The role of ADP-ribosylation in regulating DNA interstrand crosslink repair

Journal of Cell Science

Volumn 129, Issue 20, 2016, Pages 3845-3858

  Gunn, Alasdair R ^a   Banos Pinero, Benito ^b   Paschke, Peggy ^a   Sanchez Pulido, Luis ^c   Ariza, Antonio ^b   Day, Joseph ^a   Emrich, Mehera ^a   Leys, David ^d   Ponting, Chris P ^c   Ahel, Ivan ^b   Lakin, Nicholas D ^a,e  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

^e MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

ADP ribosyltransferases; Dictyostelium; Interstrand crosslink; PARPs

Indexed keywords

APRATAXIN APLF AND PNKP LIKE PROTEIN; CISPLATIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; POLY(ADENOSINE DIPHOSPHATE RIBOSE); PROTEIN; PROTEIN ADPRT1A; PROTEIN ADPRT2; UNCLASSIFIED DRUG; CHROMATIN; CROSS LINKING REAGENT; DNA; PROTEIN BINDING; PROTOZOAL PROTEIN;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ARTICLE; CHROMATIN; CONTROLLED STUDY; DICTYOSTELIUM; DNA CROSS LINKING; DNA DAMAGE; DNA END JOINING REPAIR; DNA REPAIR; DOUBLE STRANDED DNA BREAK; DRUG RESPONSE; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; CELL NUCLEUS; CHEMISTRY; DRUG EFFECTS; METABOLISM; MOLECULAR MODEL;

CELL NUCLEUS; CHROMATIN; CISPLATIN; CROSS-LINKING REAGENTS; DICTYOSTELIUM; DNA; DNA DAMAGE; DNA END-JOINING REPAIR; DNA REPAIR; MODELS, MOLECULAR; POLY ADENOSINE DIPHOSPHATE RIBOSE; PROTEIN BINDING; PROTEIN DOMAINS; PROTOZOAN PROTEINS;

EID: 84995478813     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.193375     Document Type: Article

References (112)

1. Adamo, A., Collis, S. J., Adelman, C. A., Silva, N., Horejsi, Z., Ward, J. D., Martinez-Perez, E., Boulton, S. J. and La Volpe, A. (2010). Preventing nonhomologous end joining suppresses DNA repair defects of Fanconi anemia. Mol. Cell 39, 25-35.
2. Ahel, I., Ahel, D., Matsusaka, T., Clark, A. J., Pines, J., Boulton, S. J. and West, S. C. (2008). Poly(ADP-ribose)-binding zinc finger motifs in DNA repair/checkpoint proteins. Nature 451, 81-85.
3. 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.
4. Ali, A. A., Jukes, R. M., Pearl, L. H. and Oliver, A.W. (2009). Specific recognition of a multiply phosphorylated motif in the DNA repair scaffold XRCC1 by the FHA domain of human PNK. Nucleic Acids Res. 37, 1701-1712.
5. Altschul, S. F., Madden, T. L., Schä ffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
6. Ame, J.-C., Rolli, V., Schreiber, V., Niedergang, C., Apiou, F., Decker, P., Muller, S., Hoger, T., Murcia, J. M.-d. and de Murcia, G. (1999). PARP-2, a novel mammalian DNA damage-dependent poly(ADP-ribose) polymerase. J. Biol. Chem. 274, 17860-17868.
7. Aravind, L. (2001). The WWE domain: a common interaction module in protein ubiquitination and ADP ribosylation. Trends Biochem Sci. 26, 273-275.
8. Audebert, M., Salles, B. and Calsou, P. (2004). Involvement of poly(ADP-ribose) polymerase-1 and XRCC1/DNA ligase III in an alternative route for DNA doublestrand breaks rejoining. J. Biol. Chem. 279, 55117-55126.
9. 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.
10. Basu, S., Fey, P., Jimenez-Morales, D., Dodson, R. J. and Chisholm, R. L. (2015). dictyBase 2015: expanding data and annotations in a new software environment. Genesis 53, 523-534.
11. Bekker-Jensen, S., Fugger, K., Danielsen, J. R., Gromova, I., Sehested, M., Celis, J., Bartek, J., Lukas, J. and Mailand, N. (2007). Human Xip1 (C2orf13) is a novel regulator of cellular responses to DNA strand breaks. J. Biol. Chem. 282, 19638-19643.
12. Ben-Yehoyada, M., Wang, L. C., Kozekov, I. D., Rizzo, C. J., Gottesman, M. E. and Gautier, J. (2009). Checkpoint signaling from a single DNA interstrand crosslink. Mol. Cell 35, 704-715.
13. Beucher, A., Birraux, J., Tchouandong, L., Barton, O., Shibata, A., Conrad, S., Goodarzi, A. A., Krempler, A., Jeggo, P. A. and Löbrich, M. (2009). ATM and Artemis promote homologous recombination of radiation-induced DNA doublestrand breaks in G2. EMBO J. 28, 3413-3427.
14. Block, W. D. and Lees-Miller, S. P. (2005). Putative homologues of the DNAdependent protein kinase catalytic subunit (DNA-PKcs) and other components of the non-homologous end joining machinery in Dictyostelium discoideum. DNA Repair (Amst) 4, 1061-1065.
15. 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. USA 108, 2783-2788.
16. Brown, M. L., Franco, D., Burkle, A. and Chang, Y. (2002). Role of poly(ADPribosyl) ation in DNA-PKcs-independent V(D)J recombination. Proc. Natl. Acad. Sci. USA 99, 4532-4537.
17. Bryant, H. E., Petermann, E., Schultz, N., Jemth, A.-S., Loseva, O., Issaeva, N., Johansson, F., Fernandez, S., McGlynn, P. and Helleday, T. (2009). PARP is activated at stalled forks to mediate Mre11-dependent replication restart and recombination. EMBO J. 28, 2601-2615.
18. Bunting, S. F., Callén, E., Kozak, M. L., Kim, J. M., Wong, N., López-Contreras, A. J., Ludwig, T., Baer, R., Faryabi, R. B., Malhowski, A. et al. (2012). BRCA1 functions independently of homologous recombination in DNA interstrand crosslink repair. Mol. Cell 46, 125-135.
19. Caldecott, K. W. (2008). Single-strand break repair and genetic disease. Nat. Rev. Genet. 9, 619-631.
20. Chappell, C., Hanakahi, L. A., Karimi-Busheri, F., Weinfeld, M. and West, S. C. (2002). Involvement of human polynucleotide kinase in double-strand break repair by non-homologous end joining. EMBO J. 21, 2827-2832.
21. Chen, D., Vollmar, M., Rossi, M. N., Phillips, C., Kraehenbuehl, R., Slade, D., Mehrotra, P. V., von Delft, F., Crosthwaite, S. K., Gileadi, O. et al. (2011). Identification of macrodomain proteins as novel O-acetyl-ADP-ribose deacetylases. J. Biol. Chem. 286, 13261-13271.
22. Clements, P. M., Breslin, C., Deeks, E. D., Byrd, P. J., Ju, L., Bieganowski, P., Brenner, C., Moreira, M.-C., Taylor, A. M. and Caldecott, K. W. (2004). The ataxia-oculomotor apraxia 1 gene product has a role distinct from ATM and interacts with the DNA strand break repair proteins XRCC1 and XRCC4. DNA Repair (Amst) 3, 1493-1502.
23. Corpet, F. (1988). Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16, 10881-10890.
24. Couto, C. A.-M., Wang, H. yY., Green, J. C. A., Kiely, R., Siddaway, R., Borer, C., Pears, C. J. and Lakin, N. D. (2011). PARP regulates nonhomologous end joining through retention of Ku at double-strand breaks. J. Cell Biol. 194, 367-375.
25. Couto, C. A.-M., Hsu, D.-W., Teo, R., Rakhimova, A., Lempidaki, S., Pears, C. J. and Lakin, N. D. (2013). Nonhomologous end-joining promotes resistance to DNA damage in the absence of an ADP-ribosyltransferase that signals DNA single strand breaks. J. Cell Sci. 126, 3452-3461.
26. de Murcia, J. M., Niedergang, C., Trucco, C., Ricoul, M., Dutrillaux, B., Mark, M., Oliver, F. J., Masson, M., Dierich, A., LeMeur, M. et al. (1997). Requirement of poly(ADP-ribose) polymerase in recovery from DNA damage in mice and in cells. Proc. Natl. Acad. Sci. USA 94, 7303-7307.
27. Dronkert, M. L., de Wit, J., Boeve, M., Vasconcelos, M. L., van Steeg, H., Tan, T. L., Hoeijmakers, J. H. and Kanaar, R. (2000). Disruption of mouse SNM1 causes increased sensitivity to the DNA interstrand cross-linking agent mitomycin C. Mol. Cell Biol. 20, 4553-4561.
28. Ding, R., Pommier, Y., Kang, V. H. and Smulson, M. (1992). Depletion of poly (ADP-ribose) polymerase by antisense RNA expression results in a delay in DNA strand break rejoining. J. Biol. Chem. 267, 12804-12812.
29. Dronkert, M. L. G. and Kanaar, R. (2001). Repair of DNA interstrand cross-links. Mutat. Res. 486, 217-247.
30. Eastman, A. (1983). Characterization of the adducts produced in DNA by cisdiamminedichloroplatinum( II) and cis-dichloro(ethylenediamine)platinum(II). Biochemistry 22, 3927-3933.
31. Eddy, S. R. (1996). Hidden Markov models. Curr. Opin. Struct. Biol. 6, 361-365.
32. Eddy, S. R. (1998). Profile hidden Markov models. Bioinformatics 14, 755-763.
33. Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797.
34. Emsley, P. and Cowtan, K. (2004). Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132.
35. 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.
36. Faix, J., Kreppel, L., Shaulsky, G., Schleicher, M. and Kimmel, A. R. (2004). A rapid and efficient method to generate multiple gene disruptions in Dictyostelium discoideum using a single selectable marker and the Cre-loxP system. Nucleic Acids Res. 32, e143.
37. Fichtinger-Schepman, A. M. J., van der Veer, J. L., den Hartog, J. H. J., Lohman, P. H. M. and Reedijk, J. (1985). Adducts of the antitumor drug cisdiamminedichloroplatinum( II) with DNA: formation, identification, and quantitation. Biochemistry 24, 707-713.
38. Finn, R. D., Clements, J. and Eddy, S. R. (2011). HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 39, W29-W37.
39. Finn, R. D., Coggill, P., Eberhardt, R. Y., Eddy, S. R., Mistry, J., Mitchell, A. L., Potter, S. C., Punta, M., Qureshi, M., Sangrador-Vegas, A. et al. (2016). The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res. 44, D279-D285.
40. Fischer, J. M. F., 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.
41. Fisher, A. E. O., Hochegger, H., Takeda, S. and Caldecott, K. W. (2007). Poly (ADP-ribose) polymerase 1 accelerates single-strand break repair in concert with poly(ADP-ribose) glycohydrolase. Mol. Cell. Biol. 27, 5597-5605.
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. 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.
44. 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. USA 106, 13770-13774.
45. Han, W., Li, X. and Fu, X. (2011). The macro domain protein family: structure, functions, and their potential therapeutic implications. Mutat. Res. 727, 86-103.
46. Henriques, J. A. and Moustacchi, E. (1980). Isolation and characterization of pso mutants sensitive to photo-addition of psoralen derivatives in Saccharomyces cerevisiae. Genetics 95, 273-288.
47. Hottiger, M. O., Hassa, P. O., Lüscher, B., Schüler, H. and Koch-Nolte, F. (2010). Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem. Sci. 35, 208-219.
48. Houghtaling, S., Newell, A., Akkari, Y., Taniguchi, T., Olson, S. and Grompe, M. (2005). Fancd2 functions in a double strand break repair pathway that is distinct from non-homologous end joining. Hum. Mol. Genet. 14, 3027-3033.
49. Hsu, D.-W., Gaudet, P., Hudson, J. J. R., Pears, C. J. and Lakin, N. D. (2006). DNA damage signaling and repair in Dictyostelium discoideum. Cell Cycle 5, 702-708.
50. Hsu, D.-W., Kiely, R., Couto, C. A.-M., Wang, H.-Y., Hudson, J. J. R., Borer, C., Pears, C. J. and Lakin, N. D. (2011). DNA double-strand break repair pathway choice in Dictyostelium. J. Cell Sci. 124, 1655-1663.
51. Hudson, J. J. R., Hsu, D.-W., Guo, K., Zhukovskaya, N., Liu, P.-H., Williams, J. G., Pears, C. J. and Lakin, N. D. (2005). DNA-PKcs-dependent signaling of DNA damage in Dictyostelium discoideum. Curr. Biol. 15, 1880-1885.
52. Iles, N., Rulten, S., El-Khamisy, S. F. and Caldecott, K.W. (2007). APLF (C2orf13) is a novel human protein involved in the cellular response to chromosomal DNA strand breaks. Mol. Cell. Biol. 27, 3793-3803.
53. 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.
54. Jones, D. T. (1999). Protein secondary structure prediction based on positionspecific scoring matrices. J. Mol. Biol. 292, 195-202.
55. Kanno, S.-i., Kuzuoka, H., Sasao, S., Hong, Z., Lan, L., Nakajima, S. and Yasui, A. (2007). A novel human AP endonuclease with conserved zinc-finger-like motifs involved in DNA strand break responses. EMBO J. 26, 2094-2103.
56. Karras, G. I., Kustatscher, G., Buhecha, H. R., Allen, M. D., Pugieux, C., Sait, F., Bycroft, M. and Ladurner, A. G. (2005). The macro domain is an ADP-ribose binding module. EMBO J. 24, 1911-1920.
57. Kottemann, M. C. and Smogorzewska, A. (2013). Fanconi anaemia and the repair of Watson and Crick DNA crosslinks. Nature 493, 356-363.
58. Krishnakumar, R. and Kraus, W. L. (2010). The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Mol. Cell 39, 8-24.
59. Lee, S.-K., Yu, S.-L., Garcia, M. X., Alexander, H. and Alexander, S. (1997). Differential developmental expression of the rep B and rep D xeroderma pigmentosum related DNA helicase genes from Dictyostelium discoideum. Nucleic Acids Res. 25, 2365-2374.
60. Lee, S.-K., Yu, S.-L., Alexander, H. and Alexander, S. (1998). A mutation in repB, the dictyostelium homolog of the human xeroderma pigmentosum B gene, has increased sensitivity to UV-light but normal morphogenesis. Biochim. Biophys. Acta 1399, 161-172.
61. Lehoczky, P., McHugh, P. J. and Chovanec, M. (2007). DNA interstrand cross-link repair in Saccharomyces cerevisiae. FEMS Microbiol. Rev. 31, 109-133.
62. Le Page, F., Schreiber, V., Dherin, C., de Murcia, G. and Boiteux, S. (2003). Poly (ADP-ribose) polymerase-1 (PARP-1) is required in murine cell lines for base excision repair of oxidative DNA damage in the absence of DNA polymerase beta. J. Biol. Chem. 278, 18471-18477.
63. 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. USA 107, 9129-9134.
64. Loizou, J. I., El-Khamisy, S. F., Zlatanou, A., Moore, D. J., Chan, D. W., Qin, J., Sarno, S., Meggio, F., Pinna, L. A. and Caldecott, K. W. (2004). The protein kinase CK2 facilitates repair of chromosomal DNA single-strand breaks. Cell 117, 17-28.
65. 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.
66. Luijsterburg, M. S., de Krijger, I., Wiegant, W. W., Shah, R. G., Smeenk, G., de Groot, A. J. L., Pines, A., Vertegaal, A. C. O., Jacobs, J. J. L., Shah, G. M. et al. (2016). PARP1 links CHD2-mediated chromatin expansion and H3.3 deposition to DNA repair by non-homologous end-joining. Mol. Cell 61, 547-562.
67. Luo, H., Chan, D.W., Yang, T., Rodriguez, M., Chen, B. P.-C., Leng, M., Mu, J.-J., Chen, D., Songyang, Z., Wang, Y. et al. (2004). A new XRCC1-containing complex and its role in cellular survival of methyl methanesulfonate treatment. Mol. Cell. Biol. 24, 8356-8365.
68. Matsutani, M., Nozaki, T., Nishiyama, E., Shimokawa, T., Tachi, Y., Suzuki, H., Nakagama, H., Wakabayashi, K. and Sugimura, T. (1999). Function of poly (ADP-ribose) polymerase in response to DNA damage: Gene-disruption study in mice. Mol. Cell. Biochem. 193, 149-152.
69. McVey, M. (2010). Strategies for DNA interstrand crosslink repair: insights from worms, flies, frogs, and slime molds. Environ. Mol. Mutagen. 51, 646-658.
70. Mehrotra, P. V., Ahel, D., Ryan, D. P., Weston, R., Wiechens, N., Kraehenbuehl, R., Owen-Hughes, T. and Ahel, I. (2011). DNA repair factor APLF is a histone chaperone. Mol. Cell 41, 46-55.
71. Ménissier de Murcia, J., Ricoul, M., Tartier, L., Niedergang, C., Huber, A., Dantzer, F., Schreiber, V., Amé, J. C., Dierich, A., LeMeur, M. et al. (2003). Functional interaction between PARP-1 and PARP-2 in chromosome stability and embryonic development in mouse. EMBO J. 22, 2255-2263.
72. Messner, S. and Hottiger, M. O. (2011). Histone ADP-ribosylation in DNA repair, replication and transcription. Trends Cell Biol. 21, 534-542.
73. Muniandy, P. A., Thapa, D., Thazhathveetil, A. K., Liu, S.-T. and Seidman, M. M. (2009). Repair of laser-localized DNA interstrand cross-links in G1 phase mammalian cells. J. Biol. Chem. 284, 27908-27917.
74. Muramoto, T. and Chubb, J. R. (2008). Live imaging of the Dictyostelium cell cycle reveals widespread S phase during development, a G2 bias in spore differentiation and a premitotic checkpoint. Development 135, 1647-1657.
75. Murshudov, G. N., Vagin, A. A. and Dodson, E. J. (1997). Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255.
76. Nicolae, C. M., Aho, E. R., Choe, K. N., Constantin, D., Hu, H.-J., Lee, D., Myung, K. and Moldovan, G.-L. (2015). A novel role for the mono-ADP-ribosyltransferase PARP14/ARTD8 in promoting homologous recombination and protecting against replication stress. Nucleic Acids Res. 43, 3143-3153.
77. Notredame, C., Higgins, D. G. and Heringa, J. (2000). T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302, 205-217.
78. 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.
79. Pace, P., Mosedale, G., Hodskinson, M. R., Rosado, I. V., Sivasubramaniam, M. and Patel, K. J. (2010). Ku70 corrupts DNA repair in the absence of the Fanconi anemia pathway. Science 329, 219-223.
80. Pears, C. J., Couto, C. A.-M., Wang, H.-Y., Borer, C., Kiely, R. and Lakin, N. D. (2012). The role of ADP-ribosylation in regulating DNA double-strand break repair. Cell Cycle 11, 48-56.
81. Pines, A., Vrouwe, M. G., Marteijn, J. A., Typas, D., Luijsterburg, M. S., Cansoy, M., Hensbergen, P., Deelder, A., de Groot, A., Matsumoto, S. et al. (2012). PARP1 promotes nucleotide excision repair through DDB2 stabilization and recruitment of ALC1. J. Cell Biol. 199, 235-249.
82. Ponting, C. P. and Russell, R. B. (1995). Swaposins: circular permutations within genes encoding saposin homologues. Trends Biochem. Sci. 20, 179-180.
83. Quénet, D., El Ramy, R., Schreiber, V. and Dantzer, F. (2009). The role of poly (ADP-ribosyl)ation in epigenetic events. Int. J. Biochem. Cell Biol. 41, 60-65.
84. Rack, J. G., Perina, D. and Ahel, I. (2016). Macrodomains: structure, function, evolution, and catalytic activities. Annu. Rev. Biochem. 85, 431-454.
85. Robert, I., Dantzer, F. and Reina-San-Martin, B. (2009). Parp1 facilitates alternative NHEJ, whereas Parp2 suppresses IgH/c-myc translocations during immunoglobulin class switch recombination. J. Exp. Med. 206, 1047-1056.
86. Robu, M., Shah, R. G., Petitclerc, N., Brind'Amour, J., Kandan-Kulangara, F. and Shah, G. M. (2013). Role of poly(ADP-ribose) polymerase-1 in the removal of UV-induced DNA lesions by nucleotide excision repair. Proc. Natl. Acad. Sci. USA 110, 1658-1663.
87. Rosenthal, F., Feijs, K. L. H., 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.
88. Rothkamm, K., Kruger, I., Thompson, L. H. and Lobrich, M. (2003). Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol. Cell. Biol. 23, 5706-5715.
89. 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.
90. Rulten, S. L., Fisher, A. E. O., 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.
91. Schreiber, V., Amé, J. C., Dollé, P., Schultz, I., Rinaldi, B., Fraulob, V., Ménissier-de Murcia, J. and de Murcia, G. (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.
92. Sengerová, B., Wang, A. T. and McHugh, P. J. (2011). Orchestrating the nucleases involved in DNA interstrand cross-link (ICL) repair. Cell Cycle 10, 3999-4008.
93. Sharifi, R., Morra, R., Denise Appel, C., 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.
94. 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 mechanismof a poly(ADP-ribose) glycohydrolase. Nature 477, 616-620.
95. Smeaton, M. B., Hlavin, E. M., McGregor Mason, T., Noronha, A. M., Wilds, C. J. and Miller, P. S. (2008). Distortion-dependent unhooking of interstrand crosslinks in mammalian cell extracts. Biochemistry 47, 9920-9930.
96. Soding, J., Biegert, A. and Lupas, A. N. (2005). The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33, W244-W248.
97. Sonnhammer, E. L. L. and Hollich, V. (2005). Scoredist: a simple and robust protein sequence distance estimator. BMC Bioinformatics 6, 108.
98. Storoni, L. C., McCoy, A. J. and Read, R. J. (2004). Likelihood-enhanced fast rotation functions. Acta Crystallogr. D Biol. Crystallogr. 60, 432-438.
99. Sugimura, K., Takebayashi, S.-i., Taguchi, H., Takeda, S. and Okumura, K. (2008). PARP-1 ensures regulation of replication fork progression by homologous recombination on damaged DNA. J. Cell Biol. 183, 1203-1212.
100. Terwilliger, T. C., Adams, P. D., Read, R. J., McCoy, A. J., Moriarty, N. W., Grosse-Kunstleve, R. W., Afonine, P. V., Zwart, P. H. and Hung, L.-W. (2009). Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard. Acta Crystallogr. D Biol. Crystallogr. 65, 582-601.
101. Timinszky, G., Till, S., Hassa, P. O., Hothorn, M., Kustatscher, G., Nijmeijer, B., Colombelli, J., Altmeyer, M., Stelzer, E. H. K., Scheffzek, K. et al. (2009). A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nat. Struct. Mol. Biol. 16, 923-929.
102. Trucco, C., Oliver, F. J., de Murcia, G. and Ménissier-de Murcia, J. (1998). DNA repair defect in poly(ADP-ribose) polymerase-deficient cell lines. Nucleic Acids Res. 26, 2644-2649.
103. 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.
104. Wang, M., Wu, W., Wu, W., Rosidi, B., Zhang, L., Wang, H. and Iliakis, G. (2006). PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res. 34, 6170-6182.
105. Wang, A. T., Sengerova, B., Cattell, E., Inagawa, T., Hartley, J. M., Kiakos, K., Burgess-Brown, N. A., Swift, L. P., Enzlin, J. H., Schofield, C. J. et al. (2011). Human SNM1A and XPF-ERCC1 collaborate to initiate DNA interstrand cross-link repair. Genes Dev 25, 1859-1870.
106. Weijer, C. J., Duschl, G. and David, C. N. (1984). A revision of the Dictyostelium discoideum cell cycle. J. Cell Sci. 70, 111-131.
107. Wilson, D., Pethica, R., Zhou, Y., Talbot, C., Vogel, C., Madera, M., Chothia, C. and Gough, J. (2009). SUPERFAMILY-sophisticated comparative genomics, data mining, visualization and phylogeny. Nucleic Acids Res. 37, D380-D386.
108. Winter, G., Lobley, C. M. C. and Prince, S. M. (2013). Decision making in xia2. Acta Crystallogr. D Biol. Crystallogr. 69, 1260-1273.
109. Wu, C. H., Apweiler, R., Bairoch, A., Natale, D. A., Barker, W. C., Boeckmann, B., Ferro, S., Gasteiger, E., Huang, H., Lopez, R. et al. (2006). The universal protein resource (UniProt): an expanding universe of protein information. Nucleic Acids Res. 34, D187-D191.
110. Yang, Y.-G., Cortes, U., Patnaik, S., Jasin, M. andWang, Z.-Q. (2004). Ablation of PARP-1 does not interfere with the repair of DNA double-strand breaks, but compromises the reactivation of stalled replication forks. Oncogene 23, 3872-3882.
111. Yu, S.-L., Lee, S.-K., Alexander, H. and Alexander, S. (1998). Rapid changes of nucleotide excision repair gene expression following UV-irradiation and cisplatin treatment of Dictyostelium discoideum. Nucleic Acids Res. 26, 3397-3403.
112. Zhang, X.-Y., Langenick, J., Traynor, D., Babu, M. M., Kay, R. R. and Patel, K. J. (2009). Xpf and not the Fanconi anaemia proteins or Rev3 accounts for the extreme resistance to cisplatin in Dictyostelium discoideum. PLoS Genet. 5, e1000645.