Crystal structure of a family 4 uracil-DNA glycosylase from Thermus thermophilus HB8

Journal of Molecular Biology

Volumn 333, Issue 3, 2003, Pages 515-526

  Hoseki, Jun ^a,b   Okamoto, Akihiro ^a,b   Masui, Ryoji ^a,c   Shibata, Takehiko ^a   Inoue, Yorinao ^a   Yokoyama, Shigeyuki ^a,d,e   Kuramitsu, Seiki ^a,c  

^a RIKEN HARIMA INSTITUTE   (Japan)

^b OSAKA MEDICAL COLLEGE   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e RIKEN YOKOHAMA INSTITUTE   (Japan)

Author keywords

DNA repair; Family 4 UDG; Uracil DNA glycosylase; X ray crystal structure; 4Fe 4S cluster

Indexed keywords

GUANINE; IRON; PROLINE; SULFUR; URACIL DNA GLYCOSYLTRANSFERASE;

ARTICLE; BACTERIAL STRAIN; CRYSTAL STRUCTURE; DNA BINDING; DNA STRAND; ENZYME ACTIVITY; ENZYME STRUCTURE; ESCHERICHIA COLI; HUMAN; MISMATCH REPAIR; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN INTERACTION; SURFACE PROPERTY; THERMOSTABILITY; THERMUS THERMOPHILUS;

ESCHERICHIA COLI; THERMUS; THERMUS THERMOPHILUS;

EID: 0141996214     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2003.08.030     Document Type: Article

References (51)

1. Friedberg E.C., Walker G.C., Siede W. Base excision repair. DNA Repair and Mutagenesis. 1995;ASM Press, Washington, DC.
2. Lindahl T. Instability and decay of the primary structure of DNA. Nature. 362:1993;709-715.
3. Shen J.C., Rideout III W.M., Jones P.A. The rate of hydrolytic deamination of 5-methylcytosine in double-stranded DNA. Nucl. Acids Res. 22:1994;972-976.
4. Scharer O.D., Jiricny J. Recent progress in the biology, chemistry and structural biology of DNA glycosylases. BioEssays. 23:2001;270-281.
5. Pearl L.H. Structure and function in the uracil-DNA glycosylase superfamily. Mutat. Res. 460:2000;165-181.
6. Parikh S.S., Putnam C.D., Tainer J.A. Lessons learned from structural results on uracil-DNA glycosylase. Mutat. Res. 460:2000;183-199.
7. Xiao G., Tordova M., Jagadeesh J., Drohat A.C., Stivers J.T., Gilliland G.L. Crystal structure of Escherichia coli uracil DNA glycosylase and its complexes with uracil and glycerol: structure and glycosylase mechanism revisited. Proteins: Struct. Funct. Genet. 35:1999;13-24.
8. Mol C.D., Arvai A.S., Slupphaug G., Kavii B., Alseth I., Krokan H.E., Tainer J.A. Crystal structure and mutational analysis of human uracil-DNA glycosylase: structure basis for specificity and catalysis. Cell. 80:1995;869-878.
9. 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.
10. 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.
11. Barrett T.E., Savva R., Panayotou G., Barlow T., Brown T., Jiricny J., 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.
12. Haushalter K.A., Stukenberg P.T., Kirschner M.W., Verdine G.L. Identification of a new uracil-DNA glycosylase family by expression cloning using synthetic inhibitors. Curr. Biol. 9:1999;174-185.
13. Lindahl T., Nyberg B. Heat-induced deamination of cytosine residues in deoxyribonucleic acid. Biochemistry. 13:1974;3405-3410.
14. Koulis A., Cowan D.A., Pearl L.H., Savva R. Uracil-DNA glycosylase activities in hyperthermophilic micro-organisms. FEMS Microbiol. Letters. 143:1996;267-271.
15. Sandigursky M., Franklin W.A. Thermostable uracil-DNA glycosylase from Thermotoga maritima, a member of a novel class of DNA repair enzyme. Curr. Biol. 9:1999;531-534.
16. Sandigursky M., Faje A., Franklin W.A. Characterization of the full length uracil-DNA glycosylase in the extremely thermophile Thermotoga maritima. Mutat. Res. 485:2001;187-195.
17. Sandigursky M., Franklin W.A. Uracil-DNA glycosylase in the extreme thermophile Archaeoglobus fulgidus. J. Biol. Chem. 275:2000;19146-19149.
18. Knævelsrud I., Ruoff P., Ånensen H., Klungland A., Bjelland S., Birkeland N.-K. Excision of uracil from DNA by the hyperthermophilic Afung protein is dependent on the opposite base and stimulated by heat-induced transition to a more open structure. Mutat. Res. 487:2001;173-190.
19. Sartori A.A., Schär P., Fitz-Gibbon S., Miller J.H., Jiricny J. Biochemical characterization of uracil processing activities in the hyperthermophilic archaeon Pyrobaculum aerophilum. J. Biol. Chem. 276:2001;29979-29986.
20. Hinks J.A., Evans M.C.W., Miguel Y., Sartori A.A., Jiricny J., Pearl L.H. An iron-sulfur cluster in the Family 4 uracil-DNA glycosylase. J. Biol. Chem. 277:2002;16936-16940.
21. Ramanchandran G.N., Sasisekharan V. Conformation of polypeptides and proteins. Advan. Protein Chem. 23:1968;287-437.
22. Thayer M.M., Ahern H., Xing D., Cunningham R.P., Tainer J.A. Novel DNA binding motifs in the DNA repair enzyme endonuclease III crystal. EMBO J. 14:1995;4108-4120.
23. Ito Y., Yamasaki K., Iwahara J., Terada T., Kamiya A., Shirouzu M., et al. Regional polysterism in the GTP-bound form of the human c-Ha-Ras protein. Biochemistry. 36:1997;9109-9119.
24. Hall M.D., Banaszak L.J. Crystal structure of a ternary complex of Escherichia coli malate dehydrogenase citrate and NAD at 1.9 Å resolution. J. Mol. Biol. 232:1993;213-222.
25. Dessen A., Tang J., Schmidt H., Stahl M., Clark J.D., Seehra J., Somers W.S. Crystal structure of human cytosolic phospholipase A2 reveals a novel topology and catalytic mechanism. Cell. 97:1999;349-360.
26. Fersht A. Comformational equilibria in α-and δ-chymotrypsin. The energetics and importance of the salt bridge. J. Mol. Biol. 64:1972;497-509.
27. Anderson D.E., Becktel W.J., Dahlquist F.W. pH-induced denaturation of proteins: a single salt bridge constributes 3-5 kcal/mol to the free energy of folding T4 lysozyme. Biochemistry. 29:1990;2403-2408.
28. Matthews B.W., Nicholson H., Becktel W.J. Enhanced protein thermostability from site-directed mutations that decrease the entropy of unfolding. Proc. Natl Acad. Sci. USA. 84:1987;6663-6667.
29. Ahern T.J., Casal J.I., Petsko G.A., Klibanov A.M. Control of oligomeric enzyme thermostability by protein engineering. Proc. Natl Acad. Sci. USA. 84:1987;675-679.
30. Mol D.C., Arvai A.S., Begley T.J., Cunningham R.P., Tainer J.A. Structure and activity of a thermostable thymine-DNA glycosylase: evidence for base twisting to remove mismatched normal DNA bases. J. Mol. Biol. 315:2002;373-384.
31. Holm L., Sander C. Alignment of three-dimensional protein structures: network server for database searching. Methods Enzymol. 266:1996;653-662.
32. 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 binding kinetics of human uracil-DNA glycosylase with DNA. EMBO J. 17:1998;5214-5226.
33. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D. 50:1994;760-763.
34. Lindahl T., Ljungquist S., Siegert W., Nyberg B., Sperens B. DNA N-glycosidase from Escherichia coli. J. Biol. Chem. 252:1977;3286-3294.
35. 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.
36. 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. Nucl. Acids Res. 26:1998;4953-4959.
37. Parikh S.S., Walcher G., Jones G.D., Slupphaug G., Krokan H.E., Blackburn G.M., Tainer J.A. Uracil-DNA glycosylase-DNA substrate and product structures: conformation strain promotes catalytic efficiency by coupled stereoelectronic effects. Proc. Natl Acad. Sci. USA. 97:2000;5083-5088.
38. Werner R.M., Stivers J.T. Kinetic isotope effect studies of the reaction catalyzed by uracil-DNA glycosylase: evidence for an oxocarbenium ion-uracil anion intermediate. Biochemistry. 39:2000;14054-14064.
39. Dinner A.R., Blackburn G.M., Karplus M. Uracil-DNA glycosylase acts by substrate autocatalysis. Nature. 413:2001;752-755.
40. Sartori A.A., Fitz-Gibbon S., Yang H., Miller J.H., Jiricny J. A novel uracil-DNA glycosylase with broad substrate specificity and an unusual active site. EMBO J. 21:2002;3182-3191.
41. Starkuviene V., Fritz H.-J. A novel type of uracil-DNA glycosylase mediating repair of hydrolytic DNA damage in the extremely thermophilic eubacterium Thermus thermophilus. Nucl. Acids Res. 30:2002;2097-2102.
42. 15N heteronuclear NMR studies of Escherichia coli thioredoxin in samples isotopically labeled by residue type. Biochemistry. 24:1985;7263-7268.
43. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:1997;307-326.
44. Terwilliger T.C., Berendzen J. Automated MAD and MIR structure solution. Acta Crystallog. sect. D. 55:1999;849-861.
45. Terwilliger T.C. Maximum-likelihood density modification. Acta Crystallog. sect. D. 56:2000;965-972.
46. McRee D.E. XtalView/Xfit: a versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 125:1999;156-165.
47. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D. 54:1998;905-921.
48. Kraulis P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
49. Merritt E.A., Bacon D.J. Raster3D: photorealistic molecular graphics. Methods Enzymol. 277:1997;505-524.
50. Thompson J.D., Higgins D.G., Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22:1994;4673-4680.
51. Nicholls A., Sharp K., Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins: Struct. Funct. Genet. 11:1991;281-296.