Apurinic/apyrimidinic endonuclease 1 has major impact in prevention of suicidal covalent DNA-protein crosslink with apurinic/apyrimidinic site in cellular extracts.
AP endonuclease 1
DNA–protein crosslinks
apurinic/apyrimidinic site
poly(ADP‐ribose) polymerases
tyrosyl‐DNA phosphodiesterase 1
Journal
IUBMB life
ISSN: 1521-6551
Titre abrégé: IUBMB Life
Pays: England
ID NLM: 100888706
Informations de publication
Date de publication:
04 Jul 2024
04 Jul 2024
Historique:
received:
05
03
2024
accepted:
16
05
2024
medline:
4
7
2024
pubmed:
4
7
2024
entrez:
4
7
2024
Statut:
aheadofprint
Résumé
DNA-protein crosslinks (DPC) are common DNA lesions induced by various external and endogenous agents. One of the sources of DPC is the apurinic/apyrimidinic site (AP site) and proteins interacting with it. Some proteins possessing AP lyase activity form covalent complexes with AP site-containing DNA without borohydride reduction (suicidal crosslinks). We have shown earlier that tyrosyl-DNA phosphodiesterase 1 (TDP1) but not AP endonuclease 1 (APE1) is able to remove intact OGG1 from protein-DNA adducts, whereas APE1 is able to prevent the formation of DPC by hydrolyzing the AP site. Here we demonstrate that TDP1 can remove intact PARP2 but not XRCC1 from covalent enzyme-DNA adducts with AP-DNA formed in the absence of APE1. We also analyzed an impact of APE1 and TDP1 on the efficiency of DPC formation in APE1
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Russian Science Foundation
ID : 21-64-00017
Organisme : Russian Science Foundation
ID : 22-14-00112
Organisme : Ministry of Higher Education and Science
Informations de copyright
© 2024 International Union of Biochemistry and Molecular Biology.
Références
Lindahl T, Nyberg B. Rate of depurination of native deoxyribonucleic acid. Biochemistry. 1972;11:3610–3618.
Atamna H, Cheung I, Ames BN. A method for detecting abasic sites in living cells: age‐dependent changes in base excision repair. Proc Natl Acad Sci U S A. 2000;97:686–691.
Liu ZJ, Martı'nez Cuesta S, van Delft P, Balasubramanian S. Sequencing abasic sites in DNA at singlenucleotide resolution. Nat Chem. 2019;11:629–637.
Pourquier P, Ueng L‐M, Kohlhagen G, Mazumder A, Gupta M, Kohn KW, et al. Effects of uracil incorporation, DNA mismatches, and abasic sites on cleavage and religation activities of mammalian topoisomerase I. J Biol Chem. 1997;272:7792–7796.
Doetsch PW. Translesion synthesis by RNA polymerases: occurrence and biological implications for transcriptional mutagenesis. Mutat Res. 2002;510:131–140.
Quiñones JL, Demple B. When DNA repair goes wrong: BER‐generated DNA‐protein crosslinks to oxidative lesions. DNA Repair. 2016;44:103–109.
Rahimoff R, Kosmatchev O, Kirchner A, Pfaffeneder T, Spada F, Brantl V, et al. 5‐formyl‐ and 5‐carboxydeoxycytidines do not cause accumulation of harmful repair intermediates in stem cells. J Am Chem Soc. 2017;139:10359–10364.
Klungland A, Rosewell I, Hollenbach S, Larsen E, Daly G, Epe B, et al. Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage. Proc Natl Acad Sci U S A. 1999;96:13300–13305.
Lindahl T. DNA repair enzymes. Annu Rev Biochem. 1982;51:61–87.
Lindahl T, Wood RD. Quality control by DNA repair. Science. 1999;286:1897–1905.
Khodyreva SN, Prasad R, Ilina ES, Sukhanova MV, Kutuzov MM, Liu Y, et al. Apurinic/apyrimidinic (AP) site recognition by the 5′‐dRP/AP lyase in poly(ADP‐ribose) polymerase‐1 (PARP‐1). Proc Natl Acad Sci U S A. 2010;107:22090–22095.
Lavrik OI, Prasad R, Sobol RW, Horton JK, Ackerman EJ, Wilson SH. Photoaffinity labeling of mouse fibroblast enzymes by a base excision repair intermediate. Evidence for the role of poly(ADP‐ribose) polymerase‐1 in DNA repair. J Biol Chem. 2001;276:25541–25548.
Lebedeva NA, Rechkunova NI, Lavrik OI. AP‐site cleavage activity of tyrosyl‐DNA phosphodiesterase 1. FEBS Lett. 2011;585:683–686.
Lebedeva NA, Rechkunova NI, Ishchenko AA, Saparbaev M, Lavrik OI. The mechanism of human tyrosyl‐DNA phosphodiesterase 1 in the cleavage of AP site and its synthetic analogs. DNA Repair. 2013;12:1037–1042.
Lebedeva NA, Rechkunova NI, El‐Khamisy SF, Lavrik OI. Tyrosyl‐DNA phosphodiesterase 1 initiates repair of apurinic/apyrimidinic sites. Biochimie. 2012;94:1749–1753.
Doetsch PW, Cunningham RP. The enzymology of apurinic/apyrimidinic endonucleases. Mutat Res. 1990;236:173–201.
Yang SW, Burgin AB Jr, Huizenga BN, Robertson CA, Yao KC, Nash HA. A eukaryotic enzyme that can disjoin dead‐end covalent complexes between DNA and type I topoisomerases. Proc Natl Acad Sci U S A. 1996;93:11534–11539.
Pouliot JJ, Yao KC, Robertson CA, Nash HA. Yeast gene for a Tyr‐DNA phosphodiesterase that repairs topoisomerase I complexes. Science. 1999;286:552–555.
Interthal H, Chen HJ, Champoux JJ. Human TDP1 cleaves a broad spectrum of substrates, including phosphoamide linkages. J Biol Chem. 2005;280:36518–36528.
Pommier Y, Huang SY, Gao R, Das BB, Murai J, Marchand C. Tyrosyl‐DNA‐phosphodiesterases (TDP1 and TDP2). DNA Repair. 2014;19:114–129.
Takashima H, Boerkoel CF, John J, Saifi GM, Salih MA, Armstrong D, et al. Mutation of TDP1, encoding a topoisomerase I‐dependent DNA damage repair enzyme, in spinocerebellar ataxia with axonal neuropathy. Nat Genet. 2002;32:267–272.
Interthal H, Chen HJ, Kehl‐Fie TE, Zotzmann J, Leppard JB, Champoux JJ. SCAN1 mutant Tdp1 accumulates the enzyme–DNA intermediate and causes camptothecin hypersensitivity. EMBO J. 2005;24:2224–2233.
Kuznetsov NA, Lebedeva NA, Kuznetsova AA, Rechkunova NI, Dyrkheeva NS, Kupryushkin MS, et al. Pre‐steady state kinetics of DNA binding and abasic site hydrolysis by tyrosyl‐DNA phosphodiesterase 1. J Biomol Struct Dyn. 2017;35:2314–2327.
Rass U, Ahel I, West SC. Defective DNA repair and neurodegenerative disease. Cell. 2007;130:991–1004.
Prasad R, Williams JG, Hou EW, Wilson SH. Pol beta associated complex and base excision repair factors in mouse fibroblasts. Nucleic Acids Res. 2012;40:11571–11582.
Prasad R, Horton JK, Chastain PD 2nd, Gassman NR, Freudenthal BD, Hou EW, et al. Suicidal cross‐linking of PARP‐1 to AP site intermediates in cells undergoing base excision repair. Nucleic Acids Res. 2014;42:6337–6351.
Satoh MS, Lindahl T. Role of poly(ADP‐ribose) formation in DNA repair. Nature. 1992;356:356–358.
Heacock ML, Stefanick DF, Horton JK, Wilson SH. Alkylation DNA damage in combination with PARP inhibition results in formation of S‐phase‐dependent double‐strand breaks. DNA Repair. 2010;9:929–936.
Gassman NR, Stefanick DF, Kedar PS, Horton JK, Wilson SH. Hyperactivation of PARP triggers nonhomologous end‐joining in repair‐deficient mouse fibroblasts. PLoS One. 2012;7:e49301.
Woodhouse BC, Dianova II, Parsons JL, Dianov GL. Poly(ADP‐ribose) polymerase‐1 modulates DNA repair capacity and prevents formation of DNA double strand breaks. DNA Repair. 2008;7:932–940.
Pachkowski BF, Tano K, Afonin V, Elder RH, Takeda S, Watanabe M, et al. Cells deficient in PARP‐1 show an accelerated accumulation of DNA single strand breaks, but not AP sites, over the PARP‐1‐proficient cells exposed to MMS. Mutat Res. 2009;671:93–99.
Lebedeva NA, Rechkunova NI, Endutkin AV, Lavrik OI. Apurinic/apyrimidinic endonuclease 1 and tyrosyl‐DNA phosphodiesterase 1 prevent suicidal covalent DNA‐protein crosslink at apurinic/apyrimidinic site. Front Cell Dev Biol. 2021;8:617301.
Nazarkina ZK, Khodyreva SN, Marsin S, Lavrik OI, Radicella JP. XRCC1 interactions with base excision repair DNA intermediates. DNA Repair. 2007;6:254–264.
Moor NA, Lavrik OI. Protein‐protein interactions in DNA base excision repair. Biochemistry. 2018;83:411–422.
Caldecott KW. Single‐strand break repair and genetic disease. Nat Rev Genet. 2008;9:619–631.
Beernink PT, Hwang M, Ramirez M, Murphy MB, Doyle SA, Thelen MP. Specificity of protein interactions mediated by BRCT domains of the XRCC1 DNA repair protein. J Biol Chem. 2005;280:30206–30213.
Moor NA, Vasil'eva IA, Anarbaev RO, Antson AA, Lavrik OI. Quantitative characterization of protein‐protein complexes involved in base excision DNA repair. Nucleic Acids Res. 2015;43:6009–6022.
Vasil'eva IA, Moor NA, Lavrik OI. Effect of human XRCC1 protein oxidation on the functional activity of its complexes with the key enzymes of DNA base excision repair. Biochemistry. 2020;85:288–299.
Il'ina IV, Dyrkheeva NS, Zakharenko AL, Sidorenko AY, Li‐Zhulanov NS, Korchagina DV, et al. Design, synthesis, and biological investigation of novel classes of 3‐Carene‐derived potent inhibitors of TDP1. Molecules. 2020;25:3496.
Kim DV, Kulishova LM, Torgasheva NA, Melentyev VS, Dianov GL, Medvedev SP, et al. Mild phenotype of knockouts of the major apurinic/apyrimidinic endonuclease APEX1 in a non‐cancer human cell line. PLoS One. 2021;16:e0257473.
Mani RS, Karimi‐Busheri F, Fanta M, Caldecott KW, Cass CE, Weinfeld M. Biophysical characterization of human XRCC1 and its binding to damaged and undamaged DNA. Biochemistry. 2004;43:16505–16514.
Das BB, Huang SY, Murai J, Rehman I, Amé JC, Sengupta S, et al. PARP1‐TDP1 coupling for the repair of topoisomerase I‐induced DNA damage. Nucleic Acids Res. 2014;42:4435–4449.
Sukhanova MV, Abrakhi S, Joshi V, Pastre D, Kutuzov MM, Anarbaev RO, et al. Single molecule detection of PARP1 and PARP2 interaction with DNA strand breaks and their poly(ADP‐ribosyl)ation using high‐resolution AFM imaging. Nucleic Acids Res. 2015;44:60.
Langelier MF, Riccio AA, Pascal JM. PARP‐2 and PARP‐3 are selectively activated by 5′ phosphorylated DNA breaks through an allosteric regulatory mechanism shared with PARP‐1. Nucleic Acids Res. 2014;42:7762–7775.
Ilina ES, Lavrik OI, Khodyreva SN. Ku antigen interacts with abasic sites. Biochim Biophys Acta. 2008;1784:1777–1785.
Ilina ES, Khodyreva SN, Berezhnoy AE, Larin SS, Lavrik OI. Tracking Ku antigen levels in cell extracts with DNA containing abasic sites. Mutat Res. 2010;685:90–96.
Wei X, Peng Y, Bryan C, Yang K. Mechanisms of DNA‐protein cross‐link formation and repair. Biochim Biophys Acta Proteins Proteomics. 2021;1869:140669.
Weickert P, Stingele J. DNA‐protein crosslinks and their resolution. Annu Rev Biochem. 2022;91:157–181.
Wei X, Wang Z, Hinson C, Yang K. Human TDP1, APE1 and TREX1 repair 3′‐DNA‐peptide/protein cross‐links arising from abasic sites in vitro. Nucleic Acids Res. 2022;50:3638–3657.
Lebedeva NA, Anarbaev RO, Kupryushkin MS, Rechkunova NI, Pyshnyi DV, Stetsenko DA, et al. Design of a new fluorescent oligonucleotide‐based assay for a highly specific real‐time detection of apurinic/apyrimidinic site cleavage by tyrosyl‐DNA phosphodiesterase 1. Bioconjug Chem. 2015;26:2046–2053.
Wang ZQ, Auer B, Stingl L, Berghammer H, Haidacher D, Schweiger M, et al. Mice lacking ADPRT and poly(ADP‐ribosyl)ation develop normally but are susceptible to skin disease. Genes Dev. 1995;9:509–520.
de Murcia JM, Niedergang C, Trucco C, Ricoul M, Dutrillaux B, Mark M, et al. Requirement of poly(ADP‐ribose) polymerase in recovery from DNA damage in mice and in cells. Proc Natl Acad Sci U S A. 1997;94:7303–7307.
Kamaletdinova T, Zong W, Urbánek P, Wang S, Sannai M, Grigaravičius P, et al. Poly(ADP‐ribose) polymerase‐1 lacking enzymatic activity is not compatible with mouse development. Cells. 2023;12:2078.
Kurgina TA, Moor NA, Kutuzov MM, Naumenko KN, Ukraintsev AA, Lavrik OI. Dual function of HPF1 in the modulation of PARP1 and PARP2 activities. Commun Biol. 2021;4:1259.
Ruggiano A, Vaz B, Kilgas S, Popović M, Rodriguez‐Berriguete G, Singh AN, et al. The protease SPRTN and SUMOylation coordinate DNA‐protein crosslink repair to prevent genome instability. Cell Rep. 2021;37:110080.
Essawy MM, Campbell C. Enzymatic processing of DNA‐protein crosslinks. Genes. 2024;15:85.