Literature DB >> 32762840

Mitochondrial volume fraction and translation duration impact mitochondrial mRNA localization and protein synthesis.

Tatsuhisa Tsuboi1,2,3, Matheus P Viana2, Fan Xu1, Jingwen Yu1, Raghav Chanchani1, Ximena G Arceo1, Evelina Tutucci4, Joonhyuk Choi1, Yang S Chen1, Robert H Singer4,5,6,7, Susanne M Rafelski2, Brian M Zid1.   

Abstract

Mitochondria are dynamic organelles that must precisely control their protein composition according to cellular energy demand. Although nuclear-encoded mRNAs can be localized to the mitochondrial surface, the importance of this localization is unclear. As yeast switch to respiratory metabolism, there is an increase in the fraction of the cytoplasm that is mitochondrial. Our data point to this change in mitochondrial volume fraction increasing the localization of certain nuclear-encoded mRNAs to the surface of the mitochondria. We show that mitochondrial mRNA localization is necessary and sufficient to increase protein production to levels required during respiratory growth. Furthermore, we find that ribosome stalling impacts mRNA sensitivity to mitochondrial volume fraction and counterintuitively leads to enhanced protein synthesis by increasing mRNA localization to mitochondria. This points to a mechanism by which cells are able to use translation elongation and the geometric constraints of the cell to fine-tune organelle-specific gene expression through mRNA localization.
© 2020, Tsuboi et al.

Entities:  

Keywords:  S. cerevisiae; cell biology; chromosomes; gene expression; mRNA localization; mitochondria; protein synthesis

Mesh:

Substances:

Year:  2020        PMID: 32762840      PMCID: PMC7413667          DOI: 10.7554/eLife.57814

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.140


  60 in total

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Journal:  FEBS Lett       Date:  1979-07-15       Impact factor: 4.124

2.  Single-mRNA detection in living S. cerevisiae using a re-engineered MS2 system.

Authors:  Evelina Tutucci; Maria Vera; Robert H Singer
Journal:  Nat Protoc       Date:  2018-10       Impact factor: 13.491

3.  F1-dependent translation of mitochondrially encoded Atp6p and Atp8p subunits of yeast ATP synthase.

Authors:  Malgorzata Rak; Alexander Tzagoloff
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4.  TrackMate: An open and extensible platform for single-particle tracking.

Authors:  Jean-Yves Tinevez; Nick Perry; Johannes Schindelin; Genevieve M Hoopes; Gregory D Reynolds; Emmanuel Laplantine; Sebastian Y Bednarek; Spencer L Shorte; Kevin W Eliceiri
Journal:  Methods       Date:  2016-10-03       Impact factor: 3.608

5.  Localization of mRNAs coding for mitochondrial proteins in the yeast Saccharomyces cerevisiae.

Authors:  Noga Gadir; Liora Haim-Vilmovsky; Judith Kraut-Cohen; Jeffrey E Gerst
Journal:  RNA       Date:  2011-06-24       Impact factor: 4.942

Review 6.  Roadblocks and resolutions in eukaryotic translation.

Authors:  Anthony P Schuller; Rachel Green
Journal:  Nat Rev Mol Cell Biol       Date:  2018-08       Impact factor: 94.444

7.  Synchronized mitochondrial and cytosolic translation programs.

Authors:  Mary T Couvillion; Iliana C Soto; Gergana Shipkovenska; L Stirling Churchman
Journal:  Nature       Date:  2016-05-11       Impact factor: 49.962

8.  An improved MS2 system for accurate reporting of the mRNA life cycle.

Authors:  Evelina Tutucci; Maria Vera; Jeetayu Biswas; Jennifer Garcia; Roy Parker; Robert H Singer
Journal:  Nat Methods       Date:  2017-11-13       Impact factor: 28.547

9.  Definition of a High-Confidence Mitochondrial Proteome at Quantitative Scale.

Authors:  Marcel Morgenstern; Sebastian B Stiller; Philipp Lübbert; Christian D Peikert; Stefan Dannenmaier; Friedel Drepper; Uri Weill; Philipp Höß; Reinhild Feuerstein; Michael Gebert; Maria Bohnert; Martin van der Laan; Maya Schuldiner; Conny Schütze; Silke Oeljeklaus; Nikolaus Pfanner; Nils Wiedemann; Bettina Warscheid
Journal:  Cell Rep       Date:  2017-06-27       Impact factor: 9.995

10.  Specialized ribosomes and specific ribosomal protein paralogs control translation of mitochondrial proteins.

Authors:  Nadav Segev; Jeffrey E Gerst
Journal:  J Cell Biol       Date:  2017-11-08       Impact factor: 10.539

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  7 in total

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Journal:  Life Sci Alliance       Date:  2022-10-17

Review 2.  Intracellular mRNA transport and localized translation.

Authors:  Sulagna Das; Maria Vera; Valentina Gandin; Robert H Singer; Evelina Tutucci
Journal:  Nat Rev Mol Cell Biol       Date:  2021-04-09       Impact factor: 113.915

Review 3.  Cytosolic Quality Control of Mitochondrial Protein Precursors-The Early Stages of the Organelle Biogenesis.

Authors:  Anna M Lenkiewicz; Magda Krakowczyk; Piotr Bragoszewski
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4.  Mitochondrial mRNA localization is governed by translation kinetics and spatial transport.

Authors:  Ximena G Arceo; Elena F Koslover; Brian M Zid; Aidan I Brown
Journal:  PLoS Comput Biol       Date:  2022-08-19       Impact factor: 4.779

5.  Rvb1/Rvb2 proteins couple transcription and translation during glucose starvation.

Authors:  Yang S Chen; Wanfu Hou; Sharon Tracy; Alex T Harvey; Vince Harjono; Fan Xu; James J Moresco; John R Yates; Brian M Zid
Journal:  Elife       Date:  2022-09-15       Impact factor: 8.713

Review 6.  Localization and RNA Binding of Mitochondrial Aminoacyl tRNA Synthetases.

Authors:  Shahar Garin; Ofri Levi; Bar Cohen; Adi Golani-Armon; Yoav S Arava
Journal:  Genes (Basel)       Date:  2020-10-12       Impact factor: 4.096

7.  Alternative 3' UTRs play a widespread role in translation-independent mRNA association with the endoplasmic reticulum.

Authors:  Larry C Cheng; Dinghai Zheng; Qiang Zhang; Aysegul Guvenek; Hong Cheng; Bin Tian
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  7 in total

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