The Molecular Architecture of the TRAMP Complex Reveals the Organization and Interplay of Its Two Catalytic Activities

Molecular Cell

Volumn 55, Issue 6, 2014, Pages 856-867

  Falk, Sebastian ^a   Weir, John R ^a,b   Hentschel, Jendrik ^a,c   Reichelt, Peter ^a   Bonneau, Fabien ^a   Conti, Elena ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

^c ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; HELICASE; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; PROTEIN AIR2; PROTEIN MTR4; PROTEIN TRF4; RNA; TRAMP COMPLEX; UNCLASSIFIED DRUG; DNA DIRECTED DNA POLYMERASE; PROTEIN MDM2; RNA HELICASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CATALYSIS; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOPLASM; ENZYME ACTIVITY; ENZYME BINDING; ENZYME STRUCTURE; ENZYME SUBSTRATE; EXOSOME; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR DYNAMICS; MOLECULAR MODEL; MUTATION; POLYADENYLATION; PROTEIN DOMAIN; X RAY CRYSTALLOGRAPHY; AMINO ACID SEQUENCE; CELL NUCLEUS; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; ENZYME ACTIVE SITE; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN CONFORMATION; PROTEIN QUATERNARY STRUCTURE; SACCHAROMYCES CEREVISIAE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; CATALYTIC DOMAIN; CELL NUCLEUS; CRYSTALLOGRAPHY, X-RAY; CYTOPLASM; DNA-DIRECTED DNA POLYMERASE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN STRUCTURE, QUATERNARY; PROTO-ONCOGENE PROTEINS C-MDM2; RNA HELICASES; SACCHAROMYCES CEREVISIAE;

EID: 84908006760     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.07.020     Document Type: Article

References (44)

1. Anderson J.T., Wang X. Nuclear RNA surveillance: no sign of substrates tailing off. Crit. Rev. Biochem. Mol. Biol. 2009, 44:16-24.
2. Callahan K.P., Butler J.S. Evidence for core exosome independent function of the nuclear exoribonuclease Rrp6p. Nucleic Acids Res. 2008, 36:6645-6655.
3. Carneiro T., Carvalho C., Braga J., Rino J., Milligan L., Tollervey D., Carmo-Fonseca M. Depletion of the yeast nuclear exosome subunit Rrp6 results in accumulation of polyadenylated RNAs in a discrete domain within the nucleolus. Mol. Cell. Biol. 2007, 27:4157-4165.
4. Chen V.B., Arendall W.B., Headd J.J., Keedy D.A., Immormino R.M., Kapral G.J., Murray L.W., Richardson J.S., Richardson D.C. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:12-21.
5. Cox J., Hein M.Y., Luber C.A., Paron I., Nagaraj N., Mann M. MaxLFQ allows accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction. Mol. Cell. Proteomics 2014, 10.1074/mcp.M113.031591.
6. Davis C.A., Ares M. Accumulation of unstable promoter-associated transcripts upon loss of the nuclear exosome subunit Rrp6p in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 2006, 103:3262-3267.
7. Dez C., Houseley J., Tollervey D. Surveillance of nuclear-restricted pre-ribosomes within a subnucleolar region of Saccharomyces cerevisiae. EMBO J. 2006, 25:1534-1546.
8. Eckmann C.R., Rammelt C., Wahle E. Control of poly(A) tail length. Wiley Interdiscip. Rev. RNA 2011, 2:348-361.
9. 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. 2011, 286:37429-37445.
10. Gnad F., de Godoy L.M.F., Cox J., Neuhauser N., Ren S., Olsen J.V., Mann M. High-accuracy identification and bioinformatic analysis of invivo protein phosphorylation sites in yeast. Proteomics 2009, 9:4642-4652.
11. Grzechnik P., Kufel J. Polyadenylation linked to transcription termination directs the processing of snoRNA precursors in yeast. Mol. Cell 2008, 32:247-258.
12. Halbach F., Rode M., Conti E. The crystal structure of S. cerevisiae Ski2, a DExH helicase associated with the cytoplasmic functions of the exosome. RNA 2012, 18:124-134.
13. Halbach F., Reichelt P., Rode M., Conti E. The yeast ski complex: crystal structure and RNA channeling to the exosome complex. Cell 2013, 154:814-826.
14. Hamill S., Wolin S.L., Reinisch K.M. Structure and function of the polymerase core of TRAMP, a RNA surveillance complex. Proc. Natl. Acad. Sci. USA 2010, 107:15045-15050.
15. Holub P., Lalakova J., Cerna H., Pasulka J., Sarazova M., Hrazdilova K., Arce M.S., Hobor F., Stefl R., Vaňáčová Š. Air2p is critical for the assembly and RNA-binding of the TRAMP complex and the KOW domain of Mtr4p is crucial for exosome activation. Nucleic Acids Res. 2012, 40:5679-5693.
16. Houseley J., LaCava J., Tollervey D. RNA-quality control by the exosome. Nat. Rev. Mol. Cell Biol. 2006, 7:529-539.
17. Hubner N.C., Bird A.W., Cox J., Splettstoesser B., Bandilla P., Poser I., Hyman A., Mann M. Quantitative proteomics combined with BAC TransgeneOmics reveals invivo protein interactions. J.Cell Biol. 2010, 189:739-754.
18. Jackson R.N., Klauer A.A., Hintze B.J., Robinson H., van Hoof A., Johnson S.J. The crystal structure of Mtr4 reveals a novel arch domain required for rRNA processing. EMBO J. 2010, 29:2205-2216.
19. Jia H., Wang X., Liu F., Guenther U.-P., Srinivasan S., Anderson J.T., Jankowsky E. The RNA helicase Mtr4p modulates polyadenylation in the TRAMP complex. Cell 2011, 145:890-901.
20. 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. 2004, 18:1227-1240.
21. Kadaba S., Wang X., Anderson J.T. Nuclear RNA surveillance in Saccharomyces cerevisiae: Trf4p-dependent polyadenylation of nascent hypomethylated tRNA and an aberrant form of 5S rRNA. RNA 2006, 12:508-521.
22. Kastner B., Fischer N., Golas M.M., Sander B., Dube P., Boehringer D., Hartmuth K., Deckert J., Hauer F., Wolf E., et al. GraFix: sample preparation for single-particle electron cryomicroscopy. Nat. Methods 2008, 5:53-55.
23. Keller C., Woolcock K., Hess D., Bühler M. Proteomic and functional analysis of the noncanonical poly(A) polymerase Cid14. RNA 2010, 16:1124-1129.
24. Klauer A.A., van Hoof A. Genetic interactions suggest multiple distinct roles of the arch and core helicase domains of Mtr4 in Rrp6 and exosome function. Nucleic Acids Res. 2013, 41:533-541.
25. Kühn-Hölsken E., Lenz C., Dickmanns A., Hsiao H.-H., Richter F.M., Kastner B., Ficner R., Urlaub H. Mapping the binding site of snurportin 1 on native U1 snRNP by cross-linking and mass spectrometry. Nucleic Acids Res. 2010, 38:5581-5593.
26. Kuriyan J., Eisenberg D. The origin of protein interactions and allostery in colocalization. Nature 2007, 450:983-990.
27. Kushner S.R. mRNA decay in prokaryotes and eukaryotes: different approaches to a similar problem. IUBMB Life 2004, 56:585-594.
28. 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.
29. Linke K., Mace P.D., Smith C.A., Vaux D.L., Silke J., Day C.L. Structure of the MDM2/MDMX RING domain heterodimer reveals dimerization is required for their ubiquitylation in trans. Cell Death Differ. 2008, 15:841-848.
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 2011, 43:624-637.
31. Martin G., Keller W. RNA-specific ribonucleotidyl transferases. RNA 2007, 13:1834-1849.
32. Melero R., Buchwald G., Castaño R., Raabe M., Gil D., Lázaro M., Urlaub H., Conti E., Llorca O. The cryo-EM structure of the UPF-EJC complex shows UPF1 poised toward the RNA 3' end. Nat. Struct. Mol. Biol. 2012, 19:498-505. S1-S2.
33. Mohanty B.K., Kushner S.R. Bacterial/archaeal/organellar polyadenylation. Wiley Interdiscip. Rev. RNA 2011, 2:256-276.
34. Preker P., Almvig K., Christensen M.S., Valen E., Mapendano C.K., Sandelin A., Jensen T.H. PROMoter uPstream Transcripts share characteristics with mRNAs and are produced upstream of all three major types of mammalian promoters. Nucleic Acids Res. 2011, 39:7179-7193.
35. Schiller H.B., Friedel C.C., Boulegue C., Fässler R. Quantitative proteomics of the integrin adhesome show a myosin II-dependent recruitment of LIM domain proteins. EMBO Rep. 2011, 12:259-266.
36. Schmidt K., Butler J.S. Nuclear RNA surveillance: role of TRAMP in controlling exosome specificity. Wiley Interdiscip. Rev. RNA 2013, 4:217-231.
37. Shi M., Collett M., Loros J.J., Dunlap J.C. FRQ-interacting RNA helicase mediates negative and positive feedback in the Neurospora circadian clock. Genetics 2010, 184:351-361.
38. Smolka M.B., Albuquerque C.P., Chen S.-H., Zhou H. Proteome-wide identification of invivo targets of DNA damage checkpoint kinases. Proc. Natl. Acad. Sci. USA 2007, 104:10364-10369.
39. Svergun D.I., Petoukhov M.V., Koch M.H. Determination of domain structure of proteins from X-ray solution scattering. Biophys. J. 2001, 80:2946-2953.
40. Vanácová Š., 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. 2005, 3:e189.
41. Wang Z., Castaño I.B., De Las Peñas A., Adams C., Christman M.F. Pol kappa: A DNA polymerase required for sister chromatid cohesion. Science 2000, 289:774-779.
42. Weir J.R., Bonneau F., Hentschel J., Conti E. Structural analysis reveals the characteristic features of Mtr4, a DExH helicase involved in nuclear RNA processing and surveillance. Proc. Natl. Acad. Sci. USA 2010, 107:12139-12144.
43. Wlotzka W., Kudla G., Granneman S., Tollervey D. The nuclear RNA polymerase II surveillance system targets polymerase III transcripts. EMBO J. 2011, 30:1790-1803.
44. 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 2005, 121:725-737.