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Tyrosyl-DNA-Phosphodiesterase

  • Thomas S. Dexheimer
  • Shar-yin N. Huang
  • Benu Brata Das
  • Yves Pommier
Chapter
Part of the Cancer Drug Discovery and Development book series (CDD&D)

Abstract

The abortive activity of DNA topoisomerase I (Top1) can lead to DNA single-strand breaks with 3′-protein adducts termed Top1-DNA cleavage complexes. Repair of these DNA lesions in a prompt and accurate manner is essential for cell survival. One of the cellular pathways for repairing such DNA lesions involves tyrosyl-DNA phosphodiesterase 1 (Tdp1). Tdp1 hydrolyzes the phosphodiester bond between a tyrosine residue and a terminal 3′-phosphate of DNA, the type of linkage found in Top1-DNA cleavage complexes. A mutation in Tdp1 is found to cause a rare heredity neurodegenerative disease, spinocerebellar ataxia with axonal neuropathy (SCAN1). Efforts to elucidate the mechanism of Tdp1-depedent DNA repair pathway have identified several other proteins, which form a complex response network with Tdp1. Conversely, structural and biochemical studies suggest that Tdp1 can act on a broad spectrum of 3′-phosphodiester linkages, potentially implicating Tdp1 in other DNA repair pathways. In this chapter we summarize the recent advances in research concerning Tdp1, alternative repair pathways for repairing Top1-induced DNA damage, and the rational for targeting Tdp1 as a potential anticancer therapy.

Keywords

Spinocerebellar Ataxia Phosphodiester Bond Cleavage Complex Base Excision Repair Pathway SCAN1 Patient 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Antony S, Marchand C, Stephen AG, Thibaut L, Agama KK, Fisher RJ, Pommier Y (2007) Novel high-throughput electrochemiluminescent assay for identification of human tyrosyl-DNA phosphodiesterase (Tdp1) inhibitors and characterization of furamidine (NSC 305831) as an inhibitor of Tdp1. Nucleic Acids Res 35(13): 4474–4484PubMedCentralPubMedGoogle Scholar
  2. Audebert M, Salles B, Calsou P (2004) Involvement of poly(ADP-ribose) polymerase-1 and XRCC1/DNA ligase III in an alternative route for DNA double-strand breaks rejoining. J Biol Chem 279(53): 55117–55126PubMedGoogle Scholar
  3. Bakkenist CJ, Kastan MB (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421(6922): 499–506PubMedGoogle Scholar
  4. Banerjee B, Roy A, Sen N, Majumder HK (2010) A Tyrosyl DNA phosphodiesterase 1 from kinetoplastid parasite Leishmania donovani (LdTdp1) capable of removing Topo I-DNA covalent complexes. Mol Microbiol PubMedGoogle Scholar
  5. Barthelmes HU, Habermeyer M, Christensen MO, Mielke C, Interthal H, Pouliot JJ, Boege F, Marko D (2004) TDP1 overexpression in human cells counteracts DNA damage mediated by topoisomerases I and II. J Biol Chem 279(53): 55618–55625PubMedGoogle Scholar
  6. Bastin-Shanower SA, Fricke WM, Mullen JR, Brill SJ (2003) The mechanism of Mus81-Mms4 cleavage site selection distinguishes it from the homologous endonuclease Rad1-Rad10. Mol Cell Biol 23(10): 3487–3496PubMedCentralPubMedGoogle Scholar
  7. Beretta GL, Cossa G, Gatti L, Zunino F, Perego P (2010) Tyrosyl-DNA phosphodiesterase 1 targeting for modulation of camptothecin-based treatment. Curr Med Chem 17(15): 1500–1508PubMedGoogle Scholar
  8. Caldecott KW (2007) Mammalian single-strand break repair: mechanisms and links with chromatin. DNA Repair (Amst) 6(4): 443–453Google Scholar
  9. Caldecott KW (2008) Single-strand break repair and genetic disease. Nat Rev Genet 9(8): 619–631PubMedGoogle Scholar
  10. Chatterjee S, Cheng MF, Trivedi D, Petzold SJ, Berger NA (1989) Camptothecin hypersensitivity in poly(adenosine diphosphate-ribose) polymerase-deficient cell lines. Cancer Commun 1(6): 389–394PubMedGoogle Scholar
  11. Cheng TJ, Rey PG, Poon T, Kan CC (2002) Kinetic studies of human tyrosyl-DNA phosphodiesterase, an enzyme in the topoisomerase I DNA repair pathway. Eur J Biochem 269(15): 3697–3704PubMedGoogle Scholar
  12. Chiang SC, Carroll J, El-Khamisy SF (2010) TDP1 serine 81 promotes interaction with DNA ligase IIIalpha and facilitates cell survival following DNA damage. Cell Cycle 9(3): 588–595PubMedGoogle Scholar
  13. Chou WC, Wang HC, Wong FH, Ding SL, Wu PE, Shieh SY, Shen CY (2008) Chk2-dependent phosphorylation of XRCC1 in the DNA damage response promotes base excision repair. EMBO J 27(23): 3140–3150PubMedCentralPubMedGoogle Scholar
  14. Ciccia A, McDonald N, West SC (2008) Structural and functional relationships of the XPF/MUS81 family of proteins. Annu Rev Biochem 77: 259–287PubMedGoogle Scholar
  15. Cimprich KA, Cortez D (2008) ATR: an essential regulator of genome integrity. Nat Rev Mol Cell Biol 9(8): 616–627PubMedCentralPubMedGoogle Scholar
  16. Cortes Ledesma F, El Khamisy SF, Zuma MC, Osborn K, Caldecott KW (2009) A human 5’-tyrosyl DNA phosphodiesterase that repairs topoisomerase-mediated DNA damage. Nature 461(7264): 674–678PubMedGoogle Scholar
  17. D’Amours D, Jackson SP (2002) The Mre11 complex: at the crossroads of dna repair and checkpoint signalling. Nat Rev Mol Cell Biol 3(5): 317–327PubMedGoogle Scholar
  18. D’Onofrio G, Tramontano F, Dorio AS, Muzi A, Maselli V, Fulgione D, Graziani G, Malanga M, Quesada P (2010) Poly(Adp-ribose) polymerase signaling of topoisomerase 1-dependent DNA damage in carcinoma cells. Biochem Pharmacol PubMedGoogle Scholar
  19. Das BB, Antony S, Gupta S, Dexheimer TS, Redon CE, Garfield S, Shiloh Y, Pommier Y (2009) Optimal function of the DNA repair enzyme TDP1 requires its phosphorylation by ATM and/or DNA-PK. EMBO J 28(23): 3667–3680PubMedCentralPubMedGoogle Scholar
  20. Das BB, Dexheimer TS, Maddali K, Pommier Y (2010) Role of tyrosyl-DNA phosphodiesterase (TDP1) in mitochondria. Proc Natl Acad Sci USA 107(46): 19790–19795PubMedCentralPubMedGoogle Scholar
  21. Davies DR, Interthal H, Champoux JJ, Hol WG (2002a) Insights into substrate binding and catalytic mechanism of human tyrosyl-DNA phosphodiesterase (Tdp1) from vanadate and tungstate-inhibited structures. J Mol Biol 324(5): 917–932PubMedGoogle Scholar
  22. Davies DR, Interthal H, Champoux JJ, Hol WG (2002b) The crystal structure of human tyrosyl-DNA phosphodiesterase, Tdp1. Structure 10(2): 237–248PubMedGoogle Scholar
  23. Davies DR, Interthal H, Champoux JJ, Hol WGJ (2003) Crystal structure of a transition state mimic for Tdp1 assembled from vanadate, DNA, and a topoisomerase I-derived peptide. Chem Biol 10(2): 139–147PubMedGoogle Scholar
  24. Davies DR, Interthal H, Champoux JJ, Hol WG (2004) Explorations of peptide and oligonucleotide binding sites of tyrosyl-DNA phosphodiesterase using vanadate complexes. J Med Chem 47(4): 829–837PubMedGoogle Scholar
  25. de Laat WL, Appeldoorn E, Jaspers NG, Hoeijmakers JH (1998) DNA structural elements required for ERCC1-XPF endonuclease activity. J Biol Chem 273(14): 7835–7842PubMedGoogle Scholar
  26. Debethune L, Kohlhagen G, Grandas A, Pommier Y (2002) Processing of nucleopeptides mimicking the topoisomerase I-DNA covalent complex by tyrosyl-DNA phosphodiesterase. Nucleic Acids Res 30(5): 1198–1204PubMedCentralPubMedGoogle Scholar
  27. Deng C, Brown JA, You D, Brown JM (2005) Multiple endonucleases function to repair covalent topoisomerase I complexes in Saccharomyces cerevisiae. Genetics 170(2): 591–600PubMedCentralPubMedGoogle Scholar
  28. Dexheimer TS, Antony S, Marchand C, Pommier Y (2008) Tyrosyl-DNA phosphodiesterase as a target for anticancer therapy. Anticancer Agents Med Chem 8(4): 381–389PubMedCentralPubMedGoogle Scholar
  29. Dexheimer TS, Gediya LK, Stephen AG, Weidlich I, Antony S, Marchand C, Interthal H, Nicklaus M, Fisher RJ, Njar VC, Pommier Y (2009) 4-Pregnen-21-ol-3,20-dione-21-(4-bromobenzenesulfonate) (NSC 88915) and related novel steroid derivatives as tyrosyl-DNA phosphodiesterase (Tdp1) inhibitors. J Med Chem 52(22): 7122–7131PubMedCentralPubMedGoogle Scholar
  30. Dexheimer TS, Stephen AG, Fivash MJ, Fisher RJ, Pommier Y (2010) The DNA binding and 3’-end preferential activity of human tyrosyl-DNA phosphodiesterase. Nucleic Acids Res 38(7): 2444–2452PubMedCentralPubMedGoogle Scholar
  31. El-Khamisy SF (2011) To live or to die: a matter of processing damaged DNA termini in neurons. Embo Mol Med 3(2): 78–88PubMedCentralPubMedGoogle Scholar
  32. El-Khamisy SF, Saifi GM, Weinfeld M, Johansson F, Helleday T, Lupski JR, Caldecott KW (2005) Defective DNA single-strand break repair in spinocerebellar ataxia with axonal neuropathy-1. Nature 434(7029): 108–113PubMedGoogle Scholar
  33. Farmer H, McCabe N, Lord CJ, Tutt AN, Johnson DA, Richardson TB, Santarosa M, Dillon KJ, Hickson I, Knights C, Martin NM, Jackson SP, Smith GC, Ashworth A (2005) Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434(7035): 917–921PubMedGoogle Scholar
  34. Friedberg EC (2001) How nucleotide excision repair protects against cancer. Nat Rev Cancer 1(1): 22–33PubMedGoogle Scholar
  35. Furuta T, Takemura H, Liao ZY, Aune GJ, Redon C, Sedelnikova OA, Pilch DR, Rogakou EP, Celeste A, Chen HT, Nussenzweig A, Aladjem MI, Bonner WM, Pommier Y (2003) Phosphorylation of histone H2AX and activation of Mre11, Rad50, and Nbs1 in response to replication-dependent DNA double-strand breaks induced by mammalian DNA topoisomerase I cleavage complexes. J Biol Chem 278(22): 20303–20312PubMedGoogle Scholar
  36. Gottlin EB, Rudolph AE, Zhao Y, Matthews HR, Dixon JE (1998) Catalytic mechanism of the phospholipase D superfamily proceeds via a covalent phosphohistidine intermediate. Proc Natl Acad Sci USA 95(16): 9202–9207PubMedCentralPubMedGoogle Scholar
  37. Guzder SN, Torres-Ramos C, Johnson RE, Haracska L, Prakash L, Prakash S (2004) Requirement of yeast Rad1-Rad10 nuclease for the removal of 3’-blocked termini from DNA strand breaks induced by reactive oxygen species. Genes Dev 18(18): 2283–2291PubMedCentralPubMedGoogle Scholar
  38. Hamilton NK, Maizels N (2010) MRE11 Function in Response to Topoisomerase Poisons Is Independent of its Function in Double-Strand Break Repair in Saccharomyces cerevisiae. PLoS One 5(10): e15387PubMedCentralPubMedGoogle Scholar
  39. Hartsuiker E, Neale MJ, Carr AM (2009) Distinct requirements for the Rad32(Mre11) nuclease and Ctp1(CtIP) in the removal of covalently bound topoisomerase I and II from DNA. Mol Cell 33(1): 117–123PubMedCentralPubMedGoogle Scholar
  40. Hawkins AJ, Subler MA, Akopiants K, Wiley JL, Taylor SM, Rice AC, Windle JJ, Valerie K, Povirk LF (2009) In vitro complementation of Tdp1 deficiency indicates a stabilized enzyme-DNA adduct from tyrosyl but not glycolate lesions as a consequence of the SCAN1 mutation. DNA Repair (Amst) 8(5): 654–663Google Scholar
  41. Helleday T, Petermann E, Lundin C, Hodgson B, Sharma RA (2008) DNA repair pathways as targets for cancer therapy. Nat Rev Cancer 8(3): 193–204PubMedGoogle Scholar
  42. Hirano R, Interthal H, Huang C, Nakamura T, Deguchi K, Choi K, Bhattacharjee MB, Arimura K, Umehara F, Izumo S, Northrop JL, Salih MA, Inoue K, Armstrong DL, Champoux JJ, Takashima H, Boerkoel CF (2007) Spinocerebellar ataxia with axonal neuropathy: consequence of a Tdp1 recessive neomorphic mutation? EMBO J 26(22): 4732–4743PubMedCentralPubMedGoogle Scholar
  43. Horton JK, Watson M, Stefanick DF, Shaughnessy DT, Taylor JA, Wilson SH (2008) XRCC1 and DNA polymerase beta in cellular protection against cytotoxic DNA single-strand breaks. Cell Res 18(1): 48–63PubMedCentralPubMedGoogle Scholar
  44. Inamdar KV, Pouliot JJ, Zhou T, Lees-Miller SP, Rasouli-Nia A, Povirk LF (2002) Conversion of phosphoglycolate to phosphate termini on 3’ overhangs of DNA double strand breaks by the human tyrosyl-DNA phosphodiesterase hTdp1. J Biol Chem 277(30): 27162–27168PubMedGoogle Scholar
  45. Interthal H, Chen HJ, Champoux JJ (2005a) Human Tdp1 cleaves a broad spectrum of substrates, including phosphoamide linkages. J Biol Chem 280(43): 36518–36528PubMedCentralPubMedGoogle Scholar
  46. Interthal H, Chen HJ, Kehl-Fie TE, Zotzmann J, Leppard JB, Champoux JJ (2005b) SCAN1 mutant Tdp1 accumulates the enzyme--DNA intermediate and causes camptothecin hypersensitivity. EMBO J 24(12): 2224–2233PubMedCentralPubMedGoogle Scholar
  47. Interthal H, Pouliot JJ, Champoux JJ (2001) The tyrosyl-DNA phosphodiesterase Tdp1 is a member of the phospholipase D superfamily. Proc Natl Acad Sci USA 98(21): 12009–12014PubMedCentralPubMedGoogle Scholar
  48. Iwasaki Y, Horiike S, Matsushima K, Yamane T (1999) Location of the catalytic nucleophile of phospholipase D of Streptomyces antibioticus in the C-terminal half domain. Eur J Biochem 264(2): 577–581PubMedGoogle Scholar
  49. Katyal S, el-Khamisy SF, Russell HR, Li Y, Ju L, Caldecott KW, McKinnon PJ (2007) TDP1 facilitates chromosomal single-strand break repair in neurons and is neuroprotective in vivo. EMBO J 26(22): 4720–4731PubMedCentralPubMedGoogle Scholar
  50. Kennedy RD, D’Andrea AD (2006) DNA repair pathways in clinical practice: lessons from pediatric cancer susceptibility syndromes. J Clin Oncol 24(23): 3799–3808PubMedGoogle Scholar
  51. Koonin EV (1996) A duplicated catalytic motif in a new superfamily of phosphohydrolases and phospholipid synthases that includes poxvirus envelope proteins. Trends Biochem Sci 21(7): 242–243PubMedGoogle Scholar
  52. Lavin MF (2008) Ataxia-telangiectasia: from a rare disorder to a paradigm for cell signalling and cancer. Nat Rev Mol Cell Biol 9(10): 759–769PubMedGoogle Scholar
  53. Lee JH, Paull TT (2007) Activation and regulation of ATM kinase activity in response to DNA double-strand breaks. Oncogene 26(56): 7741–7748PubMedGoogle Scholar
  54. Lee SY, Kim H, Hwang HJ, Jeong YM, Na SH, Woo JC, Kim SG (2010) Identification of tyrosyl-DNA phosphodiesterase as a novel DNA damage repair enzyme in Arabidopsis. Plant Physiol 154(3): 1460–1469PubMedCentralPubMedGoogle Scholar
  55. Leiros I, Secundo F, Zambonelli C, Servi S, Hough E (2000) The first crystal structure of a phospholipase D. Structure 8(6): 655–667PubMedGoogle Scholar
  56. Levy N, Martz A, Bresson A, Spenlehauer C, de Murcia G, Menissier-de Murcia J (2006) XRCC1 is phosphorylated by DNA-dependent protein kinase in response to DNA damage. Nucleic Acids Res 34(1): 32–41PubMedCentralPubMedGoogle Scholar
  57. Lindahl T (1993) Instability and decay of the primary structure of DNA. Nature 362(6422): 709–715PubMedGoogle Scholar
  58. Lindahl T, Wood RD (1999) Quality control by DNA repair. Science 286(5446): 1897–1905PubMedGoogle Scholar
  59. Liscovitch M, Czarny M, Fiucci G, Tang X (2000) Phospholipase D: molecular and cell biology of a novel gene family. Biochem J 345 Pt 3: 401–415PubMedCentralPubMedGoogle Scholar
  60. Liu C, Pouliot JJ, Nash HA (2002) Repair of topoisomerase I covalent complexes in the absence of the tyrosyl-DNA phosphodiesterase Tdp1. Proc Natl Acad Sci USA 99(23): 14970–14975PubMedCentralPubMedGoogle Scholar
  61. Macovei A, Balestrazzi A, Confalonieri M, Carbonera D (2010) The tyrosyl-DNA phosphodiesterase gene family in Medicago truncatula Gaertn.: bioinformatic investigation and expression profiles in response to copper- and PEG-mediated stress. Planta 232(2): 393–407PubMedGoogle Scholar
  62. Marchand C, Lea WA, Jadhav A, Dexheimer TS, Austin CP, Inglese J, Pommier Y, Simeonov A (2009) Identification of phosphotyrosine mimetic inhibitors of human tyrosyl-DNA phosphodiesterase I by a novel AlphaScreen high-throughput assay. Mol Cancer Ther 8(1): 240–248PubMedCentralPubMedGoogle Scholar
  63. Martin LP, Hamilton TC, Schilder RJ (2008) Platinum resistance: the role of DNA repair pathways. Clin Cancer Res 14(5): 1291–1295PubMedGoogle Scholar
  64. Matsuoka S, Ballif BA, Smogorzewska A, McDonald ER, 3rd, Hurov KE, Luo J, Bakalarski CE, Zhao Z, Solimini N, Lerenthal Y, Shiloh Y, Gygi SP, Elledge SJ (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316(5828): 1160–1166PubMedGoogle Scholar
  65. McKinnon PJ (2009) DNA repair deficiency and neurological disease. Nat Rev Neurosci 10(2): 100–112PubMedCentralPubMedGoogle Scholar
  66. Miao ZH, Agama K, Sordet O, Povirk L, Kohn KW, Pommier Y (2006) Hereditary ataxia SCAN1 cells are defective for the repair of transcription-dependent topoisomerase I cleavage complexes. DNA Repair (Amst) 5(12): 1489–1494Google Scholar
  67. Nilsen H, Rosewell I, Robins P, Skjelbred CF, Andersen S, Slupphaug G, Daly G, Krokan HE, Lindahl T, Barnes DE (2000) Uracil-DNA glycosylase (UNG)-deficient mice reveal a primary role of the enzyme during DNA replication. Mol Cell 5(6): 1059–1065PubMedGoogle Scholar
  68. Nitiss KC, Malik M, He X, White SW, Nitiss JL (2006) Tyrosyl-DNA phosphodiesterase (Tdp1) participates in the repair of Top2-mediated DNA damage. Proc Natl Acad Sci USA 103(24): 8953–8958PubMedCentralPubMedGoogle Scholar
  69. Nivens MC, Felder T, Galloway AH, Pena MM, Pouliot JJ, Spencer HT (2004) Engineered resistance to camptothecin and antifolates by retroviral coexpression of tyrosyl DNA phosphodiesterase-I and thymidylate synthase. Cancer Chemother Pharmacol 53(2): 107–115PubMedGoogle Scholar
  70. Nocentini S (1999) Rejoining kinetics of DNA single- and double-strand breaks in normal and DNA ligase-deficient cells after exposure to ultraviolet C and gamma radiation: an evaluation of ligating activities involved in different DNA repair processes. Radiat Res 151(4): 423–432PubMedGoogle Scholar
  71. Parsons AB, Brost RL, Ding H, Li Z, Zhang C, Sheikh B, Brown GW, Kane PM, Hughes TR, Boone C (2004) Integration of chemical-genetic and genetic interaction data links bioactive compounds to cellular target pathways. Nat Biotechnol 22(1): 62–69PubMedGoogle Scholar
  72. Parsons JL, Elder RH (2003) DNA N-glycosylase deficient mice: a tale of redundancy. Mutat Res 531(1–2): 165–175PubMedGoogle Scholar
  73. Plo I, Liao ZY, Barcelo JM, Kohlhagen G, Caldecott KW, Weinfeld M, Pommier Y (2003) Association of XRCC1 and tyrosyl DNA phosphodiesterase (Tdp1) for the repair of topoisomerase I-mediated DNA lesions. DNA Repair (Amst) 2(10): 1087–1100Google Scholar
  74. Pommier Y (2009) DNA topoisomerase I inhibitors: chemistry, biology, and interfacial inhibition. Chem Rev 109(7): 2894–2902PubMedCentralPubMedGoogle Scholar
  75. Pommier Y, Barcelo JM, Rao VA, Sordet O, Jobson AG, Thibaut L, Miao ZH, Seiler JA, Zhang H, Marchand C, Agama K, Nitiss JL, Redon C (2006) Repair of topoisomerase I-mediated DNA damage. Prog Nucleic Acid Res Mol Biol 81: 179–229PubMedCentralPubMedGoogle Scholar
  76. Pommier Y, Redon C, Rao VA, Seiler JA, Sordet O, Takemura H, Antony S, Meng L, Liao Z, Kohlhagen G, Zhang H, Kohn KW (2003) Repair of and checkpoint response to topoisomerase I-mediated DNA damage. Mutat Res 532(1–2): 173–203PubMedGoogle Scholar
  77. Ponting CP, Kerr ID (1996) A novel family of phospholipase D homologues that includes phospholipid synthases and putative endonucleases: identification of duplicated repeats and potential active site residues. Protein Sci 5(5): 914–922PubMedCentralPubMedGoogle Scholar
  78. Pouliot JJ, Robertson CA, Nash HA (2001) Pathways for repair of topoisomerase I covalent complexes in Saccharomyces cerevisiae. Genes Cells 6(8): 677–687PubMedGoogle Scholar
  79. Pouliot JJ, Yao KC, Robertson CA, Nash HA (1999) Yeast gene for a Tyr-DNA phosphodiesterase that repairs topoisomerase I complexes. Science 286(5439): 552–555PubMedGoogle Scholar
  80. Rass U, Ahel I, West SC (2007) Defective DNA repair and neurodegenerative disease. Cell 130(6): 991–1004PubMedGoogle Scholar
  81. Raymond AC, Rideout MC, Staker B, Hjerrild K, Burgin AB, Jr. (2004) Analysis of human tyrosyl-DNA phosphodiesterase I catalytic residues. J Mol Biol 338(5): 895–906PubMedGoogle Scholar
  82. Raymond AC, Staker BL, Burgin AB, Jr. (2005) Substrate specificity of tyrosyl-DNA phosphodiesterase I (Tdp1). J Biol Chem 280(23): 22029–22035PubMedGoogle Scholar
  83. Redinbo MR, Stewart L, Kuhn P, Champoux JJ, Hol WG (1998) Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA. Science 279(5356): 1504–1513PubMedGoogle Scholar
  84. Reid RJ, Gonzalez-Barrera S, Sunjevaric I, Alvaro D, Ciccone S, Wagner M, Rothstein R (2011) Selective ploidy ablation, a high-throughput plasmid transfer protocol, identifies new genes affecting topoisomerase I-induced DNA damage. Genome Res 21(3): 477–486PubMedCentralPubMedGoogle Scholar
  85. Rideout MC, Raymond AC, Burgin AB, Jr. (2004) Design and synthesis of fluorescent substrates for human tyrosyl-DNA phosphodiesterase I. Nucleic Acids Res 32(15): 4657–4664PubMedCentralPubMedGoogle Scholar
  86. Rosell R, Skrzypski M, Jassem E, Taron M, Bartolucci R, Sanchez JJ, Mendez P, Chaib I, Perez-Roca L, Szymanowska A, Rzyman W, Puma F, Kobierska-Gulida G, Farabi R, Jassem J (2007) BRCA1: a novel prognostic factor in resected non-small-cell lung cancer. PLoS ONE 2(11): e1129PubMedCentralPubMedGoogle Scholar
  87. Rosidi B, Wang M, Wu W, Sharma A, Wang H, Iliakis G (2008) Histone H1 functions as a stimulatory factor in backup pathways of NHEJ. Nucleic Acids Res 36(5): 1610–1623PubMedCentralPubMedGoogle Scholar
  88. Rudolph AE, Stuckey JA, Zhao Y, Matthews HR, Patton WA, Moss J, Dixon JE (1999) Expression, characterization, and mutagenesis of the Yersinia pestis murine toxin, a phospholipase D superfamily member. J Biol Chem 274(17): 11824–11831PubMedGoogle Scholar
  89. Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S (2004) Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 73: 39–85PubMedGoogle Scholar
  90. Schreiber V, Dantzer F, Ame JC, de Murcia G (2006) Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol 7(7): 517–528PubMedGoogle Scholar
  91. Seiler JA, Conti C, Syed A, Aladjem MI, Pommier Y (2007) The intra-S-phase checkpoint affects both DNA replication initiation and elongation: single-cell and -DNA fiber analyses. Mol Cell Biol 27(16): 5806–5818PubMedCentralPubMedGoogle Scholar
  92. Shiloh Y (2006) The ATM-mediated DNA-damage response: taking shape. Trends Biochem Sci 31(7): 402–410PubMedGoogle Scholar
  93. Sijbers AM, de Laat WL, Ariza RR, Biggerstaff M, Wei YF, Moggs JG, Carter KC, Shell BK, Evans E, de Jong MC, Rademakers S, de Rooij J, Jaspers NG, Hoeijmakers JH, Wood RD (1996) Xeroderma pigmentosum group F caused by a defect in a structure-specific DNA repair endonuclease. Cell 86(5): 811–822PubMedGoogle Scholar
  94. Sordet O, Redon CE, Guirouilh-Barbat J, Smith S, Solier S, Douarre C, Conti C, Nakamura AJ, Das BB, Nicolas E, Kohn KW, Bonner WM, Pommier Y (2009) Ataxia telangiectasia mutated activation by transcription- and topoisomerase I-induced DNA double-strand breaks. EMBO Rep 10(8): 887–893PubMedCentralPubMedGoogle Scholar
  95. Strumberg D, Pilon AA, Smith M, Hickey R, Malkas L, Pommier Y (2000) Conversion of topoisomerase I cleavage complexes on the leading strand of ribosomal DNA into 5’-phosphorylated DNA double-strand breaks by replication runoff. Mol Cell Biol 20(11): 3977–3987PubMedCentralPubMedGoogle Scholar
  96. Stuckey JA, Dixon JE (1999) Crystal structure of a phospholipase D family member. Nat Struct Biol 6(3): 278–284PubMedGoogle Scholar
  97. Sung TC, Roper RL, Zhang Y, Rudge SA, Temel R, Hammond SM, Morris AJ, Moss B, Engebrecht J, Frohman MA (1997) Mutagenesis of phospholipase D defines a superfamily including a trans-Golgi viral protein required for poxvirus pathogenicity. EMBO J 16(15): 4519–4530PubMedCentralPubMedGoogle Scholar
  98. Takao M, Kanno S, Shiromoto T, Hasegawa R, Ide H, Ikeda S, Sarker AH, Seki S, Xing JZ, Le XC, Weinfeld M, Kobayashi K, Miyazaki J, Muijtjens M, Hoeijmakers JH, van der Horst G, Yasui A (2002) Novel nuclear and mitochondrial glycosylases revealed by disruption of the mouse Nth1 gene encoding an endonuclease III homolog for repair of thymine glycols. EMBO J 21(13): 3486–3493PubMedCentralPubMedGoogle Scholar
  99. Takashima H, Boerkoel CF, John J, Saifi GM, Salih MA, Armstrong D, Mao Y, Quiocho FA, Roa BB, Nakagawa M, Stockton DW, Lupski JR (2002) Mutation of TDP1, encoding a topoisomerase I-dependent DNA damage repair enzyme, in spinocerebellar ataxia with axonal neuropathy. Nat Genet 32(2): 267–272PubMedGoogle Scholar
  100. Toulany M, Dittmann K, Fehrenbacher B, Schaller M, Baumann M, Rodemann HP (2008) PI3K-Akt signaling regulates basal, but MAP-kinase signaling regulates radiation-induced XRCC1 expression in human tumor cells in vitro. DNA Repair (Amst) 7(10): 1746–1756Google Scholar
  101. Vance JR, Wilson TE (2002) Yeast Tdp1 and Rad1-Rad10 function as redundant pathways for repairing Top1 replicative damage. Proc Natl Acad Sci USA 99(21): 13669–13674PubMedCentralPubMedGoogle Scholar
  102. Waite M (1999) The PLD superfamily: insights into catalysis. Biochim Biophys Acta 1439(2): 187–197PubMedGoogle Scholar
  103. Walton C, Interthal H, Hirano R, Salih MA, Takashima H, Boerkoel CF (2010) Spinocerebellar ataxia with axonal neuropathy. Adv Exp Med Biol 685: 75–83PubMedGoogle Scholar
  104. Weterings E, Chen DJ (2007) DNA-dependent protein kinase in nonhomologous end joining: a lock with multiple keys? J Cell Biol 179(2): 183–186PubMedCentralPubMedGoogle Scholar
  105. Whitehouse CJ, Taylor RM, Thistlethwaite A, Zhang H, Karimi-Busheri F, Lasko DD, Weinfeld M, Caldecott KW (2001) XRCC1 stimulates human polynucleotide kinase activity at damaged DNA termini and accelerates DNA single-strand break repair. Cell 104(1): 107–117PubMedGoogle Scholar
  106. Yang SW, Burgin AB, Jr., Huizenga BN, Robertson CA, Yao KC, Nash HA (1996) A eukaryotic enzyme that can disjoin dead-end covalent complexes between DNA and type I topoisomerases. Proc Natl Acad Sci USA 93(21): 11534–11539PubMedCentralPubMedGoogle Scholar
  107. Zeng Z, Cortes-Ledesma F, El-Khamisy SF, Caldecott KW (2010) TDP2/TTRAP is the major 5’-tyrosyl DNA phosphodiesterase activity in vertebrate cells and is critical for cellular resistance to topoisomerase II-induced DNA damage. J Biol Chembrsbrs Google Scholar
  108. Zhou T, Akopiants K, Mohapatra S, Lin PS, Valerie K, Ramsden DA, Lees-Miller SP, Povirk LF (2009) Tyrosyl-DNA phosphodiesterase and the repair of 3’-phosphoglycolate-terminated DNA double-strand breaks. DNA Repair (Amst) 8(8): 901–911Google Scholar
  109. Zhou T, Lee JW, Tatavarthi H, Lupski JR, Valerie K, Povirk LF (2005) Deficiency in 3’-phosphoglycolate processing in human cells with a hereditary mutation in tyrosyl-DNA phosphodiesterase (TDP1). Nucleic Acids Res 33(1): 289–297PubMedCentralPubMedGoogle Scholar

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© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Thomas S. Dexheimer
    • 1
  • Shar-yin N. Huang
    • 2
  • Benu Brata Das
    • 2
  • Yves Pommier
    • 2
  1. 1.National Chemical Genomic CenterNational Institutes of HealthRockvilleUSA
  2. 2.Laboratory of Molecular Pharmacology, Center for Cancer ResearchNational Cancer Institute, National Institutes of HealthBethesdaUSA

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