The interplay between ribosomal protein (RP) composition and mitochondrial function is essential for energy homeostasis. Balanced RP production optimizes protein synthesis while minimizing energy costs, but its impact on mitochondrial functionality remains unclear. Here, we investigated haploinsufficiency for RP genes (rps-10, rpl-5, rpl-33, and rps-23) in Caenorhabditis elegans and corresponding reductions in human lymphoblast cells. Significant mitochondrial morphological differences, upregulation of glutathione transferases, and SKN-1–dependent oxidative stress resistance were observed across mutants. Loss of a Datasingle rps-10 copy reduced mitochondrial activity, energy levels, and oxygen consumption, mirrored by similar reductions in mitochondrial activity and energy levels in lymphoblast cells with 50% lower RPS10 transcripts. Both systems exhibited altered translation efficiency (TE) of mitochondrial electron transport chain components, suggesting a conserved mechanism to adjust mitochondrial protein synthesis under ribosomal stress. Finally, mitochondrial membrane and cytosolic RPs showed significant RNA and TE covariation in lymphoblastoid cells, highlighting the interplay between protein synthesis machinery and mitochondrial energy production.
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January 09 2025
Differential impacts of ribosomal protein haploinsufficiency on mitochondrial function
Agustian Surya
,
Agustian Surya
(Formal analysis, Investigation, Methodology, Validation, Writing - original draft)
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
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Blythe Marie Bolton
,
Blythe Marie Bolton
(Data curation, Investigation, Methodology, Resources, Validation, Visualization, Writing - review & editing)
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
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Reed Rothe
,
Reed Rothe
(Formal analysis, Software, Visualization)
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
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Raquel Mejia-Trujillo
,
Raquel Mejia-Trujillo
(Data curation, Formal analysis, Visualization, Writing - review & editing)
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
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Amanda Leonita
,
Amanda Leonita
(Investigation)
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
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Qiuxia Zhao
,
Qiuxia Zhao
(Resources, Validation)
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
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Alia Arya
,
Alia Arya
(Formal analysis, Investigation)
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
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Yue Liu
,
Yue Liu
(Data curation, Visualization)
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
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Rekha Rangan
,
Rekha Rangan
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
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Yasash Gorusu
,
Yasash Gorusu
(Investigation)
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
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Pamela Nguyen
,
Pamela Nguyen
(Data curation, Formal analysis, Software)
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
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Can Cenik
,
Can Cenik
(Funding acquisition, Supervision, Writing - review & editing)
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
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Elif Sarinay Cenik
(Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Supervision, Visualization, Writing - original draft, Writing - review & editing)
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
Correspondence to Elif Sarinay Cenik: [email protected]
Search for other works by this author on:
Agustian Surya
Formal analysis, Investigation, Methodology, Validation, Writing - original draft
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
Blythe Marie Bolton
Data curation, Investigation, Methodology, Resources, Validation, Visualization, Writing - review & editing
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
Reed Rothe
Formal analysis, Software, Visualization
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
Raquel Mejia-Trujillo
Data curation, Formal analysis, Visualization, Writing - review & editing
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
Amanda Leonita
Investigation
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
Qiuxia Zhao
Resources, Validation
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
Alia Arya
Formal analysis, Investigation
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
Yue Liu
Data curation, Visualization
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
Rekha Rangan
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
Yasash Gorusu
Investigation
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
Pamela Nguyen
Data curation, Formal analysis, Software
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
Can Cenik
Funding acquisition, Supervision, Writing - review & editing
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
Elif Sarinay Cenik
Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Supervision, Visualization, Writing - original draft, Writing - review & editing
1Department of Molecular Biosciences,
University of Texas at Austin
, Austin, TX, USA
Correspondence to Elif Sarinay Cenik: [email protected]
Disclosures: The authors declare no competing interests exist.
Received:
April 17 2024
Revision Received:
October 19 2024
Accepted:
November 26 2024
Online ISSN: 1540-8140
Print ISSN: 0021-9525
Funder(s):
National Institutes of Health
Funder(s):
National Institute of General Medical Sciences
- Award Id(s): R35GM138340,R35GM150667
Funder(s):
Welch Foundation
- Award Id(s): F-2133-20230405,F-2027-20230405
Funder(s):
NIH Office of Research Infrastructure Programs
- Award Id(s): P40 OD010440
© 2025 Surya et al.
2024
Surya et al.
This article is distributed under the terms as described at https://rupress.org/pages/terms102024/.
J Cell Biol (2025) 224 (3): e202404084.
Article history
Received:
April 17 2024
Revision Received:
October 19 2024
Accepted:
November 26 2024
Citation
Agustian Surya, Blythe Marie Bolton, Reed Rothe, Raquel Mejia-Trujillo, Amanda Leonita, Qiuxia Zhao, Alia Arya, Yue Liu, Rekha Rangan, Yasash Gorusu, Pamela Nguyen, Can Cenik, Elif Sarinay Cenik; Differential impacts of ribosomal protein haploinsufficiency on mitochondrial function. J Cell Biol 3 March 2025; 224 (3): e202404084. doi: https://doi.org/10.1083/jcb.202404084
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