Identification of two apurinic/apyrimidinic endonucleases from Caenorhabditis elegans by cross-species complementation

DNA Repair

Volumn 4, Issue 6, 2005, Pages 655-670

  Shatilla, Andrea ^a   Leduc, Anick ^a   Yang, Xiaoming ^a   Ramotar, Dindial ^a  

^a MAISONNEUVE ROSEMONT HOSPITAL   (Canada)

Author keywords

Base excision; C. elegans; DNA repair; Enzymes; Mutations; Yeast

Indexed keywords

3' DIESTERASE; COMPLEMENTARY DNA; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; ENDONUCLEASE; ESTERASE; EXODEOXYRIBONUCLEASE III; GENE PRODUCT; MUTANT PROTEIN; PROTEIN APN 1; PROTEIN EXO 3; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DNA DAMAGE; DNA LIBRARY; DNA REPAIR; ENZYME ACTIVITY; ENZYME ANALYSIS; ESCHERICHIA COLI; GENE ISOLATION; GENETIC CODE; GENETIC COMPLEMENTATION; GENETIC STABILITY; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; SPONTANEOUS MUTATION;

AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DNA REPAIR; DNA, BACTERIAL; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; ENDODEOXYRIBONUCLEASES; ESCHERICHIA COLI; GENE EXPRESSION; GENE LIBRARY; GENETIC COMPLEMENTATION TEST; GENETIC VECTORS; GLUTATHIONE TRANSFERASE; HELMINTH PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; PLASMIDS; PROMOTER REGIONS (GENETICS); RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID;

CAENORHABDITIS ELEGANS; ESCHERICHIA COLI; SACCHAROMYCES CEREVISIAE;

EID: 19344378245     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2005.02.005     Document Type: Article

References (68)

1. T. Lindahl New class of enzymes acting on damaged DNA Nature 259 1976 64 66
2. H.E. Krokan, R. Standal, and G. Slupphaug DNA glycosylases in the base excision repair of DNA Biochem. J. 325 1997 1 16
3. T. Lindahl, and B. Nyberg Rate of depurination of native deoxyribonucleic acid Biochemistry 11 1972 3610 3618
4. B. Demple, and L. Harrison Repair of oxidative damage to DNA: enzymology and biology Annu. Rev. Biochem. 63 1994 915 948
5. H.R. Warner, B.F. Demple, W.A. Deutsch, C.M. Kane, and S. Linn Apurinic/apyrimidinic endonucleases in repair of pyrimidine dimers and other lesions in DNA Proc. Natl. Acad. Sci. U.S.A. 77 1980 4602 4606
6. D. Ramotar The apurinic-apyrimidinic endonuclease IV family of DNA repair enzymes Biochem. Cell Biol. 75 1997 327 336
7. S.C. Popoff, A.I. Spira, A.W. Johnson, and B. Demple Yeast structural gene (APN1) for the major apurinic endonuclease: homology to Escherichia coli endonuclease IV Proc. Natl. Acad. Sci. U.S.A. 87 1990 4193 4197
8. R.E. Johnson, C.A. Torres-Ramos, T. Izumi, S. Mitra, S. Prakash, and L. Prakash Identification of APN2, the Saccharomyces cerevisiae homolog of the major human AP endonuclease HAP1, and its role in the repair of abasic sites Genes Dev. 12 1998 3137 3143 (in process citation)
9. B. Demple, T. Herman, and D.S. Chen 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. U.S.A. 88 1991 11450 11454
10. R.P. Cunningham, S.M. Saporito, S.G. Spitzer, and B. Weiss Endonuclease IV (nfo) mutant of Escherichia coli J. Bacteriol. 168 1986 1120 1127
11. L.A. Loeb, and B.D. Preston Mutagenesis by apurinic/apyrimidinic sites Annu. Rev. Genet. 20 1986 201 230
12. J.R. Vance, and T.E. Wilson Repair of DNA strand breaks by the overlapping functions of lesion-specific and non-lesion-specific DNA 3′ phosphatases Mol. Cell. Biol. 21 2001 7191 7198
13. R.A. Bennett The Saccharomyces cerevisiae ETH1 gene, an inducible homolog of exonuclease III that provides resistance to DNA-damaging agents and limits spontaneous mutagenesis Mol. Cell. Biol. 19 1999 1800 1809
14. D. Ramotar, S.C. Popoff, E.B. Gralla, and B. Demple 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 1991 4537 4544
15. A.S. Karumbati, R.A. Deshpande, A. Jilani, J.R. Vance, D. Ramotar, and T.E. Wilson The role of yeast DNA 3′-phosphatase Tpp1 and Rad1/Rad10 endonuclease in processing spontaneous and induced base lesions J. Biol. Chem. 278 2003 31434 31443
16. J.Y. Masson, S. Tremblay, and D. Ramotar The Caenorhabditis elegans gene CeAPN1 encodes a homolog of Escherichia coli and yeast apurinic/apyrimidinic endonuclease Gene 179 1996 291 293
17. A. Shatilla, and D. Ramotar Embryonic extracts derived from the nematode Caenorhabditis elegans remove uracil from DNA by the sequential action of uracil-DNA glycosylase and AP (apurinic/apyrimidinic) endonuclease Biochem. J. 365 2002 547 553
18. D. Ramotar, and B. Demple Functional expression of Escherichia coli endonuclease IV in apurinic endonuclease-deficient yeast J. Biol. Chem. 271 1996 7368 7374
19. J.Y. Masson, and D. Ramotar Normal processing of AP sites in Apn1-deficient Saccharomyces cerevisiae is restored by Escherichia coli genes expressing either exonuclease III or endonuclease III Mol. Microbiol. 24 1997 711 721
20. D. Ramotar, S.C. Popoff, and B. Demple Complementation of DNA repair-deficient Escherichia coli by the yeast Apn1 apurinic/apyrimidinic endonuclease gene Mol. Microbiol. 5 1991 149 155
21. D.M. Wilson III, R.A. Bennett, J.C. Marquis, P. Ansari, and B. Demple Trans-complementation by human apurinic endonuclease (Ape) of hypersensitivity to DNA damage and spontaneous mutator phenotype in apn1-yeast Nucleic Acids Res. 23 1995 5027 5033
22. G. Barzilay, C.D. Mol, C.N. Robson, L.J. Walker, R.P. Cunningham, J.A. Tainer, and I.D. Hickson Identification of critical active-site residues in the multifunctional human DNA repair enzyme HAP1 Nat. Struct. Biol. 2 1995 561 568
23. G. Barzilay, L.J. Walker, C.N. Robson, and I.D. Hickson Site-directed mutagenesis of the human DNA repair enzyme HAP1: identification of residues important for AP endonuclease and RNase H activity Nucleic Acids Res. 23 1995 1544 1550
24. K.M. Chou, and Y.C. Cheng The exonuclease activity of human apurinic/apyrimidinic endonuclease (APE1) Biochemical properties and inhibition by the natural dinucleotide Gp4G J. Biol. Chem. 278 2003 18289 18296
25. G. Barzilay, and I.D. Hickson Structure and function of apurinic/apyrimidinic endonucleases Bioessays 17 1995 713 719
26. 2+ 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 J. Mol. Biol. 290 1999 447 457
27. T. Izumi, J. Malecki, M.A. Chaudhry, M. Weinfeld, J.H. Hill, J.C. Lee, and S. Mitra Intragenic suppression of an active site mutation in the human apurinic/apyrimidinic endonuclease J. Mol. Biol. 287 1999 47 57
28. D. Gietz, A. St. Jean, R.A. Woods, and R.H. Schiestl Improved method for high efficiency transformation of intact yeast cells Nucleic Acids Res. 20 1992 1425
29. J. Sambrook E.F. Fritsch T. Maniatis Molecular Cloning: A Laboratory Manual 1989 Cold Spring Harbor New York
30. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
31. J.Y. Masson, and D. Ramotar The Saccharomyces cerevisiae IMP2 gene encodes a transcriptional activator that mediates protection against DNA damage caused by bleomycin and other oxidants Mol. Cell. Biol. 16 1996 2091 2100
32. A. Jilani, R. Vongsamphanh, A. Leduc, L. Gros, M. Saparbaev, and D. Ramotar Characterization of two independent amino acid substitutions that disrupt the DNA repair functions of the yeast Apn1 Biochemistry 42 2003 6436 6445
33. E.C. Friedberg G.C. Walker W. Siede DNA Repair and Mutagenesis 1995 ASM Press Washington, DC
34. G.P. Margison, and P.J. O'Connor Biological implications of the instability of the N-glycosidic bone of 3-methyldeoxyadenosine in DNA Biochim. Biophys. Acta 331 1973 349 356
35. L. Giloni, M. Takeshita, F. Johnson, C. Iden, and A.P. Grollman Bleomycin-induced strand-scission of DNA Mechanism of deoxyribose cleavage J. Biol. Chem. 256 1981 8608 8615
36. D. Ramotar, and H. Wang Protective mechanisms against the antitumor agent bleomycin: lessons from Saccharomyces cerevisiae Curr. Genet. 43 2003 213 224
37. 2-damaged Escherichia coli Proc. Natl. Acad. Sci. U.S.A. 83 1986 7731 7735
38. A. Mazumder, J.A. Gerlt, M.J. Absalon, J. Stubbe, R.P. Cunningham, J. Withka, and P.H. Bolton Stereochemical studies of the beta-elimination reactions at aldehydic abasic sites in DNA: endonuclease III from Escherichia coli, sodium hydroxide, and Lys-Trp-Lys Biochemistry 30 1991 1119 1126
39. R.L. Swanson, N.J. Morey, P.W. Doetsch, and S. Jinks-Robertson Overlapping specificities of base excision repair, nucleotide excision repair, recombination, and translesion synthesis pathways for DNA base damage in Saccharomyces cerevisiae Mol. Cell. Biol. 19 1999 2929 2935
40. K.L. Meadows, B. Song, and P.W. Doetsch Characterization of AP lyase activities of Saccharomyces cerevisiae Ntg1p and Ntg2p: implications for biological function Nucleic Acids Res. 31 2003 5560 5567
41. M. Aouida, A. Leduc, H. Wang, and D. Ramotar Characterization of a transport and detoxification pathway for the antitumour drug bleomycin in Saccharomyces cerevisiae Biochem. J. 384 2004 47 58
42. M. Hanna, B.L. Chow, N.J. Morey, S. Jinks-Robertson, P.W. Doetsch, and W. Xiao Involvement of two endonuclease III homologs in the base excision repair pathway for the processing of DNA alkylation damage in Saccharomyces cerevisiae DNA Repair (Amsterdam) 3 2004 51 59
43. P.S. Hartman, and R.K. Herman Radiation-sensitive mutants of Caenorhabditis elegans Genetics 102 1982 159 178
44. S.J. Boulton, A. Gartner, J. Reboul, P. Vaglio, N. Dyson, D.E. Hill, and M. Vidal Combined functional genomic maps of the C. elegans DNA damage response Science 295 2002 127 131
45. M.J. Schofield, and P. Hsieh DNA mismatch repair: molecular mechanisms and biological function Annu. Rev. Microbiol. 57 2003 579 608
46. S.J. Boulton, J.S. Martin, J. Polanowska, D.E. Hill, A. Gartner, and M. Vidal BRCA1/BARD1 orthologs required for DNA repair in Caenorhabditis elegans Curr. Biol. 14 2004 33 39
47. K.O. Kelly, A.F. Dernburg, G.M. Stanfield, and A.M. Villeneuve Caenorhabditis elegans msh-5 is required for both normal and radiation-induced meiotic crossing over but not for completion of meiosis Genetics 156 2000 617 630
48. G.M. Chin, and A.M. Villeneuve C. elegans mre-11 is required for meiotic recombination and DNA repair but is dispensable for the meiotic G(2) DNA damage checkpoint Genes Dev. 15 2001 522 534
49. M.H. Lee, S.M. Han, J.W. Han, Y.M. Kim, J. Ahnn, and H.S. Koo Caenorhabditis elegans dna-2 is involved in DNA repair and is essential for germ-line development FEBS Lett. 555 2003 250 256
50. C.L. Peterson, and J. Cote Cellular machineries for chromosomal DNA repair Genes Dev. 18 2004 602 616
51. J.D. Levin, and B. Demple In vitro detection of endonuclease IV-specific DNA damage formed by bleomycin in vivo Nucleic Acids Res. 24 1996 885 889
52. M.E. Hagensee, and R.E. Moses Bleomycin-treated DNA is specifically cleaved only by endonuclease IV in E. coli Biochim. Biophys. Acta 1048 1990 19 23
53. A.A. Ischenko, and M.K. Saparbaev Alternative nucleotide incision repair pathway for oxidative DNA damage Nature 415 2002 183 187
54. C.V. Ramana, I. Boldogh, T. Izumi, and S. Mitra Activation of apurinic/apyrimidinic endonuclease in human cells by reactive oxygen species and its correlation with their adaptive response to genotoxicity of free radicals Proc. Natl. Acad. Sci. U.S.A. 95 1998 5061 5066
55. K.A. Robertson, H.A. Bullock, Y. Xu, R. Tritt, E. Zimmerman, T.M. Ulbright, R.S. Foster, L.H. Einhorn, and M.R. Kelley Altered expression of Ape1/ref-1 in germ cell tumors and overexpression in NT2 cells confers resistance to bleomycin and radiation Cancer Res. 61 2001 2220 2225
56. D. Ramotar, C. Kim, R. Lillis, and B. Demple Intracellular localization of the Apn1 DNA repair enzyme of Saccharomyces cerevisiae Nuclear transport signals and biological role J. Biol. Chem. 268 1993 20533 20539
57. R. Vongsamphanh, P.K. Fortier, and D. Ramotar Pir1p mediates translocation of the yeast Apn1p endonuclease into the mitochondria to maintain genomic stability Mol. Cell. Biol. 21 2001 1647 1655
58. I. Unk, L. Haracska, R.E. Johnson, S. Prakash, and L. Prakash Apurinic endonuclease activity of yeast Apn2 protein J. Biol. Chem. 275 2000 22427 22434
59. M.Z. Hadi, and D.M. Wilson III Second human protein with homology to the Escherichia coli abasic endonuclease exonuclease III Environ. Mol. Mutagen. 36 2000 312 324
60. J.A. Lucas, Y. Masuda, R.A. Bennett, N.S. Strauss, and P.R. Strauss Single-turnover analysis of mutant human apurinic/apyrimidinic endonuclease Biochemistry 38 1999 4958 4964
61. Y. Masuda, R.A. Bennett, and B. Demple Rapid dissociation of human apurinic endonuclease (Ape1) from incised DNA induced by magnesium J. Biol. Chem. 273 1998 30360 30365
62. Y. Masuda, R.A. Bennett, and B. Demple Dynamics of the interaction of human apurinic endonuclease (Ape1) with its substrate and product J. Biol. Chem. 273 1998 30352 30359
63. R.A. Bennett, D.M. Wilson III, D. Wong, and B. Demple Interaction of human apurinic endonuclease and DNA polymerase beta in the base excision repair pathway Proc. Natl. Acad. Sci. U.S.A. 94 1997 7166 7169
64. T.A. Ranalli, S. Tom, and R.A. Bambara AP endonuclease 1 coordinates flap endonuclease 1 and DNA ligase I activity in long patch base excision repair J. Biol. Chem. 277 2002 41715 41724
65. F. Piano, A.J. Schetter, D.G. Morton, K.C. Gunsalus, V. Reinke, S.K. Kim, and K.J. Kemphues Gene clustering based on RNAi phenotypes of ovary-enriched genes in C. elegans Curr. Biol. 12 2002 1959 1964
66. S. Xanthoudakis, R.J. Smeyne, J.D. Wallace, and T. Curran The redox/DNA repair protein, Ref-1, is essential for early embryonic development in mice Proc. Natl. Acad. Sci. U.S.A. 93 1996 8919 8923
67. S. Xanthoudakis, G. Miao, F. Wang, Y.C. Pan, and T. Curran Redox activation of Fos-Jun DNA binding activity is mediated by a DNA repair enzyme EMBO J. 11 1992 3323 3335
68. L.J. Walker, C.N. Robson, E. Black, D. Gillespie, and I.D. Hickson Identification of residues in the human DNA repair enzyme HAP1 (Ref-1) that are essential for redox regulation of Jun DNA binding Mol. Cell. Biol. 13 1993 5370 5376