Identification of TERRA locus unveils a telomere protection role through association to nearly all chromosomes

Nature Communications

Volumn 5, Issue , 2014, Pages

  De Silanes, Isabel López ^a   Graña, Osvaldo ^a   De Bonis, Maria Luigia ^a   Dominguez, Orlando ^a   Pisano, David G ^a   Blasco, Maria A ^a  

^a Centro Nacional de Investigations Oncológicas   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

RNA BINDING PROTEIN; TELOMERIC RIBONUCLEIC ACID; UNCLASSIFIED DRUG; LUCIFERASE; MESSENGER RNA; PROTEIN BINDING; TRANSCRIPTION FACTOR;

ABUNDANCE; CHROMOSOME; GENOME; RNA; RODENT;

ANIMAL CELL; ARTICLE; CELL CYCLE; CHROMOSOME 18; CHROMOSOME 9; CONTROLLED STUDY; EMBRYO; GENE LOCUS; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; RNA ANALYSIS; RNA SEQUENCE; RNA STRUCTURE; TELOMERE; TRANSCRIPTION INITIATION; TRANSCRIPTION INITIATION SITE; ANIMAL; ANIMAL EMBRYO; CHEMISTRY; CHROMOSOME; CYTOLOGY; FIBROBLAST; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; GENETICS; GENOME; HIGH THROUGHPUT SEQUENCING; METABOLISM; NUCLEOTIDE REPEAT; PRIMARY CELL CULTURE; REPORTER GENE;

ANIMALS; CELL CYCLE; CHROMOSOMES, MAMMALIAN; EMBRYO, MAMMALIAN; FIBROBLASTS; GENE EXPRESSION; GENES, REPORTER; GENETIC LOCI; GENOME; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; IN SITU HYBRIDIZATION, FLUORESCENCE; LUCIFERASES; MICE; PRIMARY CELL CULTURE; PROTEIN BINDING; REPETITIVE SEQUENCES, NUCLEIC ACID; RNA, MESSENGER; RNA-BINDING PROTEINS; TELOMERE; TRANSCRIPTION FACTORS;

EID: 84907345142     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5723     Document Type: Article

References (33)

1. Blasco, M. A. The epigenetic regulation of mammalian telomeres. Nat. Rev. Genet. 8, 299-309 (2007).
2. 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).
3. Schoeftner, S. & Blasco, M. A. Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat. Cell Biol. 10, 228-236 (2008).
4. Nergadze, S. G. et al. CpG-island promoters drive transcription of human telomeres. RNA 15, 2186-2194 (2009).
5. Luke, B. & Lingner, J. TERRA: telomeric repeat-containing RNA. EMBO J. 28, 2503-2510 (2009).
6. Feuerhahn, S., Iglesias, N., Panza, A., Porro, A. & Lingner, J. TERRA biogenesis, turnover and implications for function. FEBS Lett. 584, 3812-3818 (2010).
7. Lopez de Silanes, I., Stagno d'Alcontres, M. & Blasco, M. A. TERRA transcripts are bound by a complex array of RNA-binding proteins. Nat. Commun. 1, 33 (2010).
8. Farnung, B. O., Brun, C. M., Arora, R., Lorenzi, L. E. & Azzalin, C. M. Telomerase efficiently elongates highly transcribing telomeres in human cancer cells. PLoS One 7, e35714 (2012).
9. Arora, R., Brun, C. M. & Azzalin, C. M. Transcription regulates telomere dynamics in human cancer cells. RNA 18, 684-693 (2012).
10. 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).
11. 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).
12. Pfeiffer, V. & Lingner, J. TERRA promotes telomere shortening through exonuclease 1-mediated resection of chromosome ends. PLoS Genet. 8, e1002747 (2012).
13. Flynn, R. L. et al. TERRA and hnRNPA1 orchestrate an RPA-to-POT1 switch on telomeric single-stranded DNA. Nature 471, 532-536 (2011).
14. Cusanelli, E., Romero, C. A. & Chartrand, P. Telomeric noncoding RNA TERRA is induced by telomere shortening to nucleate telomerase molecules at short telomeres. Mol. Cell 51, 780-791 (2013).
15. Redon, S., Reichenbach, P. & Lingner, J. The non-coding RNA TERRA is a natural ligand and direct inhibitor of human telomerase. Nucleic Acids Res. 38, 5797-5806 (2010).
16. Lal, A., Kawai, T., Yang, X., Mazan-Mamczarz, K. & Gorospe, M. Antiapoptotic function of RNA-binding protein HuR effected through prothymosin alpha. EMBO J. 24, 1852-1862 (2005).
17. Marion, R. M. et al. Telomeres acquire embryonic stem cell characteristics in induced pluripotent stem cells. Cell Stem Cell 4, 141-154 (2009).
18. de Lange, T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19, 2100-2110 (2005).
19. 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).
20. Wang, W. et al. HuR regulates p21 mRNA stabilization by UV light. Mol. Cell. Biol. 20, 760-769 (2000).
21. Mellon, I., Spivak, G. & Hanawalt, P. C. Selective removal of transcriptionblocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell 51, 241-249 (1987).
22. ENCODE-Project-Consortium. A user's guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol. 9, e1001046 (2011).
23. Stamatoyannopoulos, J. A. et al. An encyclopedia of mouse DNA elements (Mouse ENCODE). Genome Biol. 13, 418 (2012).
24. Bah, A., Wischnewski, H., Shchepachev, V. & Azzalin, C. M. The telomeric transcriptome of Schizosaccharomyces pombe. Nucleic Acids Res. 40, 2995-3005 (2012).
25. Deng, Z. et al. Formation of telomeric repeat-containing RNA (TERRA) foci in highly proliferating mouse cerebellar neuronal progenitors and medulloblastoma. J. Cell Sci. 125, 4383-4394 (2012).
26. Schoeftner, S. & Blasco, M. A. Chromatin regulation and non-coding RNAs at mammalian telomeres. Semin. Cell Dev. Biol. 21, 186-193 (2010).
27. De Bonis, M. L., Ortega, S. & Blasco, M. A. SIRT1 Is Necessary for Proficient Telomere Elongation and Genomic Stability of Induced Pluripotent Stem Cells. Stem Cell Rep. 2, 690-706 (2014).
28. Blelloch, R., Venere, M., Yen, J. & Ramalho-Santos, M. Generation of induced pluripotent stem cells in the absence of drug selection. Cell Stem Cell 1, 245-247 (2007).
29. Trapnell, C. et al. Differential gene and transcript expression analysis of RNAseq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562-578 (2012).
30. 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).
31. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
32. Kent, W. J. et al. The human genome browser at UCSC. Genome Res. 12, 996-1006 (2002).
33. Saez, B. et al. Identification of recurrent chromosomal breakpoints in multiple myeloma with complex karyotypes by combined G-banding, spectral karyotyping, and fluorescence in situ hybridization analyses. Cancer Genet. Cytogenet. 169, 143-149 (2006).