publication . Article . 2017

Structure and reconstitution of yeast Mpp6-nuclear exosome complexes reveals that Mpp6 stimulates RNA decay and recruits the Mtr4 helicase.

John C. Zinder; Mom Das; Christopher D. Lima; Elizabeth V. Wasmuth; Dimitrios Zattas;
Open Access
  • Published: 25 Jul 2017 Journal: eLife, volume 6 (eissn: 2050-084X, Copyright policy)
  • Publisher: eLife Sciences Publications, Ltd
Abstract
Nuclear RNA exosomes catalyze a range of RNA processing and decay activities that are coordinated in part by cofactors, including Mpp6, Rrp47, and the Mtr4 RNA helicase. Mpp6 interacts with the nine-subunit exosome core, while Rrp47 stabilizes the exoribonuclease Rrp6 and recruits Mtr4, but it is less clear if these cofactors work together. Using biochemistry with Saccharomyces cerevisiae proteins, we show that Rrp47 and Mpp6 stimulate exosome-mediated RNA decay, albeit with unique dependencies on elements within the nuclear exosome. Mpp6-exosomes can recruit Mtr4, while Mpp6 and Rrp47 each contribute to Mtr4-dependent RNA decay, with maximal Mtr4-dependent deca...
Subjects
free text keywords: Research Article, Biochemistry, RNA decay, protein-RNA complex, helicase, x-ray crystallography, RNA degradation, S. cerevisiae, RNA, Small nuclear RNA, Cell biology, TRAMP complex, Messenger RNA, Biology, Exosome complex, RNA Helicase A, Exosome Multienzyme Ribonuclease Complex, Molecular biology, Exoribonuclease
Funded by
NIH| MOLECULAR GENETIC ANALYSIS OF THE DROSOPHILA 205K MAP
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5F32GM012006-03
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| Structural and Biochemical Characterization of the S. cerevisiae RNA Exosome
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5F31GM097910-02
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| MOUSE GENETICS
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 2P30CA008748-43
  • Funding stream: NATIONAL CANCER INSTITUTE
,
NIH| Structural studies of RNA processing and ubiquitin-like protein modification
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1R35GM118080-01
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| Structural and Functional Studies of Eukaryotic Exosomes
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01GM079196-07
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
Download fromView all 2 versions
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Article . 2017
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63 references, page 1 of 5

Adams, PD, Afonine, PV, Bunkóczi, G, Chen, VB, Davis, IW, Echols, N, Headd, JJ, Hung, LW, Kapral, GJ, Grosse-Kunstleve, RW, McCoy, AJ, Moriarty, NW, Oeffner, R, Read, RJ, Richardson, DC, Richardson, JS, Terwilliger, TC, Zwart, PH. PHENIX: a comprehensive python-based system for macromolecular structure solution. Acta Crystallographica Section D Biological Crystallography. 2010; 66: 213-221 [OpenAIRE] [PubMed] [DOI]

Allmang, C, Kufel, J, Chanfreau, G, Mitchell, P, Petfalski, E, Tollervey, D. Functions of the exosome in rRNA, snoRNA and snRNA synthesis. The EMBO Journal. 1999; 18: 5399-5410 [OpenAIRE] [PubMed] [DOI]

Allmang, C, Mitchell, P, Petfalski, E, Tollervey, D. Degradation of ribosomal RNA precursors by the exosome. Nucleic Acids Research. 2000; 28: 1684-1691 [OpenAIRE] [PubMed] [DOI]

Ashkenazy, H, Erez, E, Martz, E, Pupko, T, Ben-Tal, N. ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Research. 2010; 38: W529-W533 [OpenAIRE] [PubMed] [DOI]

Assenholt, J, Mouaikel, J, Andersen, KR, Brodersen, DE, Libri, D, Jensen, TH. Exonucleolysis is required for nuclear mRNA quality control in yeast THO mutants. RNA. 2008; 14: 2305-2313 [OpenAIRE] [PubMed] [DOI]

Basu, U, Meng, FL, Keim, C, Grinstein, V, Pefanis, E, Eccleston, J, Zhang, T, Myers, D, Wasserman, CR, Wesemann, DR, Januszyk, K, Gregory, RI, Deng, H, Lima, CD, Alt, FW. The RNA exosome targets the AID cytidine deaminase to both strands of transcribed duplex DNA substrates. Cell. 2011; 144: 353-363 [OpenAIRE] [PubMed] [DOI]

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. 2009; 139: 547-559 [OpenAIRE] [PubMed] [DOI]

Brunger, AT. Version 1.2 of the Crystallography and NMR system. Nature Protocols. 2007; 2: 2728-2733 [OpenAIRE] [PubMed] [DOI]

Butler, JS, Mitchell, P. Rrp6, rrp47 and cofactors of the nuclear exosome. Advances in Experimental Medicine and Biology. 2011; 702: 91-104 [OpenAIRE] [PubMed] [DOI]

Chen, CY, Gherzi, R, Ong, SE, Chan, EL, Raijmakers, R, Pruijn, GJ, Stoecklin, G, Moroni, C, Mann, M, Karin, M. AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell. 2001; 107: 451-464 [OpenAIRE] [PubMed] [DOI]

Chen, VB, Arendall, WB, Headd, JJ, Keedy, DA, Immormino, RM, Kapral, GJ, Murray, LW, Richardson, JS, Richardson, DC. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallographica Section D Biological Crystallography. 2010; 66: 12-21 [OpenAIRE] [PubMed] [DOI]

Cole, C, Barber, JD, Barton, GJ. The jpred 3 secondary structure prediction server. Nucleic Acids Research. 2008; 36: W197-W201 [OpenAIRE] [PubMed] [DOI]

Dedic, E, Seweryn, P, Jonstrup, AT, Flygaard, RK, Fedosova, NU, Hoffmann, SV, Boesen, T, Brodersen, DE. Structural analysis of the yeast exosome Rrp6p-Rrp47p complex by small-angle X-ray scattering. Biochemical and Biophysical Research Communications. 2014; 450: 634-640 [OpenAIRE] [PubMed] [DOI]

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 Research. 2013; 41: 3845-3858 [OpenAIRE] [PubMed] [DOI]

Emsley, P, Lohkamp, B, Scott, WG, Cowtan, K. Features and development of Coot. Acta Crystallographica Section D Biological Crystallography. 2010; 66: 486-501 [OpenAIRE] [PubMed] [DOI]

63 references, page 1 of 5
Related research
Abstract
Nuclear RNA exosomes catalyze a range of RNA processing and decay activities that are coordinated in part by cofactors, including Mpp6, Rrp47, and the Mtr4 RNA helicase. Mpp6 interacts with the nine-subunit exosome core, while Rrp47 stabilizes the exoribonuclease Rrp6 and recruits Mtr4, but it is less clear if these cofactors work together. Using biochemistry with Saccharomyces cerevisiae proteins, we show that Rrp47 and Mpp6 stimulate exosome-mediated RNA decay, albeit with unique dependencies on elements within the nuclear exosome. Mpp6-exosomes can recruit Mtr4, while Mpp6 and Rrp47 each contribute to Mtr4-dependent RNA decay, with maximal Mtr4-dependent deca...
Subjects
free text keywords: Research Article, Biochemistry, RNA decay, protein-RNA complex, helicase, x-ray crystallography, RNA degradation, S. cerevisiae, RNA, Small nuclear RNA, Cell biology, TRAMP complex, Messenger RNA, Biology, Exosome complex, RNA Helicase A, Exosome Multienzyme Ribonuclease Complex, Molecular biology, Exoribonuclease
Funded by
NIH| MOLECULAR GENETIC ANALYSIS OF THE DROSOPHILA 205K MAP
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5F32GM012006-03
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| Structural and Biochemical Characterization of the S. cerevisiae RNA Exosome
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5F31GM097910-02
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| MOUSE GENETICS
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 2P30CA008748-43
  • Funding stream: NATIONAL CANCER INSTITUTE
,
NIH| Structural studies of RNA processing and ubiquitin-like protein modification
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1R35GM118080-01
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| Structural and Functional Studies of Eukaryotic Exosomes
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01GM079196-07
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
Download fromView all 2 versions
eLife
Article . 2017
Provider: Crossref
eLife
Article
Provider: UnpayWall
63 references, page 1 of 5

Adams, PD, Afonine, PV, Bunkóczi, G, Chen, VB, Davis, IW, Echols, N, Headd, JJ, Hung, LW, Kapral, GJ, Grosse-Kunstleve, RW, McCoy, AJ, Moriarty, NW, Oeffner, R, Read, RJ, Richardson, DC, Richardson, JS, Terwilliger, TC, Zwart, PH. PHENIX: a comprehensive python-based system for macromolecular structure solution. Acta Crystallographica Section D Biological Crystallography. 2010; 66: 213-221 [OpenAIRE] [PubMed] [DOI]

Allmang, C, Kufel, J, Chanfreau, G, Mitchell, P, Petfalski, E, Tollervey, D. Functions of the exosome in rRNA, snoRNA and snRNA synthesis. The EMBO Journal. 1999; 18: 5399-5410 [OpenAIRE] [PubMed] [DOI]

Allmang, C, Mitchell, P, Petfalski, E, Tollervey, D. Degradation of ribosomal RNA precursors by the exosome. Nucleic Acids Research. 2000; 28: 1684-1691 [OpenAIRE] [PubMed] [DOI]

Ashkenazy, H, Erez, E, Martz, E, Pupko, T, Ben-Tal, N. ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Research. 2010; 38: W529-W533 [OpenAIRE] [PubMed] [DOI]

Assenholt, J, Mouaikel, J, Andersen, KR, Brodersen, DE, Libri, D, Jensen, TH. Exonucleolysis is required for nuclear mRNA quality control in yeast THO mutants. RNA. 2008; 14: 2305-2313 [OpenAIRE] [PubMed] [DOI]

Basu, U, Meng, FL, Keim, C, Grinstein, V, Pefanis, E, Eccleston, J, Zhang, T, Myers, D, Wasserman, CR, Wesemann, DR, Januszyk, K, Gregory, RI, Deng, H, Lima, CD, Alt, FW. The RNA exosome targets the AID cytidine deaminase to both strands of transcribed duplex DNA substrates. Cell. 2011; 144: 353-363 [OpenAIRE] [PubMed] [DOI]

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. 2009; 139: 547-559 [OpenAIRE] [PubMed] [DOI]

Brunger, AT. Version 1.2 of the Crystallography and NMR system. Nature Protocols. 2007; 2: 2728-2733 [OpenAIRE] [PubMed] [DOI]

Butler, JS, Mitchell, P. Rrp6, rrp47 and cofactors of the nuclear exosome. Advances in Experimental Medicine and Biology. 2011; 702: 91-104 [OpenAIRE] [PubMed] [DOI]

Chen, CY, Gherzi, R, Ong, SE, Chan, EL, Raijmakers, R, Pruijn, GJ, Stoecklin, G, Moroni, C, Mann, M, Karin, M. AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell. 2001; 107: 451-464 [OpenAIRE] [PubMed] [DOI]

Chen, VB, Arendall, WB, Headd, JJ, Keedy, DA, Immormino, RM, Kapral, GJ, Murray, LW, Richardson, JS, Richardson, DC. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallographica Section D Biological Crystallography. 2010; 66: 12-21 [OpenAIRE] [PubMed] [DOI]

Cole, C, Barber, JD, Barton, GJ. The jpred 3 secondary structure prediction server. Nucleic Acids Research. 2008; 36: W197-W201 [OpenAIRE] [PubMed] [DOI]

Dedic, E, Seweryn, P, Jonstrup, AT, Flygaard, RK, Fedosova, NU, Hoffmann, SV, Boesen, T, Brodersen, DE. Structural analysis of the yeast exosome Rrp6p-Rrp47p complex by small-angle X-ray scattering. Biochemical and Biophysical Research Communications. 2014; 450: 634-640 [OpenAIRE] [PubMed] [DOI]

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 Research. 2013; 41: 3845-3858 [OpenAIRE] [PubMed] [DOI]

Emsley, P, Lohkamp, B, Scott, WG, Cowtan, K. Features and development of Coot. Acta Crystallographica Section D Biological Crystallography. 2010; 66: 486-501 [OpenAIRE] [PubMed] [DOI]

63 references, page 1 of 5
Related research
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