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DNA Repair Polymerases

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Nucleic Acid Polymerases

Part of the book series: Nucleic Acids and Molecular Biology ((NUCLEIC,volume 30))

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Abstract

The nuclear and mitochondrial genomes are under constant attack from endogenous (metabolic) and exogenous genotoxins. The resulting genomic insults include damaged bases and nucleotides, deoxyribo- and ribonucleotide misincorporation, intra-strand and interstrand DNA cross-links, and single-strand and double-strand DNA breaks. As expected, efficient recognition and removal of these genotoxic lesions is critical to begin the repair process and restore genome integrity. With the exception of direct reversal mechanisms, repair of both the nuclear and mitochondrial genomes requires DNA synthesis to replace the nucleotides or DNA strands removed during the repair process. Whereas some DNA repair pathways co-opt replicative DNA polymerases to synthesize the DNA in the “repair patch,” other DNA repair pathways have dedicated DNA polymerase enzymes. This chapter will detail the DNA polymerases central to the major mammalian DNA repair pathways and, where applicable, highlight the unique roles these DNA polymerases may play in protecting normal cells from mutagenic or genotoxic agents and in providing resistance to genotoxic chemotherapeutic treatments.

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Abbreviations

5′dRP:

5′-deoxyribose phosphate

8-oxodG:

8-oxo-7,8-dihydro-2′-deoxyguanosine

AP:

Apurinic/apyrimidinic

APE1:

Apurinic/apyrimidinic endonuclease

BER:

Base excision repair

dsDNA:

Double-stranded DNA

FEN1:

Structure-specific flap endonuclease 1

HR:

Homologous recombination

KO:

Knockout

LigI:

DNA ligase I

LigIII:

DNA ligase III

MEF:

Mouse embryonic fibroblast

MGMT:

O6-methylguanine-DNA methyltransferase

MMR:

Mismatch repair

NER:

Nucleotide excision repair

NHEJ:

Nonhomologous end joining

PARP1:

Poly(ADP-ribose)polymerase-1

PARP2:

Poly(ADP-ribose)polymerase-2

PCNA:

Proliferating cell nuclear antigen

Polκ:

DNA polymerase kappa

Polλ:

DNA polymerase lambda

Polβ:

DNA polymerase beta

Polα:

DNA polymerase alpha

Polγ:

DNA polymerase gamma

Polδ:

DNA polymerase delta

Polη:

DNA polymerase eta

Polθ:

DNA polymerase theta

Polι:

DNA polymerase iota

Polκ:

DNA polymerase kappa

Polμ:

DNA polymerase mu

RFC:

Replication factor C

RNS:

Reactive nitrogen species

ROS:

Reactive oxygen species

SSBs:

Single-strand breaks

ssDNA:

Single-stranded DNA

TdT:

Terminal deoxynucleotidyltransferase

UV:

Ultraviolet

WRN:

Werner syndrome protein helicase

References

  • Aboussekhra A, Biggerstaff M, Shivji MK, Vilpo JA, Moncollin V, Podust VN, Protic M, Hubscher U, Egly JM, Wood RD (1995) Mammalian DNA nucleotide excision repair reconstituted with purified protein components. Cell 80(6):859–868

    PubMed  CAS  Google Scholar 

  • Ahnesorg P, Smith P, Jackson SP (2006) XLF interacts with the XRCC4-DNA ligase IV complex to promote DNA nonhomologous end-joining. Cell 124(2):301–313. doi:10.1016/j.cell.2005.12.031

    PubMed  CAS  Google Scholar 

  • Akopiants K, Zhou RZ, Mohapatra S, Valerie K, Lees-Miller SP, Lee KJ, Chen DJ, Revy P, de Villartay JP, Povirk LF (2009) Requirement for XLF/Cernunnos in alignment-based gap filling by DNA polymerases lambda and mu for nonhomologous end joining in human whole-cell extracts. Nucleic Acids Res 37(12):4055–4062. doi:10.1093/nar/gkp283

    PubMed  CAS  Google Scholar 

  • Albertson TM, Ogawa M, Bugni JM, Hays LE, Chen Y, Wang Y, Treuting PM, Heddle JA, Goldsby RE, Preston BD (2009) DNA polymerase epsilon and delta proofreading suppress discrete mutator and cancer phenotypes in mice. Proc Natl Acad Sci USA 106(40):17101–17104. doi:10.1073/pnas.0907147106

    PubMed  CAS  Google Scholar 

  • Almeida KH, Sobol RW (2005) Increased specificity and efficiency of base excision repair through complex formation. In: Siede W, Doetsch PW, Kow YW (eds) DNA damage recognition. Marcel Dekker, New York, pp 33–64

    Google Scholar 

  • Almeida KH, Sobol RW (2007) A unified view of base excision repair: lesion-dependent protein complexes regulated by post-translational modification. DNA Repair 6(6):695–711

    PubMed  CAS  Google Scholar 

  • An CL, Chen D, Makridakis NM (2011) Systematic biochemical analysis of somatic missense mutations in DNA polymerase beta found in prostate cancer reveal alteration of enzymatic function. Hum Mutat 32(4):415–423. doi:10.1002/humu.21465

    PubMed  CAS  Google Scholar 

  • Anderson RS, Lawrence CB, Wilson SH, Beattie KL (1987) Genetic relatedness of human DNA polymerase beta and terminal deoxynucleotidyltransferase. Gene 60(2–3):163–173

    PubMed  CAS  Google Scholar 

  • Andres SN, Vergnes A, Ristic D, Wyman C, Modesti M, Junop M (2012) A human XRCC4-XLF complex bridges DNA. Nucleic Acids Res 40(4):1868–1878. doi:10.1093/nar/gks022

    PubMed  CAS  Google Scholar 

  • Aoufouchi S, Flatter E, Dahan A, Faili A, Bertocci B, Storck S, Delbos F, Cocea L, Gupta N, Weill JC, Reynaud CA (2000) Two novel human and mouse DNA polymerases of the polX family. Nucleic Acids Res 28(18):3684–3693

    PubMed  CAS  Google Scholar 

  • Arana ME, Kunkel TA (2010) Mutator phenotypes due to DNA replication infidelity. Semin Cancer Biol 20(5):304–311. doi:10.1016/j.semcancer.2010.10.003

    PubMed  CAS  Google Scholar 

  • Araujo SJ, Tirode F, Coin F, Pospiech H, Syvaoja JE, Stucki M, Hubscher U, Egly JM, Wood RD (2000) Nucleotide excision repair of DNA with recombinant human proteins: definition of the minimal set of factors, active forms of TFIIH, and modulation by CAK. Genes Dev 14(3):349–359

    PubMed  CAS  Google Scholar 

  • Barakat KH, Gajewski MM, Tuszynski JA (2012) DNA polymerase beta (pol beta) inhibitors: a comprehensive overview. Drug Discov Today 17(15–16):913–920. doi:10.1016/j.drudis.2012.04.008

    PubMed  CAS  Google Scholar 

  • Barzel A, Kupiec M (2008) Finding a match: how do homologous sequences get together for recombination? Nat Rev Genet 9(1):27–37. doi:10.1038/nrg2224

    PubMed  CAS  Google Scholar 

  • Batra VK, Beard WA, Shock DD, Krahn JM, Pedersen LC, Wilson SH (2006) Magnesium-induced assembly of a complete DNA polymerase catalytic complex. Structure 14(4):757–766. doi:10.1016/j.str.2006.01.011

    PubMed  CAS  Google Scholar 

  • Baute J, Depicker A (2008) Base excision repair and its role in maintaining genome stability. Crit Rev Biochem Mol Biol 43(4):239–276. doi:10.1080/10409230802309905

    PubMed  CAS  Google Scholar 

  • Beard WA, Wilson SH (2006) Structure and mechanism of DNA polymerase beta. Chem Rev 106(2):361–382

    PubMed  CAS  Google Scholar 

  • Bebenek K, Kunkel TA (2004) Functions of DNA polymerases. Adv Protein Chem 69:137–165. doi:10.1016/S0065-3233(04)69005-X

    PubMed  CAS  Google Scholar 

  • Bebenek K, Tissier A, Frank EG, McDonald JP, Prasad R, Wilson SH, Woodgate R, Kunkel TA (2001) 5′-Deoxyribose phosphate lyase activity of human DNA polymerase iota in vitro. Science 291(5511):2156–2159

    PubMed  CAS  Google Scholar 

  • Bebenek K, Garcia-Diaz M, Blanco L, Kunkel TA (2003) The frameshift infidelity of human DNA polymerase lambda. Implications for function. J Biol Chem 278(36):34685–34690. doi:10.1074/jbc.M305705200

    PubMed  CAS  Google Scholar 

  • Begg A (2010) POLQ in breast cancer. Oncotarget 1(3):161–162

    PubMed  Google Scholar 

  • Benedict CL, Gilfillan S, Thai TH, Kearney JF (2000) Terminal deoxynucleotidyl transferase and repertoire development. Immunol Rev 175:150–157

    PubMed  CAS  Google Scholar 

  • Bennett SE, Sung JS, Mosbaugh DW (2001) Fidelity of uracil-initiated base excision DNA repair in DNA polymerase β-proficient and -deficient mouse embryonic fibroblast cell extracts. J Biol Chem 276(45):42588–42600

    PubMed  CAS  Google Scholar 

  • Bertocci B, De Smet A, Flatter E, Dahan A, Bories JC, Landreau C, Weill JC, Reynaud CA (2002) Cutting edge: DNA polymerases mu and lambda are dispensable for Ig gene hypermutation. J Immunol 168(8):3702–3706

    PubMed  CAS  Google Scholar 

  • Bertocci B, De Smet A, Berek C, Weill JC, Reynaud CA (2003) Immunoglobulin kappa light chain gene rearrangement is impaired in mice deficient for DNA polymerase mu. Immunity 19(2):203–211

    PubMed  CAS  Google Scholar 

  • Bertocci B, De Smet A, Weill JC, Reynaud CA (2006) Nonoverlapping functions of DNA polymerases mu, lambda, and terminal deoxynucleotidyltransferase during immunoglobulin V(D)J recombination in vivo. Immunity 25(1):31–41. doi:10.1016/j.immuni.2006.04.013

    PubMed  CAS  Google Scholar 

  • Biade S, Sobol RW, Wilson SH, Matsumoto Y (1998) Impairment of proliferating cell nuclear antigen-dependent apurinic/apyrimidinic site repair on linear DNA. J Biol Chem 273(2):898–902

    PubMed  CAS  Google Scholar 

  • Blank A, Kim B, Loeb LA (1994) DNA polymerase delta is required for base excision repair of DNA methylation damage in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 91(19):9047–9051

    PubMed  CAS  Google Scholar 

  • Boboila C, Alt FW, Schwer B (2012) Classical and alternative end-joining pathways for repair of lymphocyte-specific and general DNA double-strand breaks. Adv Immunol 116:1–49. doi:10.1016/B978-0-12-394300-2.00001-6

    PubMed  CAS  Google Scholar 

  • Bogenhagen DF, Pinz KG, Perez-Jannotti RM (2001) Enzymology of mitochondrial base excision repair. Prog Nucleic Acid Res Mol Biol 68:257–271

    PubMed  CAS  Google Scholar 

  • Bordeianu G, Zugun-Eloae F, Rusu MG (2011) The role of DNA repair by homologous recombination in oncogenesis. Rev Med Chir Soc Med Nat Iasi 115(4):1189–1194

    PubMed  Google Scholar 

  • Boubakour-Azzouz I, Bertrand P, Claes A, Lopez BS, Rougeon F (2012) Terminal deoxynucleotidyl transferase requires KU80 and XRCC4 to promote N-addition at non-V(D)J chromosomal breaks in non-lymphoid cells. Nucleic Acids Res 40(17):8381–8391. doi:10.1093/nar/gks585

    PubMed  CAS  Google Scholar 

  • Braithwaite EK, Kedar PS, Lan L, Polosina YY, Asagoshi K, Poltoratsky VP, Horton JK, Miller H, Teebor GW, Yasui A, Wilson SH (2005a) DNA polymerase lambda protects mouse fibroblasts against oxidative DNA damage and is recruited to sites of DNA damage/repair. J Biol Chem 280(36):31641–31647

    PubMed  CAS  Google Scholar 

  • Braithwaite EK, Prasad R, Shock DD, Hou EW, Beard WA, Wilson SH (2005b) DNA polymerase lambda mediates a back-up base excision repair activity in extracts of mouse embryonic fibroblasts. J Biol Chem 280(18):18469–18475

    PubMed  CAS  Google Scholar 

  • Braithwaite EK, Kedar PS, Stumpo DJ, Bertocci B, Freedman JH, Samson LD, Wilson SH (2010) DNA polymerases beta and lambda mediate overlapping and independent roles in base excision repair in mouse embryonic fibroblasts. PLoS One 5(8):e12229

    PubMed  Google Scholar 

  • Brandsma I, Gent DC (2012) Pathway choice in DNA double strand break repair: observations of a balancing act. Genome Integr 3(1):9. doi:10.1186/2041-9414-3-9

    PubMed  CAS  Google Scholar 

  • Brown JA, Duym WW, Fowler JD, Suo Z (2007) Single-turnover kinetic analysis of the mutagenic potential of 8-oxo-7,8-dihydro-2′-deoxyguanosine during gap-filling synthesis catalyzed by human DNA polymerases lambda and beta. J Mol Biol 367(5):1258–1269. doi:10.1016/j.jmb.2007.01.069

    PubMed  CAS  Google Scholar 

  • Brown JA, Pack LR, Sanman LE, Suo Z (2011) Efficiency and fidelity of human DNA polymerases lambda and beta during gap-filling DNA synthesis. DNA Repair (Amst) 10(1):24–33. doi:10.1016/j.dnarep.2010.09.005

    CAS  Google Scholar 

  • Buck D, Malivert L, de Chasseval R, Barraud A, Fondaneche MC, Sanal O, Plebani A, Stephan JL, Hufnagel M, le Deist F, Fischer A, Durandy A, de Villartay JP, Revy P (2006) Cernunnos, a novel nonhomologous end-joining factor, is mutated in human immunodeficiency with microcephaly. Cell 124(2):287–299. doi:10.1016/j.cell.2005.12.030

    PubMed  CAS  Google Scholar 

  • Burgers PM, Koonin EV, Bruford E, Blanco L, Burtis KC, Christman MF, Copeland WC, Friedberg EC, Hanaoka F, Hinkle DC, Lawrence CW, Nakanishi M, Ohmori H, Prakash L, Prakash S, Reynaud CA, Sugino A, Todo T, Wang Z, Weill JC, Woodgate R (2001) Eukaryotic DNA polymerases: proposal for a revised nomenclature. J Biol Chem 276(47):43487–43490

    PubMed  CAS  Google Scholar 

  • Byrnes JJ, Downey KM, Black VL, So AG (1976) A new mammalian DNA polymerase with 3′ to 5′ exonuclease activity: DNA polymerase delta. Biochemistry 15(13):2817–2823

    PubMed  CAS  Google Scholar 

  • Cabelof DC, Guo Z, Raffoul JJ, Sobol RW, Wilson SH, Richardson A, Heydari AR (2003) Base excision repair deficiency caused by polymerase β haploinsufficiency: accelerated DNA damage and increased mutational response to carcinogens. Cancer Res 63(18):5799–5807

    PubMed  CAS  Google Scholar 

  • Cabelof DC, Raffoul JJ, Nakamura J, Kapoor D, Abdalla H, Heydari AR (2004) Imbalanced base excision repair in response to folate deficiency is accelerated by polymerase beta haploinsufficiency. J Biol Chem 279(35):36504–36513

    PubMed  CAS  Google Scholar 

  • Capp JP, Boudsocq F, Besnard AG, Lopez BS, Cazaux C, Hoffmann JS, Canitrot Y (2007) Involvement of DNA polymerase mu in the repair of a specific subset of DNA double-strand breaks in mammalian cells. Nucleic Acids Res 35(11):3551–3560. doi:10.1093/nar/gkm243

    PubMed  CAS  Google Scholar 

  • Cavero S, Chahwan C, Russell P (2007) Xlf1 is required for DNA repair by nonhomologous end joining in Schizosaccharomyces pombe. Genetics 175(2):963–967. doi:10.1534/genetics.106.067850

    PubMed  CAS  Google Scholar 

  • Chapman JR, Taylor MR, Boulton SJ (2012) Playing the end game: DNA double-strand break repair pathway choice. Mol Cell 47(4):497–510. doi:10.1016/j.molcel.2012.07.029

    PubMed  CAS  Google Scholar 

  • Chayot R, Danckaert A, Montagne B, Ricchetti M (2010) Lack of DNA polymerase mu affects the kinetics of DNA double-strand break repair and impacts on cellular senescence. DNA Repair (Amst) 9(11):1187–1199. doi:10.1016/j.dnarep.2010.09.001

    CAS  Google Scholar 

  • Chayot R, Montagne B, Ricchetti M (2012) DNA polymerase mu is a global player in the repair of non-homologous end-joining substrates. DNA Repair (Amst) 11(1):22–34. doi:10.1016/j.dnarep.2011.09.016

    CAS  Google Scholar 

  • Costantini S, Woodbine L, Andreoli L, Jeggo PA, Vindigni A (2007) Interaction of the Ku heterodimer with the DNA ligase IV/Xrcc4 complex and its regulation by DNA-PK. DNA Repair (Amst) 6(6):712–722. doi:10.1016/j.dnarep.2006.12.007

    CAS  Google Scholar 

  • Coverley D, Kenny MK, Lane DP, Wood RD (1992) A role for the human single-stranded DNA binding protein HSSB/RPA in an early stage of nucleotide excision repair. Nucleic Acids Res 20(15):3873–3880

    PubMed  CAS  Google Scholar 

  • Crespan E, Czabany T, Maga G, Hubscher U (2012) Microhomology-mediated DNA strand annealing and elongation by human DNA polymerases lambda and beta on normal and repetitive DNA sequences. Nucleic Acids Res 40(12):5577–5590. doi:10.1093/nar/gks186

    PubMed  CAS  Google Scholar 

  • Cui J, Zhao W, Xu X, Yang M, Ren Y, Zhang Z (2012) DNA polymerase beta is involved in the protection against the cytotoxicity and genotoxicity of cigarette smoke. Environ Toxicol Pharmacol 34(2):370–380. doi:10.1016/j.etap.2012.05.012

    PubMed  CAS  Google Scholar 

  • Curtin NJ (2012) DNA repair dysregulation from cancer driver to therapeutic target. Nat Rev Cancer 12(12):801–817. doi:10.1038/nrc3399

    PubMed  CAS  Google Scholar 

  • Dalal S, Chikova A, Jaeger J, Sweasy JB (2008) The Leu22Pro tumor-associated variant of DNA polymerase beta is dRP lyase deficient. Nucleic Acids Res 36(2):411–422

    PubMed  CAS  Google Scholar 

  • David SS, O’Shea VL, Kundu S (2007) Base-excision repair of oxidative DNA damage. Nature 447(7147):941–950. doi:10.1038/nature05978, nature05978 [pii]

    PubMed  CAS  Google Scholar 

  • de Laat WL, Jaspers NG, Hoeijmakers JH (1999) Molecular mechanism of nucleotide excision repair. Genes Dev 13(7):768–785

    PubMed  Google Scholar 

  • de Vries A, van Oostrom CT, Hofhuis FM, Dortant PM, Berg RJ, de Gruijl FR, Wester PW, van Kreijl CF, Capel PJ, van Steeg H, Verbeek SJ (1995) Increased susceptibility to ultraviolet-B and carcinogens of mice lacking the DNA excision repair gene XPA. Nature 377(6545):169–173. doi:10.1038/377169a0

    PubMed  Google Scholar 

  • Deans AJ, West SC (2011) DNA interstrand crosslink repair and cancer. Nat Rev Cancer 11(7):467–480. doi:10.1038/nrc3088

    PubMed  CAS  Google Scholar 

  • DeMott MS, Zigman S, Bambara RA (1998) Replication protein A stimulates long patch DNA base excision repair. J Biol Chem 273(42):27492–27498

    PubMed  CAS  Google Scholar 

  • DeRose EF, Kirby TW, Mueller GA, Bebenek K, Garcia-Diaz M, Blanco L, Kunkel TA, London RE (2003) Solution structure of the lyase domain of human DNA polymerase lambda. Biochemistry 42(32):9564–9574. doi:10.1021/bi034298s

    PubMed  CAS  Google Scholar 

  • DeRose EF, Clarkson MW, Gilmore SA, Galban CJ, Tripathy A, Havener JM, Mueller GA, Ramsden DA, London RE, Lee AL (2007) Solution structure of polymerase mu’s BRCT Domain reveals an element essential for its role in nonhomologous end joining. Biochemistry 46(43):12100–12110. doi:10.1021/bi7007728

    PubMed  CAS  Google Scholar 

  • Dianov G, Price A, Lindahl T (1992) Generation of single-nucleotide repair patches following excision of uracil residues from DNA. Mol Cell Biol 12(4):1605–1612

    PubMed  CAS  Google Scholar 

  • Dianov GL, Prasad R, Wilson SH, Bohr VA (1999) Role of DNA polymerase β in the excision step of long patch mammalian base excision repair. J Biol Chem 274(20):13741–13743

    PubMed  CAS  Google Scholar 

  • DiGiuseppe JA, Dresler SL (1989) Bleomycin-induced DNA repair synthesis in permeable human fibroblasts: mediation of long-patch and short-patch repair by distinct DNA polymerases. Biochemistry 28(24):9515–9520

    PubMed  CAS  Google Scholar 

  • Doherty AJ, Jackson SP (2001) DNA repair: how Ku makes ends meet. Curr Biol 11(22):R920–R924

    PubMed  CAS  Google Scholar 

  • Dominguez O, Ruiz JF, Lain de Lera T, Garcia-Diaz M, Gonzalez MA, Kirchhoff T, Martinez AC, Bernad A, Blanco L (2000) DNA polymerase mu, homologous to TdT, could act as a DNA mutator in eukaryotic cells. EMBO J 19(7):1731–1742

    PubMed  CAS  Google Scholar 

  • Donigan KA, Sun KW, Nemec AA, Murphy DL, Cong X, Northrup V, Zelterman D, Sweasy JB (2012) Human POLB gene is mutated in high percentage of colorectal tumors. J Biol Chem 287(28):23830–23839. doi:10.1074/jbc.M111.324947

    PubMed  CAS  Google Scholar 

  • Downs JA, Nussenzweig MC, Nussenzweig A (2007) Chromatin dynamics and the preservation of genetic information. Nature 447(7147):951–958. doi:10.1038/nature05980

    PubMed  CAS  Google Scholar 

  • El-Andaloussi N, Valovka T, Toueille M, Steinacher R, Focke F, Gehrig P, Covic M, Hassa PO, Schar P, Hubscher U, Hottiger MO (2006) Arginine methylation regulates DNA polymerase β. Mol Cell 22(1):51–62

    PubMed  CAS  Google Scholar 

  • El-Andaloussi N, Valovka T, Toueille M, Hassa PO, Gehrig P, Covic M, Hubscher U, Hottiger MO (2007) Methylation of DNA polymerase beta by protein arginine methyltransferase 1 regulates its binding to proliferating cell nuclear antigen. FASEB J 21(1):26–34

    PubMed  CAS  Google Scholar 

  • Enoiu M, Jiricny J, Scharer OD (2012) Repair of cisplatin-induced DNA interstrand crosslinks by a replication-independent pathway involving transcription-coupled repair and translesion synthesis. Nucleic Acids Res 40(18):8953–8964. doi:10.1093/nar/gks670

    PubMed  CAS  Google Scholar 

  • Esposito G, Texido G, Betz UA, Gu H, Muller W, Klein U, Rajewsky K (2000) Mice reconstituted with DNA polymerase β-deficient fetal liver cells are able to mount a T cell-dependent immune response and mutate their Ig genes normally. Proc Natl Acad Sci USA 97(3):1166–1171

    PubMed  CAS  Google Scholar 

  • Fabre F, Boulet A, Faye G (1991) Possible involvement of the yeast POLIII DNA polymerase in induced gene conversion. Mol Gen Genet 229(3):353–356

    PubMed  CAS  Google Scholar 

  • Fan W, Wu X (2004) DNA polymerase lambda can elongate on DNA substrates mimicking non-homologous end joining and interact with XRCC4-ligase IV complex. Biochem Biophys Res Commun 323(4):1328–1333. doi:10.1016/j.bbrc.2004.09.002

    PubMed  CAS  Google Scholar 

  • Fortini P, Pascucci B, Parlanti E, Sobol RW, Wilson SH, Dogliotti E (1998) Different DNA polymerases are involved in the short- and long-patch base excision repair in mammalian cells. Biochemistry 37(11):3575–3580

    PubMed  CAS  Google Scholar 

  • Fortini P, Parlanti E, Sidorkina OM, Laval J, Dogliotti E (1999) The type of DNA glycosylase determines the base excision repair pathway in mammalian cells. J Biol Chem 274(21):15230–15236

    PubMed  CAS  Google Scholar 

  • Friedberg EC, Meira LB (2006) Database of mouse strains carrying targeted mutations in genes affecting biological responses to DNA damage Version 7. DNA Repair (Amst) 5(2):189–209

    CAS  Google Scholar 

  • Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, Ellenberger T (2006) DNA repair and mutagenesis, 2nd edn. ASM Press, Washington, DC

    Google Scholar 

  • Frouin I, Toueille M, Ferrari E, Shevelev I, Hubscher U (2005) Phosphorylation of human DNA polymerase lambda by the cyclin-dependent kinase Cdk2/cyclin A complex is modulated by its association with proliferating cell nuclear antigen. Nucleic Acids Res 33(16):5354–5361

    PubMed  CAS  Google Scholar 

  • Fu D, Calvo JA, Samson LD (2012) Balancing repair and tolerance of DNA damage caused by alkylating agents. Nat Rev Cancer 12(2):104–120. doi:10.1038/nrc3185

    PubMed  CAS  Google Scholar 

  • Gao Y, Katyal S, Lee Y, Zhao J, Rehg JE, Russell HR, McKinnon PJ (2011) DNA ligase III is critical for mtDNA integrity but not Xrcc1-mediated nuclear DNA repair. Nature 471(7337):240–244. doi:10.1038/nature09773

    PubMed  CAS  Google Scholar 

  • Garcia-Diaz M, Dominguez O, Lopez-Fernandez LA, de Lera LT, Saniger ML, Ruiz JF, Parraga M, Garcia-Ortiz MJ, Kirchhoff T, del Mazo J, Bernad A, Blanco L (2000) DNA polymerase lambda (Pol lambda), a novel eukaryotic DNA polymerase with a potential role in meiosis. J Mol Biol 301(4):851–867. doi:10.1006/jmbi.2000.4005

    PubMed  CAS  Google Scholar 

  • Garcia-Diaz M, Bebenek K, Kunkel TA, Blanco L (2001) Identification of an intrinsic 5′-deoxyribose-5-phosphate lyase activity in human DNA polymerase lambda: a possible role in base excision repair. J Biol Chem 276(37):34659–34663

    PubMed  CAS  Google Scholar 

  • Garcia-Diaz M, Bebenek K, Sabariegos R, Dominguez O, Rodriguez J, Kirchhoff T, Garcia-Palomero E, Picher AJ, Juarez R, Ruiz JF, Kunkel TA, Blanco L (2002) DNA polymerase lambda, a novel DNA repair enzyme in human cells. J Biol Chem 277(15):13184–13191. doi:10.1074/jbc.M111601200

    PubMed  CAS  Google Scholar 

  • Garcia-Diaz M, Bebenek K, Krahn JM, Blanco L, Kunkel TA, Pedersen LC (2004) A structural solution for the DNA polymerase lambda-dependent repair of DNA gaps with minimal homology. Mol Cell 13(4):561–572

    PubMed  CAS  Google Scholar 

  • Garcia-Diaz M, Bebenek K, Gao G, Pedersen LC, London RE, Kunkel TA (2005) Structure-function studies of DNA polymerase lambda. DNA Repair (Amst) 4(12):1358–1367

    CAS  Google Scholar 

  • Gary R, Kim K, Cornelius HL, Park MS, Matsumoto Y (1999) Proliferating cell nuclear antigen facilitates excision in long-patch base excision repair. J Biol Chem 274(7):4354–4363

    PubMed  CAS  Google Scholar 

  • Gell D, Jackson SP (1999) Mapping of protein-protein interactions within the DNA-dependent protein kinase complex. Nucleic Acids Res 27(17):3494–3502

    PubMed  CAS  Google Scholar 

  • Gillet LC, Scharer OD (2006) Molecular mechanisms of mammalian global genome nucleotide excision repair. Chem Rev 106(2):253–276. doi:10.1021/cr040483f

    PubMed  CAS  Google Scholar 

  • Giot L, Chanet R, Simon M, Facca C, Faye G (1997) Involvement of the yeast DNA polymerase delta in DNA repair in vivo. Genetics 146(4):1239–1251

    PubMed  CAS  Google Scholar 

  • Goellner EM, Grimme B, Brown AR, Lin YC, Wang XH, Sugrue KF, Mitchell L, Trivedi RN, Tang JB, Sobol RW (2011) Overcoming temozolomide resistance in glioblastoma via dual inhibition of NAD+ biosynthesis and base excision repair. Cancer Res 71(6):2308–2317. doi:10.1158/0008-5472.CAN-10-3213

    PubMed  CAS  Google Scholar 

  • Goellner EM, Svilar D, Almeida KH, Sobol RW (2012) Targeting DNA polymerase β for therapeutic intervention. Curr Mol Pharmacol 5(1):68–87

    PubMed  CAS  Google Scholar 

  • Goff JP, Shields DS, Seki M, Choi S, Epperly MW, Dixon T, Wang H, Bakkenist CJ, Dertinger SD, Torous DK, Wittschieben J, Wood RD, Greenberger JS (2009) Lack of DNA polymerase theta (POLQ) radiosensitizes bone marrow stromal cells in vitro and increases reticulocyte micronuclei after total-body irradiation. Radiat Res 172(2):165–174. doi:10.1667/RR1598.1

    PubMed  CAS  Google Scholar 

  • Gonda H, Sugai M, Katakai T, Sugo N, Aratani Y, Koyama H, Mori KJ, Shimizu A (2001) DNA polymerase β is not essential for the formation of palindromic (P) region of T cell receptor gene. Immunol Lett 78(1):45–49

    PubMed  CAS  Google Scholar 

  • Grundy GJ, Rulten SL, Zeng Z, Arribas-Bosacoma R, Iles N, Manley K, Oliver A, Caldecott KW (2013) APLF promotes the assembly and activity of non-homologous end joining protein complexes. EMBO J 32:112–125. doi:10.1038/emboj.2012.304

    PubMed  CAS  Google Scholar 

  • Gu H, Marth JD, Orban PC, Mossmann H, Rajewsky K (1994) Deletion of a DNA polymerase β gene segment in T cells using cell type-specific gene targeting. Science 265(5168):103–106

    PubMed  CAS  Google Scholar 

  • Guo A, Villen J, Kornhauser J, Lee KA, Stokes MP, Rikova K, Possemato A, Nardone J, Innocenti G, Wetzel R, Wang Y, MacNeill J, Mitchell J, Gygi SP, Rush J, Polakiewicz RD, Comb MJ (2008) Signaling networks assembled by oncogenic EGFR and c-Met. Proc Natl Acad Sci USA 105(2):692–697

    PubMed  CAS  Google Scholar 

  • Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144(5):646–674. doi:10.1016/j.cell.2011.02.013

    PubMed  CAS  Google Scholar 

  • Hanawalt PC, Spivak G (2008) Transcription-coupled DNA repair: two decades of progress and surprises. Nat Rev Mol Cell Biol 9(12):958–970. doi:10.1038/nrm2549

    PubMed  CAS  Google Scholar 

  • Harper JW, Elledge SJ (2007) The DNA damage response: ten years after. Mol Cell 28(5):739–745. doi:10.1016/j.molcel.2007.11.015

    PubMed  CAS  Google Scholar 

  • Harrigan JA, Opresko PL, von Kobbe C, Kedar PS, Prasad R, Wilson SH, Bohr VA (2003) The Werner syndrome protein stimulates DNA polymerase β strand displacement synthesis via its helicase activity. J Biol Chem 278(25):22686–22695

    PubMed  CAS  Google Scholar 

  • Harrigan JA, Wilson DM 3rd, Prasad R, Opresko PL, Beck G, May A, Wilson SH, Bohr VA (2006) The Werner syndrome protein operates in base excision repair and cooperates with DNA polymerase beta. Nucleic Acids Res 34(2):745–754

    PubMed  CAS  Google Scholar 

  • Hasan S, El-Andaloussi N, Hardeland U, Hassa PO, Burki C, Imhof R, Schar P, Hottiger MO (2002) Acetylation regulates the DNA end-trimming activity of DNA polymerase β. Mol Cell 10(5):1213–1222

    PubMed  CAS  Google Scholar 

  • Hegde ML, Hegde PM, Rao KS, Mitra S (2011) Oxidative genome damage and its repair in neurodegenerative diseases: function of transition metals as a double-edged sword. J Alzheimers Dis 24(Suppl 2):183–198. doi:10.3233/JAD-2011-110281

    PubMed  CAS  Google Scholar 

  • Higgins GS, Harris AL, Prevo R, Helleday T, McKenna WG, Buffa FM (2010a) Overexpression of POLQ confers a poor prognosis in early breast cancer patients. Oncotarget 1(3):175–184

    PubMed  Google Scholar 

  • Higgins GS, Prevo R, Lee YF, Helleday T, Muschel RJ, Taylor S, Yoshimura M, Hickson ID, Bernhard EJ, McKenna WG (2010b) A small interfering RNA screen of genes involved in DNA repair identifies tumor-specific radiosensitization by POLQ knockdown. Cancer Res 70(7):2984–2993. doi:10.1158/0008-5472.CAN-09-4040

    PubMed  CAS  Google Scholar 

  • Hinz JM (2010) Role of homologous recombination in DNA interstrand crosslink repair. Environ Mol Mutagen 51(6):582–603. doi:10.1002/em.20577

    PubMed  CAS  Google Scholar 

  • Hlavin EM, Smeaton MB, Noronha AM, Wilds CJ, Miller PS (2010) Cross-link structure affects replication-independent DNA interstrand cross-link repair in mammalian cells. Biochemistry 49(18):3977–3988. doi:10.1021/bi902169q

    PubMed  CAS  Google Scholar 

  • Ho TV, Scharer OD (2010) Translesion DNA synthesis polymerases in DNA interstrand crosslink repair. Environ Mol Mutagen 51(6):552–566. doi:10.1002/em.20573

    PubMed  CAS  Google Scholar 

  • Ho TV, Guainazzi A, Derkunt SB, Enoiu M, Scharer OD (2011) Structure-dependent bypass of DNA interstrand crosslinks by translesion synthesis polymerases. Nucleic Acids Res 39(17):7455–7464. doi:10.1093/nar/gkr448

    PubMed  CAS  Google Scholar 

  • Hoeijmakers JH (2001) Genome maintenance mechanisms for preventing cancer. Nature 411(6835):366–374

    PubMed  CAS  Google Scholar 

  • Hoeijmakers JH (2009) DNA damage, aging, and cancer. N Engl J Med 361(15):1475–1485. doi:10.1056/NEJMra0804615, 361/15/1475 [pii]

    PubMed  CAS  Google Scholar 

  • Horton JK, Baker A, Berg BJ, Sobol RW, Wilson SH (2002) Involvement of DNA polymerase β in protection against the cytotoxicity of oxidative DNA damage. DNA Repair (Amst) 1(4):317–333

    CAS  Google Scholar 

  • Horton JK, Joyce-Gray DF, Pachkowski BF, Swenberg JA, Wilson SH (2003) Hypersensitivity of DNA polymerase beta null mouse fibroblasts reflects accumulation of cytotoxic repair intermediates from site-specific alkyl DNA lesions. DNA Repair (Amst) 2(1):27–48

    CAS  Google Scholar 

  • Horton JK, Stefanick DF, Naron JM, Kedar PS, Wilson SH (2005) Poly(ADP-ribose) polymerase activity prevents signaling pathways for cell cycle arrest following DNA methylating agent exposure. J Biol Chem 280(16):15773–15785

    PubMed  CAS  Google Scholar 

  • Hubscher U (2009) DNA replication fork proteins. Methods Mol Biol 521:19–33. doi:10.1007/978-1-60327-815-7_2

    PubMed  CAS  Google Scholar 

  • Hubscher U, Kuenzle CC, Spadari S (1979) Functional roles of DNA polymerases beta and gamma. Proc Natl Acad Sci USA 76(5):2316–2320

    PubMed  CAS  Google Scholar 

  • Ibe S, Fujita K, Toyomoto T, Shimazaki N, Kaneko R, Tanabe A, Takebe I, Kuroda S, Kobayashi T, Toji S, Tamai K, Yamamoto H, Koiwai O (2001) Terminal deoxynucleotidyltransferase is negatively regulated by direct interaction with proliferating cell nuclear antigen. Genes Cells 6(9):815–824

    PubMed  CAS  Google Scholar 

  • Ishiguro T, Otsuka F, Ochi T, Ohsawa M (1987) Involvement of DNA polymerases in the repair of DNA damage by benzo[a]pyrene in cultured Chinese hamster cells. Mutat Res 184(1):57–63

    PubMed  CAS  Google Scholar 

  • Iwanaga A, Ouchida M, Miyazaki K, Hori K, Mukai T (1999) Functional mutation of DNA polymerase β found in human gastric cancer: inability of the base excision repair in vitro. Mutat Res 435(2):121–128

    PubMed  CAS  Google Scholar 

  • Jackson SP, Bartek J (2009) The DNA-damage response in human biology and disease. Nature 461(7267):1071–1078. doi:10.1038/nature08467

    PubMed  CAS  Google Scholar 

  • Jaiswal AS, Banerjee S, Panda H, Bulkin CD, Izumi T, Sarkar FH, Ostrov DA, Narayan S (2009) A novel inhibitor of DNA polymerase beta enhances the ability of temozolomide to impair the growth of colon cancer cells. Mol Cancer Res 7(12):1973–1983. doi:10.1158/1541-7786.MCR-09-0309

    PubMed  CAS  Google Scholar 

  • Jiricny J (2006) The multifaceted mismatch-repair system. Nat Rev Mol Cell Biol 7(5):335–346

    PubMed  CAS  Google Scholar 

  • Kadyrov FA, Dzantiev L, Constantin N, Modrich P (2006) Endonucleolytic function of MutLalpha in human mismatch repair. Cell 126(2):297–308. doi:10.1016/j.cell.2006.05.039

    PubMed  CAS  Google Scholar 

  • Kanagaraj R, Parasuraman P, Mihaljevic B, van Loon B, Burdova K, Konig C, Furrer A, Bohr VA, Hubscher U, Janscak P (2012) Involvement of Werner syndrome protein in MUTYH-mediated repair of oxidative DNA damage. Nucleic Acids Res 40(17):8449–8459. doi:10.1093/nar/gks648

    PubMed  CAS  Google Scholar 

  • Kass EM, Jasin M (2010) Collaboration and competition between DNA double-strand break repair pathways. FEBS Lett 584(17):3703–3708. doi:10.1016/j.febslet.2010.07.057

    PubMed  CAS  Google Scholar 

  • Kawamoto T, Araki K, Sonoda E, Yamashita YM, Harada K, Kikuchi K, Masutani C, Hanaoka F, Nozaki K, Hashimoto N, Takeda S (2005) Dual roles for DNA polymerase eta in homologous DNA recombination and translesion DNA synthesis. Mol Cell 20(5):793–799. doi:10.1016/j.molcel.2005.10.016

    PubMed  CAS  Google Scholar 

  • Kazak L, Reyes A, Holt IJ (2012) Minimizing the damage: repair pathways keep mitochondrial DNA intact. Nat Rev Mol Cell Biol 13(10):659–671. doi:10.1038/nrm3439

    PubMed  CAS  Google Scholar 

  • Kedar PS, Kim SJ, Robertson A, Hou E, Prasad R, Horton JK, Wilson SH (2002) Direct interaction between mammalian DNA polymerase β and proliferating cell nuclear antigen. J Biol Chem 277(34):31115–31123

    PubMed  CAS  Google Scholar 

  • Kim H, D’Andrea AD (2012) Regulation of DNA cross-link repair by the Fanconi anemia/BRCA pathway. Genes Dev 26(13):1393–1408. doi:10.1101/gad.195248.112

    PubMed  CAS  Google Scholar 

  • Klug AR, Harbut MB, Lloyd RS, Minko IG (2012) Replication bypass of N2-deoxyguanosine interstrand cross-links by human DNA polymerases eta and iota. Chem Res Toxicol 25(3):755–762. doi:10.1021/tx300011w

    PubMed  CAS  Google Scholar 

  • Knutson CG, Akingbade D, Crews BC, Voehler M, Stec DF, Marnett LJ (2007) Metabolism in vitro and in vivo of the DNA base adduct, M1G. Chem Res Toxicol 20(3):550–557. doi:10.1021/tx600334x

    PubMed  CAS  Google Scholar 

  • Knutson CG, Rubinson EH, Akingbade D, Anderson CS, Stec DF, Petrova KV, Kozekov ID, Guengerich FP, Rizzo CJ, Marnett LJ (2009) Oxidation and glycolytic cleavage of etheno and propano DNA base adducts. Biochemistry 48(4):800–809. doi:10.1021/bi801654j

    PubMed  CAS  Google Scholar 

  • Kothandapani A, Patrick SM (2013) Evidence for base excision repair processing of DNA interstrand crosslinks. Mutat Res 743–744:44–52. doi:10.1016/j.mrfmmm.2012.11.007

    PubMed  Google Scholar 

  • Kothandapani A, Dangeti VS, Brown AR, Banze LA, Wang XH, Sobol RW, Patrick SM (2011) Novel role of base excision repair in mediating cisplatin cytotoxicity. J Biol Chem 286(16):14564–14574. doi:10.1074/jbc.M111.225375

    PubMed  CAS  Google Scholar 

  • Krejci L, Altmannova V, Spirek M, Zhao X (2012) Homologous recombination and its regulation. Nucleic Acids Res 40(13):5795–5818. doi:10.1093/nar/gks270

    PubMed  CAS  Google Scholar 

  • Kubota Y, Nash RA, Klungland A, Schar P, Barnes DE, Lindahl T (1996) Reconstitution of DNA base excision-repair with purified human proteins: interaction between DNA polymerase β and the XRCC1 protein. EMBO J 15(23):6662–6670

    PubMed  CAS  Google Scholar 

  • Kunkel TA (2009) Evolving views of DNA replication (in)fidelity. Cold Spring Harb Symp Quant Biol 74:91–101. doi:10.1101/sqb.2009.74.027

    PubMed  CAS  Google Scholar 

  • Kunkel TA, Burgers PM (2008) Dividing the workload at a eukaryotic replication fork. Trends Cell Biol 18(11):521–527. doi:10.1016/j.tcb.2008.08.005

    PubMed  CAS  Google Scholar 

  • Kunkel TA, Erie DA (2005) DNA mismatch repair. Annu Rev Biochem 74:681–710. doi:10.1146/annurev.biochem.74.082803.133243

    PubMed  CAS  Google Scholar 

  • Kunkel TA, Van Houten B (2006) Survival choices. Nat Cell Biol 8(6):547–549. doi:10.1038/ncb0606-547

    PubMed  CAS  Google Scholar 

  • Kuper J, Kisker C (2012) Damage recognition in nucleotide excision DNA repair. Curr Opin Struct Biol 22(1):88–93. doi:10.1016/j.sbi.2011.12.002

    PubMed  CAS  Google Scholar 

  • Lai Y, Zhao W, Chen C, Wu M, Zhang Z (2011) Role of DNA polymerase beta in the genotoxicity of arsenic. Environ Mol Mutagen 52(6):460–468. doi:10.1002/em.20643

    PubMed  CAS  Google Scholar 

  • Lang T, Dalal S, Chikova A, Dimaio D, Sweasy JB (2007) The E295K DNA polymerase beta gastric cancer-associated variant interferes with base excision repair and induces cellular transformation. Mol Cell Biol 27(15):5587–5596

    PubMed  CAS  Google Scholar 

  • Lange SS, Takata K, Wood RD (2011) DNA polymerases and cancer. Nat Rev Cancer 11(2):96–110. doi:10.1038/nrc2998

    PubMed  CAS  Google Scholar 

  • Larrea AA, Lujan SA, Nick McElhinny SA, Mieczkowski PA, Resnick MA, Gordenin DA, Kunkel TA (2010) Genome-wide model for the normal eukaryotic DNA replication fork. Proc Natl Acad Sci USA 107(41):17674–17679. doi:10.1073/pnas.1010178107

    PubMed  CAS  Google Scholar 

  • Le Page F, Schreiber V, Dherin C, De Murcia G, Boiteux S (2003) Poly(ADP-ribose) polymerase-1 (PARP-1) is required in murine cell lines for base excision repair of oxidative DNA damage in the absence of DNA polymerase β. J Biol Chem 278(20):18471–18477

    PubMed  Google Scholar 

  • Lebedeva NA, Rechkunova NI, Dezhurov SV, Khodyreva SN, Favre A, Blanco L, Lavrik OI (2005) Comparison of functional properties of mammalian DNA polymerase lambda and DNA polymerase beta in reactions of DNA synthesis related to DNA repair. Biochim Biophys Acta 1751(2):150–158. doi:10.1016/j.bbapap.2005.05.012

    PubMed  CAS  Google Scholar 

  • Lee JW, Blanco L, Zhou T, Garcia-Diaz M, Bebenek K, Kunkel TA, Wang Z, Povirk LF (2004) Implication of DNA polymerase lambda in alignment-based gap filling for nonhomologous DNA end joining in human nuclear extracts. J Biol Chem 279(1):805–811. doi:10.1074/jbc.M307913200

    PubMed  CAS  Google Scholar 

  • Lehmann AR (2011) DNA polymerases and repair synthesis in NER in human cells. DNA Repair (Amst) 10(7):730–733. doi:10.1016/j.dnarep.2011.04.023

    CAS  Google Scholar 

  • Lemee F, Bergoglio V, Fernandez-Vidal A, Machado-Silva A, Pillaire MJ, Bieth A, Gentil C, Baker L, Martin AL, Leduc C, Lam E, Magdeleine E, Filleron T, Oumouhou N, Kaina B, Seki M, Grimal F, Lacroix-Triki M, Thompson A, Roche H, Bourdon JC, Wood RD, Hoffmann JS, Cazaux C (2010) DNA polymerase theta up-regulation is associated with poor survival in breast cancer, perturbs DNA replication, and promotes genetic instability. Proc Natl Acad Sci USA 107(30):13390–13395. doi:10.1073/pnas.0910759107

    PubMed  CAS  Google Scholar 

  • Li GM (2008) Mechanisms and functions of DNA mismatch repair. Cell Res 18(1):85–98. doi:10.1038/cr.2007.115

    PubMed  CAS  Google Scholar 

  • Li X, Stith CM, Burgers PM, Heyer WD (2009) PCNA is required for initiation of recombination-associated DNA synthesis by DNA polymerase delta. Mol Cell 36(4):704–713. doi:10.1016/j.molcel.2009.09.036

    PubMed  Google Scholar 

  • Li J, Luthra S, Wang XH, Chandran UR, Sobol RW (2012a) Transcriptional profiling reveals elevated Sox2 in DNA polymerase ss null mouse embryonic fibroblasts. Am J Cancer Res 2(6):699–713

    PubMed  CAS  Google Scholar 

  • Li Y, Gridley CL, Jaeger J, Sweasy JB, Schlick T (2012b) Unfavorable electrostatic and steric interactions in DNA polymerase beta E295K mutant interfere with the enzyme’s pathway. J Am Chem Soc 134(24):9999–10010. doi:10.1021/ja300361r

    PubMed  CAS  Google Scholar 

  • Liberti SE, Larrea AA, Kunkel TA (2013) Exonuclease 1 preferentially repairs mismatches generated by DNA polymerase alpha. DNA Repair (Amst) 12:92–96. doi:10.1016/j.dnarep.2012.11.001

    CAS  Google Scholar 

  • Lieber MR (2008) The mechanism of human nonhomologous DNA end joining. J Biol Chem 283(1):1–5. doi:10.1074/jbc.R700039200

    PubMed  CAS  Google Scholar 

  • Lindahl T (1993) Instability and decay of the primary structure of DNA. Nature 362(6422):709–715

    PubMed  CAS  Google Scholar 

  • Liu P, Demple B (2010) DNA repair in mammalian mitochondria: much more than we thought? Environ Mol Mutagen 51(5):417–426. doi:10.1002/em.20576

    PubMed  CAS  Google Scholar 

  • Liu P, Qian L, Sung JS, de Souza-Pinto NC, Zheng L, Bogenhagen DF, Bohr VA, Wilson DM 3rd, Shen B, Demple B (2008) Removal of oxidative DNA damage via FEN1-dependent long-patch base excision repair in human cell mitochondria. Mol Cell Biol 28(16):4975–4987

    PubMed  CAS  Google Scholar 

  • Longley MJ, Prasad R, Srivastava DK, Wilson SH, Copeland WC (1998) Identification of 5′-deoxyribose phosphate lyase activity in human DNA polymerase γ and its role in mitochondrial base excision repair in vitro. Proc Natl Acad Sci USA 95(21):12244–12248

    PubMed  CAS  Google Scholar 

  • Longley MJ, Graziewicz MA, Bienstock RJ, Copeland WC (2005) Consequences of mutations in human DNA polymerase gamma. Gene 354:125–131. doi:10.1016/j.gene.2005.03.029

    PubMed  CAS  Google Scholar 

  • Lucas D, Escudero B, Ligos JM, Segovia JC, Estrada JC, Terrados G, Blanco L, Samper E, Bernad A (2009) Altered hematopoiesis in mice lacking DNA polymerase mu is due to inefficient double-strand break repair. PLoS Genet 5(2):e1000389. doi:10.1371/journal.pgen.1000389

    PubMed  Google Scholar 

  • Lujan SA, Williams JS, Pursell ZF, Abdulovic-Cui AA, Clark AB, Nick McElhinny SA, Kunkel TA (2012) Mismatch repair balances leading and lagging strand DNA replication fidelity. PLoS Genet 8(10):e1003016. doi:10.1371/journal.pgen.1003016

    PubMed  CAS  Google Scholar 

  • Lydeard JR, Jain S, Yamaguchi M, Haber JE (2007) Break-induced replication and telomerase-independent telomere maintenance require Pol32. Nature 448(7155):820–823. doi:10.1038/nature06047

    PubMed  CAS  Google Scholar 

  • Ma Y, Lu H, Tippin B, Goodman MF, Shimazaki N, Koiwai O, Hsieh CL, Schwarz K, Lieber MR (2004) A biochemically defined system for mammalian nonhomologous DNA end joining. Mol Cell 16(5):701–713. doi:10.1016/j.molcel.2004.11.017

    PubMed  CAS  Google Scholar 

  • Mahajan KN, Mitchell BS (2003) Role of human Pso4 in mammalian DNA repair and association with terminal deoxynucleotidyl transferase. Proc Natl Acad Sci USA 100(19):10746–10751. doi:10.1073/pnas.1631060100

    PubMed  CAS  Google Scholar 

  • Mahajan KN, Gangi-Peterson L, Sorscher DH, Wang J, Gathy KN, Mahajan NP, Reeves WH, Mitchell BS (1999) Association of terminal deoxynucleotidyl transferase with Ku. Proc Natl Acad Sci USA 96(24):13926–13931

    PubMed  CAS  Google Scholar 

  • Mahajan KN, Nick McElhinny SA, Mitchell BS, Ramsden DA (2002) Association of DNA polymerase mu (pol mu) with Ku and ligase IV: role for pol mu in end-joining double-strand break repair. Mol Cell Biol 22(14):5194–5202

    PubMed  CAS  Google Scholar 

  • Maloisel L, Bhargava J, Roeder GS (2004) A role for DNA polymerase delta in gene conversion and crossing over during meiosis in Saccharomyces cerevisiae. Genetics 167(3):1133–1142. doi:10.1534/genetics.104.026260

    PubMed  CAS  Google Scholar 

  • Maloisel L, Fabre F, Gangloff S (2008) DNA polymerase delta is preferentially recruited during homologous recombination to promote heteroduplex DNA extension. Mol Cell Biol 28(4):1373–1382. doi:10.1128/MCB.01651-07

    PubMed  CAS  Google Scholar 

  • Malu S, Malshetty V, Francis D, Cortes P (2012) Role of non-homologous end joining in V(D)J recombination. Immunol Res 54(1–3):233–246. doi:10.1007/s12026-012-8329-z

    PubMed  Google Scholar 

  • Markkanen E, van Loon B, Ferrari E, Hubscher U (2011) Ubiquitylation of DNA polymerase lambda. FEBS Lett 585(18):2826–2830. doi:10.1016/j.febslet.2011.03.069

    PubMed  CAS  Google Scholar 

  • Markkanen E, van Loon B, Ferrari E, Parsons JL, Dianov GL, Hubscher U (2012) Regulation of oxidative DNA damage repair by DNA polymerase lambda and MutYH by cross-talk of phosphorylation and ubiquitination. Proc Natl Acad Sci USA 109(2):437–442. doi:10.1073/pnas.1110449109

    PubMed  CAS  Google Scholar 

  • Marnett LJ (2000) Oxyradicals and DNA damage. Carcinogenesis 21(3):361–370

    PubMed  CAS  Google Scholar 

  • Marnett LJ, Riggins JN, West JD (2003) Endogenous generation of reactive oxidants and electrophiles and their reactions with DNA and protein. J Clin Invest 111(5):583–593. doi:10.1172/JCI18022

    PubMed  CAS  Google Scholar 

  • Matsumoto Y, Kim K (1995) Excision of deoxyribose phosphate residues by DNA polymerase β during DNA repair. Science 269(5224):699–702

    PubMed  CAS  Google Scholar 

  • Matsumoto Y, Kim K, Hurwitz J, Gary R, Levin DS, Tomkinson AE, Park MS (1999) Reconstitution of proliferating cell nuclear antigen-dependent repair of apurinic/apyrimidinic sites with purified human proteins. J Biol Chem 274(47):33703–33708

    PubMed  CAS  Google Scholar 

  • Matsumoto T, Go K, Hyodo M, Koiwai K, Maezawa S, Hayano T, Suzuki M, Koiwai O (2012) BRCT domain of DNA polymerase mu has DNA-binding activity and promotes the DNA polymerization activity. Genes Cells 17(9):790–806. doi:10.1111/j.1365-2443.2012.01628.x

    PubMed  CAS  Google Scholar 

  • McCulloch SD, Kunkel TA (2008) The fidelity of DNA synthesis by eukaryotic replicative and translesion synthesis polymerases. Cell Res 18(1):148–161. doi:10.1038/cr.2008.4

    PubMed  CAS  Google Scholar 

  • McHugh PJ, Sarkar S (2006) DNA interstrand cross-link repair in the cell cycle: a critical role for polymerase zeta in G1 phase. Cell Cycle 5(10):1044–1047

    PubMed  CAS  Google Scholar 

  • McIlwraith MJ, West SC (2008) DNA repair synthesis facilitates RAD52-mediated second-end capture during DSB repair. Mol Cell 29(4):510–516. doi:10.1016/j.molcel.2007.11.037

    PubMed  CAS  Google Scholar 

  • McIlwraith MJ, Vaisman A, Liu Y, Fanning E, Woodgate R, West SC (2005) Human DNA polymerase eta promotes DNA synthesis from strand invasion intermediates of homologous recombination. Mol Cell 20(5):783–792. doi:10.1016/j.molcel.2005.10.001

    PubMed  CAS  Google Scholar 

  • McVey M, Lee SE (2008) MMEJ repair of double-strand breaks (director’s cut): deleted sequences and alternative endings. Trends Genet 24(11):529–538. doi:10.1016/j.tig.2008.08.007

    PubMed  CAS  Google Scholar 

  • Modrich P (2006) Mechanisms in eukaryotic mismatch repair. J Biol Chem 281(41):30305–30309

    PubMed  CAS  Google Scholar 

  • Moon AF, Garcia-Diaz M, Bebenek K, Davis BJ, Zhong X, Ramsden DA, Kunkel TA, Pedersen LC (2007) Structural insight into the substrate specificity of DNA polymerase mu. Nat Struct Mol Biol 14(1):45–53. doi:10.1038/nsmb1180

    PubMed  CAS  Google Scholar 

  • Mosbaugh DW, Linn S (1983) Excision repair and DNA synthesis with a combination of HeLa DNA polymerase beta and DNase V. J Biol Chem 258(1):108–118

    PubMed  CAS  Google Scholar 

  • Mosbaugh DW, Linn S (1984) Gap-filling DNA synthesis by HeLa DNA polymerase alpha in an in vitro base excision DNA repair scheme. J Biol Chem 259(16):10247–10251

    PubMed  CAS  Google Scholar 

  • Mueller GA, Moon AF, Derose EF, Havener JM, Ramsden DA, Pedersen LC, London RE (2008) A comparison of BRCT domains involved in nonhomologous end-joining: introducing the solution structure of the BRCT domain of polymerase lambda. DNA Repair (Amst) 7(8):1340–1351. doi:10.1016/j.dnarep.2008.04.018

    CAS  Google Scholar 

  • Muniandy PA, Thapa D, Thazhathveetil AK, Liu ST, Seidman MM (2009) Repair of laser-localized DNA interstrand cross-links in G1 phase mammalian cells. J Biol Chem 284(41):27908–27917. doi:10.1074/jbc.M109.029025

    PubMed  CAS  Google Scholar 

  • Murray JM, Stiff T, Jeggo PA (2012) DNA double-strand break repair within heterochromatic regions. Biochem Soc Trans 40(1):173–178. doi:10.1042/BST20110631

    PubMed  CAS  Google Scholar 

  • Nagasawa K, Kitamura K, Yasui A, Nimura Y, Ikeda K, Hirai M, Matsukage A, Nakanishi M (2000) Identification and characterization of human DNA polymerase beta 2, a DNA polymerase beta -related enzyme. J Biol Chem 275(40):31233–31238. doi:10.1074/jbc.M004263200

    PubMed  CAS  Google Scholar 

  • Nealon K, Nicholl ID, Kenny MK (1996) Characterization of the DNA polymerase requirement of human base excision repair. Nucleic Acids Res 24(19):3763–3770

    PubMed  CAS  Google Scholar 

  • Neijenhuis S, Begg AC, Vens C (2005) Radiosensitization by a dominant negative to DNA polymerase beta is DNA polymerase beta-independent and XRCC1-dependent. Radiother Oncol 76(2):123–128. doi:10.1016/j.radonc.2005.06.020, S0167-8140(05)00249-5 [pii]

    PubMed  CAS  Google Scholar 

  • Neijenhuis S, Verwijs-Janssen M, Kasten-Pisula U, Rumping G, Borgmann K, Dikomey E, Begg AC, Vens C (2009) Mechanism of cell killing after ionizing radiation by a dominant negative DNA polymerase beta. DNA Repair (Amst) 8(3):336–346. doi:10.1016/j.dnarep.2008.11.008, S1568-7864(08)00398-4 [pii]

    CAS  Google Scholar 

  • Neijenhuis S, Verwijs-Janssen M, van den Broek LJ, Begg AC, Vens C (2010) Targeted radiosensitization of cells expressing truncated DNA polymerase {beta}. Cancer Res 70(21):8706–8714. doi:10.1158/0008-5472.CAN-09-3901

    PubMed  CAS  Google Scholar 

  • Nemec AA, Donigan KA, Murphy DL, Jaeger J, Sweasy JB (2012) Colon cancer-associated DNA polymerase beta variant induces genomic instability and cellular transformation. J Biol Chem 287(28):23840–23849. doi:10.1074/jbc.M112.362111

    PubMed  CAS  Google Scholar 

  • Nick McElhinny SA, Ramsden DA (2003) Polymerase mu is a DNA-directed DNA/RNA polymerase. Mol Cell Biol 23(7):2309–2315

    PubMed  CAS  Google Scholar 

  • Nick McElhinny SA, Gordenin DA, Stith CM, Burgers PM, Kunkel TA (2008) Division of labor at the eukaryotic replication fork. Mol Cell 30(2):137–144. doi:10.1016/j.molcel.2008.02.022

    PubMed  CAS  Google Scholar 

  • Nick McElhinny SA, Kissling GE, Kunkel TA (2010) Differential correction of lagging-strand replication errors made by DNA polymerases alpha and {delta}. Proc Natl Acad Sci USA 107(49):21070–21075. doi:10.1073/pnas.1013048107

    PubMed  CAS  Google Scholar 

  • Niimi A, Limsirichaikul S, Yoshida S, Iwai S, Masutani C, Hanaoka F, Kool ET, Nishiyama Y, Suzuki M (2004) Palm mutants in DNA polymerases alpha and eta alter DNA replication fidelity and translesion activity. Mol Cell Biol 24(7):2734–2746

    PubMed  CAS  Google Scholar 

  • Niimi N, Sugo N, Aratani Y, Koyama H (2005) Genetic interaction between DNA polymerase β and DNA-PKcs in embryogenesis and neurogenesis. Cell Death Differ 12(2):184–191

    PubMed  CAS  Google Scholar 

  • Nojima K, Hochegger H, Saberi A, Fukushima T, Kikuchi K, Yoshimura M, Orelli BJ, Bishop DK, Hirano S, Ohzeki M, Ishiai M, Yamamoto K, Takata M, Arakawa H, Buerstedde JM, Yamazoe M, Kawamoto T, Araki K, Takahashi JA, Hashimoto N, Takeda S, Sonoda E (2005) Multiple repair pathways mediate tolerance to chemotherapeutic cross-linking agents in vertebrate cells. Cancer Res 65(24):11704–11711. doi:10.1158/0008-5472.CAN-05-1214

    PubMed  CAS  Google Scholar 

  • O’Driscoll M (2012) Diseases associated with defective responses to DNA damage. Cold Spring Harb Perspect Biol 4(12):a012773. doi:10.1101/cshperspect.a012773

    PubMed  Google Scholar 

  • Ochs K, Sobol RW, Wilson SH, Kaina B (1999) Cells deficient in DNA polymerase β are hypersensitive to alkylating agent-induced apoptosis and chromosomal breakage. Cancer Res 59(7):1544–1551

    PubMed  CAS  Google Scholar 

  • Ochs K, Lips J, Profittlich S, Kaina B (2002) Deficiency in DNA polymerase β provokes replication-dependent apoptosis via DNA breakage, Bcl-2 decline and caspase-3/9 activation. Cancer Res 62(5):1524–1530

    PubMed  CAS  Google Scholar 

  • Ogi T, Lehmann AR (2006) The Y-family DNA polymerase kappa (pol kappa) functions in mammalian nucleotide-excision repair. Nat Cell Biol 8(6):640–642. doi:10.1038/ncb1417

    PubMed  CAS  Google Scholar 

  • Ogi T, Kannouche P, Lehmann AR (2005) Localisation of human Y-family DNA polymerase kappa: relationship to PCNA foci. J Cell Sci 118(Pt 1):129–136. doi:10.1242/jcs.01603

    PubMed  CAS  Google Scholar 

  • Ogi T, Limsirichaikul S, Overmeer RM, Volker M, Takenaka K, Cloney R, Nakazawa Y, Niimi A, Miki Y, Jaspers NG, Mullenders LH, Yamashita S, Fousteri MI, Lehmann AR (2010) Three DNA polymerases, recruited by different mechanisms, carry out NER repair synthesis in human cells. Mol Cell 37(5):714–727. doi:10.1016/j.molcel.2010.02.009

    PubMed  CAS  Google Scholar 

  • Ohashi E, Bebenek K, Matsuda T, Feaver WJ, Gerlach VL, Friedberg EC, Ohmori H, Kunkel TA (2000) Fidelity and processivity of DNA synthesis by DNA polymerase kappa, the product of the human DINB1 gene. J Biol Chem 275(50):39678–39684. doi:10.1074/jbc.M005309200

    PubMed  CAS  Google Scholar 

  • Ohnishi T, Yuba S, Date T, Utsumi H, Matsukage A (1990) Rat DNA polymerase β gene can join in excision repair of Escherichia coli. Nucleic Acids Res 18(19):5673–5676

    PubMed  CAS  Google Scholar 

  • Ono K, Ohashi A, Tanabe K, Matsukage A, Nishizawa M, Takahashi T (1979) Unique requirements for template primers of DNA polymerase beta from rat ascites hepatoma AH130 cells. Nucleic Acids Res 7(3):715–726

    PubMed  CAS  Google Scholar 

  • Orlando P, Geremia R, Frusciante C, Tedeschi B, Grippo P (1988) DNA repair synthesis in mouse spermatogenesis involves DNA polymerase beta activity. Cell Differ 23(3):221–230

    PubMed  CAS  Google Scholar 

  • Otteneder MB, Knutson CG, Daniels JS, Hashim M, Crews BC, Remmel RP, Wang H, Rizzo C, Marnett LJ (2006) In vivo oxidative metabolism of a major peroxidation-derived DNA adduct, M1dG. Proc Natl Acad Sci USA 103(17):6665–6669. doi:10.1073/pnas.0602017103

    PubMed  CAS  Google Scholar 

  • Overmeer RM, Gourdin AM, Giglia-Mari A, Kool H, Houtsmuller AB, Siegal G, Fousteri MI, Mullenders LH, Vermeulen W (2010) Replication factor C recruits DNA polymerase delta to sites of nucleotide excision repair but is not required for PCNA recruitment. Mol Cell Biol 30(20):4828–4839. doi:10.1128/MCB.00285-10

    PubMed  CAS  Google Scholar 

  • Palles C, Cazier JB, Howarth KM, Domingo E, Jones AM, Broderick P, Kemp Z, Spain SL, Guarino E, Salguero I, Sherborne A, Chubb D, Carvajal-Carmona LG, Ma Y, Kaur K, Dobbins S, Barclay E, Gorman M, Martin L, Kovac MB, Humphray S, CORGI Consortium, WGS500 Consortium, Lucassen A, Holmes CC, Bentley D, Donnelly P, Taylor J, Petridis C, Roylance R, Sawyer EJ, Kerr DJ, Clark S, Grimes J, Kearsey SE, Thomas HJ, McVean G, Houlston RS, Tomlinson I (2013) Germline mutations affecting the proofreading domains of POLE and POLD1 predispose to colorectal adenomas and carcinomas. Nat Genet 45(2):136–144. doi:10.1038/ng.2503

    Google Scholar 

  • Park IS, Park JK, Koh HY, Park SD (1991) DNA single stranded gaps formed during DNA repair synthesis induced by methyl methanesulfonate are filled by sequential action of aphidicolin- and dideoxythymidine sensitive DNA polymerases in HeLa cells. Cell Biol Toxicol 7(1):49–58

    PubMed  CAS  Google Scholar 

  • Parlanti E, Fortini P, Macpherson P, Laval J, Dogliotti E (2002) Base excision repair of adenine/8-oxoguanine mispairs by an aphidicolin-sensitive DNA polymerase in human cell extracts. Oncogene 21(34):5204–5212. doi:10.1038/sj.onc.1205561

    PubMed  CAS  Google Scholar 

  • Parsons JL, Tait PS, Finch D, Dianova II, Allinson SL, Dianov GL (2008) CHIP-mediated degradation and DNA damage-dependent stabilization regulate base excision repair proteins. Mol Cell 29(4):477–487

    PubMed  CAS  Google Scholar 

  • Parsons JL, Tait PS, Finch D, Dianova II, Edelmann MJ, Khoronenkova SV, Kessler BM, Sharma RA, McKenna WG, Dianov GL (2009) Ubiquitin ligase ARF-BP1/Mule modulates base excision repair. EMBO J 28(20):3207–3215. doi:10.1038/emboj.2009.243, emboj2009243 [pii]

    PubMed  CAS  Google Scholar 

  • Pascucci B, Stucki M, Jonsson ZO, Dogliotti E, Hubscher U (1999) Long patch base excision repair with purified human proteins. DNA ligase I as patch size mediator for DNA polymerases delta and epsilon. J Biol Chem 274(47):33696–33702

    PubMed  CAS  Google Scholar 

  • Paull TT (2005) Saving the ends for last: the role of pol mu in DNA end joining. Mol Cell 19(3):294–296. doi:10.1016/j.molcel.2005.07.008

    PubMed  CAS  Google Scholar 

  • Pawelczak KS, Bennett SM, Turchi JJ (2011) Coordination of DNA-PK activation and nuclease processing of DNA termini in NHEJ. Antioxid Redox Signal 14(12):2531–2543. doi:10.1089/ars.2010.3368

    PubMed  CAS  Google Scholar 

  • Petta TB, Nakajima S, Zlatanou A, Despras E, Couve-Privat S, Ishchenko A, Sarasin A, Yasui A, Kannouche P (2008) Human DNA polymerase iota protects cells against oxidative stress. EMBO J 27(21):2883–2895. doi:10.1038/emboj.2008.210

    PubMed  CAS  Google Scholar 

  • Phosphosite (2010) PhosphositePlus. http://www.phosphosite.org

  • Pinz KG, Bogenhagen DF (2006) The influence of the DNA polymerase gamma accessory subunit on base excision repair by the catalytic subunit. DNA Repair (Amst) 5(1):121–128. doi:10.1016/j.dnarep.2005.08.014

    CAS  Google Scholar 

  • Podlutsky AJ, Dianova II, Podust VN, Bohr VA, Dianov GL (2001) Human DNA polymerase beta initiates DNA synthesis during long-patch repair of reduced AP sites in DNA. EMBO J 20(6):1477–1482. doi:10.1093/emboj/20.6.1477

    PubMed  CAS  Google Scholar 

  • Poltoratsky V, Horton JK, Prasad R, Wilson SH (2005) REV1 mediated mutagenesis in base excision repair deficient mouse fibroblast. DNA Repair (Amst) 4(10):1182–1188

    CAS  Google Scholar 

  • Poltoratsky V, Horton JK, Prasad R, Beard WA, Woodgate R, Wilson SH (2008) Negligible impact of pol iota expression on the alkylation sensitivity of pol beta-deficient mouse fibroblast cells. DNA Repair (Amst) 7(6):830–833

    CAS  Google Scholar 

  • Prasad R, Dianov GL, Bohr VA, Wilson SH (2000) FEN1 stimulation of DNA polymerase β mediates an excision step in mammalian long patch base excision repair. J Biol Chem 275(6):4460–4466

    PubMed  CAS  Google Scholar 

  • Prasad R, Lavrik OI, Kim SJ, Kedar P, Yang XP, Vande Berg BJ, Wilson SH (2001) DNA polymerase β-mediated long patch base excision repair. Poly(ADP-ribose)polymerase-1 stimulates strand displacement DNA synthesis. J Biol Chem 276(35):32411–32414

    PubMed  CAS  Google Scholar 

  • Prasad R, Bebenek K, Hou E, Shock DD, Beard WA, Woodgate R, Kunkel TA, Wilson SH (2003) Localization of the deoxyribose phosphate lyase active site in human DNA polymerase iota by controlled proteolysis. J Biol Chem 278(32):29649–29654

    PubMed  CAS  Google Scholar 

  • Prasad R, Longley MJ, Sharief FS, Hou EW, Copeland WC, Wilson SH (2009) Human DNA polymerase theta possesses 5′-dRP lyase activity and functions in single-nucleotide base excision repair in vitro. Nucleic Acids Res 37(6):1868–1877. doi:10.1093/nar/gkp035

    PubMed  CAS  Google Scholar 

  • Preston BD, Albertson TM, Herr AJ (2010) DNA replication fidelity and cancer. Semin Cancer Biol 20(5):281–293. doi:10.1016/j.semcancer.2010.10.009

    PubMed  CAS  Google Scholar 

  • Price A (1993) The repair of ionising radiation-induced damage to DNA. Semin Cancer Biol 4(2):61–71

    PubMed  CAS  Google Scholar 

  • Prindle MJ, Loeb LA (2012) DNA polymerase delta in DNA replication and genome maintenance. Environ Mol Mutagen 53(9):666–682. doi:10.1002/em.21745

    PubMed  CAS  Google Scholar 

  • Ramadan K, Maga G, Shevelev IV, Villani G, Blanco L, Hubscher U (2003) Human DNA polymerase lambda possesses terminal deoxyribonucleotidyl transferase activity and can elongate RNA primers: implications for novel functions. J Mol Biol 328(1):63–72

    PubMed  CAS  Google Scholar 

  • Ramsden DA (2011) Polymerases in nonhomologous end joining: building a bridge over broken chromosomes. Antioxid Redox Signal 14(12):2509–2519. doi:10.1089/ars.2010.3429

    PubMed  CAS  Google Scholar 

  • Ramsden DA, Asagoshi K (2012) DNA polymerases in nonhomologous end joining: are there any benefits to standing out from the crowd? Environ Mol Mutagen 53(9):741–751. doi:10.1002/em.21725

    PubMed  CAS  Google Scholar 

  • Raschle M, Knipscheer P, Enoiu M, Angelov T, Sun J, Griffith JD, Ellenberger TE, Scharer OD, Walter JC (2008) Mechanism of replication-coupled DNA interstrand crosslink repair. Cell 134(6):969–980. doi:10.1016/j.cell.2008.08.030

    PubMed  CAS  Google Scholar 

  • Reha-Krantz LJ (2010) DNA polymerase proofreading: multiple roles maintain genome stability. Biochim Biophys Acta 1804(5):1049–1063. doi:10.1016/j.bbapap.2009.06.012

    PubMed  CAS  Google Scholar 

  • Repasky JA, Corbett E, Boboila C, Schatz DG (2004) Mutational analysis of terminal deoxynucleotidyltransferase-mediated N-nucleotide addition in V(D)J recombination. J Immunol 172(9):5478–5488

    PubMed  CAS  Google Scholar 

  • Revy P, Malivert L, de Villartay JP (2006) Cernunnos-XLF, a recently identified non-homologous end-joining factor required for the development of the immune system. Curr Opin Allergy Clin Immunol 6(6):416–420. doi:10.1097/01.all.0000246623.72365.43

    PubMed  CAS  Google Scholar 

  • Rivera-Calzada A, Spagnolo L, Pearl LH, Llorca O (2007) Structural model of full-length human Ku70-Ku80 heterodimer and its recognition of DNA and DNA-PKcs. EMBO Rep 8(1):56–62. doi:10.1038/sj.embor.7400847

    PubMed  CAS  Google Scholar 

  • Ropars V, Drevet P, Legrand P, Baconnais S, Amram J, Faure G, Marquez JA, Pietrement O, Guerois R, Callebaut I, Le Cam E, Revy P, de Villartay JP, Charbonnier JB (2011) Structural characterization of filaments formed by human Xrcc4-Cernunnos/XLF complex involved in nonhomologous DNA end-joining. Proc Natl Acad Sci USA 108(31):12663–12668. doi:10.1073/pnas.1100758108

    PubMed  CAS  Google Scholar 

  • Ruiz JF, Dominguez O, Lain de Lera T, Garcia-Diaz M, Bernad A, Blanco L (2001) DNA polymerase mu, a candidate hypermutase? Philos Trans R Soc Lond Ser B Biol Sci 356(1405):99–109. doi:10.1098/rstb.2000.0754

    CAS  Google Scholar 

  • Ruiz JF, Lucas D, Garcia-Palomero E, Saez AI, Gonzalez MA, Piris MA, Bernad A, Blanco L (2004) Overexpression of human DNA polymerase mu in a Burkitt’s lymphoma cell line affects the somatic hypermutation rate. Nucleic Acids Res 32(19):5861–5873

    PubMed  CAS  Google Scholar 

  • Sebesta M, Burkovics P, Haracska L, Krejci L (2011) Reconstitution of DNA repair synthesis in vitro and the role of polymerase and helicase activities. DNA Repair (Amst) 10(6):567–576. doi:10.1016/j.dnarep.2011.03.003

    CAS  Google Scholar 

  • Seki S, Oda T (1986) DNA repair synthesis in bleomycin-pretreated permeable HeLa cells. Carcinogenesis 7(1):77–82

    PubMed  CAS  Google Scholar 

  • Seki M, Gearhart PJ, Wood RD (2005) DNA polymerases and somatic hypermutation of immunoglobulin genes. EMBO Rep 6(12):1143–1148. doi:10.1038/sj.embor.7400582

    PubMed  CAS  Google Scholar 

  • Senejani AG, Dalal S, Liu Y, Nottoli TP, McGrath JM, Clairmont CS, Sweasy JB (2012) Y265C DNA polymerase beta knockin mice survive past birth and accumulate base excision repair intermediate substrates. Proc Natl Acad Sci USA 109(17):6632–6637. doi:10.1073/pnas.1200800109

    PubMed  CAS  Google Scholar 

  • Setlow RB, Setlow JK (1962) Evidence that ultraviolet-induced thymine dimers in DNA cause biological damage. Proc Natl Acad Sci USA 48:1250–1257

    PubMed  CAS  Google Scholar 

  • Sharma S, Canman CE (2012) REV1 and DNA polymerase zeta in DNA interstrand crosslink repair. Environ Mol Mutagen 53(9):725–740. doi:10.1002/em.21736

    PubMed  CAS  Google Scholar 

  • Shen X, Jun S, O’Neal LE, Sonoda E, Bemark M, Sale JE, Li L (2006) REV3 and REV1 play major roles in recombination-independent repair of DNA interstrand cross-links mediated by monoubiquitinated proliferating cell nuclear antigen (PCNA). J Biol Chem 281(20):13869–13872. doi:10.1074/jbc.C600071200

    PubMed  CAS  Google Scholar 

  • Shivji KK, Kenny MK, Wood RD (1992) Proliferating cell nuclear antigen is required for DNA excision repair. Cell 69(2):367–374

    PubMed  CAS  Google Scholar 

  • Shivji MK, Podust VN, Hubscher U, Wood RD (1995) Nucleotide excision repair DNA synthesis by DNA polymerase epsilon in the presence of PCNA, RFC, and RPA. Biochemistry 34(15):5011–5017

    PubMed  CAS  Google Scholar 

  • Shuck SC, Short EA, Turchi JJ (2008) Eukaryotic nucleotide excision repair: from understanding mechanisms to influencing biology. Cell Res 18(1):64–72. doi:10.1038/cr.2008.2

    PubMed  CAS  Google Scholar 

  • Siedlecki JA, Szyszko J, Pietrzykowska I, Zmudzka B (1980) Evidence implying DNA polymerase beta function in excision repair. Nucleic Acids Res 8(2):361–375

    PubMed  CAS  Google Scholar 

  • Simsek D, Furda A, Gao Y, Artus J, Brunet E, Hadjantonakis AK, Van Houten B, Shuman S, McKinnon PJ, Jasin M (2011) Crucial role for DNA ligase III in mitochondria but not in Xrcc1-dependent repair. Nature 471(7337):245–248. doi:10.1038/nature09794

    PubMed  CAS  Google Scholar 

  • Singhal RK, Wilson SH (1993) Short gap-filling synthesis by DNA polymerase β is processive. J Biol Chem 268(21):15906–15911

    PubMed  CAS  Google Scholar 

  • Singhal RK, Prasad R, Wilson SH (1995) DNA polymerase β conducts the gap-filling step in uracil-initiated base excision repair in a bovine testis nuclear extract. J Biol Chem 270(2):949–957

    PubMed  CAS  Google Scholar 

  • Slupphaug G, Markussen FH, Olsen LC, Aasland R, Aarsaether N, Bakke O, Krokan HE, Helland DE (1993) Nuclear and mitochondrial forms of human uracil-DNA glycosylase are encoded by the same gene. Nucleic Acids Res 21(11):2579–2584

    PubMed  CAS  Google Scholar 

  • Sobol RW (2007) DNA polymerase β null mouse embryonic fibroblasts harbor a homozygous null mutation in DNA polymerase iota. DNA Repair (Amst) 6(1):3–7

    CAS  Google Scholar 

  • Sobol RW (2008) CHIPping away at base excision repair. Mol Cell 29(4):413–415

    PubMed  CAS  Google Scholar 

  • Sobol RW (2012a) For MutY, it’s all about the OG. Chem Biol 19(3):313–314. doi:10.1016/j.chembiol.2012.03.002

    PubMed  CAS  Google Scholar 

  • Sobol RW (2012b) Genome instability caused by a germline mutation in the human DNA repair gene POLB. PLoS Genet 8(11):e1003086. doi:10.1371/journal.pgen.1003086

    PubMed  CAS  Google Scholar 

  • Sobol RW, Horton JK, Kuhn R, Gu H, Singhal RK, Prasad R, Rajewsky K, Wilson SH (1996) Requirement of mammalian DNA polymerase-β in base-excision repair. Nature 379(6561):183–186

    PubMed  CAS  Google Scholar 

  • Sobol RW, Prasad R, Evenski A, Baker A, Yang XP, Horton JK, Wilson SH (2000) The lyase activity of the DNA repair protein β-polymerase protects from DNA-damage-induced cytotoxicity. Nature 405(6788):807–810

    PubMed  CAS  Google Scholar 

  • Sobol RW, Watson DE, Nakamura J, Yakes FM, Hou E, Horton JK, Ladapo J, Van Houten B, Swenberg JA, Tindall KR, Samson LD, Wilson SH (2002) Mutations associated with base excision repair deficiency and methylation-induced genotoxic stress. Proc Natl Acad Sci USA 99(10):6860–6865

    PubMed  CAS  Google Scholar 

  • Sobol RW, Kartalou M, Almeida KH, Joyce DF, Engelward BP, Horton JK, Prasad R, Samson LD, Wilson SH (2003) Base excision repair intermediates induce p53-independent cytotoxic and genotoxic responses. J Biol Chem 278(41):39951–39959

    PubMed  CAS  Google Scholar 

  • Stachelek GC, Dalal S, Donigan KA, Campisi Hegan D, Sweasy JB, Glazer PM (2010) Potentiation of temozolomide cytotoxicity by inhibition of DNA polymerase beta is accentuated by BRCA2 mutation. Cancer Res 70(1):409–417. doi:10.1158/0008-5472.CAN-09-1353, 0008-5472.CAN-09-1353 [pii]

    PubMed  CAS  Google Scholar 

  • Starcevic D, Dalal S, Sweasy JB (2004) Is there a link between DNA polymerase beta and cancer? Cell Cycle 3(8):998–1001

    PubMed  CAS  Google Scholar 

  • Staresincic L, Fagbemi AF, Enzlin JH, Gourdin AM, Wijgers N, Dunand-Sauthier I, Giglia-Mari G, Clarkson SG, Vermeulen W, Scharer OD (2009) Coordination of dual incision and repair synthesis in human nucleotide excision repair. EMBO J 28(8):1111–1120. doi:10.1038/emboj.2009.49

    PubMed  CAS  Google Scholar 

  • Strittmatter T, Bareth B, Immel TA, Huhn T, Mayer TU, Marx A (2011) Small molecule inhibitors of human DNA polymerase lambda. ACS Chem Biol 6(4):314–319. doi:10.1021/cb100382m

    PubMed  CAS  Google Scholar 

  • Stuart JA, Mayard S, Hashiguchi K, Souza-Pinto NC, Bohr VA (2005) Localization of mitochondrial DNA base excision repair to an inner membrane-associated particulate fraction. Nucleic Acids Res 33(12):3722–3732. doi:10.1093/nar/gki683

    PubMed  CAS  Google Scholar 

  • Stucki M, Pascucci B, Parlanti E, Fortini P, Wilson SH, Hubscher U, Dogliotti E (1998) Mammalian base excision repair by DNA polymerases delta and epsilon. Oncogene 17(7):835–843

    PubMed  CAS  Google Scholar 

  • Sugo N, Aratani Y, Nagashima Y, Kubota Y, Koyama H (2000) Neonatal lethality with abnormal neurogenesis in mice deficient in DNA polymerase β. EMBO J 19(6):1397–1404

    PubMed  CAS  Google Scholar 

  • Sung P, Klein H (2006) Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nat Rev Mol Cell Biol 7(10):739–750. doi:10.1038/nrm2008

    PubMed  CAS  Google Scholar 

  • Svilar D, Goellner EM, Almeida KH, Sobol RW (2011) Base excision repair and lesion-dependent sub-pathways for repair of oxidative DNA damage. Antioxid Redox Signal 14(12):2491–2507. doi:10.1089/ars.2010.3466

    PubMed  CAS  Google Scholar 

  • Sweasy JB, Lang T, DiMaio D (2006) Is base excision repair a tumor suppressor mechanism? Cell Cycle 5(3):250–259

    PubMed  CAS  Google Scholar 

  • Symington LS, Gautier J (2011) Double-strand break end resection and repair pathway choice. Annu Rev Genet 45:247–271. doi:10.1146/annurev-genet-110410-132435

    PubMed  CAS  Google Scholar 

  • Szczesny B, Tann AW, Longley MJ, Copeland WC, Mitra S (2008) Long patch base excision repair in mammalian mitochondrial genomes. J Biol Chem 283(39):26349–26356. doi:10.1074/jbc.M803491200, M803491200 [pii]

    PubMed  CAS  Google Scholar 

  • Tanabe K, Bohn EW, Wilson SH (1979) Steady-state kinetics of mouse DNA polymerase beta. Biochemistry 18(15):3401–3406

    PubMed  CAS  Google Scholar 

  • Tang J, Goellner EM, Wang XW, Trivedi RN, St. Croix CM, Jelezcova E, Svilar D, Brown AR, Sobol RW (2010) Bioenergetic metabolites regulate base excision repair-dependent cell death in response to DNA damage. Mol Cancer Res 8(1):67–79. doi:10.1158/1541-7786.MCR-09-0411, 1541-7786.MCR-09-0411 [pii]

    PubMed  CAS  Google Scholar 

  • Tang JB, Svilar D, Trivedi RN, Wang XH, Goellner EM, Moore B, Hamilton RL, Banze LA, Brown AR, Sobol RW (2011) N-methylpurine DNA glycosylase and DNA polymerase beta modulate BER inhibitor potentiation of glioma cells to temozolomide. Neuro-oncol 13(5):471–486. doi:10.1093/neuonc/nor011

    PubMed  CAS  Google Scholar 

  • Tann AW, Boldogh I, Meiss G, Qian W, Van Houten B, Mitra S, Szczesny B (2011) Apoptosis induced by persistent single-strand breaks in mitochondrial genome: critical role of EXOG (5′-EXO/endonuclease) in their repair. J Biol Chem 286(37):31975–31983. doi:10.1074/jbc.M110.215715

    PubMed  CAS  Google Scholar 

  • Tano K, Nakamura J, Asagoshi K, Arakawa H, Sonoda E, Braithwaite EK, Prasad R, Buerstedde JM, Takeda S, Watanabe M, Wilson SH (2007) Interplay between DNA polymerases beta and lambda in repair of oxidation DNA damage in chicken DT40 cells. DNA Repair (Amst) 6(6):869–875

    CAS  Google Scholar 

  • Terrados G, Capp JP, Canitrot Y, Garcia-Diaz M, Bebenek K, Kirchhoff T, Villanueva A, Boudsocq F, Bergoglio V, Cazaux C, Kunkel TA, Hoffmann JS, Blanco L (2009) Characterization of a natural mutator variant of human DNA polymerase lambda which promotes chromosomal instability by compromising NHEJ. PLoS One 4(10):e7290. doi:10.1371/journal.pone.0007290

    PubMed  Google Scholar 

  • Thomas DC, Roberts JD, Kunkel TA (1991) Heteroduplex repair in extracts of human HeLa cells. J Biol Chem 266(6):3744–3751

    PubMed  CAS  Google Scholar 

  • Tokui T, Inagaki M, Nishizawa K, Yatani R, Kusagawa M, Ajiro K, Nishimoto Y, Date T, Matsukage A (1991) Inactivation of DNA polymerase beta by in vitro phosphorylation with protein kinase C. J Biol Chem 266(17):10820–10824

    PubMed  CAS  Google Scholar 

  • Tomicic MT, Thust R, Sobol RW, Kaina B (2001) DNA polymerase β mediates protection of mammalian cells against ganciclovir-induced cytotoxicity and DNA breakage. Cancer Res 61(20):7399–7403

    PubMed  CAS  Google Scholar 

  • Trivedi RN, Almeida KH, Fornsaglio JL, Schamus S, Sobol RW (2005) The role of base excision repair in the sensitivity and resistance to temozolomide mediated cell death. Cancer Res 65(14):6394–6400

    PubMed  CAS  Google Scholar 

  • Trivedi RN, Wang XH, Jelezcova E, Goellner EM, Tang J, Sobol RW (2008) Human methyl purine DNA glycosylase and DNA polymerase β expression collectively predict sensitivity to temozolomide. Mol Pharmacol 74(2):505–516

    PubMed  CAS  Google Scholar 

  • Ukai A, Maruyama T, Mochizuki S, Ouchida R, Masuda K, Kawamura K, Tagawa M, Kinoshita K, Sakamoto A, Tokuhisa T, O-Wang J (2006) Role of DNA polymerase theta in tolerance of endogenous and exogenous DNA damage in mouse B cells. Genes Cells 11(2):111–121. doi:10.1111/j.1365-2443.2006.00922.x

    PubMed  CAS  Google Scholar 

  • van Loon B, Hubscher U (2009) An 8-oxo-guanine repair pathway coordinated by MUTYH glycosylase and DNA polymerase lambda. Proc Natl Acad Sci USA 106(43):18201–18206. doi:10.1073/pnas.0907280106, 0907280106 [pii]

    PubMed  Google Scholar 

  • Vens C, Begg AC (2010) Targeting base excision repair as a sensitization strategy in radiotherapy. Semin Radiat Oncol 20(4):241–249. doi:10.1016/j.semradonc.2010.05.005, S1053-4296(10)00039-1 [pii]

    PubMed  Google Scholar 

  • Vens C, Sobol RW (2013) Targeting DNA repair pathways for cancer therapy. In: Johnson DE (ed) Cell death signaling in cancer biology and treatment, vol 1. Springer, New York

    Google Scholar 

  • Vermeulen C, Bertocci B, Begg AC, Vens C (2007a) Ionizing radiation sensitivity of DNA polymerase lambda-deficient cells. Radiat Res 168(6):683–688. doi:10.1667/RR1057R.1

    PubMed  CAS  Google Scholar 

  • Vermeulen C, Verwijs-Janssen M, Cramers P, Begg AC, Vens C (2007b) Role for DNA polymerase beta in response to ionizing radiation. DNA Repair (Amst) 6(2):202–212

    CAS  Google Scholar 

  • Vidal AE, Woodgate R (2009) Insights into the cellular role of enigmatic DNA polymerase iota. DNA Repair (Amst) 8(3):420–423. doi:10.1016/j.dnarep.2008.12.007

    CAS  Google Scholar 

  • Wang X, Peterson CA, Zheng H, Nairn RS, Legerski RJ, Li L (2001) Involvement of nucleotide excision repair in a recombination-independent and error-prone pathway of DNA interstrand cross-link repair. Mol Cell Biol 21(3):713–720. doi:10.1128/MCB.21.3.713-720.2001

    PubMed  CAS  Google Scholar 

  • Wang X, Ira G, Tercero JA, Holmes AM, Diffley JF, Haber JE (2004) Role of DNA replication proteins in double-strand break-induced recombination in Saccharomyces cerevisiae. Mol Cell Biol 24(16):6891–6899. doi:10.1128/MCB.24.16.6891-6899.2004

    PubMed  CAS  Google Scholar 

  • Waser J, Hubscher U, Kuenzle CC, Spadari S (1979) DNA polymerase beta from brain neurons is a repair enzyme. Eur J Biochem 97(2):361–368

    PubMed  CAS  Google Scholar 

  • Wawra E, Dolejs I (1979) Evidences for the function of DNA polymerase-beta in unscheduled DNA synthesis. Nucleic Acids Res 7(6):1675–1686

    PubMed  CAS  Google Scholar 

  • Weissbach A (1977) Eukaryotic DNA polymerases. Annu Rev Biochem 46:25–47

    PubMed  CAS  Google Scholar 

  • Weissbach A, Baltimore D, Bollum F, Gallo R, Korn D (1975a) Nomenclature of eukaryotic DNA polymerases. Eur J Biochem 59(1):1–2

    PubMed  CAS  Google Scholar 

  • Weissbach A, Baltimore D, Bollum F, Gallo R, Korn D (1975b) Nomenclature of eukaryotic DNA polymerases. Science 190(4212):401–402

    PubMed  CAS  Google Scholar 

  • Wiebauer K, Jiricny J (1990) Mismatch-specific thymine DNA glycosylase and DNA polymerase β mediate the correction of G.T mispairs in nuclear extracts from human cells. Proc Natl Acad Sci USA 87(15):5842–5845

    PubMed  CAS  Google Scholar 

  • Williams HL, Gottesman ME, Gautier J (2012) Replication-independent repair of DNA interstrand crosslinks. Mol Cell 47(1):140–147. doi:10.1016/j.molcel.2012.05.001

    PubMed  CAS  Google Scholar 

  • Wilson SH, Beard WA, Shock DD, Batra VK, Cavanaugh NA, Prasad R, Hou EW, Liu Y, Asagoshi K, Horton JK, Stefanick DF, Kedar PS, Carrozza MJ, Masaoka A, Heacock ML (2010) Base excision repair and design of small molecule inhibitors of human DNA polymerase beta. Cell Mol Life Sci 67(21):3633–3647. doi:10.1007/s00018-010-0489-1

    PubMed  CAS  Google Scholar 

  • Wimmer U, Ferrari E, Hunziker P, Hubscher U (2008) Control of DNA polymerase lambda stability by phosphorylation and ubiquitination during the cell cycle. EMBO Rep 9(10):1027–1033. doi:10.1038/embor.2008.148

    PubMed  CAS  Google Scholar 

  • Wood RD (1996) DNA repair in eukaryotes. Annu Rev Biochem 65:135–167. doi:10.1146/annurev.bi.65.070196.001031

    PubMed  CAS  Google Scholar 

  • Wood RD (2010) Mammalian nucleotide excision repair proteins and interstrand crosslink repair. Environ Mol Mutagen 51(6):520–526. doi:10.1002/em.20569

    PubMed  CAS  Google Scholar 

  • Wood RD, Mitchell M, Sgouros J, Lindahl T (2001) Human DNA repair genes. Science 291(5507):1284–1289

    PubMed  CAS  Google Scholar 

  • Wood RD, Mitchell M, Lindahl T (2005) Human DNA repair genes. Mutat Res 577(1–2):275–283. doi:10.1016/j.mrfmmm.2005.03.007, S0027-5107(05)00163-6 [pii]

    PubMed  CAS  Google Scholar 

  • Woods NT, Mesquita RD, Sweet M, Carvalho MA, Li X, Liu Y, Nguyen H, Thomas CE, Iversen ES Jr, Marsillac S, Karchin R, Koomen J, Monteiro AN (2012) Charting the landscape of tandem BRCT domain-mediated protein interactions. Sci Signal 5(242):rs6. doi:10.1126/scisignal.2002255

    PubMed  Google Scholar 

  • Wyatt MD, Pittman DL (2006) Methylating agents and DNA repair responses: methylated bases and sources of strand breaks. Chem Res Toxicol 19(12):1580–1594

    PubMed  CAS  Google Scholar 

  • Yano K, Morotomi-Yano K, Wang SY, Uematsu N, Lee KJ, Asaithamby A, Weterings E, Chen DJ (2008) Ku recruits XLF to DNA double-strand breaks. EMBO Rep 9(1):91–96. doi:10.1038/sj.embor.7401137

    PubMed  CAS  Google Scholar 

  • Yano K, Morotomi-Yano K, Lee KJ, Chen DJ (2011) Functional significance of the interaction with Ku in DNA double-strand break recognition of XLF. FEBS Lett 585(6):841–846. doi:10.1016/j.febslet.2011.02.020

    PubMed  CAS  Google Scholar 

  • Yeh JI, Levine AS, Du S, Chinte U, Ghodke H, Wang H, Shi H, Hsieh CL, Conway JF, Van Houten B, Rapic-Otrin V (2012) Damaged DNA induced UV-damaged DNA-binding protein (UV-DDB) dimerization and its roles in chromatinized DNA repair. Proc Natl Acad Sci USA 109(41):E2737–E2746. doi:10.1073/pnas.1110067109

    PubMed  CAS  Google Scholar 

  • Yi C, He C (2013) DNA repair by reversal of DNA damage. Cold Spring Harb Perspect Biol 5(1):a012575. doi:10.1101/cshperspect.a012575

    PubMed  Google Scholar 

  • Yoshida S, Yamada M, Masaki S (1979) Novel properties of DNA polymerase beta with poly(rA).oligo(dT) template-primer. J Biochem (Tokyo) 85(6):1387–1395

    CAS  Google Scholar 

  • Yousefzadeh MJ, Wood RD (2013) DNA polymerase POLQ and cellular defense against DNA damage. DNA Repair (Amst) 12(1):1–9. doi:10.1016/j.dnarep.2012.10.004

    CAS  Google Scholar 

  • Zheng L, Zhou M, Guo Z, Lu H, Qian L, Dai H, Qiu J, Yakubovskaya E, Bogenhagen DF, Demple B, Shen B (2008) Human DNA2 is a mitochondrial nuclease/helicase for efficient processing of DNA replication and repair intermediates. Mol Cell 32(3):325–336. doi:10.1016/j.molcel.2008.09.024, S1097-2765(08)00698-9 [pii]

    PubMed  CAS  Google Scholar 

  • Ziv O, Geacintov N, Nakajima S, Yasui A, Livneh Z (2009) DNA polymerase zeta cooperates with polymerases kappa and iota in translesion DNA synthesis across pyrimidine photodimers in cells from XPV patients. Proc Natl Acad Sci USA 106(28):11552–11557. doi:10.1073/pnas.0812548106

    PubMed  CAS  Google Scholar 

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Sobol, R.W. (2014). DNA Repair Polymerases. In: Murakami, K., Trakselis, M. (eds) Nucleic Acid Polymerases. Nucleic Acids and Molecular Biology, vol 30. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-39796-7_3

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