Sensitivity of arabidopsis thaliana arp -/- mutants to genotoxic agents
DOI:
https://doi.org/10.26577/EB-2017-4-1305Keywords:
AP endonuclease, A.thaliana, DNA glycosylases, reactive oxygen species (ROS).Abstract
Apurinic/apyrimidinic (AP) endonucleases are important DNA repair enzymes involved in two overlapping pathways: DNA glycosylase-initiated base excision (BER) and AP endonuclease-initiated nucleotide incision repair (NIR). In the BER pathway, AP endonucleases cleave DNA at AP sites and 3'-blocking moieties generated by DNA glycosylases, whereas in NIR, the same AP endonucleases incise DNA 5' to a wide variety of oxidized bases. The flowering plant Arabidopsis thaliana contains three genes encoding homologues of major human AP endonuclease 1 (APE1): Arp, Ape1L and Ape2. ARP is a major plant AP endonuclease that removes abasic sites. However, it was not known whether the plant AP endonucleases contain the NIR activity. Here, we report that homozygous A. thaliana arp–/– mutant exhibited high sensitivity to methyl methanesulfonate and tert-butyl hydroperoxide, but not to H2O2, suggesting that ARP-catalyzed NIR activity is required to repair AP sites generated by exogenous factors and specific oxidative DNA lesions induced by t-BuO 2H in vivo. Extracts from arp–/– mutants, but not ape1L and ape2 mutants, exhibited no or very low NIR activity on the αdA•T. These results strongly suggest that ARP is a major AP site cleavage and NIR endonuclease in A. thaliana.
References
1 Cadet J., Douki T., Gasparutto D., Ravanat J.L. Oxidative damage to DNA: formation, measurement and biochemical features // Mutat. Res. – 2003. – Vol. 531. – P. 5-23.
2 Krokan H.E., Bjoras M. Base excision repair // Cold Spring Harb. Perspect. Biol. – 2013. – Vol. 5. – P. a012583.
3 Ischenko A.A., Saparbaev M.K. Alternative nucleotide incision repair pathway for oxidative DNA damage // Nature. – 2002. – Vol. 415. – P. 183-187.
4 Hitomi K., Iwai S., Tainer J.A. The intricate structural chemistry of base excision repair machinery: implications for DNA damage recognition, removal, and repair // DNA Repair (Amst). – 2007. - Vol. 6. – P. 410-428.
5 Gros L., Ishchenko A.A., Ide H., Elder R.H., Saparbaev M.K. The major human AP endonuclease (Ape1) is involved in the nucleotide incision repair pathway // Nucleic Acids Res. – 2004. – Vol. 32. - P. 73-81.
6 Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., Ellenberger T. DNA repair and mutagenesis // ASM Press. – 2006.
7 Vanyushin B.F., Ashapkin V.V. DNA methylation in higher plants: past, present and future // Biochim Biophys Acta. – 2011. – Vol. 1809. – P. 360-368.
8 He X.J., Chen T., Zhu J.K. Regulation and function of DNA methylation in plants and animals // Cell Res. – 2011. – Vol. 21. – P. 442-465.
9 Zhu J.K. Active DNA demethylation mediated by DNA glycosylases // Annu. Rev. Genet. – 2009. – Vol. 43. – P. 143-166.
10 Morales-Ruiz T., Ortega-Galisteo A.P., Ponferrada-Marin M.I., Martinez-Macias M.I., Ariza R.R., Roldan-Arjona T. Demeter and repressor of silencing 1 encode 5-methylcytosine DNA glycosylases // Proc. Natl. Acad. Sci. U.S.A. – 2006. – Vol. 103. - P. 6853-6858.
11 Babiychuk E., Kushnir S., Van Montagu M., Inze D. The Arabidopsis thaliana apurinic endonuclease Arp reduces human transcription factors Fos and Jun // Proc. Natl. Acad. Sci. U. S. A. – 1994. – Vol. 91. – P. 3299-3303.
12 Cordoba-Canero D., Roldan-Arjona T., Ariza R.R. Arabidopsis ARP endonuclease functions in a branched base excision DNA repair pathway completed by LIG1 // Plant J. – 2011. – Vol. 68. – P. 693-702.
13 Joldybayeva B., Prorok P., Grin I.R., Zharkov D.O., Ishenko A.A., Tudek B., Bissenbaev A.K., Saparbaev M. Cloning and Characterization of a Wheat Homologue of Apurinic/Apyrimidinic Endonuclease Ape1L // PLoS One. – 2014. – Vol. 9. – P. e92963.
14 Bissenbaev A.K., Ishchenko A.A., Taipakova S.M., Saparbaev M.K. Presence of base excision repair enzymes in the wheat aleurone and their activation in cells undergoing programmed cell death // Plant Physiol. Biochem. – 2011. – Vol. 49. - P. 1155-1164.
15 Ishchenko A.A., Deprez E., Maksimenko A., Brochon J.C., Tauc P., Saparbaev M.K. Uncoupling of the base excision and nucleotide incision repair pathways reveals their respective biological roles // Proc. Natl. Acad. Sci. U. S. A. – 2006. - Vol. 103. P. 2564-2569.
16 Baker M.A., He S.Q. Elaboration of cellular DNA breaks by hydroperoxides // Free Radic Biol Med. – 1991. - Vol. 11. – P. 563-572.
17 Gros L., Ishchenko A.A., Saparbaev M. Enzymology of repair of etheno-adducts // Mutat. Res. – 2003. – Vol. 531. – P. 219-229.
18 Hix S., Morais Mda S., Augusto O. DNA methylation by tert-butyl hydroperoxide-iron (II) // Free Radic Biol Med. – 1995. – Vol. 19. – P. 293-301.
19 Hix S., Kadiiska M.B., Mason R.P., Augusto O. In vivo metabolism of tert-butyl hydroperoxide to methyl radicals. EPR spin trapping and DNA methylation studies // Chem Res Toxicol. – 2000. – Vol. 13. – P. 1056-1054.
20 Gasparutto D., Dherin C., Boiteux S., Cadet J. Excision of 8-methylguanine site-specifically incorporated into oligonucleotide substrates by the AlkA protein of Escherichia coli // DNA Repair (Amst). – 2002. - Vol. 1. P. 437-447.
21 Bradford M. M. A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding // Anal. Biochem. – 1976. – Vol. 72. – P. 248-254.
22 Murphy T.M., Belmonte M., Shu S., Britt A.B., Hatteroth J. Requirement for abasic endonuclease gene homologues in Arabidopsis seed development // PLoS One. – 2009. – Vol. 4. – P. e4297.
23 Foyer C.H., Noctor G. Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria // Physiol. Plant. – 2003. – Vol. 119. – P. 355–364.
24 Jaruga P., Dizdaroglu M. 8,5'-Cyclopurine-2'-deoxynucleosides in DNA: mechanisms of formation, measurement, repair and biological effects // DNA Repair (Amst). – 2008. – Vol. 7. – P. 1413-1425.
25 Brooks P.J. The 8,5'-cyclopurine-2'-deoxynucleosides: candidate neurodegenerative DNA lesions in xeroderma pigmentosum, and unique probes of transcription and nucleotide excision repair // DNA Repair (Amst). – 2008. – Vol. 7. – P. 1168-1179.
References
1 Cadet J., Douki T., Gasparutto D., Ravanat J.L. (2003) Oxidative damage to DNA: formation, measurement and biochemical features. Mutat. Res., vol. 531, pp. 5-23.
2 Krokan H.E., Bjoras M. (2013) Base excision repair. Cold Spring Harb. Perspect. Biol., vol. 5, pp. a012583.
3 Ischenko A.A., Saparbaev M.K. (2002) Alternative nucleotide incision repair pathway for oxidative DNA damage. Nature, vol. 415, pp. 183-87.
4 Hitomi K., Iwai S., Tainer J.A. (2007) The intricate structural chemistry of base excision repair machinery: implications for DNA damage recognition, removal, and repair. DNA Repair (Amst), vol. 6, pp. 410-28.
5 Gros L., Ishchenko A.A., Ide H., Elder R.H., Saparbaev M.K. (2004) The major human AP endonuclease (Ape1) is involved in the nucleotide incision repair pathway. Nucleic Acids Res., vol. 32, pp. 73-81.
6 Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., Ellenberger T. (2006) DNA repair and mutagenesis. ASM Press.
7 Vanyushin B.F., Ashapkin V.V. (2011) DNA methylation in higher plants: past, present and future. Biochim Biophys Acta., vol. 1809, pp. 360-68.
8 He X.J., Chen T., Zhu J.K. (2011) Regulation and function of DNA methylation in plants and animals. Cell Res., vol. 21, pp. 442-65.
9 Zhu J.K. (2009) Active DNA demethylation mediated by DNA glycosylases. Annu. Rev. Genet., vol. 43, pp. 143-66.
10 Morales-Ruiz T., Ortega-Galisteo A.P., Ponferrada-Marin M.I., Martinez-Macias M.I., Ariza R.R., Roldan-Arjona T. (2006) Demeter and repressor of silencing 1 encode 5-methylcytosine DNA glycosylases. Proc. Natl. Acad. Sci. U.S.A., vol. 103, pp. 6853-58.
11 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., vol. 91, pp. 3299-303.
12 Cordoba-Canero D., Roldan-Arjona T., Ariza R.R. (2011) Arabidopsis ARP endonuclease functions in a branched base excision DNA repair pathway completed by LIG1. Plant J., vol. 68, pp. 693-702.
13 Joldybayeva B., Prorok P., Grin I.R., Zharkov D.O., Ishenko A.A., Tudek B., Bissenbaev A.K., Saparbaev M. (2014) Cloning and Characterization of a Wheat Homologue of Apurinic/Apyrimidinic Endonuclease Ape1L. PLoS One, vol. 9, pp. e92963.
14 Bissenbaev A.K., Ishchenko A.A., Taipakova S.M., Saparbaev M.K. (2011) Presence of base excision repair enzymes in the wheat aleurone and their activation in cells undergoing programmed cell death. Plant Physiol. Biochem., vol. 49, pp. 1155-64.
15 Ishchenko A.A., Deprez E., Maksimenko A., Brochon J.C., Tauc P., Saparbaev M.K. (2006) Uncoupling of the base excision and nucleotide incision repair pathways reveals their respective biological roles. Proc. Natl. Acad. Sci. U. S. A., vol. 103, pp. 2564-69.
16 Baker M.A., He S.Q. (1991) Elaboration of cellular DNA breaks by hydroperoxides. Free Radic Biol Med., vol. 11, pp. 563-72.
17 Gros L., Ishchenko A.A., Saparbaev M. (2003) Enzymology of repair of etheno-adducts. Mutat. Res. vol. 531, pp. 219-29.
18 Hix S., Morais Mda S., Augusto O. (1995) DNA methylation by tert-butyl hydroperoxide-iron (II). Free Radic Biol Med. vol. 19, pp. 293-301.
19 Hix S., Kadiiska M.B., Mason R.P., Augusto O. (2000) In vivo metabolism of tert-butyl hydroperoxide to methyl radicals. EPR spin trapping and DNA methylation studies. Chem Res Toxicol., vol. 13, pp. 1056-54.
20 Gasparutto D., Dherin C., Boiteux S., Cadet J. (2002) Excision of 8-methylguanine site-specifically incorporated into oligonucleotide substrates by the AlkA protein of Escherichia coli. DNA Repair (Amst), vol. 1, pp. 437-47.
21 Bradford M. M. (1976) A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding. Anal. Biochem., vol. 72, pp. 248-54.
22 Murphy T.M., Belmonte M., Shu S., Britt A.B., Hatteroth J. (2009) Requirement for abasic endonuclease gene homologues in Arabidopsis seed development. PLoS One, vol. 4, pp. e4297.
23 Foyer C.H., Noctor G. (2003) Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol. Plant, vol. 119, pp. 355–64.
24 Jaruga P., Dizdaroglu M. (2008) 8,5'-Cyclopurine-2'-deoxynucleosides in DNA: mechanisms of formation, measurement, repair and biological effects. DNA Repair (Amst), vol. 7, pp. 1413-25.
25 Brooks P.J. (2008) The 8,5'-cyclopurine-2'-deoxynucleosides: candidate neurodegenerative DNA lesions in xeroderma pigmentosum, and unique probes of transcription and nucleotide excision repair. DNA Repair (Amst), vol. 7, pp. 1168-79.
2 Krokan H.E., Bjoras M. Base excision repair // Cold Spring Harb. Perspect. Biol. – 2013. – Vol. 5. – P. a012583.
3 Ischenko A.A., Saparbaev M.K. Alternative nucleotide incision repair pathway for oxidative DNA damage // Nature. – 2002. – Vol. 415. – P. 183-187.
4 Hitomi K., Iwai S., Tainer J.A. The intricate structural chemistry of base excision repair machinery: implications for DNA damage recognition, removal, and repair // DNA Repair (Amst). – 2007. - Vol. 6. – P. 410-428.
5 Gros L., Ishchenko A.A., Ide H., Elder R.H., Saparbaev M.K. The major human AP endonuclease (Ape1) is involved in the nucleotide incision repair pathway // Nucleic Acids Res. – 2004. – Vol. 32. - P. 73-81.
6 Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., Ellenberger T. DNA repair and mutagenesis // ASM Press. – 2006.
7 Vanyushin B.F., Ashapkin V.V. DNA methylation in higher plants: past, present and future // Biochim Biophys Acta. – 2011. – Vol. 1809. – P. 360-368.
8 He X.J., Chen T., Zhu J.K. Regulation and function of DNA methylation in plants and animals // Cell Res. – 2011. – Vol. 21. – P. 442-465.
9 Zhu J.K. Active DNA demethylation mediated by DNA glycosylases // Annu. Rev. Genet. – 2009. – Vol. 43. – P. 143-166.
10 Morales-Ruiz T., Ortega-Galisteo A.P., Ponferrada-Marin M.I., Martinez-Macias M.I., Ariza R.R., Roldan-Arjona T. Demeter and repressor of silencing 1 encode 5-methylcytosine DNA glycosylases // Proc. Natl. Acad. Sci. U.S.A. – 2006. – Vol. 103. - P. 6853-6858.
11 Babiychuk E., Kushnir S., Van Montagu M., Inze D. The Arabidopsis thaliana apurinic endonuclease Arp reduces human transcription factors Fos and Jun // Proc. Natl. Acad. Sci. U. S. A. – 1994. – Vol. 91. – P. 3299-3303.
12 Cordoba-Canero D., Roldan-Arjona T., Ariza R.R. Arabidopsis ARP endonuclease functions in a branched base excision DNA repair pathway completed by LIG1 // Plant J. – 2011. – Vol. 68. – P. 693-702.
13 Joldybayeva B., Prorok P., Grin I.R., Zharkov D.O., Ishenko A.A., Tudek B., Bissenbaev A.K., Saparbaev M. Cloning and Characterization of a Wheat Homologue of Apurinic/Apyrimidinic Endonuclease Ape1L // PLoS One. – 2014. – Vol. 9. – P. e92963.
14 Bissenbaev A.K., Ishchenko A.A., Taipakova S.M., Saparbaev M.K. Presence of base excision repair enzymes in the wheat aleurone and their activation in cells undergoing programmed cell death // Plant Physiol. Biochem. – 2011. – Vol. 49. - P. 1155-1164.
15 Ishchenko A.A., Deprez E., Maksimenko A., Brochon J.C., Tauc P., Saparbaev M.K. Uncoupling of the base excision and nucleotide incision repair pathways reveals their respective biological roles // Proc. Natl. Acad. Sci. U. S. A. – 2006. - Vol. 103. P. 2564-2569.
16 Baker M.A., He S.Q. Elaboration of cellular DNA breaks by hydroperoxides // Free Radic Biol Med. – 1991. - Vol. 11. – P. 563-572.
17 Gros L., Ishchenko A.A., Saparbaev M. Enzymology of repair of etheno-adducts // Mutat. Res. – 2003. – Vol. 531. – P. 219-229.
18 Hix S., Morais Mda S., Augusto O. DNA methylation by tert-butyl hydroperoxide-iron (II) // Free Radic Biol Med. – 1995. – Vol. 19. – P. 293-301.
19 Hix S., Kadiiska M.B., Mason R.P., Augusto O. In vivo metabolism of tert-butyl hydroperoxide to methyl radicals. EPR spin trapping and DNA methylation studies // Chem Res Toxicol. – 2000. – Vol. 13. – P. 1056-1054.
20 Gasparutto D., Dherin C., Boiteux S., Cadet J. Excision of 8-methylguanine site-specifically incorporated into oligonucleotide substrates by the AlkA protein of Escherichia coli // DNA Repair (Amst). – 2002. - Vol. 1. P. 437-447.
21 Bradford M. M. A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding // Anal. Biochem. – 1976. – Vol. 72. – P. 248-254.
22 Murphy T.M., Belmonte M., Shu S., Britt A.B., Hatteroth J. Requirement for abasic endonuclease gene homologues in Arabidopsis seed development // PLoS One. – 2009. – Vol. 4. – P. e4297.
23 Foyer C.H., Noctor G. Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria // Physiol. Plant. – 2003. – Vol. 119. – P. 355–364.
24 Jaruga P., Dizdaroglu M. 8,5'-Cyclopurine-2'-deoxynucleosides in DNA: mechanisms of formation, measurement, repair and biological effects // DNA Repair (Amst). – 2008. – Vol. 7. – P. 1413-1425.
25 Brooks P.J. The 8,5'-cyclopurine-2'-deoxynucleosides: candidate neurodegenerative DNA lesions in xeroderma pigmentosum, and unique probes of transcription and nucleotide excision repair // DNA Repair (Amst). – 2008. – Vol. 7. – P. 1168-1179.
References
1 Cadet J., Douki T., Gasparutto D., Ravanat J.L. (2003) Oxidative damage to DNA: formation, measurement and biochemical features. Mutat. Res., vol. 531, pp. 5-23.
2 Krokan H.E., Bjoras M. (2013) Base excision repair. Cold Spring Harb. Perspect. Biol., vol. 5, pp. a012583.
3 Ischenko A.A., Saparbaev M.K. (2002) Alternative nucleotide incision repair pathway for oxidative DNA damage. Nature, vol. 415, pp. 183-87.
4 Hitomi K., Iwai S., Tainer J.A. (2007) The intricate structural chemistry of base excision repair machinery: implications for DNA damage recognition, removal, and repair. DNA Repair (Amst), vol. 6, pp. 410-28.
5 Gros L., Ishchenko A.A., Ide H., Elder R.H., Saparbaev M.K. (2004) The major human AP endonuclease (Ape1) is involved in the nucleotide incision repair pathway. Nucleic Acids Res., vol. 32, pp. 73-81.
6 Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., Ellenberger T. (2006) DNA repair and mutagenesis. ASM Press.
7 Vanyushin B.F., Ashapkin V.V. (2011) DNA methylation in higher plants: past, present and future. Biochim Biophys Acta., vol. 1809, pp. 360-68.
8 He X.J., Chen T., Zhu J.K. (2011) Regulation and function of DNA methylation in plants and animals. Cell Res., vol. 21, pp. 442-65.
9 Zhu J.K. (2009) Active DNA demethylation mediated by DNA glycosylases. Annu. Rev. Genet., vol. 43, pp. 143-66.
10 Morales-Ruiz T., Ortega-Galisteo A.P., Ponferrada-Marin M.I., Martinez-Macias M.I., Ariza R.R., Roldan-Arjona T. (2006) Demeter and repressor of silencing 1 encode 5-methylcytosine DNA glycosylases. Proc. Natl. Acad. Sci. U.S.A., vol. 103, pp. 6853-58.
11 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., vol. 91, pp. 3299-303.
12 Cordoba-Canero D., Roldan-Arjona T., Ariza R.R. (2011) Arabidopsis ARP endonuclease functions in a branched base excision DNA repair pathway completed by LIG1. Plant J., vol. 68, pp. 693-702.
13 Joldybayeva B., Prorok P., Grin I.R., Zharkov D.O., Ishenko A.A., Tudek B., Bissenbaev A.K., Saparbaev M. (2014) Cloning and Characterization of a Wheat Homologue of Apurinic/Apyrimidinic Endonuclease Ape1L. PLoS One, vol. 9, pp. e92963.
14 Bissenbaev A.K., Ishchenko A.A., Taipakova S.M., Saparbaev M.K. (2011) Presence of base excision repair enzymes in the wheat aleurone and their activation in cells undergoing programmed cell death. Plant Physiol. Biochem., vol. 49, pp. 1155-64.
15 Ishchenko A.A., Deprez E., Maksimenko A., Brochon J.C., Tauc P., Saparbaev M.K. (2006) Uncoupling of the base excision and nucleotide incision repair pathways reveals their respective biological roles. Proc. Natl. Acad. Sci. U. S. A., vol. 103, pp. 2564-69.
16 Baker M.A., He S.Q. (1991) Elaboration of cellular DNA breaks by hydroperoxides. Free Radic Biol Med., vol. 11, pp. 563-72.
17 Gros L., Ishchenko A.A., Saparbaev M. (2003) Enzymology of repair of etheno-adducts. Mutat. Res. vol. 531, pp. 219-29.
18 Hix S., Morais Mda S., Augusto O. (1995) DNA methylation by tert-butyl hydroperoxide-iron (II). Free Radic Biol Med. vol. 19, pp. 293-301.
19 Hix S., Kadiiska M.B., Mason R.P., Augusto O. (2000) In vivo metabolism of tert-butyl hydroperoxide to methyl radicals. EPR spin trapping and DNA methylation studies. Chem Res Toxicol., vol. 13, pp. 1056-54.
20 Gasparutto D., Dherin C., Boiteux S., Cadet J. (2002) Excision of 8-methylguanine site-specifically incorporated into oligonucleotide substrates by the AlkA protein of Escherichia coli. DNA Repair (Amst), vol. 1, pp. 437-47.
21 Bradford M. M. (1976) A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding. Anal. Biochem., vol. 72, pp. 248-54.
22 Murphy T.M., Belmonte M., Shu S., Britt A.B., Hatteroth J. (2009) Requirement for abasic endonuclease gene homologues in Arabidopsis seed development. PLoS One, vol. 4, pp. e4297.
23 Foyer C.H., Noctor G. (2003) Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol. Plant, vol. 119, pp. 355–64.
24 Jaruga P., Dizdaroglu M. (2008) 8,5'-Cyclopurine-2'-deoxynucleosides in DNA: mechanisms of formation, measurement, repair and biological effects. DNA Repair (Amst), vol. 7, pp. 1413-25.
25 Brooks P.J. (2008) The 8,5'-cyclopurine-2'-deoxynucleosides: candidate neurodegenerative DNA lesions in xeroderma pigmentosum, and unique probes of transcription and nucleotide excision repair. DNA Repair (Amst), vol. 7, pp. 1168-79.
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2018-05-26
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