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DNA Helicases in NER, BER, and MMR

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DNA Helicases and DNA Motor Proteins

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 767))

Abstract

Different DNA repair mechanisms have evolved to protect our genome from modifications caused by endogenous and exogenous agents, thus maintaining the integrity of the DNA. Helicases often play a central role in these repair pathways and have shown to be essential for diverse tasks within these mechanisms. In prokaryotic nucleotide excision repair (NER) for example the two helicases UvrB and UvrD assume vastly different functions. While UvrB is intimately involved in damage verification and acts as an anchor for the other prokaryotic NER proteins UvrA and UvrC, UvrD is required to resolve the post-incision complex leading to the release of UvrC and the incised ssDNA fragment. For the XPD helicase in eukaryotic NER a similar function in analogy to UvrB has been proposed, whereas XPB the second helicase uses only its ATPase activity during eukaryotic NER. In prokaryotic mismatch repair (MMR) UvrD again plays a central role. The different tasks of this protein in the different repair pathways highlight the importance of regulative protein–protein interactions to fine-tune its helicase activity. In other DNA repair pathways the role of the helicases involved is sometimes not as well characterized, and no helicase has so far been described to assume the function of UvrD in eukaryotic MMR. RecQ helicases and FancJ interact with eukaryotic MMR proteins but their involvement in this repair pathway is unclear. Lastly, long-patch base excision repair is linked to the WRN helicase and many proteins within this pathway interact with the helicase leading to increased activity of the interacting proteins as observed for pol β and FEN-1 or the helicase itself is negatively regulated through the interaction with APE-1. However, compared to the precise functions described for the helicases in the other DNA repair mechanisms the role of WRN in BER remains speculative and requires further analysis.

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References

  1. Lindahl T, Wood RD. Quality control by DNA repair. Science. 1999;286:1897–905.

    CAS  PubMed  Google Scholar 

  2. Van Houten B. Nucleotide excision repair in Escherichia coli. Microbiol Rev. 1990;54:18–51.

    PubMed  PubMed Central  Google Scholar 

  3. Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, Ellenberger T. DNA repair and mutagenesis. Washington, DC: ASM Press; 2006.

    Google Scholar 

  4. Gillet LC, Scharer OD. Molecular mechanisms of mammalian global genome nucleotide excision repair. Chem Rev. 2006;106(2):253–76.

    CAS  PubMed  Google Scholar 

  5. Sancar A. DNA excision repair. Annu Rev Biochem. 1996;65:43–81.

    CAS  PubMed  Google Scholar 

  6. Kuper J, Kisker C. Damage recognition in nucleotide excision DNA repair. Curr Opin Struct Biol. 2012;22(1):88–93.

    CAS  PubMed  Google Scholar 

  7. Petit MA, Dervyn E, Rose M, Entian KD, McGovern S, Ehrlich SD, et al. PcrA is an essential DNA helicase of Bacillus subtilis fulfilling functions both in repair and rolling-circle replication. Mol Microbiol. 1998;29(1):261–73.

    CAS  PubMed  Google Scholar 

  8. Manelyte L, Guy CP, Smith RM, Dillingham MS, McGlynn P, Savery NJ. The unstructured C-terminal extension of UvrD interacts with UvrB, but is dispensable for nucleotide excision repair. DNA Repair. 2009;8(11):1300–10.

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Yamagata A, Masui R, Kato R, Nakagawa N, Ozaki H, Sawai H, et al. Interaction of UvrA and UvrB proteins with a fluorescent single-stranded DNA. Implication for slow conformational change upon interaction of UvrB with DNA. J Biol Chem. 2000;275(18):13235–42.

    CAS  PubMed  Google Scholar 

  10. Matson SW. Escherichia coli helicase II (urvD gene product) translocates unidirectionally in a 3’ to 5’ direction. J Biol Chem. 1986;261(22):10169–75.

    CAS  PubMed  Google Scholar 

  11. Fischer CJ, Maluf NK, Lohman TM. Mechanism of ATP-dependent translocation of E. coli UvrD monomers along single-stranded DNA. J Mol Biol. 2004;344(5):1287–309.

    CAS  PubMed  Google Scholar 

  12. Anand SP, Khan SA. Structure-specific DNA binding and bipolar helicase activities of PcrA. Nucleic Acids Res. 2004;32(10):3190–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Niedziela-Majka A, Chesnik MA, Tomko EJ, Lohman TM. Bacillus stearothermophilus PcrA monomer is a single-stranded DNA translocase but not a processive helicase in vitro. J Biol Chem. 2007;282(37):27076–85.

    CAS  PubMed  Google Scholar 

  14. Pakotiprapha D, Samuels M, Shen K, Hu JH, Jeruzalmi D. Structure and mechanism of the UvrA-UvrB DNA damage sensor. Nat Struct Mol Biol. 2012;19(3):291–8.

    CAS  PubMed  Google Scholar 

  15. Verhoeven EE, Wyman C, Moolenaar GF, Goosen N. The presence of two UvrB subunits in the UvrAB complex ensures damage detection in both DNA strands. EMBO J. 2002;21(15):4196–205.

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Theis K, Skorvaga M, Machius M, Nakagawa N, Van Houten B, Kisker C. The nucleotide excision repair protein UvrB, a helicase-like enzyme with a catch. Mutat Res. 2000;460(3–4):277–300.

    CAS  PubMed  Google Scholar 

  17. Truglio JJ, Croteau DL, Van Houten B, Kisker C. Prokaryotic nucleotide excision repair: the UvrABC system. Chem Rev. 2006;106(2):233–52.

    CAS  PubMed  Google Scholar 

  18. Theis K, Chen PJ, Skorvaga M, Houten BV, Kisker C. Crystal structure of UvrB, a DNA helicase adapted for nucleotide excision repair. EMBO J. 1999;18:6899–907.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Van Houten B, Croteau DL, DellaVecchia MJ, Wang H, Kisker C. ‘Close-fitting sleeves’: DNA damage recognition by the UvrABC nuclease system. Mutat Res. 2005;577(1–2):92–117.

    PubMed  Google Scholar 

  20. Skorvaga M, Theis K, Mandavilli BS, Kisker C, Van Houten B. The beta-hairpin motif of UvrB is essential for DNA binding, damage processing, and UvrC-mediated incisions. J Biol Chem. 2002;277(2):1553–9.

    CAS  PubMed  Google Scholar 

  21. Moolenaar GF, Hoglund L, Goosen N. Clue to damage recognition by UvrB: residues in the beta-hairpin structure prevent binding to non-damaged DNA. EMBO J. 2001;20(21):6140–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Moolenaar GF, Schut M, Goosen N. Binding of the UvrB dimer to non-damaged and damaged DNA: residues Y92 and Y93 influence the stability of both subunits. DNA Repair (Amst). 2005;4(6):699–713.

    CAS  PubMed  Google Scholar 

  23. Truglio JJ, Karakas E, Rhau B, Wang H, DellaVecchia MJ, Van Houten B, et al. Structural basis for DNA recognition and processing by UvrB. Nat Struct Mol Biol. 2006;13(4):360–4.

    CAS  PubMed  Google Scholar 

  24. Wang H, DellaVecchia MJ, Skorvaga M, Croteau DL, Erie DA, Van Houten B. UvrB domain 4, an autoinhibitory gate for regulation of DNA binding and ATPase activity. J Biol Chem. 2006;281(22):15227–37.

    CAS  PubMed  Google Scholar 

  25. Oh EY, Grossman L. Characterization of the helicase activity of the Escherichia coli UvrAB protein complex. J Biol Chem. 1989;264:1336–43.

    CAS  PubMed  Google Scholar 

  26. Moolenaar GF, Monaco V, van der Marel GA, van Boom JH, Visse R, Goosen N. The effect of the DNA flanking the lesion on formation of the UvrB-DNA preincision complex. Mechanism for the UvrA-mediated loading of UvrB onto a DNA damaged site. J Biol Chem. 2000;275(11):8038–43.

    CAS  PubMed  Google Scholar 

  27. Zou Y, Ma H, Minko IG, Shell SM, Yang Z, Qu Y, et al. DNA damage recognition of mutated forms of UvrB proteins in nucleotide excision repair. Biochemistry. 2004;43(14):4196–205.

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Sancar A, Franklin KA, Sancar GB. Escherichia coli DNA photolyase stimulates uvrABC excision nuclease in vitro. Proc Natl Acad Sci USA. 1984;81(23):7397–401.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Lee JY, Yang W. UvrD helicase unwinds DNA one base pair at a time by a two-part power stroke. Cell. 2006;127(7):1349–60.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Jia H, Korolev S, Niedziela-Majka A, Maluf NK, Gauss GH, Myong S, et al. Rotations of the 2B sub-domain of E. coli UvrD helicase/translocase coupled to nucleotide and DNA binding. J Mol Biol. 2011;411(3):633–48.

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Atkinson J, Guy CP, Cadman CJ, Moolenaar GF, Goosen N, McGlynn P. Stimulation of UvrD helicase by UvrAB. J Biol Chem. 2009;284(14):9612–23.

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Coin F, Oksenych V, Egly JM. Distinct roles for the XPB/p52 and XPD/p44 subcomplexes of TFIIH in damaged DNA opening during nucleotide excision repair. Mol Cell. 2007;26(2):245–56.

    CAS  PubMed  Google Scholar 

  33. Ogi T, Limsirichaikul S, Overmeer RM, Volker M, Takenaka K, Cloney R, et al. Three DNA polymerases, recruited by different mechanisms, carry out NER repair synthesis in human cells. Mol Cell. 2010;37(5):714–27.

    CAS  PubMed  Google Scholar 

  34. Moser J, Kool H, Giakzidis I, Caldecott K, Mullenders LH, Fousteri MI. Sealing of chromosomal DNA nicks during nucleotide excision repair requires XRCC1 and DNA ligase III alpha in a cell-cycle-specific manner. Mol Cell. 2007;27(2):311–23.

    CAS  PubMed  Google Scholar 

  35. Fan L, Arvai AS, Cooper PK, Iwai S, Hanaoka F, Tainer JA. Conserved XPB core structure and motifs for DNA unwinding: implications for pathway selection of transcription or excision repair. Mol Cell. 2006;22(1):27–37.

    CAS  PubMed  Google Scholar 

  36. Oksenych V, de Jesus BB, Zhovmer A, Egly JM, Coin F. Molecular insights into the recruitment of TFIIH to sites of DNA damage. EMBO J. 2009;28(19):2971–80.

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Egly JM, Coin F. A history of TFIIH: two decades of molecular biology on a pivotal transcription/repair factor. DNA Repair. 2011;10(7):714–21.

    CAS  PubMed  Google Scholar 

  38. Fan L, Fuss JO, Cheng QJ, Arvai AS, Hammel M, Roberts VA, et al. XPD helicase structures and activities: insights into the cancer and aging phenotypes from XPD mutations. Cell. 2008;133(5):789–800.

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Liu H, Rudolf J, Johnson KA, McMahon SA, Oke M, Carter L, et al. Structure of the DNA repair helicase XPD. Cell. 2008;133(5):801–12.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Wolski SC, Kuper J, Hanzelmann P, Truglio JJ, Croteau DL, Van Houten B, et al. Crystal structure of the FeS cluster-containing nucleotide excision repair helicase XPD. PLoS Biol. 2008;6(6):e149.

    PubMed  PubMed Central  Google Scholar 

  41. Rudolf J, Makrantoni V, Ingledew WJ, Stark MJ, White MF. The DNA repair helicases XPD and FancJ have essential iron-sulfur domains. Mol Cell. 2006;23(6):801–8.

    CAS  PubMed  Google Scholar 

  42. Kuper J, Wolski SC, Michels G, Kisker C. Functional and structural studies of the nucleotide excision repair helicase XPD suggest a polarity for DNA translocation. EMBO J. 2012;31(2):494–502.

    CAS  PubMed  Google Scholar 

  43. Rudolf J, Rouillon C, Schwarz-Linek U, White MF. The helicase XPD unwinds bubble structures and is not stalled by DNA lesions removed by the nucleotide excision repair pathway. Nucleic Acids Res. 2010;38(3):931–41.

    CAS  PubMed  Google Scholar 

  44. Coin F, Marinoni JC, Rodolfo C, Fribourg S, Pedrini AM, Egly JM. Mutations in the XPD helicase gene result in XP and TTD phenotypes, preventing interaction between XPD and the p44 subunit of TFIIH. Nat Genet. 1998;20(2):184–8.

    CAS  PubMed  Google Scholar 

  45. Sandrock B, Egly JM. A yeast four-hybrid system identifies Cdk-activating kinase as a regulator of the XPD helicase, a subunit of transcription factor IIH. J Biol Chem. 2001;276(38):35328–33.

    CAS  PubMed  Google Scholar 

  46. Coin F, Oksenych V, Mocquet V, Groh S, Blattner C, Egly JM. Nucleotide excision repair driven by the dissociation of CAK from TFIIH. Mol Cell. 2008;31(1):9–20.

    CAS  PubMed  Google Scholar 

  47. Weber A, Chung HJ, Springer E, Heitzmann D, Warth R. The TFIIH subunit p89 (XPB) localizes to the centrosome during mitosis. Cell Oncol. 2010;32(1–2):121–30.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Ito S, Tan LJ, Andoh D, Narita T, Seki M, Hirano Y, et al. MMXD, a TFIIH-independent XPD-MMS19 protein complex involved in chromosome segregation. Mol Cell. 2010;39(4):632–40.

    CAS  PubMed  Google Scholar 

  49. Chen J, Larochelle S, Li X, Suter B. Xpd/Ercc2 regulates CAK activity and mitotic progression. Nature. 2003;424(6945):228–32.

    CAS  PubMed  Google Scholar 

  50. Li X, Urwyler O, Suter B. Drosophila Xpd regulates Cdk7 localization, mitotic kinase activity, spindle dynamics, and chromosome segregation. PLoS Genet. 2010;6(3):e1000876.

    PubMed  PubMed Central  Google Scholar 

  51. Wu Y, Suhasini AN, Brosh Jr RM. Welcome the family of FANCJ-like helicases to the block of genome stability maintenance proteins. Cell Mol Life Sci. 2009;66(7):1209–22.

    CAS  PubMed  PubMed Central  Google Scholar 

  52. White MF. Structure, function and evolution of the XPD family of iron-sulfur-containing 5’–>3’ DNA helicases. Biochem Soc Trans. 2009;37(Pt 3):547–51.

    CAS  PubMed  Google Scholar 

  53. Drapkin R, Reardon JT, Ansari A, Huang JC, Zawel L, Ahn K, et al. Dual role of TFIIH in DNA excision repair and in transcription by RNA polymerase II. Nature. 1994;368(6473):769–72.

    CAS  PubMed  Google Scholar 

  54. Sung P, Bailly V, Weber C, Thompson LH, Prakash L, Prakash S. Human xeroderma pigmentosum group D gene encodes a DNA helicase. Nature. 1993;365(6449):852–5.

    CAS  PubMed  Google Scholar 

  55. Farina A, Shin JH, Kim DH, Bermudez VP, Kelman Z, Seo YS, et al. Studies with the human cohesin establishment factor, ChlR1. Association of ChlR1 with Ctf18-RFC and Fen1. J Biol Chem. 2008;283(30):20925–36.

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Parish JL, Rosa J, Wang X, Lahti JM, Doxsey SJ, Androphy EJ. The DNA helicase ChlR1 is required for sister chromatid cohesion in mammalian cells. J Cell Sci. 2006;119(pt 23):4857–65.

    CAS  PubMed  Google Scholar 

  57. Cantor SB, Bell DW, Ganesan S, Kass EM, Drapkin R, Grossman S, et al. BACH1, a novel helicase-like protein, interacts directly with BRCA1 and contributes to its DNA repair function. Cell. 2001;105(1):149–60.

    CAS  PubMed  Google Scholar 

  58. Ding H, Schertzer M, Wu X, Gertsenstein M, Selig S, Kammori M, et al. Regulation of murine telomere length by Rtel: an essential gene encoding a helicase-like protein. Cell. 2004;117(7):873–86.

    CAS  PubMed  Google Scholar 

  59. Honda M, Park J, Pugh RA, Ha T, Spies M. Single-molecule analysis reveals differential effect of ssDNA-binding proteins on DNA translocation by XPD helicase. Mol Cell. 2009;35(5):694–703.

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Fromme JC, Banerjee A, Huang SJ, Verdine GL. Structural basis for removal of adenine mispaired with 8-oxoguanine by MutY adenine DNA glycosylase. Nature. 2004;427(6975):652–6.

    CAS  PubMed  Google Scholar 

  61. Guan Y, Manuel RC, Arvai AS, Parikh SS, Mol CD, Miller JH, et al. MutY catalytic core, mutant and bound adenine structures define specificity for DNA repair enzyme superfamily. Nat Struct Biol. 1998;5(12):1058–64.

    CAS  PubMed  Google Scholar 

  62. Thayer MM, Ahern H, Xing D, Cunningham RP, Tainer JA. Novel DNA binding motifs in the DNA repair enzyme endonuclease III crystal structure. EMBO J. 1995;14(16):4108–20.

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Boal AK, Yavin E, Lukianova OA, O’Shea VL, David SS, Barton JK. DNA-bound redox activity of DNA repair glycosylases containing [4Fe-4S] clusters. Biochemistry. 2005;44(23):8397–407.

    CAS  PubMed  Google Scholar 

  64. Merino EJ, Boal AK, Barton JK. Biological contexts for DNA charge transport chemistry. Curr Opin Chem Biol. 2008;12(2):229–37.

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Boal AK, Yavin E, Barton JK. DNA repair glycosylases with a [4Fe-4S] cluster: a redox cofactor for DNA-mediated charge transport? J Inorg Biochem. 2007;101(11–12):1913–21.

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Mui TP, Fuss JO, Ishida JP, Tainer JA, Barton JK. ATP-stimulated, DNA-mediated redox signaling by XPD, a DNA repair and transcription helicase. J Am Chem Soc. 2011;133:16378–81.

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Mathieu N, Kaczmarek N, Naegeli H. Strand- and site-specific DNA lesion demarcation by the xeroderma pigmentosum group D helicase. Proc Natl Acad Sci USA. 2010;107:17545–50.

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Sontz PA, Mui TP, Fuss JO, Tainer JA, Barton JK. DNA charge transport as a first step in coordinating the detection of lesions by repair proteins. Proc Natl Acad Sci USA. 2012;109(6):1856–61.

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Suhasini AN, Sommers JA, Mason AC, Voloshin ON, Camerini-Otero RD, Wold MS, et al. FANCJ helicase uniquely senses oxidative base damage in either strand of duplex DNA and is stimulated by replication protein A to unwind the damaged DNA substrate in a strand-specific manner. J Biol Chem. 2009;284(27):18458–70.

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Song L, Yuan F, Zhang Y. Does a helicase activity help mismatch repair in eukaryotes? IUBMB Life. 2010;62(7):548–53.

    CAS  PubMed  Google Scholar 

  71. Fukui K. DNA mismatch repair in eukaryotes and bacteria. J Nucleic Acids. 2010;2010:1–6.

    Google Scholar 

  72. Matson SW, Robertson AB. The UvrD helicase and its modulation by the mismatch repair protein MutL. Nucleic Acids Res. 2006;34(15):4089–97.

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Maluf NK, Ali JA, Lohman TM. Kinetic mechanism for formation of the active, dimeric UvrD helicase-DNA complex. J Biol Chem. 2003;278(34):31930–40.

    CAS  PubMed  Google Scholar 

  74. Ali JA, Lohman TM. Kinetic measurement of the step size of DNA unwinding by Escherichia coli UvrD helicase. Science. 1997;275(5298):377–80.

    CAS  PubMed  Google Scholar 

  75. Dao V, Modrich P. Mismatch-, MutS-, MutL-, and helicase II-dependent unwinding from the single-strand break of an incised heteroduplex. J Biol Chem. 1998;273(15):9202–7.

    CAS  PubMed  Google Scholar 

  76. Hall MC, Jordan JR, Matson SW. Evidence for a physical interaction between the Escherichia coli methyl-directed mismatch repair proteins MutL and UvrD. EMBO J. 1998;17(5):1535–41.

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Hall MC, Matson SW. The Escherichia coli MutL protein physically interacts with MutH and stimulates the MutH-associated endonuclease activity. J Biol Chem. 1999;274(3):1306–12.

    CAS  PubMed  Google Scholar 

  78. Mechanic LE, Frankel BA, Matson SW. Escherichia coli MutL loads DNA helicase II onto DNA. J Biol Chem. 2000;275(49):38337–46.

    CAS  PubMed  Google Scholar 

  79. Jiricny J. The multifaceted mismatch-repair system. Nat Rev Mol Cell Biol. 2006;7(5):335–46.

    CAS  PubMed  Google Scholar 

  80. Zhang Y, Yuan F, Presnell SR, Tian K, Gao Y, Tomkinson AE, et al. Reconstitution of 5’-directed human mismatch repair in a purified system. Cell. 2005;122(5):693–705.

    CAS  PubMed  Google Scholar 

  81. Dzantiev L, Constantin N, Genschel J, Iyer RR, Burgers PM, Modrich P. A defined human system that supports bidirectional mismatch-provoked excision. Mol Cell. 2004;15(1):31–41.

    CAS  PubMed  Google Scholar 

  82. Genschel J, Modrich P. Mechanism of 5’-directed excision in human mismatch repair. Mol Cell. 2003;12(5):1077–86.

    CAS  PubMed  Google Scholar 

  83. Lindahl T. Instability and decay of the primary structure of DNA. Nature. 1993;362(6422):709–15.

    CAS  PubMed  Google Scholar 

  84. Sedgwick B, Bates PA, Paik J, Jacobs SC, Lindahl T. Repair of alkylated DNA: recent advances. DNA Repair. 2007;6(4):429–42.

    CAS  PubMed  Google Scholar 

  85. Kavli B, Otterlei M, Slupphaug G, Krokan HE. Uracil in DNA–general mutagen, but normal intermediate in acquired immunity. DNA Repair. 2007;6(4):505–16.

    CAS  PubMed  Google Scholar 

  86. Kubota Y, Nash RA, Klungland A, Schar P, Barnes DE, Lindahl T. Reconstitution of DNA base excision-repair with purified human proteins: interaction between DNA polymerase beta and the XRCC1 protein. EMBO J. 1996;15(23):6662–70.

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Kim K, Biade S, Matsumoto Y. Involvement of flap endonuclease 1 in base excision DNA repair. J Biol Chem. 1998;273(15):8842–8.

    CAS  PubMed  Google Scholar 

  88. Klungland A, Lindahl T. Second pathway for completion of human DNA base excision-repair: reconstitution with purified proteins and requirement for DNase IV (FEN1). EMBO J. 1997;16(11):3341–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Robertson AB, Klungland A, Rognes T, Leiros I. DNA repair in mammalian cells: base excision repair: the long and short of it. Cell Mol Life Sci. 2009;66(6):981–93.

    CAS  PubMed  Google Scholar 

  90. Martin GM, Oshima J, Gray MD, Poot M. What geriatricians should know about the Werner syndrome. J Am Geriatr Soc. 1999;47(9):1136–44.

    CAS  PubMed  Google Scholar 

  91. Martin GM, Oshima J. Lessons from human progeroid syndromes. Nature. 2000;408(6809):263–6.

    CAS  PubMed  Google Scholar 

  92. Bohr VA, Deficient DNA. repair in the human progeroid disorder, Werner syndrome. Mutat Res. 2005;577(1–2):252–9.

    CAS  PubMed  Google Scholar 

  93. Blank A, Bobola MS, Gold B, Varadarajan S, D Kolstoe D, Meade EH, et al. The Werner syndrome protein confers resistance to the DNA lesions N3-methyladenine and O6-methylguanine: implications for WRN function. DNA Repair. 2004;3(6):629–38.

    CAS  PubMed  Google Scholar 

  94. Harrigan JA, Wilson III DM, Prasad R, Opresko PL, Beck G, May A, et al. The Werner syndrome protein operates in base excision repair and cooperates with DNA polymerase beta. Nucleic Acids Res. 2006;34(2):745–54.

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Imamura O, Fujita K, Itoh C, Takeda S, Furuichi Y, Matsumoto T. Werner and Bloom helicases are involved in DNA repair in a complementary fashion. Oncogene. 2002;21(6):954–63.

    CAS  PubMed  Google Scholar 

  96. Szekely AM, Bleichert F, Numann A, Van Komen S, Manasanch E, Ben Nasr A, et al. Werner protein protects nonproliferating cells from oxidative DNA damage. Mol Cell Biol. 2005;25(23):10492–506.

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Von Kobbe C, May A, Grandori C, Bohr VA. Werner syndrome cells escape hydrogen peroxide-induced cell proliferation arrest. FASEB J. 2004;18(15):1970–2.

    Google Scholar 

  98. Ahn B, Harrigan JA, Indig FE, Wilson III DM, Bohr VA. Regulation of WRN helicase activity in human base excision repair. J Biol Chem. 2004;279(51):53465–74.

    CAS  PubMed  Google Scholar 

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Kuper, J., Kisker, C. (2013). DNA Helicases in NER, BER, and MMR. In: Spies, M. (eds) DNA Helicases and DNA Motor Proteins. Advances in Experimental Medicine and Biology, vol 767. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-5037-5_10

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