Advertisement

Chromosoma

, Volume 123, Issue 1–2, pp 79–90 | Cite as

Poly(ADP-ribosyl)ation in regulation of chromatin structure and the DNA damage response

  • Michael Tallis
  • Rosa Morra
  • Eva Barkauskaite
  • Ivan Ahel
Review

Abstract

Poly(ADP-ribose) (PAR) is a post-translational modification of proteins and is synthesised by PAR polymerases (PARPs), which have long been associated with the coordination of the cellular response to DNA damage, amongst other processes. Binding of some PARPs such as PARP1 to broken DNA induces a substantial wave of PARylation, which results in significant re-structuring of the chromatin microenvironment through modification of chromatin-associated proteins and recruitment of chromatin-modifying proteins. Similarly, other DNA damage response proteins are recruited to the damaged sites via PAR-specific binding modules, and in this way, PAR mediates not only local chromatin architecture but also DNA repair. Here, we discuss the expanding role of PAR in the DNA damage response, with particular focus on chromatin regulation.

Keywords

Stall Replication Fork Catalytic PARP Domain Puff Locus NuRD Chromatin Remodelling Complex Chromatin Microenvironment 
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.

Notes

Acknowledgements

We are grateful to G. Timinszky and A. Jefferson for their helpful comments. This work was funded by Cancer Research UK and European Research Council (grant no. 281739).

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abd Elmageed ZY, Naura AS, Errami Y, Zerfaoui M (2012) The poly(ADP-ribose) polymerases (PARPs): new roles in intracellular transport. Cell Signal 24(1):1–8PubMedGoogle Scholar
  2. Adelfalk C, Kontou M, Hirsch-Kauffmann M, Schweiger M (2003) Physical and functional interaction of the Werner syndrome protein with poly-ADP ribosyl transferase. FEBS Lett 554(1–2):55–58PubMedGoogle Scholar
  3. Ahel D, Horejsi Z, Wiechens N, Polo SE, Garcia-Wilson E, Ahel I, Flynn H, Skehel M, West SC, Jackson SP, Owen-Hughes T, Boulton SJ (2009) Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science 325(5945):1240–1243PubMedCentralPubMedGoogle Scholar
  4. Ahel I, Ahel D, Matsusaka T, Clark AJ, Pines J, Boulton SJ, West SC (2008) Poly(ADP-ribose)-binding zinc finger motifs in DNA repair/checkpoint proteins. Nature 451(7174):81–85PubMedGoogle Scholar
  5. Ali AA, Timinszky G, Arribas-Bosacoma R, Kozlowski M, Hassa PO, Hassler M, Ladurner AG, Pearl LH, Oliver AW (2012) The zinc-finger domains of PARP1 cooperate to recognize DNA strand breaks. Nat Struct Mol Biol 19(7):685–692PubMedGoogle Scholar
  6. Althaus FR, Kleczkowska HE, Malanga M, Muntener CR, Pleschke JM, Ebner M, Auer B (1999) Poly ADP-ribosylation: a DNA break signal mechanism. Mol Cell Biochem 193(1–2):5–11PubMedGoogle Scholar
  7. Alvarez-Gonzalez R, Althaus FR (1989) Poly(ADP-ribose) catabolism in mammalian cells exposed to DNA-damaging agents. Mutat Res 218(2):67–74PubMedGoogle Scholar
  8. Alvarez-Gonzalez R, Jacobson MK (1987) Characterization of polymers of adenosine diphosphate ribose generated in vitro and in vivo. Biochemistry 26(11):3218–3224PubMedGoogle Scholar
  9. Ame JC, Fouquerel E, Gauthier LR, Biard D, Boussin FD, Dantzer F, de Murcia G, Schreiber V (2009) Radiation-induced mitotic catastrophe in PARG-deficient cells. J Cell Sci 122(Pt 12):1990–2002PubMedGoogle Scholar
  10. Ame JC, Rolli V, Schreiber V, Niedergang C, Apiou F, Decker P, Muller S, Hoger T, Menissier-de Murcia J, de Murcia G (1999) PARP-2, A novel mammalian DNA damage-dependent poly(ADP-ribose) polymerase. J Biol Chem 274(25):17860–17868PubMedGoogle Scholar
  11. Ame JC, Spenlehauer C, de Murcia G (2004) The PARP superfamily. Bioessays 26(8):882–893PubMedGoogle Scholar
  12. Aravind L (2001) The WWE domain: a common interaction module in protein ubiquitination and ADP ribosylation. Trends Biochem Sci 26(5):273–275PubMedGoogle Scholar
  13. Aubin RJ, Dam VT, Miclette J, Brousseau Y, Huletsky A, Poirier GG (1982) Hyper(ADP-ribosyl)ation of histone H1. Can J Biochem 60(12):1085–1094PubMedGoogle Scholar
  14. 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
  15. Audebert M, Salles B, Weinfeld M, Calsou P (2006) Involvement of polynucleotide kinase in a poly(ADP-ribose) polymerase-1-dependent DNA double-strand breaks rejoining pathway. J Mol Biol 356(2):257–265PubMedGoogle Scholar
  16. Barkauskaite E, Brassington A, Tan ES, Warwicker J, Dunstan MS, Banos B, Lafite P, Ahel M, Mitchison TJ, Ahel I, Leys D (2013) Visualization of poly(ADP-ribose) bound to PARG reveals inherent balance between exo- and endo-glycohydrolase activities. Nat Commun 4:2164PubMedCentralPubMedGoogle Scholar
  17. Bekker-Jensen S, Fugger K, Danielsen JR, Gromova I, Sehested M, Celis J, Bartek J, Lukas J, Mailand N (2007) Human Xip1 (C2orf13) is a novel regulator of cellular responses to DNA strand breaks. J Biol Chem 282(27):19638–19643PubMedGoogle Scholar
  18. Beneke S (2012) Regulation of chromatin structure by poly(ADP-ribosyl)ation. Front Genet 3:169PubMedCentralPubMedGoogle Scholar
  19. Berti M, Chaudhuri AR, Thangavel S, Gomathinayagam S, Kenig S, Vujanovic M, Odreman F, Glatter T, Graziano S, Mendoza-Maldonado R, Marino F, Lucic B, Biasin V, Gstaiger M, Aebersold R, Sidorova JM, Monnat RJ Jr, Lopes M, Vindigni A (2013) Human RECQ1 promotes restart of replication forks reversed by DNA topoisomerase I inhibition. Nat Struct Mol Biol 20(3):347–354PubMedCentralPubMedGoogle Scholar
  20. Boehler C, Gauthier LR, Mortusewicz O, Biard DS, Saliou JM, Bresson A, Sanglier-Cianferani S, Smith S, Schreiber V, Boussin F, Dantzer F (2011) Poly(ADP-ribose) polymerase 3 (PARP3), a newcomer in cellular response to DNA damage and mitotic progression. Proc Natl Acad Sci U S A 108(7):2783–2788PubMedCentralPubMedGoogle Scholar
  21. Boulton S, Kyle S, Durkacz BW (1999) Interactive effects of inhibitors of poly(ADP-ribose) polymerase and DNA-dependent protein kinase on cellular responses to DNA damage. Carcinogenesis 20(2):199–203PubMedGoogle Scholar
  22. Bryant HE, Petermann E, Schultz N, Jemth AS, Loseva O, Issaeva N, Johansson F, Fernandez S, McGlynn P, Helleday T (2009) PARP is activated at stalled forks to mediate Mre11-dependent replication restart and recombination. EMBO J 28(17):2601–2615PubMedCentralPubMedGoogle Scholar
  23. Bryant HE, Schultz N, Thomas HD, Parker KM, Flower D, Lopez E, Kyle S, Meuth M, Curtin NJ, Helleday T (2005) Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 434(7035):913–917PubMedGoogle Scholar
  24. Caldecott KW (2003) XRCC1 and DNA strand break repair. DNA Repair (Amst) 2(9):955–969Google Scholar
  25. Chambon P, Weill JD, Mandel P (1963) Nicotinamide mononucleotide activation of new DNA-dependent polyadenylic acid synthesizing nuclear enzyme. Biochem Biophys Res Commun 11:39–43PubMedGoogle Scholar
  26. Chang WJ, Alvarez-Gonzalez R (2001) The sequence-specific DNA binding of NF-kappa B is reversibly regulated by the automodification reaction of poly (ADP-ribose) polymerase 1. J Biol Chem 276(50):47664–47670PubMedGoogle Scholar
  27. Chapman JD, Gagne JP, Poirier GG, Goodlett DR (2013) Mapping PARP-1 auto-ADP-ribosylation sites by liquid chromatography-tandem mass spectrometry. J Proteome Res. doi: 10.1021/pr301219h Google Scholar
  28. Chen M, Huang JD, Hu L, Zheng BJ, Chen L, Tsang SL, Guan XY (2009) Transgenic CHD1L expression in mouse induces spontaneous tumors. PLoS One 4(8):e6727PubMedCentralPubMedGoogle Scholar
  29. Chen D, Vollmar M, Rossi MN, Phillips C, Kraehenbuehl R, Slade D, Mehrotra PV, von Delft F, Crosthwaite SK, Gileadi O, Denu JM, Ahel I (2011) Identification of macrodomain proteins as novel O-acetyl-ADP-ribose deacetylases. J Biol Chem 286(15):13261–13271PubMedCentralPubMedGoogle Scholar
  30. Chou DM, Adamson B, Dephoure NE, Tan X, Nottke AC, Hurov KE, Gygi SP, Colaiacovo MP, Elledge SJ (2010) A chromatin localization screen reveals poly (ADP ribose)-regulated recruitment of the repressive polycomb and NuRD complexes to sites of DNA damage. Proc Natl Acad Sci U S A 107(43):18475–18480PubMedCentralPubMedGoogle Scholar
  31. Clark NJ, Kramer M, Muthurajan UM, Luger K (2012) Alternative modes of binding of poly(ADP-ribose) polymerase 1 to free DNA and nucleosomes. J Biol Chem 287(39):32430–32439PubMedCentralPubMedGoogle Scholar
  32. Cregan SP, Dawson VL, Slack RS (2004) Role of AIF in caspase-dependent and caspase-independent cell death. Oncogene 23(16):2785–2796PubMedGoogle Scholar
  33. D’Amours D, Desnoyers S, D’Silva I, Poirier GG (1999) Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem J 342(Pt 2):249–268PubMedCentralPubMedGoogle Scholar
  34. Dantzer F, de La Rubia G, Menissier-De Murcia J, Hostomsky Z, de Murcia G, Schreiber V (2000) Base excision repair is impaired in mammalian cells lacking Poly(ADP-ribose) polymerase-1. Biochemistry 39(25):7559–7569PubMedGoogle Scholar
  35. David KK, Andrabi SA, Dawson TM, Dawson VL (2009) Parthanatos, a messenger of death. Front Biosci 14:1116–1128Google Scholar
  36. De Vos M, Schreiber V, Dantzer F (2012) The diverse roles and clinical relevance of PARPs in DNA damage repair: current state of the art. Biochem Pharmacol 84(2):137–146PubMedGoogle Scholar
  37. Ding R, Pommier Y, Kang VH, Smulson M (1992) Depletion of poly(ADP-ribose) polymerase by antisense RNA expression results in a delay in DNA strand break rejoining. J Biol Chem 267(18):12804–12812PubMedGoogle Scholar
  38. Doil C, Mailand N, Bekker-Jensen S, Menard P, Larsen DH, Pepperkok R, Ellenberg J, Panier S, Durocher D, Bartek J, Lukas J, Lukas C (2009) RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 136(3):435–446PubMedGoogle Scholar
  39. Dregalla RC, Zhou J, Idate RR, Battaglia CL, Liber HL, Bailey SM (2010) Regulatory roles of tankyrase 1 at telomeres and in DNA repair: suppression of T-SCE and stabilization of DNA-PKcs. Aging 2(10):691–708PubMedCentralPubMedGoogle Scholar
  40. Dunstan MS, Barkauskaite E, Lafite P, Knezevic CE, Brassington A, Ahel M, Hergenrother PJ, Leys D, Ahel I (2012) Structure and mechanism of a canonical poly(ADP-ribose) glycohydrolase. Nat Commun 3:878PubMedGoogle Scholar
  41. El-Khamisy SF, Masutani M, Suzuki H, Caldecott KW (2003) A requirement for PARP-1 for the assembly or stability of XRCC1 nuclear foci at sites of oxidative DNA damage. Nucleic Acids Res 31(19):5526–5533PubMedCentralPubMedGoogle Scholar
  42. Eustermann S, Brockmann C, Mehrotra PV, Yang JC, Loakes D, West SC, Ahel I, Neuhaus D (2010) Solution structures of the two PBZ domains from human APLF and their interaction with poly(ADP-ribose). Nat Struct Mol Biol 17(2):241–243PubMedCentralPubMedGoogle Scholar
  43. Eustermann S, Videler H, Yang JC, Cole PT, Gruszka D, Veprintsev D, Neuhaus D (2011) The DNA-binding domain of human PARP-1 interacts with DNA single-strand breaks as a monomer through its second zinc finger. J Mol Biol 407(1):149–170PubMedCentralPubMedGoogle Scholar
  44. 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
  45. Feng X, Koh DW (2013) Inhibition of poly(ADP-ribose) polymerase-1 or poly(ADPribose) glycohydrolase individually, but not in combination, leads to improved chemotherapeutic efficacy in HeLa cells. Int J Oncol 42(2):749–756PubMedCentralPubMedGoogle Scholar
  46. Fenton AL, Shirodkar P, Macrae CJ, Meng L, Kock CA (2013) The PARP3- and ATM-dependent phosphorylation of APLF facilitates DNA double-strand break repair. Nucleic Acids Res 41(7):4080–4092PubMedCentralPubMedGoogle Scholar
  47. Fisher AE, Hochegger H, Takeda S, Caldecott KW (2007) Poly(ADP-ribose) polymerase 1 accelerates single-strand break repair in concert with poly(ADP-ribose) glycohydrolase. Mol Cell Biol 27(15):5597–5605PubMedCentralPubMedGoogle Scholar
  48. Gibson BA, Kraus WL (2012) New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat Rev Mol Cell Biol 13(7):411–424PubMedGoogle Scholar
  49. Gomez M, Wu J, Schreiber V, Dunlap J, Dantzer F, Wang Y, Liu Y (2006) PARP1 is a TRF2-associated poly(ADP-ribose)polymerase and protects eroded telomeres. Mol Biol Cell 17(4):1686–1696PubMedCentralPubMedGoogle Scholar
  50. Gottschalk AJ, Timinszky G, Kong SE, Jin J, Cai Y, Swanson SK, Washburn MP, Florens L, Ladurner AG, Conaway JW, Conaway RC (2009) Poly(ADP-ribosyl)ation directs recruitment and activation of an ATP-dependent chromatin remodeler. Proc Natl Acad Sci U S A 106(33):13770–13774PubMedCentralPubMedGoogle Scholar
  51. Gottschalk AJ, Trivedi RD, Conaway JW, Conaway RC (2012) Activation of the SNF2 family ATPase ALC1 by poly(ADP-ribose) in a stable ALC1.PARP1.nucleosome intermediate. J Biol Chem 287(52):43527–43532PubMedCentralPubMedGoogle Scholar
  52. Ha HC, Snyder SH (1999) Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc Natl Acad Sci U S A 96(24):13978–13982PubMedCentralPubMedGoogle Scholar
  53. Haince JF, McDonald D, Rodrigue A, Dery U, Masson JY, Hendzel MJ, Poirier GG (2008) PARP1-dependent kinetics of recruitment of MRE11 and NBS1 proteins to multiple DNA damage sites. J Biol Chem 283(2):1197–1208PubMedGoogle Scholar
  54. Hanai S, Kanai M, Ohashi S, Okamoto K, Yamada M, Takahashi H, Miwa M (2004) Loss of poly(ADP-ribose) glycohydrolase causes progressive neurodegeneration in Drosophila melanogaster. Proc Natl Acad Sci U S A 101(1):82–86PubMedCentralPubMedGoogle Scholar
  55. Hassa PO, Covic M, Hasan S, Imhof R, Hottiger MO (2001) The enzymatic and DNA binding activity of PARP-1 are not required for NF-kappa B coactivator function. J Biol Chem 276(49):45588–45597PubMedGoogle Scholar
  56. Hassa PO, Haenni SS, Buerki C, Meier NI, Lane WS, Owen H, Gersbach M, Imhof R, Hottiger MO (2005) Acetylation of poly(ADP-ribose) polymerase-1 by p300/CREB-binding protein regulates coactivation of NF-kappaB-dependent transcription. J Biol Chem 280(49):40450–40464PubMedGoogle Scholar
  57. Hassa PO, Hottiger MO (1999) A role of poly (ADP-ribose) polymerase in NF-kappaB transcriptional activation. Biol Chem 380(7–8):953–959PubMedGoogle Scholar
  58. He F, Tsuda K, Takahashi M, Kuwasako K, Terada T, Shirouzu M, Watanabe S, Kigawa T, Kobayashi N, Guntert P, Yokoyama S, Muto Y (2012) Structural insight into the interaction of ADP-ribose with the PARP WWE domains. FEBS Lett 586(21):3858–3864PubMedGoogle Scholar
  59. Heo K, Kim H, Choi SH, Choi J, Kim K, Gu J, Lieber MR, Yang AS, An W (2008) FACT-mediated exchange of histone variant H2AX regulated by phosphorylation of H2AX and ADP-ribosylation of Spt16. Mol Cell 30(1):86–97PubMedGoogle Scholar
  60. Hochegger H, Dejsuphong D, Fukushima T, Morrison C, Sonoda E, Schreiber V, Zhao GY, Saberi A, Masutani M, Adachi N, Koyama H, de Murcia G, Takeda S (2006) Parp-1 protects homologous recombination from interference by Ku and Ligase IV in vertebrate cells. EMBO J 25(6):1305–1314PubMedCentralPubMedGoogle Scholar
  61. Huang JY, Chen WH, Chang YL, Wang HT, Chuang WT, Lee SC (2006) Modulation of nucleosome-binding activity of FACT by poly(ADP-ribosyl)ation. Nucleic Acids Res 34(8):2398–2407PubMedCentralPubMedGoogle Scholar
  62. Iles N, Rulten S, El-Khamisy SF, Caldecott KW (2007) APLF (C2orf13) is a novel human protein involved in the cellular response to chromosomal DNA strand breaks. Mol Cell Biol 27(10):3793–3803PubMedCentralPubMedGoogle Scholar
  63. Jankevicius G, Hassler M, Golia B, Rybin V, Zacharias M, Timinszky G, Ladurner AG (2013) A family of macrodomain proteins reverses cellular mono-ADP-ribosylation. Nat Struct Mol Biol 20(4):508–514PubMedGoogle Scholar
  64. Ji Y, Tulin AV (2010) The roles of PARP1 in gene control and cell differentiation. Curr Opin Genet Dev 20(5):512–518PubMedCentralPubMedGoogle Scholar
  65. Juarez-Salinas H, Levi V, Jacobson EL, Jacobson MK (1982) Poly(ADP-ribose) has a branched structure in vivo. J Biol Chem 257(2):607–609PubMedGoogle Scholar
  66. Kanai M, Hanashiro K, Kim SH, Hanai S, Boulares AH, Miwa M, Fukasawa K (2007) Inhibition of Crm1-p53 interaction and nuclear export of p53 by poly(ADP-ribosyl)ation. Nat Cell Biol 9(10):1175–1183PubMedGoogle Scholar
  67. Kanai M, Tong WM, Sugihara E, Wang ZQ, Fukasawa K, Miwa M (2003) Involvement of poly(ADP-ribose) polymerase 1 and poly(ADP-ribosyl)ation in regulation of centrosome function. Mol Cell Biol 23(7):2451–2462PubMedCentralPubMedGoogle Scholar
  68. Kang HC, Lee YI, Shin JH, Andrabi SA, Chi Z, Gagne JP, Lee Y, Ko HS, Lee BD, Poirier GG, Dawson VL, Dawson TM (2011) Iduna is a poly(ADP-ribose) (PAR)-dependent E3 ubiquitin ligase that regulates DNA damage. Proc Natl Acad Sci U S A 108(34):14103–14108PubMedCentralPubMedGoogle Scholar
  69. Kashima L, Idogawa M, Mita H, Shitashige M, Yamada T, Ogi K, Suzuki H, Toyota M, Ariga H, Sasaki Y, Tokino T (2012) CHFR protein regulates mitotic checkpoint by targeting PARP-1 protein for ubiquitination and degradation. J Biol Chem 287(16):12975–12984PubMedCentralPubMedGoogle Scholar
  70. Kauppinen TM, Chan WY, Suh SW, Wiggins AK, Huang EJ, Swanson RA (2006) Direct phosphorylation and regulation of poly(ADP-ribose) polymerase-1 by extracellular signal-regulated kinases 1/2. Proc Natl Acad Sci U S A 103(18):7136–7141PubMedCentralPubMedGoogle Scholar
  71. Kim IK, Kiefer JR, Ho CM, Stegeman RA, Classen S, Tainer JA, Ellenberger T (2012) Structure of mammalian poly(ADP-ribose) glycohydrolase reveals a flexible tyrosine clasp as a substrate-binding element. Nat Struct Mol Biol 19(6):653–656PubMedCentralPubMedGoogle Scholar
  72. Kim MY, Mauro S, Gevry N, Lis JT, Kraus WL (2004) NAD+-dependent modulation of chromatin structure and transcription by nucleosome binding properties of PARP-1. Cell 119(6):803–814PubMedGoogle Scholar
  73. Koh DW, Lawler AM, Poitras MF, Sasaki M, Wattler S, Nehls MC, Stoger T, Poirier GG, Dawson VL, Dawson TM (2004) Failure to degrade poly(ADP-ribose) causes increased sensitivity to cytotoxicity and early embryonic lethality. Proc Natl Acad Sci U S A 101(51):17699–17704PubMedCentralPubMedGoogle Scholar
  74. Kotova E, Lodhi N, Jarnik M, Pinnola AD, Ji Y, Tulin AV (2011) Drosophila histone H2A variant (H2Av) controls poly(ADP-ribose) polymerase 1 (PARP1) activation in chromatin. Proc Natl Acad Sci U S A 108(15):6205–6210PubMedCentralPubMedGoogle Scholar
  75. Kraus WL (2008) Transcriptional control by PARP-1: chromatin modulation, enhancer-binding, coregulation, and insulation. Curr Opin Cell Biol 20(3):294–302PubMedCentralPubMedGoogle Scholar
  76. Krupitza G, Cerutti P (1989) Poly(ADP-ribosylation) of histones in intact human keratinocytes. Biochemistry 28(9):4054–4060PubMedGoogle Scholar
  77. Kutuzov MM, Khodyreva SN, Ame JC, Ilina ES, Sukhanova MV, Schreiber V, Lavrik OI (2013) Interaction of PARP-2 with DNA structures mimicking DNA repair intermediates and consequences on activity of base excision repair proteins. Biochimie 95(6):1208–1215PubMedGoogle Scholar
  78. Langelier MF, Planck JL, Roy S, Pascal JM (2011) Crystal structures of poly(ADP-ribose) polymerase-1 (PARP-1) zinc fingers bound to DNA: structural and functional insights into DNA-dependent PARP-1 activity. J Biol Chem 286(12):10690–10701PubMedCentralPubMedGoogle Scholar
  79. Langelier MF, Planck JL, Roy S, Pascal JM (2012) Structural basis for DNA damage-dependent poly(ADP-ribosyl)ation by human PARP-1. Science 336(6082):728–732PubMedCentralPubMedGoogle Scholar
  80. Larsen DH, Poinsignon C, Gudjonsson T, Dinant C, Payne MR, Hari FJ, Rendtlew Danielsen JM, Menard P, Sand JC, Stucki M, Lukas C, Bartek J, Andersen JS, Lukas J (2010) The chromatin-remodeling factor CHD4 coordinates signaling and repair after DNA damage. J Cell Biol 190(5):731–740PubMedCentralPubMedGoogle Scholar
  81. Lazebnik YA, Kaufmann SH, Desnoyers S, Poirier GG, Earnshaw WC (1994) Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 371(6495):346–347PubMedGoogle Scholar
  82. Leppard JB, Dong Z, Mackey ZB, Tomkinson AE (2003) Physical and functional interaction between DNA ligase IIIalpha and poly(ADP-Ribose) polymerase 1 in DNA single-strand break repair. Mol Cell Biol 23(16):5919–5927PubMedCentralPubMedGoogle Scholar
  83. Li B, Navarro S, Kasahara N, Comai L (2004) Identification and biochemical characterization of a Werner’s syndrome protein complex with Ku70/80 and poly(ADP-ribose) polymerase-1. J Biol Chem 279(14):13659–13667PubMedGoogle Scholar
  84. Liu C, Wu J, Paudyal SC, You Z, Yu X (2013) CHFR is important for the first wave of ubiquitination at DNA damage sites. Nucleic Acids Res 41(3):1698–1710PubMedCentralPubMedGoogle Scholar
  85. Lonskaya I, Potaman VN, Shlyakhtenko LS, Oussatcheva EA, Lyubchenko YL, Soldatenkov VA (2005) Regulation of poly(ADP-ribose) polymerase-1 by DNA structure-specific binding. J Biol Chem 280(17):17076–17083PubMedGoogle Scholar
  86. Ludwig A, Behnke B, Holtlund J, Hilz H (1988) Immunoquantitation and size determination of intrinsic poly(ADP-ribose) polymerase from acid precipitates. An analysis of the in vivo status in mammalian species and in lower eukaryotes. J Biol Chem 263(15):6993–6999PubMedGoogle Scholar
  87. Luo X, Kraus WL (2012) On PAR with PARP: cellular stress signaling through poly(ADP-ribose) and PARP-1. Genes Dev 26(5):417–432PubMedCentralPubMedGoogle Scholar
  88. Ma NF, Hu L, Fung JM, Xie D, Zheng BJ, Chen L, Tang DJ, Fu L, Wu Z, Chen M, Fang Y, Guan XY (2008) Isolation and characterization of a novel oncogene, amplified in liver cancer 1, within a commonly amplified region at 1q21 in hepatocellular carcinoma. Hepatology 47(2):503–510PubMedGoogle Scholar
  89. Malanga M, Althaus FR (2005) The role of poly(ADP-ribose) in the DNA damage signaling network. Biochem Cell Biol 83(3):354–364PubMedGoogle Scholar
  90. Malanga M, Pleschke JM, Kleczkowska HE, Althaus FR (1998) Poly(ADP-ribose) binds to specific domains of p53 and alters its DNA binding functions. J Biol Chem 273(19):11839–11843PubMedGoogle Scholar
  91. Mao Z, Hine C, Tian X, Van Meter M, Au M, Vaidya A, Seluanov A, Gorbunova V (2011) SIRT6 promotes DNA repair under stress by activating PARP1. Science 332(6036):1443–1446PubMedGoogle Scholar
  92. Masson M, Niedergang C, Schreiber V, Muller S, Menissier-de Murcia J, de Murcia G (1998) XRCC1 is specifically associated with poly(ADP-ribose) polymerase and negatively regulates its activity following DNA damage. Mol Cell Biol 18(6):3563–3571PubMedCentralPubMedGoogle Scholar
  93. Matic I, Ahel I, Hay RT (2012) Reanalysis of phosphoproteomics data uncovers ADP-ribosylation sites. Nat Methods 9(8):771–772PubMedCentralPubMedGoogle Scholar
  94. Mehrotra PV, Ahel D, Ryan DP, Weston R, Wiechens N, Kraehenbuehl R, Owen-Hughes T, Ahel I (2011) DNA repair factor APLF is a histone chaperone. Mol Cell 41(1):46–55PubMedCentralPubMedGoogle Scholar
  95. Mendoza-Alvarez H, Alvarez-Gonzalez R (2001) Regulation of p53 sequence-specific DNA-binding by covalent poly(ADP-ribosyl)ation. J Biol Chem 276(39):36425–36430PubMedGoogle Scholar
  96. Menissier de Murcia J, Ricoul M, Tartier L, Niedergang C, Huber A, Dantzer F, Schreiber V, Ame JC, Dierich A, LeMeur M, Sabatier L, Chambon P, de Murcia G (2003) Functional interaction between PARP-1 and PARP-2 in chromosome stability and embryonic development in mouse. EMBO J 22(9):2255–2263PubMedCentralPubMedGoogle Scholar
  97. Messner S, Altmeyer M, Zhao H, Pozivil A, Roschitzki B, Gehrig P, Rutishauser D, Huang D, Caflisch A, Hottiger MO (2010) PARP1 ADP-ribosylates lysine residues of the core histone tails. Nucleic Acids Res 38(19):6350–6362PubMedCentralPubMedGoogle Scholar
  98. Miwa M, Saikawa N, Yamaizumi Z, Nishimura S, Sugimura T (1979) Structure of poly(adenosine diphosphate ribose): identification of 2′-[1″-ribosyl-2″-(or 3″-)(1‴-ribosyl)]adenosine-5′,5″,5‴-tris(phosphate) as a branch linkage. Proc Natl Acad Sci U S A 76(2):595–599PubMedCentralPubMedGoogle Scholar
  99. Miwa M, Sugimura T (1971) Splitting of the ribose–ribose linkage of poly(adenosine diphosphate-robose) by a calf thymus extract. J Biol Chem 246(20):6362–6364PubMedGoogle Scholar
  100. Mortusewicz O, Ame JC, Schreiber V, Leonhardt H (2007) Feedback-regulated poly(ADP-ribosyl)ation by PARP-1 is required for rapid response to DNA damage in living cells. Nucleic Acids Res 35(22):7665–7675PubMedCentralPubMedGoogle Scholar
  101. Mueller-Dieckmann C, Kernstock S, Lisurek M, von Kries JP, Haag F, Weiss MS, Koch-Nolte F (2006) The structure of human ADP-ribosylhydrolase 3 (ARH3) provides insights into the reversibility of protein ADP-ribosylation. Proc Natl Acad Sci U S A 103(41):15026–15031PubMedCentralPubMedGoogle Scholar
  102. Murawska M, Hassler M, Renkawitz-Pohl R, Ladurner A, Brehm A (2011) Stress-induced PARP activation mediates recruitment of Drosophila Mi-2 to promote heat shock gene expression. PLoS Genet 7(7):e1002206PubMedCentralPubMedGoogle Scholar
  103. Nicolas L, Martinez C, Baro C, Rodriguez M, Baroja-Mazo A, Sole F, Flores JM, Ampurdanes C, Dantzer F, Martin-Caballero J, Aparicio P, Yelamos J (2010) Loss of poly(ADP-ribose) polymerase-2 leads to rapid development of spontaneous T-cell lymphomas in p53-deficient mice. Oncogene 29(19):2877–2883PubMedGoogle Scholar
  104. Niere M, Mashimo M, Agledal L, Dolle C, Kasamatsu A, Kato J, Moss J, Ziegler M (2012) ADP-ribosylhydrolase 3 (ARH3), not poly(ADP-ribose) glycohydrolase (PARG) isoforms, is responsible for degradation of mitochondrial matrix-associated poly(ADP-ribose). J Biol Chem 287(20):16088–16102PubMedCentralPubMedGoogle Scholar
  105. Noren Hooten N, Kompaniez K, Barnes J, Lohani A, Evans MK (2011) Poly(ADP-ribose) polymerase 1 (PARP-1) binds to 8-oxoguanine-DNA glycosylase (OGG1). J Biol Chem 286(52):44679–44690PubMedCentralPubMedGoogle Scholar
  106. Oberoi J, Richards MW, Crumpler S, Brown N, Blagg J, Bayliss R (2010) Structural basis of poly(ADP-ribose) recognition by the multizinc binding domain of checkpoint with forkhead-associated and RING domains (CHFR). J Biol Chem 285(50):39348–39358PubMedCentralPubMedGoogle Scholar
  107. Oei SL, Griesenbeck J, Ziegler M, Schweiger M (1998) A novel function of poly(ADP-ribosyl)ation: silencing of RNA polymerase II-dependent transcription. Biochemistry 37(6):1465–1469PubMedGoogle Scholar
  108. Ogata N, Ueda K, Hayaishi O (1980) ADP-ribosylation of histone H2B. Identification of glutamic acid residue 2 as the modification site. J Biol Chem 255(16):7610–7615PubMedGoogle Scholar
  109. Ogata N, Ueda K, Kawaichi M, Hayaishi O (1981) Poly(ADP-ribose) synthetase, a main acceptor of poly(ADP-ribose) in isolated nuclei. J Biol Chem 256(9):4135–4137PubMedGoogle Scholar
  110. Okano S, Lan L, Caldecott KW, Mori T, Yasui A (2003) Spatial and temporal cellular responses to single-strand breaks in human cells. Mol Cell Biol 23(11):3974–3981PubMedCentralPubMedGoogle Scholar
  111. Otto H, Reche PA, Bazan F, Dittmar K, Haag F, Koch-Nolte F (2005) In silico characterization of the family of PARP-like poly(ADP-ribosyl)transferases (pARTs). BMC Genomics 6:139PubMedCentralPubMedGoogle Scholar
  112. Pan MR, Hsieh HJ, Dai H, Hung WC, Li K, Peng G, Lin SY (2012) Chromodomain helicase DNA-binding protein 4 (CHD4) regulates homologous recombination DNA repair, and its deficiency sensitizes cells to poly(ADP-ribose) polymerase (PARP) inhibitor treatment. J Biol Chem 287(9):6764–6772PubMedCentralPubMedGoogle Scholar
  113. Pears CJ, Couto CA, Wang HY, Borer C, Kiely R, Lakin ND (2012) The role of ADP-ribosylation in regulating DNA double-strand break repair. Cell Cycle 11(1):48–56PubMedCentralPubMedGoogle Scholar
  114. Pehrson JR, Fried VA (1992) MacroH2A, a core histone containing a large nonhistone region. Science 257(5075):1398–1400PubMedGoogle Scholar
  115. Peterson FC, Chen D, Lytle BL, Rossi MN, Ahel I, Denu JM, Volkman BF (2011) Orphan macrodomain protein (human C6orf130) is an O-acyl-ADP-ribose deacylase: solution structure and catalytic properties. J Biol Chem 286(41):35955–35965PubMedCentralPubMedGoogle Scholar
  116. Petesch SJ, Lis JT (2008) Rapid, transcription-independent loss of nucleosomes over a large chromatin domain at Hsp70 loci. Cell 134(1):74–84PubMedCentralPubMedGoogle Scholar
  117. Pinnola A, Naumova N, Shah M, Tulin AV (2007) Nucleosomal core histones mediate dynamic regulation of poly(ADP-ribose) polymerase 1 protein binding to chromatin and induction of its enzymatic activity. J Biol Chem 282(44):32511–32519PubMedGoogle Scholar
  118. Pleschke JM, Kleczkowska HE, Strohm M, Althaus FR (2000) Poly(ADP-ribose) binds to specific domains in DNA damage checkpoint proteins. J Biol Chem 275(52):40974–40980PubMedGoogle Scholar
  119. Poirier GG, de Murcia G, Jongstra-Bilen J, Niedergang C, Mandel P (1982) Poly(ADP-ribosyl)ation of polynucleosomes causes relaxation of chromatin structure. Proc Natl Acad Sci U S A 79(11):3423–3427PubMedCentralPubMedGoogle Scholar
  120. Polo SE, Kaidi A, Baskcomb L, Galanty Y, Jackson SP (2010) Regulation of DNA-damage responses and cell-cycle progression by the chromatin remodelling factor CHD4. EMBO J 29(18):3130–3139PubMedCentralPubMedGoogle Scholar
  121. Rawling JM, Alvarez-Gonzalez R (1997) TFIIF, a basal eukaryotic transcription factor, is a substrate for poly(ADP-ribosyl)ation. Biochem J 324(Pt 1):249–253PubMedCentralPubMedGoogle Scholar
  122. Ray Chaudhuri A, Hashimoto Y, Herrador R, Neelsen KJ, Fachinetti D, Bermejo R, Cocito A, Costanzo V, Lopes M (2012) Topoisomerase I poisoning results in PARP-mediated replication fork reversal. Nat Struct Mol Biol 19(4):417–423PubMedGoogle Scholar
  123. Riquelme PT, Burzio LO, Koide SS (1979) ADP ribosylation of rat liver lysine-rich histone in vitro. J Biol Chem 254(8):3018–3028PubMedGoogle Scholar
  124. Rosenthal F, Feijs KL, Frugier E, Bonalli M, Forst AH, Imhof R, Winkler HC, Fischer D, Caflisch A, Hassa PO, Luscher B, Hottiger MO (2013) Macrodomain-containing proteins are new mono-ADP-ribosylhydrolases. Nat Struct Mol Biol 20(4):502–507PubMedGoogle Scholar
  125. Rouleau M, Patel A, Hendzel MJ, Kaufmann SH, Poirier GG (2010) PARP inhibition: PARP1 and beyond. Nat Rev Cancer 10(4):293–301PubMedCentralPubMedGoogle Scholar
  126. Ruf A, Rolli V, de Murcia G, Schulz GE (1998) The mechanism of the elongation and branching reaction of poly(ADP-ribose) polymerase as derived from crystal structures and mutagenesis. J Mol Biol 278(1):57–65PubMedGoogle Scholar
  127. Rulten SL, Cortes-Ledesma F, Guo L, Iles NJ, Caldecott KW (2008) APLF (C2orf13) is a novel component of poly(ADP-ribose) signaling in mammalian cells. Mol Cell Biol 28(14):4620–4628PubMedCentralPubMedGoogle Scholar
  128. Rulten SL, Fisher AE, Robert I, Zuma MC, Rouleau M, Ju L, Poirier G, Reina-San-Martin B, Caldecott KW (2011) PARP-3 and APLF function together to accelerate nonhomologous end-joining. Mol Cell 41(1):33–45PubMedGoogle Scholar
  129. Schreiber V, Ame JC, Dolle P, Schultz I, Rinaldi B, Fraulob V, Menissier-de Murcia J, de Murcia G (2002) Poly(ADP-ribose) polymerase-2 (PARP-2) is required for efficient base excision DNA repair in association with PARP-1 and XRCC1. J Biol Chem 277(25):23028–23036PubMedGoogle Scholar
  130. 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
  131. Schultz N, Lopez E, Saleh-Gohari N, Helleday T (2003) Poly(ADP-ribose) polymerase (PARP-1) has a controlling role in homologous recombination. Nucleic Acids Res 31(17):4959–4964PubMedCentralPubMedGoogle Scholar
  132. Sharifi R, Morra R, Denise Appel C, Tallis M, Chioza B, Jankevicius G, Simpson MA, Matic I, Ozkan E, Golia B, Schellenberg MJ, Weston R, Williams JG, Rossi MN, Galehdari H, Krahn J, Wan A, Trembath RC, Crosby AH, Ahel D, Hay R, Ladurner AG, Timinszky G, Williams RS, Ahel I (2013) Deficiency of terminal ADP-ribose protein glycohydrolase TARG1/C6orf130 in neurodegenerative disease. EMBO J 32(9):1225–1237PubMedPubMedCentralGoogle Scholar
  133. 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):245–248PubMedCentralPubMedGoogle Scholar
  134. Slade D, Dunstan MS, Barkauskaite E, Weston R, Lafite P, Dixon N, Ahel M, Leys D, Ahel I (2011) The structure and catalytic mechanism of a poly(ADP-ribose) glycohydrolase. Nature 477(7366):616–620PubMedCentralPubMedGoogle Scholar
  135. Slattery E, Dignam JD, Matsui T, Roeder RG (1983) Purification and analysis of a factor which suppresses nick-induced transcription by RNA polymerase II and its identity with poly(ADP-ribose) polymerase. J Biol Chem 258(9):5955–5959PubMedGoogle Scholar
  136. Smeenk G, Wiegant WW, Marteijn JA, Luijsterburg MS, Sroczynski N, Costelloe T, Romeijn RJ, Pastink A, Mailand N, Vermeulen W, van Attikum H (2013) Poly(ADP-ribosyl)ation links the chromatin remodeler SMARCA5/SNF2H to RNF168-dependent DNA damage signaling. J Cell Sci 126(Pt 4):889–903PubMedGoogle Scholar
  137. Spagnolo L, Barbeau J, Curtin NJ, Morris EP, Pearl LH (2012) Visualization of a DNA-PK/PARP1 complex. Nucleic Acids Res 40(9):4168–4177PubMedCentralPubMedGoogle Scholar
  138. Stilmann M, Hinz M, Arslan SC, Zimmer A, Schreiber V, Scheidereit C (2009) A nuclear poly(ADP-ribose)-dependent signalosome confers DNA damage-induced IkappaB kinase activation. Mol Cell 36(3):365–378PubMedGoogle Scholar
  139. Sugimura K, Takebayashi S, Taguchi H, Takeda S, Okumura K (2008) PARP-1 ensures regulation of replication fork progression by homologous recombination on damaged DNA. J Cell Biol 183(7):1203–1212PubMedCentralPubMedGoogle Scholar
  140. Szabo C, Pacher P, Swanson RA (2006) Novel modulators of poly(ADP-ribose) polymerase. Trends Pharmacol Sci 27(12):626–630PubMedCentralPubMedGoogle Scholar
  141. Tao Z, Gao P, Liu HW (2009) Identification of the ADP-ribosylation sites in the PARP-1 automodification domain: analysis and implications. J Am Chem Soc 131(40):14258–14260. doi: 10.1021/ja906135d PubMedGoogle Scholar
  142. Timinszky G, Till S, Hassa PO, Hothorn M, Kustatscher G, Nijmeijer B, Colombelli J, Altmeyer M, Stelzer EH, Scheffzek K, Hottiger MO, Ladurner AG (2009) A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nat Struct Mol Biol 16(9):923–929PubMedGoogle Scholar
  143. Trucco C, Oliver FJ, de Murcia G, Menissier-de Murcia J (1998) DNA repair defect in poly(ADP-ribose) polymerase-deficient cell lines. Nucleic Acids Res 26(11):2644–2649PubMedCentralPubMedGoogle Scholar
  144. Tulin A, Spradling A (2003) Chromatin loosening by poly(ADP)-ribose polymerase (PARP) at Drosophila puff loci. Science 299(5606):560–562PubMedGoogle Scholar
  145. Ueda K, Oka J, Naruniya S, Miyakawa N, Hayaishi O (1972) Poly ADP-ribose glycohydrolase from rat liver nuclei, a novel enzyme degrading the polymer. Biochem Biophys Res Commun 46(2):516–523PubMedGoogle Scholar
  146. Ushiroyama T, Tanigawa Y, Tsuchiya M, Matsuura R, Ueki M, Sugimoto O, Shimoyama M (1985) Amino acid sequence of histone H1 at the ADP-ribose-accepting site and ADP-ribose X histone-H1 adduct as an inhibitor of cyclic-AMP-dependent phosphorylation. Eur J Biochem 151(1):173–177PubMedGoogle Scholar
  147. Valenzuela MT, Guerrero R, Nunez MI, Ruiz De Almodovar JM, Sarker M, de Murcia G, Oliver FJ (2002) PARP-1 modifies the effectiveness of p53-mediated DNA damage response. Oncogene 21(7):1108–1116PubMedGoogle Scholar
  148. Virag L, Robaszkiewicz A, Vargas JM, Javier Oliver F (2013) Poly(ADP-ribose) signaling in cell death. Mol Aspects Med. doi: 10.1016/j.mam.2013.01.007 Google Scholar
  149. Wacker DA, Ruhl DD, Balagamwala EH, Hope KM, Zhang T, Kraus WL (2007) The DNA binding and catalytic domains of poly(ADP-ribose) polymerase 1 cooperate in the regulation of chromatin structure and transcription. Mol Cell Biol 27(21):7475–7485PubMedCentralPubMedGoogle Scholar
  150. Wang Y, Dawson VL, Dawson TM (2009) Poly(ADP-ribose) signals to mitochondrial AIF: a key event in parthanatos. Exp Neurol 218(2):193–202PubMedCentralPubMedGoogle Scholar
  151. Wang Y, Kim NS, Haince JF, Kang HC, David KK, Andrabi SA, Poirier GG, Dawson VL, Dawson TM (2011) Poly(ADP-ribose) (PAR) binding to apoptosis-inducing factor is critical for PAR polymerase-1-dependent cell death (parthanatos). Sci Signal 4(167):ra20PubMedCentralPubMedGoogle Scholar
  152. Wang Z, Michaud GA, Cheng Z, Zhang Y, Hinds TR, Fan E, Cong F, Xu W (2012) Recognition of the iso-ADP-ribose moiety in poly(ADP-ribose) by WWE domains suggests a general mechanism for poly(ADP-ribosyl)ation-dependent ubiquitination. Genes Dev 26(3):235–240PubMedCentralPubMedGoogle Scholar
  153. Wang ZQ, Stingl L, Morrison C, Jantsch M, Los M, Schulze-Osthoff K, Wagner EF (1997) PARP is important for genomic stability but dispensable in apoptosis. Genes Dev 11(18):2347–2358PubMedCentralPubMedGoogle Scholar
  154. Wesierska-Gadek J, Bugajska-Schretter A, Cerni C (1996) ADP-ribosylation of p53 tumor suppressor protein: mutant but not wild-type p53 is modified. J Cell Biochem 62(1):90–101PubMedGoogle Scholar
  155. Wielckens K, Schmidt A, George E, Bredehorst R, Hilz H (1982) DNA fragmentation and NAD depletion. Their relation to the turnover of endogenous mono(ADP-ribosyl) and poly(ADP-ribosyl) proteins. J Biol Chem 257(21):12872–12877PubMedGoogle Scholar
  156. Xu C, Xu Y, Gursoy-Yuzugullu O, Price BD (2012) The histone variant macroH2A1.1 is recruited to DSBs through a mechanism involving PARP1. FEBS Lett 586(21):3920–3925PubMedCentralPubMedGoogle Scholar
  157. Yamanaka H, Penning CA, Willis EH, Wasson DB, Carson DA (1988) Characterization of human poly(ADP-ribose) polymerase with autoantibodies. J Biol Chem 263(8):3879–3883PubMedGoogle Scholar
  158. Yang YG, Cortes U, Patnaik S, Jasin M, Wang ZQ (2004) Ablation of PARP-1 does not interfere with the repair of DNA double-strand breaks, but compromises the reactivation of stalled replication forks. Oncogene 23(21):3872–3882PubMedGoogle Scholar
  159. Yelamos J, Schreiber V, Dantzer F (2008) Toward specific functions for poly(ADP-ribose) polymerase-2. Trends Mol Med 14(4):169–178PubMedGoogle Scholar
  160. Žaja R, Mikoč A, Barkauskaite E, Ahel I (2013) Molecular insights into poly(ADP-ribose) recognition and processing. Biomolecules 3:1–17Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Michael Tallis
    • 1
  • Rosa Morra
    • 1
  • Eva Barkauskaite
    • 1
  • Ivan Ahel
    • 1
    • 2
  1. 1.Cancer Research UK, Paterson Institute for Cancer ResearchUniversity of ManchesterManchesterUK
  2. 2.Sir William Dunn School of PathologyUniversity of OxfordOxfordUK

Personalised recommendations