Isolation and characterization of Arabidopsis thaliana poly(ADP-ribose) polymerase 2 cDNA
DOI:
https://doi.org/10.26577/eb-2018-1-1319Abstract
Poly(ADP-ribose) polymerases (PARPs) catalyse the synthesis of polymers of ADP-ribose (PAR) covalently attached to acceptor proteins using nicotinamide adenine dinucleotide (NAD+) as a substrate. The genome of Arabidopsis thaliana, a widely used model plant organism, encodes at least three putative PARPs: AtPARP1 (At4g02390), AtPARP2 (At2g31320) and AtPARP3 (At5g22470). There is evidence that plant PARPs are structurally homologous to mammalian PARP proteins. The high degree of conservation at the amino acid level between Arabidopsis and mammalian forms of these enzymes suggests that PARP function is conserved between plants and animals. Plant PARPs also have enzymatic activities that are functionally homologous to mammalian PARPs. In contrast to mammalian systems, surprisingly very little is known about PARPs-catalyzed PARylation in plants.
Here, we isolated the AtPARP2 cDNA gene encoding the Arabidopsis thaliana Poly(ADP-ribose) polymerase 2 using the reverse transcription - polymerase chain reaction (RT-PCR). AtPARP2 with a 6xHis end was functionally expressed in E. coli and purified by nickel affinity chromatography. Amino acid sequencing of the putative recombinant protein by MALDI-TOF MS and its analysis using NCBI BLAST indicated that the enzyme belongs to poly (ADP-ribose) polymerases family. It was revealed that the product of gene expression is a globular protein with a mass of 72 kDa, consisting of 637 amino acids (pI 5.92). Purified AtPARP2 was used as an immunogen to generate rabbit polyclonal anti- AtPARP2 antibodies. A specific AtPARP2 reaction using an oligonucleotide duplex containing a chain break to activate the poly ADP-ribosylation process in the presence of NAD showed the auto-poly-ADP-ribosylation activity of recombinant proteins.
Key words: Poly(ADP-ribose) polymerase, PARP2, poly-ADP-ribosylation, NAD+, reactive oxygen species, Arabidopsis thaliana.
References
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2 Foyer C.H., Noctor G. Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria // Physiol. Plant. - 2003. - Vol. 119. - P.355–364.
3 Weitzman M.D., Weitzman J.B. What's the damage? The impact of pathogens on pathways that maintain host genome integrity //Cell Host Microbe. -2014. -Vol.15. - №3. -P.283-294.
4 Papamichos-Chronakis M., Peterson C.L. Chromatin and the genome integrity network // Nat Rev Genet. - 2013. - Vol. 14. - № 1. - P.62–75.
5 Ermolaeva M.A., Schumacher B. Systemic DNA damage responses: organismal adaptations to genome instability // Trends Genet. - 2014. - Vol. 30. - № 3. - P.95–102.
6 Schreiber V., Dantzer F., Ame J.C., de Murcia G. Poly (ADP-ribose): novel functions for an old molecule // Nat. Rev. Mol. Cell. Biol. - 2006. - Vol 7. - P.517–528.
7 Kim M.Y., Zhang T., Kraus W.L. Poly(ADP-ribosyl)ation by PARP-1: ’PAR-laying’ NAD+ into a nuclear signal // Genes Dev. - 2005. - Vol. 19. - P.1951–1967.
8 Ame´ J-C., Spenlehauer C., de Murcia G. The PARP superfamily // BioEssays. - 2004. - Vol. 26. - P.882–893
9 Woodhouse B.C., Dianov G.L. Poly ADP-ribose polymerase-1: an international molecule of mystery // DNA Repair. - 2008. - Vol. 7. - P.1077–1086.
10 Kraus W.L., Hottiger M.O. PARP-1 and gene regulation: progress and puzzles // Mol. Aspects Med. - 2013. - Vol. 34. - P.1109–1123.
11 Caldecott K.W. Mammalian single-strand break repair: mechanisms and links with chromatin // DNA Repair. - 2007. - Vol. 6. - P.443–453.
12 Shieh W.M., Ame J.C., Wilson M.V., Wang Z.Q., Koh D.W., JacobsonM.K., Jacobson E.L. Poly(ADP-ribose) polymerase null mouse cells synthesize ADP-ribose polymers // J.Biol.Chem. - 1998. - Vol. 273. - P.30069–30072.
13 de Murcia G., Menissier de Murcia J. Poly(ADP-ribose)polymerase: a molecular nick-sensor // Trends Biochem. Sci. - 1994. - Vol. 19. - P.172–176.
14 Tanaka Y., Yoshihara K., Itaya A., Kamiya T., Koide S.S. Mechanism of the inhibition of Ca2+, Mg2+-dependentendonuclease of bull seminal plasma induced by ADP-ribosylation // J.Biol. Chem. - 1984. - Vol. 259. - P.6579–6585.
15 Satoh M.S., Poirier G.G. and Lindahl T. Dual function forpoly(ADP-ribose) synthesis in response to DNA strand breakage // Biochemistry. - 1994. - Vol. 33. - P.7099–7106.
16 Caldecott K.W. Protein ADP-ribosylation and the cellularresponse to DNA strand breaks // DNA Repair. - 2014. - Vol. 19. - P.108–113.
17 Briggs A.G., Bent A.F. Poly(ADP-ribosyl)ation in plants // Trends Plant Sci. - 2011. - Vol. 16. - № 7. - P.372–80.
18 Lamb R.S., Citarelli M., Teotia S. Functions of the poly(ADP-ribose) polymerase superfamily in plants // Cell Mol Life Sci. - 2012. - Vol. 69. - № 2. - P.175–89.
19 Briggs A.G., Bent A.F. Poly(ADP-ribosyl)ation in plants // Trends in Plant Science. - 2011. - Vol. 16. - № 7. - P.360-1385.
20 Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4 // Nature. – 1970. – Vol. 227. - № 5259. – P. 680-685.
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. 248-302.
22 Vainonen J.P., Shapiguzov A., Vaattovaara A., Kangasjärvi J. Plant PARPs, PARGs and PARP-like Proteins // Current Protein and Peptide Science. – 2016. – Vol. 17. - P.713-723
23 Hinz J.M., Rodriguez Y., Smerdon M.J. Rotational dynamics of DNA on the nucleosome surface markedly impact accessibility to a DNA repair enzyme // Proc. Natl. Acad. Sci. U.S.A. - 2010. - Vol. 107. - P.4646–4651.
24 Odell I.D., Barbour J.E., Murphy D.L., Della-Maria J.A., Sweasy J.B., Tomkinson A.E., Wallace S.S., Pederson D.S. Nucleosome disruption by DNA ligase III-XRCC1 promotes efficient base excision repair // Mol. Cell. Biol. - 2011. - Vol. 31. - P.4623–4632.
25 Zhang F., Wang Y., Wang L., Luo X., Huang K., Wang C., Du M., Liu F., Luo T., Huang D., Huang K. Poly(ADP-ribose) Polymerase 1 Is a Key Regulator of Estrogen Receptor α-dependent Gene Transcription // J. Biol. Chem. – 2013. - Vol. 288. - № 16. – P. 11348–11357.
References
1. Ame´ J-C., Spenlehauer C., de Murcia G. (2004) The PARP superfamily. BioEssays, vol. 26, pp. 882–893.
2. Briggs A.G, Bent A.F. (2011) Poly(ADP-ribosyl)ation in plants. Trends Plant Sci., vol. 16 (7), pp.372–80.
3. Briggs A.G., Bent A.F. (2011) Poly(ADP-ribosyl)ation in plants. Trends in Plant Science., vol. 16 (7), pp.360-1385.
4. 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.
5. 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.
6. Caldecott K.W. (2007) Mammalian single-strand break repair: mechanisms and links with chromatin. DNA Repair., vol. 6, pp.443–453.
7. Caldecott K.W. (2014) Protein ADP-ribosylation and the cellularresponse to DNA strand breaks. DNA Repair, vol. 19, pp.108–113.
8. de Murcia G., Menissier de Murcia J. (1994) Poly(ADP-ribose)polymerase: a molecular nick-sensor. Trends Biochem. Sci., vol. 19, pp.172–176.
9. Ermolaeva M.A., Schumacher B. (2014) Systemic DNA damage responses: organismal adaptations to genome instability. Trends Genet., vol. 30 (3), pp.95–102.
10. Foyer C.H., Noctor G. (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol. Plant, vol. 119, pp. 355–364.
11. Hinz J.M., Rodriguez Y., Smerdon M.J. (2010) Rotational dynamics of DNA on the nucleosome surface markedly impact accessibility to a DNA repair enzyme. Proc. Natl. Acad. Sci. U.S.A., vol. 107, pp.4646–4651.
12. Kim M.Y., Zhang T., Kraus W.L. (2005) Poly(ADP-ribosyl)ation by PARP-1: ’PAR-laying’ NAD+ into a nuclear signal. Genes Dev., vol. 19, pp.1951–1967.
13. Kraus W.L., Hottiger M.O. (2013) PARP-1 and gene regulation: progress and puzzles. Mol. Aspects Med., vol. 34, pp.1109–1123.
14. Laemmli U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, vol. 227 (5259), pp. 680-685.
15. Lamb R.S., Citarelli M., Teotia S. (2012) Functions of the poly(ADP-ribose) polymerase superfamily in plants. Cell Mol Life Sci., vol. 69 (2). - P.175–89.
16. Odell I.D., Barbour J.E., Murphy D.L., Della-Maria J.A., Sweasy J.B., Tomkinson A.E., Wallace S.S., Pederson D.S. (2011) Nucleosome disruption by DNA ligase III-XRCC1 promotes efficient base excision repair. Mol. Cell. Biol., vol. 31, pp.4623–4632.
17. Papamichos-Chronakis M., Peterson C.L. (2013) Chromatin and the genome integrity network. Nat Rev Genet., vol. 14 (1), pp.62–75.
18. Schreiber V., Dantzer F., Ame J.C., de Murcia,G. (2006) Poly(ADP-ribose): novel functions for an old molecule // Nat. Rev. Mol. Cell. Biol., vol 7, pp.517–528.
19. Shieh W.M., Ame J.C., Wilson M.V., Wang Z.Q., Koh D.W., JacobsonM.K., Jacobson E.L. (1998) Poly(ADP-ribose) polymerase null mouse cells synthesize ADP-ribose polymers. J.Biol.Chem., vol. 273, pp.30069–30072.
20. Satoh,M.S., Poirier,G.G. and Lindahl,T. (1994) Dual function forpoly(ADP-ribose) synthesis in response to DNA strand breakage. Biochemistry, vol. 33, pp.7099–7106.
21. Tanaka Y., Yoshihara K., Itaya A., Kamiya T., Koide S.S. (1984) Mechanism of the inhibition of Ca2+, Mg2+-dependentendonuclease of bull seminal plasma induced by ADP-ribosylation. J.Biol. Chem., vol. 259, pp.6579–6585.
22. Vainonen J.P., Shapiguzov A., Vaattovaara A., Kangasjärvi J. (2016) Plant PARPs, PARGs and PARP-like Proteins. Current Protein and Peptide Science., vol. 17, pp.713-723
23. Weitzman M.D, Weitzman J.B. (2014) What's the damage? The impact of pathogens on pathways that maintain host genome integrity. Cell Host Microbe, vol.15 (3), pp. 283-294.
24. Woodhouse B.C., Dianov G.L. (2008) Poly ADP-ribose polymerase-1: an international molecule of mystery. DNA Repair., vol. 7, pp.1077–1086.
25. Zhang F., Wang Y., Wang L., Luo X., Huang K., Wang C., Du M., Liu F., Luo T., Huang D., Huang K. (2013) Poly(ADP-ribose) Polymerase 1 Is a Key Regulator of Estrogen Receptor α-dependent Gene Transcription. J. Biol. Chem., vol. 288 (16), pp. 11348–11357.
2 Foyer C.H., Noctor G. Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria // Physiol. Plant. - 2003. - Vol. 119. - P.355–364.
3 Weitzman M.D., Weitzman J.B. What's the damage? The impact of pathogens on pathways that maintain host genome integrity //Cell Host Microbe. -2014. -Vol.15. - №3. -P.283-294.
4 Papamichos-Chronakis M., Peterson C.L. Chromatin and the genome integrity network // Nat Rev Genet. - 2013. - Vol. 14. - № 1. - P.62–75.
5 Ermolaeva M.A., Schumacher B. Systemic DNA damage responses: organismal adaptations to genome instability // Trends Genet. - 2014. - Vol. 30. - № 3. - P.95–102.
6 Schreiber V., Dantzer F., Ame J.C., de Murcia G. Poly (ADP-ribose): novel functions for an old molecule // Nat. Rev. Mol. Cell. Biol. - 2006. - Vol 7. - P.517–528.
7 Kim M.Y., Zhang T., Kraus W.L. Poly(ADP-ribosyl)ation by PARP-1: ’PAR-laying’ NAD+ into a nuclear signal // Genes Dev. - 2005. - Vol. 19. - P.1951–1967.
8 Ame´ J-C., Spenlehauer C., de Murcia G. The PARP superfamily // BioEssays. - 2004. - Vol. 26. - P.882–893
9 Woodhouse B.C., Dianov G.L. Poly ADP-ribose polymerase-1: an international molecule of mystery // DNA Repair. - 2008. - Vol. 7. - P.1077–1086.
10 Kraus W.L., Hottiger M.O. PARP-1 and gene regulation: progress and puzzles // Mol. Aspects Med. - 2013. - Vol. 34. - P.1109–1123.
11 Caldecott K.W. Mammalian single-strand break repair: mechanisms and links with chromatin // DNA Repair. - 2007. - Vol. 6. - P.443–453.
12 Shieh W.M., Ame J.C., Wilson M.V., Wang Z.Q., Koh D.W., JacobsonM.K., Jacobson E.L. Poly(ADP-ribose) polymerase null mouse cells synthesize ADP-ribose polymers // J.Biol.Chem. - 1998. - Vol. 273. - P.30069–30072.
13 de Murcia G., Menissier de Murcia J. Poly(ADP-ribose)polymerase: a molecular nick-sensor // Trends Biochem. Sci. - 1994. - Vol. 19. - P.172–176.
14 Tanaka Y., Yoshihara K., Itaya A., Kamiya T., Koide S.S. Mechanism of the inhibition of Ca2+, Mg2+-dependentendonuclease of bull seminal plasma induced by ADP-ribosylation // J.Biol. Chem. - 1984. - Vol. 259. - P.6579–6585.
15 Satoh M.S., Poirier G.G. and Lindahl T. Dual function forpoly(ADP-ribose) synthesis in response to DNA strand breakage // Biochemistry. - 1994. - Vol. 33. - P.7099–7106.
16 Caldecott K.W. Protein ADP-ribosylation and the cellularresponse to DNA strand breaks // DNA Repair. - 2014. - Vol. 19. - P.108–113.
17 Briggs A.G., Bent A.F. Poly(ADP-ribosyl)ation in plants // Trends Plant Sci. - 2011. - Vol. 16. - № 7. - P.372–80.
18 Lamb R.S., Citarelli M., Teotia S. Functions of the poly(ADP-ribose) polymerase superfamily in plants // Cell Mol Life Sci. - 2012. - Vol. 69. - № 2. - P.175–89.
19 Briggs A.G., Bent A.F. Poly(ADP-ribosyl)ation in plants // Trends in Plant Science. - 2011. - Vol. 16. - № 7. - P.360-1385.
20 Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4 // Nature. – 1970. – Vol. 227. - № 5259. – P. 680-685.
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. 248-302.
22 Vainonen J.P., Shapiguzov A., Vaattovaara A., Kangasjärvi J. Plant PARPs, PARGs and PARP-like Proteins // Current Protein and Peptide Science. – 2016. – Vol. 17. - P.713-723
23 Hinz J.M., Rodriguez Y., Smerdon M.J. Rotational dynamics of DNA on the nucleosome surface markedly impact accessibility to a DNA repair enzyme // Proc. Natl. Acad. Sci. U.S.A. - 2010. - Vol. 107. - P.4646–4651.
24 Odell I.D., Barbour J.E., Murphy D.L., Della-Maria J.A., Sweasy J.B., Tomkinson A.E., Wallace S.S., Pederson D.S. Nucleosome disruption by DNA ligase III-XRCC1 promotes efficient base excision repair // Mol. Cell. Biol. - 2011. - Vol. 31. - P.4623–4632.
25 Zhang F., Wang Y., Wang L., Luo X., Huang K., Wang C., Du M., Liu F., Luo T., Huang D., Huang K. Poly(ADP-ribose) Polymerase 1 Is a Key Regulator of Estrogen Receptor α-dependent Gene Transcription // J. Biol. Chem. – 2013. - Vol. 288. - № 16. – P. 11348–11357.
References
1. Ame´ J-C., Spenlehauer C., de Murcia G. (2004) The PARP superfamily. BioEssays, vol. 26, pp. 882–893.
2. Briggs A.G, Bent A.F. (2011) Poly(ADP-ribosyl)ation in plants. Trends Plant Sci., vol. 16 (7), pp.372–80.
3. Briggs A.G., Bent A.F. (2011) Poly(ADP-ribosyl)ation in plants. Trends in Plant Science., vol. 16 (7), pp.360-1385.
4. 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.
5. 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.
6. Caldecott K.W. (2007) Mammalian single-strand break repair: mechanisms and links with chromatin. DNA Repair., vol. 6, pp.443–453.
7. Caldecott K.W. (2014) Protein ADP-ribosylation and the cellularresponse to DNA strand breaks. DNA Repair, vol. 19, pp.108–113.
8. de Murcia G., Menissier de Murcia J. (1994) Poly(ADP-ribose)polymerase: a molecular nick-sensor. Trends Biochem. Sci., vol. 19, pp.172–176.
9. Ermolaeva M.A., Schumacher B. (2014) Systemic DNA damage responses: organismal adaptations to genome instability. Trends Genet., vol. 30 (3), pp.95–102.
10. Foyer C.H., Noctor G. (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol. Plant, vol. 119, pp. 355–364.
11. Hinz J.M., Rodriguez Y., Smerdon M.J. (2010) Rotational dynamics of DNA on the nucleosome surface markedly impact accessibility to a DNA repair enzyme. Proc. Natl. Acad. Sci. U.S.A., vol. 107, pp.4646–4651.
12. Kim M.Y., Zhang T., Kraus W.L. (2005) Poly(ADP-ribosyl)ation by PARP-1: ’PAR-laying’ NAD+ into a nuclear signal. Genes Dev., vol. 19, pp.1951–1967.
13. Kraus W.L., Hottiger M.O. (2013) PARP-1 and gene regulation: progress and puzzles. Mol. Aspects Med., vol. 34, pp.1109–1123.
14. Laemmli U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, vol. 227 (5259), pp. 680-685.
15. Lamb R.S., Citarelli M., Teotia S. (2012) Functions of the poly(ADP-ribose) polymerase superfamily in plants. Cell Mol Life Sci., vol. 69 (2). - P.175–89.
16. Odell I.D., Barbour J.E., Murphy D.L., Della-Maria J.A., Sweasy J.B., Tomkinson A.E., Wallace S.S., Pederson D.S. (2011) Nucleosome disruption by DNA ligase III-XRCC1 promotes efficient base excision repair. Mol. Cell. Biol., vol. 31, pp.4623–4632.
17. Papamichos-Chronakis M., Peterson C.L. (2013) Chromatin and the genome integrity network. Nat Rev Genet., vol. 14 (1), pp.62–75.
18. Schreiber V., Dantzer F., Ame J.C., de Murcia,G. (2006) Poly(ADP-ribose): novel functions for an old molecule // Nat. Rev. Mol. Cell. Biol., vol 7, pp.517–528.
19. Shieh W.M., Ame J.C., Wilson M.V., Wang Z.Q., Koh D.W., JacobsonM.K., Jacobson E.L. (1998) Poly(ADP-ribose) polymerase null mouse cells synthesize ADP-ribose polymers. J.Biol.Chem., vol. 273, pp.30069–30072.
20. Satoh,M.S., Poirier,G.G. and Lindahl,T. (1994) Dual function forpoly(ADP-ribose) synthesis in response to DNA strand breakage. Biochemistry, vol. 33, pp.7099–7106.
21. Tanaka Y., Yoshihara K., Itaya A., Kamiya T., Koide S.S. (1984) Mechanism of the inhibition of Ca2+, Mg2+-dependentendonuclease of bull seminal plasma induced by ADP-ribosylation. J.Biol. Chem., vol. 259, pp.6579–6585.
22. Vainonen J.P., Shapiguzov A., Vaattovaara A., Kangasjärvi J. (2016) Plant PARPs, PARGs and PARP-like Proteins. Current Protein and Peptide Science., vol. 17, pp.713-723
23. Weitzman M.D, Weitzman J.B. (2014) What's the damage? The impact of pathogens on pathways that maintain host genome integrity. Cell Host Microbe, vol.15 (3), pp. 283-294.
24. Woodhouse B.C., Dianov G.L. (2008) Poly ADP-ribose polymerase-1: an international molecule of mystery. DNA Repair., vol. 7, pp.1077–1086.
25. Zhang F., Wang Y., Wang L., Luo X., Huang K., Wang C., Du M., Liu F., Luo T., Huang D., Huang K. (2013) Poly(ADP-ribose) Polymerase 1 Is a Key Regulator of Estrogen Receptor α-dependent Gene Transcription. J. Biol. Chem., vol. 288 (16), pp. 11348–11357.
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Kuanbay, A. K., Smekenov, I. T., Saparbayev, M. K., Ishchenko А. А., Taipakova, S. M., & Bissenbaev, A. K. (2018). Isolation and characterization of Arabidopsis thaliana poly(ADP-ribose) polymerase 2 cDNA. Experimental Biology, 74(1), 99–111. https://doi.org/10.26577/eb-2018-1-1319
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МOLECULAR BIOLOGY AND GENETICS
