Coupling of ribosome biogenesis and translation initiation in human mitochondria

Abstract Biogenesis of mitoribosomes requires dedicated chaperones, RNA-modifying enzymes, and GTPases, and defects in mitoribosome assembly lead to severe mitochondriopathies in humans. Here, we characterize late-step assembly states of the small mitoribosomal subunit (mtSSU) by combining genetic p...

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Main Authors: Marleen Heinrichs, Anna Franziska Finke, Shintaro Aibara, Angelique Krempler, Angela Boshnakovska, Peter Rehling, Hauke S. Hillen, Ricarda Richter-Dennerlein
Format: Article
Language:English
Published: Nature Portfolio 2025-04-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-58827-x
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author Marleen Heinrichs
Anna Franziska Finke
Shintaro Aibara
Angelique Krempler
Angela Boshnakovska
Peter Rehling
Hauke S. Hillen
Ricarda Richter-Dennerlein
author_facet Marleen Heinrichs
Anna Franziska Finke
Shintaro Aibara
Angelique Krempler
Angela Boshnakovska
Peter Rehling
Hauke S. Hillen
Ricarda Richter-Dennerlein
author_sort Marleen Heinrichs
collection DOAJ
description Abstract Biogenesis of mitoribosomes requires dedicated chaperones, RNA-modifying enzymes, and GTPases, and defects in mitoribosome assembly lead to severe mitochondriopathies in humans. Here, we characterize late-step assembly states of the small mitoribosomal subunit (mtSSU) by combining genetic perturbation and mutagenesis analysis with biochemical and structural approaches. Isolation of native mtSSU biogenesis intermediates via a FLAG-tagged variant of the GTPase MTG3 reveals three distinct assembly states, which show how factors cooperate to mature the 12S rRNA. In addition, we observe four distinct primed initiation mtSSU states with an incompletely matured rRNA, suggesting that biogenesis and translation initiation are not mutually exclusive processes but can occur simultaneously. Together, these results provide insights into mtSSU biogenesis and suggest a functional coupling between ribosome biogenesis and translation initiation in human mitochondria.
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spelling doaj-art-5ddfc481cd164091ba9d7325f128c8812025-08-20T02:28:09ZengNature PortfolioNature Communications2041-17232025-04-0116111610.1038/s41467-025-58827-xCoupling of ribosome biogenesis and translation initiation in human mitochondriaMarleen Heinrichs0Anna Franziska Finke1Shintaro Aibara2Angelique Krempler3Angela Boshnakovska4Peter Rehling5Hauke S. Hillen6Ricarda Richter-Dennerlein7Department of Molecular Biology, University Medical Center GöttingenDepartment of Cellular Biochemistry, University Medical Center GöttingenDepartment of Molecular Biology, Max Planck Institute for Multidisciplinary SciencesDepartment of Molecular Biology, University Medical Center GöttingenDepartment of Cellular Biochemistry, University Medical Center GöttingenCluster of Excellence “Multiscale Bioimaging: from Molecular Machines to Networks of Excitable Cells” (MBExC), University of GöttingenCluster of Excellence “Multiscale Bioimaging: from Molecular Machines to Networks of Excitable Cells” (MBExC), University of GöttingenDepartment of Molecular Biology, University Medical Center GöttingenAbstract Biogenesis of mitoribosomes requires dedicated chaperones, RNA-modifying enzymes, and GTPases, and defects in mitoribosome assembly lead to severe mitochondriopathies in humans. Here, we characterize late-step assembly states of the small mitoribosomal subunit (mtSSU) by combining genetic perturbation and mutagenesis analysis with biochemical and structural approaches. Isolation of native mtSSU biogenesis intermediates via a FLAG-tagged variant of the GTPase MTG3 reveals three distinct assembly states, which show how factors cooperate to mature the 12S rRNA. In addition, we observe four distinct primed initiation mtSSU states with an incompletely matured rRNA, suggesting that biogenesis and translation initiation are not mutually exclusive processes but can occur simultaneously. Together, these results provide insights into mtSSU biogenesis and suggest a functional coupling between ribosome biogenesis and translation initiation in human mitochondria.https://doi.org/10.1038/s41467-025-58827-x
spellingShingle Marleen Heinrichs
Anna Franziska Finke
Shintaro Aibara
Angelique Krempler
Angela Boshnakovska
Peter Rehling
Hauke S. Hillen
Ricarda Richter-Dennerlein
Coupling of ribosome biogenesis and translation initiation in human mitochondria
Nature Communications
title Coupling of ribosome biogenesis and translation initiation in human mitochondria
title_full Coupling of ribosome biogenesis and translation initiation in human mitochondria
title_fullStr Coupling of ribosome biogenesis and translation initiation in human mitochondria
title_full_unstemmed Coupling of ribosome biogenesis and translation initiation in human mitochondria
title_short Coupling of ribosome biogenesis and translation initiation in human mitochondria
title_sort coupling of ribosome biogenesis and translation initiation in human mitochondria
url https://doi.org/10.1038/s41467-025-58827-x
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