Nuclear RNA Exosome at 3.1 Å Reveals Substrate Specificities, RNA Paths, and Allosteric Inhibition of Rrp44/Dis3

Molecular Cell

Volumn 64, Issue 4, 2016, Pages 734-745

  Zinder, John C ^a,b   Wasmuth, Elizabeth V ^b   Lima, Christopher D ^b,c  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b NEW YORK STRUCTURAL BIOLOGY CENTER   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

click chemistry; exoribonuclease; exosome; multi subunit complex; nuclear; RNA; RNA decay; structure; X ray crystallography

Indexed keywords

DIS3 PROTEIN; EXORIBONUCLEASE; NUCLEAR RNA; RRP44 PROTEIN; RRP6 PROTEIN; UNCLASSIFIED DRUG; DIS3 PROTEIN, S CEREVISIAE; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; FUNGAL RNA; PROTEIN BINDING; PROTEIN SUBUNIT; RECOMBINANT PROTEIN; RRP6 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ALLOSTERISM; ARTICLE; CRYSTAL STRUCTURE; ENZYME INHIBITION; ENZYME SPECIFICITY; EXOSOME; NONHUMAN; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; RNA DEGRADATION; ALPHA HELIX; BETA SHEET; BINDING SITE; CELL NUCLEUS; CHEMISTRY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR MODEL; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN SUBUNIT; RNA CLEAVAGE; SACCHAROMYCES CEREVISIAE; THERMODYNAMICS; ULTRASTRUCTURE; X RAY CRYSTALLOGRAPHY;

ALLOSTERIC REGULATION; AMINO ACID MOTIFS; BINDING SITES; CELL NUCLEUS; CLONING, MOLECULAR; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; GENE EXPRESSION; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION, ALPHA-HELICAL; PROTEIN CONFORMATION, BETA-STRAND; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN SUBUNITS; RECOMBINANT PROTEINS; RNA CLEAVAGE; RNA, FUNGAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUBSTRATE SPECIFICITY; THERMODYNAMICS;

EID: 84995545531     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.09.038     Document Type: Article

References (45)

1. Allmang, C., Kufel, J., Chanfreau, G., Mitchell, P., Petfalski, E., Tollervey, D., Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO J. 18 (1999), 5399–5410.
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. Bonneau, F., Basquin, J., Ebert, J., Lorentzen, E., Conti, E., The yeast exosome functions as a macromolecular cage to channel RNA substrates for degradation. Cell 139 (2009), 547–559.
4. Briggs, M.W., Burkard, K.T., Butler, J.S., Rrp6p, the yeast homologue of the human PM-Scl 100-kDa autoantigen, is essential for efficient 5.8 S rRNA 3′ end formation. J. Biol. Chem. 273 (1998), 13255–13263.
5. Brouwer, R., Allmang, C., Raijmakers, R., van Aarssen, Y., Egberts, W.V., Petfalski, E., van Venrooij, W.J., Tollervey, D., Pruijn, G.J.M., Three novel components of the human exosome. J. Biol. Chem. 276 (2001), 6177–6184.
6. Burkard, K.T., Butler, J.S., A nuclear 3′-5′ exonuclease involved in mRNA degradation interacts with poly(A) polymerase and the hnRNA protein Npl3p. Mol. Cell. Biol. 20 (2000), 604–616.
7. Cech, T.R., Steitz, J.A., The noncoding RNA revolution—trashing old rules to forge new ones. Cell 157 (2014), 77–94.
8. Chapman, M.A., Lawrence, M.S., Keats, J.J., Cibulskis, K., Sougnez, C., Schinzel, A.C., Harview, C.L., Brunet, J.-P., Ahmann, G.J., Adli, M., et al. Initial genome sequencing and analysis of multiple myeloma. Nature 471 (2011), 467–472.
9. Cheng, Z.-F., Deutscher, M.P., Purification and characterization of the Escherichia coli exoribonuclease RNase R. Comparison with RNase II. J. Biol. Chem. 277 (2002), 21624–21629.
10. Domanski, M., Upla, P., Rice, W.J., Molloy, K.R., Ketaren, N.E., Stokes, D.L., Jensen, T.H., Rout, M.P., LaCava, J., Purification and analysis of endogenous human RNA exosome complexes. RNA 22 (2016), 1467–1475.
11. Drazkowska, K., Tomecki, R., Stodus, K., Kowalska, K., Czarnocki-Cieciura, M., Dziembowski, A., The RNA exosome complex central channel controls both exonuclease and endonuclease Dis3 activities in vivo and in vitro. Nucleic Acids Res. 41 (2013), 3845–3858.
12. Dziembowski, A., Lorentzen, E., Conti, E., Séraphin, B., A single subunit, Dis3, is essentially responsible for yeast exosome core activity. Nat. Struct. Mol. Biol. 14 (2007), 15–22.
13. El-Sagheer, A.H., Brown, T., Click nucleic acid ligation: applications in biology and nanotechnology. Acc. Chem. Res. 45 (2012), 1258–1267.
14. ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 489 (2012), 57–74.
15. Fabre, A., Badens, C., Human Mendelian diseases related to abnormalities of the RNA exosome or its cofactors. Intractable Rare Dis. Res. 3 (2014), 8–11.
16. Gasse, L., Flemming, D., Hurt, E., Coordinated ribosomal ITS2 RNA processing by the Las1 complex integrating endonuclease, polynucleotide kinase, and exonuclease activities. Mol. Cell 60 (2015), 808–815.
17. Greimann, J.C., Lima, C.D., Reconstitution of RNA exosomes from human and Saccharomyces cerevisiae cloning, expression, purification, and activity assays. Methods Enzymol. 448 (2008), 185–210.
18. Han, J., van Hoof, A., The RNA exosome channeling and direct access conformations have distinct in vivo functions. Cell Rep. 16 (2016), 3348–3358.
19. Houseley, J., Tollervey, D., The many pathways of RNA degradation. Cell 136 (2009), 763–776.
20. Januszyk, K., Lima, C.D., The eukaryotic RNA exosome. Curr. Opin. Struct. Biol. 24 (2014), 132–140.
21. Kadaba, S., Krueger, A., Trice, T., Krecic, A.M., Hinnebusch, A.G., Anderson, J., Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae. Genes Dev. 18 (2004), 1227–1240.
22. Kowalinski, E., Kögel, A., Ebert, J., Reichelt, P., Stegmann, E., Habermann, B., Conti, E., Structure of a cytoplasmic 11-subunit RNA exosome complex. Mol. Cell 63 (2016), 125–134.
23. 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.
24. Liu, Q., Greimann, J.C., Lima, C.D., Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell 127 (2006), 1223–1237.
25. Liu, J.-J., Bratkowski, M.A., Liu, X., Niu, C.-Y., Ke, A., Wang, H.-W., Visualization of distinct substrate-recruitment pathways in the yeast exosome by EM. Nat. Struct. Mol. Biol. 21 (2014), 95–102.
26. Liu, J.-J., Niu, C.-Y., Wu, Y., Tan, D., Wang, Y., Ye, M.-D., Liu, Y., Zhao, W., Zhou, K., Liu, Q.-S., et al. CryoEM structure of yeast cytoplasmic exosome complex. Cell Res. 26 (2016), 822–837.
27. Lorentzen, E., Basquin, J., Tomecki, R., Dziembowski, A., Conti, E., Structure of the active subunit of the yeast exosome core, Rrp44: diverse modes of substrate recruitment in the RNase II nuclease family. Mol. Cell 29 (2008), 717–728.
28. Lubas, M., Chlebowski, A., Dziembowski, A., Jensen, T.H., Biochemistry and function of RNA exosomes. Enzymes 31 (2012), 1–30.
29. Lubas, M., Damgaard, C.K., Tomecki, R., Cysewski, D., Jensen, T.H., Dziembowski, A., Exonuclease hDIS3L2 specifies an exosome-independent 3′-5′ degradation pathway of human cytoplasmic mRNA. EMBO J. 32 (2013), 1855–1868.
30. Makino, D.L., Halbach, F., Conti, E., The RNA exosome and proteasome: common principles of degradation control. Nat. Rev. Mol. Cell Biol. 14 (2013), 654–660.
31. Makino, D.L., Baumgärtner, M., Conti, E., Crystal structure of an RNA-bound 11-subunit eukaryotic exosome complex. Nature 495 (2013), 70–75.
32. Makino, D.L., Schuch, B., Stegmann, E., Baumgärtner, M., Basquin, C., Conti, E., RNA degradation paths in a 12-subunit nuclear exosome complex. Nature 524 (2015), 54–58.
33. Malet, H., Topf, M., Clare, D.K., Ebert, J., Bonneau, F., Basquin, J., Drazkowska, K., Tomecki, R., Dziembowski, A., Conti, E., et al. RNA channelling by the eukaryotic exosome. EMBO Rep. 11 (2010), 936–942.
34. Midtgaard, S.F., Assenholt, J., Jonstrup, A.T., Van, L.B., Jensen, T.H., Brodersen, D.E., Structure of the nuclear exosome component Rrp6p reveals an interplay between the active site and the HRDC domain. Proc. Natl. Acad. Sci. USA 103 (2006), 11898–11903.
35. Mitchell, P., Petfalski, E., Shevchenko, A., Mann, M., Tollervey, D., The exosome: a conserved eukaryotic RNA processing complex containing multiple 3′→5′ exoribonucleases. Cell 91 (1997), 457–466.
36. Paredes, E., Das, S.R., Click chemistry for rapid labeling and ligation of RNA. ChemBioChem 12 (2011), 125–131.
37. 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.
38. Rinn, J.L., Chang, H.Y., Genome regulation by long noncoding RNAs. Annu. Rev. Biochem. 81 (2012), 145–166.
39. 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.
40. Vincent, H.A., Deutscher, M.P., Substrate recognition and catalysis by the exoribonuclease RNase R. J. Biol. Chem. 281 (2006), 29769–29775.
41. Wasmuth, E.V., Lima, C.D., Structure and activities of the eukaryotic RNA exosome. Enzymes 31 (2012), 53–75.
42. Wasmuth, E.V., Lima, C.D., Exo- and endoribonucleolytic activities of yeast cytoplasmic and nuclear RNA exosomes are dependent on the noncatalytic core and central channel. Mol. Cell 48 (2012), 133–144.
43. Wasmuth, E.V., Januszyk, K., Lima, C.D., Structure of an Rrp6-RNA exosome complex bound to poly(A) RNA. Nature 511 (2014), 435–439.
44. Wu, J., Hopper, A.K., Healing for destruction: tRNA intron degradation in yeast is a two-step cytoplasmic process catalyzed by tRNA ligase Rlg1 and 5′-to-3′ exonuclease Xrn1. Genes Dev. 28 (2014), 1556–1561.
45. 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.