Survey and summary readers of poly(ADP-ribose): Designed to be fit for purpose

Nucleic Acids Research

Volumn 44, Issue 3, 2016, Pages 993-1006

  Teloni, Federico ^a   Altmeyer, Matthias ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

POLY(ADENOSINE DIPHOSPHATE RIBOSE); PROTEOME;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ARTICLE; CELL FUNCTION; CELL MATURATION; CELL METABOLISM; CHROMATIN; GENE SEQUENCE; GENETIC TRANSCRIPTION; GENOMIC INSTABILITY; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PROCESSING; METABOLISM; NEOPLASM;

HUMANS; NEOPLASMS; POLY ADENOSINE DIPHOSPHATE RIBOSE; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84964893893     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv1383     Document Type: Article

References (136)

1. Schreiber, V., Dantzer, F., Ame, J.C. and de Murcia, G. (2006) Poly(ADP-ribose): novel functions for an old molecule. Nat. Rev. Mol. Cell Biol., 7, 517-528.
2. Burkle, A. (2005) Poly(ADP-ribose). The most elaborate metabolite of NAD+. FEBS J., 272, 4576-4589.
3. Hassa, P.O. and Hottiger, M.O. (2008) The diverse biological roles of mammalian PARPS, a small but powerful family of poly-ADP-ribose polymerases. Front. Biosci., 13, 3046-3082.
4. Barkauskaite, E., Jankevicius, G., Ladurner, A.G., Ahel, I. and Timinszky, G. (2013) The recognition and removal of cellular poly(ADP-ribose) signals. FEBS J., 280, 3491-3507.
5. Chambon, P., Weill, J.D. and Mandel, P. (1963) Nicotinamide mononucleotide activation of new DNA-dependent polyadenylic acid synthesizing nuclear enzyme. Bioch. Biophys. Res. Commun., 11, 39-43.
6. Kraus, W.L. (2015) PARPs and ADP-Ribosylation: 50 Years . . . and Counting. Mol. Cell, 58, 902-910.
7. Bai, P. (2015) Biology of Poly(ADP-Ribose) Polymerases: The Factotums of Cell Maintenance. Mol. Cell, 58, 947-958.
8. Barkauskaite, E., Jankevicius, G. and Ahel, I. (2015) Structures and Mechanisms of Enzymes Employed in the Synthesis and Degradation of PARP-Dependent Protein ADP-Ribosylation. Mol. Cell, 58, 935-946.
9. Hottiger, M.O. (2015) Nuclear ADP-Ribosylation and Its Role in Chromatin Plasticity, Cell Differentiation, and Epigenetics. Annu. Rev. Biochem., 84, 227-263.
10. Hottiger, M.O., Hassa, P.O., Luscher, B., Schuler, H. and Koch-Nolte, F. (2010) Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem. Sci., 35, 208-219.
11. Bock, F.J., Todorova, T.T. and Chang, P. (2015) RNA Regulation by Poly(ADP-Ribose) Polymerases. Mol. Cell, 58, 959-969.
12. Smeenk, G. and van Attikum, H. (2013) The chromatin response to DNA breaks: leaving a mark on genome integrity. Annu. Rev. Biochem., 82, 55-80.
13. Gibson, B.A. and Kraus, W.L. (2012) New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat. Rev. Mol. Cell Biol., 13, 411-424.
14. Luo, X. and Kraus, W.L. (2012) On PAR with PARP: cellular stress signaling through poly(ADP-ribose) and PARP-1. Genes Dev., 26, 417-432.
15. Menissier de Murcia, J., Ricoul, M., Tartier, L., Niedergang, C., Huber, A., Dantzer, F., Schreiber, V., Ame, 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.
16. Beck, C., Robert, I., Reina-San-Martin, B., Schreiber, V. and Dantzer, F. (2014) Poly(ADP-ribose) polymerases in double-strand break repair: focus on PARP1, PARP2 and PARP3. Exp. Cell Res., 329, 18-25.
17. Boehler, C., Gauthier, L.R., Mortusewicz, O., Biard, D.S., Saliou, J.M., Bresson, A., Sanglier-Cianferani, S., Smith, S., Schreiber, V., Boussin, F. et al. (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, 2783-2788.
18. Altmeyer, M., Messner, S., Hassa, P.O., Fey, M. and Hottiger, M.O. (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.
19. Loseva, O., Jemth, A.S., Bryant, H.E., Schuler, H., Lehtio, L., Karlberg, T. and Helleday, T. (2010) PARP-3 is a mono-ADP-ribosylase that activates PARP-1 in the absence of DNA. J. Biol. Chem., 285, 8054-8060.
20. Rulten, S.L., Fisher, A.E., Robert, I., Zuma, M.C., Rouleau, M., Ju, L., Poirier, G., Reina-San-Martin, B. and Caldecott, K.W. (2011) PARP-3 and APLF function together to accelerate nonhomologous end-joining. Mol. Cell, 41, 33-45.
21. Vyas, S., Matic, I., Uchima, L., Rood, J., Zaja, R., Hay, R.T., Ahel, I. and Chang, P. (2014) Family-wide analysis of poly(ADP-ribose) polymerase activity. Nat. Commun., 5, 4426.
22. Smith, S., Giriat, I., Schmitt, A. and de Lange, T. (1998) Tankyrase, a poly(ADP-ribose) polymerase at human telomeres. Science, 282, 1484-1487.
23. Cook, B.D., Dynek, J.N., Chang, W., Shostak, G. and Smith, S. (2002) Role for the related poly(ADP-Ribose) polymerases tankyrase 1 and 2 at human telomeres. Mol. Cell. Biol., 22, 332-342.
24. Chang, P., Coughlin, M. and Mitchison, T.J. (2005) Tankyrase-1 polymerization of poly(ADP-ribose) is required for spindle structure and function. Nat. Cell Biol., 7, 1133-1139.
25. Kim, M.K., Dudognon, C. and Smith, S. (2012) Tankyrase 1 regulates centrosome function by controlling CPAP stability. EMBO Rep., 13, 724-732.
26. Ozaki, Y., Matsui, H., Asou, H., Nagamachi, A., Aki, D., Honda, H., Yasunaga, S., Takihara, Y., Yamamoto, T., Izumi, S. et al. (2012) Poly-ADP ribosylation of Miki by tankyrase-1 promotes centrosome maturation. Mol. Cell, 47, 694-706.
27. Cho-Park, P.F. and Steller, H. (2013) Proteasome regulation by ADP-ribosylation. Cell, 153, 614-627.
28. Huang, S.M., Mishina, Y.M., Liu, S., Cheung, A., Stegmeier, F., Michaud, G.A., Charlat, O., Wiellette, E., Zhang, Y., Wiessner, S. et al. (2009) Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature, 461, 614-620.
29. Zhang, Y., Liu, S., Mickanin, C., Feng, Y., Charlat, O., Michaud, G.A., 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.
30. Li, N., Zhang, Y., Han, X., Liang, K., Wang, J., Feng, L., Wang, W., Songyang, Z., Lin, C., Yang, L. et al. (2015) Poly-ADP ribosylation of PTEN by tankyrases promotes PTEN degradation and tumor growth. Genes Dev., 29, 157-170.
31. Wang, W., Li, N., Li, X., Tran, M.K., Han, X. and Chen, J. (2015) Tankyrase Inhibitors Target YAP by Stabilizing Angiomotin Family Proteins. Cell Rep., 13, 524-532.
32. Levaot, N., Voytyuk, O., Dimitriou, I., Sircoulomb, F., Chandrakumar, A., Deckert, M., Krzyzanowski, P.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.
33. Guettler, S., LaRose, J., Petsalaki, E., Gish, G., Scotter, A., Pawson, T., Rottapel, R. and Sicheri, F. (2011) Structural basis and sequence rules for substrate recognition by Tankyrase explain the basis for cherubism disease. Cell, 147, 1340-1354.
34. Pic, E., Gagne, J.P. and Poirier, G.G. (2011) Mass spectrometry-based functional proteomics of poly(ADP-ribose) polymerase-1. Exp. Rev. Proteomic., 8, 759-774.
35. Simbulan-Rosenthal, C.M., Rosenthal, D.S. and Smulson, M.E. (2011) Purification and characterization of poly(ADP-ribosyl)ated DNA replication/repair complexes. Methods Mol. Biol., 780, 165-190.
36. Matic, I., Ahel, I. and Hay, R.T. (2012) Reanalysis of phosphoproteomics data uncovers ADP-ribosylation sites. Nat. Methods, 9, 771-772.
37. Chapman, J.D., Gagne, J.P., Poirier, G.G. and Goodlett, D.R. (2013) Mapping PARP-1 auto-ADP-ribosylation sites by liquid chromatography-tandem mass spectrometry. J. Proteome Res., 12, 1868-1880.
38. Gagne, J.P., Ethier, C., Defoy, D., Bourassa, S., Langelier, M.F., Riccio, A.A., Pascal, J.M., Moon, K.M., Foster, L.J., Ning, Z. et al. (2015) Quantitative site-specific ADP-ribosylation profiling of DNA-dependent PARPs. DNA Repair, 30, 68-79.
39. Daniels, C.M., Ong, S.E. and Leung, A.K. (2014) Phosphoproteomic Approach to Characterize Protein Mono- And Poly(ADP-ribosyl)ation Sites from Cells. J. Proteome Res., 13, 3510-3522.
40. Daniels, C.M., Ong, S.E. and Leung, A.K. (2015) The Promise of Proteomics for the Study of ADP-Ribosylation. Mol. Cell, 58, 911-924.
41. Rosenthal, F. and Hottiger, M.O. (2014) Identification of ADP-ribosylated peptides and ADP-ribose acceptor sites. Front. Biosci., 19, 1041-1056.
42. Gagne, J.P., Isabelle, M., Lo, K.S., Bourassa, S., Hendzel, M.J., Dawson, V.L., Dawson, T.M. and Poirier, G.G. (2008) Proteome-wide identification of poly(ADP-ribose) binding proteins and poly(ADP-ribose)-associated protein complexes. Nucleic Acids Res., 36, 6959-6976.
43. Isabelle, M., Gagne, J.P., Gallouzi, I.E. and Poirier, G.G. (2012) Quantitative proteomics and dynamic imaging reveal that G3BP-mediated stress granule assembly is poly(ADP-ribose)-dependent following exposure to MNNG-induced DNA alkylation. J. Cell Sci., 125, 4555-4566.
44. Jungmichel, S., Rosenthal, F., Altmeyer, M., Lukas, J., Hottiger, M.O. and Nielsen, M.L. (2013) Proteome-wide identification of poly(ADP-Ribosyl)ation targets in different genotoxic stress responses. Mol. Cell, 52, 272-285.
45. Zhang, Y., Wang, J., Ding, M. and Yu, Y. (2013) Site-specific characterization of the Asp- And Glu-ADP-ribosylated proteome. Nat. Methods, 10, 981-984.
46. Psakhye, I. and Jentsch, S. (2012) Protein group modification and synergy in the SUMO pathway as exemplified in DNA repair. Cell, 151, 807-820.
47. Krietsch, J., Rouleau, M., Pic, E., Ethier, C., Dawson, T.M., Dawson, V.L., Masson, J.Y., Poirier, G.G. and Gagne, J.P. (2013) Reprogramming cellular events by poly(ADP-ribose)-binding proteins. Mol. Aspects Med., 34, 1066-1087.
48. Gagne, J.P., Haince, J.F., Pic, E. and Poirier, G.G. (2011) Affinity-based assays for the identification and quantitative evaluation of noncovalent poly(ADP-ribose)-binding proteins. Methods Mol. Biol., 780, 93-115.
49. Malanga, M. and Althaus, F.R. (2011) Noncovalent protein interaction with poly(ADP-ribose). Methods Mol. Biol., 780, 67-82.
50. Kalisch, T., Ame, J.C., Dantzer, F. and Schreiber, V. (2012) New readers and interpretations of poly(ADP-ribosyl)ation. Trends Biochem. Sci., 37, 381-390.
51. Pleschke, J.M., Kleczkowska, H.E., Strohm, M. and Althaus, F.R. (2000) Poly(ADP-ribose) binds to specific domains in DNA damage checkpoint proteins. J. Biol. Chem., 275, 40974-40980.
52. Fahrer, J., Kranaster, R., Altmeyer, M., Marx, A. and Burkle, 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.
53. Fahrer, J., Popp, O., Malanga, M., Beneke, S., Markovitz, D.M., Ferrando-May, E., Burkle, A. and Kappes, F. (2010) High-affinity interaction of poly(ADP-ribose) and the human DEK oncoprotein depends upon chain length. Biochemistry, 49, 7119-7130.
54. Popp, O., Veith, S., Fahrer, J., Bohr, V.A., Burkle, A. and Mangerich, A. (2013) Site-specific noncovalent interaction of the biopolymer poly(ADP-ribose) with the Werner syndrome protein regulates protein functions. ACS Chem. Biol., 8, 179-188.
55. Fischer, J.M., Popp, O., Gebhard, D., Veith, S., Fischbach, A., Beneke, S., Leitenstorfer, A., Bergemann, J., Scheffner, M., Ferrando-May, E. et al. (2014) Poly(ADP-ribose)-mediated interplay of XPA and PARP1 leads to reciprocal regulation of protein function. FEBS J., 281, 3625-3641.
56. Ahel, I., Ahel, D., Matsusaka, T., Clark, A.J., Pines, J., Boulton, S.J., andWest, S.C. (2008) Poly(ADP-ribose)-binding zinc finger motifs in DNA repair/checkpoint proteins. Nature, 451, 81-85.
57. Isogai, S., Kanno, S., Ariyoshi, M., Tochio, H., Ito, Y., Yasui, A. and Shirakawa, M. (2010) Solution structure of a zinc-finger domain that binds to poly-ADP-ribose. Genes Cells, 15, 101-110.
58. Oberoi, J., Richards, M.W., Crumpler, S., Brown, N., Blagg, J. and 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.
59. Eustermann, S., Brockmann, C., Mehrotra, P.V., Yang, J.C., Loakes, D., West, S.C., Ahel, I. and 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.
60. Li, G.Y., McCulloch, R.D., Fenton, A.L., Cheung, M., Meng, L., Ikura, M. and Koch, C.A. (2010) Structure and identification of ADP-ribose recognition motifs of APLF and role in the DNA damage response. Proc. Natl. Acad. Sci. U.S.A., 107, 9129-9134.
61. Rulten, S.L., Cortes-Ledesma, F., Guo, L., Iles, N.J. and Caldecott, K.W. (2008) APLF (C2orf13) is a novel component of poly(ADP-ribose) signaling in mammalian cells. Mol. Cell. Biol., 28, 4620-4628.
62. Min, W., Bruhn, C., Grigaravicius, P., Zhou, Z.W., Li, F., Kruger, A., Siddeek, B., Greulich, K.O., Popp, O., Meisezahl, C. et al. (2013) Poly(ADP-ribose) binding to Chk1 at stalled replication forks is required for S-phase checkpoint activation. Nat. Commun., 4, 2993.
63. Ahel, D., Horejsi, Z., Wiechens, N., Polo, S.E., Garcia-Wilson, E., Ahel, I., Flynn, H., Skehel, M., West, S.C., Jackson, S.P. et al. (2009) Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science, 325, 1240-1243.
64. Gottschalk, A.J., Timinszky, G., Kong, S.E., Jin, J., Cai, Y., Swanson, S.K., Washburn, M.P., Florens, L., Ladurner, A.G., Conaway, J.W. et al. (2009) Poly(ADP-ribosyl)ation directs recruitment and activation of an ATP-dependent chromatin remodeler. Proc. Natl. Acad. Sci. U.S.A., 106, 13770-13774.
65. Timinszky, G., Till, S., Hassa, P.O., Hothorn, M., Kustatscher, G., Nijmeijer, B., Colombelli, J., Altmeyer, M., Stelzer, E.H., Scheffzek, K. et al. (2009) A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nat. Struct. Mol. Biol., 16, 923-929.
66. Aguiar, R.C., Takeyama, K., He, C., Kreinbrink, K. and Shipp, M.A. (2005) B-aggressive lymphoma family proteins have unique domains that modulate transcription and exhibit poly(ADP-ribose) polymerase activity. J. Biol. Chem., 280, 33756-33765.
67. Wang, Z., Michaud, G.A., Cheng, Z., Zhang, Y., Hinds, T.R., Fan, E., Cong, F. and 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.
68. Kang, H.C., Lee, Y.I., Shin, J.H., Andrabi, S.A., Chi, Z., Gagne, J.P., Lee, Y., Ko, H.S., Lee, B.D., Poirier, G.G. et al. (2011) Iduna is a poly(ADP-ribose) (PAR)-dependent E3 ubiquitin ligase that regulates DNA damage. Proc. Natl. Acad. Sci. U.S.A., 108, 14103-14108.
69. Perry, J.J., Tainer, J.A. and Boddy, M.N. (2008) A SIM-ultaneous role for SUMO and ubiquitin. Trends Biochem. Sci., 33, 201-208.
70. DaRosa, P.A., Wang, Z., Jiang, X., Pruneda, J.N., Cong, F., Klevit, R.E. and Xu, W. (2015) Allosteric activation of the RNF146 ubiquitin ligase by a poly(ADP-ribosyl)ation signal. Nature, 517, 223-226.
71. Khoronenkova, S.V. and Dianov, G.L. (2011) The emerging role of Mule and ARF in the regulation of base excision repair. FEBS Lett., 585, 2831-2835.
72. Gudjonsson, T., Altmeyer, M., Savic, V., Toledo, L., Dinant, C., Grofte, M., Bartkova, J., Poulsen, M., Oka, Y., Bekker-Jensen, S. et al. (2012) TRIP12 and UBR5 suppress spreading of chromatin ubiquitylation at damaged chromosomes. Cell, 150, 697-709.
73. Reinhardt, H.C. and Yaffe, M.B. (2013) Phospho-Ser/Thr-binding domains: navigating the cell cycle and DNA damage response. Nat. Rev. Mol. Cell Biol., 14, 563-580.
74. Breslin, C., Hornyak, P., Ridley, A., Rulten, S.L., Hanzlikova, H., Oliver, A.W. and Caldecott, K.W. (2015) The XRCC1 phosphate-binding pocket binds poly (ADP-ribose) and is required for XRCC1 function. Nucleic Acids Res., 43, 6934-6944.
75. Li, M., Lu, L.Y., Yang, C.Y., Wang, S. and Yu, X. (2013) The FHA and BRCT domains recognize ADP-ribosylation during DNA damage response. Genes Dev., 27, 1752-1768.
76. Li, M. and Yu, X. (2013) Function of BRCA1 in the DNA damage response is mediated by ADP-ribosylation. Cancer Cell, 23, 693-704.
77. Gagne, J.P., Hunter, J.M., Labrecque, B., Chabot, B. and Poirier, G.G. (2003) A proteomic approach to the identification of heterogeneous nuclear ribonucleoproteins as a new family of poly(ADP-ribose)-binding proteins. Biochem. J., 371, 331-340.
78. Ji, Y. and Tulin, A.V. (2009) Poly(ADP-ribosyl)ation of heterogeneous nuclear ribonucleoproteins modulates splicing. Nucleic Acids Res., 37, 3501-3513.
79. Krietsch, J., Caron, M.C., Gagne, J.P., Ethier, C., Vignard, J., Vincent, M., Rouleau, M., Hendzel, M.J., Poirier, G.G. and Masson, J.Y. (2012) PARP activation regulates the RNA-binding protein NONO in the DNA damage response to DNA double-strand breaks. Nucleic Acids Res., 40, 10287-10301.
80. Adamson, B., Smogorzewska, A., Sigoillot, F.D., King, R.W. and Elledge, S.J. (2012) A genome-wide homologous recombination screen identifies the RNA-binding protein RBMX as a component of the DNA-damage response. Nat. Cell Biol., 14, 318-328.
81. Izhar, L., Adamson, B., Ciccia, A., Lewis, J., Pontano-Vaites, L., Leng, Y., Liang, A.C., Westbrook, T.F., Harper, J.W. and Elledge, S.J. (2015) A systematic analysis of factors localized to damaged chromatin reveals parp-dependent recruitment of transcription factors. Cell Rep., 11, 1486-1500.
82. Malanga, M., Czubaty, A., Girstun, A., Staron, K. and Althaus, F.R. (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.
83. Murawska, M., Hassler, M., Renkawitz-Pohl, R., Ladurner, A. and Brehm, A. (2011) Stress-induced PARP activation mediates recruitment of Drosophila Mi-2 to promote heat shock gene expression. PLoS Genet., 7, e1002206.
84. Zhang, F., Chen, Y., Li, M. and Yu, X. (2014) The oligonucleotide/oligosaccharide-binding fold motif is a poly(ADP-ribose)-binding domain that mediates DNA damage response. Proc. Natl. Acad. Sci. U.S.A., 111, 7278-7283.
85. Zhang, F., Shi, J., Bian, C. and Yu, X. (2015) Poly(ADP-Ribose) Mediates the BRCA2-Dependent Early DNA Damage Response. Cell Rep., 13, 678-689.
86. Zhang, F., Shi, J., Chen, S.H., Bian, C. and Yu, X. (2015) The PIN domain of EXO1 recognizes poly(ADP-ribose) in DNA damage response. Nucleic Acids Res., doi:10.1093/nar/gkv939.
87. Thandapani, P., O'Connor, T.R., Bailey, T.L. and Richard, S. (2013) Defining the RGG/RG motif. Mol. Cell, 50, 613-623.
88. Haince, J.F., McDonald, D., Rodrigue, A., Dery, U., Masson, J.Y., Hendzel, M.J. and Poirier, G.G. (2008) PARP1-dependent kinetics of recruitment of MRE11 and NBS1 proteins to multiple DNA damage sites. J. Biol. Chem., 283, 1197-1208.
89. Altmeyer, M., Toledo, L., Gudjonsson, T., Grofte, M., Rask, M.B., Lukas, C., Akimov, V., Blagoev, B., Bartek, J. and Lukas, J. (2013) The chromatin scaffold protein SAFB1 renders chromatin permissive for DNA damage signaling. Mol. Cell, 52, 206-220.
90. Mastrocola, A.S., Kim, S.H., Trinh, A.T., Rodenkirch, L.A. and Tibbetts, R.S. (2013) The RNA-binding protein fused in sarcoma (FUS) functions downstream of poly(ADP-ribose) polymerase (PARP) in response to DNA damage. J. Biol. Chem., 288, 24731-24741.
91. Rulten, S.L., Rotheray, A., Green, R.L., Grundy, G.J., Moore, D.A., Gomez-Herreros, F., Hafezparast, M. and Caldecott, K.W. (2014) PARP-1 dependent recruitment of the amyotrophic lateral sclerosis-associated protein FUS/TLS to sites of oxidative DNA damage. Nucleic Acids Res., 42, 307-314.
92. Polo, S.E., Blackford, A.N., Chapman, J.R., Baskcomb, L., Gravel, S., Rusch, A., Thomas, A., Blundred, R., Smith, P., Kzhyshkowska, J. et al. (2012) Regulation of DNA-end resection by hnRNPU-like proteins promotes DNA double-strand break signaling and repair. Mol. Cell, 45, 505-516.
93. Hong, Z., Jiang, J., Ma, J., Dai, S., Xu, T., Li, H. and Yasui, A. (2013) The role of hnRPUL1 involved in DNA damage response is related to PARP1. PLoS One, 8, e60208.
94. Britton, S., Dernoncourt, E., Delteil, C., Froment, C., Schiltz, O., Salles, B., Frit, P. and Calsou, P. (2014) DNA damage triggers SAF-A and RNA biogenesis factors exclusion from chromatin coupled to R-loops removal. Nucleic Acids Res., 42, 9047-9062.
95. Altmeyer, M., Neelsen, K.J., Teloni, F., Pozdnyakova, I., Pellegrino, S., Grofte, M., Rask, M.B., Streicher, W., Jungmichel, S., Nielsen, M.L. et al. (2015) Liquid demixing of intrinsically disordered proteins is seeded by poly(ADP-ribose). Nat. Commun., 6, 8088.
96. Kato, M., Han, T.W., Xie, S., Shi, K., Du, X., Wu, L.C., Mirzaei, H., Goldsmith, E.J., Longgood, J., Pei, J. et al. (2012) Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell, 149, 753-767.
97. Han, T.W., Kato, M., Xie, S., Wu, L.C., Mirzaei, H., Pei, J., Chen, M., Xie, Y., Allen, J., Xiao, G. et al. (2012) Cell-free formation of RNA granules: bound RNAs identify features and components of cellular assemblies. Cell, 149, 768-779.
98. Hyman, A.A. and Simons, K. (2012) Cell biology. Beyond oil and water-phase transitions in cells. Science, 337, 1047-1049.
99. Hyman, A.A., Weber, C.A. and Julicher, F. (2014) Liquid-liquid phase separation in biology. Annu. Rev. Cell Dev. Biol., 30, 39-58.
100. Patel, A., Lee, H.O., Jawerth, L., Maharana, S., Jahnel, M., Hein, M.Y., Stoynov, S., Mahamid, J., Saha, S., Franzmann, T.M. et al. (2015) A Liquid-to-Solid Phase Transition of the ALS Protein FUS Accelerated by Disease Mutation. Cell, 162, 1066-1077.
101. Leung, A.K., Vyas, S., Rood, J.E., Bhutkar, A., Sharp, P.A. and Chang, P. (2011) Poly(ADP-ribose) regulates stress responses and microRNA activity in the cytoplasm. Mol. Cell, 42, 489-499.
102. Boamah, E.K., Kotova, E., Garabedian, M., Jarnik, M. and Tulin, A.V. (2012) Poly(ADP-Ribose) polymerase 1 (PARP-1) regulates ribosomal biogenesis in Drosophila nucleoli. PLoS Genet., 8, e1002442.
103. Guetg, C., Scheifele, F., Rosenthal, F., Hottiger, M.O. and Santoro, R. (2012) Inheritance of silent rDNA chromatin is mediated by PARP1 via noncoding RNA. Mol. Cell, 45, 790-800.
104. Kotova, E., Jarnik, M. and Tulin, A.V. (2009) Poly (ADP-ribose) polymerase 1 is required for protein localization to Cajal body. PLoS Genet., 5, e1000387.
105. Ji, Y. and Tulin, A.V. (2013) Post-transcriptional regulation by poly(ADP-ribosyl)ation of the RNA-binding proteins. Int. J. Mol. Sci., 14, 16168-16183.
106. Kraus, W.L. and Hottiger, M.O. (2013) PARP-1 and gene regulation: progress and puzzles. Mol. Aaspects Med., 34, 1109-1123.
107. Kwon, I., Kato, M., Xiang, S., Wu, L., Theodoropoulos, P., Mirzaei, H., Han, T., Xie, S., Corden, J.L. and McKnight, S.L. (2013) Phosphorylation-regulated binding of RNA polymerase II to fibrous polymers of low-complexity domains. Cell, 155, 1049-1060.
108. Andrabi, S.A., Umanah, G.K., Chang, C., Stevens, D.A., Karuppagounder, S.S., Gagne, J.P., Poirier, G.G., Dawson, V.L. and Dawson, T.M. (2014) Poly(ADP-ribose) polymerase-dependent energy depletion occurs through inhibition of glycolysis. Proc. Natl. Acad. Sci. U.S.A., 111, 10209-10214.
109. Fouquerel, E., Goellner, E.M., Yu, Z., Gagne, J.P., Barbi de Moura, M., Feinstein, T., Wheeler, D., Redpath, P., Li, J., Romero, G. et al. (2014) ARTD1/PARP1 negatively regulates glycolysis by inhibiting hexokinase 1 independent of NAD+ depletion. Cell Rep., 8, 1819-1831.
110. Wang, Z., Gagne, J.P., Poirier, G.G. and Xu, W. (2014) Crystallographic and biochemical analysis of the mouse poly(ADP-ribose) glycohydrolase. PLoS One, 9, e86010.
111. Slade, D., Dunstan, M.S., Barkauskaite, E., Weston, R., Lafite, P., Dixon, N., Ahel, M., Leys, D. and Ahel, I. (2011) The structure and catalytic mechanism of a poly(ADP-ribose) glycohydrolase. Nature, 477, 616-620.
112. Dunstan, M.S., Barkauskaite, E., Lafite, P., Knezevic, C.E., Brassington, A., Ahel, M., Hergenrother, P.J., Leys, D. and Ahel, I. (2012) Structure and mechanism of a canonical poly(ADP-ribose) glycohydrolase. Nat. Commun., 3, 878.
113. Lambrecht, M.J., Brichacek, M., Barkauskaite, E., Ariza, A., Ahel, I. and Hergenrother, P.J. (2015) Synthesis of dimeric ADP-ribose and its structure with human poly(ADP-ribose) glycohydrolase. J. Am. Chem. Soc., 137, 3558-3564.
114. Jankevicius, G., Hassler, M., Golia, B., Rybin, V., Zacharias, M., Timinszky, G. and Ladurner, A.G. (2013) A family of macrodomain proteins reverses cellular mono-ADP-ribosylation. Nat. Struct. Mol. Biol., 20, 508-514.
115. Rosenthal, F., Feijs, K.L., Frugier, E., Bonalli, M., Forst, A.H., Imhof, R., Winkler, H.C., Fischer, D., Caflisch, A., Hassa, P.O. et al. (2013) Macrodomain-containing proteins are new mono-ADP-ribosylhydrolases. Nat. Struct. Mol. Biol., 20, 502-507.
116. Sharifi, R., Morra, R., Appel, C.D., Tallis, M., Chioza, B., Jankevicius, G., Simpson, M.A., 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.
117. Mashimo, M., Kato, J. and Moss, J. (2013) ADP-ribosyl-acceptor hydrolase 3 regulates poly (ADP-ribose) degradation and cell death during oxidative stress. Proc. Natl. Acad. Sci. U.S.A., 110, 18964-18969.
118. Palazzo, L., Thomas, B., Jemth, A.S., Colby, T., Leidecker, O., Feijs, K.L., Zaja, R., Loseva, O., Puigvert, J.C., Matic, I. et al. (2015) Processing of protein ADP-ribosylation by Nudix hydrolases. Biochem. J., 468, 293-301.
119. Bryant, H.E., Schultz, N., Thomas, H.D., Parker, K.M., Flower, D., Lopez, E., Kyle, S., Meuth, M., Curtin, N.J. and Helleday, T. (2005) Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature, 434, 913-917.
120. Farmer, H., McCabe, N., Lord, C.J., Tutt, A.N., Johnson, D.A., Richardson, T.B., Santarosa, M., Dillon, K.J., Hickson, I., Knights, C. et al. (2005) Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature, 434, 917-921.
121. Lord, C.J. and Ashworth, A. (2013) Mechanisms of resistance to therapies targeting BRCA-mutant cancers. Nat. Med., 19, 1381-1388.
122. Feng, F.Y., de Bono, J.S., Rubin, M.A. and Knudsen, K.E. (2015) Chromatin to Clinic: The Molecular Rationale for PARP1 Inhibitor Function. Mol. Cell, 58, 925-934.
123. Curtin, N.J. and Szabo, C. (2013) Therapeutic applications of PARP inhibitors: Anticancer therapy and beyond. Mol. Aspects Med., 34, 1217-1256.
124. Hottiger, M.O. (2015) Poly(ADP-ribose) polymerase inhibitor therapeutic effect: Are we just scratching the surface? Expert Opin. Ther. Targets, 19, 1149-1152.
125. Haikarainen, T., Krauss, S. and Lehtio, L. (2014) Tankyrases: structure, function and therapeutic implications in cancer. Curr. Pharm. Des., 20, 6472-6488.
126. Riffell, J.L., Lord, C.J. and Ashworth, A. (2012) Tankyrase-targeted therapeutics: Expanding opportunities in the PARP family. Nat. Rev. Drug Disc., 11, 923-936.
127. Vyas, S. and Chang, P. (2014) New PARP targets for cancer therapy. Nat. Rev. Cancer, 14, 502-509.
128. Steffen, J.D., Coyle, D.L., Damodaran, K., Beroza, P. and Jacobson, M.K. (2011) Discovery and structure-activity relationships of modified salicylanilides as cell permeable inhibitors of poly(ADP-ribose) glycohydrolase (PARG). J. Med. Chem., 54, 5403-5413.
129. Finch, K.E., Knezevic, C.E., Nottbohm, A.C., Partlow, K.C. and Hergenrother, P.J. (2012) Selective small molecule inhibition of poly(ADP-ribose) glycohydrolase (PARG). ACS Chem. Biol., 7, 563-570.
130. Illuzzi, G., Fouquerel, E., Ame, J.C., Noll, A., Rehmet, K., Nasheuer, H.P., Dantzer, F. and Schreiber, V. (2014) PARG is dispensable for recovery from transient replicative stress but required to prevent detrimental accumulation of poly(ADP-ribose) upon prolonged replicative stress. Nucleic Acids Res., 42, 7776-7792.
131. Filippakopoulos, P., Qi, J., Picaud, S., Shen, Y., Smith, W.B., Fedorov, O., Morse, E.M., Keates, T., Hickman, T.T., Felletar, I. et al. (2010) Selective inhibition of BET bromodomains. Nature, 468, 1067-1073.
132. Cozzi, A., Cipriani, G., Fossati, S., Faraco, G., Formentini, L., Min, W., Cortes, U., Wang, Z.Q., Moroni, F. and 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.
133. Hanai, S., Kanai, M., Ohashi, S., Okamoto, K., Yamada, M., Takahashi, H. and Miwa, M. (2004) Loss of poly(ADP-ribose) glycohydrolase causes progressive neurodegeneration in Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A., 101, 82-86.
134. Abeti, R. and Duchen, M.R. (2012) Activation of PARP by oxidative stress induced by beta-amyloid: implications for Alzheimer's disease. Neurochem. Res., 37, 2589-2596.
135. Jankowsky, E. and Harris, M.E. (2015) Specificity and nonspecificity in RNA-protein interactions. Nat. Rev. Mol. Cell Biol., 16, 533-544.
136. Dundr, M. and Misteli, T. (2010) Biogenesis of nuclear bodies. Cold Spring Harb. Perspect. Biol., 2, a000711.