Cockayne syndrome group B protein regulates DNA double-strand break repair and checkpoint activation

EMBO Journal

Volumn 34, Issue 10, 2015, Pages 1399-1416

  Batenburg, Nicole L ^a   Thompson, Elizabeth L ^b   Hendrickson, Eric A ^b   Zhu, Xu Dong ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

CSB; DNA damage checkpoint; DNA double strand break repair

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BRCA1 PROTEIN; COCKAYNE SYNDROME GROUP B PROTEIN; DACTINOMYCIN; DOUBLE STRANDED DNA; ETOPOSIDE; GENOMIC DNA; HYBRID PROTEIN; OLAPARIB; PROTEIN; RAD51 PROTEIN; UNCLASSIFIED DRUG; BRAP PROTEIN, HUMAN; DNA HELICASE; DNA LIGASE; ERCC6 PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE;

ALTERNATIVE RNA SPLICING; AMINO ACID SUBSTITUTION; ARTICLE; AUTOPHOSPHORYLATION; CELL FRACTIONATION; CELL SURVIVAL; CHROMATIN; COCKAYNE SYNDROME; CONTROLLED STUDY; DISEASE ASSOCIATION; DNA DAMAGE CHECKPOINT; DNA DOUBLE STRAND BREAK REPAIR; DNA END JOINING REPAIR; DNA REPAIR; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; DRUG SENSITIVITY; EXON; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; G2 PHASE CELL CYCLE CHECKPOINT; GENE ACTIVATION; GENE MUTATION; GENE SILENCING; GENE TARGETING; HELA CELL LINE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IONIZING RADIATION; M PHASE CELL CYCLE CHECKPOINT; MITOSIS; MUTATIONAL ANALYSIS; NONSENSE MUTATION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION; WILD TYPE; BIOLOGICAL MODEL; CELL CULTURE; CELL CYCLE CHECKPOINT; CELL LINE; DNA DAMAGE; GENETICS; KINETICS; METABOLISM; PHYSIOLOGY;

CELL CYCLE CHECKPOINTS; CELL LINE; CELLS, CULTURED; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA HELICASES; DNA REPAIR ENZYMES; HUMANS; KINETICS; MODELS, BIOLOGICAL; UBIQUITIN-PROTEIN LIGASES;

EID: 84929179852     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201490041     Document Type: Article

References (87)

1. Aamann MD, Sorensen MM, Hvitby C, Berquist BR, Muftuoglu M, Tian J, de Souza-Pinto NC, Scheibye-Knudsen M, Wilson DM 3rd, Stevnsner T, Bohr VA, (2010) Cockayne syndrome group B protein promotes mitochondrial DNA stability by supporting the DNA repair association with the mitochondrial membrane. FASEB J 24: 2334-2346
2. Aydin OZ, Marteijn JA, Ribeiro-Silva C, Rodriguez Lopez A, Wijgers N, Smeenk G, van Attikum H, Poot RA, Vermeulen W, Lans H, (2014) Human ISWI complexes are targeted by SMARCA5 ATPase and SLIDE domains to help resolve lesion-stalled transcription. Nucleic Acids Res 42: 8473-8485
3. Aymard F, Bugler B, Schmidt CK, Guillou E, Caron P, Briois S, Iacovoni JS, Daburon V, Miller KM, Jackson SP, Legube G, (2014) Transcriptionally active chromatin recruits homologous recombination at DNA double-strand breaks. Nat Struct Mol Biol 21: 366-374
4. Bakkenist CJ, Kastan MB, (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421: 499-506
5. Batenburg NL, Mitchell TR, Leach DM, Rainbow AJ, Zhu XD, (2012) Cockayne Syndrome group B protein interacts with TRF2 and regulates telomere length and stability. Nucleic Acids Res 40: 9661-9674
6. Bouwman P, Aly A, Escandell JM, Pieterse M, Bartkova J, van der Gulden H, Hiddingh S, Thanasoula M, Kulkarni A, Yang Q, Haffty BG, Tommiska J, Blomqvist C, Drapkin R, Adams DJ, Nevanlinna H, Bartek J, Tarsounas M, Ganesan S, Jonkers J, (2010) 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat Struct Mol Biol 17: 688-695
7. Bunting SF, Callen E, Wong N, Chen HT, Polato F, Gunn A, Bothmer A, Feldhahn N, Fernandez-Capetillo O, Cao L, Xu X, Deng CX, Finkel T, Nussenzweig M, Stark JM, Nussenzweig A, (2010) 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 141: 243-254
8. Burkard ME, Randall CL, Larochelle S, Zhang C, Shokat KM, Fisher RP, Jallepalli PV, (2007) Chemical genetics reveals the requirement for Polo-like kinase 1 activity in positioning RhoA and triggering cytokinesis in human cells. Proc Natl Acad Sci USA 104: 4383-4388
9. Caldecott KW, (2008) Single-strand break repair and genetic disease. Nat Rev Genet 9: 619-631
10. Cao L, Xu X, Bunting SF, Liu J, Wang RH, Cao LL, Wu JJ, Peng TN, Chen J, Nussenzweig A, Deng CX, Finkel T, (2009) A selective requirement for 53BP1 in the biological response to genomic instability induced by Brca1 deficiency. Mol Cell 35: 534-541
11. Carvalho S, Vitor AC, Sridhara SC, Martins FB, Raposo AC, Desterro JM, Ferreira J, de Almeida SF, (2014) SETD2 is required for DNA double-strand break repair and activation of the p53-mediated checkpoint. Elife 3: e02482
12. Chapman JR, Taylor MR, Boulton SJ, (2012) Playing the end game: DNA double-strand break repair pathway choice. Mol Cell 47: 497-510
13. Chapman JR, Barral P, Vannier JB, Borel V, Steger M, Tomas-Loba A, Sartori AA, Adams IR, Batista FD, Boulton SJ, (2013) RIF1 Is essential for 53BP1-dependent nonhomologous end joining and suppression of DNA double-strand break resection. Mol Cell 49: 858-871
14. Chiolo I, Minoda A, Colmenares SU, Polyzos A, Costes SV, Karpen GH, (2011) Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell 144: 732-744
15. Cho I, Tsai PF, Lake RJ, Basheer A, Fan HY, (2013) ATP-dependent chromatin remodeling by Cockayne syndrome protein B and NAP1-like histone chaperones is required for efficient transcription-coupled DNA repair. PLoS Genet 9: e1003407
16. Citterio E, Rademakers S, van der Horst GT, van Gool AJ, Hoeijmakers JH, Vermeulen W, (1998) Biochemical and biological characterization of wild-type and ATPase-deficient Cockayne syndrome B repair protein. J Biol Chem 273: 11844-11851
17. Citterio E, Van Den Boom V, Schnitzler G, Kanaar R, Bonte E, Kingston RE, Hoeijmakers JH, Vermeulen W, (2000) ATP-dependent chromatin remodeling by the Cockayne syndrome B DNA repair-transcription-coupling factor. Mol Cell Biol 20: 7643-7653
18. Daley JM, Sung P, (2014) 53BP1, BRCA1, and the choice between recombination and end joining at DNA double-strand breaks. Mol Cell Biol 34: 1380-1388
19. Dang LH, Chen F, Ying C, Chun SY, Knock SA, Appelman HD, Dang DT, (2006) CDX2 has tumorigenic potential in the human colon cancer cell lines LOVO and SW48. Oncogene 25: 2264-2272
20. Dhawan A, Anderson D, de Pascual-Teresa S, Santos-Buelga C, Clifford MN, Ioannides C, (2002) Evaluation of the antigenotoxic potential of monomeric and dimeric flavanols, and black tea polyphenols against heterocyclic amine-induced DNA damage in human lymphocytes using the Comet assay. Mut Res 515: 39-56
21. Di Nicolantonio F, Arena S, Gallicchio M, Zecchin D, Martini M, Flonta SE, Stella GM, Lamba S, Cancelliere C, Russo M, Geuna M, Appendino G, Fantozzi R, Medico E, Bardelli A, (2008) Replacement of normal with mutant alleles in the genome of normal human cells unveils mutation-specific drug responses. Proc Natl Acad Sci USA 105: 20864-20869
22. Di Virgilio M, Callen E, Yamane A, Zhang W, Jankovic M, Gitlin AD, Feldhahn N, Resch W, Oliveira TY, Chait BT, Nussenzweig A, Casellas R, Robbiani DF, Nussenzweig MC, (2013) Rif1 prevents resection of DNA breaks and promotes immunoglobulin class switching. Science 339: 711-715
23. Elli R, Chessa L, Antonelli A, Petrinelli P, Ambra R, Marcucci L, (1996) Effects of topoisomerase II inhibition in lymphoblasts from patients with progeroid and "chromosome instability" syndromes. Cancer Genet Cytogenet 87: 112-116
24. Escribano-Diaz C, Orthwein A, Fradet-Turcotte A, Xing M, Young JT, Tkac J, Cook MA, Rosebrock AP, Munro M, Canny MD, Xu D, Durocher D, (2013) A cell cycle-dependent regulatory circuit composed of 53BP1-Rif1 and BRCA1-CtIP controls DNA repair pathway choice. Mol Cell 49: 872-883
25. Fattah F, Lee EH, Weisensel N, Wang Y, Lichter N, Hendrickson EA, (2010) Ku regulates the non-homologous end joining pathway choice of DNA double-strand break repair in human somatic cells. PLoS Genet 6: e1000855
26. Feng L, Fong KW, Wang J, Wang W, Chen J, (2013) RIF1 counteracts BRCA1-mediated end resection during DNA repair. J Biol Chem 288: 11135-11143
27. Goodarzi AA, Jeggo P, Lobrich M, (2010) The influence of heterochromatin on DNA double strand break repair: getting the strong, silent type to relax. DNA Repair 9: 1273-1282
28. Gottipati P, Helleday T, (2009) Transcription-associated recombination in eukaryotes: link between transcription, replication and recombination. Mutagenesis 24: 203-210
29. Hashimoto S, Suga T, Kudo E, Ihn H, Uchino M, Tateishi S, (2008) Adult-onset neurological degeneration in a patient with Cockayne syndrome and a null mutation in the CSB gene. J Invest Dermatol 128: 1597-1599
30. Horibata K, Iwamoto Y, Kuraoka I, Jaspers NG, Kurimasa A, Oshimura M, Ichihashi M, Tanaka K, (2004) Complete absence of Cockayne syndrome group B gene product gives rise to UV-sensitive syndrome but not Cockayne syndrome. Proc Natl Acad Sci USA 101: 15410-15415
31. van der Horst GT, van Steeg H, Berg RJ, van Gool AJ, de Wit J, Weeda G, Morreau H, Beems RB, van Kreijl CF, de Gruijl FR, Bootsma D, Hoeijmakers JH, (1997) Defective transcription-coupled repair in Cockayne syndrome B mice is associated with skin cancer predisposition. Cell 89: 425-435
32. Hucl T, Rago C, Gallmeier E, Brody JR, Gorospe M, Kern SE, (2008) A syngeneic variance library for functional annotation of human variation: application to BRCA2. Cancer Res 68: 5023-5030
33. Huertas P, Jackson SP, (2009) Human CtIP mediates cell cycle control of DNA end resection and double strand break repair. J Biol Chem 284: 9558-9565
34. Iyama T, Lee SY, Berquist BR, Gileadi O, Bohr VA, Seidman MM, McHugh PJ, Wilson DM 3rd, (2015) CSB interacts with SNM1A and promotes DNA interstrand crosslink processing. Nucleic Acids Res 43: 247-258
35. Jha DK, Strahl BD, (2014) An RNA polymerase II-coupled function for histone H3K36 methylation in checkpoint activation and DSB repair. Nat Commun 5: 3965
36. Kan Y, Ruis B, Lin S, Hendrickson EA, (2014) The mechanism of gene targeting in human somatic cells. PLoS Genet 10: e1004251
37. Kohli M, Rago C, Lengauer C, Kinzler KW, Vogelstein B, (2004) Facile methods for generating human somatic cell gene knockouts using recombinant adeno-associated viruses. Nucleic Acids Res 32: e3
38. Kotin RM, Linden RM, Berns KI, (1992) Characterization of a preferred site on human chromosome 19q for integration of adeno-associated virus DNA by non-homologous recombination. EMBO J 11: 5071-5078
39. Lake RJ, Geyko A, Hemashettar G, Zhao Y, Fan HY, (2010) UV-induced association of the CSB remodeling protein with chromatin requires ATP-dependent relief of N-terminal autorepression. Mol Cell 37: 235-246
40. Lan L, Ui A, Nakajima S, Hatakeyama K, Hoshi M, Watanabe R, Janicki SM, Ogiwara H, Kohno T, Kanno S, Yasui A, (2010) The ACF1 complex is required for DNA double-strand break repair in human cells. Mol Cell 40: 976-987
41. Laugel V, Dalloz C, Stary A, Cormier-Daire V, Desguerre I, Renouil M, Fourmaintraux A, Velez-Cruz R, Egly JM, Sarasin A, Dollfus H, (2008) Deletion of 5′ sequences of the CSB gene provides insight into the pathophysiology of Cockayne syndrome. Eur J Hum Genet 16: 320-327
42. Leadon SA, Cooper PK, (1993) Preferential repair of ionizing radiation-induced damage in the transcribed strand of an active human gene is defective in Cockayne syndrome. Proc Natl Acad Sci USA 90: 10499-10503
43. Lee JH, Paull TT, (2004) Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science 304: 93-96
44. Lee JH, Paull TT, (2005) ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 308: 551-554
45. Lukas J, Lukas C, Bartek J, (2011) More than just a focus: the chromatin response to DNA damage and its role in genome integrity maintenance. Nat Cell Biol 13: 1161-1169
46. McKerlie M, Zhu XD, (2011) Cyclin B-dependent kinase 1 regulates human TRF1 to modulate the resolution of sister telomeres. Nat Commun 2: 371
47. McKerlie M, Lin S, Zhu XD, (2012) ATM regulates proteasome-dependent subnuclear localization of TRF1, which is important for telomere maintenance. Nucleic Acids Res 40: 3975-3989
48. McKerlie M, Walker JR, Mitchell TR, Wilson FR, Zhu XD, (2013) Phosphorylated (pT371)TRF1 is recruited to sites of DNA damage to facilitate homologous recombination and checkpoint activation. Nucleic Acids Res 41: 10268-10282
49. Mitchell TR, Glenfield K, Jeyanthan K, Zhu XD, (2009) Arginine methylation regulates telomere length and stability. Mol Cell Biol 29: 4918-4934
50. Mitchell TR, Zhu XD, (2014) Methylated TRF2 associates with the nuclear matrix and serves as a potential biomarker for cellular senescence. Aging (Albany NY) 6: 248-263
51. Newman JC, Bailey AD, Weiner AM, (2006) Cockayne syndrome group B protein (CSB) plays a general role in chromatin maintenance and remodeling. Proc Natl Acad Sci USA 103: 9613-9618
52. Newman JC, Bailey AD, Fan HY, Pavelitz T, Weiner AM, (2008) An abundant evolutionarily conserved CSB-PiggyBac fusion protein expressed in Cockayne syndrome. PLoS Genet 4: e1000031
53. Oh S, Wang Y, Zimbric J, Hendrickson EA, (2013) Human LIGIV is synthetically lethal with the loss of Rad54B-dependent recombination and is required for certain chromosome fusion events induced by telomere dysfunction. Nucleic Acids Res 41: 1734-1749
54. Pai CC, Deegan RS, Subramanian L, Gal C, Sarkar S, Blaikley EJ, Walker C, Hulme L, Bernhard E, Codlin S, Bahler J, Allshire R, Whitehall S, Humphrey TC, (2014) A histone H3K36 chromatin switch coordinates DNA double-strand break repair pathway choice. Nat Commun 5: 4091
55. Panier S, Boulton SJ, (2014) Double-strand break repair: 53BP1 comes into focus. Nat Rev Mol Cell Biol 15: 7-18
56. Pfister SX, Ahrabi S, Zalmas LP, Sarkar S, Aymard F, Bachrati CZ, Helleday T, Legube G, La Thangue NB, Porter AC, Humphrey TC, (2014) SETD2-dependent histone H3K36 trimethylation is required for homologous recombination repair and genome stability. Cell Rep 7: 2006-2018
57. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM, (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273: 5858-5868
58. Rogakou EP, Boon C, Redon C, Bonner WM, (1999) Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146: 905-916
59. Ruis BL, Fattah KR, Hendrickson EA, (2008) The catalytic subunit of DNA-dependent protein kinase regulates proliferation, telomere length, and genomic stability in human somatic cells. Mol Cell Biol 28: 6182-6195
60. Ryan AJ, Squires S, Strutt HL, Johnson RT, (1991) Camptothecin cytotoxicity in mammalian cells is associated with the induction of persistent double strand breaks in replicating DNA. Nucleic Acids Res 19: 3295-3300
61. Sakai A, Sakasai R, Kakeji Y, Kitao H, Maehara Y, (2012) PARP and CSB modulate the processing of transcription-mediated DNA strand breaks. Genes Genet Syst 87: 265-272
62. Sakasai R, Teraoka H, Takagi M, Tibbetts RS, (2010) Transcription-dependent activation of ataxia telangiectasia mutated prevents DNA-dependent protein kinase-mediated cell death in response to topoisomerase I poison. J Biol Chem 285: 15201-15208
63. Savolainen L, Cassel T, Helleday T, (2010) The XPD subunit of TFIIH is required for transcription-associated but not DNA double-strand break-induced recombination in mammalian cells. Mutagenesis 25: 623-629
64. Scheibye-Knudsen M, Ramamoorthy M, Sykora P, Maynard S, Lin PC, Minor RK, Wilson DM 3rd, Cooper M, Spencer R, de Cabo R, Croteau DL, Bohr VA, (2012) Cockayne syndrome group B protein prevents the accumulation of damaged mitochondria by promoting mitochondrial autophagy. J Exp Med 209: 855-869
65. Seluanov A, Mittelman D, Pereira-Smith OM, Wilson JH, Gorbunova V, (2004) DNA end joining becomes less efficient and more error-prone during cellular senescence. Proc Natl Acad Sci USA 101: 7624-7629
66. Selzer RR, Nyaga S, Tuo J, May A, Muftuoglu M, Christiansen M, Citterio E, Brosh RM Jr, Bohr VA, (2002) Differential requirement for the ATPase domain of the Cockayne syndrome group B gene in the processing of UV-induced DNA damage and 8-oxoguanine lesions in human cells. Nucleic Acids Res 30: 782-793
67. Shen M, Zhou T, Xie W, Ling T, Zhu Q, Zong L, Lyu G, Gao Q, Zhang F, Tao W, (2013) The chromatin remodeling factor CSB recruits histone acetyltransferase PCAF to rRNA gene promoters in active state for transcription initiation. PLoS ONE 8: e62668
68. Shiloh Y, (2003) ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer 3: 155-168
69. Sollier J, Stork CT, Garcia-Rubio ML, Paulsen RD, Aguilera A, Cimprich KA, (2014) Transcription-coupled nucleotide excision repair factors promote R-loop-induced genome instability. Mol Cell 56: 777-785
70. Squires S, Ryan AJ, Strutt HL, Johnson RT, (1993) Hypersensitivity of Cockayne's syndrome cells to camptothecin is associated with the generation of abnormally high levels of double strand breaks in nascent DNA. Cancer Res 53: 2012-2019
71. Stevnsner T, Muftuoglu M, Aamann MD, Bohr VA, (2008) The role of Cockayne Syndrome group B (CSB) protein in base excision repair and aging. Mech Ageing Dev 129: 441-448
72. Thorslund T, von Kobbe C, Harrigan JA, Indig FE, Christiansen M, Stevnsner T, Bohr VA, (2005) Cooperation of the Cockayne syndrome group B protein and poly(ADP-ribose) polymerase 1 in the response to oxidative stress. Mol Cell Biol 25: 7625-7636
73. Troelstra C, van Gool A, de Wit J, Vermeulen W, Bootsma D, Hoeijmakers JH, (1992) ERCC6, a member of a subfamily of putative helicases, is involved in Cockayne's syndrome and preferential repair of active genes. Cell 71: 939-953
74. Tuo J, Jaruga P, Rodriguez H, Dizdaroglu M, Bohr VA, (2002) The cockayne syndrome group B gene product is involved in cellular repair of 8-hydroxyadenine in DNA. J Biol Chem 277: 30832-30837
75. Tuo J, Jaruga P, Rodriguez H, Bohr VA, Dizdaroglu M, (2003) Primary fibroblasts of Cockayne syndrome patients are defective in cellular repair of 8-hydroxyguanine and 8-hydroxyadenine resulting from oxidative stress. FASEB J 17: 668-674
76. Velez-Cruz R, Egly JM, (2013) Cockayne syndrome group B (CSB) protein: at the crossroads of transcriptional networks. Mech Ageing Dev 134: 234-242
77. Veuger SJ, Curtin NJ, Richardson CJ, Smith GC, Durkacz BW, (2003) 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 63: 6008-6015
78. Wong HK, Muftuoglu M, Beck G, Imam SZ, Bohr VA, Wilson DM 3rd, (2007) Cockayne syndrome B protein stimulates apurinic endonuclease 1 activity and protects against agents that introduce base excision repair intermediates. Nucleic Acids Res 35: 4103-4113
79. Wu Y, Xiao S, Zhu XD, (2007a) MRE11-RAD50-NBS1 and ATM function as co-mediators of TRF1 in telomere length control. Nat Struct Mol Biol 14: 832-840
80. Wu Y, Zacal NJ, Rainbow AJ, Zhu XD, (2007b) XPF with mutations in its conserved nuclease domain is defective in DNA repair but functions in TRF2-mediated telomere shortening. DNA Repair (Amst) 6: 157-166
81. Wu Y, Mitchell TR, Zhu XD, (2008) Human XPF controls TRF2 and telomere length maintenance through distinctive mechanisms. Mech Ageing Dev 129: 602-610
82. Xie A, Hartlerode A, Stucki M, Odate S, Puget N, Kwok A, Nagaraju G, Yan C, Alt FW, Chen J, Jackson SP, Scully R, (2007) Distinct roles of chromatin-associated proteins MDC1 and 53BP1 in mammalian double-strand break repair. Mol Cell 28: 1045-1057
83. Xie W, Ling T, Zhou Y, Feng W, Zhu Q, Stunnenberg HG, Grummt I, Tao W, (2012) The chromatin remodeling complex NuRD establishes the poised state of rRNA genes characterized by bivalent histone modifications and altered nucleosome positions. Proc Natl Acad Sci USA 109: 8161-8166
84. Yuan X, Feng W, Imhof A, Grummt I, Zhou Y, (2007) Activation of RNA polymerase I transcription by cockayne syndrome group B protein and histone methyltransferase G9a. Mol Cell 27: 585-595
85. Zhu XD, Kuster B, Mann M, Petrini JH, Lange T, (2000) Cell-cycle-regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres. Nat Genet 25: 347-352
86. Zhu XD, Niedernhofer L, Kuster B, Mann M, Hoeijmakers JH, de Lange T, (2003) ERCC1/XPF removes the 3′ overhang from uncapped telomeres and represses formation of telomeric DNA-containing double minute chromosomes. Mol Cell 12: 1489-1498
87. Zimmermann M, Lottersberger F, Buonomo SB, Sfeir A, de Lange T, (2013) 53BP1 regulates DSB repair using Rif1 to control 5′ end resection. Science 339: 700-704