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The molecular architecture of the TRAMP complex reveals the organization and interplay of its two catalytic activities.

Falk S, Weir JR, Hentschel J, Reichelt P, Bonneau F, Conti E
Mol Cell 55 856-867 (2014)
Cited: 47 times
EuropePMC logo PMID: 25175027

Abstract

The TRAMP complex is involved in the nuclear surveillance and turnover of noncoding RNAs and intergenic transcripts. TRAMP is associated with the nuclear exosome and consists of a poly(A)polymerase subcomplex (Trf4-Air2) and a helicase (Mtr4). We found that N-terminal low-complexity regions of Trf4 and Air2 bind Mtr4 in a cooperative manner. The 2.4 Å resolution crystal structure of the corresponding ternary complex reveals how Trf4 and Air2 wrap around the DExH core of the helicase. Structure-based mutations on the DExH core impair binding to Trf4 and Air2, and also to Trf5 and Air1. The combination of structural, biochemical, and biophysical data suggests that the poly(A)polymerase core of Trf4-Air2 is positioned below the base of the helicase, where the unwound 3' end of an RNA substrate is expected to emerge. The results reveal conceptual similarities between the two major regulators of the exosome, the nuclear TRAMP and cytoplasmic Ski complexes.

Reviews - 4u4c mentioned but not cited (3)

  1. Targeting RNA for processing or destruction by the eukaryotic RNA exosome and its cofactors. Zinder JC, Lima CD. Genes Dev 31 88-100 (2017)
  2. RNA helicases are hubs that orchestrate exosome-dependent 3'-5' decay. Weick EM, Lima CD. Curr Opin Struct Biol 67 86-94 (2021)
  3. Mtr4 RNA helicase structures and interactions. Olsen KJ, Johnson SJ. Biol Chem 402 605-616 (2021)

Articles - 4u4c mentioned but not cited (7)

  1. Structural basis for MTR4-ZCCHC8 interactions that stimulate the MTR4 helicase in the nuclear exosome-targeting complex. Puno MR, Lima CD. Proc Natl Acad Sci U S A 115 E5506-E5515 (2018)
  2. NRDE2 negatively regulates exosome functions by inhibiting MTR4 recruitment and exosome interaction. Wang J, Chen J, Wu G, Zhang H, Du X, Chen S, Zhang L, Wang K, Fan J, Gao S, Wu X, Zhang S, Kuai B, Zhao P, Chi B, Wang L, Li G, Wong CCL, Zhou Y, Li J, Yun C, Cheng H. Genes Dev 33 536-549 (2019)
  3. Structure of the frequency-interacting RNA helicase: a protein interaction hub for the circadian clock. Conrad KS, Hurley JM, Widom J, Ringelberg CS, Loros JJ, Dunlap JC, Crane BR. EMBO J 35 1707-1719 (2016)
  4. The zinc-finger protein Red1 orchestrates MTREC submodules and binds the Mtl1 helicase arch domain. Dobrev N, Ahmed YL, Sivadas A, Soni K, Fischer T, Sinning I. Nat Commun 12 3456 (2021)
  5. Structure of frequency-interacting RNA helicase from Neurospora crassa reveals high flexibility in a domain critical for circadian rhythm and RNA surveillance. Morales Y, Olsen KJ, Bulcher JM, Johnson SJ. PLoS One 13 e0196642 (2018)
  6. Structural basis for RNA surveillance by the human nuclear exosome targeting (NEXT) complex. Puno MR, Lima CD. Cell 185 2132-2147.e26 (2022)
  7. ELM-the Eukaryotic Linear Motif resource-2024 update. Kumar M, Michael S, Alvarado-Valverde J, Zeke A, Lazar T, Glavina J, Nagy-Kanta E, Donagh JM, Kalman ZE, Pascarelli S, Palopoli N, Dobson L, Suarez CF, Van Roey K, Krystkowiak I, Griffin JE, Nagpal A, Bhardwaj R, Diella F, Mészáros B, Dean K, Davey NE, Pancsa R, Chemes LB, Gibson TJ. Nucleic Acids Res 52 D442-D455 (2024)


Reviews citing this publication (9)

  1. The conformational plasticity of eukaryotic RNA-dependent ATPases. Ozgur S, Buchwald G, Falk S, Chakrabarti S, Prabu JR, Conti E. FEBS J 282 850-863 (2015)
  2. Terminal nucleotidyl transferases (TENTs) in mammalian RNA metabolism. Warkocki Z, Liudkovska V, Gewartowska O, Mroczek S, Dziembowski A. Philos Trans R Soc Lond B Biol Sci 373 20180162 (2018)
  3. The multitasking polyA tail: nuclear RNA maturation, degradation and export. Tudek A, Lloret-Llinares M, Jensen TH. Philos Trans R Soc Lond B Biol Sci 373 20180169 (2018)
  4. Writing a wrong: Coupled RNA polymerase II transcription and RNA quality control. Peck SA, Hughes KD, Victorino JF, Mosley AL. Wiley Interdiscip Rev RNA 10 e1529 (2019)
  5. A Tale of Two RNAs during Viral Infection: How Viruses Antagonize mRNAs and Small Non-Coding RNAs in The Host Cell. Herbert KM, Nag A. Viruses 8 E154 (2016)
  6. Noncoding RNA Surveillance: The Ends Justify the Means. Belair C, Sim S, Wolin SL. Chem Rev 118 4422-4447 (2018)
  7. DEAD/DExH-Box RNA Helicases in Selected Human Parasites. Marchat LA, Arzola-Rodríguez SI, Hernandez-de la Cruz O, Lopez-Rosas I, Lopez-Camarillo C. Korean J Parasitol 53 583-595 (2015)
  8. Cellular functions of eukaryotic RNA helicases and their links to human diseases. Bohnsack KE, Yi S, Venus S, Jankowsky E, Bohnsack MT. Nat Rev Mol Cell Biol 24 749-769 (2023)
  9. RNA Exosomes and Their Cofactors. Kilchert C. Methods Mol Biol 2062 215-235 (2020)

Articles citing this publication (28)

  1. Identification of a Nuclear Exosome Decay Pathway for Processed Transcripts. Meola N, Domanski M, Karadoulama E, Chen Y, Gentil C, Pultz D, Vitting-Seerup K, Lykke-Andersen S, Andersen JS, Sandelin A, Jensen TH. Mol Cell 64 520-533 (2016)
  2. The Exosome Is Recruited to RNA Substrates through Specific Adaptor Proteins. Thoms M, Thomson E, Baßler J, Gnädig M, Griesel S, Hurt E. Cell 162 1029-1038 (2015)
  3. The fission yeast MTREC complex targets CUTs and unspliced pre-mRNAs to the nuclear exosome. Zhou Y, Zhu J, Schermann G, Ohle C, Bendrin K, Sugioka-Sugiyama R, Sugiyama T, Fischer T. Nat Commun 6 7050 (2015)
  4. Structure of a Cytoplasmic 11-Subunit RNA Exosome Complex. Kowalinski E, Kögel A, Ebert J, Reichelt P, Stegmann E, Habermann B, Conti E. Mol Cell 63 125-134 (2016)
  5. Global analysis of transcriptionally engaged yeast RNA polymerase III reveals extended tRNA transcripts. Turowski TW, Leśniewska E, Delan-Forino C, Sayou C, Boguta M, Tollervey D. Genome Res 26 933-944 (2016)
  6. RNA surveillance by the nuclear RNA exosome: mechanisms and significance. Ogami K, Chen Y, Manley JL. Noncoding RNA 4 8 (2018)
  7. Transcriptome-wide analysis of alternative routes for RNA substrates into the exosome complex. Delan-Forino C, Schneider C, Tollervey D. PLoS Genet 13 e1006699 (2017)
  8. Altered RNA metabolism due to a homozygous RBM7 mutation in a patient with spinal motor neuropathy. Giunta M, Edvardson S, Xu Y, Schuelke M, Gomez-Duran A, Boczonadi V, Elpeleg O, Müller JS, Horvath R. Hum Mol Genet 25 2985-2996 (2016)
  9. Structure of the RBM7-ZCCHC8 core of the NEXT complex reveals connections to splicing factors. Falk S, Finogenova K, Melko M, Benda C, Lykke-Andersen S, Jensen TH, Conti E. Nat Commun 7 13573 (2016)
  10. Mpp6 Incorporation in the Nuclear Exosome Contributes to RNA Channeling through the Mtr4 Helicase. Falk S, Bonneau F, Ebert J, Kögel A, Conti E. Cell Rep 20 2279-2286 (2017)
  11. The MTR4 helicase recruits nuclear adaptors of the human RNA exosome using distinct arch-interacting motifs. Lingaraju M, Johnsen D, Schlundt A, Langer LM, Basquin J, Sattler M, Heick Jensen T, Falk S, Conti E. Nat Commun 10 3393 (2019)
  12. Letter Interaction properties of human TRAMP-like proteins and their role in pre-rRNA 5'ETS turnover. Sudo H, Nozaki A, Uno H, Ishida Y, Nagahama M. FEBS Lett 590 2963-2972 (2016)
  13. Structural insights into the interaction of the nuclear exosome helicase Mtr4 with the preribosomal protein Nop53. Falk S, Tants JN, Basquin J, Thoms M, Hurt E, Sattler M, Conti E. RNA 23 1780-1787 (2017)
  14. The Mtr4 ratchet helix and arch domain both function to promote RNA unwinding. Taylor LL, Jackson RN, Rexhepaj M, King AK, Lott LK, van Hoof A, Johnson SJ. Nucleic Acids Res 42 13861-13872 (2014)
  15. Distinct and evolutionary conserved structural features of the human nuclear exosome complex. Gerlach P, Schuller JM, Bonneau F, Basquin J, Reichelt P, Falk S, Conti E. Elife 7 e38686 (2018)
  16. Targeting the nuclear RNA exosome: Poly(A) binding proteins enter the stage. Meola N, Jensen TH. RNA Biol 14 820-826 (2017)
  17. Loss of the Yeast SR Protein Npl3 Alters Gene Expression Due to Transcription Readthrough. Holmes RK, Tuck AC, Zhu C, Dunn-Davies HR, Kudla G, Clauder-Munster S, Granneman S, Steinmetz LM, Guthrie C, Tollervey D. PLoS Genet 11 e1005735 (2015)
  18. Substrate specificity of the TRAMP nuclear surveillance complexes. Delan-Forino C, Spanos C, Rappsilber J, Tollervey D. Nat Commun 11 3122 (2020)
  19. Interaction between the RNA-dependent ATPase and poly(A) polymerase subunits of the TRAMP complex is mediated by short peptides and important for snoRNA processing. Losh JS, King AK, Bakelar J, Taylor L, Loomis J, Rosenzweig JA, Johnson SJ, van Hoof A. Nucleic Acids Res 43 1848-1858 (2015)
  20. The human SKI complex regulates channeling of ribosome-bound RNA to the exosome via an intrinsic gatekeeping mechanism. Kögel A, Keidel A, Bonneau F, Schäfer IB, Conti E. Mol Cell 82 756-769.e8 (2022)
  21. Exosomal Protein Deficiencies: How Abnormal RNA Metabolism Results in Childhood-Onset Neurological Diseases. Müller JS, Giunta M, Horvath R. J Neuromuscul Dis 2 S31-S37 (2015)
  22. The ribosome assembly factor Nop53 controls association of the RNA exosome with pre-60S particles in yeast. Cepeda LPP, Bagatelli FFM, Santos RM, Santos MDM, Nogueira FCS, Oliveira CC. J Biol Chem 294 19365-19380 (2019)
  23. Gateway Arch to the RNA Exosome. Losh JS, van Hoof A. Cell 162 940-941 (2015)
  24. Hydrogen-deuterium exchange mass spectrometry of Mtr4 with diverse RNAs reveals substrate-dependent dynamics and interfaces in the arch. Zhang N, Olsen KJ, Ball D, Johnson SJ, D'Arcy S. Nucleic Acids Res 50 4042-4053 (2022)
  25. In vivo characterization of the critical interaction between the RNA exosome and the essential RNA helicase Mtr4 in Saccharomyces cerevisiae. Sterrett MC, Farchi D, Strassler SE, Boise LH, Fasken MB, Corbett AH. G3 (Bethesda) 13 jkad049 (2023)
  26. RNA substrate length as an indicator of exosome interactions in vivo. Delan-Forino C, Schneider C, Tollervey D. Wellcome Open Res 2 34 (2017)
  27. Structure and regulation of the nuclear exosome targeting complex guides RNA substrates to the exosome. Gerlach P, Garland W, Lingaraju M, Salerno-Kochan A, Bonneau F, Basquin J, Jensen TH, Conti E. Mol Cell 82 2505-2518.e7 (2022)
  28. Purification and Reconstitution of the S. cerevisiae TRAMP and Ski Complexes for Biochemical and Structural Studies. Keidel A, Conti E, Falk S. Methods Mol Biol 2062 491-513 (2020)


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