A Polyadenylation-Dependent 3′ End Maturation Pathway Is Required for the Synthesis of the Human Telomerase RNA

Cell Reports

Volumn 13, Issue 10, 2015, Pages 2244-2257

  Nguyen, Duy ^a   Grenier St Sauveur, Valérie ^a   Bergeron, Danny ^a   Dupuis Sandoval, Fabien ^a   Scott, Michelle S ^a   Bachand, François ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DYSKERIN; HOLOENZYME; POLY(A) SPECIFIC RNASE; POLYADENYLIC ACID BINDING PROTEIN; RIBONUCLEASE; RNA; TELOMERASE; UNCLASSIFIED DRUG; EXORIBONUCLEASE; PABPN1 PROTEIN, HUMAN; POLY(A)-SPECIFIC RIBONUCLEASE; TELOMERASE RNA;

ARTICLE; BINDING AFFINITY; BIOGENESIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; EXOSOME; FLUORESCENCE IN SITU HYBRIDIZATION; GENETIC CONSERVATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INTRON; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; RESTRICTION FRAGMENT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA DEGRADATION; RNA SYNTHESIS; SCHIZOSACCHAROMYCES POMBE; SIGNAL TRANSDUCTION; TRANSCRIPTION TERMINATION; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

BLOTTING, WESTERN; EXORIBONUCLEASES; HEK293 CELLS; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION, FLUORESCENCE; POLY(A)-BINDING PROTEIN I; POLYADENYLATION; POLYMERASE CHAIN REACTION; RNA; TELOMERASE;

EID: 84982954679     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.11.003     Document Type: Article

References (52)

1. Artandi, S.E., DePinho, R.A., Telomeres and telomerase in cancer. Carcinogenesis 31 (2010), 9–18.
2. Bachand, F., Autexier, C., Functional regions of human telomerase reverse transcriptase and human telomerase RNA required for telomerase activity and RNA-protein interactions. Mol. Cell. Biol. 21 (2001), 1888–1897.
3. Bachand, F., Silver, P.A., PRMT3 is a ribosomal protein methyltransferase that affects the cellular levels of ribosomal subunits. EMBO J. 23 (2004), 2641–2650.
4. Bachand, F., Boisvert, F.M., Côté, J., Richard, S., Autexier, C., The product of the survival of motor neuron (SMN) gene is a human telomerase-associated protein. Mol. Biol. Cell 13 (2002), 3192–3202.
5. Beattie, T.L., Zhou, W., Robinson, M.O., Harrington, L., Reconstitution of human telomerase activity in vitro. Curr. Biol. 8 (1998), 177–180.
6. Beaulieu, Y.B., Kleinman, C.L., Landry-Voyer, A.M., Majewski, J., Bachand, F., Polyadenylation-dependent control of long noncoding RNA expression by the poly(A)-binding protein nuclear 1. PLoS Genet., 8, 2012, e1003078.
7. Bergeron, D., Pal, G., Beaulieu, Y.B., Chabot, B., Bachand, F., Regulated Intron Retention and Nuclear Pre-mRNA Decay Contribute to PABPN1 Autoregulation. Mol. Cell. Biol. 35 (2015), 2503–2517.
8. Berndt, H., Harnisch, C., Rammelt, C., Stöhr, N., Zirkel, A., Dohm, J.C., Himmelbauer, H., Tavanez, J.P., Hüttelmaier, S., Wahle, E., Maturation of mammalian H/ACA box snoRNAs: PAPD5-dependent adenylation and PARN-dependent trimming. RNA 18 (2012), 958–972.
9. Bresson, S.M., Conrad, N.K., The human nuclear poly(a)-binding protein promotes RNA hyperadenylation and decay. PLoS Genet., 9, 2013, e1003893.
10. Bryan, T.M., Marusic, L., Bacchetti, S., Namba, M., Reddel, R.R., The telomere lengthening mechanism in telomerase-negative immortal human cells does not involve the telomerase RNA subunit. Hum. Mol. Genet. 6 (1997), 921–926.
11. Calado, A., Kutay, U., Kühn, U., Wahle, E., Carmo-Fonseca, M., Deciphering the cellular pathway for transport of poly(A)-binding protein II. RNA 6 (2000), 245–256.
12. Chlebowski, A., Lubas, M., Jensen, T.H., Dziembowski, A., RNA decay machines: the exosome. Biochim. Biophys. Acta 1829 (2013), 552–560.
13. Cristofari, G., Adolf, E., Reichenbach, P., Sikora, K., Terns, R.M., Terns, M.P., Lingner, J., Human telomerase RNA accumulation in Cajal bodies facilitates telomerase recruitment to telomeres and telomere elongation. Mol. Cell 27 (2007), 882–889.
14. Darzacq, X., Kittur, N., Roy, S., Shav-Tal, Y., Singer, R.H., Meier, U.T., Stepwise RNP assembly at the site of H/ACA RNA transcription in human cells. J. Cell Biol. 173 (2006), 207–218.
15. Dieci, G., Preti, M., Montanini, B., Eukaryotic snoRNAs: a paradigm for gene expression flexibility. Genomics 94 (2009), 83–88.
16. Egan, E.D., Collins, K., Biogenesis of telomerase ribonucleoproteins. RNA 18 (2012), 1747–1759.
17. Fasken, M.B., Leung, S.W., Banerjee, A., Kodani, M.O., Chavez, R., Bowman, E.A., Purohit, M.K., Rubinson, M.E., Rubinson, E.H., Corbett, A.H., Air1 zinc knuckles 4 and 5 and a conserved IWRXY motif are critical for the function and integrity of the Trf4/5-Air1/2-Mtr4 polyadenylation (TRAMP) RNA quality control complex. J. Biol. Chem. 286 (2011), 37429–37445.
18. Freund, A., Zhong, F.L., Venteicher, A.S., Meng, Z., Veenstra, T.D., Frydman, J., Artandi, S.E., Proteostatic control of telomerase function through TRiC-mediated folding of TCAB1. Cell 159 (2014), 1389–1403.
19. Göhring, J., Fulcher, N., Jacak, J., Riha, K., TeloTool: a new tool for telomere length measurement from terminal restriction fragment analysis with improved probe intensity correction. Nucleic Acids Res., 42, 2014, e21.
20. Goldfarb, K.C., Cech, T.R., 3′ terminal diversity of MRP RNA and other human noncoding RNAs revealed by deep sequencing. BMC Mol. Biol., 14, 2013, 23.
21. Grzechnik, P., Kufel, J., Polyadenylation linked to transcription termination directs the processing of snoRNA precursors in yeast. Mol. Cell 32 (2008), 247–258.
22. Jády, B.E., Bertrand, E., Kiss, T., Human telomerase RNA and box H/ACA scaRNAs share a common Cajal body-specific localization signal. J. Cell Biol. 164 (2004), 647–652.
23. Kim, N.W., Piatyszek, M.A., Prowse, K.R., Harley, C.B., West, M.D., Ho, P.L., Coviello, G.M., Wright, W.E., Weinrich, S.L., Shay, J.W., Specific association of human telomerase activity with immortal cells and cancer. Science 266 (1994), 2011–2015.
24. Kim, M., Vasiljeva, L., Rando, O.J., Zhelkovsky, A., Moore, C., Buratowski, S., Distinct pathways for snoRNA and mRNA termination. Mol. Cell 24 (2006), 723–734.
25. Kimura, M., Stone, R.C., Hunt, S.C., Skurnick, J., Lu, X., Cao, X., Harley, C.B., Aviv, A., Measurement of telomere length by the Southern blot analysis of terminal restriction fragment lengths. Nat. Protoc. 5 (2010), 1596–1607.
26. Kiss, T., Fayet-Lebaron, E., Jády, B.E., Box H/ACA small ribonucleoproteins. Mol. Cell 37 (2010), 597–606.
27. Körner, C.G., Wahle, E., Poly(A) tail shortening by a mammalian poly(A)-specific 3′-exoribonuclease. J. Biol. Chem. 272 (1997), 10448–10456.
28. Larochelle, M., Lemay, J.F., Bachand, F., The THO complex cooperates with the nuclear RNA surveillance machinery to control small nucleolar RNA expression. Nucleic Acids Res. 40 (2012), 10240–10253.
29. Lemay, J.F., D'Amours, A., Lemieux, C., Lackner, D.H., St-Sauveur, V.G., Bähler, J., Bachand, F., The nuclear poly(A)-binding protein interacts with the exosome to promote synthesis of noncoding small nucleolar RNAs. Mol. Cell 37 (2010), 34–45.
30. Lemay, J.F., Larochelle, M., Marguerat, S., Atkinson, S., Bähler, J., Bachand, F., The RNA exosome promotes transcription termination of backtracked RNA polymerase II. Nat. Struct. Mol. Biol. 21 (2014), 919–926.
31. Lubas, M., Christensen, M.S., Kristiansen, M.S., Domanski, M., Falkenby, L.G., Lykke-Andersen, S., Andersen, J.S., Dziembowski, A., Jensen, T.H., Interaction profiling identifies the human nuclear exosome targeting complex. Mol. Cell 43 (2011), 624–637.
32. Mitchell, J.R., Cheng, J., Collins, K., A box H/ACA small nucleolar RNA-like domain at the human telomerase RNA 3′ end. Mol. Cell. Biol. 19 (1999), 567–576.
33. Mitchell, J.R., Wood, E., Collins, K., A telomerase component is defective in the human disease dyskeratosis congenita. Nature 402 (1999), 551–555.
34. Noël, J.F., Larose, S., Abou Elela, S., Wellinger, R.J., Budding yeast telomerase RNA transcription termination is dictated by the Nrd1/Nab3 non-coding RNA termination pathway. Nucleic Acids Res. 40 (2012), 5625–5636.
35. Porrua, O., Libri, D., Transcription termination and the control of the transcriptome: why, where and how to stop. Nat. Rev. Mol. Cell Biol. 16 (2015), 190–202.
36. Preker, P., Nielsen, J., Kammler, S., Lykke-Andersen, S., Christensen, M.S., Mapendano, C.K., Schierup, M.H., Jensen, T.H., RNA exosome depletion reveals transcription upstream of active human promoters. Science 322 (2008), 1851–1854.
37. Schmidt, K., Butler, J.S., Nuclear RNA surveillance: role of TRAMP in controlling exosome specificity. Wiley Interdiscip. Rev. RNA 4 (2013), 217–231.
38. Shi, Y., Manley, J.L., The end of the message: multiple protein-RNA interactions define the mRNA polyadenylation site. Genes Dev. 29 (2015), 889–897.
39. Steinmetz, E.J., Conrad, N.K., Brow, D.A., Corden, J.L., RNA-binding protein Nrd1 directs poly(A)-independent 3′-end formation of RNA polymerase II transcripts. Nature 413 (2001), 327–331.
40. Stuart, B.D., Choi, J., Zaidi, S., Xing, C., Holohan, B., Chen, R., Choi, M., Dharwadkar, P., Torres, F., Girod, C.E., et al. Exome sequencing links mutations in PARN and RTEL1 with familial pulmonary fibrosis and telomere shortening. Nat. Genet. 47 (2015), 512–517.
41. Theimer, C.A., Jády, B.E., Chim, N., Richard, P., Breece, K.E., Kiss, T., Feigon, J., Structural and functional characterization of human telomerase RNA processing and cajal body localization signals. Mol. Cell 27 (2007), 869–881.
42. Tseng, C.-K., Wang, H.-F., Burns, A.M., Schroeder, M.R., Gaspari, M., Baumann, P., Human telomerase RNA processing and quality control. Cell Rep. 13 (2015), 2232–2243 this issue.
43. Tudek, A., Porrua, O., Kabzinski, T., Lidschreiber, M., Kubicek, K., Fortova, A., Lacroute, F., Vanacova, S., Cramer, P., Stefl, R., Libri, D., Molecular basis for coordinating transcription termination with noncoding RNA degradation. Mol. Cell 55 (2014), 467–481.
44. Tummala, H., Walne, A., Collopy, L., Cardoso, S., de la Fuente, J., Lawson, S., Powell, J., Cooper, N., Foster, A., Mohammed, S., et al. Poly(A)-specific ribonuclease deficiency impacts telomere biology and causes dyskeratosis congenita. J. Clin. Invest. 125 (2015), 2151–2160.
45. van Dijk, E.L., Schilders, G., Pruijn, G.J.M., Human cell growth requires a functional cytoplasmic exosome, which is involved in various mRNA decay pathways. RNA 13 (2007), 1027–1035.
46. Vulliamy, T., Beswick, R., Kirwan, M., Marrone, A., Digweed, M., Walne, A., Dokal, I., Mutations in the telomerase component NHP2 cause the premature ageing syndrome dyskeratosis congenita. Proc. Natl. Acad. Sci. USA 105 (2008), 8073–8078.
47. Wahle, E., A novel poly(A)-binding protein acts as a specificity factor in the second phase of messenger RNA polyadenylation. Cell 66 (1991), 759–768.
48. Webb, C.J., Wu, Y., Zakian, V.A., DNA repair at telomeres: keeping the ends intact. Cold Spring Harb. Perspect. Biol., 5, 2013, a012666.
49. West, S., Gromak, N., Norbury, C.J., Proudfoot, N.J., Adenylation and exosome-mediated degradation of cotranscriptionally cleaved pre-messenger RNA in human cells. Mol. Cell 21 (2006), 437–443.
50. Xi, L., Cech, T.R., Inventory of telomerase components in human cells reveals multiple subpopulations of hTR and hTERT. Nucleic Acids Res. 42 (2014), 8565–8577.
51. Yi, X., Tesmer, V.M., Savre-Train, I., Shay, J.W., Wright, W.E., Both transcriptional and posttranscriptional mechanisms regulate human telomerase template RNA levels. Mol. Cell. Biol. 19 (1999), 3989–3997.
52. Zhu, Y., Tomlinson, R.L., Lukowiak, A.A., Terns, R.M., Terns, M.P., Telomerase RNA accumulates in Cajal bodies in human cancer cells. Mol. Biol. Cell 15 (2004), 81–90.