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

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, ther...

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Main Authors: Tatsuhisa Tsuboi, Matheus P Viana, Fan Xu, Jingwen Yu, Raghav Chanchani, Ximena G Arceo, Evelina Tutucci, Joonhyuk Choi, Yang S Chen, Robert H Singer, Susanne M Rafelski, Brian M Zid
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-08-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/57814
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spelling doaj-50c39e2aaf1d4fd7a576af51695215702021-05-05T21:23:40ZengeLife Sciences Publications LtdeLife2050-084X2020-08-01910.7554/eLife.57814Mitochondrial volume fraction and translation duration impact mitochondrial mRNA localization and protein synthesisTatsuhisa Tsuboi0https://orcid.org/0000-0003-3249-030XMatheus P Viana1Fan Xu2Jingwen Yu3Raghav Chanchani4Ximena G Arceo5Evelina Tutucci6https://orcid.org/0000-0002-1998-7146Joonhyuk Choi7Yang S Chen8Robert H Singer9https://orcid.org/0000-0002-6725-0093Susanne M Rafelski10Brian M Zid11https://orcid.org/0000-0003-1876-2479Department of Chemistry and Biochemistry, University of California San Diego, La Jolla, United States; Department of Developmental and Cell Biology and Center for Complex Biological Systems, University of California Irvine, Irvine, United States; Division of Biological Science, Graduate School of Science, Nagoya University, Nagoya, JapanDepartment of Developmental and Cell Biology and Center for Complex Biological Systems, University of California Irvine, Irvine, United StatesDepartment of Chemistry and Biochemistry, University of California San Diego, La Jolla, United StatesDepartment of Chemistry and Biochemistry, University of California San Diego, La Jolla, United StatesDepartment of Chemistry and Biochemistry, University of California San Diego, La Jolla, United StatesDepartment of Chemistry and Biochemistry, University of California San Diego, La Jolla, United StatesDepartment of Anatomy and Structural Biology, Albert Einstein College of Medicine, Bronx, United StatesDepartment of Chemistry and Biochemistry, University of California San Diego, La Jolla, United StatesDepartment of Chemistry and Biochemistry, University of California San Diego, La Jolla, United StatesDepartment of Anatomy and Structural Biology, Albert Einstein College of Medicine, Bronx, United States; Gruss-Lipper Biophotonics Center, Albert Einstein College of Medicine, Bronx, United States; Department of Neuroscience, Albert Einstein College of Medicine, Bronx, United States; Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesDepartment of Developmental and Cell Biology and Center for Complex Biological Systems, University of California Irvine, Irvine, United StatesDepartment of Chemistry and Biochemistry, University of California San Diego, La Jolla, United StatesMitochondria 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.https://elifesciences.org/articles/57814mRNA localizationmitochondriaprotein synthesis
collection DOAJ
language English
format Article
sources DOAJ
author Tatsuhisa Tsuboi
Matheus P Viana
Fan Xu
Jingwen Yu
Raghav Chanchani
Ximena G Arceo
Evelina Tutucci
Joonhyuk Choi
Yang S Chen
Robert H Singer
Susanne M Rafelski
Brian M Zid
spellingShingle Tatsuhisa Tsuboi
Matheus P Viana
Fan Xu
Jingwen Yu
Raghav Chanchani
Ximena G Arceo
Evelina Tutucci
Joonhyuk Choi
Yang S Chen
Robert H Singer
Susanne M Rafelski
Brian M Zid
Mitochondrial volume fraction and translation duration impact mitochondrial mRNA localization and protein synthesis
eLife
mRNA localization
mitochondria
protein synthesis
author_facet Tatsuhisa Tsuboi
Matheus P Viana
Fan Xu
Jingwen Yu
Raghav Chanchani
Ximena G Arceo
Evelina Tutucci
Joonhyuk Choi
Yang S Chen
Robert H Singer
Susanne M Rafelski
Brian M Zid
author_sort Tatsuhisa Tsuboi
title Mitochondrial volume fraction and translation duration impact mitochondrial mRNA localization and protein synthesis
title_short Mitochondrial volume fraction and translation duration impact mitochondrial mRNA localization and protein synthesis
title_full Mitochondrial volume fraction and translation duration impact mitochondrial mRNA localization and protein synthesis
title_fullStr Mitochondrial volume fraction and translation duration impact mitochondrial mRNA localization and protein synthesis
title_full_unstemmed Mitochondrial volume fraction and translation duration impact mitochondrial mRNA localization and protein synthesis
title_sort mitochondrial volume fraction and translation duration impact mitochondrial mrna localization and protein synthesis
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2020-08-01
description 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.
topic mRNA localization
mitochondria
protein synthesis
url https://elifesciences.org/articles/57814
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