APOBEC3A damages the cellular genome during DNA replication

References

• Jarmuz A, Chester A, Bayliss J, Gisbourne J, Dunham I, Scott J, Navaratnam N. An anthropoid-specific locus of orphan C to U RNA-editing enzymes on chromosome 22. Genomics 2002; 79:285-96; PMID:11863358; http://dx.doi.org/10.1006/geno.2002.6718.
   PubMed Web of Science ®Google Scholar
• Conticello SG, Thomas CJ, Petersen-Mahrt SK, Neuberger MS. Evolution of the AID/APOBEC family of polynucleotide (deoxy)cytidine deaminases. Mol Biol Evol 2005; 22:367-77; PMID:15496550; http://dx.doi.org/10.1093/molbev/msi026.
   PubMed Web of Science ®Google Scholar
• Muramatsu M, Sankaranand VS, Anant S, Sugai M, Kinoshita K, Davidson NO, Honjo T. Specific expression of activation-induced cytidine deaminase (AID), a novel member of the RNA-editing deaminase family in germinal center B cells. J Biol Chem 1999; 274:18470-6; PMID:10373455; http://dx.doi.org/10.1074/jbc.274.26.18470.
   PubMed Web of Science ®Google Scholar
• Di Noia JM, Neuberger MS. Molecular mechanisms of antibody somatic hypermutation. Annual Rev Biochem 2007; 76:1-22; http://dx.doi.org/10.1146/annurev.biochem.76.061705.090740.
   PubMed Web of Science ®Google Scholar
• Sheehy AM, Gaddis NC, Choi JD, Malim MH. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 2002; 418:646-50; PMID:12167863; http://dx.doi.org/10.1038/nature00939.
   PubMed Web of Science ®Google Scholar
• Harris RS, Bishop KN, Sheehy AM, Craig HM, Petersen-Mahrt SK, Watt IN, Neuberger MS, Malim MH. DNA deamination mediates innate immunity to retroviral infection. Cell 2003; 113:803-9; PMID:12809610; http://dx.doi.org/10.1016/S0092-8674(03)00423-9.
   PubMed Web of Science ®Google Scholar
• Harris RS, Dudley JP. APOBECs and virus restriction. Virology 2015; 479-480:131-45; PMID:25818029.
   PubMed Web of Science ®Google Scholar
• Chen H, Lilley CE, Yu Q, Lee DV, Chou J, Narvaiza I, Landau NR, Weitzman MD. APOBEC3A is a potent inhibitor of adeno-associated virus and retrotransposons. Curr Biol 2006; 16:480-5; PMID:16527742; http://dx.doi.org/10.1016/j.cub.2006.01.031.
   PubMed Web of Science ®Google Scholar
• Richardson SR, Narvaiza I, Planegger RA, Weitzman MD, Moran JV. APOBEC3A deaminates transiently exposed single-strand DNA during LINE-1 retrotransposition. eLife 2014; 3:e02008.
   PubMed Web of Science ®Google Scholar
• Bogerd HP, Wiegand HL, Hulme AE, Garcia-Perez JL, O'Shea KS, Moran JV, Cullen BR. Cellular inhibitors of long interspersed element 1 and Alu retrotransposition. Proc Natl Acad Sci USA 2006; 103:8780-5; PMID:16728505; http://dx.doi.org/10.1073/pnas.0603313103.
   PubMed Web of Science ®Google Scholar
• Muckenfuss H, Hamdorf M, Held U, Perkovic M, Lower J, Cichutek K, Flory E, Schumann GG, Munk C. APOBEC3 proteins inhibit human LINE-1 retrotransposition. J Biol Chem 2006; 281:22161-72; PMID:16735504; http://dx.doi.org/10.1074/jbc.M601716200.
   PubMed Web of Science ®Google Scholar
• Narvaiza I, Landry S, Weitzman MD. APOBEC3 proteins and genomic stability: the high cost of a good defense. Cell Cycle 2012; 11:33-8; PMID:22157092; http://dx.doi.org/10.4161/cc.11.1.18706.
   PubMed Web of Science ®Google Scholar
• Henderson S, Fenton T. APOBEC3 genes: retroviral restriction factors to cancer drivers. Trends Mol Med 2015; 21:274-84; PMID:25820175; http://dx.doi.org/10.1016/j.molmed.2015.02.007.
   PubMed Web of Science ®Google Scholar
• Okazaki IM, Hiai H, Kakazu N, Yamada S, Muramatsu M, Kinoshita K, Honjo T. Constitutive expression of AID leads to tumorigenesis. J Exp Med 2003; 197:1173-81; PMID:12732658; http://dx.doi.org/10.1084/jem.20030275.
   PubMed Web of Science ®Google Scholar
• Klemm L, Duy C, Iacobucci I, Kuchen S, von Levetzow G, Feldhahn N, Henke N, Li Z, Hoffmann TK, Kim YM, et al. The B cell mutator AID promotes B lymphoid blast crisis and drug resistance in chronic myeloid leukemia. Cancer Cell 2009; 16:232-45; PMID:19732723; http://dx.doi.org/10.1016/j.ccr.2009.07.030.
   PubMed Web of Science ®Google Scholar
• Greisman HA, Lu Z, Tsai AG, Greiner TC, Yi HS, Lieber MR. IgH partner breakpoint sequences provide evidence that AID initiates t(11;14) and t(8;14) chromosomal breaks in mantle cell and Burkitt lymphomas. Blood 2012; 120:2864-7; PMID:22915650; http://dx.doi.org/10.1182/blood-2012-02-412791.
   PubMed Web of Science ®Google Scholar
• Nik-Zainal S, Alexandrov LB, Wedge DC, Van Loo P, Greenman CD, Raine K, Jones D, Hinton J, Marshall J, Stebbings LA, et al. Mutational processes molding the genomes of 21 breast cancers. Cell 2012; 149:979-93; PMID:22608084; http://dx.doi.org/10.1016/j.cell.2012.04.024.
   PubMed Web of Science ®Google Scholar
• Burns MB, Lackey L, Carpenter MA, Rathore A, Land AM, Leonard B, Refsland EW, Kotandeniya D, Tretyakova N, Nikas JB, et al. APOBEC3B is an enzymatic source of mutation in breast cancer. Nature 2013; 494:366-70; PMID:23389445; http://dx.doi.org/10.1038/nature11881.
   PubMed Web of Science ®Google Scholar
• Alexandrov LB, Nik-Zainal S, Wedge DC, Aparicio SA, Behjati S, Biankin AV, Bignell GR, Bolli N, Borg A, Borresen-Dale AL, et al. Signatures of mutational processes in human cancer. Nature 2013; 500:415-21; PMID:23945592; http://dx.doi.org/10.1038/nature12477.
   PubMed Web of Science ®Google Scholar
• Lawrence MS, Stojanov P, Polak P, Kryukov GV, Cibulskis K, Sivachenko A, Carter SL, Stewart C, Mermel CH, Roberts SA, et al. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 2013; 499:214-8; PMID:23770567; http://dx.doi.org/10.1038/nature12213.
   PubMed Web of Science ®Google Scholar
• Lada AG, Stepchenkova EI, Waisertreiger IS, Noskov VN, Dhar A, Eudy JD, Boissy RJ, Hirano M, Rogozin IB, Pavlov YI. Genome-Wide mutation avalanches induced in diploid yeast cells by a base analog or an APOBEC deaminase. PLoS Genet 2013; 9:e1003736; PMID:24039593; http://dx.doi.org/10.1371/journal.pgen.1003736.
   PubMedGoogle Scholar
• Taylor BJ, Nik-Zainal S, Wu YL, Stebbings LA, Raine K, Campbell PJ, Rada C, Stratton MR, Neuberger MS. DNA deaminases induce break-associated mutation showers with implication of APOBEC3B and 3A in breast cancer kataegis. eLife 2013; 2:e00534; PMID:23599896; http://dx.doi.org/10.7554/eLife.00534.
   PubMed Web of Science ®Google Scholar
• Roberts SA, Sterling J, Thompson C, Harris S, Mav D, Shah R, Klimczak LJ, Kryukov GV, Malc E, Mieczkowski PA, et al. Clustered mutations in yeast and in human cancers can arise from damaged long single-strand DNA regions. Mol Cell 2012; 46:424-35; PMID:22607975; http://dx.doi.org/10.1016/j.molcel.2012.03.030.
   PubMed Web of Science ®Google Scholar
• Lada AG, Dhar A, Boissy RJ, Hirano M, Rubel AA, Rogozin IB, Pavlov YI. AID/APOBEC cytosine deaminase induces genome-wide kataegis. Biol Direct 2012; 7:47; discussion; PMID:23249472; http://dx.doi.org/10.1186/1745-6150-7-47.
   PubMed Web of Science ®Google Scholar
• Chan K, Sterling JF, Roberts SA, Bhagwat AS, Resnick MA, Gordenin DA. Base damage within single-strand DNA underlies in vivo hypermutability induced by a ubiquitous environmental agent. PLoS genetics 2012; 8:e1003149; PMID:23271983; http://dx.doi.org/10.1371/journal.pgen.1003149.
   PubMedGoogle Scholar
• Mitra M, Hercik K, Byeon IJ, Ahn J, Hill S, Hinchee-Rodriguez K, Singer D, Byeon CH, Charlton LM, Nam G, et al. Structural determinants of human APOBEC3A enzymatic and nucleic acid binding properties. Nucleic Acids Res 2014; 42:1095-110; PMID:24163103; http://dx.doi.org/10.1093/nar/gkt945.
   PubMed Web of Science ®Google Scholar
• Pham P, Landolph A, Mendez C, Li N, Goodman MF. A biochemical analysis linking APOBEC3A to disparate HIV-1 restriction and skin cancer. J Biol Chem 2013; 288(41):29294-304.
   PubMed Web of Science ®Google Scholar
• Chaudhuri J, Tian M, Khuong C, Chua K, Pinaud E, Alt FW. Transcription-targeted DNA deamination by the AID antibody diversification enzyme. Nature 2003; 422:726-30; PMID:12692563; http://dx.doi.org/10.1038/nature01574.
   PubMed Web of Science ®Google Scholar
• Yu K, Chedin F, Hsieh CL, Wilson TE, Lieber MR. R-loops at immunoglobulin class switch regions in the chromosomes of stimulated B cells. Nature Immunol 2003; 4:442-51; http://dx.doi.org/10.1038/ni919.
   PubMed Web of Science ®Google Scholar
• Bhagwat AS, Hao W, Townes JP, Lee H, Tang H, Foster PL. Strand-biased cytosine deamination at the replication fork causes cytosine to thymine mutations in Escherichia coli. Proc Natl Acad Sci USA 2016; 113:2176-2181; PMID:26839411.
   PubMed Web of Science ®Google Scholar
• Hoopes JI, Cortez LM, Mertz TM, Malc EP, Mieczkowski PA, Roberts SA. APOBEC3A and APOBEC3B preferentially deaminate the lagging strand template during DNA replication. Cell Reports 2016; 14:1273-1282; PMID:26832400.
   PubMed Web of Science ®Google Scholar
• Seplyarskiy VB, Soldatov RA, Popadin KY, Antonarakis SE, Bazykin GA, Nikolaev SI. APOBEC-induced mutations in human cancers are strongly enriched on the lagging DNA strand during replication. Genome Res 2016; 25:174-182; http://dx.doi.org/10.1101/gr.197046.115.
   Web of Science ®Google Scholar
• Haradhvala NJ, Polak P, Stojanov P, Covington KR, Shinbrot E, Hess JM, Rheinbay E, Kim J, Maruvka YE, Braunstein LZ, et al. Mutational strand asymmetries in cancer genomes reveal mechanisms of DNA damage and repair. Cell 2016; 164:538-49; PMID:26806129; http://dx.doi.org/10.1016/j.cell.2015.12.050.
   PubMed Web of Science ®Google Scholar
• Bogerd HP, Wiegand HL, Doehle BP, Lueders KK, Cullen BR. APOBEC3A and APOBEC3B are potent inhibitors of LTR-retrotransposon function in human cells. Nucleic Acids Res 2006; 34:89-95; PMID:16407327; http://dx.doi.org/10.1093/nar/gkj416.
   PubMed Web of Science ®Google Scholar
• Vartanian JP, Guetard D, Henry M, Wain-Hobson S. Evidence for editing of human papillomavirus DNA by APOBEC3 in benign and precancerous lesions. Science 2008; 320:230-3; PMID:18403710; http://dx.doi.org/10.1126/science.1153201.
   PubMed Web of Science ®Google Scholar
• Warren CJ, Xu T, Guo K, Griffin LM, Westrich JA, Lee D, Lambert PF, Santiago ML, Pyeon D. APOBEC3A functions as a restriction factor of human papillomavirus. J Virol 2015; 89:688-702; PMID:25355878; http://dx.doi.org/10.1128/JVI.02383-14.
   PubMed Web of Science ®Google Scholar
• Landry S, Narvaiza I, Linfesty DC, Weitzman MD. APOBEC3A can activate the DNA damage response and cause cell-cycle arrest. EMBO Rep 2011; 12:444-50; PMID:21460793; http://dx.doi.org/10.1038/embor.2011.46.
   PubMed Web of Science ®Google Scholar
• Zhou BB, Elledge SJ. The DNA damage response: putting checkpoints in perspective. Nature 2000; 408:433-9; PMID:11100718; http://dx.doi.org/10.1038/35044005.
   PubMed Web of Science ®Google Scholar
• Kastan MB, Bartek J. Cell-cycle checkpoints and cancer. Nature 2004; 432:316-23; PMID:15549093; http://dx.doi.org/10.1038/nature03097.
   PubMed Web of Science ®Google Scholar
• Marechal A, Zou L. DNA damage sensing by the ATM and ATR kinases. Cold Spring Harb Perspect Biol 2013; 5:a012716; PMID:24003211; http://dx.doi.org/10.1101/cshperspect.a012716.
   PubMed Web of Science ®Google Scholar
• Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003; 421:499-506; PMID:12556884; http://dx.doi.org/10.1038/nature01368.
   PubMed Web of Science ®Google Scholar
• Ahn JY, Schwarz JK, Piwnica-Worms H, Canman CE. Threonine 68 phosphorylation by ataxia telangiectasia mutated is required for efficient activation of Chk2 in response to ionizing radiation. Cancer Res 2000; 60:5934-6; PMID:11085506.
   PubMed Web of Science ®Google Scholar
• Falck J, Mailand N, Syljuasen RG, Bartek J, Lukas J. The ATM-Chk2-Cdc25A checkpoint pathway guards against radioresistant DNA synthesis. Nature 2001; 410:842-7; PMID:11298456; http://dx.doi.org/10.1038/35071124.
   PubMed Web of Science ®Google Scholar
• Shiloh Y. The ATM-Mediated DNA-Damage response: taking shape. Trends Biochem Sci 2006; 31:402-10; PMID:16774833; http://dx.doi.org/10.1016/j.tibs.2006.05.004.
   PubMed Web of Science ®Google Scholar
• Ciccia A, Elledge SJ. The DNA damage response: making it safe to play with knives. Mol Cell 2010; 40:179-204; PMID:20965415; http://dx.doi.org/10.1016/j.molcel.2010.09.019.
   PubMed Web of Science ®Google Scholar
• Paulsen RD, Cimprich KA. The ATR pathway: fine-tuning the fork. DNA Repair 2007; 6:953-66; PMID:17531546; http://dx.doi.org/10.1016/j.dnarep.2007.02.015.
   PubMed Web of Science ®Google Scholar
• Cimprich KA, Cortez D. ATR: an essential regulator of genome integrity. Nat Rev Mol Cell Biol 2008; 9:616-27; PMID:18594563; http://dx.doi.org/10.1038/nrm2450.
   PubMed Web of Science ®Google Scholar
• Zhao H, Piwnica-Worms H. ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. Mol Cell Biol 2001; 21:4129-39; PMID:11390642; http://dx.doi.org/10.1128/MCB.21.13.4129-4139.2001.
   PubMed Web of Science ®Google Scholar
• Liu Q, Guntuku S, Cui XS, Matsuoka S, Cortez D, Tamai K, Luo G, Carattini-Rivera S, DeMayo F, Bradley A, et al. Chk1 is an essential kinase that is regulated by ATR and required for the G(2)/M DNA damage checkpoint. Genes Devel 2000; 14:1448-59; PMID:10859164; http://dx.doi.org/10.1101/gad.840500.
   PubMed Web of Science ®Google Scholar
• Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 1998; 273:5858-68; PMID:9488723; http://dx.doi.org/10.1074/jbc.273.10.5858.
   PubMed Web of Science ®Google Scholar
• Ziv Y, Jaspers NG, Etkin S, Danieli T, Trakhtenbrot L, Amiel A, Ravia Y, Shiloh Y. Cellular and molecular characteristics of an immortalized ataxia-telangiectasia (group AB) cell line. Cancer Res 1989; 49:2495-501; PMID:2539904.
   PubMed Web of Science ®Google Scholar
• Fokas E, Prevo R, Pollard JR, Reaper PM, Charlton PA, Cornelissen B, Vallis KA, Hammond EM, Olcina MM, Gillies McKenna W, et al. Targeting ATR in vivo using the novel inhibitor VE-822 results in selective sensitization of pancreatic tumors to radiation. Cell Death Dis 2012; 3:e441; PMID:23222511; http://dx.doi.org/10.1038/cddis.2012.181.
   PubMed Web of Science ®Google Scholar
• Zeman MK, Cimprich KA. Causes and consequences of replication stress. Nat Cell Biol 2014; 16:2-9; PMID:24366029; http://dx.doi.org/10.1038/ncb2897.
   PubMed Web of Science ®Google Scholar
• Petermann E, Orta ML, Issaeva N, Schultz N, Helleday T. Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol Cell 2010; 37:492-502; PMID:20188668; http://dx.doi.org/10.1016/j.molcel.2010.01.021.
   PubMed Web of Science ®Google Scholar
• Cifuentes E, Croxen R, Menon M, Barrack ER, Reddy GP. Synchronized prostate cancer cells for studying androgen regulated events in cell cycle progression from G1 into S phase. J Cell Physiol 2003; 195:337-45; PMID:12704643; http://dx.doi.org/10.1002/jcp.10317.
   PubMed Web of Science ®Google Scholar
• Shalhout S, Haddad D, Sosin A, Holland TC, Al-Katib A, Martin A, Bhagwat AS. Genomic uracil homeostasis during normal B cell maturation and loss of this balance during B cell cancer development. Mol Cell Biol 2014; 34:4019-32; PMID:25154417; http://dx.doi.org/10.1128/MCB.00589-14.
   PubMed Web of Science ®Google Scholar
• Leonard B, Hart SN, Burns MB, Carpenter MA, Temiz NA, Rathore A, Vogel RI, Nikas JB, Law EK, Brown WL, et al. APOBEC3B upregulation and genomic mutation patterns in serous ovarian carcinoma. Cancer Res 2013; 73:7222-31; PMID:24154874; http://dx.doi.org/10.1158/0008-5472.CAN-13-1753.
   PubMed Web of Science ®Google Scholar
• Roberts SA, Lawrence MS, Klimczak LJ, Grimm SA, Fargo D, Stojanov P, Kiezun A, Kryukov GV, Carter SL, Saksena G, et al. An APOBEC cytidine deaminase mutagenesis pattern is widespread in human cancers. Nat Genet 2013; 45:970-6; PMID:23852170; http://dx.doi.org/10.1038/ng.2702.
   PubMed Web of Science ®Google Scholar
• Chan K, Roberts SA, Klimczak LJ, Sterling JF, Saini N, Malc EP, Kim J, Kwiatkowski DJ, Fargo DC, Mieczkowski PA, et al. An APOBEC3A hypermutation signature is distinguishable from the signature of background mutagenesis by APOBEC3B in human cancers. Nat Genet 2015; 47(9):1067-72.
   PubMed Web of Science ®Google Scholar
• Ramiro AR, Stavropoulos P, Jankovic M, Nussenzweig MC. Transcription enhances AID-mediated cytidine deamination by exposing single-stranded DNA on the nontemplate strand. Nat Immunol 2003; 4:452-6; PMID:12692548; http://dx.doi.org/10.1038/ni920.
   PubMed Web of Science ®Google Scholar
• Sohail A, Klapacz J, Samaranayake M, Ullah A, Bhagwat AS. Human activation-induced cytidine deaminase causes transcription-dependent, strand-biased C to U deaminations. Nucleic Acids Res 2003; 31:2990-4; PMID:12799424; http://dx.doi.org/10.1093/nar/gkg464.
   PubMed Web of Science ®Google Scholar
• Love RP, Xu H, Chelico L. Biochemical analysis of hypermutation by the deoxycytidine deaminase APOBEC3A. J Biol Chem 2012; 287:30812-22; PMID:22822074; http://dx.doi.org/10.1074/jbc.M112.393181.
   PubMed Web of Science ®Google Scholar
• Zou L, Liu D, Elledge SJ. Replication protein A-mediated recruitment and activation of Rad17 complexes. Proc Natl Acad Sci USA 2003; 100:13827-32; PMID:14605214; http://dx.doi.org/10.1073/pnas.2336100100.
   PubMed Web of Science ®Google Scholar
• Krokan HE, Bjoras M. Base excision repair. Cold Spring Harb Perspect Biol 2013; 5:a012583; PMID:23545420; http://dx.doi.org/10.1101/cshperspect.a012583.
   PubMed Web of Science ®Google Scholar
• Krokan HE, Saetrom P, Aas PA, Pettersen HS, Kavli B, Slupphaug G. Error-free vs. mutagenic processing of genomic uracil–relevance to cancer. DNA Repair 2014; 19:38-47; PMID:24746924; http://dx.doi.org/10.1016/j.dnarep.2014.03.028.
   PubMed Web of Science ®Google Scholar
• Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144:646-74; PMID:21376230; http://dx.doi.org/10.1016/j.cell.2011.02.013.
   PubMed Web of Science ®Google Scholar
• Everett RD, Parsy ML, Orr A. Analysis of the functions of herpes simplex virus type 1 regulatory protein ICP0 that are critical for lytic infection and derepression of quiescent viral genomes. J Virol 2009; 83:4963-77; PMID:19264778; http://dx.doi.org/10.1128/JVI.02593-08.
   PubMed Web of Science ®Google Scholar
• Shin KJ, Wall EA, Zavzavadjian JR, Santat LA, Liu J, Hwang JI, Rebres R, Roach T, Seaman W, Simon MI, et al. A single lentiviral vector platform for microRNA-based conditional RNA interference and coordinated transgene expression. Proc Natl Acad Sci USA 2006; 103:13759-64; PMID:16945906; http://dx.doi.org/10.1073/pnas.0606179103.
   PubMed Web of Science ®Google Scholar
• Langan TJ, Chou RC. Synchronization of mammalian cell cultures by serum deprivation. Methods Mol Biol 2011; 761:75-83; PMID:21755442; http://dx.doi.org/10.1007/978-1-61779-182-6_5.
   PubMedGoogle Scholar