The role of Mg2+ and specific amino acid residues in the catalytic reaction of the major human abasic endonuclease: New insights from EDTA-resistant incision of acyclic abasic site analogs and site-directed mutagenesis

Journal of Molecular Biology

Volumn 290, Issue 2, 1999, Pages 447-457

  Erzberger, Jan P ^a   Wilson III, David M ^a  

^a LAWRENCE LIVERMORE NATIONAL LABORATORY   (United States)

Author keywords

Ape1; DNA repair; Hap1; Nuclease; Phosphate hydrolysis

Indexed keywords

EDETIC ACID; ENDONUCLEASE; ETHANE; MAGNESIUM ION; PROPANE; TETRAHYDROFURAN; ALKANE; AMINO ACID; APEX1 PROTEIN, HUMAN; DEOXYRIBONUCLEASE IV; DNA; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; FURAN DERIVATIVE; LYASE; MAGNESIUM; PROTON;

AMINO ACID SEQUENCE; ARTICLE; CATALYSIS; CONFORMATIONAL TRANSITION; DNA CLEAVAGE; HUMAN; HYDROGEN BOND; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; AMINO ACID SUBSTITUTION; BINDING SITE; CHEMICAL MODEL; CHEMISTRY; DRUG EFFECT; GENETICS; KINETICS; METABOLISM; PH;

ALKANES; AMINO ACID SUBSTITUTION; AMINO ACIDS; BINDING SITES; CARBON-OXYGEN LYASES; CATALYSIS; DEOXYRIBONUCLEASE IV (PHAGE T4-INDUCED); DNA; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; EDETIC ACID; ETHANE; FURANS; HUMANS; HYDROGEN BONDING; HYDROGEN-ION CONCENTRATION; HYDROLYSIS; KINETICS; MAGNESIUM; MODELS, CHEMICAL; MUTAGENESIS, SITE-DIRECTED; PROPANE; PROTONS;

EID: 0033538343     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.2888     Document Type: Article

References (34)

1. Ausubel F. M. Editor of Current Protocols in Molecular Biology. 1997;John Wiley & Sons, New York.
2. Barzilay G., Mol C. D., Robson C. N., Walker L. J., Cunningham R. P., Tainer J. A., Hickson I. D. Identification of critical active-site residues in the multifunctional human DNA repair enzyme HAP1. Nature Struct. Biol. 2:1995;561-568.
3. Beese L. S., Steitz T. A. Structural basis for the 3′-5′ exonuclease activity of Escherichia coli DNA polymerase I: a two metal ion mechanism. EMBO J. 10:1991;25-33.
4. Black C. B., Cowan J. A. Inert chromium and cobalt complexes as probes of magnesium-dependent enzymes. Evaluation of the mechanistic role of the essential metal cofactor in Escherichia coli exonuclease III. Eur. J. Biochem. 243:1997;684-689.
5. Cal S., Tan K. L., McGregor A., Connolly B. A. Conversion of bovine pancreatic DNase I to a repair endonuclease with a high selectivity for abasic sites. EMBO J. 17:1998;7128-7138.
6. Demple B., Harrison L. Repair of oxidative damage to DNA: enzymology and biology. Annu. Rev. Biochem. 3:1994;915-948.
7. Demple B., Herman T., Chen D. S. Cloning and expression of APE1, the cDNA encoding the major human apurinic endonuclease: definition of a family of DNA repair enzymes. Proc. Natl Acad. Sci. USA. 88:1991;11450-11454.
8. Demple B., Harrison L., Wilson D. M. III, Bennett R. A., Takagi T., Ascione A. G. Regulation of eukaryotic abasic endonucleases and their role in genetic stability. Environ. Health Perspect. 105:1997;931-934.
9. Denu J. M., Lohse D. L., Vijayalakshmi J., Saper M. A., Dixon J. E. Visualization of intermediate and transition-state structures in protein-tyrosine phosphatase catalysis. Proc. Natl Acad. Sci. USA. 93:1996;2493-2498.
10. Erzberger J. P., Barsky D., Schärer O. D., Colvin M. E., Wilson D. M. III. Elements in abasic site recognition by the major human and Escherichia coli apurinic/apyrimidinic endonucleases. Nucl. Acids Res. 26:1998;2771-2778.
11. Gerlt J. A. Mechanistic principles of enzyme- catalyzed cleavage of phosphodiester bonds. Nucleases. 1993;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York. p. 1-34.
12. Gorman M. A., Morera S., Rothwell D. G., de La 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.
13. Hang B., Rothwell D. G., Sagi J., Hickson I. D., Singer B. Evidence for a common active site for cleavage of an AP site and the benzene-derived exocyclic adduct, 3, N4-benzetheno-dC, in the major human AP endonuclease. Biochemistry. 36:1997;15411-15418.
14. Hondal R. J., Zhao Z., Kravchuk A. V., Liao H., Riddle S. R., Yue X., Bruzik K. S., Tsai M. D. Mechanism of phosphatidylinositol-specific phospholipase C: a unified view of the mechanism of catalysis. Biochemistry. 37:1998;4568-4580.
15. Izumi T., Malecki J., Chaudhry M. A., Weinfeld M., Hill J. H., Lee J. C., Mitra S. Intragenic suppression of an active site mutation in the human apurinic/apyrimidinic endonuclease. J. Mol. Biol. 287:1999;47-57.
16. Jones S. J., Worrall A. F., Connolly B. A. Site-directed mutagenesis of the catalytic residues of bovine pancreatic deoxyribonuclease I. J. Mol. Biol. 264:1996;1154-1163.
17. Kalnik M. W., Chang C. N., Johnson F., Grollman A. P., Patel D. J. NMR studies of abasic sites in DNA duplexes: deoxyadenosine stacks into the helix opposite acyclic lesions. Biochemistry. 28:1989;3373-3383.
18. Kane C. M., Linn S. Purification and characterization of an apurinic/apyrimidinic endonuclease from HeLa cells. J. Biol. Chem. 256:1981;3405-3414.
19. Krokan H. E., Standal R., Slupphaug G. DNA glycosylases in the base excision repair of DNA. Biochem. J. 325:1997;1-16.
20. Lindahl T. Instability and decay of the primary structure of DNA. Nature. 362:1993;709-715.
21. Loeb L. A., Preston B. D. Mutagenesis by apurinic/apyrimidinic sites. Annu. Rev. Genet. 20:1986;201-230.
22. Masuda Y., Bennett R. A. O., Demple B. Rapid dissociation of human apurinic endonuclease (Ape1) from incised DNA induced by magnesium. J. Biol. Chem. 273:1998;30360-30365.
23. Mol C. D., Kuo C. F., Thayer M. M., Cunningham R. P., Tainer J. A. Structure and function of the multifunctional DNA-repair enzyme exonuclease III. Nature. 374:1995;381-386.
24. Robson C. N., Hochhauser D., Craig R., Rack K., Buckle V. J., Hickson I. D. Structure of the human DNA repair gene HAP1 and its localisation to chromosome 14q 11.2-12. Nucl. Acids Res. 20:1992;4417-4421.
25. Robson C. N., Hickson I. D. Isolation of cDNA clones encoding a human apurinic/apyrimidinic endonuclease that corrects DNA repair and mutagenesis defects in E. coli xth (exonuclease III) mutants. Nucl. Acids Res. 19:1991;5519-5523.
26. Suck D., Oefner C. Structure of DNase I at 2.0 Å resolution suggests a mechanism for binding to and cutting DNA. Nature. 321:1986;620-625.
27. Takeshita M., Chang C. N., Johnson F., Will S., Grollman A. P. Oligodeoxynucleotides containing synthetic abasic sites. Model substrates for DNA polymerases and apurinic/apyrimidinic endonucleases. J. Biol. Chem. 262:1987;10171-10179.
28. Weston S. A., Lahm A., Suck D. X-ray structure of the DNase I-d(GGTATACC)2 complex at 2.3 Å resolution. J. Mol. Biol. 226:1992;1237-1256.
29. Wilson S. H. Mammalian base excision repair and DNA polymerase beta. Mutat. Res. 407:1998;203-215.
30. Wilson D. M. III, Thompson L. H. Life without DNA repair. Proc. Natl Acad. Sci. USA. 94:1997;12754-12757.
31. Wilson D. M. III, Takeshita M., Grollman A. P., Demple B. Incision activity of human apurinic endonuclease (Ape1) at abasic site analogs in DNA. J. Biol. Chem. 270:1995;16002-16007.
32. Wilson D. M. III, Takeshita M., Demple B. Abasic site binding by the human apurinic endonuclease, Ape1, and determination of the DNA contact sites. Nucl. Acids Res. 25:1997;933-939.
33. Wu L., Zhang Z. Y. Probing the function of Asp128 in the lower molecular weight protein-tyrosine phosphatase-catalyzed reaction. A pre-steady-state and steady-state kinetic investigation. Biochemistry. 35:1996;5426-5434.
34. Xanthoudakis S., Smeyne R. J., Wallace J. D., Curran T. The redox/DNA repair protein, Ref-1, is essential for early embryonic development in mice. Proc. Natl Acad. Sci. USA. 93:1996;8919-8923.