The E3 ubiquitin ligase FBXL6 controls the quality of newly synthesized mitochondrial ribosomal proteins
In mammals, about 99% of mitochondrial proteins are synthesized in the cytosol as precursors that are subsequently imported into the organelle. The mitochondrial health and functions rely on an accurate quality control of these imported proteins. Here, we show that the E3 ubiquitin ligase F box/leuc...
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Published in | Cell reports (Cambridge) Vol. 42; no. 6; p. 112579 |
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Main Authors | , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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27.06.2023
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Abstract | In mammals, about 99% of mitochondrial proteins are synthesized in the cytosol as precursors that are subsequently imported into the organelle. The mitochondrial health and functions rely on an accurate quality control of these imported proteins. Here, we show that the E3 ubiquitin ligase F box/leucine-rich-repeat protein 6 (FBXL6) regulates the quality of cytosolically translated mitochondrial proteins. Indeed, we found that FBXL6 substrates are newly synthesized mitochondrial ribosomal proteins. This E3 binds to chaperones involved in the folding and trafficking of newly synthesized peptide and to ribosomal-associated quality control proteins. Deletion of these interacting partners is sufficient to hamper interactions between FBXL6 and its substrate. Furthermore, we show that cells lacking FBXL6 fail to degrade specifically mistranslated mitochondrial ribosomal proteins. Finally, showing the role of FBXL6-dependent mechanism, FBXL6-knockout (KO) cells display mitochondrial ribosomal protein aggregations, altered mitochondrial metabolism, and inhibited cell cycle in oxidative conditions.
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•FBXL6 is a cytosolic E3 ubiquitin ligase contributing to mitochondrial functions•FBXL6 ensures the quality of newly synthesized mitochondrial ribosomal proteins•FBXL6 contributes to the translational-associated quality control
Lavie et al. find that FBXL6 contributes to mitochondrial health by controlling the quality of mitochondrial ribosome proteins prior to their import into the organelle. Moreover, they show that this mechanism is connected to the cytosolic translation-associated quality control and to the folding of newly synthesized proteins. |
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AbstractList | In mammals, about 99% of mitochondrial proteins are synthesized in the cytosol as precursors that are subsequently imported into the organelle. The mitochondrial health and functions rely on an accurate quality control of these imported proteins. Here, we show that the E3 ubiquitin ligase F box/leucine-rich-repeat protein 6 (FBXL6) regulates the quality of cytosolically translated mitochondrial proteins. Indeed, we found that FBXL6 substrates are newly synthesized mitochondrial ribosomal proteins. This E3 binds to chaperones involved in the folding and trafficking of newly synthesized peptide and to ribosomal-associated quality control proteins. Deletion of these interacting partners is sufficient to hamper interactions between FBXL6 and its substrate. Furthermore, we show that cells lacking FBXL6 fail to degrade specifically mistranslated mitochondrial ribosomal proteins. Finally, showing the role of FBXL6-dependent mechanism, FBXL6-knockout (KO) cells display mitochondrial ribosomal protein aggregations, altered mitochondrial metabolism, and inhibited cell cycle in oxidative conditions. In mammals, about 99% of mitochondrial proteins are synthesized in the cytosol as precursors that are subsequently imported into the organelle. The mitochondrial health and functions rely on an accurate quality control of these imported proteins. Here, we show that the E3 ubiquitin ligase F box/leucine-rich-repeat protein 6 (FBXL6) regulates the quality of cytosolically translated mitochondrial proteins. Indeed, we found that FBXL6 substrates are newly synthesized mitochondrial ribosomal proteins. This E3 binds to chaperones involved in the folding and trafficking of newly synthesized peptide and to ribosomal-associated quality control proteins. Deletion of these interacting partners is sufficient to hamper interactions between FBXL6 and its substrate. Furthermore, we show that cells lacking FBXL6 fail to degrade specifically mistranslated mitochondrial ribosomal proteins. Finally, showing the role of FBXL6-dependent mechanism, FBXL6-knockout (KO) cells display mitochondrial ribosomal protein aggregations, altered mitochondrial metabolism, and inhibited cell cycle in oxidative conditions. [Display omitted] •FBXL6 is a cytosolic E3 ubiquitin ligase contributing to mitochondrial functions•FBXL6 ensures the quality of newly synthesized mitochondrial ribosomal proteins•FBXL6 contributes to the translational-associated quality control Lavie et al. find that FBXL6 contributes to mitochondrial health by controlling the quality of mitochondrial ribosome proteins prior to their import into the organelle. Moreover, they show that this mechanism is connected to the cytosolic translation-associated quality control and to the folding of newly synthesized proteins. |
ArticleNumber | 112579 |
Author | Lalou, Claude Lavie, Julie Duchêne, Anne-Marie Dupuy, Jean-William Lacaule, Aurélie Bénard, Giovanni Mahfouf, Walid Raymond, Anne-Aurélie Rezvani, Hamid Reza Ngondo, Richard Patryk Lacombe, Didier Cywinska, Agata Ars |
Author_xml | – sequence: 1 givenname: Julie surname: Lavie fullname: Lavie, Julie organization: Laboratoire Maladies Rares: Génétique et Métabolisme, INSERM U1211, 33076 Bordeaux, France – sequence: 2 givenname: Claude surname: Lalou fullname: Lalou, Claude organization: Laboratoire Maladies Rares: Génétique et Métabolisme, INSERM U1211, 33076 Bordeaux, France – sequence: 3 givenname: Walid surname: Mahfouf fullname: Mahfouf, Walid organization: Université de Bordeaux, 33000 Bordeaux, France – sequence: 4 givenname: Jean-William surname: Dupuy fullname: Dupuy, Jean-William organization: Université de Bordeaux, 33000 Bordeaux, France – sequence: 5 givenname: Aurélie surname: Lacaule fullname: Lacaule, Aurélie organization: Laboratoire Maladies Rares: Génétique et Métabolisme, INSERM U1211, 33076 Bordeaux, France – sequence: 6 givenname: Agata Ars surname: Cywinska fullname: Cywinska, Agata Ars organization: Laboratoire Maladies Rares: Génétique et Métabolisme, INSERM U1211, 33076 Bordeaux, France – sequence: 7 givenname: Didier surname: Lacombe fullname: Lacombe, Didier organization: Laboratoire Maladies Rares: Génétique et Métabolisme, INSERM U1211, 33076 Bordeaux, France – sequence: 8 givenname: Anne-Marie surname: Duchêne fullname: Duchêne, Anne-Marie organization: Université de Strasbourg, CNRS, Institut de Biologie Moléculaire des Plantes, UPR2357, 67000 Strasbourg, France – sequence: 9 givenname: Anne-Aurélie surname: Raymond fullname: Raymond, Anne-Aurélie organization: Université de Bordeaux, 33000 Bordeaux, France – sequence: 10 givenname: Hamid Reza surname: Rezvani fullname: Rezvani, Hamid Reza organization: Université de Bordeaux, 33000 Bordeaux, France – sequence: 11 givenname: Richard Patryk surname: Ngondo fullname: Ngondo, Richard Patryk organization: Université de Strasbourg, CNRS, Institut de Biologie Moléculaire des Plantes, UPR2357, 67000 Strasbourg, France – sequence: 12 givenname: Giovanni orcidid: 0000-0003-0036-9425 surname: Bénard fullname: Bénard, Giovanni email: giovanni.benard@inserm.fr organization: Laboratoire Maladies Rares: Génétique et Métabolisme, INSERM U1211, 33076 Bordeaux, France |
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Keywords | ribosomal proteins protein quality control F box leucin-rich repeat E3 ubiquitin ligase CP: Cell biology mitochondria FBXL6 Mitochondria, ubiquitin, metabolism, protein quality control |
Language | English |
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SubjectTerms | Biochemistry, Molecular Biology CP: Cell biology F box leucin-rich repeat E3 ubiquitin ligase FBXL6 Life Sciences mitochondria protein quality control ribosomal proteins |
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Title | The E3 ubiquitin ligase FBXL6 controls the quality of newly synthesized mitochondrial ribosomal proteins |
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