The recognition and removal of cellular poly(ADP-ribose) signals

FEBS Journal

Volumn 280, Issue 15, 2013, Pages 3491-3507

  Barkauskaite, Eva ^a   Jankevicius, Gytis ^b   Ladurner, Andreas G ^b,c   Ahel, Ivan ^a   Timinszky, Gyula ^b,d  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MUNICH   (Germany)

^c MPI of Biochemistry   (Germany)

^d Munich Cluster for Systems Neurology ^*  (Germany)

Author keywords

ADP ribosylation; macrodomain; PAR binding zinc finger domain; poly(ADP ribose); poly(ADP ribose) glycohydrolase; poly(ADP ribose) polymerase; WWE domain

Indexed keywords

GLYCOSIDASE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 2; POLY(ADENOSINE DIPHOSPHATE RIBOSE); ZINC FINGER PROTEIN;

ADENOSINE DIPHOSPHATE RIBOSYLATION; AMINO ACID SEQUENCE; CATALYSIS; CELL DEATH; COVALENT BOND; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME RELEASE; HUMAN; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; UBIQUITINATION;

ADP-RIBOSYLATION; MACRODOMAIN; PAR-BINDING ZINC FINGER DOMAIN; POLY(ADP-RIBOSE); POLY(ADP-RIBOSE) GLYCOHYDROLASE; POLY(ADP-RIBOSE) POLYMERASE; WWE DOMAIN;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; CATALYTIC DOMAIN; DNA DAMAGE; GLYCOSIDE HYDROLASES; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; POLY ADENOSINE DIPHOSPHATE RIBOSE; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEINS; SIGNAL TRANSDUCTION;

EID: 84880333185     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12358     Document Type: Review

References (137)

1. Gibson B, &, Kraus L, (2012) New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat Rev Mol Cell Biol 13, 411-424.
2. Kraus L, (2008) Transcriptional control by PARP-1: chromatin modulation, enhancer-binding, coregulation, and insulation. Curr Opin Cell Biol 20, 294-302.
3. 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, 249-268.
4. 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.
5. Hottiger M, Hassa P, Lüscher B, Schüler H, &, Koch-Nolte F, (2010) Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem Sci 35, 208-219.
6. Žaja R, Mikoč A, Barkauskaite E, &, Ahel I, (2013) Molecular Insights into poly(ADP-ribose) recognition and processing. Biomolecules 3, 1-17.
7. Nishizuka Y, Ueda K, Nakazawa K, &, Hayaishi O, (1967) Studies on the polymer of adenosine diphosphate ribose. I. Enzymic formation from nicotinamide adenine dinuclotide in mammalian nuclei. J Biol Chem 242, 3164-3171.
8. Chambon P, Weill JD, &, Mandel P, (1963) Nicotinamide mononucleotide activation of new DNA-dependent polyadenylic acid synthesizing nuclear enzyme. Biochem Biophys Res Commun 11, 39-43.
9. Amé JC, Rolli V, Schreiber V, Niedergang C, Apiou F, Decker P, Muller S, Höger T, Ménissier-de Murcia J, &, de Murcia G, (1999) PARP-2, A novel mammalian DNA damage-dependent poly(ADP-ribose) polymerase. J Biol Chem 274, 17860-17868.
10. Rulten S, Fisher A, Robert I, Zuma M, Rouleau M, Ju L, Poirier G, Reina-San-Martin B, &, Caldecott K, (2011) PARP-3 and APLF function together to accelerate nonhomologous end-joining. Mol Cell 41, 33-45.
11. Hassa P, Haenni S, Elser M, &, Hottiger M, (2006) Nuclear ADP-ribosylation reactions in mammalian cells: where are we today and where are we going? Microbiol Mol Biol Rev 70, 789-829.
12. Slade D, Dunstan M, 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, 616-620.
13. 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, 6993-6999.
14. Yamanaka H, Penning CA, Willis EH, Wasson DB, &, Carson DA, (1988) Characterization of human poly(ADP-ribose) polymerase with autoantibodies. J Biol Chem 263, 3879-3883.
15. 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, 12872-12877.
16. Ménissier de Murcia J, Ricoul M, Tartier L, Niedergang C, Huber A, Dantzer F, Schreiber V, Amé J-C, Dierich A, LeMeur M, et al,. (2003) Functional interaction between PARP-1 and PARP-2 in chromosome stability and embryonic development in mouse. EMBO J 22, 2255-2263.
17. Langelier M-F, Planck J, Roy S, &, Pascal J, (2012) Structural basis for DNA damage-dependent poly(ADP-ribosyl)ation by human PARP-1. Science 336, 728-732.
18. Langelier M-F, Planck J, Roy S, &, Pascal J, (2011) Crystal structures of poly(ADP-ribose) polymerase-1 (PARP-1) zinc fingers bound to DNA. J Biol Chem 286, 10690-10701.
19. Langelier M-F, Ruhl D, Planck J, Kraus L, &, Pascal J, (2010) The Zn3 Domain of Human Poly(ADP-ribose) Polymerase-1 (PARP-1) Functions in both DNA-dependent poly(ADP-ribose) synthesis activity and chromatin compaction. J Biol Chem 285, 18877-18887.
20. 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, 685-692.
21. Tao Z, Gao P, &, Liu H-W, (2009) Identification of the ADP-ribosylation sites in the PARP-1 automodification domain: analysis and implications. J Am Chem Soc 131, 14258-14260.
22. 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, 137-146.
23. Mehrotra PV, Ahel D, Ryan D, Weston R, Wiechens N, Kraehenbuehl R, Owen-Hughes T, &, Ahel I, (2011) DNA repair factor APLF is a histone chaperone. Mol Cell 41, 46-55.
24. Ahel D, Hořejší Z, Wiechens N, Polo S, Garcia-Wilson E, Ahel I, Flynn H, Skehel M, West S, Jackson S, et al,. (2009) Poly(ADP-ribose)-dependent regulation of DNA Repair by the chromatin remodeling enzyme ALC1. Science 325, 1240-1243.
25. Gottschalk A, Timinszky G, Kong S, Jin J, Cai Y, Swanson S, Washburn M, Florens L, Ladurner A, Conaway J, et al,. (2009) Poly(ADP-ribosyl)ation directs recruitment and activation of an ATP-dependent chromatin remodeler. Proc Natl Acad Sci USA 106, 13770-13774.
26. Ogata N, Ueda K, &, Hiyaishi O, (1980) ADP-ribosylation of histone H2B. Identification of glutamic acid residue 2 as the modification site. J Biol Chem 255, 7610-7615.
27. Riquelme PT, Burzio LO, &, Koide SS, (1979) ADP ribosylation of rat liver lysine-rich histone in vitro. J Biol Chem 254, 3018-3028.
28. Matic I, Ahel I, &, Hay R, (2012) Reanalysis of phosphoproteomics data uncovers ADP-ribosylation sites. Nat Methods 9, 771-772.
29. Sharifi R, Morra R, Denise Appel C, Tallis M, Chioza B, Jankevicius G, Simpson MA, Matic I, Ozkan E, Golia B, et al,. (2013) Deficiency of terminal ADP-ribose protein glycohydrolase TARG1/C6orf130 in neurodegenerative disease. EMBO J 32, 1225-1237.
30. Altmeyer M, Messner S, Hassa P, Fey M, &, Hottiger M, (2009) Molecular mechanism of poly(ADP-ribosyl)ation by PARP1 and identification of lysine residues as ADP-ribose acceptor sites. Nucleic Acids Res 37, 3723-3738.
31. Messner S, Altmeyer M, Zhao H, Pozivil A, Roschitzki B, Gehrig P, Rutishauser D, Huang D, Caflisch A, &, Hottiger M, (2010) PARP1 ADP-ribosylates lysine residues of the core histone tails. Nucleic Acids Res 38, 6350-6362.
32. 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″-)(1â€́- ribosyl)]adenosine-5′,5″,5â€́-tris(phosphate) as a branch linkage. Proc Natl Acad Sci USA 76, 595-599.
33. Juarez-Salinas H, Levi V, Jacobson EL, &, Jacobson MK, (1982) Poly(ADP-ribose) has a branched structure in vivo. J Biol Chem 257, 607-609.
34. Kanai M, Miwa M, Kuchino Y, &, Sugimura T, (1982) Presence of branched portion in poly(adenosine diphosphate ribose) in vivo. J Biol Chem 257, 6217-6223.
35. Rolli V, O'Farrell M, Ménissier-de Murcia J, &, De Murcia G, (1997) Random mutagenesis of the poly(ADP-ribose) polymerase catalytic domain reveals amino acids involved in polymer branching. Biochemistry 36, 12147-12154.
36. Alvarez-Gonzalez R, &, Althaus F, (1989) Poly(ADP-ribose) catabolism in mammalian cells exposed to DNA-damaging agents. Mutat Res/DNA Repair 218, 67-74.
37. 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, 6362-6364.
38. Oka S, Kato J, &, Moss J, (2006) Identification and characterization of a mammalian 39-kDa poly(ADP-ribose) glycohydrolase. J Biol Chem 281, 705-713.
39. 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, 516-523.
40. Williams JC, Chambers JP, &, Liehr JG, (1984) Glutamyl ribose 5-phosphate storage disease. A hereditary defect in the degradation of poly(ADP-ribosylated) proteins. J Biol Chem 259, 1037-1042.
41. Oka J, Ueda K, Hayaishi O, Komura H, &, Nakanishi K, (1984) ADP-ribosyl protein lyase, Purification, properties, and identification of the product. J Biol Chem 259, 986-995.
42. 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, 508-514.
43. Rosenthal F, Feijs KL, Frugier E, Bonalli M, Forst AH, Imhof R, Winkler HC, Fischer D, Caflisch A, Hassa PO, et al,. (2013) Macrodomain-containing proteins are new mono-ADP-ribosylhydrolases. Nat Struct Mol Biol 20, 502-507.
44. 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, 11839-11843.
45. 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, 5-11.
46. 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, 40974-40980.
47. Gagné J-P, Isabelle M, Lo KS, Bourassa S, Hendzel MJ, Dawson VL, Dawson TM, &, Poirier GG, (2008) Proteome-wide identification of poly(ADP-ribose) binding proteins and poly(ADP-ribose)-associated protein complexes. Nucleic Acids Res 36, 6959-6976.
48. Fahrer J, Kranaster R, Altmeyer M, Marx A, &, Bürkle A, (2007) Quantitative analysis of the binding affinity of poly(ADP-ribose) to specific binding proteins as a function of chain length. Nucleic Acids Res 35, e143.
49. Wang Y, Kim NS, Haince J-F, 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, ra20.
50. Malanga M, Czubaty A, Girstun A, Staron K, &, Althaus FR, (2008) Poly(ADP-ribose) binds to the splicing factor ASF/SF2 and regulates its phosphorylation by DNA topoisomerase I. J Biol Chem 283, 19991-19998.
51. 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, 3130-3139.
52. 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, e1002206.
53. Krietsch J, Rouleau M, Pic E, Ethier C, Dawson TM, Dawson VL, Masson JY, Poirier GG, &, Gagne JP, (2012) Reprogramming cellular events by poly(ADP-ribose)-binding proteins. Mol Aspects Med. doi: 10.1016/j.mam.2012.12. 005.
54. Pehrson JR, &, Fried VA, (1992) MacroH2A, a core histone containing a large nonhistone region. Science 257, 1398-1400.
55. Costanzi C, &, Pehrson JR, (1998) Histone macroH2A1 is concentrated in the inactive X chromosome of female mammals. Nature 393, 599-601.
56. Karras G, Kustatscher G, Buhecha H, Allen M, Pugieux C, Sait F, Bycroft M, &, Ladurner A, (2005) The macro domain is an ADP-ribose binding module. EMBO J 24, 1911-1920.
57. Allen MD, Buckle AM, Cordell SC, Lowe J, &, Bycroft M, (2003) The crystal structure of AF1521 a protein from Archaeoglobus fulgidus with homology to the non-histone domain of macroH2A. J Mol Biol 330, 503-511.
58. Ladurner AG, (2003) Inactivating chromosomes: a macro domain that minimizes transcription. Mol Cell 12, 1-3.
59. Chen D, Vollmar M, Rossi M, Phillips C, Kraehenbuehl R, Slade D, Mehrotra P, von Delft F, Crosthwaite S, Gileadi O, et al,. (2011) Identification of macrodomain proteins as novel O-acetyl-ADP-ribose deacetylases. J Biol Chem 286, 13261-13271.
60. Kustatscher G, Hothorn M, Pugieux C, Scheffzek K, &, Ladurner AG, (2005) Splicing regulates NAD metabolite binding to histone macroH2A. Nat Struct Mol Biol 12, 624-625.
61. Peterson F, Chen D, Lytle B, Rossi M, Ahel I, Denu J, &, Volkman B, (2011) Orphan macrodomain protein (human C6orf130) is an O-acyl-ADP-ribose deacylase: solution structure and catalytic properties. J Biol Chem 286, 35955-35965.
62. Timinszky G, Till S, Hassa P, Hothorn M, Kustatscher G, Nijmeijer B, Colombelli J, Altmeyer M, Stelzer E, Scheffzek K, et al,. (2009) A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nat Struct Mol Biol 16, 923-929.
63. Sporn JC, Kustatscher G, Hothorn T, Collado M, Serrano M, Muley T, Schnabel P, &, Ladurner AG, (2009) Histone macroH2A isoforms predict the risk of lung cancer recurrence. Oncogene 28, 3423-3428.
64. Buschbeck M, Uribesalgo I, Wibowo I, Rue P, Martin D, Gutierrez A, Morey L, Guigo R, Lopez-Schier H, &, Di Croce L, (2009) The histone variant macroH2A is an epigenetic regulator of key developmental genes. Nat Struct Mol Biol 16, 1074-1079.
65. Kapoor A, Goldberg MS, Cumberland LK, Ratnakumar K, Segura MF, Emanuel PO, Menendez S, Vardabasso C, Leroy G, Vidal CI, et al,. (2010) The histone variant macroH2A suppresses melanoma progression through regulation of CDK8. Nature 468, 1105-1109.
66. Creppe C, Janich P, Cantarino N, Noguera M, Valero V, Musulen E, Douet J, Posavec M, Martin-Caballero J, Sumoy L, et al,. (2012) MacroH2A1 regulates the balance between self-renewal and differentiation commitment in embryonic and adult stem cells. Mol Cell Biol 32, 1442-1452.
67. Egloff M-P, Malet H, Putics A, Heinonen M, Dutartre H, Frangeul A, Gruez A, Campanacci V, Cambillau C, Ziebuhr J, et al,. (2006) Structural and functional basis for ADP-ribose and poly(ADP-ribose) binding by viral macro domains. J Virol 80, 8493-8502.
68. Neuvonen M, &, Ahola T, (2009) Differential activities of cellular and viral macro domain proteins in binding of ADP-ribose metabolites. J Mol Biol 385, 212-225.
69. Malet H, Coutard B, Jamal S, Dutartre H, Papageorgiou N, Neuvonen M, Ahola T, Forrester N, Gould EA, Lafitte D, et al,. (2009) The crystal structures of Chikungunya and Venezuelan equine encephalitis virus nsP3 macro domains define a conserved adenosine binding pocket. J Virol 83, 6534-6545.
70. Atasheva S, Akhrymuk M, Frolova EI, &, Frolov I, (2012) New PARP gene with an anti-alphavirus function. J Virol 86, 8147-8160.
71. Martzen MR, McCraith SM, Spinelli SL, Torres FM, Fields S, Grayhack EJ, &, Phizicky EM, (1999) A biochemical genomics approach for identifying genes by the activity of their products. Science 286, 1153-1155.
72. 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, 81-85.
73. 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, 4620-4628.
74. Li G-Y, McCulloch RD, Fenton AL, Cheung M, Meng L, Ikura M, &, Koch CA, (2010) Structure and identification of ADP-ribose recognition motifs of APLF and role in the DNA damage response. Proc Natl Acad Sci USA 107, 9129-9134.
75. Eustermann S, Brockmann C, Mehrotra PV, Yang J-C, 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, 241-243.
76. 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, 39348-39358.
77. 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, 3793-3803.
78. Couto CA-M, Wang H-Y, Green JCA, Kiely R, Siddaway R, Borer C, Pears CJ, &, Lakin ND, (2011) PARP regulates nonhomologous end joining through retention of Ku at double-strand breaks. J Cell Biol 194, 367-375.
79. Grundy GJ, Rulten SL, Zeng Z, Arribas-Bosacoma R, Iles N, Manley K, Oliver A, &, Caldecott KW, (2013) APLF promotes the assembly and activity of non-homologous end joining protein complexes. EMBO J 32, 112-125.
80. Kashima L, Idogawa M, Mita H, Shitashige M, Yamada T, Ogi K, Suzuki H, Toyota M, Ariga H, Sasaki Y, et al,. (2012) CHFR protein regulates mitotic checkpoint by targeting PARP-1 protein for ubiquitination and degradation. J Biol Chem 287, 12975-12984.
81. Zweifel ME, Leahy DJ, &, Barrick D, (2005) Structure and notch receptor binding of the tandem WWE domain of deltex. Structure 13, 1599-1611.
82. Aravind L, (2001) The WWE domain: a common interaction module in protein ubiquitination and ADP ribosylation. Trends Biochem Sci 26, 273-275.
83. Zhang Y, Liu S, Mickanin C, Feng Y, Charlat O, Michaud GA, Schirle M, Shi X, Hild M, Bauer A, et al,. (2011) RNF146 is a poly(ADP-ribose)-directed E3 ligase that regulates axin degradation and Wnt signalling. Nat Cell Biol 13, 623-629.
84. Kang HC, Lee Y-I, Shin J-H, Andrabi SA, Chi Z, Gagné J-P, Lee Y, Ko HS, Lee BD, Poirier GG, et al,. (2011) Iduna is a poly(ADP-ribose) (PAR)-dependent E3 ubiquitin ligase that regulates DNA damage. Proc Natl Acad Sci USA 108, 14103-14108.
85. Andrabi SA, Kang HC, Haince J-F, Lee Y-I, Zhang J, Chi Z, West AB, Koehler RC, Poirier GG, Dawson TM, et al,. (2011) Iduna protects the brain from glutamate excitotoxicity and stroke by interfering with poly(ADP-ribose) polymer-induced cell death. Nat Med 17, 692-699.
86. 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, 235-240.
87. He F, Tsuda K, Takahashi M, Kuwasako K, Terada T, Shirouzu M, Watanabe S, Kigawa T, Kobayashi N, Güntert P, et al,. (2012) Structural insight into the interaction of ADP-ribose with the PARP WWE domains. FEBS Lett 586, 3858-3864.
88. Levaot N, Voytyuk O, Dimitriou I, Sircoulomb F, Chandrakumar A, Deckert M, Krzyzanowski Paul M, Scotter A, Gu S, Janmohamed S, et al,. (2011) Loss of tankyrase-mediated destruction of 3BP2 is the underlying pathogenic mechanism of cherubism. Cell 147, 1324-1339.
89. Lin W, Amé JC, Aboul-Ela N, Jacobson EL, &, Jacobson MK, (1997) Isolation and characterization of the cDNA encoding bovine poly(ADP-ribose) glycohydrolase. J Biol Chem 272, 11895-11901.
90. Hatakeyama K, Nemoto Y, Ueda K, &, Hayaishi O, (1986) Purification and characterization of poly(ADP-ribose) glycohydrolase. Different modes of action on large and small poly(ADP-ribose). J Biol Chem 261, 14902-14911.
91. Shimokawa T, Masutani M, Nagasawa S, Nozaki T, Ikota N, Aoki Y, Nakagama H, &, Sugimura T, (1999) Isolation and cloning of rat poly(ADP-ribose) glycohydrolase: presence of a potential nuclear export signal conserved in mammalian orthologs. J Biochem 126, 748-755.
92. Botta D, &, Jacobson M, (2010) Identification of a regulatory segment of poly(ADP-ribose) glycohydrolase. Biochemistry 49, 7674-7682.
93. Meyer R, Meyer-Ficca M, Whatcott C, Jacobson E, &, Jacobson M, (2007) Two small enzyme isoforms mediate mammalian mitochondrial poly(ADP-ribose) glycohydrolase (PARG) activity. Exp Cell Res 313, 2920-2936.
94. Meyer-Ficca M, Meyer R, Coyle D, Jacobson E, &, Jacobson M, (2004) Human poly(ADP-ribose) glycohydrolase is expressed in alternative splice variants yielding isoforms that localize to different cell compartments. Exp Cell Res 297, 521-532.
95. Niere M, Mashimo M, Agledal L, Dölle 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, 16088-16102.
96. Whatcott CJ, Meyer-Ficca ML, Meyer RG, &, Jacobson MK, (2009) A specific isoform of poly(ADP-ribose) glycohydrolase is targeted to the mitochondrial matrix by a N-terminal mitochondrial targeting sequence. Exp Cell Res 315, 3477-3485.
97. Kothe G, Kitamura M, Masutani M, Selker E, &, Inoue H, (2010) PARP is involved in replicative aging in Neurospora crassa. Fungal Genet Biol 47, 297-309.
98. Semighini C, Savoldi M, Goldman G, &, Harris S, (2006) Functional characterization of the putative Aspergillus nidulans poly(ADP-ribose) polymerase homolog PrpA. Genetics 173, 87-98.
99. Adams-Phillips L, Wan J, Tan X, Dunning M, Meyers B, Michelmore R, &, Bent A, (2008) Discovery of ADP-ribosylation and other plant defense pathway elements through expression profiling of four different Arabidopsis-Pseudomonas R-avr interactions, Molecular Plant-Microbe. Interactions 21, 646-657.
100. St-Laurent J-F, Gagnon S, Dequen F, Hardy I, &, Desnoyers S, (2007) Altered DNA damage response in Caenorhabditis elegans with impaired poly(ADP-ribose) glycohydrolases genes expression. DNA Repair (Amst) 6, 329-343.
101. Patel C, Koh D, Jacobson M, &, Oliveira M, (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.
102. Brochu G, Duchaine C, Thibeault L, Lagueux J, Shah GM, &, Poirier GG, (1994) Mode of action of poly(ADP-ribose) glycohydrolase. Biochim Biophys Acta 1219, 342-350.
103. Ikejima M, &, Gill DM, (1988) Poly(ADP-ribose) degradation by glycohydrolase starts with an endonucleolytic incision. J Biol Chem 263, 11037-11040.
104. Braun SA, Panzeter PL, Collinge MA, &, Althaus FR, (1994) Endoglycosidic cleavage of branched polymers by poly(ADP-ribose) glycohydrolase. Eur J Biochem 220, 369-375.
105. Dunstan M, Barkauskaite E, Lafite P, Knezevic C, Brassington A, Ahel M, Hergenrother P, Leys D, &, Ahel I, (2012) Structure and mechanism of a canonical poly(ADP-ribose) glycohydrolase. Nat Commun 3, 878.
106. Kim I-K, Kiefer J, Ho C, Stegeman R, Classen S, Tainer J, &, 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, 653-656.
107. Tucker J, Bennett N, Brassington C, Durant S, Hassall G, Holdgate G, McAlister M, Nissink W, Truman C, &, Watson M, (2012) Structures of the human poly (ADP-ribose) glycohydrolase catalytic domain confirm catalytic mechanism and explain inhibition by ADP-HPD derivatives. PLoS ONE 7, e50889.
108. Mortusewicz O, Fouquerel E, Amé J-C, Leonhardt H, &, Schreiber V, (2011) PARG is recruited to DNA damage sites through poly(ADP-ribose)- and PCNA-dependent mechanisms. Nucleic Acids Res 39, 5045-5056.
109. Koh D, Patel C, Ramsinghani S, Slama J, Oliveira M, &, Jacobson M, (2003) Identification of an inhibitor binding site of poly(ADP-ribose) glycohydrolase. Biochemistry 42, 4855-4863.
110. Tan E, Krukenberg K, &, Mitchison T, (2012) Large scale preparation and characterization of poly(ADP-ribose) and defined length polymers. Anal Biochem 428, 126-136.
111. Bryant H, Schultz N, Thomas H, Parker K, Flower D, Lopez E, Kyle S, Meuth M, Curtin N, &, Helleday T, (2005) Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 434, 913-917.
112. Farmer H, McCabe N, Lord C, Tutt A, Johnson D, Richardson T, Santarosa M, Dillon K, Hickson I, Knights C, et al,. (2005) Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434, 917-921.
113. Rouleau M, Patel A, Hendzel M, Kaufmann S, &, Poirier G, (2010) PARP inhibition: PARP1 and beyond. Nat Rev Cancer 10, 293-301.
114. Fisher A, Hochegger H, Takeda S, &, Caldecott K, (2007) Poly(ADP-ribose) polymerase 1 accelerates single-strand break repair in concert with poly(ADP-ribose) glycohydrolase. Mol Cell Biol 27, 5597-5605.
115. Feng X, &, Koh D, (2013) Inhibition of poly(ADP-ribose) polymerase-1 or poly(ADP-ribose) glycohydrolase individually, but not in combination, leads to improved chemotherapeutic efficacy in HeLa cells. Int J Oncol 42, 749-756.
116. Erdélyi K, Bai P, Kovács I, Szabõ E, Mocsár G, Kakuk A, Szabõ C, Gergely P, &, Virág L, (2009) Dual role of poly(ADP-ribose) glycohydrolase in the regulation of cell death in oxidatively stressed A549 cells. FASEB J 23, 3553-3563.
117. Keil C, Gröbe T, &, Oei SL, (2006) MNNG-induced cell death is controlled by interactions between PARP-1, poly(ADP-ribose) glycohydrolase, and XRCC1. J Biol Chem 281, 34394-34405.
118. Fathers C, Drayton R, Solovieva S, &, Bryant H, (2012) Inhibition of poly(ADP-ribose) glycohydrolase (PARG) specifically kills BRCA2-deficient tumor cells. Cell Cycle (Georgetown, Tex), 11, 990-997.
119. Koh D, Lawler A, Poitras M, Sasaki M, Wattler S, Nehls M, Stöger T, Poirier G, Dawson V, &, Dawson T, (2004) Failure to degrade poly(ADP-ribose) causes increased sensitivity to cytotoxicity and early embryonic lethality. Proc Natl Acad Sci USA 101, 17699-17704.
120. Cortes U, Tong W-M, Coyle D, Meyer-Ficca M, Meyer R, Petrilli V, Herceg Z, Jacobson E, Jacobson M, &, Wang Z-Q, (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, 7163-7178.
121. Cuzzocrea S, Di Paola R, Mazzon E, Cortes U, Genovese T, Muià C, Li W, Xu W, Li J-H, Zhang J, et al,. (2005) PARG activity mediates intestinal injury induced by splanchnic artery occlusion and reperfusion. FASEB J 19, 558-566.
122. Patel N, Cortes U, Di Poala R, Mazzon E, Mota-Filipe H, Cuzzocrea S, Wang Z-Q, &, Thiemermann C, (2005) Mice lacking the 110-kD isoform of poly(ADP-ribose) glycohydrolase are protected against renal ischemia/reperfusion injury. J Am Soc Nephrol 16, 712-719.
123. Bürkle A, &, Virág L, (2013) Poly(ADP-ribose): PARadigms and PARadoxes. Mol Aspects Med. doi: 10.1016/j.mam.2012.12.010.
124. Cozzi A, Cipriani G, Fossati S, Faraco G, Formentini L, Min W, Cortes U, Wang Z-Q, Moroni F, &, Chiarugi A, (2006) Poly(ADP-ribose) accumulation and enhancement of postischemic brain damage in 110-kDa poly(ADP-ribose) glycohydrolase null mice. J Cereb Blood Flow Metab 26, 684-695.
125. Slama JT, Aboul-Ela N, &, Jacobson MK, (1995) Mechanism of inhibition of poly(ADP-ribose) glycohydrolase by adenosine diphosphate (hydroxymethyl)pyrrolidinediol. J Med Chem 38, 4332-4336.
126. Finch K, Knezevic C, Nottbohm A, Partlow K, &, Hergenrother P, (2012) Selective small molecule inhibition of poly(ADP-ribose) glycohydrolase (PARG). ACS Chem Biol 7, 563-570.
127. Mueller-Dieckmann C, Kernstock S, Lisurek M, Von Kries JP, Haag F, Weiss M, &, 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 USA 103, 15026-15031.
128. Niere M, Kernstock S, Koch-Nolte F, &, Ziegler M, (2008) Functional localization of two poly(ADP-ribose)-degrading enzymes to the mitochondrial matrix. Mol Cell Biol 28, 814-824.
129. Ono T, Kasamatsu A, Oka S, &, Moss J, (2006) The 39-kDa poly(ADP-ribose) glycohydrolase ARH3 hydrolyzes O-acetyl-ADP-ribose, a product of the Sir2 family of acetyl-histone deacetylases. Proc Natl Acad Sci USA 103, 16687-16691.
130. Han WD, Zhao YL, Meng YG, Zang L, Wu ZQ, Li Q, Si YL, Huang K, Ba JM, Morinaga H, et al,. (2007) Estrogenically regulated LRP16 interacts with estrogen receptor alpha and enhances the receptor's transcriptional activity. Endocr Relat Cancer 14, 741-753.
131. Yang J, Zhao YL, Wu ZQ, Si YL, Meng YG, Fu XB, Mu YM, &, Han WD, (2009) The single-macro domain protein LRP16 is an essential cofactor of androgen receptor. Endocr Relat Cancer 16, 139-153.
132. Maas NM, Van de Putte T, Melotte C, Francis A, Schrander-Stumpel CT, Sanlaville D, Genevieve D, Lyonnet S, Dimitrov B, Devriendt K, et al,. (2007) The C20orf133 gene is disrupted in a patient with Kabuki syndrome. J Med Genet 44, 562-569.
133. Maas NM, Van de Putte T, Melotte C, Francis A, Schrander-Stumpel CT, Sanlaville D, Genevieve D, Lyonnet S, Dimitrov B, Devriendt K, et al,. (2009) The C20orf133 gene is disrupted in a patient with Kabuki syndrome. BMJ Case Rep, doi: 10.1136/bcr.06.2009.1994
134. Feijs KL, Kleine H, Braczynski A, Forst AH, Herzog N, Verheugd P, Linzen U, Kremmer E, &, Luscher B, (2013) ARTD10 substrate identification on protein microarrays: regulation of GSK3beta by mono-ADP-ribosylation. Cell Commun Signal 11, 5.
135. Andrabi SA, Kim NS, Yu SW, Wang H, Koh DW, Sasaki M, Klaus JA, Otsuka T, Zhang Z, Koehler RC, et al,. (2006) Poly(ADP-ribose) (PAR) polymer is a death signal. Proc Natl Acad Sci USA 103, 18308-18313.
136. Yu SW, Andrabi SA, Wang H, Kim NS, Poirier GG, Dawson TM, &, Dawson VL, (2006) Apoptosis-inducing factor mediates poly(ADP-ribose) (PAR) polymer-induced cell death. Proc Natl Acad Sci USA 103, 18314-18319.
137. Forst AH, Karlberg T, Herzog N, Thorsell AG, Gross A, Feijs KL, Verheugd P, Kursula P, Nijmeijer B, Kremmer E, et al,. (2013) Recognition of mono-ADP-ribosylated ARTD10 substrates by ARTD8 macrodomains. Structure 21, 462-475.