Structure of a Cytoplasmic 11-Subunit RNA Exosome Complex

Molecular Cell

Volumn 63, Issue 1, 2016, Pages 125-134

  Kowalinski, Eva ^a   Kögel, Alexander ^a   Ebert, Judith ^a   Reichelt, Peter ^a   Stegmann, Elisabeth ^a   Habermann, Bianca ^a   Conti, Elena ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CSL4 PROTEIN; CYTOPLASMIC 11 SUBUNIT RNA EXOSOME COMPLEX; MTR3 PROTEIN; RRP4 PROTEIN; RRP40 PROTEIN; RRP41 PROTEIN; RRP42 PROTEIN; RRP43 PROTEIN; RRP45 PROTEIN; RRP46 PROTEIN; UNCLASSIFIED DRUG; CSL4 PROTEIN, S CEREVISIAE; ELONGATION FACTOR; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; GUANINE NUCLEOTIDE BINDING PROTEIN; HBS1 PROTEIN, HUMAN; HEAT SHOCK PROTEIN 70; ISOPROTEIN; MTR3 PROTEIN, S CEREVISIAE; NUCLEAR PROTEIN; PROTEIN BINDING; RRP6 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SKI7 PROTEIN, S CEREVISIAE;

ALTERNATIVE RNA SPLICING; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOPLASM; EXOSOME; GENETIC CONSERVATION; NONHUMAN; PROTEIN CONFORMATION; PROTEIN CROSS LINKING; PROTEIN DEGRADATION; PROTEIN ENGINEERING; PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN STRUCTURE; RNA DEGRADATION; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; STEREOCHEMISTRY; AMINO ACID SEQUENCE; CHEMICAL PHENOMENA; CHEMISTRY; CONSERVED SEQUENCE; GENETICS; HUMAN; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR MODEL; MUTATION; PROTEIN DOMAIN; STRUCTURE ACTIVITY RELATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; BINDING SITES; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; GTP-BINDING PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MODELS, MOLECULAR; MUTATION; NUCLEAR PROTEINS; PEPTIDE ELONGATION FACTORS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN ISOFORMS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84992358935     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.05.028     Document Type: Article

References (56)

1. Afonine, P.V., Grosse-Kunstleve, R.W., Echols, N., Headd, J.J., Moriarty, N.W., Mustyakimov, M., Terwilliger, T.C., Urzhumtsev, A., Zwart, P.H., Adams, P.D., Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr. D Biol. Crystallogr. 68 (2012), 352–367.
2. 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.
3. Anderson, J.S., Parker, R.P., The 3′ to 5′ degradation of yeast mRNAs is a general mechanism for mRNA turnover that requires the SKI2 DEVH box protein and 3′ to 5′ exonucleases of the exosome complex. EMBO J. 17 (1998), 1497–1506.
4. Araki, Y., Takahashi, S., Kobayashi, T., Kajiho, H., Hoshino, S., Katada, T., Ski7p G protein interacts with the exosome and the Ski complex for 3′-to-5′ mRNA decay in yeast. EMBO J. 20 (2001), 4684–4693.
5. Becker, T., Armache, J.-P., Jarasch, A., Anger, A.M., Villa, E., Sieber, H., Motaal, B.A., Mielke, T., Berninghausen, O., Beckmann, R., Structure of the no-go mRNA decay complex Dom34-Hbs1 bound to a stalled 80S ribosome. Nat. Struct. Mol. Biol. 18 (2011), 715–720.
6. 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.
7. Brown, J.T., Bai, X., Johnson, A.W., The yeast antiviral proteins Ski2p, Ski3p, and Ski8p exist as a complex in vivo. RNA 6 (2000), 449–457.
8. Butler, J.S., Mitchell, P., Rrp6, Rrp47 and cofactors of the nuclear exosome. Adv. Exp. Med. Biol. 702 (2010), 91–104.
9. Chlebowski, A., Lubas, M., Jensen, T.H., Dziembowski, A., RNA decay machines: the exosome. Biochim. Biophys. Acta 1829 (2013), 552–560.
10. Chun, E., Thompson, A.A., Liu, W., Roth, C.B., Griffith, M.T., Katritch, V., Kunken, J., Xu, F., Cherezov, V., Hanson, M.A., Stevens, R.C., Fusion partner toolchest for the stabilization and crystallization of G protein-coupled receptors. Structure 20 (2012), 967–976.
11. Cowtan, K., The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr. D Biol. Crystallogr. 62 (2006), 1002–1011.
12. Davis, I.W., Leaver-Fay, A., Chen, V.B., Block, J.N., Kapral, G.J., Wang, X., Murray, L.W., Arendall, W.B. 3rd, Snoeyink, J., Richardson, J.S., Richardson, D.C., MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35 (2007), W375–W383.
13. Doma, M.K., Parker, R., Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation. Nature 440 (2006), 561–564.
14. Drazkowska, K., Tomecki, R., Stoduś, 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.
15. 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.
16. Emsley, P., Cowtan, K., Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60 (2004), 2126–2132.
17. 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.
18. 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.
19. 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.
20. Guydosh, N.R., Green, R., Dom34 rescues ribosomes in 3′ untranslated regions. Cell 156 (2014), 950–962.
21. Halbach, F., Reichelt, P., Rode, M., Conti, E., The yeast ski complex: crystal structure and RNA channeling to the exosome complex. Cell 154 (2013), 814–826.
22. Houseley, J., LaCava, J., Tollervey, D., RNA-quality control by the exosome. Nat. Rev. Mol. Cell Biol. 7 (2006), 529–539.
23. Inada, T., Quality control systems for aberrant mRNAs induced by aberrant translation elongation and termination. Biochim. Biophys. Acta 1829 (2013), 634–642.
24. Januszyk, K., Lima, C.D., The eukaryotic RNA exosome. Curr. Opin. Struct. Biol. 24 (2014), 132–140.
25. Kabsch, W., XDS. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 125–132.
26. Klauer, A.A., van Hoof, A., Degradation of mRNAs that lack a stop codon: a decade of nonstop progress. Wiley Interdiscip. Rev. RNA 3 (2012), 649–660.
27. Kowalinski, E., Schuller, A., Green, R., Conti, E., Saccharomyces cerevisiae Ski7 is a GTP-binding protein adopting the characteristic conformation of active translational GTPases. Structure 23 (2015), 1336–1343.
28. Krissinel, E., Henrick, K., Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372 (2007), 774–797.
29. Lebreton, A., Séraphin, B., Exosome-mediated quality control: substrate recruitment and molecular activity. Biochim. Biophys. Acta 1779 (2008), 558–565.
30. Lebreton, A., Tomecki, R., Dziembowski, A., Séraphin, B., Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature 456 (2008), 993–996.
31. Liu, Q., Greimann, J.C., Lima, C.D., Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell 127 (2006), 1223–1237.
32. Lykke-Andersen, J., Bennett, E.J., Protecting the proteome: Eukaryotic cotranslational quality control pathways. J. Cell Biol. 204 (2014), 467–476.
33. Lykke-Andersen, S., Brodersen, D.E., Jensen, T.H., Origins and activities of the eukaryotic exosome. J. Cell Sci. 122 (2009), 1487–1494.
34. Makino, D.L., Baumgärtner, M., Conti, E., Crystal structure of an RNA-bound 11-subunit eukaryotic exosome complex. Nature 495 (2013), 70–75.
35. 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.
36. Marshall, A.N., Montealegre, M.C., Jiménez-López, C., Lorenz, M.C., van Hoof, A., Alternative splicing and subfunctionalization generates functional diversity in fungal proteomes. PLoS Genet., 9, 2013, e1003376.
37. Matsuda, R., Ikeuchi, K., Nomura, S., Inada, T., Protein quality control systems associated with no-go and nonstop mRNA surveillance in yeast. Genes Cells 19 (2014), 1–12.
38. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C., Read, R.J., Phaser crystallographic software. J. Appl. Cryst. 40 (2007), 658–674.
39. 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.
40. Rigby, R.E., Rehwinkel, J., RNA degradation in antiviral immunity and autoimmunity. Trends Immunol. 36 (2015), 179–188.
41. Saito, S., Hosoda, N., Hoshino, S., The Hbs1-Dom34 protein complex functions in non-stop mRNA decay in mammalian cells. J. Biol. Chem. 288 (2013), 17832–17843.
42. Schaeffer, D., Clark, A., Klauer, A.A., Tsanova, B., van Hoof, A., Functions of the cytoplasmic exosome. Adv. Exp. Med. Biol. 702 (2011), 79–90.
43. Schilders, G., van Dijk, E., Pruijn, G.J.M., C1D and hMtr4p associate with the human exosome subunit PM/Scl-100 and are involved in pre-rRNA processing. Nucleic Acids Res. 35 (2007), 2564–2572.
44. Schrödinger, L. (2011). The PyMOL Graphics System. Version. v1.5.0.4.
45. Schuch, B., Feigenbutz, M., Makino, D.L., Falk, S., Basquin, C., Mitchell, P., Conti, E., The exosome-binding factors Rrp6 and Rrp47 form a composite surface for recruiting the Mtr4 helicase. EMBO J. 33 (2014), 2829–2846.
46. Shi, Y., Pellarin, R., Fridy, P.C., Fernandez-Martinez, J., Thompson, M.K., Li, Y., Wang, Q.J., Sali, A., Rout, M.P., Chait, B.T., A strategy for dissecting the architectures of native macromolecular assemblies. Nat. Methods 12 (2015), 1135–1138.
47. Shoemaker, C.J., Green, R., Translation drives mRNA quality control. Nat. Struct. Mol. Biol. 19 (2012), 594–601.
48. Shoemaker, C.J., Eyler, D.E., Green, R., Dom34:Hbs1 promotes subunit dissociation and peptidyl-tRNA drop-off to initiate no-go decay. Science 330 (2010), 369–372.
49. Staals, R.H.J., Pruijn, G.J.M., The human exosome and disease. Adv. Exp. Med. Biol. 702 (2010), 132–142.
50. Toh-E, A., Guerry, P., Wickner, R.B., Chromosomal superkiller mutants of Saccharomyces cerevisiae. J. Bacteriol. 136 (1978), 1002–1007.
51. Tsuboi, T., Kuroha, K., Kudo, K., Makino, S., Inoue, E., Kashima, I., Inada, T., Dom34:hbs1 plays a general role in quality-control systems by dissociation of a stalled ribosome at the 3′ end of aberrant mRNA. Mol. Cell 46 (2012), 518–529.
52. van Hoof, A., Staples, R.R., Baker, R.E., Parker, R., Function of the ski4p (Csl4p) and Ski7p proteins in 3′-to-5′ degradation of mRNA. Mol. Cell. Biol. 20 (2000), 8230–8243.
53. van Hoof, A., Frischmeyer, P.A., Dietz, H.C., Parker, R., Exosome-mediated recognition and degradation of mRNAs lacking a termination codon. Science 295 (2002), 2262–2264.
54. Wang, L., Lewis, M.S., Johnson, A.W., Domain interactions within the Ski2/3/8 complex and between the Ski complex and Ski7p. RNA 11 (2005), 1291–1302.
55. 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.
56. 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.