Function and molecular mechanisms of APE2 in genome and epigenome integrity

Mutation Research/Reviews in Mutation Research - Tập 787 - Trang 108347 - 2021
Yunfeng Lin1, Anne McMahon1, Garrett Driscoll1, Sharon Bullock1, Jianjun Zhao2, Shan Yan1
1Department of Biological Sciences, University of North Carolina at Charlotte, Charlotte, NC, 28223, United States
2Department of Cancer Biology, Lerner Research Institute, Cleveland Clinic, Cleveland, OH, 44195, United States

Tài liệu tham khảo

Lindahl, 1993, Instability and decay of the primary structure of DNA, Nature, 362, 709, 10.1038/362709a0 Boiteux, 2004, Abasic sites in DNA: repair and biological consequences in Saccharomyces cerevisiae, DNA Repair (Amst), 3, 1, 10.1016/j.dnarep.2003.10.002 Thompson, 2020, New insights into abasic site repair and tolerance, DNA Repair (Amst), 90, 10.1016/j.dnarep.2020.102866 Ciccia, 2010, The DNA damage response: making it safe to play with knives, Mol. Cell, 40, 179, 10.1016/j.molcel.2010.09.019 Yan, 2014, Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress, Cell. Mol. Life Sci., 71, 3951, 10.1007/s00018-014-1666-4 Jackson, 2009, The DNA-damage response in human biology and disease, Nature, 461, 1071, 10.1038/nature08467 Demple, 1986, Exonuclease III and endonuclease IV remove 3’ blocks from DNA synthesis primers in H2O2-damaged Escherichia coli, Proc. Natl. Acad. Sci. U.S.A., 83, 7731, 10.1073/pnas.83.20.7731 Li, 2014, 3rd, Human apurinic/apyrimidinic endonuclease 1, Antioxid. Redox Signal., 20, 678, 10.1089/ars.2013.5492 Demple, 1991, 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, 11450, 10.1073/pnas.88.24.11450 Robson, 1991, Isolation of cDNA clones encoding a human apurinic/apyrimidinic endonuclease that corrects DNA repair and mutagenesis defects in E. Coli xth (exonuclease III) mutants, Nucleic Acids Res., 19, 5519, 10.1093/nar/19.20.5519 Xanthoudakis, 1992, Identification and characterization of Ref-1, a nuclear protein that facilitates AP-1 DNA-binding activity, EMBO J., 11, 653, 10.1002/j.1460-2075.1992.tb05097.x Johnson, 1998, 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, 3137, 10.1101/gad.12.19.3137 Hadi, 2000, 3rd, Second human protein with homology to the Escherichia coli abasic endonuclease exonuclease III, Environ. Mol. Mutagen., 36, 312, 10.1002/1098-2280(2000)36:4<312::AID-EM7>3.0.CO;2-K Tsuchimoto, 2001, Human APE2 protein is mostly localized in the nuclei and to some extent in the mitochondria, while nuclear APE2 is partly associated with proliferating cell nuclear antigen, Nucleic Acids Res., 29, 2349, 10.1093/nar/29.11.2349 Willis, 2013, APE2 is required for ATR-Chk1 checkpoint activation in response to oxidative stress, Proc. Natl. Acad. Sci. U.S.A., 110, 10592, 10.1073/pnas.1301445110 Wallace, 2017, APE2 Zf-GRF facilitates 3’-5’ resection of DNA damage following oxidative stress, Proc. Natl. Acad. Sci. U.S.A., 114, 304, 10.1073/pnas.1610011114 Lin, 2018, APE2 promotes DNA damage response pathway from a single-strand break, Nucleic Acids Res., 46, 2479, 10.1093/nar/gky020 Lin, 2020, APE1 senses DNA single-strand breaks for repair and signaling, Nucleic Acids Res., 48, 1925, 10.1093/nar/gkz1175 Cupello, 2019, Distinct roles of XRCC1 in genome integrity in Xenopus egg extracts, Biochem. J., 476, 3791, 10.1042/BCJ20190798 Kumar, 2018, Role of apurinic/apyrimidinic nucleases in the regulation of homologous recombination in myeloma: mechanisms and translational significance, Blood Cancer J., 8, 92, 10.1038/s41408-018-0129-9 Mengwasser, 2019, Genetic screens reveal FEN1 and APEX2 as BRCA2 synthetic lethal targets, Mol. Cell, 73, 885, 10.1016/j.molcel.2018.12.008 Li, 2018, Apurinic/apyrimidinic endonuclease 2 and Zinc finger DNA 3’-phosphoesterase play overlapping roles in the maintenance of epigenome and genome stability, Plant Cell, 30, 1954, 10.1105/tpc.18.00287 Jensen, 2020, Genomic alterations and abnormal expression of APE2 in multiple cancers, Sci. Rep., 10, 3758, 10.1038/s41598-020-60656-5 Yan, 2019, Resolution of a complex crisis at DNA 3’ termini, Nat. Struct. Mol. Biol., 26, 335, 10.1038/s41594-019-0215-0 Li, 2019, Apn2 resolves blocked 3’ ends and suppresses Top1-induced mutagenesis at genomic rNMP sites, Nat. Struct. Mol. Biol., 26, 155, 10.1038/s41594-019-0186-1 Stavnezer, 2014, Differential expression of APE1 and APE2 in germinal centers promotes error-prone repair and A:t mutations during somatic hypermutation, Proc. Natl. Acad. Sci. U.S.A., 111, 9217, 10.1073/pnas.1405590111 Ide, 2004, Growth retardation and dyslymphopoiesis accompanied by G2/M arrest in APEX2-null mice, Blood, 104, 4097, 10.1182/blood-2004-04-1476 Funakoshi, 2017, CiAPEX2 and CiP0, candidates of AP endonucleases in Ciona intestinalis, have 3’-5’ exonuclease activity and contribute to protection against oxidative stress, Genes Environ., 39, 27, 10.1186/s41021-017-0087-7 Ribar, 2004, The major role of human AP-endonuclease homolog Apn2 in repair of abasic sites in Schizosaccharomyces pombe, Nucleic Acids Res., 32, 115, 10.1093/nar/gkh151 Sepulveda, 2014, Expression, functionality, and localization of apurinic/apyrimidinic endonucleases in replicative and non-replicative forms of Trypanosoma cruzi, J. Cell. Biochem., 115, 397, 10.1002/jcb.24675 Ide, 2003, Characterization of the genomic structure and expression of the mouse Apex2 gene, Genomics, 81, 47, 10.1016/S0888-7543(02)00009-5 Jin, 2014, Interaction of apurinic/apyrimidinic endonuclease 2 (Apn2) with Myh1 DNA glycosylase in fission yeast, DNA Repair (Amst), 15, 1, 10.1016/j.dnarep.2014.01.001 Unk, 2001, 3’-phosphodiesterase and 3’--&5’ exonuclease activities of yeast Apn2 protein and requirement of these activities for repair of oxidative DNA damage, Mol. Cell. Biol., 21, 1656, 10.1128/MCB.21.5.1656-1661.2001 Burkovics, 2006, Human Ape2 protein has a 3’-5’ exonuclease activity that acts preferentially on mismatched base pairs, Nucleic Acids Res., 34, 2508, 10.1093/nar/gkl259 Burkovics, 2009, Role of PCNA-dependent stimulation of 3’-phosphodiesterase and 3’-5’ exonuclease activities of human Ape2 in repair of oxidative DNA damage, Nucleic Acids Res., 37, 4247, 10.1093/nar/gkp357 Unk, 2000, Apurinic endonuclease activity of yeast Apn2 protein, J. Biol. Chem., 275, 22427, 10.1074/jbc.M002845200 Unk, 2002, Stimulation of 3’-->5’ exonuclease and 3’-phosphodiesterase activities of yeast apn2 by proliferating cell nuclear antigen, Mol. Cell. Biol., 22, 6480, 10.1128/MCB.22.18.6480-6486.2002 Wu, 2019, TRAIP is a master regulator of DNA interstrand crosslink repair, Nature, 567, 267, 10.1038/s41586-019-1002-0 Ha, 2020, A non-canonical role for the DNA glycosylase NEIL3 in suppressing APE1 endonuclease-mediated ssDNA damage, J. Biol. Chem., 295, 14222, 10.1074/jbc.RA120.014228 Alvarez-Quilon, 2020, Endogenous DNA 3’ blocks are vulnerabilities for BRCA1 and BRCA2 deficiency and are reversed by the APE2 nuclease, Mol. Cell, 78, 1152, 10.1016/j.molcel.2020.05.021 Johnson, 1988, Yeast DNA 3’-repair diesterase is the major cellular apurinic/apyrimidinic endonuclease: substrate specificity and kinetics, J. Biol. Chem., 263, 18017, 10.1016/S0021-9258(19)81317-0 Wilson, 1995, Incision activity of human apurinic endonuclease (Ape) at abasic site analogs in DNA, J. Biol. Chem., 270, 16002, 10.1074/jbc.270.27.16002 Li, 2015, An AP endonuclease functions in active DNA demethylation and gene imprinting in Arabidopsis [corrected], PLoS Genet., 11, 10.1371/journal.pgen.1004905 Hadi, 2002, Determinants in nuclease specificity of Ape1 and Ape2, human homologues of Escherichia coli exonuclease III, J. Mol. Biol., 316, 853, 10.1006/jmbi.2001.5382 Andres, 2015, Recognition and repair of chemically heterogeneous structures at DNA ends, Environ. Mol. Mutagen., 56, 1, 10.1002/em.21892 Sugimoto, 2005, Roles of base excision repair enzymes Nth1p and Apn2p from Schizosaccharomyces pombe in processing alkylation and oxidative DNA damage, DNA Repair (Amst), 4, 1270, 10.1016/j.dnarep.2005.06.009 Hossain, 2018, Single-strand break end resection in genome integrity: mechanism and regulation by APE2, Int. J. Mol. Sci., 19, 2389, 10.3390/ijms19082389 Caldecott, 2008, Single-strand break repair and genetic disease, Nat. Rev. Genet., 9, 619, 10.1038/nrg2380 Kim, 2011, Mutagenic processing of ribonucleotides in DNA by yeast topoisomerase I, Science, 332, 1561, 10.1126/science.1205016 Sekiguchi, 1997, Site-specific ribonuclease activity of eukaryotic DNA topoisomerase I, Mol. Cell, 1, 89, 10.1016/S1097-2765(00)80010-6 Mailand, 2013, Regulation of PCNA-protein interactions for genome stability, Nat. Rev. Mol. Cell Biol., 14, 269, 10.1038/nrm3562 Kumagai, 2000, Claspin, a novel protein required for the activation of Chk1 during a DNA replication checkpoint response in Xenopus egg extracts, Mol. Cell, 6, 839, 10.1016/S1097-2765(05)00092-4 Kumagai, 2003, Repeated phosphopeptide motifs in Claspin mediate the regulated binding of Chk1, Nat. Cell Biol., 5, 161, 10.1038/ncb921 Tell, 2009, The many functions of APE1/Ref-1: not only a DNA repair enzyme, Antioxid. Redox Signal., 11, 601, 10.1089/ars.2008.2194 Hoitsma, 2020, Structure and function relationships in mammalian DNA polymerases, Cell. Mol. Life Sci., 77, 35, 10.1007/s00018-019-03368-y Dan, 2008, Altered gene expression profiles and higher frequency of spontaneous DNA strand breaks in APEX2-null thymus, DNA Repair (Amst), 7, 1437, 10.1016/j.dnarep.2008.05.003 Mol, 2000, Abasic site recognition by two apurinic/apyrimidinic endonuclease families in DNA base excision repair: the 3’ ends justify the means, Mutat. Res., 460, 211, 10.1016/S0921-8777(00)00028-8 Hegde, 2008, Early steps in the DNA base excision/single-strand interruption repair pathway in mammalian cells, Cell Res., 18, 27, 10.1038/cr.2008.8 Krokan, 2013, Base excision repair, Cold Spring Harb. Perspect. Biol., 5, 10.1101/cshperspect.a012583 Svilar, 2011, Base excision repair and lesion-dependent subpathways for repair of oxidative DNA damage, Antioxid. Redox Signal., 14, 2491, 10.1089/ars.2010.3466 Nakabeppu, 2004, Biological significance of the defense mechanisms against oxidative damage in nucleic acids caused by reactive oxygen species: from mitochondria to nuclei, Ann. N. Y. Acad. Sci., 1011, 101, 10.1196/annals.1293.011 Davis, 2014, Homology-directed repair of DNA nicks via pathways distinct from canonical double-strand break repair, Proc. Natl. Acad. Sci. U.S.A., 111, E924, 10.1073/pnas.1400236111 Brem, 2005, XRCC1 is required for DNA single-strand break repair in human cells, Nucleic Acids Res., 33, 2512, 10.1093/nar/gki543 Eustermann, 2015, Structural basis of detection and signaling of DNA single-strand breaks by human PARP-1, Mol. Cell, 60, 742, 10.1016/j.molcel.2015.10.032 Cupello, 2016, Cell-free Xenopus egg extracts for studying DNA damage response pathways, Int. J. Dev. Biol., 60, 229, 10.1387/ijdb.160113sy Malyarchuk, 2008, DNA repair of clustered lesions in mammalian cells: involvement of non-homologous end-joining, Nucleic Acids Res., 36, 4872, 10.1093/nar/gkn450 Lin, 2019, Methods for studying DNA single-strand break repair and signaling in Xenopus laevis egg extracts, Methods Mol. Biol., 1999, 161, 10.1007/978-1-4939-9500-4_9 Stratigopoulou, 2020, Base excision repair in the immune system: small DNA lesions with big consequences, Front. Immunol., 11, 1084, 10.3389/fimmu.2020.01084 Schrader, 2009, The roles of APE1, APE2, DNA polymerase beta and mismatch repair in creating S region DNA breaks during antibody class switch, Philos. Trans. R. Soc. Lond., B, Biol. Sci., 364, 645, 10.1098/rstb.2008.0200 Guikema, 2007, APE1- and APE2-dependent DNA breaks in immunoglobulin class switch recombination, J. Exp. Med., 204, 3017, 10.1084/jem.20071289 Sabouri, 2009, Apex2 is required for efficient somatic hypermutation but not for class switch recombination of immunoglobulin genes, Int. Immunol., 21, 947, 10.1093/intimm/dxp061 Masani, 2013, Apurinic/apyrimidinic endonuclease 1 is the essential nuclease during immunoglobulin class switch recombination, Mol. Cell. Biol., 33, 1468, 10.1128/MCB.00026-13 Guikema, 2010, The role of Apex2 in class-switch recombination of immunoglobulin genes, Int. Immunol., 22, 213, 10.1093/intimm/dxq003 Zhu, 2009, Active DNA demethylation mediated by DNA glycosylases, Annu. Rev. Genet., 43, 143, 10.1146/annurev-genet-102108-134205 Kohli, 2013, TET enzymes, TDG and the dynamics of DNA demethylation, Nature, 502, 472, 10.1038/nature12750 Xanthoudakis, 1996, The redox/DNA repair protein, Ref-1, is essential for early embryonic development in mice, Proc. Natl. Acad. Sci. U.S.A., 93, 8919, 10.1073/pnas.93.17.8919 Murphy, 2009, Requirement for abasic endonuclease gene homologues in Arabidopsis seed development, PLoS One, 4, e4297, 10.1371/journal.pone.0004297 Guikema, 2011, Apurinic/apyrimidinic endonuclease 2 is necessary for normal B cell development and recovery of lymphoid progenitors after chemotherapeutic challenge, J. Immunol., 186, 1943, 10.4049/jimmunol.1002422 Omeroglu Simsek, 2020, Evaluation of gene expression levels in the diagnosis of lung adenocarcinoma and malignant pleural mesothelioma, Turk Gogus Kalp Damar Cerrahisi Derg, 28, 188, 10.5606/tgkdc.dergisi.2020.17279 Metintas, 1999, Environmental asbestos exposure and malignant pleural mesothelioma, Respir. Med., 93, 349, 10.1016/S0954-6111(99)90318-9 Zheng, 2020, Identification of APEX2 as an oncogene in liver cancer, World J. Clin. Cases, 8, 2917, 10.12998/wjcc.v8.i14.2917 Hustedt, 2019, A consensus set of genetic vulnerabilities to ATR inhibition, Open Biol., 9, 10.1098/rsob.190156 Petrucelli, 2010, Hereditary breast and ovarian cancer due to mutations in BRCA1 and BRCA2, Genet. Med., 12, 245, 10.1097/GIM.0b013e3181d38f2f Akbari, 2008, Mitochondrial base excision repair of uracil and AP sites takes place by single-nucleotide insertion and long-patch DNA synthesis, DNA Repair (Amst), 7, 605, 10.1016/j.dnarep.2008.01.002 Wang, 2011, Identification of rare DNA variants in mitochondrial disorders with improved array-based sequencing, Nucleic Acids Res., 39, 44, 10.1093/nar/gkq750 Yui, 2014, The DNA repair enzyme Apurinic/Apyrimidinic Endonuclease (Apex Nuclease) 2 has the potential to protect against down-regulation of chondrocyte activity in osteoarthritis, Int. J. Mol. Sci., 15, 14921, 10.3390/ijms150914921