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PMID: 24362565 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Architecture of the large subunit of the mammalian mitochondrial ribosome.

Nature ·Vol. 505 ·No. 7484 ·2014-01-23 ·Pages 515-9

Greber BJ, Boehringer D, Leitner A, Bieri P, Voigts-Hoffmann F, Erzberger JP, Leibundgut M, Aebersold R, Ban N

Abstract

Mitochondrial ribosomes synthesize a number of highly hydrophobic proteins encoded on the genome of mitochondria, the organelles in eukaryotic cells that are responsible for energy conversion by oxidative phosphorylation. The ribosomes in mammalian mitochondria have undergone massive structural changes throughout their evolution, including ribosomal RNA shortening and acquisition of mitochondria-specific ribosomal proteins. Here we present the three-dimensional structure of the 39S large subunit of the porcine mitochondrial ribosome determined by cryo-electron microscopy at 4.9 Å resolution. The structure, combined with data from chemical crosslinking and mass spectrometry experiments, reveals the unique features of the 39S subunit at near-atomic resolution and provides detailed insight into the architecture of the polypeptide exit site. This region of the mitochondrial ribosome has been considerably remodelled compared to its bacterial counterpart, providing a specialized platform for the synthesis and membrane insertion of the highly hydrophobic protein components of the respiratory chain.

MeSH Terms
Animals Cattle Cryoelectron Microscopy Hydrophobic and Hydrophilic Interactions Mass Spectrometry Mitochondria/chemistry,ultrastructure Mitochondrial Proteins/chemistry,ultrastructure Models, Molecular Nucleic Acid Conformation Protein Conformation RNA, Ribosomal, 16S/chemistry,ultrastructure Ribosomal Proteins/chemistry,ultrastructure Ribosome Subunits/chemistry,ultrastructure Swine
Chemicals
Mitochondrial Proteins RNA, Ribosomal, 16S Ribosomal Proteins
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Greber Basil J
1] Department of Biology, Institute of Molecular Biology and Biophysics, Schafmattstrasse 20, ETH Zurich, CH-8093 Zurich, Switzerland [2].
Boehringer Daniel
1] Department of Biology, Institute of Molecular Biology and Biophysics, Schafmattstrasse 20, ETH Zurich, CH-8093 Zurich, Switzerland [2].
Leitner Alexander
Department of Biology, Institute of Molecular Systems Biology, Wolfgang-Pauli-Strasse 16, ETH Zurich, CH-8093 Zurich, Switzerland.
Bieri Philipp
Department of Biology, Institute of Molecular Biology and Biophysics, Schafmattstrasse 20, ETH Zurich, CH-8093 Zurich, Switzerland.
Voigts-Hoffmann Felix
Department of Biology, Institute of Molecular Biology and Biophysics, Schafmattstrasse 20, ETH Zurich, CH-8093 Zurich, Switzerland.
Erzberger Jan P
Department of Biology, Institute of Molecular Biology and Biophysics, Schafmattstrasse 20, ETH Zurich, CH-8093 Zurich, Switzerland.
Leibundgut Marc
Department of Biology, Institute of Molecular Biology and Biophysics, Schafmattstrasse 20, ETH Zurich, CH-8093 Zurich, Switzerland.
Aebersold Ruedi
1] Department of Biology, Institute of Molecular Systems Biology, Wolfgang-Pauli-Strasse 16, ETH Zurich, CH-8093 Zurich, Switzerland [2] Faculty of Science, University of Zurich, CH-8057 Zurich, Switzerland.
Ban Nenad
Department of Biology, Institute of Molecular Biology and Biophysics, Schafmattstrasse 20, ETH Zurich, CH-8093 Zurich, Switzerland.
References (54)
54 references, click to expand
  1. EMAN: semiautomated software for high-resolution single-particle reconstructions.
    J Struct Biol. 1999 Dec 1;128(1):82-97 PMID: 10600563
  2. Mass spectrometry supported determination of protein complex structure.
    Curr Opin Struct Biol. 2013 Apr;23(2):252-60 PMID: 23522702
  3. A new generation of the IMAGIC image processing system.
    J Struct Biol. 1996 Jan-Feb;116(1):17-24 PMID: 8742718
  4. Identification of cross-linked peptides from large sequence databases.
    Nat Methods. 2008 Apr;5(4):315-8 PMID: 18327264
  5. Atomic structures of the eukaryotic ribosome.
    Trends Biochem Sci. 2012 May;37(5):189-98 PMID: 22436288
  6. Mitochondrial Hsp70/MIM44 complex facilitates protein import.
    Nature. 1994 Oct 27;371(6500):768-74 PMID: 7935837
  7. Expanding the chemical cross-linking toolbox by the use of multiple proteases and enrichment by size exclusion chromatography.
    Mol Cell Proteomics. 2012 Mar;11(3):M111.014126 PMID: 22286754
  8. Membrane binding mechanism of yeast mitochondrial peripheral membrane protein TIM44.
    Protein Pept Lett. 2011 Jul;18(7):718-25 PMID: 21342097
  9. Structural basis for the rescue of stalled ribosomes: structure of YaeJ bound to the ribosome.
    Science. 2012 Mar 16;335(6074):1370-2 PMID: 22422986
  10. Mba1, a membrane-associated ribosome receptor in mitochondria.
    EMBO J. 2006 Apr 19;25(8):1603-10 PMID: 16601683
  11. A functional peptidyl-tRNA hydrolase, ICT1, has been recruited into the human mitochondrial ribosome.
    EMBO J. 2010 Mar 17;29(6):1116-25 PMID: 20186120
  12. Protein structure prediction on the Web: a case study using the Phyre server.
    Nat Protoc. 2009;4(3):363-71 PMID: 19247286
  13. Structural compensation for the deficit of rRNA with proteins in the mammalian mitochondrial ribosome. Systematic analysis of protein components of the large ribosomal subunit from mammalian mitochondria.
    J Biol Chem. 2001 Jun 15;276(24):21724-36 PMID: 11279069
  14. A cross-platform toolkit for mass spectrometry and proteomics.
    Nat Biotechnol. 2012 Oct;30(10):918-20 PMID: 23051804
  15. Biological significance of 5S rRNA import into human mitochondria: role of ribosomal protein MRP-L18.
    Genes Dev. 2011 Jun 15;25(12):1289-305 PMID: 21685364
  16. UCSF Chimera--a visualization system for exploratory research and analysis.
    J Comput Chem. 2004 Oct;25(13):1605-12 PMID: 15264254
  17. RPG: the Ribosomal Protein Gene database.
    Nucleic Acids Res. 2004 Jan 1;32(Database issue):D168-70 PMID: 14681386
  18. Integration of biological networks and gene expression data using Cytoscape.
    Nat Protoc. 2007;2(10):2366-82 PMID: 17947979
  19. Solution structure of the catalytic domain of the mitochondrial protein ICT1 that is essential for cell vitality.
    J Mol Biol. 2010 Nov 26;404(2):260-73 PMID: 20869366
  20. False discovery rate estimation for cross-linked peptides identified by mass spectrometry.
    Nat Methods. 2012 Sep;9(9):901-3 PMID: 22772729
  21. The large subunit of the mammalian mitochondrial ribosome. Analysis of the complement of ribosomal proteins present.
    J Biol Chem. 2001 Nov 23;276(47):43958-69 PMID: 11551941
  22. Mitochondrial diseases: translation matters.
    Mol Cell Neurosci. 2013 Jul;55:1-12 PMID: 22986124
  23. Heart-specific splice-variant of a human mitochondrial ribosomal protein (mRNA processing; tissue specific splicing).
    Gene. 2000 Dec 31;261(2):229-34 PMID: 11167009
  24. Structure of the mammalian mitochondrial ribosome reveals an expanded functional role for its component proteins.
    Cell. 2003 Oct 3;115(1):97-108 PMID: 14532006
  25. Yeast Oxa1 interacts with mitochondrial ribosomes: the importance of the C-terminal region of Oxa1.
    EMBO J. 2003 Dec 15;22(24):6438-47 PMID: 14657017
  26. Mba1, a novel component of the mitochondrial protein export machinery of the yeast Saccharomyces cerevisiae.
    J Cell Biol. 2001 May 28;153(5):1085-96 PMID: 11381092
  27. Interaction of mammalian mitochondrial ribosomes with the inner membrane.
    J Biol Chem. 2000 Sep 22;275(38):29400-6 PMID: 10887179
  28. Improved methods for building protein models in electron density maps and the location of errors in these models.
    Acta Crystallogr A. 1991 Mar 1;47 ( Pt 2):110-9 PMID: 2025413
  29. Proteins at the polypeptide tunnel exit of the yeast mitochondrial ribosome.
    J Biol Chem. 2010 Jun 18;285(25):19022-8 PMID: 20404317
  30. Multiparticle cryo-EM of ribosomes.
    Methods Enzymol. 2010;483:161-77 PMID: 20888474
  31. Features and development of Coot.
    Acta Crystallogr D Biol Crystallogr. 2010 Apr;66(Pt 4):486-501 PMID: 20383002
  32. Structural basis for translation termination on the 70S ribosome.
    Nature. 2008 Aug 14;454(7206):852-7 PMID: 18596689
  33. Reconstructing the evolution of the mitochondrial ribosomal proteome.
    Nucleic Acids Res. 2007;35(14):4686-703 PMID: 17604309
  34. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution.
    Science. 2000 Aug 11;289(5481):905-20 PMID: 10937989
  35. PHENIX: a comprehensive Python-based system for macromolecular structure solution.
    Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):213-21 PMID: 20124702
  36. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields.
    J Struct Biol. 1996 Jan-Feb;116(1):190-9 PMID: 8742743
  37. How hibernation factors RMF, HPF, and YfiA turn off protein synthesis.
    Science. 2012 May 18;336(6083):915-8 PMID: 22605777
  38. Mitochondrial ribssome in HeLa cells.
    Nat New Biol. 1971 Feb 3;229(5):133-6 PMID: 5280091
  39. On the origin of mitosing cells
    J Theor Biol. 1967 Mar;14(3):255-74 PMID: 11541392
  40. Crystal structure of yeast mitochondrial peripheral membrane protein Tim44p C-terminal domain.
    J Mol Biol. 2006 Jun 9;359(3):798-804 PMID: 16647716
  41. Accurate determination of local defocus and specimen tilt in electron microscopy.
    J Struct Biol. 2003 Jun;142(3):334-47 PMID: 12781660
  42. Ongoing and future developments at the Universal Protein Resource.
    Nucleic Acids Res. 2011 Jan;39(Database issue):D214-9 PMID: 21051339
  43. On the last common ancestor and early evolution of eukaryotes: reconstructing the history of mitochondrial ribosomes.
    Res Microbiol. 2011 Jan;162(1):53-70 PMID: 21034815
  44. Knockdown of human Oxa1l impairs the biogenesis of F1Fo-ATP synthase and NADH:ubiquinone oxidoreductase.
    J Mol Biol. 2007 Nov 23;374(2):506-16 PMID: 17936786
  45. The comparative RNA web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs.
    BMC Bioinformatics. 2002;3:2 PMID: 11869452
  46. Domain structure and lipid interaction of recombinant yeast Tim44.
    Proc Natl Acad Sci U S A. 1999 Aug 3;96(16):8890-4 PMID: 10430866
  47. Solution structure of the E. coli 70S ribosome at 11.5 A resolution.
    Cell. 2000 Mar 3;100(5):537-49 PMID: 10721991
  48. Co-translational membrane insertion of mitochondrially encoded proteins.
    Biochim Biophys Acta. 2010 Jun;1803(6):767-75 PMID: 19962410
  49. Structural aspects of mitochondrial translational apparatus.
    Curr Opin Struct Biol. 2012 Dec;22(6):797-803 PMID: 22959417
  50. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  51. Whole-exome sequencing identifies a mutation in the mitochondrial ribosome protein MRPL44 to underlie mitochondrial infantile cardiomyopathy.
    J Med Genet. 2013 Mar;50(3):151-9 PMID: 23315540
  52. A structural model for the large subunit of the mammalian mitochondrial ribosome.
    J Mol Biol. 2006 Apr 21;358(1):193-212 PMID: 16510155
  53. Crystal structure of the ribosome at 5.5 A resolution.
    Science. 2001 May 4;292(5518):883-96 PMID: 11283358
  54. RELION: implementation of a Bayesian approach to cryo-EM structure determination.
    J Struct Biol. 2012 Dec;180(3):519-30 PMID: 23000701
Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
Published
2014-01-23
Epub
2013-00-22
Pages
515-9
Language
English
Region
England
NLM ID
0410462
Subset
IM
Databases
PDB
Analysis Services
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