficient rats. Carcinogenesis. 18:1997;2071-2076.
37. Ahmad S.I., Kirk S.H., Eisenstork A. Thymine metabolism and thymine-less death in prokaryotes and eukaryotes. Annu. Rev. Microbiol. 52:1998;591-625.
38. Warner H.R., Duncan B.K., Garrett C., Neuhard J. Synthesis and metabolism of uracil-containing deoxyribonucleic acid in Escherichia coli. J. Bacteriol. 145:1981;687-695.
39. Takahashi I., Marmur J. Replacement of thymidylic acid by deoxyuridylic acid in the deoxyribonucleic acid of a transducing phage for Bacillus subtilis. Nature. 197:1963;794-795.
40. Vieria G., de Lencastre H., Archer L. Restriction analysis of PBS 1-related phages. Arch. Virol. 106:1989;121-126.
41. Cone R., Bonura T., Friedberg E.C. Inhibitor of uracil-DNA glycosylase induced by bacteriophage PBS2. Purification and preliminary characterization. J. Biol. Chem. 255:1980;10354-10358.
42. Friedberg E.C., Ganeson A.K., Minton K. N-Glycosidase activity in extracts of Bacillus subtilis and its inhibition after infection with bacteriophage PBS2. J. Virol. 16:1975;315-321.
43. Savva R., McAuley-Hecht K., Brown T., Pearl L. The structural basis of specific base-excision repair by uracil-DNA glycosylase. Nature. 373:1995;487-493.
44. Mol C.D., Arvai A.S., Slupphaug G., Kavli B., Alseth I., Krokan H.E., Tainer J.A. Crystal structure and mutational analysis of human uracil-DNA glycosylase: structural basis for specificity and catalysis. Cell. 80:1995;869-878.
45. Putnam C.D., Shroyer M.J., Lundquist A.J., Mol C.D., Arvai A.S., Mosbaugh D.W., Tainer J.A. Protein mimicry of DNA from crystal structures of the uracil-DNA glycosylase inhibitor protein and its complex with Escherichia coli uracil-DNA glycosylase. J. Mol. Biol. 287:1999;331-346.
46. Xiao G., Tordova M., Jagadeesh J., Drohat A.C., Stivers J.T., Gilliland G.L. Crystal structures of Escherichia coli uracil DNA glycosylase and its complexes with uracil and glycerol: structure and glycosylase mechanism revisited. Proteins. 35:1999;13-24.
47. Ravishankar R., Sagar M.B., Roy S., Purnapatre K., Handa P., Varshney U., Vijayan M. X-ray analysis of a complex of Escherichia coli uracil DNA glycosylase (EcUDG) with a proteinacious inhibitor. The structure elucidation of a prokaryotic UDG. Nucleic Acids Res. 26:1998;4880-4887.
48. Parikh S.S., Walcher G., Jones G.D., Slupphaug G., Krokan H.E., Blackburn G.M., Tainer J.A. UDG-DNA substrate and product structures: conformational strain promotes catalytic efficiency by coupled stereoelectronic effects. Proc. Natl. Acad. Sci. U. S. A. 97:2000;5083-5088.
49. Parikh S.S., Mol C.D., Slupphaug G., Bharati S., Krokan H.E., Tainer J.A. Base-excision repair initiation revealed by crystal structures and DNA-binding kinetics of human uracil-DNA glycosylase bound to DNA. EMBO J. 17:1998;5412-5426.
50. Slupphaug G., Mol C.D., Kavli B., Arvai A.S., Krokan H.E., Tainer J.A. A nucleotide-flipping mechanism from the structure of human uracil-DNA glycosylase bound to DNA. Nature. 384:1996;87-92.
51. Higley M., Lloyd R.S. Processivity of uracil DNA glycosylase. Mutat. Res. 294:1993;109-116.
52. 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. 38:1999;952-963.
53. Bennett S.E., Sanderson R.J., Mosbaugh D.W. Processivity of Escherichia coli and rat liver mitochondrial uracil-DNA glycosylase is affected by NaCl concentration. Biochemistry. 34:1995;6109-6119.
54. Panayotou G., Brown T., Barlow T., Pearl L.H., Savva R. Direct measurement of the substrate preference of uracil-DNA glycosylase. J. Biol. Chem. 273:1998;45-50.
55. Vassylyev D.G., Morikawa K. Precluding uracil from DNA. Structure. 4:1996;1381-1385.
56. Cheng X., Blumenthal R.M. Finding a basis for flipping bases. Structure. 4:1996;639-645.
57. Verdine G.L., Bruner S.D. How do DNA repair proteins locate damaged bases in the genome? Chem. Biol. 4:1997;329-334.
58. Mol C.D., Parikh S.S., Putnam C.D., Lo T.P., Tainer J.A. DNA repair mechanisms for the recognition and removal of damaged DNA bases. Annu. Rev. Biophys. Biomol. Struct. 28:1999;101-128.
59. Verri A., Mazzarello P., Spadari S., Focher F. Uracil-DNA glycosylases preferentially excise mispaired uracil. Biochem. J. 287:1992;1007-1010.
60. Barrett T.E., Savva R., Panayotou G., Barlow T., Brown T., Pearl L.H. Crystal structure of a G:T/U mismatch-specific DNA glycosylase: Mismatch recognition by complementary-strand interactions. Cell. 92:1998;117-129.
61. Mol C.D., Arvai A.S., Sanderson R.J., Slupphaug G., Kavli B., Krokan H.E., Mosbaugh D.W., Tainer J.A. Crystal structure of human uracil-DNA glycosylase in complex with a protein inhibitor: protein mimicry of DNA. Cell. 82:1995;701-708.
62. Savva R., Pearl L.H. Nucleotide mimicry in the crystal structure of the uracil-DNA glycosylase-uracil glycosylase inhibitor protein complex. Nat. Struct. Biol. 2:1995;752-757.
63. Saenger W. Principles of Nucleic Acid Structure. 1984;Springer-Verlag, New York.
64. Kavli B., Slupphaug G., Mol C.D., Arvai A.S., Petersen S.B., Tainer J.A., Krokan H.E. Excision of cytosine and thymine from DNA by mutants of human uracil-DNA glycosylase. EMBO J. 15:1996;3442-3447.
65. Dunathan H.C. Conformational and reaction specificity in pyridoxal phosphate enzymes. Proc. Natl. Acad. Sci. U. S. A. 55:1966;712-716.
66. Shroyer M.J., Bennett S.E., Putnam C.D., Tainer J.A., Mosbaugh D.W. Mutation of an active site residue in Escherichia coli uracil-DNA glycosylase: effect on DNA binding, uracil inhibition and catalysis. Biochemistry. 38:1999;4834-4845.
67. Drohat A.C., Xiao G., Tordova M., Jagadeesh J., Pankiewicz K.W., Watanabe K.A., Gilliland G.L., Stivers J.T. Heteronuclear NMR and crystallographic studies of wild-type and H187Q Escherichia coli uracil DNA glycosylase: electrophilic catalysis of uracil expulsion by a neutral histidine 187. Biochemistry. 38:1999;11876-11886.
68. Domena J.D., Timmer R.T., Dicharry S.A., Mosbaugh D.W. Purification and properties of mitochondrial uracil-DNA glycosylase from rat liver. Biochemistry. 27:1988;6742-6751.
69. Gorman M.A., Morera S., Rothwell D.G., deLa Fortelle E., Mol C.D., Tainer J.A., Hickson I.D., Freemont P.S. The crystal structure of the human DNA repair endonuclease HAP1 suggests the recognition of extra-helical deoxyribose at DNA abasic sites. EMBO J. 16:1997;6548-6558.
70. Mol C.D., Izumi T., Mitra S., Tainer J.A. DNA-bound structures and mutants reveal abasic DNA binding by APE1 coordinates DNA repair. Nature. 403:2000;451-456.
71. Wilson D.M. III, Takeshita M., Demple B. Abasic site binding by the human apurinic endonuclease, Ape, and determination of the DNA contact sites. Nucleic Acids Res. 25:1997;933-939.
72. Carey D.C., Strauss P.R. Human apurinic/apyrimidinic endonuclease is processive. Biochemistry. 38:1999;16553-16560.
73. Bennett R.A.O., Wilson D.M. III, Wong D., Demple B. Interaction of human apurinic endonuclease and DNA polymerase β in the base excision repair pathway. Proc. Natl. Acad. Sci. U. S. A. 94:1997;7166-7169.
74. Haug T., Skorpen F., Lund H., Krokan H.E. Structure of the gene for human uracil-DNA glycosylase and analysis of the promoter function. FEBS Lett. 353:1994;180-184.
75. Svendsen P.C., Yee H.A., Winkfein R.J., van de Sande J.H. The mouse uracil-DNA glycosylase gene: isolation of cDNA and genomic clones and mapping ung to mouse chromosome 5. Gene. 189:1997;175-181.
76. Varshney U., Hutcheon T., van deSande J.H. Sequence analysis, expression, and conservation of Escherichia coli uracil DNA glycosylase and its gene (ung). J. Biol. Chem. 263:1988;7776-7784.
77. McGeoch D.J., Dalrymple M.A., Davison A.J., Dolan A., Frame M.C., McNab D., Perry L.J., Scott J.E., Taylor P. The complete DNA sequence of the long unique region in the genome of herpes simplex virus type 1. J. Gen. Virol. 69:1988;1531-1574.
78. Chee M.S., Bankier A.T., Beck S., Bohni R., Brown C.M., Cerny R., Horsnell T. III, Hutchison C.A., Kouzarides T., Martignetti J.A., Preddie E., Satchwell S.C., Tomlinson P., Weston K.M., Barrel B.G. Analysis of the protein-coding content of the sequence of human cytomegalovirus strain AD169. Curr. Top. Microbiol. Immunol. 154:1990;125-169.
79. Goebel S.J., Johnson G.P., Perkus M.E., Davis S.W., Winslow J.P., Paoletti E. The complete DNA sequence of vaccinia virus. Virology. 179:1990;247-266.