Molecular dissection of telomeric repeat-containing RNA biogenesis unveils the presence of distinct and multiple regulatory pathways

Molecular and Cellular Biology

Volumn 30, Issue 20, 2010, Pages 4808-4817

  Porro, Antonio ^a   Feuerhahn, Sascha ^a   Reichenbach, Patrick ^a   Lingner, Joachim ^a  

^a EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CAPPED RNA; MESSENGER RNA; RNA;

ARTICLE; BIOSYNTHESIS; CELL CYCLE; CELL FRACTIONATION; CELL LINE; GENETICS; HELA CELL; HUMAN; METABOLISM; NUCLEOTIDE SEQUENCE; RNA PROCESSING; RNA STABILITY; TANDEM REPEAT; TELOMERE;

BASE SEQUENCE; CELL CYCLE; CELL LINE; HELA CELLS; HUMANS; RNA; RNA CAPS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; RNA, MESSENGER; SUBCELLULAR FRACTIONS; TANDEM REPEAT SEQUENCES; TELOMERE;

EID: 78049386911     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00460-10     Document Type: Article

References (50)

1. Artandi, S. E., and R. A. DePinho. 2010. Telomeres and telomerase in cancer. Carcinogenesis 31:9-18.
2. Azzalin, C. M., and J. Lingner. 2008. Telomeres: the silence is broken. Cell Cycle 7:1161-1165.
3. Azzalin, C. M., and J. Lingner. 2006. The human RNA surveillance factor UPF1 is required for S phase progression and genome stability. Curr. Biol. 16:433-439.
4. Azzalin, C. M., P. Reichenbach, L. Khoriauli, E. Giulotto, and J. Lingner. 2007. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 318:798-801.
5. Baird, D. M., A. J. Jeffreys, and N. J. Royle. 1995. Mechanisms underlying telomere repeat turnover, revealed by hypervariable variant repeat distribution patterns in the human Xp/Yp telomere. EMBO J. 14:5433-5443.
6. Belotserkovskii, B. P., R. Liu, S. Tornaletti, M. M. Krasilnikova, S. M. Mirkin, and P. C. Hanawalt. 2010. Mechanisms and implications of transcription blockage by guanine-rich DNA sequences. Proc. Natl. Acad. Sci. U. S. A. 107:12816-12821.
7. Bodnar, A. G., M. Ouellette, M. Frolkis, S. E. Holt, C. P. Chiu, G. B. Morin, C. B. Harley, J. W. Shay, S. Lichtsteiner, and W. E. Wright. 1998. Extension of life-span by introduction of telomerase into normal human cells. Science 279:349-352.
8. Brockdorff, N., and S. M. Duthie. 1998. X chromosome inactivation and the Xist gene. Cell. Mol. Life Sci. 54:104-112.
9. Brown, S. D. 1991. XIST and the mapping of the X chromosome inactivation centre. Bioessays 13:607-612.
10. Carastro, L. M., C. K. Tan, M. Selg, H. M. Jack, A. G. So, and K. M. Downey. 2002. Identification of delta helicase as the bovine homolog of HUPF1: demonstration of an interaction with the third subunit of DNA polymerase delta. Nucleic Acids Res. 30:2232-2243.
11. Chanfreau, G., G. Rotondo, P. Legrain, and A. Jacquier. 1998. Processing of a dicistronic small nucleolar RNA precursor by the RNA endonuclease Rnt1. EMBO J. 17:3726-3737.
12. Choi, Y. H., and C. H. Hagedorn. 2003. Purifying mRNAs with a high-affinity eIF4E mutant identifies the short 3' poly(A) end phenotype. Proc. Natl. Acad. Sci. U. S. A. 100:7033-7038.
13. Clemson, C. M., J. N. Hutchinson, S. A. Sara, A. W. Ensminger, A. H. Fox, A. Chess, and J. B. Lawrence. 2009. An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Mol. Cell 33:717-726.
14. Cougot, N., E. van Dijk, S. Babajko, and B. Seraphin. 2004. 'Cap-tabolism.' Trends Biochem. Sci. 29:436-444.
15. Cristofari, G., and J. Lingner. 2006. Telomere length homeostasis requires that telomerase levels are limiting. EMBO J. 25:565-574.
16. d'Adda di Fagagna, F., P. M. Reaper, L. Clay-Farrace, H. Fiegler, P. Carr, T. Von Zglinicki, G. Saretzki, N. P. Carter, and S. P. Jackson. 2003. A DNA damage checkpoint response in telomere-initiated senescence. Nature 426: 194-198.
17. de Lange, T. 2009. How telomeres solve the end-protection problem. Science 326:948-952.
18. de Lange, T. 2005. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19:2100-2110.
19. de Lange, T., L. Shiue, R. M. Myers, D. R. Cox, S. L. Naylor, A. M. Killery, and H. E. Varmus. 1990. Structure and variability of human chromosome ends. Mol. Cell. Biol. 10:518-527.
20. Deng, Z., A. E. Campbell, and P. M. Lieberman. 2010. TERRA, CpG methylation and telomere heterochromatin: lessons from ICF syndrome cells. Cell Cycle 9:69-74.
21. Deng, Z., J. Norseen, A. Wiedmer, H. Riethman, and P. M. Lieberman. 2009. TERRA RNA binding to TRF2 facilitates heterochromatin formation and ORC recruitment at telomeres. Mol. Cell 35:403-413.
22. Greider, C. W., and E. H. Blackburn. 1989. A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature 337:331-337.
23. Greider, C. W., and E. H. Blackburn. 1985. Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43:405- 413.
24. Hann, S. R., and R. N. Eisenman. 1984. Proteins encoded by the human c-myc oncogene: differential expression in neoplastic cells. Mol. Cell. Biol. 4:2486-2497.
25. Jia, D., L. Cai, H. He, G. Skogerbo, T. Li, M. N. Aftab, and R. Chen. 2007. Systematic identification of non-coding RNA 2,2,7-trimethylguanosine cap structures in Caenorhabditis elegans. BMC Mol. Biol. 8:86.
26. Kim, S. H., P. Kaminker, and J. Campisi. 2002. Telomeres, aging and cancer: in search of a happy ending. Oncogene 21:503-511.
27. King, M. W., J. M. Roberts, and R. N. Eisenman. 1986. Expression of the c-myc proto-oncogene during development of Xenopus laevis. Mol. Cell. Biol. 6:4499-4508.
28. LaCava, J., J. Houseley, C. Saveanu, E. Petfalski, E. Thompson, A. Jacquier, and D. Tollervey. 2005. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121:713-724.
29. Lingner, J., T. R. Hughes, A. Shevchenko, M. Mann, V. Lundblad, and T. R. Cech. 1997. Reverse transcriptase motifs in the catalytic subunit of telomerase. Science 276:561-567.
30. '-end labeling of RNA with recombinant yeast poly(A) polymerase. Nucleic Acids Res. 21:2917-2920.
31. Luke, B., A. Panza, S. Redon, N. Iglesias, Z. Li, and J. Lingner. 2008. The Rat1p 5 to 3 exonuclease degrades telomeric repeat-containing RNA and promotes telomere elongation in Saccharomyces cerevisiae. Mol. Cell 32: 465-477.
32. Nergadze, S. G., B. O. Farnung, H. Wischnewski, L. Khoriauli, V. Vitelli, R. Chawla, E. Giulotto, and C. M. Azzalin. 2009. CpG-island promoters drive transcription of human telomeres. RNA 15:2186-2194.
33. Neugebauer, K. M. 2002. On the importance of being co-transcriptional. J. Cell Sci. 115:3865-3871.
34. Proudfoot, N. J., A. Furger, and M. J. Dye. 2002. Integrating mRNA processing with transcription. Cell 108:501-512.
35. Redon, S., P. Reichenbach, and J. Lingner. 2007. Protein RNA and protein protein interactions mediate association of human EST1A/SMG6 with telomerase. Nucleic Acids Res. 35:7011-7022.
36. Redon, S., P. Reichenbach, and J. Lingner. 11 May 2010. The noncoding RNA TERRA is a natural ligand and direct inhibitor of human telomerase. Nucleic Acids Res. [Epub ahead of print.]
37. Reichenbach, P., M. Hoss, C. M. Azzalin, M. Nabholz, P. Bucher, and J. Lingner. 2003. A human homolog of yeast Est1 associates with telomerase and uncaps chromosome ends when overexpressed. Curr. Biol. 13: 568-574.
38. Riethman, H. 2008. Human telomere structure and biology. Annu. Rev. Genomics Hum. Genet. 9:1-19.
39. Sandell, L. L., D. E. Gottschling, and V. A. Zakian. 1994. Transcription of a yeast telomere alleviates telomere position effect without affecting chromosome stability. Proc. Natl. Acad. Sci. U. S. A. 91:12061-12065.
40. Schoeftner, S., and M. A. Blasco. 2008. Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat. Cell Biol. 10:228-236.
41. Shatkin, A. J. 1976. Capping of eucaryotic mRNAs. Cell 9:645-653.
42. Snow, B. E., N. Erdmann, J. Cruickshank, H. Goldman, R. M. Gill, M. O. Robinson, and L. Harrington. 2003. Functional conservation of the telomerase protein Est1p in humans. Curr. Biol. 13:698-704.
43. Vanacova, S., and R. Stefl. 2007. The exosome and RNA quality control in the nucleus. EMBO Rep. 8:651-657.
44. Vanacova, S., J. Wolf, G. Martin, D. Blank, S. Dettwiler, A. Friedlein, H. Langen, G. Keith, and W. Keller. 2005. A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol. 3:e189.
45. Waters, C. M., T. D. Littlewood, D. C. Hancock, J. P. Moore, and G. I. Evan. 1991. c-myc protein expression in untransformed fibroblasts. Oncogene 6:797-805.
46. Wellinger, R. J., K. Ethier, P. Labrecque, and V. A. Zakian. 1996. Evidence for a new step in telomere maintenance. Cell 85:423-433.
47. Wellinger, R. J., and D. Sen. 1997. The DNA structures at the ends of eukaryotic chromosomes. Eur. J. Cancer 33:735-749.
48. Wyers, F., M. Rougemaille, G. Badis, J. C. Rousselle, M. E. Dufour, J. Boulay, B. Regnault, F. Devaux, A. Namane, B. Seraphin, D. Libri, and A. Jacquier. 2005. Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121: 725-737.
49. Xu, Y., K. Kaminaga, and M. Komiyama. 2008. G-quadruplex formation by human telomeric repeats-containing RNA in Na+ solution. J. Am. Chem. Soc. 130:11179-11184.
50. Yehezkel, S., Y. Segev, E. Viegas-Pequignot, K. Skorecki, and S. Selig. 2008. 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.