The PARP family: insights into functional aspects of poly (ADP-ribose) polymerase-1 in cell growth and survival

Cell Proliferation

Volumn 49, Issue 4, 2016, Pages 421-437

  Jubin, T ^a   Kadam, A ^a   Jariwala, M ^a   Bhatt, S ^a   Sutariya, S ^a   Gani, A R ^a   Gautam, S ^b   Begum, R ^a  

^a M S UNIVERSITY OF BARODA   (India)

^b BHABHA ATOMIC RESEARCH CENTRE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1;

CELL DEATH; CELL DIFFERENTIATION; CELL GROWTH; CELL STRUCTURE; CELL SURVIVAL; DNA DAMAGE; DNA REPAIR; DNA STRUCTURE; EMBRYO DEVELOPMENT; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; EPIGENETICS; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; METABOLIC REGULATION; NONHUMAN; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SPERMATOGENESIS;

EID: 84978872873     PISSN: 09607722     EISSN: 13652184     Source Type: Journal    
DOI: 10.1111/cpr.12268     Document Type: Review

References (188)

1. D'Amours D, Desnoyers S, D'Silva I, Poirier GG. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem J. 1999;342:249–268.
2. Schreiber V, Dantzer F, Ame JC, de Murcia G. Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol. 2006;7:517–528.
3. Lautier D, Lagueaux J, Thibodeau J, Ménard L, Poirier GG. Molecular and biochemical features of poly (ADP-ribose) metabolism. Mol Cell Biochem. 1993;122:171–193.
4. Meyer-Ficca ML, Meyer RG, Coyle DL, Jacobson EL, Jacobson MK. Human poly(ADP-ribose) glycohydrolase is expressed in alternative splice variants yielding isoforms that localize to different cell compartments. Exp Cell Res. 2004;297:521–532.
5. Min W, Wang ZQ. Poly (ADP-ribose) glycohydrolase (PARG) and its therapeutic potential. Front Biosci (Landmark Ed). 2009;14:1619–1626.
6. Oka S, Kato J, Moss J. Identification and Characterization of a Mammalian 39-kDa Poly(ADP-ribose) Glycohydrolase. JBC. 2006;281:705–713.
7. Dunn CA, O'Handley SF, Frick DN, Bessman MJ. Studies on the ADP-ribose pyrophosphatase subfamily of the nudix hydrolases and tentative identification of trgB, a gene associated with tellurite resistance. J Biol Chem. 1999;274:32318–32324.
8. Rosenthal F, Feijs KLH, Frugier E, et al. Macrodomain-containing proteins are new mono-ADP-ribosylhydrolases. Nat Struct Mol. 2013;20:502–509.
9. Ame JC, Spenlehauer C, de Murcia G. The PARP superfamily. BioEssays. 2004;26:882–893.
10. Hottiger MO, Hassa PO, Luscher B, Schuler H, Koch-Nolte F. Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem Sci. 2010;35:208–219.
11. Morales J, Li L, Fattah FJ, et al. Review of poly(ADP-Ribose) polymerase (PARP) mechanisms of action and rationale for targeting in cancer and other diseases. Crit Rev Eukaryot Gene Expr. 2014;24:15–28.
12. Loseva O, Jemth AS, Bryant HE, et al. PARP-3 is a mono-ADP-ribosylase that activates PARP-1 in the absence of DNA. J Biol Chem. 2010;285:8054–8060.
13. Hassa PO, Haenni SS, Elser M, Hottiger MO. Nuclear ADP-ribosylation reactions in mammalian cells: where are we today and where are we going? Microbiol Mol Biol Rev. 2006;70:789–829.
14. Kickhoefer VA, Siva AC, Kedersha NL, et al. The 193-kD vault protein, VPARP, is a novel poly(ADP-ribose) polymerase. J Cell Biol. 1999;146:917–928.
15. Smith S, Giriat I, Schmitt A, de Lange T. Tankyrase, a poly(ADP-ribose) polymerase at human telomeres. Science. 1998;282:1484–1487.
16. Seimiya H. The telomeric PARP, tankyrases, as targets for cancer therapy. Br J Cancer. 2006;94:341–345.
17. Leung AK, Vyas S, Rood JE, Bhutkar A, Sharp PA, Chang P. Poly(ADP-Ribose) Regulates Stress Responses and MicroRNA Activity in the Cytoplasm. Mol Cell. 2011;42:489–499.
18. Ma Q, Baldwin KT, Renzelli AJ, McDaniel A, Dong L. TCDD-inducible poly(ADP-ribose) polymerase: a novel response to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Biochem Biophys Res Commun. 2001;289:499–506.
19. Vyas S, Chesarone-Cataldo M, Todorova T, Huang YH, Chang P. A systematic analysis of the PARP protein family identifies new functions critical for cell physiology. Nat Commun. 2013;4:2240.
20. Barkauskaite E, Jankevicius G, Ladurner AG, Ahel I, Timinszky G. The recognition and removal of cellular poly(ADP-ribose) signals. FEBS J. 2013;280:3491–3507.
21. Slade D, Dunstan MS, Barkauskaite E, et al. The structure and catalytic mechanism of a poly(ADP-ribose) glycohydrolase. Nature. 2011;477:616–620.
22. Perina D, Mikoč A, Ahel J, Ćetković H, Žaja R, Ahel I. Distribution of protein poly(ADP-ribosyl)ation systems across all domains of life. DNA Repair. 2014;23:4–16.
23. Faraone-Mennella MR, Gambacorta A, Nicolaus B, Farina B. Purification and biochemical characterization of a poly(ADP-ribose) polymerase-like enzyme from the thermophilic archaeon Sulfolobus solfataricus. Biochem J. 1998;335:441–447.
24. Otto H, Reche PA, Bazan F, Dittmar K, Haag F, Koch-Nolte F. In silico characterization of the family of PARP-like poly(ADP-ribosyl) transferases (pARTs). BMC Genom. 2005;6:139.
25. Li Z, Yamauchi Y, Kamakura M, et al. Herpes simplex virus requires poly(ADP-ribose) polymerase activity for efficient replication and induces extracellular signal-related kinase-dependent phosphorylation and ICP0-dependent nuclear localization of tankyrase 1. J Virol. 2012;86:492–503.
26. Mattiussi S, Tempera I, Matusali G, Mearini G, Lenti L, Fratarcangeli S. Inhibition of poly(ADP-ribose)polymerase impairs Epstein Barr Virus lytic cycle progression. Infect Agent Cancer. 2007;2:18.
27. Ogura T, Takenouchi N, Yamaguchi M, Matsukage A, Sugimura T, Esumi H. Striking similarity of the distribution patterns of the poly(ADP-ribose) polymerase and DNA polymerase beta among various mouse organs. Biochem Biophys Res Commun. 1990;172:377–384.
28. Babiychuk E, Cottrill PB, Storozhenko S, Fuangthong M, Chen Y, O'Farrell MK. Higher plants possess two structurally different poly(ADP-ribose) polymerases. Plant J. 1998;15:635–645.
29. Citarelli M, Teotia S, Lamb RS. Evolutionary history of the poly(ADP-ribose) polymerase gene family in eukaryotes. BMC Evol Biol. 2010;10:308.
30. Kawal AM, Mir H, Ramniklal CK, Rajawat J, Begum R. Structural and evolutionary analysis of PARPs in D. discoideum. Am J Infect Dis. 2011;7:67–74.
31. Kameshita I, Matsuda Z, Taniguchi T, Shizuta Y. Poly(ADP-ribose) synthetase. Separation and identification of three proteolytic fragments as the substrate-binding domain, the DNA-binding domain and the automodification domain. J Biol Chem. 1984;259:4770–4776.
32. Langelier MF, Ruhl DD, Planck JL, Kraus WL, Pascal JM. 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. 2010;285:18877–18887.
33. Langelier MF, Servent KM, Rogers EE, Pascal JM. A third zinc-binding domain of human poly(ADP-ribose) polymerase-1 coordinates DNA dependent enzyme activation. J Biol Chem. 2008;283:4105–4114.
34. Ye'lamos J, Farres J, Llacuna L, Ampurdanes C, Martin-Caballero J. PARP-1 and PARP-2: new players in tumour development. Am J Cancer Res. 2011;1:328–346.
35. Kinoshita T, Nakanishi I, Warizaya M, et al. Inhibitor-induced structural change of the active site of human poly(ADP-ribose) polymerase. FEBS Lett. 2004;556:43–46.
36. Masson MV, Rolli FD, Dantzer F, et al. Poly(ADP-ribose) polymerase: structure-function relationship. Biochimie. 1995;77:456–461.
37. Langelier MF, Planck JL, Roy S, Pascal JM. Structural basis for DNA damage–dependent poly (ADP-ribosyl)ation by human PARP-1. Science. 2012;336:728–732.
38. Altmeyer M, Messner S, Hassa PO, Fey M, Hottiger MO. Molecular mechanism of poly(ADP-ribosyl)ation by PARP1 and identification of lysine residues as ADP-ribose acceptor sites. Nucleic Acids Res. 2009;37:3723–3738.
39. Beckert S, Farrahi F, Perween GQ, et al. IGF-I-induced VEGF expression in HUVEC involves phosphorylation and inhibition of poly(ADP-ribose) polymerase. Biochem Biophys Res Commun. 2006;341:67–72.
40. Hassa PO, Haenni SS, Buerki C, Meier NI, Lane WS, Owen H. Acetylation of poly(ADP-ribose) polymerase-1 by p300/CREB-binding protein regulates coactivation of NF-kappaB-dependent transcription. J Biol Chem. 2005;280:40450–40464.
41. Kauppinen TM, Chan WY, Suh SW, Wiggins AK, Huang EJ, Swanson RA. Direct phosphorylation and regulation of poly(ADP-ribose) polymerase-1 by extracellular signal regulated kinases 1/2. Proc Natl Acad Sci USA. 2006;103:7136–7141.
42. Mao Z, Hine C, Tian X, et al. SIRT6 promotes DNA repair under stress by activating PARP-1. Science. 2011;332:1443–1446.
43. Zilio N, Williamson CT, Eustermann S, et al. DNA-dependent SUMO modification of PARP-1. DNA Repair. 2013;12:761–773.
44. +into a nuclear signal. Genes Dev. 2005;19:1951–1967.
45. Kun E, Kirsten E, Ordahl CP. Coenzymatic activity of randomly broken or intact double-stranded DNAs in auto and histone H1 trans-poly(ADP-ribosylation), catalyzed by poly(ADP-ribose) polymerase (PARP I). J Biol Chem. 2002;277:39066–39069.
46. Oei SL, Shi Y. Poly (ADP-ribosyl)ation of transcription factor Y in Yang 1 under conditions of DNA damage. Biochem Biophys Res Commun. 2001;285:27–31.
47. Lonskaya I, Potaman VN, Shlyakhtenko LS, Oussatcheva EA, Lyubchenko YL, Soldatenkov VA. Regulation of poly(ADP-ribose) polymerase-1 by DNA structure-specific binding. J Biol Chem. 2005;280:17076–17083.
48. Eustermann S, Videler H, Yang JC, et al. The DNA-binding domain of human PARP-1 interacts with DNA single-strand breaks as a monomer through its second zinc finger. J Mol Biol. 2011;407:149–170.
49. Langelier MF, Planck JL, Roy S, Pascal JM. Crystal structures of poly (ADP-ribose) polymerase-1 (PARP-1) zinc fingers bound to DNA structural and functional insights into DNA-dependent PARP-1 activity. J Biol Chem. 2011;286:10690–10701.
50. Eustermann S, Wu WF, Langelier MF, et al. Structural Basis of Detection and Signaling of DNA Single-Strand Breaks by Human PARP-1. Mol Cell 2015;60:742–754.
51. Ko HL, Ren EC. Novel poly(ADP-ribose) polymerase 1 binding motif in hepatitis B virus core promoter impairs DNA damage repair. Hepatology. 2011;54:1190–1198.
52. Cohen-Armon M, Visochek L, Rozensal D, et al. DNA-independent PARP-1 activation by phosphorylated ERK2 increases Elk1 activity: a link to histone acetylation. Mol Cell. 2007;25:297–308.
53. Cohen-Armon M. PARP-1 activation in the ERK signaling pathway. Trends Pharmacol Sci. 2007;28:556–560.
54. Ju B, Solum D, Song EJ, et al. Activating the PARP-1 sensor component of the Groucho/TLE1 corepressor complex mediates a CaMKinase IIdelta-dependent neurogenic gene activation pathway. Cell. 2004;119:815–829.
55. Dong F, Soubeyrand S, Haché RJ. Activation of PARP-1 in response to bleomycin depends on the Ku antigen and protein phosphatase 5. Oncogene. 2010;29:2093–2103.
56. +synthase. J Biol Chem. 2012;287:12405–12416.
57. Ouararhni K, Hadj-Slimane R, Ait-Si-Ali S, Robin P, Mietton F, Harel-Bellan A. The histone variant mH2A1.1 interferes with transcription by down-regulating PARP-1 enzymatic activity. Genes Dev. 2006;20:3324–3336.
58. Midorikawa R, Takei Y, Hirokawa N. KIF4 motor regulates activity-dependent neuronal survival by suppressing PARP-1 enzymatic activity. Cell. 2006;125:371–383.
59. Tulin A, Spradling A. Chromatin loosening by poly(ADP-ribose) polymerase (PARP) at Drosophila Puff Loci. Science. 2003;299:560–562.
60. Virág L, Szabó C. The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol Rev. 2002;54:375–429.
61. Masutani M, Nakagama H, Sugimura T. Poly(ADP-ribose) and carcinogenesis. Genes Chromosom Cancer. 2003;38:339–348.
62. Dantzer F, de La Rubia G, Menissier-De MJ, Hostomsky Z, de Murcia G, Schreiber V. Base excision repair is impaired in mammalian cells lacking poly(ADP-ribose) polymerase-1. Biochemistry. 2000;39:7559–7569.
63. Izhar L, Adamson B, Ciccia A, et al. A systematic analysis of factors localized to damaged chromatin reveals PARP-dependent recruitment of transcription factors. Cell Rep. 2015;11:1486–1500.
64. Ahel D, Hořejší Z, Wiechens N, et al. Poly (ADP-ribose) dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science. 2009;325:1240–1243.
65. Altmeyer M, Toledo L, Gudjonsson T, et al. The chromatin scaffold protein SAFB1 renders chromatin permissive for DNA damage signaling. Mol Cell. 2013;52:206–220.
66. Timinszky G, Till S, Hassa PO, et al. A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nat Struct Mol Biol. 2009;16:923–929.
67. Ahel I, Ahel D, Matsusaka T, et al. Poly (ADP-ribose)-binding zinc finger motifs in DNA repair/checkpoint proteins. Nature. 2008;451:81–85.
68. Rulten SL, Cortes-Ledesma F, Guo L, Iles NJ, Caldecott KW. APLF (C2orf13) is a novel component of poly (ADP-ribose) signaling in mammalian cells. Mol Cell Biol. 2008;28:4620–4628.
69. Mortusewicz O, Amé JC, Schreiber V, Leonhardt H. Feedback-regulated poly(ADP-ribosyl)ation by PARP-1 is required for rapid response to DNA damage in living cells. Nucleic Acids Res. 2007;35:7665–7675.
70. Robu M, Shah RG, Petitclerc N, Brind'Amour J, Kandan-Kulangara F, Shah GM. Role of poly(ADP-ribose) polymerase-1 in the removal of UV-induced DNA lesions by nucleotide excision repair. Proc Natl Acad Sci USA 2013;110:1658–1663.
71. Adamson B, Smogorzewska A, Sigoillot FD, King RW, Elledge SJ. A genome-wide homologous recombination screen identifies the RNA-binding protein RBMX as a component of the DNA-damage response. Nat Cell Biol. 2012;14:318–328.
72. Patel AG, Sarkaria JN, Kaufmann SH. Nonhomologous end joining drives poly(ADP-ribose) polymerase (PARP) inhibitor lethality in homologous recombination-deficient cells. Proc Natl Acad Sci USA. 2011;108:3406–3411.
73. Xie S, Mortusewicz O, Ma HT, et al. Timeless interacts with PARP-1 to promote homologous recombination repair. Mol Cell. 2015;60:163–167.
74. Galluzzi L, Joza N, Tasdemir E, et al. No death without life: vital functions of apoptotic effectors. Cell Death Differ. 2008;15:1113–1123.
75. Soldani C, Scovassi AI. Poly(ADP-ribose) polymerase-1 cleavage during apoptosis: an update. Apoptosis. 2002;7:321–328.
76. Tewari M, Quan LT, O'Rourke K, et al. Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell. 1995;81:801–809.
77. Scovassi AI, Diederich M. Modulation of poly(ADP-ribosylation) in apoptotic cells. Biochem Pharmacol. 2004;68:1041–1047.
78. Sosna J, Voigt S, Mathieu S, et al. TNF-induced necroptosis and PARP-1-mediated necrosis represent distinct routes to programmed necrotic cell death. Cell Mol Life Sci. 2014;71:331–348.
79. Gerö D, Szoleczky P, Chatzianastasiou A, Papapetropoulos A, Szabo C. Modulation of Poly (ADP-Ribose) Polymerase-1 (PARP-1)-Mediated Oxidative Cell Injury by Ring Finger Protein 146 (RNF146) in Cardiac Myocytes. Mol Med. 2014;20:313.
80. Yu SW, Andrabi SA, Wang H, et al. Apoptosis-inducing factor mediates poly(ADP-ribose) (PAR) polymer-induced cell death. Proc Natl Acad Sci USA. 2006;103:18314–18319.
81. Donizy P, Halon A, Surowiak P, Pietrzyk G, Kozyra C, Matkowski R. Correlation between PARP-1 immunoreactivity and cytomorphological features of parthanatos, a specific cellular death in breast cancer cells. Eur J Histochem. 2013;57:35.
82. Andrabi SA, Dawson TM, Dawson VL. Mitochondrial and nuclear cross talk in cell death. Ann NY Acad Sci. 2008;1147:233–241.
83. Rajawat J, Alex T, Mir H, Kadam A, Begum R. Proteases involved during oxidative stress induced poly(ADP-ribose) polymerase mediated cell death in D. discoideum. Microbiology. 2014;160:1101–1111.
84. Rajawat J, Mir H, Alex T, Bakshi S, Begum R. Involvement of poly(ADP-ribose) polymerase in paraptotic cell death of D. discoideum. Apoptosis. 2014;19:90–101.
85. Rajawat J, Vohra I, Mir H, Gohel D, Begum R. Effect of oxidative stress and involvement of poly(ADP-ribose) polymerase (PARP) in Dictyostelium discoideum development. FEBS J. 2007;274:5611–5618.
86. Mir H, Rajawat J, Begum R. Staurosporine induced cell death in D. discoideum is independent of PARP. Indian J Exp Biol. 2012;50:80–86.
87. Muñoz-Gámez JA, Rodríguez-Vargas JM, Quiles-Pérez R, et al. PARP-1 is involved in autophagy induced by DNA damage. Autophagy. 2009;5:61–74.
88. Huang Q, Shen HM. To die or to live: the dual role of poly(ADP-ribose) polymerase-1 in autophagy and necrosis under oxidative stress and DNA damage. Autophagy. 2009;5:273–276.
89. Son YO, Wang X, Hitron JA, et al. Cadmium induces autophagy through ROS-dependent activation of the LKB1–AMPK signaling in skin epidermal cells. Toxicol Appl Pharmacol. 2011;255:287–296.
90. Wyrsch P, Blenn C, Bader J, Althaus FR. Cell death and autophagy under oxidative stress: roles of poly(ADP-Ribose) polymerases and Ca(2+). Mol Cell Biol. 2012;32:3541–3553.
91. Mansuri MS, Singh M, Jadeja SD, et al. Could ER stress be a major link between oxidative stress and autoimmunity in Vitiligo? Pigmentary Disord. 2014;1:123.
92. Jog NR, Caricchio R. Differential regulation of cell death programs in males and females by Poly (ADP-Ribose) Polymerase-1 and 17β estradiol. Cell Death Dis. 2013;4:e758.
93. Caiafa P, Guastafierro T, Zampieri M. Epigenetics: poly(ADP-ribosyl)ation of PARP-1 regulates genomic methylation patterns. FASEB J. 2009;23:672–678.
94. Lodhi N, Kossenkov AV, Tulin AV. Bookmarking promoters in mitotic chromatin: poly(ADP-ribose) polymerase-1 as an epigenetic mark. Nucleic Acids Res. 2014;42:7028–7038.
95. Lapucci A, Pittelli M, Rapizzi E, Felici R, Moroni F, Chiarugi A. Poly(ADP-ribose) polymerase-1 is a nuclear epigenetic regulator of mitochondrial DNA repair and transcription. Mol Pharmacol. 2011;79:932–940.
96. Nalabothula N, Al-jumaily T, Eteleeb AM, Flight RM, Xiaorong S, Moseley H, et al. Genome-wide profiling of PARP1 reveals an interplay with gene regulatory regions and DNA methylation. PLoS ONE. 2015;10:e0135410.
97. Caiafa P, Zlatanova J. CCCTC-binding factor meets poly(ADP-ribose) polymerase-1. J Cell Physiol. 2009;219:265–270.
98. Vitale AM, Wolvetang E, Mackay-Sim A. Induced pluripotent stem cells: a new technology to study human diseases. Int J Biochem Cell Biol. 2011;43:843–846.
99. Doege CA, Inoue K, Yamashita T, et al. Early-stage epigenetic modification during somatic cell reprogramming by PARP-1 and Tet2. Nature. 2012;488:652–655.
100. Guetg C, Scheifele F, Rosenthal F, Hottiger MO, Santoro R. Inheritance of silent rDNA chromatin is mediated by PARP1 via noncoding RNA. Mol Cell. 2012;45:790–800.
101. Huletsky A, de Murcia G, Muller S, et al. The effect of poly(ADP- ribosyl)ation on native and H1-depleted chromatin. A role of poly(ADP-ribosyl)ation on core nucleosome structure. J Biol Chem. 1989;264:8878–8886.
102. Wacker DA, Ruhl DD, Balagamwala EH, Hope KM, Zhang T, Kraus WL. The DNA binding and catalytic domains of poly(ADP-ribose) polymerase 1 cooperate in the regulation of chromatin structure and transcription. Mol Cell Biol. 2007;27:475–7485.
103. Pinnola A, Naumova N, Shah M, Tulin AV. 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. 2007;282:32511–32519.
104. Krishnakumar R, Gamble MJ, Frizzell KM, Berrocal JG, Kininis M, Kraus WL. Reciprocal binding of PARP-1 and histone H1 at promoters specifies transcriptional outcomes. Science. 2008;319:819–821.
105. Frizzell KM, Gamble MJ, Berrocal JG, Zhang T, Krishnakumar R, Cen Y. 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. 2009;284:33926–33938.
106. Berger SL. Thecomplex language of chromatin regulation during transcription. Nature. 2007;447:407–412.
107. Kotova E, Lodhi N, Jarnik M, Pinnola AD, Ji Y, Tulin AV. Drosophila histone H2A variant (H2Av) controls poly (ADP-ribose) polymerase1 (PARP1) activation in chromatin. Proc Natl Acad Sci. 2011;108:6205–6210.
108. Kraus WL. New functions for an ancient domain. Nat Struct Mol Biol. 2009;16:904–907.
109. Chen H, Ruiz PD, Novikov L, Casill AD, Park JW, Gamble MJ. MacroH2A1.1 and PARP-1 cooperate to regulate transcription by promoting CBP-mediated H2B acetylation. Nat Struct Mol Biol. 2014;21:981–989.
110. Krishnakumar R, Kraus WL. PARP-1 regulates chromatin structure and transcription through a KDM5B-dependent pathway. Mol Cell. 2010;39:736–749.
111. Wu T, Wang XJ, Tian W, Jaramillo MC, Lau A, Zhang DD. Poly (ADP-ribose) polymerase-1 modulates Nrf2-dependent transcription. Free Radic Biol Med. 2014;67:69–80.
112. Okada H, Inoue T, Kikuta T, et al. Poly(ADP-ribose) polymerase-1 enhances transcription of the profibrotic CCN2 gene. J Am Soc Nephrol. 2008;19:933–942.
113. Ong CT, Van Bortle K, Ramos E, Corces VG. Poly(ADP-ribosyl)ation regulates insulator function and intrachromosomal interactions in Drosophila. Cell. 2013;155:148–159.
114. Zhao H, Sifakis EG, Sumida N, et al. PARP1-and CTCF-mediated interactions between active and repressed chromatin at the lamina promote oscillating transcription. Mol Cell. 2015;59:984–997.
115. O'Donnell A, Yang SH, Sharrocks AD. PARP1 orchestrates variant histone exchange in signal-mediated transcriptional activation. EMBO J. 2013;14:1084–1091.
116. Agarwal A, Mahfouz RZ, Sharma RK, Sarkar O, Mangrola D, Mathur PP. Potential biological role of poly(ADP-ribose) polymerase (PARP) in male gametes. Reprod Biol Endocrinol. 2009;7:143.
117. Di Meglio S, Denegri M, Vallefuoco S, Tramontano F, Scovassi AI, Quesada P. Poly(ADPR) polymerase-1 and poly(ADPR) glycohydrolase level and distribution in differentiating rat germinal cells. Mol Cell Biochem. 2003;248:85–91.
118. Quesada P, Atorino L, Cardone A, Ciarcia G, Farina B. Poly(ADP-ribosyl)ation system in rat germinal cells at different stages of differentiation. Exp Cell Res. 1996;226:183–190.
119. Schreiber V, Ame JC, Dolle P, Schultz I, Rinaldi B, Fraulob V. Poly(ADP-ribose) polymerase-2 (PARP-2) is required for efficient base excision DNA repair in association with PARP-1 and XRCC1. J Biol Chem. 2002;277:23028–23036.
120. Meyer-Ficca ML, Scherthan H, Burkle A, Meyer RG. Poly(ADP-ribosyl)ation during chromatin remodeling steps in rat spermiogenesis. Chromosoma. 2005;114:67–74.
121. Marcon L, Boissonneault G. Transient DNA strand breaks during mouse and human spermiogenesis new insights in stage specificity and link to chromatin remodeling. Biol Reprod. 2004;70:910–918.
122. Rouleau M, Saxena V, Rodrigue A, et al. A key role for poly(ADP-ribose) polymerase 3 in ectodermal specification and neural crest development. PLoS ONE. 2011;6:e15834.
123. Rajawat J, Mir H, Begum R. Differential role of poly(ADP-ribose) polymerase (PARP) in D. discoideum. BMC Dev Biol. 2011;11:14.
124. Jubin T, Kadam A, Saran S, Begum R. Poly (ADP-ribose) polymerase1 regulates growth and multicellularity in D. discoideum. Differentiation 2016;pii:S0301-4681(15)30081-5. doi:10.1016/j.diff.2016.03.002.
125. Couto CA, Wang HY, Green JC, et al. PARP regulates nonhomologous end joining through retention of Ku at double-strand breaks. J Cell Biol. 2011;194:367–375.
126. Mir H, Alex T, Rajawat J, Kadam A, Begum R. Response of D. discoideum to UV-C and involvement of poly(ADP-ribose) polymerase. Cell Prolif. 2015;48:363–374.
127. Kothe GO, Kitamura M, Masutani M, Selker EU, Inoue H. PARP is involved in replicative aging in Neurospora crassa. Fungal Genet Biol. 2010;47:297–309.
128. Müller-Ohldach M, Brust D, Hamann A, Osiewacz HD. Overexpression of PaParp encoding the poly(ADP-ribose) polymerase of Podospora anserina affects organismal aging. Mech Ageing Dev. 2011;132:33–42.
129. Semighini CP, Savoldi M, Goldman GH, Harris SD. Functional characterization of the putative Aspergillus nidulans poly(ADP-ribose) polymerase homolog PrpA. Genetics. 2006;173:87–98.
130. De Block M, Verduyn C, De Brouwer D, Cornelissen M. Poly(ADP-ribose) polymerase in plants affects energy homeostasis, cell death and stress tolerance. Plant J. 2005;41:95–106.
131. Vanderauwera S, De Block M, Van de Steene N, van de Cotte B, Metzlaff M, Van Breusegem F. Silencing of poly(ADP-ribose) polymerase in plants alters abiotic stress signal transduction. Proc Natl Acad Sci USA. 2007;104:15150–15155.
132. Fletcher JC, Burtis KC, Hogness DS, Thummel CS. The Drosophila E74 gene is required for metamorphosis and plays a role in the polytene chromosome puffing response to ecdysone. Development. 1995;121:1455–1465.
133. De Murcia JM, Ricoul M, Tartier L, et al. Functional interaction between PARP-1 and PARP-2 in chromosome stability and embryonic development in mouse. EMBO J. 2003;22:2255–2263.
134. Hamazaki N, Uesaka M, Nakashima K, Agata K, Imamura T. Gene activation-associated long noncoding RNAs function in mouse preimplantation development. Development. 2015;142:910–920.
135. Bai P, Canto C, Brunyanszki A, et al. PARP 1 regulates SIRT1 expression and whole body energy expenditure. Cell Metab. 2011a;13:450–460.
136. Devalaraja-Narashimha K, Padanilam BJ. PARP1 deficiency exacerbates diet-induced obesity in mice. J Endocrinol. 2010;205:243–252.
137. Wang ZQ, Auer B, Stingl L, et al. Mice lacking ADPRT and poly(ADP-ribosyl)ation develop normally but are susceptible to skin disease. Genes Dev. 1995;9:509–520.
138. Bai P, Canto C, Oudart H, et al. PARP-1 inhibition increases mitochondrial metabolism through SIRT1 activation. Cell Metab. 2011b;13:461–468.
139. Houtkooper RH, Williams RW, Auwerx J. Metabolic networks of longevity. Cell. 2010;142:9–14.
140. Ying W, Chen Y, Alano CC, Swanson RA. Tricarboxylic acid cycle substrates prevent PARP-mediated death of neurons and astrocytes. J Cereb Blood Flow Metab. 2002;22:774–779.
141. Andrabi SA, Umanah GKE, Chang C, et al. Poly(ADP-ribose) polymerase-dependent energy depletion occurs through inhibition of glycolysis. Proc Natl Acad Sci USA. 2014;111:10209–10214.
142. Bai P, Nagy L, Fodor T, Liaudet L, Pacher P. Poly (ADP-ribose) polymerases as modulators of mitochondrial activity. Trends Endocrinol Metab. 2015;26:75–83.
143. Asher G, Reinke H, Altmeyer M, Gutierrez-Arcelus M, Hottiger MO, Schibler U. Poly(ADP-ribose) polymerase 1 participates in the phase entrainment of circadian clocks to feeding. Cell. 2010;142:943–953.
144. Erener S, Mirsaidi A, Hesse M, et al. ARTD1 deletion causes increased hepatic lipid accumulation in mice fed a high-fat diet and impairs adipocyte function and differentiation. FASEB J. 2012b;26:2631–2638.
145. Erener S, Hesse M, Kostadinova R, Hottiger MO. Poly(ADP-ribose)polymerase-1 (PARP-1) controls adipogenic gene expression and adipocyte function. Mol Endocrinol. 2012a;26:79–86.
146. Hennessy BT, Timms KM, Carey MS, Gutin A, Meyer LA, Flake DD 2nd. Somatic mutations in BRCA1 and BRCA2 could expand the number of patients that benefit from poly(ADP-ribose) polymerase inhibitors in ovarian cancer. J Clin Oncol. 2010;28:3570–3576.
147. El-Khamisy SF, Masutani M, Suzuki H, Caldecott KW. A requirement for PARP-1 for the assembly or stability of XRCC1 nuclear foci at sites of oxidative DNA damage. Nucleic Acids Res. 2003;31:5526–5533.
148. Houtgraaf JH, Versmissen J, van der Giessen WJ. A concise review of DNA damage checkpoints and repair in mammalian cells. Cardiovasc Revasc Med. 2006;7:165–172.
149. Haince JF, McDonald D, Rodrigue A, et al. PARP-1 dependent kinetics of recruitment of MRE11 and NBS1 proteins to multiple DNA damage sites. J Biol Chem. 2008;283:1197–1208.
150. Tutt A, Ashworth A. The relationship between the roles of BRCA genes in DNA repair and cancer predisposition. Trends Mol Med. 2002;8:571–576.
151. Arun B, Akar U, Gutierrez-Barrera AM, Hortobagyi GN, Ozpolat B. The PARP inhibitor AZD2281 (Olaparib) induces autophagy/mitophagy in BRCA1 and BRCA2 mutant breast cancer cells. Int J Oncol. 2015;47:262–268.
152. Fong PC, Yap TA, Boss DS, et al. Poly(ADP-ribose) polymerase inhibition: frequent durable responses in BRCA carrier ovarian cancer correlating with platinum-free interval. J Clin Oncol. 2010;28:2512–2519.
153. Do K, Chen AP. Molecular Pathways: targeting PARP in cancer treatment. Clin Cancer Res. 2013;19:977–984.
154. Gottschalk AJ, Timinszky G, Kong SE, et al. Poly(ADP-ribosyl)ation directs recruitment and activation of an ATP-dependent chromatin remodeler. Proc Natl Acad Sci USA. 2009;106:13770–13774.
155. Zaremba T, Ketzer P, Cole M, Coulthard S, Plummer ER, Curtin NJ. Poly(ADP-ribose) polymerase-1 polymorphisms, expression and activity in selected human tumour cell lines. Br J Cancer. 2009;101:256–262.
156. Espinoza LA. The Role of PARP Activation in Prostate Cancer. Advances in Prostate Cancer, Dr. Gerhard Hamilton (Ed.). Croatia: InTech, 2013.
157. Mendoza-Alvarez H, Alvarez-Gonzalez R. Regulation of p53 sequence-specific DNA-binding by covalent poly(ADP-ribosyl)ation. J Biol Chem. 2001;276:36425–36430.
158. Idogawa M, Masutani M, Shitashige M, et al. Ku70 and poly(ADP-ribose) polymerase-1 competitively regulate beta-catenin and T-cell factor-4-mediated gene transactivation: possible linkage of DNA damage recognition and Wnt signaling. Cancer Res. 2007;67:911–918.
159. Idogawa M, Yamada T, Honda K, Sato S, Imai K, Hirohashi S. Poly(ADP-ribose) polymerase-1 is a component of the oncogenic T-cell factor-4/beta-catenin complex. Gastroenterology. 2005;128:1919–1936.
160. Schiewer MJ, Goodwin JF, Han S, Brenner JC, Augello MA, Dean JL. Dual Roles of PARP-1 Promote Cancer Growth and Progression. Cancer Discov. 2012;2:1134–1149.
161. Martire S, Mosca L, d'Erme M. PARP-1 involvement in neurodegeneration: A focus on Alzheimer's and Parkinson's diseases. Mech Ageing Dev. 2015;146–148:53–64.
162. Moroni F, Cozzi A, Chiarugi A, et al. Long-lasting neuroprotection and neurological improvement in stroke models with new, potent and brain permeable inhibitors of poly(ADP-ribose) polymerase. British J Pharmacol. 2012;165:1487–1500.
163. Ba X, Gupta S, Davidson M, Garg NJ. Trypanosoma cruzi induces the reactive oxygen species-PARP-1-RelA pathway for up-regulation of cytokine expression in cardiomyocytes. J Biol Chem. 2010;285:11596–11606.
164. Beneke S. Poly(ADP-ribose) polymerase activity in different pathologies: the link to inflammation and infarction. Exp Gerontol. 2008;43:605–614.
165. Zhang P, Maruyama T, Konkel JE, et al. PARP-1 controls immunosuppressive function of regulatory T cells by destabilizing Foxp3. PLoS ONE. 2013;8:e71590.
166. +regulatory T cells in poly(ADP-ribose) polymerase-1 deficiency. J Immunol. 2010;184:3470–3477.
167. Kaye SB, Lubinski J, Matulonis U, et al. Phase II, open-label, randomized, multicenter study comparing the efficacy and safety of olaparib, a poly (ADP-ribose) polymerase inhibitor, and pegylated liposomal doxorubicin in patients with BRCA1 or BRCA2 mutations and recurrent ovarian cancer. J Clin Oncol. 2011;30:372–379.
168. Mateo J, Friedlander M, Sessa C, et al. Administration of continuous/intermittent olaparib in ovarian cancer patients with a germline BRCA1/2 mutation to determine an optimal dosing schedule for the tablet formulation. Eur J Cancer. 2013;49:S161.
169. Gelmon KA, Tischkowitz M, Mackay H, et al. Olaparib in patients with recurrent high-grade serous or poorly differentiated ovarian carcinoma or triple-negative breast cancer: a phase 2, multicentre, open-label, non-randomised study. Lancet Oncol. 2011;12:852–861.
170. Ledermann J, Harter P, Gourley C, et al. Olaparib maintenance therapy in platinum-sensitive relapsed ovarian cancer. N Engl J Med. 2012;366:1382–1392.
171. Kaufman B, Shapira-Frommer R, Schmutzler RK, et al. Olaparib monotherapy in patients with advanced cancer and a germline BRCA1/2 mutation. J Clin Oncol. 2015;33:244–250.
172. Tutt A, Robson M, Garber JE, et al. Oral poly (ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and advanced breast cancer: a proof-of-concept trial. Lancet. 2010;376:235–244.
173. Liu JF, Tolaney SM, Birrer M, et al. A Phase 1 trial of the poly(ADP-ribose) polymerase inhibitor olaparib (AZD2281) in combination with the anti-angiogenic cediranib (AZD2171) in recurrent epithelial ovarian or triple-negative breast cancer. Eur J Cancer. 2013;49:2972–2978.
174. Liu JF, Barry WT, Birrer M, et al. Combination cediranib and olaparib versus olaparib alone for women with recurrent platinum-sensitive ovarian cancer: a randomised phase 2 study. Lancet Oncol. 2014;15:1207–1214.
175. Oza AM, Cibula D, Benzaquen AO, et al. Olaparib combined with chemotherapy for recurrent platinum-sensitive ovarian cancer: a randomised phase 2 trial. Lancet Oncol. 2015;16:87–97.
176. Rivkin SE, Iriarte D, Sloan H, Wiseman C, Moon J. Phase Ib/II with expansion of patients at the MTD study of olaparib plus weekly (metronomic) carboplatin and paclitaxel in relapsed ovarian cancer patients. ASCO Annu Meet Proc 2014;15(Suppl):5527.
177. Choy E, Butrynski JE, Harmon DC, et al. Phase II study of olaparib in patients with refractory Ewing sarcoma following failure of standard chemotherapy. BMC Cancer. 2014;14:813.
178. Waxweiler TV, Bowles D, Reddy K, et al. Safety and feasibility update of olaparib, an orally bioavailable PARP inhibitor, with concurrent cetuximab and radiation therapy in heavy smokers with stage III-IVB squamous cell carcinoma of the head/neck: a phase 1 trial. Int J Radiation Oncol Biol Phys. 2014;90:S559.
179. Chalmers AJ, Jackson A, Swaisland H, et al. Results of stage 1 of the oparatic trial: a phase I study of olaparib in combination with temozolomide in patients with relapsed glioblastoma. J Clin Oncol. 2014;32:5S.
180. Samol J, Ranson M, Scott E, et al. Safety and tolerability of the poly(ADP-ribose) polymerase (PARP) inhibitor, olaparib (AZD2281) in combination with topotecan for the treatment of patients with advanced solid tumors: a phase I study. Invest New Drugs. 2012;30:1493–1500.
181. Coleman RL, Sill MW, Bell-McGuinn K, et al. A phase II evaluation of the potent, highly selective PARP inhibitor veliparib in the treatment of persistent or recurrent epithelial ovarian, fallopian tube, or primary peritoneal cancer in patients who carry a germline BRCA1 or BRCA2 mutation-An NRG Oncology/Gynecologic Oncology Group study. Gynecol Oncol. 2015;137:386–391.
182. Pahuja S, Appleman LJ, Belani CP, et al. Preliminary activity of veliparib (V) in BRCA2-mutated metastatic castration-resistant prostate cancer (mCRPC). J Clin Oncol. 2015;33.
183. LoRusso PM, Tolaney SM, Wong S, et al. Combination of the PARP inhibitor veliparib (ABT888) with irinotecan in patients with triple negative breast cancer: Preliminary activity and signature of response. Cancer Res. 2015;75:CT325.
184. Owonikoko TK, Dahlberg SE, Khan SA, et al. A phase 1 safety study of veliparib combined with cisplatin and etoposide in extensive stage small cell lung cancer: A trial of the ECOG–ACRIN Cancer Research Group (E2511). Lung Cancer. 2015;89:66–70.
185. McKee MD, Bondarenko I, Guclu SZ, et al. Veliparib (ABT-888) or placebo combined with carboplatin and paclitaxel in patients with previously untreated advanced/metastatic squamous (Sq) non-small cell lung cancer (NSCLC): a randomized phase 3 trial. J Clin Oncol. 2015;33.
186. Kummar S, Ji J, Morgan R, et al. A Phase I Study of Veliparib in Combination with Metronomic Cyclophosphamide in Adults with Refractory Solid Tumors and Lymphomas. Clin Cancer Res. 2012;18:1726–1734.
187. O'Reilly EM, Lowery MA, Segal MF, et al. Phase IB trial of cisplatin (C), gemcitabine (G), and veliparib (V) in patients with known or potential BRCA or PALB2-mutated pancreas adenocarcinoma (PC). ASCO Annual Meeting Proceedings 2014;32(15 suppl):4023.
188. Hussain M, Carducci MA, Slovin S, et al. Targeting DNA repair with combination veliparib (ABT-888) and temozolomide in patients with metastatic castration-resistant prostate cancer. Invest New Drugs. 2014;32:904–912.