Structure of the DNA repair enzyme endonuclease IV and its DNA complex: Double-nucleotide flipping at abasic sites and three-metal-ion catalysis

Cell

Volumn 98, Issue 3, 1999, Pages 397-408

  Hosfield, David J ^a   Guan, Yue ^a   Haas, Brian J ^b   Cunningham, Richard P ^b   Tainer, John A ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; ENDONUCLEASE; ZINC ION;

ARTICLE; DNA BINDING; DNA REPAIR; ENZYME STRUCTURE; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; STEREOCHEMISTRY; X RAY CRYSTALLOGRAPHY;

EID: 0033529716     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81968-6     Document Type: Article

References (62)

1. Aravind, L., Walker, D.R., and Kroonin, E.V. (1999). Conserved domains in DNA repair proteins and evolution of repair systems. Nucleic Acids Res. 27, 1223-1242.
2. Banner, D.W., Bloomer, A.C., Petsko, G.A., Phillips, D.C., Pogson, C.I., Wilson, I.A., Coran, P.H., Furth, A.J., Milman, J.D., Offord, R.E., et al. (1975). Structure of chicken muscle triose phosphate isomerase determined crystallographically at 2.5 Aresolution using amino acid sequence data. Nature 255, 609-614.
3. Barren, I.E., Savva, R., Panayotou, G., Barlow, T., Brown, T., and Pearl, L.H. (1998). Crystal structure of a G:T/U mismatch-specific DNA glycosylase: mismatch recognition by complementary-strand interactions. Cell 92, 117-129.
4. Brünger, A.T. (1993). Assessment of phase accuracy by cross validation: the free R value. Methods and applications. Acta Crystallogr. D 49, 24-36.
5. Brünger, A.T., Kuriyan, J., and Karplus, M. (1987). Crystallographic R factor refinement by molecular dynamics. Science 235, 458-460.
6. Brünger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.-S., Kuszewski, J., Nilges, M., Pannu, N.S., et al. (1998). Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905-921.
7. Chan, E., and Weiss, B. (1987). Endonuclease IV of Escherichia coli is induced by paraquat. Proc. Natl. Acad. Sci. USA 84, 3189-3193.
8. Coleman, P.E. (1998). Zinc enzymes. Curr. Opin. Chem. Biol. 2, 222-234.
9. Collaborative Computational Project Number 4 (1994). The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760-763.
10. Cunningham, R.P. (1997). DNA glycosylases. Mutat. Res. 383, 189-196.
11. Davis, M.E., Madura, J.D., Luty, B.A., and McCammon, J.A. (1991). Electrostatics and diffusion of molecules in solution: simulations with the University of Houston brownian dynamics program. Comp. Phys. Commun. 62, 187-197.
12. Demple, B., and Harrison, L. (1994). Repair of oxidative damage to DNA: enzymology and biology. Annu. Rev. Biochem. 63, 915-948.
13. 2-damaged Escherichia coli. Proc. Natl. Acad. Sci. USA 83, 7731-7735.
14. Demple, B., Herman, T., and Chen, D.S. (1991). Cloning and expression of APE, the cDNA encoding the major human apurinic endonuclease: definition of a family of DNA repair enzymes. Proc. Natl. Acad. Sci. USA 88, 11450-11454.
15. Demple, B., Harrison, L., Wilson, D.M., III, Bennett, R.A., Takagi, T., and Ascione, A.G. (1997). Regulation of eukaryotic abasic endonucleases and their role in genetic stability. Environ. Health Perspect. 105, 931-934.
16. Farber, G.K., and Petsko, G.A. (1990). The evolution of alpha/beta barrel enzymes. Trends Biochem. Sci. 15, 228-234.
17. Friedberg, E.C., Walker, G.C., and Siede, W. (1995). DNA Repair and Mutagenesis. (Washington, D.C.: ASM Press).
18. Getzoff, E.D., Cabelli, D.E., Fisher, C.L., Parge, H.E., Viezzoli, M.S., Banci, L., and Hallewell, R.A. (1992). Faster superoxide dismutase mutants designed by enhancing electrostatic guidance. Nature 358, 347-351.
19. Gorman, M.A., Morera, S., Rothwell, D.G., de La Fortelle, E., Mol, C.D., Tainer, J.A., Hickson, I.D., and Freemont, P.S. (1997). The crystal structure of the human DNA repair endonuclease HAP1 suggests the recognition of extra-helical deoxyribose at DNA abasic sites. EMBO J. 16, 6548-6558.
20. Guan, Y., Manuel, R.C., Arvai, A.S., Parikh, S.S., Mol, C.D., Miller, J.H., Lloyd, R.S., and Tainer, J.A. (1998). 1.2 Å structure of MutY: bound adenine defines specificity for DNA repair enzyme superfamily. Nat. Struct. Biol. 5, 22-27.
21. Haas, B.J., Sandigursky, M., Tainer, J.A., Franklin, W.A., and Cunningham, R.P. (1999). Purification and characterization of Thermotoga maritima endonuclease IV, a thermostable apurinic apyrimidinic endonuclease and 3′-repair diesterase. J. Bacteriol. 181, 2834-2839.
22. Hansen, S., Hansen, L.K., and Hough, E. (1992). Crystal structures of phosphate, iodide and iodate-inhibited phospholipase C from Bacillus cereus and structural investigations of the binding of reaction products and a substrate analogue. J. Mol. Biol. 225, 543-549.
23. Hansen, S., Hough, E., Svensson, LA., Wong, Y.L., and Martin, S.F. (1993). Crystal structure of phospholipase C from Bacillus cereus complexed with a substrate analog. J. Mol. Biol. 234, 179-187.
24. Hough, E., Hansen, L.K., Birknes, B., Jynge, K., Hansen, S., Hodvik, A., Little, C., Dodson, E., and Derewenda, Z. (1989). High-resolution (1.5 A) crystal structure of phospholipase C from Bacillus cereus. Nature 338, 357-360.
25. Ide, H., Tedzuka, K., Shimzu, H., Kimura, Y., Purmal, A.A., Wallace, S.S., and Kow, Y.W. (1994). Alpha-deoxyadenosine, a major anoxic radiolysis product of adenine in DNA, is a substrate for Escherichia coli endonuclease IV. Biochemistry 33, 7842-7847.
26. Kingma, P.S., Corbett, A.H., Burcham, P.C., Marnett, L.J., and Osheroff, N. (1995). Abasic sites stimulate double-stranded DNA cleavage mediated by topoisomerase II. J. Biol. Chem. 270, 21441-21444.
27. Kissinger, C.R., Gehlhaar, D.K., and Fogel, D.B. (1999). Rapid automated molecular replacement by evolutionary search. Acta Crystallogr. D 55, 484-491.
28. Krokan, H.E., Standal, R., and Slupphaug, G. (1997). DNA glycosylases in the base excision repair of DNA. Biochem. J. 325, 1-16.
29. Kunz, B.A., Henson, E.S., Roche, H., Ramotar, D., Nunoshiba, T., and Demple, B. (1994). Specificity of the mutator caused by deletion of the yeast structural gene (APN1) for the major apurinic endonuclease. Proc. Natl. Acad. Sci. USA 91, 8165-8169.
30. Lau, A.Y., Scharer, O.D., Samson, L., Verdine, G.L., and Ellenberger, T. (1998). Crystal structure of a human alkylbase- DNA repair enzyme complexed to DNA: mechanisms for nucleotide flipping and base excision. Cell 95, 249-258.
31. Levin, J.D., Shapiro, R., and Demple, B. (1991). Metalloenzymes in DNA repair. J. Biol. Chem. 266, 22893-22898.
32. Lindahl, T. (1993). Instability and decay of the primary structure of DNA. Nature 362, 709-715.
33. Loeb, L.A. (1985). Apurinic sites as mutagenic intermediates. Cell 40, 483-484.
34. Masson, J.Y., Tremblay, S., and Ramotar, D. (1996). The Caenorhabditis elegans gene CeAPN1 encodes a homolog of Escherichia coli and yeast apurinic/apyrimidinic endonuclease. Gene 179, 291-293.
35. McRee, D.E. (1999). Xtalview/Xfit - a versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 125, 156-165.
36. Merritt, E., and Murphy, M.E.P. (1994). Raster3D Version 2.0. A program for photorealistic molecular graphics. Acta Crystallogr. D 50, 869-873.
37. Mol, C.D., Arvai, A.S., Sanderson, R.J., Slupphaug, G., Kavli, B., Krokan, H.E., Mosbaugh, D.W., and Tainer, J.A. (1995a). Crystal structure of human uracil-DNA glycosylase in complex with a protein inhibitor: protein mimicry of DNA. Cell 82, 701-708.
38. Mol, C.D., Kuo, C.-F., Thayer, M.M., Cunningham, R.P., and Tainer, J.A. (1995b). Structure and function of the multifunctional DNA-repair enzyme exonuclease III. Nature 374, 381-386.
39. Mol, C.D., Parikh, S.S., Lo, T.P., and Tainer, J.A. (1998). Structural phylogenetics of DNA base-excision repair. In DNA Repair, Nucleic Acids and Molecular Biology, Vol. 12, F. Eckstein and D.M.J. Lilley, eds. (Berlin: Springer), pp. 29-69.
40. Otwinowski, Z. (1993). In Data Collection and Processing, L. Sawyer, N. Isaacs, and S. Bailey, eds. (Warrington, UK: Science and Engineering Research Council), pp. 56-62.
41. Parikh, S.S., Mol, C.D., and Tainer, J.A. (1997). Base excision repair enzyme family portrait: integrating the structure and chemistry of an entire DNA repair pathway. Structure 5, 1543-1550.
42. Parikh, S.S., Mol, C.D., Slupphaug, G., Bharati, S., Krokan, H.E., and Tainer, J.A. (1998). Base-excision repair initiation revealed by crystal structures and binding kinetics of human uracil-DNA glycosylase with DNA. EMBO J. 17, 5214-5226.
43. Parikh, S.S., Mol, C.D., Hosfield, D.J., and Tainer, J.A. (1999). Envisioning the molecular choreography of DNA base excision repair. Curr. Opin. Struct. Biol. 9, 37-47.
44. Pelletier, H., Sawaya, M.R., Kumar, A., Wilson, S.H., and Kraut, J. (1994). Structures of ternary complexes of rat DNA polymerase beta, a DNA template-primer, and ddCTP. Science 264, 1891-1903.
45. Popoff, S.C., Spira, A.I., Johnson, A.W., and Demple, B. (1990). Yeast structural gene (APNI)forthe major apurinic endonuclease: homology to Escherichia coli endonuclease IV. Proc. Natl. Acad. Sci. USA 87, 4193-4197.
46. Ramotar, D. (1997). The apurinic-apyrimidinic endonuclease IV family of DNA repair enzymes. Biochem. Cell Biol. 75, 327-336.
47. Ramotar, D., Popoff, S.C., Gralla, E.B., and Demple, B. (1991). Cellular role of yeast Apn1 apurinic endonuclease/3′-diesterase: repair of oxidative and alkylation DNA damage and control of spontaneous mutation. Mol. Cell. Biol. 11, 4537-4544.
48. Ramotar, D., Vadnais, J., Mason, J.Y., and Tremblay, S. (1998). Schizosaccharomyces pombe apn1 encodes a homologue of the Escherichia coli endonuclease IV family of DNA repair proteins. Biochim. Biophys. Acta 1396, 15-20.
49. Read, R.J. (1986). Improved Fourier coefficients for maps using phases from partial structures with errors. Acta Crystallogr. A 42, 140-149.
50. Reardon, D., and Farber, G.K. (1995). The structure and evolution of alpha/beta barrel proteins. FASEB J. 9, 497-503.
51. Romier, C., Dominguez, R., Lahm, A., Dahl, O., and Suck, D. (1998). Recognition of single-stranded DNA by nuclease P1: high resolution crystal structures of complexes with substrate analogs. Proteins 32, 414-424.
52. Saporito, S.M., and Cunningham, R.P. (1988). Nucleotide sequence of the nfo gene of Escherichia coli K-12. J. Bacteriol. 170, 5141-5145.
53. Saporito, S.M., Smith-White, B.J., and Cunningham, R.P. (1988). Nucleotide sequence of the xth gene of Escherichia coli K-12. J. Bacteriol. 170, 4542-4547.
54. Sawaya, M.R., Prasad, R., Wilson, S.H., Kraut, J., and Pelletier, H. (1997). Crystal structure of human DNA polymerase beta complexed with gapped and nicked DNA: evidence for an induced fit mechanism. Biochemistry 36, 11205-11215.
55. Sheldrick, G.M. (1997). High resolution structure refinement. In Crystallographic Computing (Oxford: University Press).
56. Shida, T., Noda, M., and Sekiguchi, L. (1996). Cleavage of single-and double-stranded DNAs containing an abasic residue by Escherichia coli exonuclease III (AP endonuclease VI). Nucleic Acids Res. 24, 4572-4576.
57. Slupphaug, G., Mol, C.D., Kavli, B., Arvai, A.S., Krokan, H.E., and Tainer, J.A. (1996). A nucleotide-flipping mechanism from the structure of human uracil-DNA glycosylase bound to DNA. Nature 384, 87-92.
58. Terwilliger, T.C., and Berendzen, J. (1999). Automated MAD and MIR structure solution. Acta Crystallogr. D 55, 849-861.
59. Volbeda, A., Lahm, A., Sakiyama, F., and Suck, D. (1991). Crystal structure of Penicillium citrinum P1 nuclease at 2.8 Å resolution. EMBO J. 10, 1607-1618.
60. Walkup, L.K., and Kogoma, T. (1989). Escherichia coli proteins inducible by oxidative stress mediated by the Superoxide radical. J. Bacteriol. 171, 1476-1484.
61. Weiss, B. (1976). Endonuclease II of Escherichia coli is exonuclease III. J. Biol. Chem. 251, 1896-1901.
62. Zhong, X., Patel, S.S., Werneburg, B.G., and Tsai, M.D. (1997). DNA polymerase beta: multiple conformational changes in the mechanism of catalysis. Biochemistry 36, 11891-11900.