Functional characterization of the TERRA transcriptome at damaged telomeres

Nature Communications

Volumn 5, Issue , 2014, Pages

  Porro, Antonio ^a,b,e   Feuerhahn, Sascha ^a,b,e   Delafontaine, Julien ^a,c   Riethman, Harold ^d   Rougemont, Jacques ^a,c   Lingner, Joachim ^a,b  

^a EPFL   (Switzerland)

^b SWISS INST FOR EXP CANCER RESEARCH   (Switzerland)

^c SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^d WISTAR INSTITUTE   (United States)

^e UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE METHYLTRANSFERASE; INTERFERON REGULATORY FACTOR; MYOGENIC FACTOR; SHORT HAIRPIN RNA; TERRA TRANSCRIPTOME; TRANSCRIPTION FACTOR; TRANSCRIPTOME; UNCLASSIFIED DRUG; HISTONE ACETYLTRANSFERASE; KAT5 PROTEIN, HUMAN; LONG UNTRANSLATED RNA; METHYLTRANSFERASE; REPRESSOR PROTEIN; SUV39H1 PROTEIN, HUMAN; TELOMERIC REPEAT BINDING FACTOR 2; TERF2 PROTEIN, HUMAN;

DNA; ENZYME ACTIVITY;

ARTICLE; CHROMATIN; CHROMOSOME; COLORECTAL CARCINOMA; CONTROLLED STUDY; CPG ISLAND; DNA BASE COMPOSITION; DNA BINDING; DNA DAMAGE; HELA CELL LINE; HIGH THROUGHPUT SEQUENCING; HISTONE METHYLATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MITOSIS INHIBITION; NORTHERN BLOTTING; PROTEIN PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA HYBRIDIZATION; RNA TRANSCRIPTION; SIGNAL TRANSDUCTION; TELOMERE; TRANSCRIPTION INITIATION SITE; UPREGULATION; WESTERN BLOTTING; GENE EXPRESSION PROFILING; METABOLISM; PROTEIN TERTIARY STRUCTURE;

DNA DAMAGE; GENE EXPRESSION PROFILING; HELA CELLS; HISTONE ACETYLTRANSFERASES; HUMANS; METHYLTRANSFERASES; PROTEIN STRUCTURE, TERTIARY; REPRESSOR PROTEINS; RNA, LONG NONCODING; TELOMERE; TELOMERIC REPEAT BINDING PROTEIN 2; TRANSCRIPTOME; UP-REGULATION;

EID: 84923355398     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6379     Document Type: Article

References (63)

1. Cann, K. L. & Dellaire, G. Heterochromatin and the DNA damage response: the need to relax. Biochem. Cell Biol. 89, 45-60 (2011).
2. Ward, G. K., Stewart, S. S., Price, G. B. & Mackillop, W. J. Cellular heterogeneity in normal human urothelium: quantitative studies of lectin binding. Histochem. J. 19, 337-344 (1987).
3. Shanbhag, N. M., Rafalska-Metcalf, I. U., Balane-Bolivar, C., Janicki, S. M. & Greenberg, R. A. ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell 141, 970-981 (2010).
4. Price, B. D. & D'Andrea, A. D. Chromatin remodeling at DNA double-strand breaks. Cell 152, 1344-1354 (2013).
5. Greenberg, R. A. Histone tails: directing the chromatin response to DNA damage. FEBS Lett. 585, 2883-2890 (2011).
6. Goodarzi, A. A. et al. ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol. Cell 31, 167-177 (2008).
7. Ayoub, N., Jeyasekharan, A. D., Bernal, J. A. & Venkitaraman, A. R. HP1-beta mobilization promotes chromatin changes that initiate the DNA damage response. Nature 453, 682-686 (2008).
8. Murr, R. et al. Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat. Cell Biol. 8, 91-99 (2006).
9. Bird, A. W. et al. Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature 419, 411-415 (2002).
10. Sun, Y. et al. Histone H3 methylation links DNA damage detection to activation of the tumour suppressor Tip60. Nat. Cell Biol. 11, 1376-1382 (2009).
11. Sun, Y., Xu, Y., Roy, K. & Price, B. D. DNA damage-induced acetylation of lysine 3016 of ATM activates ATM kinase activity. Mol. Cell. Biol. 27, 8502-8509 (2007).
12. Kaidi, A. & Jackson, S. P. KAT5 tyrosine phosphorylation couples chromatin sensing to ATM signalling. Nature 498, 70-74 (2013).
13. Benetti, R. et al. Suv4-20h deficiency results in telomere elongation and derepression of telomere recombination. J. Cell Biol. 178, 925-936 (2007).
14. Hewitt, G. et al. Telomeres are favoured targets of a persistent DNA damage response in ageing and stress-induced senescence. Nat. Commun. 3, 708 (2012).
15. Fumagalli, M. et al. Telomeric DNA damage is irreparable and causes persistent DNA-damage-response activation. Nat. Cell Biol. 14, 355-365 (2012).
16. de Lange, T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19, 2100-2110 (2005).
17. de Lange, T. How telomeres solve the end-protection problem. Science 326, 948-952 (2009).
18. Denchi, E. L. & de Lange, T. Protection of telomeres through independent control of ATM and ATR by TRF2 and POT1. Nature 448, 1068-1071 (2007).
19. Sharpless, N. E. & DePinho, R. A. Cancer: crime and punishment. Nature 436, 636-637 (2005).
20. Feldser, D. M. & Greider, C. W. Short telomeres limit tumor progression in vivo by inducing senescence. Cancer Cell 11, 461-469 (2007).
21. Cosme-Blanco, W. et al. Telomere dysfunction suppresses spontaneous tumorigenesis in vivo by initiating p53-dependent cellular senescence. EMBO Rep. 8, 497-503 (2007).
22. d'Adda di Fagagna, F. et al. A DNA damage checkpoint response in telomereinitiated senescence. Nature 426, 194-198 (2003).
23. Azzalin, C. M., Reichenbach, P., Khoriauli, L., Giulotto, E. & Lingner, J. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 318, 798-801 (2007).
24. Schoeftner, S. & Blasco, M. A. Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat. Cell Biol. 10, 228-236 (2008).
25. Nergadze, S. G. et al. CpG-island promoters drive transcription of human telomeres. RNA 15, 2186-2194 (2009).
26. Yehezkel, S., Segev, Y., Viegas-Pequignot, E., Skorecki, K. & Selig, S. Hypomethylation of subtelomeric regions in ICF syndrome is associated with abnormally short telomeres and enhanced transcription from telomeric regions. Hum. Mol. Genet. 17, 2776-2789 (2008).
27. Arnoult, N., Van Beneden, A. & Decottignies, A. Telomere length regulates TERRA levels through increased trimethylation of telomeric H3K9 and HP1alpha. Nat. Struct. Mol. Biol. 19, 948-956 (2012).
28. Porro, A., Feuerhahn, S., Reichenbach, P. & Lingner, J. Molecular dissection of telomeric repeat-containing RNA biogenesis unveils the presence of distinct and multiple regulatory pathways. Mol. Cell. Biol. 30, 4808-4817 (2010).
29. Deng, Z., Norseen, J., Wiedmer, A., Riethman, H. & Lieberman, P. M. TERRA RNA binding to TRF2 facilitates heterochromatin formation and ORC recruitment at telomeres. Mol. Cell 35, 403-413 (2009).
30. Hayashi, M. T., Cesare, A. J., Fitzpatrick, J. A., Lazzerini-Denchi, E. & Karlseder, J. A telomere-dependent DNA damage checkpoint induced by prolonged mitotic arrest. Nat. Struct. Mol. Biol. 19, 387-394 (2012).
31. Stong, N. et al. Subtelomeric CTCF and cohesin binding site organization using improved subtelomere assemblies and a novel annotation pipeline. Genome Res. 24, 1039-1050 (2014).
32. Deng, Z. et al. A role for CTCF and cohesin in subtelomere chromatin organization, TERRA transcription, and telomere end protection. EMBO J. 31, 4165-4178 (2012).
33. Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L. & Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621-628 (2008).
34. Hann, S. R. & Eisenman, R. N. Proteins encoded by the human c-myc oncogene: differential expression in neoplastic cells. Mol. Cell. Biol. 4, 2486-2497 (1984).
35. King, M. W., Roberts, J. M. & Eisenman, R. N. Expression of the c-myc proto-oncogene during development of Xenopus laevis. Mol. Cell. Biol. 6, 4499-4508 (1986).
36. Waters, C.M., Littlewood, T. D., Hancock, D. C., Moore, J. P. & Evan, G. I. c-myc protein expression in untransformed fibroblasts. Oncogene 6, 797-805 (1991).
37. Yamashita, A., Ohnishi, T., Kashima, I., Taya, Y. & Ohno, S. Human SMG-1, a novel phosphatidylinositol 3-kinase-related protein kinase, associates with components of the mRNA surveillance complex and is involved in the regulation of nonsense-mediated mRNA decay. Genes Dev. 15, 2215-2228 (2001).
38. Brumbaugh, K. M. et al. The mRNA surveillance protein hSMG-1 functions in genotoxic stress response pathways in mammalian cells. Mol. Cell 14, 585-598 (2004).
39. Bunz, F. et al. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282, 1497-1501 (1998).
40. Fairall, L., Chapman, L., Moss, H., de Lange, T. & Rhodes, D. Structure of the TRFH dimerization domain of the human telomeric proteins TRF1 and TRF2. Mol. Cell 8, 351-361 (2001).
41. Baker, A. M. et al. The telomere binding protein TRF2 induces chromatin compaction. PLoS ONE 6, e19124 (2011).
42. Poulet, A. et al. The N-terminal domains of TRF1 and TRF2 regulate their ability to condense telomeric DNA. Nucleic Acids Res. 40, 2566-2576 (2012).
43. Broccoli, D., Smogorzewska, A., Chong, L. & de Lange, T. Human telomeres contain two distinct Myb-related proteins, TRF1 and TRF2. Nat. Genet. 17, 231-235 (1997).
44. Okamoto, K. et al. A two-step mechanism for TRF2-mediated chromosomeend protection. Nature 494, 502-505 (2013).
45. Grolimund, L. et al. A quantitative telomeric chromatin isolation protocol identifies different telomeric states. Nat. Commun. 4, 2848 (2013).
46. Bartocci, C. et al. Isolation of chromatin from dysfunctional telomeres reveals an important role for Ring1b in NHEJ-mediated chromosome fusions. Cell Rep. 7, 1320-1332 (2014).
47. Caslini, C., Connelly, J. A., Serna, A., Broccoli, D. & Hess, J. L. MLL associates with telomeres and regulates telomeric repeat-containing RNA transcription. Mol. Cell. Biol. 29, 4519-4526 (2009).
48. de Lange, T. T-loops and the origin of telomeres. Nat. Rev. Mol. Cell Biol. 5, 323-329 (2004).
49. Doksani, Y., Wu, J. Y., de Lange, T. & Zhuang, X. Super-resolution fluorescence imaging of telomeres reveals TRF2-dependent T-loop formation. Cell 155, 345-356 (2013).
50. Porro, A., Feuerhahn, S. & Lingner, J. TERRA-reinforced association of LSD1 with MRE11 promotes processing of uncapped telomeres. Cell Rep. 6, 765-776 (2014).
51. Abreu, E. et al. TIN2-tethered TPP1 recruits human telomerase to telomeres in vivo. Mol. Cell. Biol. 30, 2971-2982 (2010).
52. Xu, L. & Blackburn, E. H. Human cancer cells harbor T-stumps, a distinct class of extremely short telomeres. Mol. Cell 28, 315-327 (2007).
53. Azzalin, C. M. & Lingner, J. The human RNA surveillance factor UPF1 is required for S phase progression and genome stability. Curr. Biol. 16, 433-439 (2006).
54. McKerlie, M. & Zhu, X. D. Cyclin B-dependent kinase 1 regulates human TRF1 to modulate the resolution of sister telomeres. Nat. Commun. 2, 371 (2011).
55. Crabbe, L., Cesare, A. J., Kasuboski, J. M., Fitzpatrick, J. A. & Karlseder, J. Human telomeres are tethered to the nuclear envelope during postmitotic nuclear assembly. Cell Rep. 2, 1521-1529 (2012).
56. Liu, B. et al. Depleting the methyltransferase Suv39h1 improves DNA repair and extends lifespan in a progeria mouse model. Nat. Commun. 4, 1868 (2013).
57. Ayrapetov, M. K., Gursoy-Yuzugullu, O., Xu, C., Xu, Y. & Price, B. D. DNA double-strand breaks promote methylation of histone H3 on lysine 9 and transient formation of repressive chromatin. Proc. Natl Acad. Sci. USA 111, 9169-9174 (2014).
58. Magoc, T. & Salzberg, S. L. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957-2963 (2011).
59. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memoryefficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
60. David, F. P. et al. HTSstation: a web application and open-access libraries for high-throughput sequencing data analysis. PLoS ONE 9, e85879 (2014).
61. Youngman, S. et al. The telomeric 60 kb of chromosome arm 4p is homologous to telomeric regions on 13p, 15p, 21p, and 22p. Genomics 14, 350-356 (1992).
62. Chawla, R. et al. Human UPF1 interacts with TPP1 and telomerase and sustains telomere leading-strand replication. EMBO J. 30, 4047-4058 (2011).
63. Celli, G. B. & de Lange, T. DNA processing is not required for ATM-mediated telomere damage response after TRF2 deletion. Nat. Cell Biol. 7, 712-718 (2005).