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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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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1714604785880006656 |