Base Excision Repair of Oxidative DNA lesions in plants
162 64
Keywords:
Reactive oxygen species, Base excision repair, DNA-glycosylase, AP-endonuclease, DNA-polymerase,Abstract
Reactive oxygen species cause damage to all cellular macromolecules including membrane lipids, proteins and nucleic acids. Increased level of reactive oxygen species triggers cell death in plant and animal organisms indicating common mechanisms and targets of the free radicals action. DNA is the main cellular target for reactive oxygen species, currently, about 80 different types of oxidative damage to DNA have been identified including strand breaks, base and sugar modifications. In cells reactive oxygen species generate mostly non-bulky DNA lesions, the majority of which are substrates for the base excision repair.
Until now, molecular characterizations of the DNA repair mechanisms have been mainly focused on E. coli, yeast and mammalian cells. As sessile organisms, plants are continuously exposed to a range of environmental genotoxic agents, including the ultraviolet (UV) component of sunlight, soil and air pollutants. In addition, plants continuously generate reactive oxygen species (ROS) as byproducts of metabolic reactions that take place in chloroplasts, mitochondria and peroxisomes. Oxidative damage to DNA caused by ROS is believed to be a major type of endogenous cellular damage. Moreover, plants lack a reserved germline and produce meiotic cells late in development, so mutations arising in somatic cells may be represented in gametes. To keep genome integrity and to assure faithful transfer of genetic information during cell division, living organisms develop several distinct DNA repair systems that remove and/or tolerate the DNA lesions. Although DNA repair mechanisms are well studied in bacteria, yeast, nematode and mammalian cells, little is known about the base excision repair pathway in plant. Recent advances in the study of DNA repair in higher plants show that they use mechanisms similar to those present in other eukaryotes to remove oxidized bases and other oxidative DNA lesions. In plants DNA repair is not only a fundamental cellular process for protecting cells against the damage, but is also essential to ensure faithful transmission of genetic information from one generation to the next.
References
1 Dizdaroglu M, Jaruga P, Birincioglu M, Rodriguez H (2002) Free radical-induced damage to DNA: mechanisms and measurement, Free Radic Biol Med, 32:1102-1115.
2 Hegde ML, Hazra TK, Mitra S (2008) Early steps in the DNA base excision/single-strand interruption repair pathway in mammalian cells, Cell Research, 18:27–47.
3 Hoeijmakers JH (2009) DNA damage, aging, and cancer, N Engl J Med, 361:1475-1485.
4 Roldaґn-Arjona T, Ariza RR (2009) Repair and tolerance of oxidative DNA damage in plants, Mutation Research, 681:169–179.
5 Foyer CH, Noctor G. (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria, Physiol Plant, 119:355-364.
6 Bissenbaev AK, Ishchenko AA, Taipakova SM, Saparbaev MK (2011) Presence of base excision repair enzymes in the wheat aleurone and their activation in cells undergoing programmed cell death, Plant Physiol Biochem, 49:1155-1164.
7 Bissenbaev AK, Altybaeva NA, Kolbaeva GA (2007) Role of reactive oxygen species and antioxidant enzymes in hormone regulating programmed cell death of wheat aleurone layer, Journal of Cell and Molecular Biology, 6(1): 41-48.
8 Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction, Annu Rev Plant Biol, 55:373-399.
9 Mehlhorn H, Tabner BJ, Wellburn AR (1990) Electron-spin-resonance evidence for the formation of free-radicals in plants exposed to ozone, Physiol Plant, 79: 377-383.
10 Landry LG, Chapple CC, Last RL (1995) Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced ultraviolet-B injury and oxidative damage, Plant Physiol, 109:1159-1166.
11 Ward JF (1988) DNA damage produced by ionizing radiation in mammalian cells: identities, mechanisms of formation, and reparability, Prog Nucleic Acid Res Mol Biol, 35: 95-125.
12 Hutchinson F (1957) The distance that a radical formed by ionizing radiation candiffuse in a yeast cell, Radiat Res, 7: 473-483.
13 Conklin PL, Williams EH, Last RL (1996) Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant, Proc Natl Acad Sci U S A, 93: 9970-9974.
14 Dizdaroglu M (1993) Chemistry of free radical damage to DNA and nucleoproteins, in: B Halliwell, OI Aruoma (Eds.). DNA and Free Radicals. Ellis Horwood, London. - P.19
15 Furlong EA, Jorgenson TJ, Henner WD (1986) Production of dihydrothymine stereoisomers in DNA by gamma-radiation, Biochemistry, 25: 4344-4349.
16 Teoule R (1987) Radiation-induced DNA damage and its repair, Int J Radiat Biol, 51: 589.
17 Dizdaroglu M (1985) Formation of an 8-hydroxyguanine moiety in deoxyribonucleic acid on gamma-irradiation in aqueous solution, Biochemistry, 24: 4476- 4481.
18 Fuciarelli AF, Wegher BJ, Blakely WF, Dizdaroglu M (1990) Yields of radiationinduced base products in DNA: effects of DNA conformation and gassing conditions, Int J Radiat Biol, 58: 397-415.
19 Fink SP, Reddy GR, Marnett LJ (1997) Mutagenicity in Escherichia coli of the major DNA adduct derived from the endogenous mutagen malondialdehyde, Proc Natl Acad Sci U S A, 94: 8652-8657.
20 Saparbaev M, Laval J (1998) 3,N4-ethenocytosine, a highly mutagenic adduct, is a primary substrate for Escherichia coli double-stranded uracil-DNA glycosylase and human mismatch-specific thymine-DNA glycosylase, Proc Natl Acad Sci U.S.A., 95: 8508-8513.
21 Ide H, Kow YW, Wallace SS (1985) Thymine glycols and urea residues in M13 DNA constitute replicative blocks in vitro, Nucleic Acids Res, 13: 8032-8052.
22 Evans J, Maccabee M, Hatahet Z, Courcelle J, Bockrath R, Ide H, Wallace S (1993) Thymine ring saturation and fragmentation products: lesion bypass, misinsertion and implications for mutagenesis, Mutat Res, 299: 147-156.
23 Boorstein RJ, Hilbert TP, Cadet J, Cunningham RP, Teebor GW (1989) UV-induced pyrimidine hydrates in DNA are repaired by bacterial and mammalian DNA glycosylase activities, Biochemistry, 28: 6164-6170.
24 Roldan-Arjona T, Garcia-Ortiz MV, Ruiz-Rubio M, Ariza RR (2000) cDNA cloning, expression and functional characterization of an Arabidopsis thaliana homologue of the Escherichia coli DNA repair enzyme endonuclease III, Plant Mol Biol, 44: 43-52.
25 Krokan HE, Standal R, Slupphaug G (1997) DNA glycosylases in the base excision repair of DNA, Biochem J, 325: 1-16.
26 Girard PM, Boiteux S (1997) Repair of oxidized DNA bases in the yeast Saccharomyces cerevisiae, Biochimie, 79:559-566.
27 Denver DR, Swenson SL, Lynch M (2003) An evolutionary analysis of the helix-hairpin-helix superfamily of DNA repair glycosylases, Mol Biol Evol, 20: 1603-1611.
28 Alseth I, Eide L, Pirovano M, Rognes T, Seeberg E, Bjoras M (1999) The Saccharomyces cerevisiae homologues of endonuclease III from Escherichia coli, Ntg1 and Ntg2, are both required for efficient repair of spontaneous and induced oxidative DNA damage in yeast, Mol Cell Biol, 19: 3779-3787.
29 Jiang D, Hatahet Z, Blaisdell JO, Melamede RJ, Wallace SS (1997) Escherichia coli endonuclease VIII: cloning, sequencing, and overexpression of the nei structural gene and characterization of nei and nei nth mutants, J Bacteriol, 179: 3773-3782.
30 Grin IR, Zharkov DO (2011) Eukaryotic homologs of endonuclease VIII: new elements of excision repair of DNA base [Biohimya]. 76(1):99 – 114.
31 Tchou J, Kasai H, Shibutani S, Chung MH, Laval J, Grollman AP, Nishimura S (1991) 8-Oxoguanine (8-hydroxyguanine) DNA glycosylase and its substrate specificity, Proc. Natl. Acad. Sci. U S A, 88:4690-4694.
32 Eisen JA, Hanawalt PC (1999) A phylogenomic study of DNA repair genes, proteins, and processes, Mutat Res, 435:171-213.
33 van der Kemp PA, Thomas D, Barbey R, de Oliveira R, Boiteux S (1996) Cloning and expression in Escherichia coli of the OGG1 gene of Saccharomyces cerevisiae, which codes for a DNA glycosylase that excises 7,8-dihydro-8-oxoguanine and 2,6-diamino-4-hydroxy-5-N-methylformamidopyrimidine, Proc Natl Acad Sci U S A, 93: 5197-5202.
34 Roldan-Arjona T, Wei YF, Carter KC, Klungland A, Anselmino C, Wang RP, Augustus M, Lindahl T (1997) Molecular cloning and functional expression of a human cDNA encoding the antimutator enzyme 8-hydroxyguanine-DNA glycosylase, Proc Natl Acad Sci U S A, 94:8016-8020.
35 Ohtsubo T, Matsuda O, Iba K, Terashima I, Sekiguchi M, Nakabeppu Y (1998) Molecular cloning of AtMMH, an Arabidopsis thaliana ortholog of the Escherichia coli mutM gene, and analysis of functional domains of its product, Mol Gen Genet, 259:577-590.
36 Dany AL, Tissier A (2001) A functional OGG1 homologue from Arabidopsis thaliana, Mol Genet Genom, 265: 293-301.
37 Garcia-Ortiz MV, Ariza RR, Roldan-Arjona T (2001) An OGG1 orthologue encoding a functional 8-oxoguanine DNA glycosylase/lyase in Arabidopsis thaliana, Plant Mol Biol, 47: 795-804.
38 Scortecci KC, Lima AF, Carvalho FM, Silva UB, Agnez-Lima LF, Batistuzzo de Medeiros SR (2007) A characterization of a MutM/Fpg ortholog in sugarcane—a monocot plant, Biochem Biophys Res Commun, 361: 1054-1060.
39 Morales-Ruiz T, Birincioglu M, Jaruga P, Rodriguez H, Roldan-Arjona T, Dizdaroglu M (2003) Arabidopsis thaliana Ogg1 protein excises 8-hydroxyguanine and 2,6-diamino-4-hydroxy-5-formamidopyrimidine from oxidatively damaged DNA containing multiple lesions, Biochemistry, 42: 3089-3095.
40 Murphy TM (2005) What is base excision repair good for? knockout mutants for FPG and OGG glycosylase genes in Arabidopsis, Physiol Plant, 123: 227-232.
41 Leprince O, Atherton NM, Deltour R, Hendry G (1994) The involvement of respiration in free radical processes during loss of desiccation tolerance in germinating Zea mays L, Plant Physiol, 104: 1333-1339.
42 Reuzeau C, Cavalie G (1995) Activities of free-radical processing enzymes in dry sunflower Seeds, New Phytol, 130: 59-66.
43 Bird AP (1980) DNA methylation and the frequency of CpG in animal DNA, Nucleic Acids Res, 8: 1499-1504.
44 Hendrich B, Hardeland U, Ng HH, Jiricny J, Bird A (1999) The thymine glycosylase MBD4 can bind to the product of deamination at methylated CpG sites, Nature, 401: 301–304.
45 Petronzelli F, Riccio A, Markham GD, Seeholzer SH, Genuardi M, Karbowski M, Yeung AT, Matsumoto Y and Bellacosa A (2000) Investigation of the substrate spectrum of the human mismatch-specific DNA N-glycosylase MED1 (MBD4): fundamental role of the catalytic domain, J Cell Physiol, 185: 473–480.
46 Nota F, Cambiagno DA, Ribone P, Alvarez ME (2015) Expression and function of AtMBD4L, the single gene encoding the nuclear DNA glycosylase MBD4L in Arabidopsis, Plant Sci, 235:122-129.
47 He XJ, Chen T, Zhu JK (2011) Regulation and function of DNA methylation in plants and animals, Cell Res, 21: 442–465.
48 Zhu JK (2009) Active DNA demethylation mediated by DNA glycosylases, Annu Rev Genet, 43: 143–166.
49 Chou KM, Cheng YC (2002) An exonucleolytic activity of human apurinic/apyrimidinic endonuclease on 3' mispaired DNA, Nature, 415: 655-659.
50 Babiychuk E, Kushnir S, Van Montagu M, Inze D (1994) The Arabidopsis thaliana apurinic endonuclease Arp reduces human transcription factors Fos and Jun, Proc Natl Acad Sci U S A, 91:3299-3303.
51 Murphy TM, Belmonte M, Shu S, Britt AB, Hatteroth J (2009) Requirement for abasic endonuclease gene homologues in Arabidopsis seed development, PLoS One, 4: e4297.
52 Joldybayeva B, Prorok P, Grin IR, Zharkov DO, Ishenko AA, et al. (2014) Cloning and Characterization of a Wheat Homologue of Apurinic/Apyrimidinic Endonuclease Ape1L // PLoS ONE, 9(3): e92963, doi:10.1371/journal.pone.0092963.
53 Wiederhold L, Leppard JB, Kedar P, Karimi-Busheri F, Rasouli-Nia A, Weinfeld M, Tomkinson AE, Izumi T, Prasad R, Wilson SH, Mitra S, Hazra TK (2004) AP endonuclease-independent DNA base excision repair in human cells, Mol Cell, 15: 209-220.
54 Whitehouse CJ, Taylor RM, Thistlethwaite A, Zhang H, Karimi-Busheri F, Lasko DD, Weinfeld M, Caldecott KW (2001) XRCC1 stimulates human polynucleotide kinase activity at damaged DNA termini and accelerates DNA single-strand break repair, Cell, 104: 107-117.
55 55 Betti M, Petrucco S, Bolchi A, Dieci G, Ottonello S (2001) A plant 30-phosphoesterase involved in the repair of DNA strand breaks generated by oxidative damage, J Biol Chem, 276: 18038-18045.
56 Petrucco S, Volpi G, Bolchi A, Rivetti C, Ottonello S (2002) A nick-sensing DNA 30- repair enzyme from Arabidopsis, J Biol Chem, 277: 23675-23683.
57 Martinez-Macias MI, Qian W, Miki D, Pontes O, Liu Y, et al. (2012) A DNA 3' -phosphatase functions in active DNA demethylation in Arabidopsis, Mol Cell, 45: 357–370.
58 Garcia-Diaz M, Dominguez O, Lopez-Fernandez LA, de Lera LT, Saniger ML, Ruiz JF, Parraga M, Garcia-Ortiz MJ, Kirchhoff T, del Mazo J, Bernad A, Blanco L (2000) DNA polymerase lambda (Pol lambda), a novel eukaryotic DNA polymerase with a potential role in meiosis, J Mol Biol, 301: 851-867.
59 Uchiyama Y, Kimura S, Yamamoto T, Ishibashi T, Sakaguchi K (2004) Plant DNA polymerase lambda, a DNA repair enzyme that functions in plant meristematic and meiotic tissues, Eur J Biochem, 271: 2799-2807.
60 Mori Y, Kimura S, Saotome A, Kasai N, Sakaguchi N, Uchiyama Y, Ishibashi T, Yamamoto T, Chiku H, Sakaguchi K (2005) Plastid DNA polymerases from higher plants, Arabidopsis thaliana, Biochem Biophys Res Commun, 334: 43-50.
61 Takeuchi R, Kimura S, Saotome A, Sakaguchi K (2007) Biochemical properties of a plastidial DNA polymerase of rice, Plant Mol Biol, 64: 601-611.
62 Vidal AE, Boiteux S, Hickson ID, Radicella JP (2001) XRCC1 coordinates the initial and late stages of DNA abasic site repair through protein-protein interactions, EMBO J, 20: 6530-6539.
63 Taylor RM, Thistlethwaite A, Caldecott KW (2002) Central role for the XRCC1 BRCT I domain in mammalian DNA single-strand break repair, Mol Cell Biol, 22: 2556-2563.
64 Taylor RM, Hamer MJ, Rosamond J, Bray CM (1998) Molecular cloning and functional analysis of the Arabidopsis thaliana DNA ligase I homologue, Plant J, 14: 75-81.
65 Wu YQ, Hohn B, Ziemienowic A (2001) Characterization of an ATP-dependent type I DNA ligase from Arabidopsis thaliana, Plant Mol Biol, 46: 161-170.
2 Hegde ML, Hazra TK, Mitra S (2008) Early steps in the DNA base excision/single-strand interruption repair pathway in mammalian cells, Cell Research, 18:27–47.
3 Hoeijmakers JH (2009) DNA damage, aging, and cancer, N Engl J Med, 361:1475-1485.
4 Roldaґn-Arjona T, Ariza RR (2009) Repair and tolerance of oxidative DNA damage in plants, Mutation Research, 681:169–179.
5 Foyer CH, Noctor G. (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria, Physiol Plant, 119:355-364.
6 Bissenbaev AK, Ishchenko AA, Taipakova SM, Saparbaev MK (2011) Presence of base excision repair enzymes in the wheat aleurone and their activation in cells undergoing programmed cell death, Plant Physiol Biochem, 49:1155-1164.
7 Bissenbaev AK, Altybaeva NA, Kolbaeva GA (2007) Role of reactive oxygen species and antioxidant enzymes in hormone regulating programmed cell death of wheat aleurone layer, Journal of Cell and Molecular Biology, 6(1): 41-48.
8 Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction, Annu Rev Plant Biol, 55:373-399.
9 Mehlhorn H, Tabner BJ, Wellburn AR (1990) Electron-spin-resonance evidence for the formation of free-radicals in plants exposed to ozone, Physiol Plant, 79: 377-383.
10 Landry LG, Chapple CC, Last RL (1995) Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced ultraviolet-B injury and oxidative damage, Plant Physiol, 109:1159-1166.
11 Ward JF (1988) DNA damage produced by ionizing radiation in mammalian cells: identities, mechanisms of formation, and reparability, Prog Nucleic Acid Res Mol Biol, 35: 95-125.
12 Hutchinson F (1957) The distance that a radical formed by ionizing radiation candiffuse in a yeast cell, Radiat Res, 7: 473-483.
13 Conklin PL, Williams EH, Last RL (1996) Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant, Proc Natl Acad Sci U S A, 93: 9970-9974.
14 Dizdaroglu M (1993) Chemistry of free radical damage to DNA and nucleoproteins, in: B Halliwell, OI Aruoma (Eds.). DNA and Free Radicals. Ellis Horwood, London. - P.19
15 Furlong EA, Jorgenson TJ, Henner WD (1986) Production of dihydrothymine stereoisomers in DNA by gamma-radiation, Biochemistry, 25: 4344-4349.
16 Teoule R (1987) Radiation-induced DNA damage and its repair, Int J Radiat Biol, 51: 589.
17 Dizdaroglu M (1985) Formation of an 8-hydroxyguanine moiety in deoxyribonucleic acid on gamma-irradiation in aqueous solution, Biochemistry, 24: 4476- 4481.
18 Fuciarelli AF, Wegher BJ, Blakely WF, Dizdaroglu M (1990) Yields of radiationinduced base products in DNA: effects of DNA conformation and gassing conditions, Int J Radiat Biol, 58: 397-415.
19 Fink SP, Reddy GR, Marnett LJ (1997) Mutagenicity in Escherichia coli of the major DNA adduct derived from the endogenous mutagen malondialdehyde, Proc Natl Acad Sci U S A, 94: 8652-8657.
20 Saparbaev M, Laval J (1998) 3,N4-ethenocytosine, a highly mutagenic adduct, is a primary substrate for Escherichia coli double-stranded uracil-DNA glycosylase and human mismatch-specific thymine-DNA glycosylase, Proc Natl Acad Sci U.S.A., 95: 8508-8513.
21 Ide H, Kow YW, Wallace SS (1985) Thymine glycols and urea residues in M13 DNA constitute replicative blocks in vitro, Nucleic Acids Res, 13: 8032-8052.
22 Evans J, Maccabee M, Hatahet Z, Courcelle J, Bockrath R, Ide H, Wallace S (1993) Thymine ring saturation and fragmentation products: lesion bypass, misinsertion and implications for mutagenesis, Mutat Res, 299: 147-156.
23 Boorstein RJ, Hilbert TP, Cadet J, Cunningham RP, Teebor GW (1989) UV-induced pyrimidine hydrates in DNA are repaired by bacterial and mammalian DNA glycosylase activities, Biochemistry, 28: 6164-6170.
24 Roldan-Arjona T, Garcia-Ortiz MV, Ruiz-Rubio M, Ariza RR (2000) cDNA cloning, expression and functional characterization of an Arabidopsis thaliana homologue of the Escherichia coli DNA repair enzyme endonuclease III, Plant Mol Biol, 44: 43-52.
25 Krokan HE, Standal R, Slupphaug G (1997) DNA glycosylases in the base excision repair of DNA, Biochem J, 325: 1-16.
26 Girard PM, Boiteux S (1997) Repair of oxidized DNA bases in the yeast Saccharomyces cerevisiae, Biochimie, 79:559-566.
27 Denver DR, Swenson SL, Lynch M (2003) An evolutionary analysis of the helix-hairpin-helix superfamily of DNA repair glycosylases, Mol Biol Evol, 20: 1603-1611.
28 Alseth I, Eide L, Pirovano M, Rognes T, Seeberg E, Bjoras M (1999) The Saccharomyces cerevisiae homologues of endonuclease III from Escherichia coli, Ntg1 and Ntg2, are both required for efficient repair of spontaneous and induced oxidative DNA damage in yeast, Mol Cell Biol, 19: 3779-3787.
29 Jiang D, Hatahet Z, Blaisdell JO, Melamede RJ, Wallace SS (1997) Escherichia coli endonuclease VIII: cloning, sequencing, and overexpression of the nei structural gene and characterization of nei and nei nth mutants, J Bacteriol, 179: 3773-3782.
30 Grin IR, Zharkov DO (2011) Eukaryotic homologs of endonuclease VIII: new elements of excision repair of DNA base [Biohimya]. 76(1):99 – 114.
31 Tchou J, Kasai H, Shibutani S, Chung MH, Laval J, Grollman AP, Nishimura S (1991) 8-Oxoguanine (8-hydroxyguanine) DNA glycosylase and its substrate specificity, Proc. Natl. Acad. Sci. U S A, 88:4690-4694.
32 Eisen JA, Hanawalt PC (1999) A phylogenomic study of DNA repair genes, proteins, and processes, Mutat Res, 435:171-213.
33 van der Kemp PA, Thomas D, Barbey R, de Oliveira R, Boiteux S (1996) Cloning and expression in Escherichia coli of the OGG1 gene of Saccharomyces cerevisiae, which codes for a DNA glycosylase that excises 7,8-dihydro-8-oxoguanine and 2,6-diamino-4-hydroxy-5-N-methylformamidopyrimidine, Proc Natl Acad Sci U S A, 93: 5197-5202.
34 Roldan-Arjona T, Wei YF, Carter KC, Klungland A, Anselmino C, Wang RP, Augustus M, Lindahl T (1997) Molecular cloning and functional expression of a human cDNA encoding the antimutator enzyme 8-hydroxyguanine-DNA glycosylase, Proc Natl Acad Sci U S A, 94:8016-8020.
35 Ohtsubo T, Matsuda O, Iba K, Terashima I, Sekiguchi M, Nakabeppu Y (1998) Molecular cloning of AtMMH, an Arabidopsis thaliana ortholog of the Escherichia coli mutM gene, and analysis of functional domains of its product, Mol Gen Genet, 259:577-590.
36 Dany AL, Tissier A (2001) A functional OGG1 homologue from Arabidopsis thaliana, Mol Genet Genom, 265: 293-301.
37 Garcia-Ortiz MV, Ariza RR, Roldan-Arjona T (2001) An OGG1 orthologue encoding a functional 8-oxoguanine DNA glycosylase/lyase in Arabidopsis thaliana, Plant Mol Biol, 47: 795-804.
38 Scortecci KC, Lima AF, Carvalho FM, Silva UB, Agnez-Lima LF, Batistuzzo de Medeiros SR (2007) A characterization of a MutM/Fpg ortholog in sugarcane—a monocot plant, Biochem Biophys Res Commun, 361: 1054-1060.
39 Morales-Ruiz T, Birincioglu M, Jaruga P, Rodriguez H, Roldan-Arjona T, Dizdaroglu M (2003) Arabidopsis thaliana Ogg1 protein excises 8-hydroxyguanine and 2,6-diamino-4-hydroxy-5-formamidopyrimidine from oxidatively damaged DNA containing multiple lesions, Biochemistry, 42: 3089-3095.
40 Murphy TM (2005) What is base excision repair good for? knockout mutants for FPG and OGG glycosylase genes in Arabidopsis, Physiol Plant, 123: 227-232.
41 Leprince O, Atherton NM, Deltour R, Hendry G (1994) The involvement of respiration in free radical processes during loss of desiccation tolerance in germinating Zea mays L, Plant Physiol, 104: 1333-1339.
42 Reuzeau C, Cavalie G (1995) Activities of free-radical processing enzymes in dry sunflower Seeds, New Phytol, 130: 59-66.
43 Bird AP (1980) DNA methylation and the frequency of CpG in animal DNA, Nucleic Acids Res, 8: 1499-1504.
44 Hendrich B, Hardeland U, Ng HH, Jiricny J, Bird A (1999) The thymine glycosylase MBD4 can bind to the product of deamination at methylated CpG sites, Nature, 401: 301–304.
45 Petronzelli F, Riccio A, Markham GD, Seeholzer SH, Genuardi M, Karbowski M, Yeung AT, Matsumoto Y and Bellacosa A (2000) Investigation of the substrate spectrum of the human mismatch-specific DNA N-glycosylase MED1 (MBD4): fundamental role of the catalytic domain, J Cell Physiol, 185: 473–480.
46 Nota F, Cambiagno DA, Ribone P, Alvarez ME (2015) Expression and function of AtMBD4L, the single gene encoding the nuclear DNA glycosylase MBD4L in Arabidopsis, Plant Sci, 235:122-129.
47 He XJ, Chen T, Zhu JK (2011) Regulation and function of DNA methylation in plants and animals, Cell Res, 21: 442–465.
48 Zhu JK (2009) Active DNA demethylation mediated by DNA glycosylases, Annu Rev Genet, 43: 143–166.
49 Chou KM, Cheng YC (2002) An exonucleolytic activity of human apurinic/apyrimidinic endonuclease on 3' mispaired DNA, Nature, 415: 655-659.
50 Babiychuk E, Kushnir S, Van Montagu M, Inze D (1994) The Arabidopsis thaliana apurinic endonuclease Arp reduces human transcription factors Fos and Jun, Proc Natl Acad Sci U S A, 91:3299-3303.
51 Murphy TM, Belmonte M, Shu S, Britt AB, Hatteroth J (2009) Requirement for abasic endonuclease gene homologues in Arabidopsis seed development, PLoS One, 4: e4297.
52 Joldybayeva B, Prorok P, Grin IR, Zharkov DO, Ishenko AA, et al. (2014) Cloning and Characterization of a Wheat Homologue of Apurinic/Apyrimidinic Endonuclease Ape1L // PLoS ONE, 9(3): e92963, doi:10.1371/journal.pone.0092963.
53 Wiederhold L, Leppard JB, Kedar P, Karimi-Busheri F, Rasouli-Nia A, Weinfeld M, Tomkinson AE, Izumi T, Prasad R, Wilson SH, Mitra S, Hazra TK (2004) AP endonuclease-independent DNA base excision repair in human cells, Mol Cell, 15: 209-220.
54 Whitehouse CJ, Taylor RM, Thistlethwaite A, Zhang H, Karimi-Busheri F, Lasko DD, Weinfeld M, Caldecott KW (2001) XRCC1 stimulates human polynucleotide kinase activity at damaged DNA termini and accelerates DNA single-strand break repair, Cell, 104: 107-117.
55 55 Betti M, Petrucco S, Bolchi A, Dieci G, Ottonello S (2001) A plant 30-phosphoesterase involved in the repair of DNA strand breaks generated by oxidative damage, J Biol Chem, 276: 18038-18045.
56 Petrucco S, Volpi G, Bolchi A, Rivetti C, Ottonello S (2002) A nick-sensing DNA 30- repair enzyme from Arabidopsis, J Biol Chem, 277: 23675-23683.
57 Martinez-Macias MI, Qian W, Miki D, Pontes O, Liu Y, et al. (2012) A DNA 3' -phosphatase functions in active DNA demethylation in Arabidopsis, Mol Cell, 45: 357–370.
58 Garcia-Diaz M, Dominguez O, Lopez-Fernandez LA, de Lera LT, Saniger ML, Ruiz JF, Parraga M, Garcia-Ortiz MJ, Kirchhoff T, del Mazo J, Bernad A, Blanco L (2000) DNA polymerase lambda (Pol lambda), a novel eukaryotic DNA polymerase with a potential role in meiosis, J Mol Biol, 301: 851-867.
59 Uchiyama Y, Kimura S, Yamamoto T, Ishibashi T, Sakaguchi K (2004) Plant DNA polymerase lambda, a DNA repair enzyme that functions in plant meristematic and meiotic tissues, Eur J Biochem, 271: 2799-2807.
60 Mori Y, Kimura S, Saotome A, Kasai N, Sakaguchi N, Uchiyama Y, Ishibashi T, Yamamoto T, Chiku H, Sakaguchi K (2005) Plastid DNA polymerases from higher plants, Arabidopsis thaliana, Biochem Biophys Res Commun, 334: 43-50.
61 Takeuchi R, Kimura S, Saotome A, Sakaguchi K (2007) Biochemical properties of a plastidial DNA polymerase of rice, Plant Mol Biol, 64: 601-611.
62 Vidal AE, Boiteux S, Hickson ID, Radicella JP (2001) XRCC1 coordinates the initial and late stages of DNA abasic site repair through protein-protein interactions, EMBO J, 20: 6530-6539.
63 Taylor RM, Thistlethwaite A, Caldecott KW (2002) Central role for the XRCC1 BRCT I domain in mammalian DNA single-strand break repair, Mol Cell Biol, 22: 2556-2563.
64 Taylor RM, Hamer MJ, Rosamond J, Bray CM (1998) Molecular cloning and functional analysis of the Arabidopsis thaliana DNA ligase I homologue, Plant J, 14: 75-81.
65 Wu YQ, Hohn B, Ziemienowic A (2001) Characterization of an ATP-dependent type I DNA ligase from Arabidopsis thaliana, Plant Mol Biol, 46: 161-170.
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Bissenbaev, A. K. (2016). Base Excision Repair of Oxidative DNA lesions in plants. Experimental Biology, 66(1), 120–133. Retrieved from https://bb.kaznu.kz/index.php/biology/article/view/1167
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