PARPs and the DNA damage response

Carcinogenesis

Volumn 33, Issue 8, 2012, Pages 1433-1440

  Sousa, Fabricio G ^a,b,c,d   Matuo, Renata ^a,b,c,d   Soares, Daniele G ^b,c,d   Escargueil, Alexandre E ^b,c,d   Henriques, João A P ^a,e   Larsen, Annette K ^b,c,d   Saffi, Jenifer ^a,f  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b CENTRE DE RECHERCHE SAINT ANTOINE   (France)

^c INSERM   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e UNIVERSITY OF CAXIAS DO SUL   (Brazil)

^f UNIVERSIDADE FEDERAL DE CIÊNCIAS DA SAÚDE DE PORTO ALEGRE   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE DIPHOSPHATE RIBOSE; AGO 14699; DNA; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 2; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 3; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; OLAPARIB; POLYMER; UNCLASSIFIED DRUG; VELIPARIB;

ADENOSINE DIPHOSPHATE RIBOSYLATION; BREAST CANCER; CATALYSIS; CELL DEATH; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME ABERRATION; CYTOTOXICITY; DNA DAMAGE; DNA DAMAGE RESPONSE; DOUBLE STRANDED DNA BREAK; DRUG MEGADOSE; ENZYME ACTIVITY; ENZYME STRUCTURE; G2 PHASE CELL CYCLE CHECKPOINT; GENETIC TRANSCRIPTION; GLIOBLASTOMA; HUMAN; LEUKEMIA; M PHASE CELL CYCLE CHECKPOINT; MELANOMA; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW; SIGNAL TRANSDUCTION; SOLID TUMOR; TUMOR SUPPRESSOR GENE; UNSPECIFIED SIDE EFFECT;

ANIMALS; DNA DAMAGE; HUMANS; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN CONFORMATION;

EID: 84865313346     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgs132     Document Type: Review

References (102)

1. Smith,J. et al. (2010) The ATM-Chk2 and ATR-Chk1 pathways in DNA damage signaling and cancer. Adv. Cancer Res., 108, 73-112.
2. Harper,J.W. et al. (2007) The DNA damage response: ten years after. Mol. Cell, 28, 739-745.
3. Bernstein,C. et al. (2002) DNA repair/pro-apoptotic dual-role proteins in five major DNA repair pathways: fail-safe protection against carcinogenesis. Mutat. Res., 511, 145-178.
4. Amé,J.C. et al. (2004) The PARP superfamily. BioEssays, 26, 882-893.
5. Nguewa,P.A. et al. (2005) Poly(ADP-Ribose) polymerases: homology, structural domains and functions. Novel Therapeutical applications. Prog. Biophys. Mol. Biol., 88, 143-172.
6. Quénet,D. et al. (2009) The role of poly(ADP-ribosyl)ation in epigenetic events. Int. J. Biochem. Cell Biol., 41, 60-65.
7. Gagné,J.P. et al. (2006) The expanding role of poly(ADP-ribose) metabolism: current challenges and new perspectives. Curr. Opin. Cell Biol., 18, 145-151.
8. Hakmé,A. et al. (2008) The expanding field of poly(ADP-ribosyl)ation reactions. 'Protein Modifications: Beyond the Usual Suspects' Review Series. EMBO Rep., 9, 1094-1100.
9. Krishnakumar,R. et al. (2010) The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Mol. Cell, 39, 8-23.
10. Schreiber,V. et al. (2006) Poly(ADPribose): novel functions for an old molecule. Nat. Rev. Mol. Cell Biol., 7, 517-528.
11. Hottiger,M.O. et al. (2010) Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem. Sci., 35, 208-219.
12. Rulten,S.L. et al. (2011) PARP-3 and APLF function together to accelerate nonhomologous end-Joining. Mol. Cell, 41, 33-45.
13. Langelier,M.F. et al. (2008) A third zinc-binding domain of human poly (ADP-ribose) polymerase-1 coordinates DNA-dependent enzyme activation. J. Biol. Chem., 283, 4105-4114.
14. Yélamos,J. et al. (2011) PARP-1 and PARP-2: new players in tumour development. Am. J. Cancer Res., 1, 328-346.
15. Oliver,A.W. et al. (2004) Crystal structure of the catalytic fragment of murine poly(ADP-ribose) polymerase-2. Nucleic Acids Res., 32, 456-464.
16. Yélamos,J. et al. (2008) Toward specific functions of poly(ADP-ribose) polymerase-2. Trends Mol. Med., 14, 169-178.
17. Lehtiö,L. et al. (2009) Structural basis for inhibitor specificity in human poly(ADP-ribose) polymerase-3. J. Med. Chem., 52, 3108-3111.
18. Loseva,O. et al. (2010) PARP-3 is a mono-ADP-ribosylase that activates PARP-1 in the absence of DNA. J. Biol. Chem., 285, 8054-8060.
19. Kleine,H. et al. (2009) Learning how to read ADP-ribosylation. Cell, 139, 17-19.
20. Min,W. et al. (2009) Poly(ADP-ribose) glycohydrolase (PARG) and its therapeutic potential. Front. Biosci., 14, 1619-1626.
21. Min,W. et al. (2010) Deletion of the nuclear isoform of poly(ADP-ribose) glycohydrolase (PARG) reveals its function in DNA repair, genomic stability and tumorigenesis. Carcinogenesis, 31, 2058-2065.
22. D'Amours,D. et al. (1999) Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem. J., 342, 249-268.
23. Amé,J.C. et al. (1999) PARP-2, a novelmammalian DNA damage-dependent poly(ADP-ribose) polymerase. J. Biol. Chem., 274, 17860-17868.
24. Mortusewicz,O. et al. (2007) Feedback-regulated poly(ADP-ribosyl)ation by PARP-1 is required for rapid response to DNA damage in living cells. Nucleic Acids Res., 35, 7665-7675.
25. Vodenicharov,M.D. et al. (2005) Mechanism of early biphasic activation of poly(ADPribose) polymerase-1 in response to ultraviolet B radiation. J. Cell Sci., 118, 589-599.
26. Khodyreva,S.N. et al. (2010) Apurinic/apyrimidinic (AP) site recognition by the 5#-dRP/AP lyase in poly(ADP-ribose) polymerase-1 (PARP-1). Proc. Natl Acad. Sci. USA, 107, 22090-22095.
27. Sukhanova,M. et al. (2010) Poly(ADP-ribose) polymerase 1 regulates activity of DNA polymerase beta in long patch base excision repair. Mutat. Res., 685, 80-89.
28. Schreiber,V. et al. (2002) Poly(ADP-ribose) polymerase-2 (PARP-2) is required for efficient base excision DNA repair in association with PARP-1 and XRCC1. J. Biol. Chem., 277, 23028-23036.
29. El-Khamisy,S.F. et al. (2003) A requirement for PARP-1 for the assembly or stability of XRCC1 nuclear foci at sites of oxidative DNA damage. Nucleic Acids Res., 31, 5526-5533.
30. Gagné,J.P. et al. (2008) Proteome-wide identification of poly(ADP-ribose) binding proteins and poly(ADP-ribose)-associated protein complexes. Nucleic Acids Res., 36, 6959-6976.
31. Leppard,J.B. et al. (2003) Physical and functional interaction between DNA ligase IIIa and poly(ADP-ribose) polymerase 1 in DNA singlestrand break repair. Mol. Cell. Biol., 23, 5919-5927.
32. Harris,J.L. et al. (2009) Aprataxin, poly-ADP ribose polymerase 1 (PARP-1) and apurinic endonuclease 1 (APE1) function together to protect the genome against oxidative damage. Hum. Mol. Genet., 18, 4102-4117.
33. Heale,J.T. et al. (2006) Condensin I interacts with the PARP-1-XRCC1 complex and functions in DNA single-strand break repair. Mol. Cell, 21, 837-848.
34. Bekker-Jensen,S. et al. (2007) Human Xip1 (C2orf13) is a novel regulator of cellular responses to DNA strand breaks. J. Biol. Chem., 282, 19638-19643.
35. Kedar,P.S. et al. (2008) Interaction between PARP-1 and ATR in mouse fibroblasts is blocked by PARP inhibition. DNA Repair (Amst.), 7, 1787- 1798.
36. Tong,W.M. et al. (2001) DNA strand break-sensing molecule poly(ADPribose) polymerase cooperates with p53 in telomere function, chromosome stability, and tumor suppression. Mol. Cell. Biol., 21, 4046-4054.
37. Nicolás,L. et al. (2010) Loss of poly(ADP-ribose) polymerase-2 leads to rapid development of spontaneous T-cell lymphomas in p53-deficient mice. Oncogene, 29, 2877-2883.
38. Cazzalinia,O. et al. (2010) p21CDKN1A participates in base excision repair by regulating the activity of poly(ADP-ribose) polymerase-1. DNA Repair (Amst.), 9, 627-635.
39. Haince,J.F. et al. (2007) Ataxia telangiectasia mutated (ATM) signaling network is modulated by a novel poly(ADP-ribose)-dependent pathway in the early response to DNA-damaging agents. J. Biol. Chem., 282, 16441-
40. Huber,A. et al. (2004) PARP-1, PARP-2 and ATM in the DNA damage response: functional synergy in mouse development. DNA Repair (Amst.), 3, 1103-1108.
41. Haince,J.F. et al. (2008) PARP1-dependent kinetics of recruitment of MRE11 and NBS1 proteins to multiple DNA damage sites. J. Biol. Chem., 283, 1197-1208.
42. Rouleau,M. et al. (2007) PARP-3 associates with polycomb group bodies and with components of the DNA damage repair machinery. J. Cell. Biochem., 100, 385-401.
43. Paddock,M.N. et al. (2011) Competition between PARP-1 and Ku70 control the decision between high-fidelity and mutagenic DNA repair. DNA Repair (Amst.), 10, 338-343.
44. Tong,W.M. et al. (2002) Synergistic role of Ku80 and poly(ADP-ribose) polymerase in suppressing chromosomal aberrations and liver cancer formation. Cancer Res., 62, 6990-6996.
45. Mitchell,J. et al. (2009) Poly(ADP-ribose) polymerase-1 and DNAdependent protein kinase have equivalent roles in double strand break repair following ionizing radiation. Int. J. Radiat. Oncol. Biol. Phys., 75, 1520- 1527.
46. Chou,D.M. et al. (2010) A chromatin localization screen reveals poly (ADP ribose)-regulated recruitment of the repressive polycomb and NuRD complexes to sites of DNA damage. Proc. Natl Acad. Sci. USA, 107, 18475-18480.
47. Huang,J.Y. et al. (2006) Modulation of nucleosome-binding activity of FACT by poly(ADP-ribosyl)ation. Nucleic Acids Res., 34, 2398-2407.
48. Timinszky,G. et al. (2009) A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nat. Struct. Mol. Biol., 16, 923-929.
49. Ahel,D. et al. (2009) Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science, 325, 1240-1243.
50. Ahel,I. et al. (2008) Poly(ADP-ribose)-binding zinc finger motifs in DNA repair/checkpoint proteins. Nature, 451, 81-85.
51. Rulten,S.L. et al. (2008) APLF (C2orf13) is a novel component of poly (ADP-ribose) signaling in mammalian cells. Mol. Cell. Biol., 28, 4620-4628.
52. Yu,S.W. et al. (2006) Apoptosis-inducing factor mediates poly(ADPribose) (PAR) polymer-induced cell death. Proc. Natl Acad. Sci. USA, 103, 18314-18319.
53. Andrabi,S.A. et al. (2006) Poly(ADP-ribose) (PAR) polymer is a death signal. Proc. Natl Acad. Sci. USA, 103, 18308-18313.
54. D'Amours,D. et al. (2001) Gain-of-function of poly(ADP-ribose) polymerase- upon cleavage by apoptotic proteases: implications for apoptosis. J. Cell Sci., 114, 3771-3778.
55. Benchoua,A. et al. (2002) Active caspase-8 translocates into the nucleus of apoptotic cells to inactivate poly(ADP-ribose) polymerase-2. J. Biol. Chem., 277, 34217-34222.
56. Murcia,M.J. et al. (2003) Functional interaction between PARP-1 and PARP-2 in chromosome stability and embryonic development in mouse. EMBO J., 22, 2255-2263.
57. Boehler,C. et al. (2011) Poly(ADP-ribose) polymerase 3 (PARP3), a newcomer in cellular response to DNA damage and mitotic progression. Proc. Natl Acad. Sci. USA, 108, 2783-2788.
58. Chasovskikh,S. et al. (2005) DNA transitions induced by binding of PARP-1 to cruciform structures in supercoiled plasmids. Cytometry, 68, 21-27.
59. Lonskaya,I. et al. (2005) Regulation of poly(ADP-ribose) polymerase-1 by DNA structure-specific binding. J. Biol. Chem., 280, 17076-17083.
60. Potaman,V.N. et al. (2005) Specific binding of poly(ADP-ribose) polymerase-to cruciform hairpins. J. Mol. Biol., 348, 609-615.
61. Langelier,M.F. et al. (2010) The Zn3 domain of human poly(ADP-ribose) polymerase-1 (PARP-1) functions in both DNA-dependent poly(ADPribose) synthesis activity and chromatin compaction. J. Biol. Chem., 285, 18877-18887.
62. Pion,E. et al. (2005) DNA-induced dimerization of poly(ADP-ribose) polymerase-1 triggers its activation. Biochemistry, 44, 14670-14681.
63. Malanga,M. et al. (1994) Poly(ADP-ribose) molecules formed during DNA repair in vivo. J. Mol. Biol., 269, 17691-17696.
64. Boehler,C. et al. (2011) PARP-3, a DNA-dependent PARP with emerging roles in double-strand break repair and mitotic progression. Cell Cycle, 10, 1-2.
65. Kraus,W.L. (2009) New functions for an ancient domain. Nat. Struct. Mol. Biol., 16, 904-907.
66. Pleschke,J.M. et al. (2000) Poly(ADP-ribose) binds to specific domains in DNA damage checkpoint proteins. J. Biol. Chem., 275, 40974-40980.
67. Gottschalk,A.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.
68. Aguilar-Quesada,R. et al. (2007) Interaction between ATM and PARP-1 in response to DNA damage and sensitization of ATM deficient cells through PARP inhibition. BMC Mol. Biol., 8, 29.
69. Weston,V.J. et al. (2010) The PARP inhibitor olaparib induces significant killing of ATM-deficient lymphoid tumor cells in vitro and in vivo. Blood, 116, 4578-4587.
70. Williamson,C.T. et al. (2010) ATM deficiency sensitizes mantle cell lymphoma cells to poly(ADP-ribose) polymerase-1 inhibitors. Mol. Cancer Ther., 9, 347-357.
71. Carrozza,M.J. et al. (2009) PARP inhibition during alkylation-induced genotoxic stress signals a cell cycle checkpoint response mediated by ATM. DNA Repair (Amst.), 8, 1264-1272.
72. Bryant,H.E. et al. (2006) Inhibition of poly (ADP-ribose) polymerase activates ATM which is required for subsequent homologous recombination repair. Nucleic Acids Res., 34, 1685-1691.
73. Horton,J.K. et al. (2007) ATR signaling mediates an S-phase checkpoint after inhibition of poly(ADP-ribose) polymerase activity. DNA Repair (Amst.), 6, 742-750.
74. Lu,H.R. et al. (2006) A stronger DNA damage-induced G2 checkpoint due to over-activated CHK1 in the absence of PARP-1. Cell Cycle, 5, 2364-2370.
75. Frouin,I. et al. (2003) Human proliferating cell nuclear antigen, poly(-ADP-ribose) polymerase-1, and p21waf1/cip1. A dynamic exchange of partners. J. Biol. Chem., 278, 39265-39268.
76. Woodhouse,B.C. et al. (2008) Poly(ADP-ribose) polymerase-1 modulates DNA repair capacity and prevents formation of DNA double strand breaks. DNA Repair (Amst.), 7, 932-940.
77. Parsons,J.L. et al. (2005) Poly(ADP-ribose) polymerase-1 protects excessive DNA strand breaks from deterioration during repair in human cell extracts. FEBS J., 272, 2012-2021.
78. Escargueil,A.E. et al. (2008) What histone code for DNA repair? Mutat. Res., 658, 259-270.
79. Krishnakumar,R. et al. (2008) Reciprocal binding of PARP-1 and histone H1 at promoters specifies transcriptional outcomes. Science, 319, 819-821.
80. Heo,K. et al. (2008) FACT-mediated exchange of histone variant H2AX regulated by phosphorylation of H2AX and ADP-ribosylation of Spt16. Mol. Cell, 30, 86-97.
81. Poirier,G.G. et al. (1982) Poly(ADP-ribosyl)ation of polynucleosomes causes relaxation of chromatin structure. Proc. Natl Acad. Sci. USA, 79, 3423-3427.
82. Niedergang,C. et al. (1985) Time course of polynucleosome relaxation and ADP-ribosylation correlation between relaxation and histone H1 hyper-ADP-ribosylation. Eur. J. Biochem., 146, 185-191.
83. Huletsky,A. et al. (1985) Sequential ADP-ribosylation pattern of nucleosomal histones ADP-ribosylation of nucleosomal histones. Eur. J. Biochem., 146, 277-285.
84. Herceg,Z. et al. (2001) Functions of poly(ADP-ribose) polymerase (PARP) in DNA repair, genomic integrity and cell death. Mutat. Res., 477, 97-110.
85. Andrabi,S.A. et al. (2008) Mitochondrial and nuclear cross talk in cell death: parthanatos. Ann. N. Y. Acad. Sci., 1147, 233-241.
86. Yu,S.W. et al. (2002) Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science, 297, 259-263.
87. Jagtap,P. et al. (2005) Poly(ADP-ribose) polymerase and the therapeutic effects of its inhibitors. Nat. Rev. Drug Discov., 4, 421-440.
88. Lord,C.J. et al. (2008) Targeted therapy for cancer using PARP inhibitors. Curr. Opin. Pharmacol., 8, 363-369.
89. Rouleau,M. et al. (2010) PARP inhibition: pARP1 and beyond. Nat. Rev. Cancer, 10, 293-301.
90. Banerjee,S. et al. (2010) Making the best of PARP inhibitors in ovarian cancer. Nat. Rev. Clin. Oncol., 7, 508-519.
91. Anders,C.K. et al. (2010) Poly(ADP-ribose) polymerase inhibition: "targeted" therapy for triple-negative breast cancer. Clin. Cancer Res., 16, 4702-4710.
92. Carden,C.P. et al. (2010) PARP inhibition: targeting the Achilles' heel of DNA repair to treat germline and sporadic ovarian cancers. Curr. Opin. Oncol., 22, 473-480.
93. Helleday,T. (2011) The underlying mechanism for the PARP and BRCA synthetic lethality: clearing up the misunderstandings. Mol. Oncol., 5, 387-
94. Farmer,H. et al. (2005) Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature, 434, 917-921.
95. Bryant,H.E. et al. (2005) Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature, 434, 913-917.
96. Rottenberg,S. et al. (2008) High sensitivity of BRCA1-deficient mammary tumors to the PARP inhibitor AZD2281 alone and in combination with platinum drugs. Proc. Natl Acad. Sci. USA, 105, 17079-17084.
97. Smith,L.M. et al. (2005) The novel poly(ADP-ribose) polymerase inhibitor, AG14361, sensitizes cells to topoisomerase I poisons by increasing the persistence of DNA strand breaks. Clin. Cancer Res., 11, 8449-8457.
98. Gaymes,T.J. et al. (2009) Inhibitors of poly ADP-ribose polymerase (PARP) induce apoptosis of myeloid leukemic cells: potential for therapy of myeloid leukemia and myelodysplastic syndromes. Haematologica, 94, 638-646.
99. Gangopadhyay,N.N. et al. (2011) Inhibition of poly(ADP-ribose) polymerase (PARP) induces apoptosis in lung cancer cell lines. Cancer Invest., 29, 608-616.
100. Sandhu,S.K. et al. (2010) Poly(ADP-ribose) polymerase inhibitors in cancer treatment: a clinical perspective. Eur. J. Cancer, 46, 9-20.
101. Kummar,S. et al. (2011) Phase I study of PARP inhibitor ABT-888 in combination with topotecan in adults with refractory solid tumors and lymphomas. Cancer Res., 71, 5626-5634.
102. Plummer,R. et al. (2008) Phase I study of the poly(ADP-ribose) polymerase inhibitor, AG014699, in combination with temozolomide in patients with advanced solid tumors. Clin. Cancer Res., 14, 7917-7923.