TERRA biogenesis, turnover and implications for function

FEBS Letters

Volumn 584, Issue 17, 2010, Pages 3812-3818

  Feuerhahn, Sascha ^a   Iglesias, Nahid ^a   Panza, Andrea ^a   Porro, Antonio ^a   Lingner, Joachim ^a  

^a EPFL   (Switzerland)

Author keywords

Non coding RNA; Telomerase; Telomere; TERRA

Indexed keywords

DNA; TELOMERASE; TELOMERIC REPEAT CONTAINING RNA; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

BIOGENESIS; DNA REPLICATION; ENZYME REGULATION; HETEROCHROMATIN; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; RNA DEGRADATION; RNA METABOLISM; RNA STRUCTURE; RNA SYNTHESIS; RNA TRANSCRIPTION; TELOMERE;

ANIMALS; CHROMATIN; CHROMOSOMES; DNA DAMAGE; DNA REPLICATION; HETEROCHROMATIN; HUMANS; KINETICS; MAMMALS; NEOPLASMS; RNA; RNA, UNTRANSLATED; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; TELOMERASE; TELOMERE; TRANSCRIPTION, GENETIC;

EUKARYOTA;

EID: 77955844757     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2010.07.032     Document Type: Review

References (68)

1. de Lange T. How telomeres solve the end-protection problem. Science 2009, 326:948-952.
2. Greider C.W., Blackburn E.H. Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 1985, 43:405-413.
3. Greider C.W., Blackburn E.H. A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature 1989, 337:331-337.
4. Lingner J., Hughes T.R., Shevchenko A., Mann M., Lundblad V., Cech T.R. Reverse transcriptase motifs in the catalytic subunit of telomerase. Science 1997, 276:561-567.
5. Bodnar A.G., et al. Extension of life-span by introduction of telomerase into normal human cells. Science 1998, 279:349-352.
6. Kim N.W., et al. Specific association of human telomerase activity with immortal cells and cancer. Science 1994, 266:2011-2015.
7. Azzalin C.M., Reichenbach P., Khoriauli L., Giulotto E., Lingner J. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 2007, 318:798-801.
8. Schoeftner S., Blasco M.A. Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat. Cell Biol. 2008, 10:228-236.
9. Luke B., Panza A., Redon S., Iglesias N., Li Z., Lingner J. The Rat1p 5' to 3' exonuclease degrades telomeric repeat-containing RNA and promotes telomere elongation in Saccharomyces cerevisiae. Mol. Cell 2008, 32:465-477.
10. Vrbsky J., Akimcheva S., Watson J.M., Turner T.L., Daxinger L., Vyskot B., Aufsatz W., Riha K. SiRNA-mediated methylation of Arabidopsis telomeres. PLoS Genet. 2010, 6:e1000986.
11. Luke B., Lingner J. TERRA: telomeric repeat-containing RNA. EMBO J. 2009, 28:2503-2510.
12. Azzalin C.M., Lingner J. Telomeres: the silence is broken. Cell Cycle 2008, 7:1161-1165.
13. Xu Y., Kimura T., Komiyama M. Human telomere RNA and DNA form an intermolecular G-quadruplex. Nucleic Acids Symp. Ser. (Oxf) 2008, 169:70.
14. Martadinata H., Phan A.T. Structure of propeller-type parallel-stranded RNA G-quadruplexes, formed by human telomeric RNA sequences in K+ solution. J. Am. Chem. Soc. 2009, 131:2570-2578.
15. Randall A., Griffith J.D. Structure of long telomeric RNA transcripts: the G-rich RNA forms a compact repeating structure containing G-quartets. J. Biol. Chem. 2009, 284:13980-13986.
16. Collie, G.W., Haider, S.M., Neidle, S. and Parkinson, G.N. (2010) A crystallographic and modelling study of a human telomeric RNA (TERRA) quadruplex. Nucleic Acids Res., Epub ahead of print.
17. Lipps H.J., Rhodes D. G-quadruplex structures: in vivo evidence and function. Trends Cell Biol. 2009, 19:414-422.
18. Nergadze S.G., Farnung B.O., Wischnewski H., Khoriauli L., Vitelli V., Chawla R., Giulotto E., Azzalin C.M. CpG-island promoters drive transcription of human telomeres. RNA 2009, 15:2186-2194.
19. 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. 2009, 29:4519-4526.
20. Jones B., et al. The histone H3K79 methyltransferase Dot1L is essential for mammalian development and heterochromatin structure. PLoS Genet. 2008, 4:e1000190.
21. Marcand S., Gilson E., Shore D. A protein-counting mechanism for telomere length regulation in yeast. Science 1997, 275:986-990.
22. Marcand S., Pardo B., Gratias A., Cahun S., Callebaut I. Multiple pathways inhibit NHEJ at telomeres. Genes Dev. 2008, 22:1153-1158.
23. Gottschling D.E., Aparicio O.M., Billington B.L., Zakian V.A. Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell 1990, 63:751-762.
24. Shore D. Telomeric chromatin: replicating and wrapping up chromosome ends. Curr. Opin. Genet. Dev. 2001, 11:189-198.
25. Chan C.S., Tye B.K. Organization of DNA sequences and replication origins at yeast telomeres. Cell 1983, 33:563-573.
26. Walmsley R.W., Chan C.S., Tye B.K., Petes T.D. Unusual DNA sequences associated with the ends of yeast chromosomes. Nature 1984, 310:157-160.
27. Louis E.J. The chromosome ends of Saccharomyces cerevisiae. Yeast 1995, 11:1553-1573.
28. Pryde F.E., Louis E.J. Limitations of silencing at native yeast telomeres. EMBO J. 1999, 18:2538-2550.
29. Zhu X., Gustafsson C.M. Distinct differences in chromatin structure at subtelomeric X and Y' elements in budding yeast. PLoS One 2009, 4:e6363.
30. Sfeir A., Kabir S., van Overbeek M., Celli G.B., de Lange T. Loss of Rap1 induces telomere recombination in the absence of NHEJ or a DNA damage signal. Science 2010, 327:1657-1661.
31. Li B., Oestreich S., de Lange T. Identification of human Rap1: implications for telomere evolution. Cell 2000, 101:471-483.
32. Silverman J., Takai H., Buonomo S.B., Eisenhaber F., de Lange T. Human Rif1, ortholog of a yeast telomeric protein, is regulated by ATM and 53BP1 and functions in the S-phase checkpoint. Genes Dev. 2004, 18:2108-2119.
33. 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. 2008, 17:2776-2789.
34. Dehe P.M., Geli V. The multiple faces of Set1. Biochem. Cell Biol. 2006, 84:536-548.
35. Goldberg A.D., et al. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 2010, 140:678-691.
36. LaCava J., Houseley J., Saveanu C., Petfalski E., Thompson E., Jacquier A., Tollervey D. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 2005, 121:713-724.
37. Vanacova S., et al. A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol. 2005, 3:e189.
38. Isken O., Maquat L.E. Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA function. Genes Dev. 2007, 21:1833-1856.
39. Baker K.E., Parker R. Nonsense-mediated mRNA decay: terminating erroneous gene expression. Curr. Opin. Cell Biol. 2004, 16:293-299.
40. Luke B., Azzalin C.M., Hug N., Deplazes A., Peter M., Lingner J. Saccharomyces cerevisiae Ebs1p is a putative ortholog of human Smg7 and promotes nonsense-mediated mRNA decay. Nucleic Acids Res. 2007, 35:7688-7697.
41. Sayani S., Janis M., Lee C.Y., Toesca I., Chanfreau G.F. Widespread impact of nonsense-mediated mRNA decay on the yeast intronome. Mol. Cell 2008, 31:360-370.
42. Azzalin C.M., Lingner J. The human RNA surveillance factor UPF1 is required for S phase progression and genome stability. Curr. Biol. 2006, 16:433-439.
43. He F., Brown A.H., Jacobson A. Interaction between Nmd2p and Upf1p is required for activity but not for dominant-negative inhibition of the nonsense-mediated mRNA decay pathway in yeast. RNA 1996, 2:153-170.
44. Shirley R.L., Lelivelt M.J., Schenkman L.R., Dahlseid J.N., Culbertson M.R. A factor required for nonsense-mediated mRNA decay in yeast is exported from the nucleus to the cytoplasm by a nuclear export signal sequence. J. Cell Sci. 1998, 111(Pt 21):3129-3143.
45. Dahlseid J.N., et al. MRNAs encoding telomerase components and regulators are controlled by UPF genes in Saccharomyces cerevisiae. Eukaryot. Cell 2003, 2:134-142.
46. Enomoto S., Glowczewski L., Lew-Smith J., Berman J.G. Telomere cap components influence the rate of senescence in telomerase-deficient yeast cells. Mol. Cell. Biol. 2004, 24:837-845.
47. Miller K.M., Rog O., Cooper J.P. Semi-conservative DNA replication through telomeres requires Taz1. Nature 2006, 440:824-828.
48. Sfeir A., Kosiyatrakul S.T., Hockemeyer D., MacRae S.L., Karlseder J., Schildkraut C.L., de Lange T. Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell 2009, 138:90-103.
49. Mirkin S.M. DNA structures, repeat expansions and human hereditary disorders. Curr. Opin. Struct. Biol. 2006, 16:351-358.
50. Gilson E., Geli V. How telomeres are replicated. Nat. Rev. Mol. Cell Biol. 2007, 8:825-838.
51. McCord R.A., Broccoli D. Telomeric chromatin: roles in aging, cancer and hereditary disease. Mutat. Res. 2008, 647:86-93.
52. Carastro L.M., Tan C.K., Selg M., Jack H.M., So A.G., Downey K.M. 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. 2002, 30:2232-2243.
53. Snow B.E., Erdmann N., Cruickshank J., Goldman H., Gill R.M., Robinson M.O., Harrington L. Functional conservation of the telomerase protein Est1p in humans. Curr. Biol. 2003, 13:698-704.
54. Redon S., Reichenbach P., Lingner J. Protein RNA and protein-protein interactions mediate association of human EST1A/SMG6 with telomerase. Nucleic Acids Res. 2007, 35:7011-7022.
55. Reichenbach P., Hoss M., Azzalin C.M., Nabholz M., Bucher P., Lingner J. A human homolog of yeast Est1 associates with telomerase and uncaps chromosome ends when overexpressed. Curr. Biol. 2003, 13:568-574.
56. 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 2009, 35:403-413.
57. Ho C.Y., Murnane J.P., Yeung A.K., Ng H.K., Lo A.W. Telomeres acquire distinct heterochromatin characteristics during siRNA-induced RNA interference in mouse cells. Curr. Biol. 2008, 18:183-187.
58. Li G.Z., Eller M.S., Firoozabadi R., Gilchrest B.A. Evidence that exposure of the telomere 3' overhang sequence induces senescence. Proc. Natl. Acad. Sci. USA 2003, 100:527-531.
59. Benetti R., Gonzalo S., Jaco I., Schotta G., Klatt P., Jenuwein T., Blasco M.A. Suv4-20h deficiency results in telomere elongation and derepression of telomere recombination. J. Cell Biol. 2007, 178:925-936.
60. Blasco M.A. The epigenetic regulation of mammalian telomeres. Nat. Rev. Genet. 2007, 8:299-309.
61. Zhao J., Sun B.K., Erwin J.A., Song J.J., Lee J.T. Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 2008, 322:750-756.
62. Kuramochi-Miyagawa S., et al. DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev. 2008, 22:908-917.
63. Aravin A.A., Sachidanandam R., Bourc'his D., Schaefer C., Pezic D., Toth K.F., Bestor T., Hannon G.J. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol. Cell 2008, 31:785-799.
64. Cao F., Li X., Hiew S., Brady H., Liu Y., Dou Y. Dicer independent small RNAs associate with telomeric heterochromatin. RNA 2009, 15:1274-1281.
65. Zhao Y., Sfeir A.J., Zou Y., Buseman C.M., Chow T.T., Shay J.W., Wright W.E. Telomere extension occurs at most chromosome ends and is uncoupled from fill-in in human cancer cells. Cell 2009, 138:463-475.
66. Redon, S., Reichenbach, P. and Lingner, J. (2010) The non-coding RNA TERRA is a natural ligand and direct inhibitor of human telomerase. Nucleic Acids Res., Epub ahead of print.
67. Zaug A.J., Podell E.R., Cech T.R. Mutation in TERT separates processivity from anchor-site function. Nat. Struct. Mol. Biol. 2008, 15:870-872.
68. Sandell L.L., Gottschling D.E., Zakian V.A. Transcription of a yeast telomere alleviates telomere position effect without affecting chromosome stability. Proc. Natl. Acad. Sci. USA 1994, 91:12061-12065.