Ratchet, swivel, tilt and roll: a complete description of subunit rotation in the ribosome.


Journal

Nucleic acids research
ISSN: 1362-4962
Titre abrégé: Nucleic Acids Res
Pays: England
ID NLM: 0411011

Informations de publication

Date de publication:
25 01 2023
Historique:
accepted: 06 12 2022
revised: 01 12 2022
received: 23 08 2022
pubmed: 31 12 2022
medline: 31 1 2023
entrez: 30 12 2022
Statut: ppublish

Résumé

Protein synthesis by the ribosome requires large-scale rearrangements of the 'small' subunit (SSU; ∼1 MDa), including inter- and intra-subunit rotational motions. However, with nearly 2000 structures of ribosomes and ribosomal subunits now publicly available, it is exceedingly difficult to design experiments based on analysis of all known rotation states. To overcome this, we developed an approach where the orientation of each SSU head and body is described in terms of three angular coordinates (rotation, tilt and tilt direction) and a single translation. By considering the entire RCSB PDB database, we describe 1208 fully-assembled ribosome complexes and 334 isolated small subunits, which span >50 species. This reveals aspects of subunit rearrangements that are universal, and others that are organism/domain-specific. For example, we show that tilt-like rearrangements of the SSU body (i.e. 'rolling') are pervasive in both prokaryotic and eukaryotic (cytosolic and mitochondrial) ribosomes. As another example, domain orientations associated with frameshifting in bacteria are similar to those found in eukaryotic ribosomes. Together, this study establishes a common foundation with which structural, simulation, single-molecule and biochemical efforts can more precisely interrogate the dynamics of this prototypical molecular machine.

Identifiants

pubmed: 36583339
pii: 6965446
doi: 10.1093/nar/gkac1211
pmc: PMC9881166
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

919-934

Subventions

Organisme : NIGMS NIH HHS
ID : T32 GM135060
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM093278
Pays : United States

Informations de copyright

© The Author(s) 2022. Published by Oxford University Press on behalf of Nucleic Acids Research.

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Auteurs

Asem Hassan (A)

Department of Physics, Northeastern University, Dana Research Center 111, 360 Huntington Ave, Boston, MA 02115, USA.
Center for Theoretical Biological Physics, Northeastern University, 360 Huntington Ave, Boston, MA 02115, USA.

Sandra Byju (S)

Department of Physics, Northeastern University, Dana Research Center 111, 360 Huntington Ave, Boston, MA 02115, USA.
Center for Theoretical Biological Physics, Northeastern University, 360 Huntington Ave, Boston, MA 02115, USA.

Frederico Campos Freitas (FC)

Laboratório de Biofísica Teórica, Departamento de Física, Instituto de Ciências Exatas, Naturais e Educação, Universidade Federal do Triângulo Mineiro, Uberaba, MG 38064-200, Brazil.

Claude Roc (C)

Department of Physics, Northeastern University, Dana Research Center 111, 360 Huntington Ave, Boston, MA 02115, USA.

Nisaa Pender (N)

Department of Physics, Northeastern University, Dana Research Center 111, 360 Huntington Ave, Boston, MA 02115, USA.

Kien Nguyen (K)

Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.

Evelyn M Kimbrough (EM)

Department of Biochemistry, Emory University, Rollins Research Center 4027, 1510 Clifton Rd NE, Atlanta, GA 30322, USA.
Department of Chemistry, Emory University, 1515 Dickey Dr, Atlanta, GA 30322, USA.

Jacob M Mattingly (JM)

Department of Biochemistry, Emory University, Rollins Research Center 4027, 1510 Clifton Rd NE, Atlanta, GA 30322, USA.

Ruben L Gonzalez (RL)

Department of Chemistry, Columbia University, New York, NY 10027, USA.

Ronaldo Junio de Oliveira (RJ)

Laboratório de Biofísica Teórica, Departamento de Física, Instituto de Ciências Exatas, Naturais e Educação, Universidade Federal do Triângulo Mineiro, Uberaba, MG 38064-200, Brazil.

Christine M Dunham (CM)

Department of Biochemistry, Emory University, Rollins Research Center 4027, 1510 Clifton Rd NE, Atlanta, GA 30322, USA.

Paul C Whitford (PC)

Department of Physics, Northeastern University, Dana Research Center 111, 360 Huntington Ave, Boston, MA 02115, USA.
Center for Theoretical Biological Physics, Northeastern University, 360 Huntington Ave, Boston, MA 02115, USA.

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Classifications MeSH