1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Biochemistry
  4. Volume 84, 2015
  5. Article

Annual Review of Biochemistry

Volume 84, 2015

Nuclear ADP-Ribosylation and Its Role in Chromatin Plasticity, Cell Differentiation, and Epigenetics

Abstract

Protein ADP-ribosylation is an ancient posttranslational modification with high biochemical complexity. It alters the function of modified proteins or provides a scaffold for the recruitment of other proteins and thus regulates several cellular processes. ADP-ribosylation is governed by ADP-ribosyltransferases and a subclass of sirtuins (writers), is sensed by proteins that contain binding modules (readers) that recognize specific parts of the ADP-ribosyl posttranslational modification, and is removed by ADP-ribosylhydrolases (erasers). The large amount of experimental data generated and technical progress made in the last decade have significantly advanced our knowledge of the function of ADP-ribosylation at the molecular level. This review summarizes the current knowledge of nuclear ADP-ribosylation reactions and their role in chromatin plasticity, cell differentiation, and epigenetics and discusses current progress and future perspectives.

Keyword(s): ADP-ribosylation, ARTD, chromatin, histone, NAD, PAR, PARP
Loading

Article metrics loading...

/content/journals/10.1146/annurev-biochem-060614-034506
2015-06-02
2025-04-19
Loading full text...

Full text loading...

/deliver/fulltext/biochem/84/1/annurev-biochem-060614-034506.html?itemId=/content/journals/10.1146/annurev-biochem-060614-034506&mimeType=html&fmt=ahah

Literature Cited

  1. Gossmann TI, Ziegler M. 1.  2014. Sequence divergence and diversity suggests ongoing functional diversification of vertebrate NAD metabolism. DNA Repair 23:29–48 [Google Scholar]
  2. Hottiger MO, Hassa PO, Lüscher B, Schüler H, Koch-Nolte F. 2.  2010. Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem. Sci. 35:208–19 [Google Scholar]
  3. Houtkooper RH, Pirinen E, Auwerx J. 3.  2012. Sirtuins as regulators of metabolism and healthspan. Nat. Rev. Mol. Cell Biol. 13:225–38 [Google Scholar]
  4. Aravind L, Zhang D, de Souza RF, Anand S, Iyer LM. 4.  2014. The natural history of ADP-ribosyltransferases and the ADP-ribosylation system. Curr. Top. Microbiol. Immunol. 384:3–32 [Google Scholar]
  5. Chambon P, Weill J, Mandel P. 5.  1963. Nicotinamide mononucleotide activation of new DNA-dependent polyadenylic acid synthesizing nuclear enzyme. Biochem. Biophys. Res. Commun. 11:39–43 [Google Scholar]
  6. Ha HC, Snyder SH. 6.  1999. Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. PNAS 96:13978–82 [Google Scholar]
  7. Andrabi SA, Umanah GK, Chang C, Stevens DA, Karuppagounder SS. 7.  et al. 2014. Poly(ADP-ribose) polymerase–dependent energy depletion occurs through inhibition of glycolysis. PNAS 111:10209–14 [Google Scholar]
  8. Alvarez-Gonzalez R, Mendoza-Alvarez H. 8.  1995. Dissection of ADP-ribose polymer synthesis into individual steps of initiation, elongation, and branching. Biochimie 77:403–7 [Google Scholar]
  9. Wielckens K, Bredehorst R, Adamietz P, Hilz H. 9.  1981. Protein-bound polymeric and monomeric ADP-ribose residues in hepatic tissues. Comparative analyses using a new procedure for the quantification of poly(ADP-ribose). Eur. J. Biochem. 117:69–74 [Google Scholar]
  10. Wielckens K, Schmidt A, George E, Bredehorst R, Hilz H. 10.  1982. DNA fragmentation and NAD depletion. Their relation to the turnover of endogenous mono(ADP-ribosyl) and poly(ADP-ribosyl) proteins. J. Biol. Chem. 257:12872–77 [Google Scholar]
  11. Jacobson EL, Antol KM, Juarez-Salinas H, Jacobson MK. 11.  1983. Poly(ADP-ribose) metabolism in ultraviolet irradiated human fibroblasts. J. Biol. Chem. 258:103–7 [Google Scholar]
  12. Hilz H. 12.  1981. ADP-ribosylation of proteins—a multifunctional process. Hoppe-Seyler's Z. Physiol. Chem. 362:1415–25 [Google Scholar]
  13. Gibson BA, Kraus WL. 13.  2012. New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat. Rev. Mol. Cell Biol. 13:411–24 [Google Scholar]
  14. Malanga M, Althaus FR. 14.  2005. The role of poly(ADP-ribose) in the DNA damage signaling network. Biochem. Cell Biol. 83:354–64 [Google Scholar]
  15. Chang P, Jacobson MK, Mitchison TJ. 15.  2004. Poly(ADP-ribose) is required for spindle assembly and structure. Nature 432:645–49 [Google Scholar]
  16. Yu S-W, Wang H, Poitras M, Coombs C, Bowers W. 16.  et al. 2002. Mediation of poly(ADP-ribose) polymerase 1–dependent cell death by apoptosis-inducing factor. Science 297:259–63 [Google Scholar]
  17. Desmarais Y, Menard L, Lagueux J, Poirier GG. 17.  1991. Enzymological properties of poly(ADP-ribose)polymerase: characterization of automodification sites and NADase activity. Biochim. Biophys. Acta 1078:179–86 [Google Scholar]
  18. Cervantes-Laurean D, Jacobson E, Jacobson M. 18.  1996. Glycation and glycoxidation of histones by ADP-ribose. J. Biol. Chem. 271:10461–69 [Google Scholar]
  19. Kawamitsu H, Hoshino H, Okada H, Miwa M, Momoi H, Sugimura T. 19.  1984. Monoclonal antibodies to poly(adenosine diphosphate ribose) recognize different structures. Biochemistry 23:3771–77 [Google Scholar]
  20. Martinez-Zamudio R, Ha HC. 20.  2012. Histone ADP-ribosylation facilitates gene transcription by directly remodeling nucleosomes. Mol. Cell. Biol. 32:2490–502 [Google Scholar]
  21. Carter-O'Connell I, Jin H, Morgan RK, David LL, Cohen MS. 21.  2014. Engineering the substrate specificity of ADP-ribosyltransferases for identifying direct protein targets. J. Am. Chem. Soc. 136:5201–4 [Google Scholar]
  22. Okayama H, Ueda K, Hayaishi O. 22.  1978. Purification of ADP-ribosylated nuclear proteins by covalent chromatography on dihydroxyboryl polyacrylamide beads and their characterization. PNAS 75:1111–15 [Google Scholar]
  23. Rosenthal F, Messner S, Roschitzki B, Gehrig P, Nanni P, Hottiger MO. 23.  2011. Identification of distinct amino acids as ADP-ribose acceptor sites by mass spectrometry. Methods Mol. Biol. 780:57–66 [Google Scholar]
  24. Dani N, Stilla A, Marchegiani A, Tamburro A, Till S. 24.  et al. 2009. Combining affinity purification by ADP-ribose-binding macro domains with mass spectrometry to define the mammalian ADP-ribosyl proteome. PNAS 106:4243–48 [Google Scholar]
  25. Daniels CM, Ong SE, Leung AK. 25.  2014. Phosphoproteomic approach to characterize protein mono- and poly(ADP-ribosyl)ation sites from cells. J. Proteome Res. 13:3510–22 [Google Scholar]
  26. Jungmichel S, Rosenthal F, Altmeyer M, Lukas J, Hottiger MO, Nielsen ML. 26.  2013. Proteome-wide identification of poly(ADP-ribosyl)ation targets in different genotoxic stress responses. Mol. Cell 52:272–85 [Google Scholar]
  27. Zhang Y, Wang J, Ding M, Yu Y. 27.  2013. Site-specific characterization of the Asp- and Glu-ADP-ribosylated proteome. Nat. Methods 10:981–84 [Google Scholar]
  28. Bredehorst R, Wielckens K, Gartemann A, Lengyel H, Klapproth K, Hilz H. 28.  1978. Two different types of bonds linking single ADP-ribose residues covalently to proteins. Quantification in eukaryotic cells. Eur. J. Biochem. 92:129–35 [Google Scholar]
  29. Smith JA, Stocken LA. 29.  1975. Chemical and metabolic properties of adenosine diphosphate ribose derivatives of nuclear proteins. Biochem. J. 147:523–29 [Google Scholar]
  30. Rosenthal F, Hottiger MO. 30.  2014. Identification of ADP-ribosylated peptides and ADP-ribose acceptor sites. Front. Biosci. (Landmark Ed.) 19:1041–56 [Google Scholar]
  31. Shimizu Y, Hasegawa S, Fujimura S, Sugimura T. 31.  1967. Solubilization of enzyme forming ADPR polymer from NAD. Biochem. Biophys. Res. Commun. 29:80–83 [Google Scholar]
  32. Schreiber V, Dantzer F, Amé JC, de Murcia G. 32.  2006. Poly(ADP-ribose): novel functions for an old molecule. Nat. Rev. Mol. Cell Biol. 7:517–28 [Google Scholar]
  33. De Flora A, Zocchi E, Guida L, Franco L, Bruzzone S. 33.  2004. Autocrine and paracrine calcium signaling by the CD38/NAD+/cyclic ADP-ribose system. Ann. N.Y. Acad. Sci. 1028:176–91 [Google Scholar]
  34. Seman M, Adriouch S, Haag F, Koch-Nolte F. 34.  2004. Ecto-ADP-ribosyltransferases (ARTs): emerging actors in cell communication and signaling. Curr. Med. Chem. 11:857–72 [Google Scholar]
  35. Leung A, Todorova T, Ando Y, Chang P. 35.  2012. Poly(ADP-ribose) regulates post-transcriptional gene regulation in the cytoplasm. RNA Biol. 9:542–548 [Google Scholar]
  36. Vyas S, Chesarone-Cataldo M, Todorova T, Huang YH, Chang P. 36.  2013. A systematic analysis of the PARP protein family identifies new functions critical for cell physiology. Nat. Commun. 4:2240 [Google Scholar]
  37. Liu Y, Snow BE, Kickhoefer VA, Erdmann N, Zhou W. 37.  et al. 2004. Vault poly(ADP-ribose) polymerase is associated with mammalian telomerase and is dispensable for telomerase function and vault structure in vivo. Mol. Cell. Biol. 24:5314–23 [Google Scholar]
  38. Smith S, Giriat I, Schmitt A, de Lange T. 38.  1998. Tankyrase, a poly(ADP-ribose) polymerase at human telomeres. Science 282:1484–87 [Google Scholar]
  39. Chi NW, Lodish HF. 39.  2000. Tankyrase is a Golgi-associated mitogen-activated protein kinase substrate that interacts with IRAP in GLUT4 vesicles. J. Biol. Chem. 275:38437–44 [Google Scholar]
  40. Chou H-Y, Chou H, Lee S-C. 40.  2006. CDK-dependent activation of poly(ADP-ribose) polymerase member 10 (PARP10). J. Biol. Chem. 281:15201–7 [Google Scholar]
  41. Karlberg T, Langelier MF, Pascal JM, Schüler H. 41.  2013. Structural biology of the writers, readers, and erasers in mono- and poly(ADP-ribose) mediated signaling. Mol. Aspects Med. 34:1088–108 [Google Scholar]
  42. Hassa PO, Haenni S, Elser M, Hottiger MO. 42.  2006. Nuclear ADP-ribosylation reactions in mammalian cells: Where are we today and where are we going?. Microbiol. Mol. Biol. Rev. 70:789–829 [Google Scholar]
  43. Leung AK. 43.  2014. Poly(ADP-ribose): an organizer of cellular architecture. J. Cell Biol. 205:613–19 [Google Scholar]
  44. Vyas S, Matic I, Uchima L, Rood J, Žaja R. 44.  et al. 2014. Family-wide analysis of poly(ADP-ribose) polymerase activity. Nat. Commun. 5:4426 [Google Scholar]
  45. Shieh W, Amé J, Wilson M, Wang Z, Koh D. 45.  et al. 1998. Poly(ADP-ribose) polymerase null mouse cells synthesize ADP-ribose polymers. J. Biol. Chem. 273:30069–72 [Google Scholar]
  46. Amé JC, Rolli V, Schreiber V, Niedergang C, Apiou F. 46.  et al. 1999. PARP-2, a novel mammalian DNA damage–dependent poly(ADP-ribose) polymerase. J. Biol. Chem. 274:17860–68 [Google Scholar]
  47. Cook BD, Dynek JN, Chang W, Shostak G, Smith S. 47.  2002. Role for the related poly(ADP-ribose) polymerases tankyrase 1 and 2 at human telomeres. Mol. Cell. Biol. 22:332–42 [Google Scholar]
  48. Langelier MF, Riccio AA, Pascal JM. 48.  2014. PARP-2 and PARP-3 are selectively activated by 5′ phosphorylated DNA breaks through an allosteric regulatory mechanism shared with PARP-1. Nucleic Acids Res. 42:7762–75 [Google Scholar]
  49. Bürkle A, Virág L. 49.  2013. Poly(ADP-ribose): PARadigms and PARadoxes. Mol. Aspects Med. 34:1046–65 [Google Scholar]
  50. Léger K, Bar D, Savić N, Santoro R, Hottiger MO. 50.  2014. ARTD2 activity is stimulated by RNA. Nucleic Acids Res. 42:5072–82 [Google Scholar]
  51. Kleine H, Poreba E, Lesniewicz K, Hassa PO, Hottiger MO. 51.  et al. 2008. Substrate-assisted catalysis by PARP10 limits its activity to mono-ADP-ribosylation. Mol. Cell 32:57–69 [Google Scholar]
  52. Ogata N, Ueda K, Kawaichi M, Hayaishi O. 52.  1981. Poly(ADP-ribose) synthetase, a main acceptor of poly(ADP-ribose) in isolated nuclei. J. Biol. Chem. 256:4135–37 [Google Scholar]
  53. Haenni SS, Hassa PO, Altmeyer M, Fey M, Imhof R, Hottiger MO. 53.  2008. Identification of lysines 36 and 37 of PARP-2 as targets for acetylation and auto-ADP-ribosylation. Int. J. Biochem. Cell Biol. 40:2274–83 [Google Scholar]
  54. Altmeyer M, Messner S, Hassa PO, Fey M, Hottiger MO. 54.  2009. Molecular mechanism of poly(ADP-ribosyl)ation by PARP1 and identification of lysine residues as ADP-ribose acceptor sites. Nucleic Acids Res. 37:3723–38 [Google Scholar]
  55. Gagné J-P, Isabelle M, Lo K, Bourassa S, Hendzel M. 55.  et al. 2008. Proteome-wide identification of poly(ADP-ribose) binding proteins and poly(ADP-ribose)-associated protein complexes. Nucleic Acids Res. 36:6959–76 [Google Scholar]
  56. Kraus WL, Hottiger MO. 56.  2013. PARP-1 and gene regulation: progress and puzzles. Mol. Aspects Med. 34:1109–23 [Google Scholar]
  57. Virág L, Robaszkiewicz A, Rodriguez-Vargas JM, Oliver FJ. 57.  2013. Poly(ADP-ribose) signaling in cell death. Mol. Aspects Med. 34:1153–67 [Google Scholar]
  58. Durkacz BW, Omidiji O, Gray DA, Shall S. 58.  1980. (ADP-ribose)n participates in DNA excision repair. Nature 283:593–96 [Google Scholar]
  59. Rouleau M, Patel A, Hendzel M, Kaufmann S, Poirier G. 59.  2010. PARP inhibition: PARP1 and beyond. Nat. Rev. Cancer 10:293–301 [Google Scholar]
  60. Steffen JD, Brody JR, Armen RS, Pascal JM. 60.  2013. Structural implications for selective targeting of PARPs. Front. Oncol. 3:301 [Google Scholar]
  61. Lindgren AE, Karlberg T, Thorsell AG, Hesse M, Spjut S. 61.  et al. 2013. PARP inhibitor with selectivity toward ADP-ribosyltransferase ARTD3/PARP3. ACS Chem. Biol. 8:1698–703 [Google Scholar]
  62. Riffell JL, Lord CJ, Ashworth A. 62.  2012. Tankyrase-targeted therapeutics: expanding opportunities in the PARP family. Nat. Rev. Drug Discov. 11:923–36 [Google Scholar]
  63. Wahlberg E, Karlberg T, Kouznetsova E, Markova N, Macchiarulo A. 63.  et al. 2012. Family-wide chemical profiling and structural analysis of PARP and tankyrase inhibitors. Nat. Biotechnol. 30:283–88 [Google Scholar]
  64. Bryant H, Schultz N, Thomas H, Parker K, Flower D. 64.  et al. 2005. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 434:913–17 [Google Scholar]
  65. Farmer H, McCabe N, Lord C, Tutt A, Johnson D. 65.  et al. 2005. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434:917–21 [Google Scholar]
  66. Zaremba T, Curtin NJ. 66.  2007. PARP inhibitor development for systemic cancer targeting. Anticancer Agents Med. Chem. 7:515–23 [Google Scholar]
  67. Lord CJ, Ashworth A. 67.  2013. Mechanisms of resistance to therapies targeting BRCA-mutant cancers. Nat. Med. 19:1381–88 [Google Scholar]
  68. Kalisch T, Amé JC, Dantzer F, Schreiber V. 68.  2012. New readers and interpretations of poly(ADP-ribosyl)ation. Trends Biochem. Sci. 37:381–90 [Google Scholar]
  69. Žaja R, Mikoč A, Barkauskaite E, Ahel I. 69.  2012. Molecular insights into poly(ADP-ribose) recognition and processing. Biomolecules 3:1–17 [Google Scholar]
  70. Krietsch J, Rouleau M, Pic E, Ethier C, Dawson TM. 70.  et al. 2013. Reprogramming cellular events by poly(ADP-ribose)-binding proteins. Mol. Aspects Med. 34:1066–87 [Google Scholar]
  71. Barkauskaite E, Jankevicius G, Ladurner AG, Ahel I, Timinszky G. 71.  2013. The recognition and removal of cellular poly(ADP-ribose) signals. FEBS J. 280:3491–507 [Google Scholar]
  72. Panzeter PL, Realini CA, Althaus FR. 72.  1992. Noncovalent interactions of poly(adenosine diphosphate ribose) with histones. Biochemistry 31:1379–85 [Google Scholar]
  73. Pleschke J, Kleczkowska H, Strohm M, Althaus F. 73.  2000. Poly(ADP-ribose) binds to specific domains in DNA damage checkpoint proteins. J. Biol. Chem. 275:40974–80 [Google Scholar]
  74. Wang Y, Kim NS, Haince JF, Kang HC, David KK. 74.  et al. 2011. Poly(ADP-ribose) (PAR) binding to apoptosis-inducing factor is critical for PAR polymerase 1–dependent cell death (parthanatos). Sci. Signal 4:ra20 [Google Scholar]
  75. Ahel I, Ahel D, Matsusaka T, Clark AJ, Pines J. 75.  et al. 2008. Poly(ADP-ribose)-binding zinc finger motifs in DNA repair/checkpoint proteins. Nature 451:81–85 [Google Scholar]
  76. Eustermann S, Brockmann C, Mehrotra P, Yang J-C, Loakes D. 76.  et al. 2010. Solution structures of the two PBZ domains from human APLF and their interaction with poly(ADP-ribose). Nat. Struct. Mol. Biol. 17:241–43 [Google Scholar]
  77. Oberoi J, Richards MW, Crumpler S, Brown N, Blagg J, Bayliss R. 77.  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. 285:39348–58 [Google Scholar]
  78. Li GY, McCulloch RD, Fenton AL, Cheung M, Meng L. 78.  et al. 2010. Structure and identification of ADP-ribose recognition motifs of APLF and role in the DNA damage response. PNAS 107:9129–34 [Google Scholar]
  79. Aravind L. 79.  2001. The WWE domain: a common interaction module in protein ubiquitination and ADP ribosylation. Trends Biochem. Sci. 26:273–75 [Google Scholar]
  80. Wang Z, Michaud GA, Cheng Z, Zhang Y, Hinds TR. 80.  et al. 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. 26:235–40 [Google Scholar]
  81. He F, Tsuda K, Takahashi M, Kuwasako K, Terada T. 81.  et al. 2012. Structural insight into the interaction of ADP-ribose with the PARP WWE domains. FEBS Lett. 586:3858–64 [Google Scholar]
  82. Zhang Y, Liu S, Mickanin C, Feng Y, Charlat O. 82.  et al. 2011. RNF146 is a poly(ADP-ribose)-directed E3 ligase that regulates axin degradation and Wnt signalling. Nat. Cell Biol. 13:623–29 [Google Scholar]
  83. Gorbalenya AE, Koonin EV, Lai MM. 83.  1991. Putative papain-related thiol proteases of positive-strand RNA viruses. Identification of rubi- and aphthovirus proteases and delineation of a novel conserved domain associated with proteases of rubi-, alpha- and coronaviruses. FEBS Lett. 288:201–5 [Google Scholar]
  84. Pehrson J, Fried V. 84.  1992. MacroH2A, a core histone containing a large nonhistone region. Science 257:1398–400 [Google Scholar]
  85. Karras G, Kustatscher G, Buhecha H, Allen M, Pugieux C. 85.  et al. 2005. The macro domain is an ADP-ribose binding module. EMBO J. 24:1911–20 [Google Scholar]
  86. Han W, Li X, Fu X. 86.  2011. The macro domain protein family: structure, functions, and their potential therapeutic implications. Mutat. Res. 727:86–103 [Google Scholar]
  87. Feijs KL, Forst AH, Verheugd P, Lüscher B. 87.  2013. Macrodomain-containing proteins: regulating new intracellular functions of mono(ADP-ribosyl)ation. Nat. Rev. Mol. Cell Biol. 14:443–51 [Google Scholar]
  88. Allen MD, Buckle AM, Cordell SC, Lowe J, Bycroft M. 88.  2003. The crystal structure of AF1521 a protein from Archaeoglobus fulgidus with homology to the non-histone domain of macroH2A. J. Mol. Biol. 330:503–11 [Google Scholar]
  89. Timinszky G, Till S, Hassa PO, Hothorn M, Kustatscher G. 89.  et al. 2009. A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nat. Struct. Mol. Biol. 16:923–29 [Google Scholar]
  90. Aguiar RC, Yakushijin Y, Kharbanda S, Salgia R, Fletcher JA, Shipp MA. 90.  2000. BAL is a novel risk-related gene in diffuse large B-cell lymphomas that enhances cellular migration. Blood 96:4328–34 [Google Scholar]
  91. Cho SH, Goenka S, Henttinen T, Gudapati P, Reinikainen A. 91.  et al. 2009. PARP-14, a member of the B aggressive lymphoma family, transduces survival signals in primary B cells. Blood 113:2416–25 [Google Scholar]
  92. Kapoor A, Goldberg MS, Cumberland LK, Ratnakumar K, Segura MF. 92.  et al. 2010. The histone variant macroH2A suppresses melanoma progression through regulation of CDK8. Nature 468:1105–9 [Google Scholar]
  93. Koch-Nolte F, Kernstock S, Mueller-Dieckmann C, Weiss M, Haag F. 93.  2008. Mammalian ADP-ribosyltransferases and ADP-ribosylhydrolases. Front. Biosci. 13:671629 [Google Scholar]
  94. Alvarez-Gonzalez R, Althaus FR. 94.  1989. Poly(ADP-ribose) catabolism in mammalian cells exposed to DNA-damaging agents. Mutat. Res. 218:67–74 [Google Scholar]
  95. Bonicalzi ME, Haince JF, Droit A, Poirier GG. 95.  2005. Regulation of poly(ADP-ribose) metabolism by poly(ADP-ribose) glycohydrolase: Where and when?. Cell Mol. Life Sci. 62:739–50 [Google Scholar]
  96. Mashimo M, Kato J, Moss J. 96.  2014. Structure and function of the ARH family of ADP-ribosyl-acceptor hydrolases. DNA Repair 23:88–94 [Google Scholar]
  97. Haince JF, Ouellet ME, McDonald D, Hendzel MJ, Poirier GG. 97.  2006. Dynamic relocation of poly(ADP-ribose) glycohydrolase isoforms during radiation-induced DNA damage. Biochim. Biophys. Acta 1763:226–37 [Google Scholar]
  98. Hatakeyama K, Nemoto Y, Ueda K, Hayaishi O. 98.  1986. Purification and characterization of poly(ADP-ribose) glycohydrolase. Different modes of action on large and small poly(ADP-ribose). J. Biol. Chem. 261:14902–11 [Google Scholar]
  99. Slade D, Dunstan MS, Barkauskaite E, Weston R, Lafite P. 99.  et al. 2011. The structure and catalytic mechanism of a poly(ADP-ribose) glycohydrolase. Nature 477:616–20 [Google Scholar]
  100. Patel CN, Koh DW, Jacobson MK, Oliveira MA. 100.  2005. Identification of three critical acidic residues of poly(ADP-ribose) glycohydrolase involved in catalysis: determining the PARG catalytic domain. Biochem. J. 388:493–500 [Google Scholar]
  101. Min W, Wang Z-Q. 101.  2009. Poly(ADP-ribose) glycohydrolase (PARG) and its therapeutic potential. Front. Biosci. 14:1619–26 [Google Scholar]
  102. Braun SA, Panzeter PL, Collinge MA, Althaus FR. 102.  1994. Endoglycosidic cleavage of branched polymers by poly(ADP-ribose) glycohydrolase. Eur. J. Biochem. 220:369–75 [Google Scholar]
  103. Uchida K, Suzuki H, Maruta H, Abe H, Aoki K. 103.  et al. 1993. Preferential degradation of protein-bound (ADP-ribose)n by nuclear poly(ADP-ribose) glycohydrolase from human placenta. J. Biol. Chem. 268:3194–200 [Google Scholar]
  104. Amé JC, Jacobson EL, Jacobson MK. 104.  1999. Molecular heterogeneity and regulation of poly(ADP-ribose) glycohydrolase. Mol. Cell Biochem. 193:75–81 [Google Scholar]
  105. Feng X, Koh DW. 105.  2013. Roles of poly(ADP-ribose) glycohydrolase in DNA damage and apoptosis. Int. Rev. Cell Mol. Biol. 304:227–81 [Google Scholar]
  106. Blenn C, Wyrsch P, Althaus FR. 106.  2011. The ups and downs of tannins as inhibitors of poly(ADP-ribose)glycohydrolase. Molecules 16:1854–77 [Google Scholar]
  107. Slama JT, Aboul-Ela N, Jacobson MK. 107.  1995. Mechanism of inhibition of poly(ADP-ribose) glycohydrolase by adenosine diphosphate (hydroxymethyl)pyrrolidinediol. J. Med. Chem. 38:4332–36 [Google Scholar]
  108. Steffen JD, Coyle DL, Damodaran K, Beroza P, Jacobson MK. 108.  2011. Discovery and structure–activity relationships of modified salicylanilides as cell permeable inhibitors of poly(ADP-ribose) glycohydrolase (PARG). J. Med. Chem. 54:5403–13 [Google Scholar]
  109. Finch KE, Knezevic CE, Nottbohm AC, Partlow KC, Hergenrother PJ. 109.  2012. Selective small molecule inhibition of poly(ADP-ribose) glycohydrolase (PARG). ACS Chem. Biol. 7:563–70 [Google Scholar]
  110. Islam R, Koizumi F, Kodera Y, Inoue K, Okawara T, Masutani M. 110.  2014. Design and synthesis of phenolic hydrazide hydrazones as potent poly(ADP-ribose) glycohydrolase (PARG) inhibitors. Bioorg. Med. Chem. Lett. 24:3802–6 [Google Scholar]
  111. Fathers C, Drayton RM, Solovieva S, Bryant HE. 111.  2012. Inhibition of poly(ADP-ribose) glycohydrolase (PARG) specifically kills BRCA2-deficient tumor cells. Cell Cycle 11:990–97 [Google Scholar]
  112. Moss J, Stanley SJ, Nightingale MS, Murtagh JJ Jr, Monaco L. 112.  et al. 1992. Molecular and immunological characterization of ADP-ribosylarginine hydrolases. J. Biol. Chem. 267:10481–88 [Google Scholar]
  113. Mashimo M, Kato J, Moss J. 113.  2013. ADP-ribosyl-acceptor hydrolase 3 regulates poly(ADP-ribose) degradation and cell death during oxidative stress. PNAS 110:18964–69 [Google Scholar]
  114. Mueller-Dieckmann C, Kernstock S, Lisurek M, von Kries J, Haag F. 114.  et al. 2006. The structure of human ADP-ribosylhydrolase 3 (ARH3) provides insights into the reversibility of protein ADP-ribosylation. PNAS 103:15026–31 [Google Scholar]
  115. Oka S, Kato J, Moss J. 115.  2006. Identification and characterization of a mammalian 39-kDa poly(ADP-ribose) glycohydrolase. J. Biol. Chem. 281:705–13 [Google Scholar]
  116. Ono T, Kasamatsu A, Oka S, Moss J. 116.  2006. The 39-kDa poly(ADP-ribose) glycohydrolase ARH3 hydrolyzes O-acetyl-ADP-ribose, a product of the Sir2 family of acetyl-histone deacetylases. PNAS 103:16687–91 [Google Scholar]
  117. Niere M, Mashimo M, Agledal L, Dolle C, Kasamatsu A. 117.  et al. 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. 287:16088–102 [Google Scholar]
  118. Kasamatsu A, Nakao M, Smith BC, Comstock LR, Ono T. 118.  et al. 2011. Hydrolysis of O-acetyl-ADP-ribose isomers by ADP-ribosylhydrolase 3. J. Biol. Chem. 286:21110–17 [Google Scholar]
  119. Sharifi R, Morra R, Appel CD, Tallis M, Chioza B. 119.  et al. 2013. Deficiency of terminal ADP-ribose protein glycohydrolase TARG1/C6orf130 in neurodegenerative disease. EMBO J. 32:1225–37 [Google Scholar]
  120. Neuvonen M, Ahola T. 120.  2009. Differential activities of cellular and viral macro domain proteins in binding of ADP-ribose metabolites. J. Mol. Biol. 385:212–25 [Google Scholar]
  121. Chen D, Vollmar M, Rossi MN, Phillips C, Kraehenbuehl R. 121.  et al. 2011. Identification of macrodomain proteins as novel O-acetyl-ADP-ribose deacetylases. J. Biol. Chem. 286:13261–71 [Google Scholar]
  122. Rosenthal F, Feijs KLH, Frugier E, Bonalli M, Forst AH. 122.  et al. 2013. Macrodomain-containing proteins are novel mono-ADP-ribosylhydrolases. Nat. Struct. Mol. Biol. 20:502–7 [Google Scholar]
  123. Jankevicius G, Hassler M, Golia B, Rybin V, Zacharias M. 123.  et al. 2013. A family of macrodomain proteins reverses cellular mono-ADP-ribosylation. Nat. Struct. Mol. Biol. 20:508–14 [Google Scholar]
  124. Yang J, Zhao YL, Wu ZQ, Si YL, Meng YG. 124.  et al. 2009. The single-macrodomain protein LRP16 is an essential cofactor of androgen receptor. Endocr. Relat. Cancer 16:139–53 [Google Scholar]
  125. Wolffe AP, Guschin D. 125.  2000. Review: Chromatin structural features and targets that regulate transcription. J. Struct. Biol. 129:102–22 [Google Scholar]
  126. Voigt P, Tee WW, Reinberg D. 126.  2013. A double take on bivalent promoters. Genes Dev. 27:1318–38 [Google Scholar]
  127. Pinnola A, Naumova N, Shah M, Tulin A. 127.  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. 282:32511–19 [Google Scholar]
  128. Clark NJ, Kramer M, Muthurajan UM, Luger K. 128.  2012. Alternative modes of binding of poly(ADP-ribose) polymerase 1 to free DNA and nucleosomes. J. Biol. Chem. 287:32430–39 [Google Scholar]
  129. Krishnakumar R, Gamble M, Frizzell K, Berrocal J, Kininis M, Kraus W. 129.  2008. Reciprocal binding of PARP-1 and histone H1 at promoters specifies transcriptional outcomes. Science 319:819–21 [Google Scholar]
  130. Frizzell K, Gamble M, Berrocal J, Zhang T, Krishnakumar R. 130.  et al. 2009. Global analysis of transcriptional regulation by poly(ADP-ribose) polymerase 1 and poly(ADP-ribose) glycohydrolase in MCF-7 human breast cancer cells. J. Biol. Chem. 284:33926–38 [Google Scholar]
  131. Szántó M, Brunyánszki A, Kiss B, Nagy L, Gergely P. 131.  et al. 2012. Poly(ADP-ribose) polymerase 2: emerging transcriptional roles of a DNA-repair protein. Cell Mol. Life Sci. 69:4079–92 [Google Scholar]
  132. Bai P, Canto C, Brunyánszki A, Huber A, Szántó M. 132.  et al. 2011. PARP-2 regulates SIRT1 expression and whole-body energy expenditure. Cell Metab. 13:450–60 [Google Scholar]
  133. Rouleau M, Saxena V, Rodrigue A, Paquet ER, Gagnon A. 133.  et al. 2011. A key role for poly(ADP-ribose) polymerase 3 in ectodermal specification and neural crest development. PLOS ONE 6:e15834 [Google Scholar]
  134. Guetg C, Santoro R. 134.  2012. Formation of nuclear heterochromatin: the nucleolar point of view. Epigenetics 7:811–14 [Google Scholar]
  135. Boamah EK, Kotova E, Garabedian M, Jarnik M, Tulin AV. 135.  2012. Poly(ADP-ribose) polymerase 1 (PARP-1) regulates ribosomal biogenesis in Drosophila nucleoli. PLOS Genet. 8:e1002442 [Google Scholar]
  136. Meder VS, Boeglin M, de Murcia G, Schreiber V. 136.  2005. PARP-1 and PARP-2 interact with nucleophosmin/B23 and accumulate in transcriptionally active nucleoli. J. Cell Sci. 118:211–22 [Google Scholar]
  137. Kanai M, Uchida M, Hanai S, Uematsu N, Uchida K, Miwa M. 137.  2000. Poly(ADP-ribose) polymerase localizes to the centrosomes and chromosomes. Biochem. Biophys. Res. Commun. 278:385–89 [Google Scholar]
  138. Saxena A, Wong LH, Kalitsis P, Earle E, Shaffer LG, Choo KH. 138.  2002. Poly(ADP-ribose) polymerase 2 localizes to mammalian active centromeres and interacts with PARP-1, Cenpa, Cenpb and Bub3, but not Cenpc. Hum. Mol. Genet. 11:2319–29 [Google Scholar]
  139. Quénet D, Gasser V, Fouillen L, Cammas F, Sanglier-Cianferani S. 139.  et al. 2008. The histone subcode: Poly(ADP-ribose) polymerase 1 (Parp-1) and Parp-2 control cell differentiation by regulating the transcriptional intermediary factor TIF1β and the heterochromatin protein HP1α. FASEB J. 22:3853–65 [Google Scholar]
  140. Chang W, Dynek JN, Smith S. 140.  2005. NuMA is a major acceptor of poly(ADP-ribosyl)ation by tankyrase 1 in mitosis. Biochem. J. 391:177–84 [Google Scholar]
  141. Hsiao S, Smith S. 141.  2008. Tankyrase function at telomeres, spindle poles, and beyond. Biochimie 90:83–92 [Google Scholar]
  142. Ju B-G, Lunyak V, Perissi V, Garcia-Bassets I, Rose D. 142.  et al. 2006. A topoisomerase IIβ–mediated dsDNA break required for regulated transcription. Science 312:1798–802 [Google Scholar]
  143. Erener S, Hesse M, Kostadinova R, Hottiger MO. 143.  2012. Poly(ADP-ribose)polymerase 1 (PARP1) controls adipogenic gene expression and adipocyte function. Mol. Endocrinol. 26:79–86 [Google Scholar]
  144. Luo X, Kraus WL. 144.  2012. On PAR with PARP: cellular stress signaling through poly(ADP-ribose) and PARP-1. Genes Dev. 26:417–32 [Google Scholar]
  145. Kim M, Mauro S, Gévry N, Lis J, Kraus W. 145.  2004. NAD+-dependent modulation of chromatin structure and transcription by nucleosome binding properties of PARP-1. Cell 119:803–14 [Google Scholar]
  146. Thomas CJ, Kotova E, Andrake M, Adolf-Bryfogle J, Glaser R. 146.  et al. 2014. Kinase-mediated changes in nucleosome conformation trigger chromatin decondensation via poly(ADP-ribosyl)ation. Mol. Cell 53:831–42 [Google Scholar]
  147. Guastafierro T, Cecchinelli B, Zampieri M, Reale A, Riggio G. 147.  et al. 2008. CCCTC-binding factor activates PARP-1 affecting DNA methylation machinery. J. Biol. Chem. 283:21873–80 [Google Scholar]
  148. Ouararhni K, Hadj-Slimane R, Ait-Si-Ali S, Robin P, Mietton F. 148.  et al. 2006. The histone variant mH2A1.1 interferes with transcription by down-regulating PARP-1 enzymatic activity. Genes Dev. 20:3324–36 [Google Scholar]
  149. Wright RH, Castellano G, Bonet J, Le Dily F, Font-Mateu J. 149.  et al. 2012. CDK2-dependent activation of PARP-1 is required for hormonal gene regulation in breast cancer cells. Genes Dev. 26:1972–83 [Google Scholar]
  150. Kassner I, Andersson A, Fey M, Tomas M, Ferrando-May E, Hottiger MO. 150.  2013. SET7/9-dependent methylation of ARTD1 at K508 stimulates poly-ADP-ribose formation after oxidative stress. Open Biol. 3:120173 [Google Scholar]
  151. Krishnakumar R, Kraus W. 151.  2010. The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Mol. Cell 39:8–24 [Google Scholar]
  152. Tulin A, Spradling A. 152.  2003. Chromatin loosening by poly(ADP)-ribose polymerase (PARP) at Drosophila puff loci. Science 299:560–62 [Google Scholar]
  153. Zhang T, Berrocal JG, Yao J, DuMond ME, Krishnakumar R. 153.  et al. 2012. Regulation of poly(ADP-ribose) polymerase-1-dependent gene expression through promoter-directed recruitment of a nuclear NAD+ synthase. J. Biol. Chem. 287:12405–16 [Google Scholar]
  154. Bintu L, Ishibashi T, Dangkulwanich M, Wu YY, Lubkowska L. 154.  et al. 2012. Nucleosomal elements that control the topography of the barrier to transcription. Cell 151:738–49 [Google Scholar]
  155. Petesch SJ, Lis JT. 155.  2012. Overcoming the nucleosome barrier during transcript elongation. Trends Genet. 28:285–94 [Google Scholar]
  156. Poirier G, de Murcia G, Jongstra-Bilen J, Niedergang C, Mandel P. 156.  1982. Poly(ADP-ribosyl)ation of polynucleosomes causes relaxation of chromatin structure. PNAS 79:3423–27 [Google Scholar]
  157. Gaudreau A, Menard L, de Murcia G, Poirier GG. 157.  1986. Poly(ADP-ribose) accessibility to poly(ADP-ribose) glycohydrolase activity on poly(ADP-ribosyl)ated nucleosomal proteins. Biochem. Cell Biol. 64:146–53 [Google Scholar]
  158. Realini C, Althaus F. 158.  1992. Histone shuttling by poly(ADP-ribosylation). J. Biol. Chem. 267:18858–65 [Google Scholar]
  159. Erener S, Petrilli V, Kassner I, Minotti R, Castillo R. 159.  et al. 2012. Inflammasome-activated caspase 7 cleaves PARP1 to enhance the expression of a subset of NF-κB target genes. Mol. Cell 46:200–11 [Google Scholar]
  160. Hough C, Smulson M. 160.  1984. Association of poly(adenosine diphosphate ribosylated) nucleosomes with transcriptionally active and inactive regions of chromatin. Biochemistry 23:5016–23 [Google Scholar]
  161. Perez-Lamigueiro MA, Alvarez-Gonzalez R. 161.  2004. Polynucleosomal synthesis of poly(ADP-ribose) causes chromatin unfolding as determined by micrococcal nuclease digestion. Ann. N. Y. Acad. Sci. 1030:593–98 [Google Scholar]
  162. Yoon YS, Kim JW, Kang KW, Kim YS, Choi KH, Joe CO. 162.  1996. Poly(ADP-ribosyl)ation of histone H1 correlates with internucleosomal DNA fragmentation during apoptosis. J. Biol. Chem. 271:9129–34 [Google Scholar]
  163. Aubin RJ, Frechette A, de Murcia G, Mandel P, Lord A. 163.  et al. 1983. Correlation between endogenous nucleosomal hyper(ADP-ribosyl)ation of histone H1 and the induction of chromatin relaxation. EMBO J. 2:1685–93 [Google Scholar]
  164. Wacker D, Ruhl D, Balagamwala E, Hope K, Zhang T, Kraus W. 164.  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. 27:7475–85 [Google Scholar]
  165. Ahel D, Horejsí Z, Wiechens N, Polo SE, Garcia-Wilson E. 165.  et al. 2009. Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science 325:1240–43 [Google Scholar]
  166. Gottschalk A, Timinszky G, Kong S, Jin J, Cai Y. 166.  et al. 2009. Poly(ADP-ribosyl)ation directs recruitment and activation of an ATP-dependent chromatin remodeler. PNAS 106:13770–74 [Google Scholar]
  167. Sala A, La Rocca G, Burgio G, Kotova E, Di Gesu D. 167.  et al. 2008. The nucleosome-remodeling ATPase ISWI is regulated by poly-ADP-ribosylation. PLOS Biol. 6:e252 [Google Scholar]
  168. Heo K, Kim H, Choi SH, Choi J, Kim K. 168.  et al. 2008. FACT-mediated exchange of histone variant H2AX regulated by phosphorylation of H2AX and ADP-ribosylation of Spt16. Mol. Cell 30:86–97 [Google Scholar]
  169. Messner S, Hottiger MO. 169.  2011. Histone ADP-ribosylation in DNA repair, replication and transcription. Trends Cell Biol. 21:534–42 [Google Scholar]
  170. Alvarez F, Muñoz F, Schilcher P, Imhof A, Almouzni G, Loyola A. 170.  2011. Sequential establishment of marks on soluble histones H3 and H4. J. Biol. Chem. 286:17714–21 [Google Scholar]
  171. Adamietz P, Bredehorst R, Hilz H. 171.  1978. ADP-ribosylated histone H1 from HeLa cultures: fundamental differences to (ADP-ribose)n–histone H1 conjugates formed in vitro. Eur. J. Biochem. 91:317–26 [Google Scholar]
  172. Burzio L, Riquelme P, Koide S. 172.  1979. ADP ribosylation of rat liver nucleosomal core histones. J. Biol. Chem. 254:3029–37 [Google Scholar]
  173. Messner S, Altmeyer M, Zhao H, Pozivil A, Roschitzki B. 173.  et al. 2010. PARP1 ADP-ribosylates lysine residues of the core histone tails. Nucleic Acids Res. 38:6350–62 [Google Scholar]
  174. Rulten SL, Fisher AE, Robert I, Zuma MC, Rouleau M. 174.  et al. 2011. PARP-3 and APLF function together to accelerate nonhomologous end-joining. Mol. Cell 41:33–45 [Google Scholar]
  175. MacPherson L, Tamblyn L, Rajendra S, Bralha F, McPherson JP, Matthews J. 175.  2013. 2,3,7,8-Tetrachlorodibenzo-p-dioxin poly(ADP-ribose) polymerase (TiPARP, ARTD14) is a mono-ADP-ribosyltransferase and repressor of aryl hydrocarbon receptor transactivation. Nucleic Acids Res. 41:1604–21 [Google Scholar]
  176. Ogata N, Ueda K, Kagamiyama H, Hayaishi O. 176.  1980. ADP-ribosylation of histone H1. Identification of glutamic acid residues 2, 14, and the COOH-terminal lysine residue as modification sites. J. Biol. Chem. 255:7616–20 [Google Scholar]
  177. Ogata N, Ueda K, Hayaishi O. 177.  1980. ADP-ribosylation of histone H2B. Identification of glutamic acid residue 2 as the modification site. J. Biol. Chem. 255:7610–15 [Google Scholar]
  178. Ushiroyama T, Tanigawa Y, Tsuchiya M, Matsuura R, Ueki M. 178.  et al. 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. 151:173–77 [Google Scholar]
  179. Fischle W, Wang Y, Allis CD. 179.  2003. Binary switches and modification cassettes in histone biology and beyond. Nature 425:475–79 [Google Scholar]
  180. Hassa PO, Hottiger MO. 180.  2005. An epigenetic code for DNA damage repair pathways?. Biochem. Cell Biol. 83:270–85 [Google Scholar]
  181. Malik N, Smulson M. 181.  1984. A relationship between nuclear poly(adenosine diphosphate ribosylation) and acetylation posttranslational modifications. 1. Nucleosome studies. Biochemistry 23:3721–25 [Google Scholar]
  182. Wong M, Miwa M, Sugimura T, Smulson M. 182.  1983. Relationship between histone H1 poly(adenosine diphosphate ribosylation) and histone H1 phosphorylation using anti-poly(adenosine diphosphate ribose) antibody. Biochemistry 22:2384–89 [Google Scholar]
  183. Tanigawa Y, Tsuchiya M, Imai Y, Shimoyama M. 183.  1983. Mono (ADP-ribosyl)ation of hen liver nuclear proteins suppresses phosphorylation. Biochem. Biophys. Res. Commun. 113:135–41 [Google Scholar]
  184. Kassner I, Barandun M, Fey M, Rosenthal F, Hottiger MO. 184.  2013. Crosstalk between SET7/9-dependent methylation and ARTD1-mediated ADP-ribosylation of histone H1.4. Epigenetics Chromatin 6:1 [Google Scholar]
  185. Krishnakumar R, Kraus W. 185.  2010. PARP-1 regulates chromatin structure and transcription through a KDM5B-dependent pathway. Mol. Cell 39:736–49 [Google Scholar]
  186. Le May N, Iltis I, Amé JC, Zhovmer A, Biard D. 186.  et al. 2012. Poly(ADP-ribose) glycohydrolase regulates retinoic acid receptor–mediated gene expression. Mol. Cell 48:785–98 [Google Scholar]
  187. Bird A. 187.  2007. Perceptions of epigenetics. Nature 447:396–98 [Google Scholar]
  188. Attwood JT, Yung RL, Richardson BC. 188.  2002. DNA methylation and the regulation of gene transcription. Cell Mol. Life Sci. 59:241–57 [Google Scholar]
  189. de Capoa A, Febbo F, Giovannelli F, Niveleau A, Zardo G. 189.  et al. 1999. Reduced levels of poly(ADP-ribosyl)ation result in chromatin compaction and hypermethylation as shown by cell-by-cell computer-assisted quantitative analysis. FASEB J. 13:89–93 [Google Scholar]
  190. Reale A, Matteis GD, Galleazzi G, Zampieri M, Caiafa P. 190.  2005. Modulation of DNMT1 activity by ADP-ribose polymers. Oncogene 24:13–19 [Google Scholar]
  191. Zampieri M, Guastafierro T, Calabrese R, Ciccarone F, Bacalini MG. 191.  et al. 2012. ADP-ribose polymers localized on Ctcf–Parp1–Dnmt1 complex prevent methylation of Ctcf target sites. Biochem. J. 441:645–52 [Google Scholar]
  192. Yu W, Ginjala V, Pant V, Chernukhin I, Whitehead J. 192.  et al. 2004. Poly(ADP-ribosyl)ation regulates CTCF-dependent chromatin insulation. Nat. Genet. 36:1105–10 [Google Scholar]
  193. Sparago A, Cerrato F, Vernucci M, Ferrero GB, Silengo MC, Riccio A. 193.  2004. Microdeletions in the human H19 DMR result in loss of IGF2 imprinting and Beckwith–Wiedemann syndrome. Nat. Genet. 36:958–60 [Google Scholar]
  194. Wossidlo M, Arand J, Sebastiano V, Lepikhov K, Boiani M. 194.  et al. 2010. Dynamic link of DNA demethylation, DNA strand breaks and repair in mouse zygotes. EMBO J. 29:1877–88 [Google Scholar]
  195. Surani MA, Hajkova P. 195.  2010. Epigenetic reprogramming of mouse germ cells toward totipotency. Cold Spring Harb. Symp. Quant. Biol. 75:211–18 [Google Scholar]
  196. Sharif O, Bolshakov V, Raines S, Newham P, Perkins N. 196.  2007. Transcriptional profiling of the LPS induced NF-κB response in macrophages. BMC Immunol. 8:1 [Google Scholar]
  197. de Vos M, El Ramy R, Quenet D, Wolf P, Spada F. 197.  et al. 2014. Poly(ADP-ribose) polymerase 1 (PARP1) associates with E3 ubiquitin–protein ligase UHRF1 and modulates UHRF1 biological functions. J. Biol. Chem. 289:16223–38 [Google Scholar]
  198. Fontán-Lozano A, Suárez-Pereira I, Horrillo A, del Pozo–Martín Y, Hmadcha A, Carrión A. 198.  2010. Histone H1 poly(ADP)-ribosylation regulates the chromatin alterations required for learning consolidation. J. Neurosci. 30:13305–13 [Google Scholar]
  199. Dantzer F, Mark M, Quenet D, Scherthan H, Huber A. 199.  et al. 2006. Poly(ADP-ribose) polymerase 2 contributes to the fidelity of male meiosis I and spermiogenesis. PNAS 103:14854–59 [Google Scholar]
  200. Rouleau M, McDonald D, Gagne P, Ouellet ME, Droit A. 200.  et al. 2007. PARP-3 associates with Polycomb group bodies and with components of the DNA damage repair machinery. J. Cell Biochem. 100:385–401 [Google Scholar]
  201. Lodhi N, Kossenkov AV, Tulin AV. 201.  2014. Bookmarking promoters in mitotic chromatin: poly(ADP-ribose)polymerase 1 as an epigenetic mark. Nucleic Acids Res. 42:7028–38 [Google Scholar]
  202. Shall S, de Murcia G. 202.  2000. Poly(ADP-ribose) polymerase 1: What have we learned from the deficient mouse model?. Mutat. Res. 460:1–15 [Google Scholar]
  203. Nasta F, Laudisi F, Sambucci M, Rosado M, Pioli C. 203.  2010. Increased Foxp3+ regulatory T cells in poly(ADP-ribose) polymerase-1 deficiency. J. Immunol. 184:3470–77 [Google Scholar]
  204. Sambucci M, Laudisi F, Novelli F, Bennici E, Rosado MM, Pioli C. 204.  2013. Effects of PARP-1 deficiency on Th1 and Th2 cell differentiation. Sci. World J. 2013:375024 [Google Scholar]
  205. von Lukowicz T, Hassa PO, Lohmann C, Borén J, Braunersreuther V. 205.  et al. 2008. PARP1 is required for adhesion molecule expression in atherogenesis. Cardiovasc. Res. 78:158–66 [Google Scholar]
  206. Pieper AA, Walles T, Wei G, Clements EE, Verma A. 206.  et al. 2000. Myocardial postischemic injury is reduced by polyADPripose polymerase 1 gene disruption. Mol. Med. 6:271–82 [Google Scholar]
  207. Erener S, Mirsaidi A, Hesse M, Tiaden AN, Ellingsgaard H. 207.  et al. 2012. ARTD1 deletion causes increased hepatic lipid accumulation in mice fed a high-fat diet and impairs adipocyte function and differentiation. FASEB J. 26:2631–38 [Google Scholar]
  208. Menissier de Murcia J, Ricoul M, Tartier L, Niedergang C, Huber A. 208.  et al. 2003. Functional interaction between PARP-1 and PARP-2 in chromosome stability and embryonic development in mouse. EMBO J. 22:2255–63 [Google Scholar]
  209. Yelamos J, Schreiber V, Dantzer F. 209.  2008. Toward specific functions of poly(ADP-ribose) polymerase-2. Trends Mol. Med. 14:169–78 [Google Scholar]
  210. Yelamos J, Monreal Y, Saenz L, Aguado E, Schreiber V. 210.  et al. 2006. PARP-2 deficiency affects the survival of CD4+CD8+ double-positive thymocytes. EMBO J. 25:4350–60 [Google Scholar]
  211. Bai P, Houten SM, Huber A, Schreiber V, Watanabe M. 211.  et al. 2007. Poly(ADP-ribose) polymerase (PPAR)-2 controls adipocyte differentiation and adipose tissue function through the regulation of the activity of the retinoid X receptor/PPAR2γ heterodimer. J. Biol. Chem. 282:37738–46 [Google Scholar]
  212. Dantzer F, Giraud-Panis MJ, Jaco I, Amé JC, Schultz I. 212.  et al. 2004. Functional interaction between poly(ADP-ribose) polymerase 2 (PARP-2) and TRF2: PARP activity negatively regulates TRF2. Mol. Cell. Biol. 24:1595–607 [Google Scholar]
  213. Szántó M, Brunyánszki A, Marton J, Vamosi G, Nagy L. 213.  et al. 2014. Deletion of PARP-2 induces hepatic cholesterol accumulation and decrease in HDL levels. Biochim. Biophys. Acta 1842:594–602 [Google Scholar]
  214. Boehler C, Gauthier LR, Mortusewicz O, Biard DS, Saliou JM. 214.  et al. 2011. Poly(ADP-ribose) polymerase 3 (PARP3), a newcomer in cellular response to DNA damage and mitotic progression. PNAS 108:2783–88 [Google Scholar]
  215. Raval-Fernandes S, Kickhoefer VA, Kitchen C, Rome LH. 215.  2005. Increased susceptibility of vault poly(ADP-ribose) polymerase–deficient mice to carcinogen-induced tumorigenesis. Cancer Res. 65:8846–52 [Google Scholar]
  216. Hsiao SJ, Poitras MF, Cook BD, Liu Y, Smith S. 216.  2006. Tankyrase 2 poly(ADP-ribose) polymerase domain–deleted mice exhibit growth defects but have normal telomere length and capping. Mol. Cell. Biol. 26:2044–54 [Google Scholar]
  217. Yeh TY, Beiswenger KK, Li P, Bolin KE, Lee RM. 217.  et al. 2009. Hypermetabolism, hyperphagia, and reduced adiposity in tankyrase-deficient mice. Diabetes 58:2476–85 [Google Scholar]
  218. Chiang YJ, Nguyen ML, Gurunathan S, Kaminker P, Tessarollo L. 218.  et al. 2006. Generation and characterization of telomere length maintenance in tankyrase 2–deficient mice. Mol. Cell. Biol. 26:2037–43 [Google Scholar]
  219. Chiang YJ, Hsiao SJ, Yver D, Cushman SW, Tessarollo L. 219.  et al. 2008. Tankyrase 1 and tankyrase 2 are essential but redundant for mouse embryonic development. PLOS ONE 3e2639 [Google Scholar]
  220. Mehrotra P, Hollenbeck A, Riley JP, Li F, Patel RJ. 220.  et al. 2013. Poly(ADP-ribose) polymerase 14 and its enzyme activity regulates TH2 differentiation and allergic airway disease. J. Allergy Clin. Immunol. 131:521–31 [Google Scholar]
  221. Goenka S, Boothby M. 221.  2006. Selective potentiation of Stat-dependent gene expression by collaborator of Stat6 (CoaSt6), a transcriptional cofactor. PNAS 103:4210–15 [Google Scholar]
  222. Schmahl J, Raymond CS, Soriano P. 222.  2007. PDGF signaling specificity is mediated through multiple immediate early genes. Nat. Genet. 39:52–60 [Google Scholar]
  223. Koh D, Lawler A, Poitras M, Sasaki M, Wattler S. 223.  et al. 2004. Failure to degrade poly(ADP-ribose) causes increased sensitivity to cytotoxicity and early embryonic lethality. PNAS 101:17699–704 [Google Scholar]
  224. Cortes U, Tong WM, Coyle DL, Meyer-Ficca ML, Meyer RG. 224.  et al. 2004. Depletion of the 110-kilodalton isoform of poly(ADP-ribose) glycohydrolase increases sensitivity to genotoxic and endotoxic stress in mice. Mol. Cell. Biol. 24:7163–78 [Google Scholar]
  225. Chabert M, Niedergang C, Hog F, Partisani M, Mandel P. 225.  1992. Poly(ADPR)polymerase expression and activity during proliferation and differentiation of rat astrocyte and neuronal cultures. Biochim. Biophys. Acta 1136:196–202 [Google Scholar]
  226. Ju B-G, Solum D, Song E, Lee K-J, Rose D. 226.  et al. 2004. Activating the PARP-1 sensor component of the groucho/TLE1 corepressor complex mediates a CaM kinase IIδ–dependent neurogenic gene activation pathway. Cell 119:815–29 [Google Scholar]
  227. Fujiki K, Shinoda A, Kano F, Sato R, Shirahige K, Murata M. 227.  2013. PPARγ-induced PARylation promotes local DNA demethylation by production of 5-hydroxymethylcytosine. Nat. Commun. 4:2262 [Google Scholar]
  228. Robaszkiewicz A, Erdélyi K, Kovács K, Kovács I, Bai P. 228.  et al. 2012. Hydrogen peroxide–induced poly(ADP-ribosyl)ation regulates osteogenic differentiation-associated cell death. Free Radic. Biol. Med. 53:1552–64 [Google Scholar]
  229. Chen J, Sun Y, Mao X, Liu Q, Wu H, Chen Y. 229.  2010. RANKL up-regulates brain-type creatine kinase via poly(ADP-ribose) polymerase 1 during osteoclastogenesis. J. Biol. Chem. 285:36315–21 [Google Scholar]
  230. Hu B, Wu Z, Hergert P, Henke CA, Bitterman PB, Phan SH. 230.  2013. Regulation of myofibroblast differentiation by poly(ADP-ribose) polymerase 1. Am. J. Pathol. 182:71–83 [Google Scholar]
  231. Hang CT, Yang J, Han P, Cheng HL, Shang C. 231.  et al. 2010. Chromatin regulation by Brg1 underlies heart muscle development and disease. Nature 466:62–67 [Google Scholar]
  232. Celik-Ozenci C, Tasatargil A. 232.  2013. Role of poly(ADP-ribose) polymerases in male reproduction. Spermatogenesis 3:e24194 [Google Scholar]
  233. Gungor-Ordueri NE, Sahin Z, Sahin P, Celik-Ozenci C. 233.  2014. The expression pattern of PARP-1 and PARP-2 in the developing and adult mouse testis. Acta Histochem. 116:958–64 [Google Scholar]
  234. Meyer-Ficca ML, Lonchar JD, Ihara M, Meistrich ML, Austin CA, Meyer RG. 234.  2011. Poly(ADP-ribose) polymerases PARP1 and PARP2 modulate topoisomerase IIβ (TOP2B) function during chromatin condensation in mouse spermiogenesis. Biol. Reprod. 84:900–9 [Google Scholar]
  235. Nusinow D, Hernández-Muñoz I, Fazzio T, Shah G, Kraus W, Panning B. 235.  2007. Poly(ADP-ribose) polymerase 1 is inhibited by a histone H2A variant, macroH2A, and contributes to silencing of the inactive X chromosome. J. Biol. Chem. 282:12851–59 [Google Scholar]
  236. Osada T, Ryden AM, Masutani M. 236.  2013. Poly(ADP-ribosylation) regulates chromatin organization through histone H3 modification and DNA methylation of the first cell cycle of mouse embryos. Biochem. Biophys. Res. Commun. 434:15–21 [Google Scholar]
  237. Roper SJ, Chrysanthou S, Senner CE, Sienerth A, Gnan S. 237.  et al. 2014. ADP-ribosyltransferases Parp1 and Parp7 safeguard pluripotency of ES cells. Nucleic Acids Res. 428914–27 [Google Scholar]
  238. Takahashi K, Yamanaka S. 238.  2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–76 [Google Scholar]
  239. Chiou SH, Jiang BH, Yu YL, Chou SJ, Tsai PH. 239.  et al. 2013. Poly(ADP-ribose) polymerase 1 regulates nuclear reprogramming and promotes iPSC generation without c-Myc. J. Exp. Med. 210:85–98 [Google Scholar]
  240. Weber FA, Bartolomei G, Hottiger MO, Cinelli P. 240.  2013. Artd1/Parp1 regulates reprogramming by transcriptional regulation of Fgf4 via Sox2 ADP-ribosylation. Stem Cells 31:2364–73 [Google Scholar]
  241. Doege CA, Inoue K, Yamashita T, Rhee DB, Travis S. 241.  et al. 2012. Early-stage epigenetic modification during somatic cell reprogramming by Parp1 and Tet2. Nature 488:652–55 [Google Scholar]
  242. Sassone-Corsi P. 242.  2012. Minireview: NAD+, a circadian metabolite with an epigenetic twist. Endocrinology 153:1–5 [Google Scholar]
  243. Asher G, Reinke H, Altmeyer M, Gutierrez-Arcelus M, Hottiger MO, Schibler U. 243.  2010. Poly(ADP-ribose) polymerase 1 participates in the phase entrainment of circadian clocks to feeding. Cell 142:943–53 [Google Scholar]
  244. Kaelin WG Jr, McKnight SL. 244.  2013. Influence of metabolism on epigenetics and disease. Cell 153:56–69 [Google Scholar]
  245. Moyle P, Muir T. 245.  2010. Method for the synthesis of Mono-ADP-ribose conjugated peptides. J. Am. Chem. Soc. 132:15878–80 [Google Scholar]
  246. Kistemaker HA, van der Heden van Noort GJ, Overkleeft HS, van der Marel GA, Filippov DV. 246.  2013. Stereoselective ribosylation of amino acids. Org. Lett. 15:2306–9 [Google Scholar]
  247. Wang Y, Rosner D, Grzywa M, Marx A. 247.  2014. Chain-terminating and clickable NAD+ analogues for labeling the target proteins of ADP-ribosyltransferases. Angew. Chem. Int. Ed. Engl. 53:8159–62 [Google Scholar]
  248. Barbarulo A, Iansante V, Chaidos A, Naresh K, Rahemtulla A. 248.  et al. 2013. Poly(ADP-ribose) polymerase family member 14 (PARP14) is a novel effector of the JNK2-dependent pro-survival signal in multiple myeloma. Oncogene 32:4231–42 [Google Scholar]
  249. Bachmann SB, Frommel SC, Camicia R, Winkler HC, Santoro R, Hassa PO. 249.  2014. DTX3L and ARTD9 inhibit IRF1 expression and mediate in cooperation with ARTD8 survival and proliferation of metastatic prostate cancer cells. Mol. Cancer 13:125 [Google Scholar]
  250. Ha K, Fiskus W, Choi DS, Bhaskara S, Cerchietti L. 250.  et al. 2014. Histone deacetylase inhibitor treatment induces ‘BRCAness’ and synergistic lethality with PARP inhibitor and cisplatin against human triple negative breast cancer cells. Oncotarget 30:5637–50 [Google Scholar]
  251. Chao OS, Goodman OB Jr. 251.  2014. Synergistic loss of prostate cancer cell viability by co-inhibition of HDAC and PARP. Mol. Cancer Res. 12:1755–66 [Google Scholar]
  252. Okayama H, Honda M, Hayaishi O. 252.  1978. Novel enzyme from rat liver that cleaves an ADP-ribosyl histone linkage. PNAS 75:2254–57 [Google Scholar]
  253. Oka J, Ueda K, Hayaishi O, Komura H, Nakanishi K. 253.  1984. ADP-ribosyl protein lyase. Purification, properties, and identification of the product. J. Biol. Chem. 259:986–95 [Google Scholar]
  254. Canto C, Sauve AA, Bai P. 254.  2013. Crosstalk between poly(ADP-ribose) polymerase and sirtuin enzymes. Mol. Aspects Med. 34:1168–201 [Google Scholar]
  255. Bai P, Canto C, Oudart H, Brunyánszki A, Cen Y. 255.  et al. 2011. PARP-1 inhibition increases mitochondrial metabolism through SIRT1 activation. Cell Metab. 13:461–68 [Google Scholar]
  256. Verdin E. 256.  2014. The many faces of sirtuins: coupling of NAD metabolism, sirtuins and lifespan. Nat. Med. 20:25–27 [Google Scholar]
  257. Kolthur-Seetharam U, Dantzer F, McBurney MW, de Murcia G, Sassone-Corsi P. 257.  2006. Control of AIF-mediated cell death by the functional interplay of SIRT1 and PARP-1 in response to DNA damage. Cell Cycle 5:873–77 [Google Scholar]
  258. Rajamohan SB, Pillai VB, Gupta M, Sundaresan NR, Birukov KG. 258.  et al. 2009. SIRT1 promotes cell survival under stress by deacetylation-dependent deactivation of poly(ADP-ribose) polymerase 1. Mol. Cell. Biol. 29:4116–29 [Google Scholar]
  259. Haenni SS, Altmeyer M, Hassa PO, Valovka T, Fey M, Hottiger MO. 259.  2008. Importin α binding and nuclear localization of PARP-2 is dependent on lysine 36, which is located within a predicted classical NLS. BMC Cell Biol. 9:39 [Google Scholar]
  260. Augustin A, Spenlehauer C, Dumond H, Menissier de Murcia J, Piel M. 260.  et al. 2003. PARP-3 localizes preferentially to the daughter centriole and interferes with the G1/S cell cycle progression. J. Cell Sci. 116:1551–62 [Google Scholar]
  261. Kickhoefer VA, Siva AC, Kedersha NL, Inman EM, Ruland C. 261.  et al. 1999. The 193-kD vault protein, VPARP, is a novel poly(ADP-ribose) polymerase. J. Cell Biol. 146:917–28 [Google Scholar]
  262. Smith S, de Lange T. 262.  1999. Cell cycle dependent localization of the telomeric PARP, tankyrase, to nuclear pore complexes and centrosomes. J. Cell Sci. 112:3649–56 [Google Scholar]
  263. Chang P, Coughlin M, Mitchison TJ. 263.  2005. Tankyrase-1 polymerization of poly(ADP-ribose) is required for spindle structure and function. Nat. Cell Biol. 7:1133–39 [Google Scholar]
  264. Leung AK, Vyas S, Rood JE, Bhutkar A, Sharp PA, Chang P. 264.  2011. Poly(ADP-ribose) regulates stress responses and microRNA activity in the cytoplasm. Mol. Cell 42:489–99 [Google Scholar]
  265. Kaminker PG, Kim SH, Taylor RD, Zebarjadian Y, Funk WD. 265.  et al. 2001. TANK2, a new TRF1-associated poly(ADP-ribose) polymerase, causes rapid induction of cell death upon overexpression. J. Biol. Chem. 276:35891–99 [Google Scholar]
  266. Yu M, Schreek S, Cerni C, Schamberger C, Lesniewicz K. 266.  et al. 2005. PARP-10, a novel Myc-interacting protein with poly(ADP-ribose) polymerase activity, inhibits transformation. Oncogene 24:1982–93 [Google Scholar]
  267. Kleine H, Herrmann A, Lamark T, Forst AH, Verheugd P. 267.  et al. 2012. Dynamic subcellular localization of the mono-ADP-ribosyltransferase ARTD10 and interaction with the ubiquitin receptor p62. Cell Commun. Signal. 10:28 [Google Scholar]
  268. Di Paola S, Micaroni M, Di Tullio G, Buccione R, Di Girolamo M. 268.  2012. PARP16/ARTD15 is a novel endoplasmic-reticulum-associated mono-ADP-ribosyltransferase that interacts with, and modifies karyopherin-ss1. PLOS ONE 7:e37352 [Google Scholar]
  269. Jwa M, Chang P. 269.  2012. PARP16 is a tail-anchored endoplasmic reticulum protein required for the PERK- and IRE1α-mediated unfolded protein response. Nat. Cell Biol. 14:1223–30 [Google Scholar]
  270. Hofmann A, Zdanov A, Genschik P, Ruvinov S, Filipowicz W, Wlodawer A. 270.  2000. Structure and mechanism of activity of the cyclic phosphodiesterase of Appr>p, a product of the tRNA splicing reaction. EMBO J. 19:6207–17 [Google Scholar]
  271. Sawaya R, Schwer B, Shuman S. 271.  2005. Structure–function analysis of the yeast NAD+-dependent tRNA 2′-phosphotransferase Tpt1. RNA 11:107–13 [Google Scholar]
  272. Bonicalzi ME, Vodenicharov M, Coulombe M, Gagne JP, Poirier GG. 272.  2003. Alteration of poly(ADP-ribose) glycohydrolase nucleocytoplasmic shuttling characteristics upon cleavage by apoptotic proteases. Biol. Cell 95:635–44 [Google Scholar]
  273. Ohashi S, Kanai M, Hanai S, Uchiumi F, Maruta H. 273.  et al. 2003. Subcellular localization of poly(ADP-ribose) glycohydrolase in mammalian cells. Biochem. Biophys. Res. Commun. 307:915–21 [Google Scholar]
  274. Meyer-Ficca ML, Meyer RG, Coyle DL, Jacobson EL, Jacobson MK. 274.  2004. Human poly(ADP-ribose) glycohydrolase is expressed in alternative splice variants yielding isoforms that localize to different cell compartments. Exp. Cell Res. 297:521–32 [Google Scholar]
  275. Meyer RG, Meyer-Ficca ML, Whatcott CJ, Jacobson EL, Jacobson MK. 275.  2007. Two small enzyme isoforms mediate mammalian mitochondrial poly(ADP-ribose) glycohydrolase (PARG) activity. Exp. Cell Res. 313:2920–36 [Google Scholar]
  276. Niere M, Kernstock S, Koch-Nolte F, Ziegler M. 276.  2008. Functional localization of two poly(ADP-ribose)-degrading enzymes to the mitochondrial matrix. Mol. Cell. Biol. 28:814–24 [Google Scholar]
  277. Wu Z, Li Y, Li X, Ti D, Zhao Y. 277.  et al. 2011. LRP16 integrates into NF-κB transcriptional complex and is required for its functional activation. PLOS ONE 6:e18157 [Google Scholar]
  278. Kang HC, Lee YI, Shin JH, Andrabi SA, Chi Z. 278.  et al. 2011. Iduna is a poly(ADP-ribose) (PAR)-dependent E3 ubiquitin ligase that regulates DNA damage. PNAS 108:14103–8 [Google Scholar]
  279. de Vos M, Schreiber V, Dantzer F. 279.  2012. The diverse roles and clinical relevance of PARPs in DNA damage repair: current state of the art. Biochem. Pharmacol. 84:137–46 [Google Scholar]
/content/journals/10.1146/annurev-biochem-060614-034506
Loading
Nuclear ADP-Ribosylation and Its Role in Chromatin Plasticity, Cell Differentiation, and Epigenetics
Annual Review of Biochemistry 84, 227 (2015); https://doi.org/10.1146/annurev-biochem-060614-034506
/content/journals/10.1146/annurev-biochem-060614-034506
/content/journals/10.1146/annurev-biochem-060614-034506
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error