Touching base with PARPs: Moonlighting in the repair of UV lesions and double-strand breaks

Trends in Biochemical Sciences

Volumn 38, Issue 6, 2013, Pages 321-330

  Pines, Alex ^a   Mullenders, Leon H ^a   van Attikum, Haico ^a   Luijsterburg, Martijn S ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

DNA repair; Double strand break; Homologous recombination; Non homologous end joining; Nucleotide excision repair; Poly(ADP ribose) polymerase (PARP); UV induced DNA damage

Indexed keywords

BINDING PROTEIN; CELL DNA; COMPLEMENTARY DNA; DOUBLE STRANDED DNA; GENOMIC DNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PAR BINDING PROTEIN; POLY(ADENOSINE DIPHOSPHATE RIBOSE); POLYMER; PROTEIN PARP3; UNCLASSIFIED DRUG;

CATALYSIS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA END JOINING REPAIR; DNA TEMPLATE; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME STRUCTURE; EXCISION REPAIR; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN PROCESSING; RADIATION INJURY; REVIEW; ULTRAVIOLET RADIATION;

DNA DAMAGE; DNA REPAIR; POLY(ADP-RIBOSE) POLYMERASES; ULTRAVIOLET RAYS;

EID: 84878117602     PISSN: 09680004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tibs.2013.03.002     Document Type: Review

References (82)

1. Hottiger M.O., et al. Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem. Sci. 2010, 35:208-219.
2. Rulten S.L., et al. PARP-3 and APLF function together to accelerate nonhomologous end-joining. Mol. Cell 2011, 41:33-45.
3. Langelier M.F., et al. Structural basis for DNA damage-dependent poly(ADP-ribosyl)ation by human PARP-1. Science 2012, 336:728-732.
4. D'Amours D., et al. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem. J. 1999, 342:249-268.
5. Fisher A.E., et al. Poly(ADP-ribose) polymerase 1 accelerates single-strand break repair in concert with poly(ADP-ribose) glycohydrolase. Mol. Cell. Biol. 2007, 27:5597-5605.
6. Strom C.E., et al. Poly (ADP-ribose) polymerase (PARP) is not involved in base excision repair but PARP inhibition traps a single-strand intermediate. Nucleic Acids Res. 2011, 39:3166-3175.
7. Campalans A., et al. Distinct spatiotemporal patterns and PARP dependence of XRCC1 recruitment to single-strand break and base excision repair. Nucleic Acids Res. 2013, 41:3115-3129.
8. Hochegger H., et al. Parp-1 protects homologous recombination from interference by Ku and Ligase IV in vertebrate cells. EMBO J. 2006, 25:1305-1314.
9. Sugimura K., et al. PARP-1 ensures regulation of replication fork progression by homologous recombination on damaged DNA. J. Cell Biol. 2008, 183:1203-1212.
10. Yang Y.G., et al. Ablation of PARP-1 does not interfere with the repair of DNA double-strand breaks, but compromises the reactivation of stalled replication forks. Oncogene 2004, 23:3872-3882.
11. Bryant H.E., et al. PARP is activated at stalled forks to mediate Mre11-dependent replication restart and recombination. EMBO J. 2009, 28:2601-2615.
12. Haince J.F., et al. PARP1-dependent kinetics of recruitment of MRE11 and NBS1 proteins to multiple DNA damage sites. J. Biol. Chem. 2008, 283:1197-1208.
13. Dinant C., et al. Activation of multiple DNA repair pathways by sub-nuclear damage induction methods. J. Cell Sci. 2007, 120:2731-2740.
14. Min W., et al. Deletion of the nuclear isoform of poly(ADP-ribose) glycohydrolase (PARG) reveals its function in DNA repair, genomic stability and tumorigenesis. Carcinogenesis 2010, 31:2058-2065.
15. Schultz N., et al. Poly(ADP-ribose) polymerase (PARP-1) has a controlling role in homologous recombination. Nucleic Acids Res. 2003, 31:4959-4964.
16. Orsburn B., et al. Differential requirement for H2AX and 53BP1 in organismal development and genome maintenance in the absence of poly(ADP)ribosyl polymerase 1. Mol. Cell. Biol. 2010, 30:2341-2352.
17. Adamson B., et al. 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.
18. Wang H., et al. DNA ligase III as a candidate component of backup pathways of nonhomologous end joining. Cancer Res. 2005, 65:4020-4030.
19. Audebert M., et al. Involvement of poly(ADP-ribose) polymerase-1 and XRCC1/DNA ligase III in an alternative route for DNA double-strand breaks rejoining. J. Biol. Chem. 2004, 279:55117-55126.
20. Ruscetti T., et al. Stimulation of the DNA-dependent protein kinase by poly(ADP-ribose) polymerase. J. Biol. Chem. 1998, 273:14461-14467.
21. Spagnolo L., et al. Visualization of a DNA-PK/PARP1 complex. Nucleic Acids Res. 2012, 40:4168-4177.
22. Rybanska I., et al. PARP1 and DNA-PKcs synergize to suppress p53 mutation and telomere fusions during T-lineage lymphomagenesis. Oncogene 2012, 10.1038/onc.2012.199.
23. Mitchell J., et al. Poly(ADP-ribose) polymerase-1 and DNA-dependent protein kinase have equivalent roles in double strand break repair following ionizing radiation. Int. J. Radiat. Oncol. Biol. Phys. 2009, 75:1520-1527.
24. Veuger S.J., et al. Radiosensitization and DNA repair inhibition by the combined use of novel inhibitors of DNA-dependent protein kinase and poly(ADP-ribose) polymerase-1. Cancer Res. 2003, 63:6008-6015.
25. Finnie N.J., et al. DNA-dependent protein kinase activity is absent in xrs-6 cells: implications for site-specific recombination and DNA double-strand break repair. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:320-324.
26. Wang M., et al. PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res. 2006, 34:6170-6182.
27. McVey M., Lee S.E. MMEJ repair of double-strand breaks (director's cut): deleted sequences and alternative endings. Trends Genet. 2008, 24:529-538.
28. Yan C.T., et al. IgH class switching and translocations use a robust non-classical end-joining pathway. Nature 2007, 449:478-482.
29. Cheng Q., et al. Ku counteracts mobilization of PARP1 and MRN in chromatin damaged with DNA double-strand breaks. Nucleic Acids Res. 2011, 39:9605-9619.
30. Mansour W.Y., et al. The alternative end-joining pathway for repair of DNA double-strand breaks requires PARP1 but is not dependent upon microhomologies. Nucleic Acids Res. 2010, 38:6065-6077.
31. Fattah F., et al. Ku regulates the non-homologous end joining pathway choice of DNA double-strand break repair in human somatic cells. PLoS Genet. 2010, 6:e1000855.
32. Guirouilh-Barbat J., et al. Defects in XRCC4 and KU80 differentially affect the joining of distal nonhomologous ends. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:20902-20907.
33. Sfeir A., de Lange T. Removal of shelterin reveals the telomere end-protection problem. Science 2012, 336:593-597.
34. Robert I., et al. Parp1 facilitates alternative NHEJ, whereas Parp2 suppresses IgH/c-myc translocations during immunoglobulin class switch recombination. J. Exp. Med. 2009, 206:1047-1056.
35. Bentley J., et al. DNA double strand break repair in human bladder cancer is error prone and involves microhomology-associated end-joining. Nucleic Acids Res. 2004, 32:5249-5259.
36. Tobin L.A., et al. Targeting abnormal DNA repair in therapy-resistant breast cancers. Mol. Cancer Res. 2012, 10:96-107.
37. Boehler C., et al. Poly(ADP-ribose) polymerase 3 (PARP3), a newcomer in cellular response to DNA damage and mitotic progression. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:2783-2788.
38. Kalisch T., et al. New readers and interpretations of poly(ADP-ribosyl)ation. Trends Biochem. Sci. 2012, 37:381-390.
39. Kanno S., et al. A novel human AP endonuclease with conserved zinc-finger-like motifs involved in DNA strand break responses. EMBO J. 2007, 26:2094-2103.
40. Mehrotra P.V., et al. DNA repair factor APLF is a histone chaperone. Mol. Cell 2011, 41:46-55.
41. Ahel D., et al. Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin-remodeling enzyme ALC1. Science 2009, 325:1240-1243.
42. Gottschalk A.J., et al. Poly(ADP-ribosyl)ation directs recruitment and activation of an ATP-dependent chromatin remodeler. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:13770-13774.
43. Larsen D.H., et al. The chromatin-remodeling factor CHD4 coordinates signaling and repair after DNA damage. J. Cell Biol. 2010, 190:731-740.
44. Luijsterburg M.S., et al. A new non-catalytic role for ubiquitin ligase RNF8 in unfolding higher-order chromatin structure. EMBO J. 2012, 31:2511-2527.
45. Smeenk G., et al. The NuRD chromatin-remodeling complex regulates signaling and repair of DNA damage. J. Cell Biol. 2010, 190:741-749.
46. Chou D.M., et al. 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. U.S.A. 2010, 107:18475-18480.
47. Polo S.E., et al. Regulation of DNA-damage responses and cell-cycle progression by the chromatin remodelling factor CHD4. EMBO J. 2010, 29:3130-3139.
48. Luijsterburg M.S., van Attikum H. Close encounters of the RNF8th kind: when chromatin meets DNA repair. Curr. Opin. Cell Biol. 2012, 24:439-447.
49. Smeenk G., et al. Poly(ADP-ribosyl)ation links the chromatin remodeler SMARCA5/SNF2H to RNF168-dependent DNA damage signaling. J. Cell Sci. 2012, 10.1242/jcs.109413.
50. Ismail I.H., et al. CBX4-mediated SUMO modification regulates BMI1 recruitment at sites of DNA damage. Nucleic Acids Res. 2012, 40:5497-5510.
51. Cleaver J.E., et al. Poly(ADP-ribose): spectator or participant in excision repair of DNA damage. Princess Takamatsu Symp. 1983, 13:195-207.
52. Vodenicharov M.D., et al. Mechanism of early biphasic activation of poly(ADP-ribose) polymerase-1 in response to ultraviolet B radiation. J. Cell Sci. 2005, 118:589-599.
53. Luijsterburg M.S., et al. DDB2 promotes chromatin decondensation at UV-induced DNA damage. J. Cell Biol. 2012, 197:267-281.
54. Pines A., et al. PARP1 promotes nucleotide excision repair through DDB2 stabilization and recruitment of ALC1. J. Cell Biol. 2012, 199:235-249.
55. Kamileri I., et al. Nucleotide excision repair: new tricks with old bricks. Trends Genet. 2012, 28:566-573.
56. Robu M., et al. Role of poly(ADP-ribose) polymerase-1 in the removal of UV-induced DNA lesions by nucleotide excision repair. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:1658-1663.
57. Flohr C., et al. Poly(ADP-ribosyl)ation accelerates DNA repair in a pathway dependent on Cockayne syndrome B protein. Nucleic Acids Res. 2003, 31:5332-5337.
58. Ghodgaonkar M.M., et al. Depletion of poly(ADP-ribose) polymerase-1 reduces host cell reactivation of a UV-damaged adenovirus-encoded reporter gene in human dermal fibroblasts. DNA Repair (Amst.) 2008, 7:617-632.
59. Lakatos P., et al. 3-Aminobenzamide protects primary human keratinocytes from UV-induced cell death by a poly(ADP-ribosyl)ation independent mechanism. Biochim. Biophys. Acta 2013, 1833:743-751.
60. Alekseev S., et al. Enhanced DDB2 expression protects mice from carcinogenic effects of chronic UV-B irradiation. Cancer Res. 2005, 65:10298-10306.
61. Gagne J.P., et al. Proteome-wide identification of poly(ADP-ribose) binding proteins and poly(ADP-ribose)-associated protein complexes. Nucleic Acids Res. 2008, 36:6959-6976.
62. King B.S., et al. Poly(ADP-ribose) contributes to an association between Poly(ADP-ribose)polymerase-1 and xeroderma pigmentosum complementation group A in nucleotide excision repair. J. Biol. Chem. 2012, 287:39824-39833.
63. Cohen-Armon M., et al. DNA-independent PARP-1 activation by phosphorylated ERK2 increases Elk1 activity: a link to histone acetylation. Mol. Cell 2007, 25:297-308.
64. Hassa P.O., et al. Transcriptional coactivation of nuclear factor-kappaB-dependent gene expression by p300 is regulated by poly(ADP)-ribose polymerase-1. J. Biol. Chem. 2003, 278:45145-45153.
65. Rajamohan S.B., et al. SIRT1 promotes cell survival under stress by deacetylation-dependent deactivation of poly(ADP-ribose) polymerase 1. Mol. Cell. Biol. 2009, 29:4116-4129.
66. Martin N., et al. PARP-1 transcriptional activity is regulated by sumoylation upon heat shock. EMBO J. 2009, 28:3534-3548.
67. Messner S., et al. Sumoylation of poly(ADP-ribose) polymerase 1 inhibits its acetylation and restrains transcriptional coactivator function. FASEB J. 2009, 23:3978-3989.
68. Kang H.C., et al. Iduna is a poly(ADP-ribose) (PAR)-dependent E3 ubiquitin ligase that regulates DNA damage. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:14103-14108.
69. Moser J., et al. Sealing of chromosomal DNA nicks during nucleotide excision repair requires XRCC1 and DNA ligase III alpha in a cell-cycle-specific manner. Mol. Cell 2007, 27:311-323.
70. Cleaver J.E., et al. Differences in the regulation by poly(ADP-ribose) of repair of DNA damage from alkylating agents and ultraviolet light according to cell type. J. Biol. Chem. 1983, 258:9059-9068.
71. Epstein J.H., Cleaver J.E. 3-Aminobenzamide can act as a cocarcinogen for ultraviolet light-induced carcinogenesis in mouse skin. Cancer Res. 1992, 52:4053-4054.
72. Gunji A., et al. Parp-1 deficiency does not increase the frequency of tumors in the oral cavity and esophagus of ICR/129Sv mice by 4-nitroquinoline 1-oxide, a carcinogen producing bulky adducts. Cancer Lett. 2006, 241:87-92.
73. Ogawa K., et al. Parp-1 deficiency does not enhance liver carcinogenesis induced by 2-amino-3-methylimidazo[4,5-f]quinoline in mice. Cancer Lett. 2006, 236:32-38.
74. Qin X.J., et al. Poly(ADP-ribose) polymerase-1 inhibition by arsenite promotes the survival of cells with unrepaired DNA lesions induced by UV exposure. Toxicol. Sci. 2012, 127:120-129.
75. Jans J., et al. Powerful skin cancer protection by a CPD-photolyase transgene. Curr. Biol. 2005, 15:105-115.
76. Gagne J.P., et al. Quantitative proteomics profiling of the poly(ADP-ribose)-related response to genotoxic stress. Nucleic Acids Res. 2012, 40:7788-7805.
77. Shall S., de Murcia G. Poly(ADP-ribose) polymerase-1: what have we learned from the deficient mouse model?. Mutat. Res. 2000, 460:1-15.
78. Menissier de Murcia J., et al. Functional interaction between PARP-1 and PARP-2 in chromosome stability and embryonic development in mouse. EMBO J. 2003, 22:2255-2263.
79. Ame J.C., et al. Radiation-induced mitotic catastrophe in PARG-deficient cells. J. Cell Sci. 2009, 122:1990-2002.
80. Bryant H.E., et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 2005, 434:913-917.
81. Farmer H., et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005, 434:917-921.
82. Fong P.C., et al. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N. Engl. J. Med. 2009, 361:123-134.