Identification of a Nuclear Exosome Decay Pathway for Processed Transcripts

Molecular Cell

Volumn 64, Issue 3, 2016, Pages 520-533

  Meola, Nicola ^a   Domanski, Michal ^a   Karadoulama, Evdoxia ^a,b   Chen, Yun ^b   Gentil, Coline ^a   Pultz, Dennis ^c   Vitting Seerup, Kristoffer ^b   Lykke Andersen, Søren ^a   Andersen, Jens S ^c   Sandelin, Albin ^b   Jensen, Torben Heick ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

NEXT complex; nuclear RNA decay; PAXT connection; poly(A) tail; RNA exosome

Indexed keywords

CAPPED RNA; HYBRID PROTEIN; NUCLEAR RNA; POLYADENYLIC ACID BINDING PROTEIN; RIBONUCLEASE A; SMALL INTERFERING RNA; TRANSCRIPTOME; ZINC FINGER PROTEIN; CARRIER PROTEIN; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; MESSENGER RNA; NUCLEAR PROTEIN; PABPN1 PROTEIN, HUMAN; POLYADENYLIC ACID; PROTEIN BINDING; RBM7 PROTEIN, HUMAN; RNA BINDING PROTEIN; RNA HELICASE; SKIV2L2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR; ZCCHC8 PROTEIN, HUMAN; ZFC3H1 PROTEIN, HUMAN;

ARTICLE; BIOCHEMICAL ANALYSIS; CONTROLLED STUDY; EXOSOME; FEMALE; GENE INTERACTION; GENETIC CODE; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; POLYADENYLATION; PROTEIN DEPLETION; RNA DEGRADATION; TRANSCRIPTION INITIATION SITE; ANTAGONISTS AND INHIBITORS; BINDING SITE; CELL NUCLEUS; GENETICS; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; RNA STABILITY;

BINDING SITES; CARRIER PROTEINS; CELL NUCLEUS; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; HEK293 CELLS; HELA CELLS; HUMANS; NUCLEAR PROTEINS; POLY A; POLY(A)-BINDING PROTEIN I; PROTEIN BINDING; RNA HELICASES; RNA STABILITY; RNA, MESSENGER; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; TRANSCRIPTION FACTORS;

EID: 84995459544     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.09.025     Document Type: Article

References (55)

1. Ahmad, Y., Boisvert, F.M., Gregor, P., Cobley, A., Lamond, A.I., NOPdb: Nucleolar Proteome Database—2008 update. Nucleic Acids Res. 37 (2009), D181–D184.
2. Allmang, C., Petfalski, E., Podtelejnikov, A., Mann, M., Tollervey, D., Mitchell, P., The yeast exosome and human PM-Scl are related complexes of 3′ → 5′ exonucleases. Genes Dev. 13 (1999), 2148–2158.
3. Andersen, P.R., Domanski, M., Kristiansen, M.S., Storvall, H., Ntini, E., Verheggen, C., Schein, A., Bunkenborg, J., Poser, I., Hallais, M., et al. The human cap-binding complex is functionally connected to the nuclear RNA exosome. Nat. Struct. Mol. Biol. 20 (2013), 1367–1376.
4. Andersson, R., Gebhard, C., Miguel-Escalada, I., Hoof, I., Bornholdt, J., Boyd, M., Chen, Y., Zhao, X., Schmidl, C., Suzuki, T., et al., FANTOM Consortium. An atlas of active enhancers across human cell types and tissues. Nature 507 (2014), 455–461.
5. Arigo, J.T., Eyler, D.E., Carroll, K.L., Corden, J.L., Termination of cryptic unstable transcripts is directed by yeast RNA-binding proteins Nrd1 and Nab3. Mol. Cell 23 (2006), 841–851.
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. Bresson, S.M., Conrad, N.K., The human nuclear poly(a)-binding protein promotes RNA hyperadenylation and decay. PLoS Genet., 9, 2013, e1003893.
8. Bresson, S.M., Hunter, O.V., Hunter, A.C., Conrad, N.K., Canonical poly(A) polymerase activity promotes the decay of a wide variety of mammalian nuclear RNAs. PLoS Genet., 11, 2015, e1005610.
9. Brown, J.A., Valenstein, M.L., Yario, T.A., Tycowski, K.T., Steitz, J.A., Formation of triple-helical structures by the 3′-end sequences of MALAT1 and MENβ noncoding RNAs. Proc. Natl. Acad. Sci. USA 109 (2012), 19202–19207.
10. Chen, Y., Pai, A.A., Herudek, J., Lubas, M., Meola, N., Järvelin, A.I., Andersson, R., Pelechano, V., Steinmetz, L.M., Jensen, T.H., Sandelin, A., Principles for RNA metabolism and alternative transcription initiation within closely spaced promoters. Nat. Genet. 48 (2016), 984–994.
11. Chlebowski, A., Lubas, M., Jensen, T.H., Dziembowski, A., RNA decay machines: the exosome. Biochim. Biophys. Acta 1829 (2013), 552–560.
12. de la Cruz, J., Kressler, D., Tollervey, D., Linder, P., Dob1p (Mtr4p) is a putative ATP-dependent RNA helicase required for the 3′ end formation of 5.8S rRNA in Saccharomyces cerevisiae. EMBO J. 17 (1998), 1128–1140.
13. Djebali, S., Davis, C.A., Merkel, A., Dobin, A., Lassmann, T., Mortazavi, A., Tanzer, A., Lagarde, J., Lin, W., Schlesinger, F., et al. Landscape of transcription in human cells. Nature 489 (2012), 101–108.
14. Domanski, M., Molloy, K., Jiang, H., Chait, B.T., Rout, M.P., Jensen, T.H., LaCava, J., Improved methodology for the affinity isolation of human protein complexes expressed at near endogenous levels. Biotechniques 0 (2012), 1–6.
15. Egan, E.D., Braun, C.R., Gygi, S.P., Moazed, D., Post-transcriptional regulation of meiotic genes by a nuclear RNA silencing complex. RNA 20 (2014), 867–881.
16. ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 489 (2012), 57–74.
17. Falk, S., Weir, J.R., Hentschel, J., Reichelt, P., Bonneau, F., Conti, E., The molecular architecture of the TRAMP complex reveals the organization and interplay of its two catalytic activities. Mol. Cell 55 (2014), 856–867.
18. Hallais, M., Pontvianne, F., Andersen, P.R., Clerici, M., Lener, D., Benbahouche, Nel.H., Gostan, T., Vandermoere, F., Robert, M.C., Cusack, S., et al. CBC-ARS2 stimulates 3′-end maturation of multiple RNA families and favors cap-proximal processing. Nat. Struct. Mol. Biol. 20 (2013), 1358–1366.
19. Harrow, J., Frankish, A., Gonzalez, J.M., Tapanari, E., Diekhans, M., Kokocinski, F., Aken, B.L., Barrell, D., Zadissa, A., Searle, S., et al. GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res. 22 (2012), 1760–1774.
20. Houseley, J., LaCava, J., Tollervey, D., RNA-quality control by the exosome. Nat. Rev. Mol. Cell Biol. 7 (2006), 529–539.
21. Hrossova, D., Sikorsky, T., Potesil, D., Bartosovic, M., Pasulka, J., Zdrahal, Z., Stefl, R., Vanacova, S., RBM7 subunit of the NEXT complex binds U-rich sequences and targets 3′-end extended forms of snRNAs. Nucleic Acids Res. 43 (2015), 4236–4248.
22. Kerwitz, Y., Kühn, U., Lilie, H., Knoth, A., Scheuermann, T., Friedrich, H., Schwarz, E., Wahle, E., Stimulation of poly(A) polymerase through a direct interaction with the nuclear poly(A) binding protein allosterically regulated by RNA. EMBO J. 22 (2003), 3705–3714.
23. Kilchert, C., Wittmann, S., Vasiljeva, L., The regulation and functions of the nuclear RNA exosome complex. Nat. Rev. Mol. Cell Biol. 17 (2016), 227–239.
24. Kühn, U., Gündel, M., Knoth, A., Kerwitz, Y., Rüdel, S., Wahle, E., Poly(A) tail length is controlled by the nuclear poly(A)-binding protein regulating the interaction between poly(A) polymerase and the cleavage and polyadenylation specificity factor. J. Biol. Chem. 284 (2009), 22803–22814.
25. 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 121 (2005), 713–724.
26. Lee, N.N., Chalamcharla, V.R., Reyes-Turcu, F., Mehta, S., Zofall, M., Balachandran, V., Dhakshnamoorthy, J., Taneja, N., Yamanaka, S., Zhou, M., Grewal, S.I., Mtr4-like protein coordinates nuclear RNA processing for heterochromatin assembly and for telomere maintenance. Cell 155 (2013), 1061–1074.
27. 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.
28. Lemieux, C., Marguerat, S., Lafontaine, J., Barbezier, N., Bähler, J., Bachand, F., A Pre-mRNA degradation pathway that selectively targets intron-containing genes requires the nuclear poly(A)-binding protein. Mol. Cell 44 (2011), 108–119.
29. Libri, D., Nuclear poly(A)-binding proteins and nuclear degradation: take the mRNA and run?. Mol. Cell 37 (2010), 3–5.
30. 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.
31. Lubas, M., Andersen, P.R., Schein, A., Dziembowski, A., Kudla, G., Jensen, T.H., The human nuclear exosome targeting complex is loaded onto newly synthesized RNA to direct early ribonucleolysis. Cell Rep. 10 (2015), 178–192.
32. Mitchell, P., Exosome substrate targeting: the long and short of it. Biochem. Soc. Trans. 42 (2014), 1129–1134.
33. Moon, D.H., Segal, M., Boyraz, B., Guinan, E., Hofmann, I., Cahan, P., Tai, A.K., Agarwal, S., Poly(A)-specific ribonuclease (PARN) mediates 3′-end maturation of the telomerase RNA component. Nat. Genet. 47 (2015), 1482–1488.
34. Nguyen, D., Grenier St-Sauveur, V., Bergeron, D., Dupuis-Sandoval, F., Scott, M.S., Bachand, F., A polyadenylation-dependent 3′ end maturation pathway is required for the synthesis of the human telomerase RNA. Cell Rep. 13 (2015), 2244–2257.
35. Paulsen, M.T., Veloso, A., Prasad, J., Bedi, K., Ljungman, E.A., Tsan, Y.C., Chang, C.W., Tarrier, B., Washburn, J.G., Lyons, R., et al. Coordinated regulation of synthesis and stability of RNA during the acute TNF-induced proinflammatory response. Proc. Natl. Acad. Sci. USA 110 (2013), 2240–2245.
36. Schmid, M., Poulsen, M.B., Olszewski, P., Pelechano, V., Saguez, C., Gupta, I., Steinmetz, L.M., Moore, C., Jensen, T.H., Rrp6p controls mRNA poly(A) tail length and its decoration with poly(A) binding proteins. Mol. Cell 47 (2012), 267–280.
37. Schmid, M., Olszewski, P., Pelechano, V., Gupta, I., Steinmetz, L.M., Jensen, T.H., The nuclear polyA-binding protein Nab2p is essential for mRNA production. Cell Rep. 12 (2015), 128–139.
38. Schneider, C., Tollervey, D., Threading the barrel of the RNA exosome. Trends Biochem. Sci. 38 (2013), 485–493.
39. Shcherbik, N., Wang, M., Lapik, Y.R., Srivastava, L., Pestov, D.G., Polyadenylation and degradation of incomplete RNA polymerase I transcripts in mammalian cells. EMBO Rep. 11 (2010), 106–111.
40. Shi, Y., Di Giammartino, D.C., Taylor, D., Sarkeshik, A., Rice, W.J., Yates, J.R. 3rd, Frank, J., Manley, J.L., Molecular architecture of the human pre-mRNA 3′ processing complex. Mol. Cell 33 (2009), 365–376.
41. St-André, O., Lemieux, C., Perreault, A., Lackner, D.H., Bähler, J., Bachand, F., Negative regulation of meiotic gene expression by the nuclear poly(a)-binding protein in fission yeast. J. Biol. Chem. 285 (2010), 27859–27868.
42. Tafforeau, L., Zorbas, C., Langhendries, J.L., Mullineux, S.T., Stamatopoulou, V., Mullier, R., Wacheul, L., Lafontaine, D.L., The complexity of human ribosome biogenesis revealed by systematic nucleolar screening of Pre-rRNA processing factors. Mol. Cell 51 (2013), 539–551.
43. Thiebaut, M., Kisseleva-Romanova, E., Rougemaille, M., Boulay, J., Libri, D., Transcription termination and nuclear degradation of cryptic unstable transcripts: a role for the nrd1-nab3 pathway in genome surveillance. Mol. Cell 23 (2006), 853–864.
44. Thoms, M., Thomson, E., Baßler, J., Gnädig, M., Griesel, S., Hurt, E., The exosome is recruited to RNA substrates through specific adaptor proteins. Cell 162 (2015), 1029–1038.
45. Tomecki, R., Kristiansen, M.S., Lykke-Andersen, S., Chlebowski, A., Larsen, K.M., Szczesny, R.J., Drazkowska, K., Pastula, A., Andersen, J.S., Stepien, P.P., et al. The human core exosome interacts with differentially localized processive RNases: hDIS3 and hDIS3L. EMBO J. 29 (2010), 2342–2357.
46. Tomita, T., Ieguchi, K., Coin, F., Kato, Y., Kikuchi, H., Oshima, Y., Kurata, S., Maru, Y., ZFC3H1, a zinc finger protein, modulates IL-8 transcription by binding with celastramycin A, a potential immune suppressor. PLoS ONE, 9, 2014, e108957.
47. 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.
48. 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.
49. Vanácová, S., Wolf, J., Martin, G., Blank, D., Dettwiler, S., Friedlein, A., Langen, H., Keith, G., Keller, W., A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol., 3, 2005, e189.
50. Vasiljeva, L., Buratowski, S., Nrd1 interacts with the nuclear exosome for 3′ processing of RNA polymerase II transcripts. Mol. Cell 21 (2006), 239–248.
51. Wickham, H., Ggplot2: Elegant Graphics for Data Analysis. 2009, Springer-Verlag.
52. Wlotzka, W., Kudla, G., Granneman, S., Tollervey, D., The nuclear RNA polymerase II surveillance system targets polymerase III transcripts. EMBO J. 30 (2011), 1790–1803.
53. Wyers, F., Rougemaille, M., Badis, G., Rousselle, J.C., Dufour, M.E., Boulay, J., Régnault, B., Devaux, F., Namane, A., Séraphin, B., et al. Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121 (2005), 725–737.
54. Yang, Q., Nausch, L.W., Martin, G., Keller, W., Doublié, S., Crystal structure of human poly(A) polymerase gamma reveals a conserved catalytic core for canonical poly(A) polymerases. J. Mol. Biol. 426 (2014), 43–50.
55. Zhou, Y., Zhu, J., Schermann, G., Ohle, C., Bendrin, K., Sugioka-Sugiyama, R., Sugiyama, T., Fischer, T., The fission yeast MTREC complex targets CUTs and unspliced pre-mRNAs to the nuclear exosome. Nat. Commun., 6, 2015, 7050.