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  • 1. Bauerschmitt, Heike
    et al.
    Mick, David
    Deckers, Markus
    Vollmer, C
    Funes, S
    Kehrein, Kirsten
    University of Kaiserslautern, Germany.
    Ott, Martin
    University of Kaiserslautern, Germany.
    Rehling, Peter
    Herrmann, Johannes
    Ribosome-binding proteins Mdm38 and Mba1 display overlapping functions for regulation of mitochondrial translation2010In: Molecular Biology of the Cell, ISSN 1059-1524, E-ISSN 1939-4586, Vol. 21, no 12, p. 1937-1944Article in journal (Other academic)
    Abstract [en]

    Biogenesis of respiratory chain complexes depends on the expression of mitochondrial-encoded subunits. Their synthesis occurs on membrane-associated ribosomes and is probably coupled to their membrane insertion. Defects in expression of mitochondrial translation products are among the major causes of mitochondrial disorders. Mdm38 is related to Letm1, a protein affected in Wolf-Hirschhorn syndrome patients. Like Mba1 and Oxa1, Mdm38 is an inner membrane protein that interacts with ribosomes and is involved in respiratory chain biogenesis. We find that simultaneous loss of Mba1 and Mdm38 causes severe synthetic defects in the biogenesis of cytochrome reductase and cytochrome oxidase. These defects are not due to a compromised membrane binding of ribosomes but the consequence of a mis-regulation in the synthesis of Cox1 and cytochrome b. Cox1 expression is restored by replacing Cox1-specific regulatory regions in the mRNA. We conclude, that Mdm38 and Mba1 exhibit overlapping regulatory functions in translation of selected mitochondrial mRNAs.

  • 2.
    Gruschke, Steffi
    et al.
    Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics.
    Kehrein, Kirsten
    Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics.
    Roempler, Katharina
    Groene, Kerstin
    Israel, Lars
    Imhof, Axel
    Herrmann, Johannes M.
    Ott, Martin
    Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics.
    Cbp3-Cbp6 interacts with the yeast mitochondrial ribosomal tunnel exit and promotes cytochrome b synthesis and assembly2011In: Journal of Cell Biology, ISSN 0021-9525, E-ISSN 1540-8140, Vol. 193, no 6, p. 1101-1114Article in journal (Refereed)
    Abstract [en]

    Mitochondria contain their own genetic system to express a small number of hydrophobic polypeptides, including cytochrome b, an essential subunit of the bc(1) complex of the respiratory chain. In this paper, we show in yeast that Cbp3, a bc(1) complex assembly factor, and Cbp6, a regulator of cytochrome b translation, form a complex that associates with the polypeptide tunnel exit of mitochondrial ribosomes and that exhibits two important functions in the biogenesis of cytochrome b. On the one hand, the interaction of Cbp3 and Cbp6 with mitochondrial ribosomes is necessary for efficient translation of cytochrome b messenger ribonucleic acid or transcript. On the other hand, the Cbp3-Cbp6 complex interacts directly with newly synthesized cytochrome b in an assembly intermediate that is not ribosome bound and that contains the assembly factor Cbp4. Our results suggest that synthesis of cytochrome b occurs preferentially on those ribosomes that have the Cbp3-Cbp6 complex bound to their tunnel exit, an arrangement that may ensure tight coordination of cytochrome b synthesis and assembly.

  • 3.
    Gruschke, Steffi
    et al.
    Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics.
    Römpler, Katharina
    Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics.
    Hildenbeutel, Markus
    Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics.
    Kehrein, Kirsten
    Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics.
    Kuehl, Inge
    Bonnefoy, Nathalie
    Ott, Martin
    Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics.
    The Cbp3-Cbp6 complex coordinates cytochrome b synthesis with bc(1) complex assembly in yeast mitochondria2012In: Journal of Cell Biology, ISSN 0021-9525, E-ISSN 1540-8140, Vol. 199, no 1, p. 137-150Article in journal (Refereed)
    Abstract [en]

    Respiratory chain complexes in mitochondria are assembled from subunits derived from two genetic systems. For example, the bc1 complex consists of nine nuclear encoded subunits and the mitochondrially encoded subunit cytochrome b. We recently showed that the Cbp3-Cbp6 complex has a dual function for biogenesis of cytochrome b: it is both required for efficient synthesis of cytochrome b and for protection of the newly synthesized protein from proteolysis. Here, we report that Cbp3-Cbp6 also coordinates cytochrome b synthesis with bc1 complex assembly. We show that newly synthesized cytochrome b assembled through a series of four assembly intermediates. Blocking assembly at early and intermediate steps resulted in sequestration of Cbp3-Cbp6 in a cytochrome b-containing complex, thereby making Cbp3-Cbp6 unavailable for cytochrome b synthesis and thus reducing overall cytochrome b levels. This feedback loop regulates protein synthesis at the inner mitochondrial membrane by directly monitoring the efficiency of bc1 complex assembly.

  • 4.
    Kehrein, Kirsten
    Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics.
    Organization of mitochondrial gene expression in yeast: Specific features of organellar protein synthesis2014Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    Mitochondria contain their own genetic system, encoding key subunits of the oxidative phosphorylation system. These subunits are expressed by an organelle-specific gene expression machinery. This work revealed a number of fundamental aspects of mitochondrial gene expression and provides evidence that this process is organized in a unique and organelle-specific manner which likely evolved to optimize protein synthesis and assembly in mitochondria. Most importantly, improving the experimental handling of ribosomes we could show that mitochondrial ribosomes are organized in large assemblies that we termed MIOREX complexes. Ribosomes present in these complexes organize gene expression by recruiting multiple factors required for post-transcriptional steps. In addition, we could reveal mechanisms by which ribosome-interactor complexes modulate and coordinate the expression and assembly of the respiratory chain subunits. For example we showed that the Cbp3-Cbp6 complex binds to the ribosome in proximity to the tunnel exit to coordinate synthesis and assembly of cytochrome b. This location perfectly positions Cbp3-Cbp6 for direct binding to newly synthesized cytochrome b and permits Cbp3-Cbp6 to establish a feedback loop that allows modulation of cytochrome b synthesis in response to assembly efficiency. Likewise the interaction of the membrane-anchor proteins Mba1 and Mdm38 with the tunnel exit region enables them to participate in the translation of the two intron-encoding genes COX1 and COB in addition to their role in membrane insertion.  In summary, work presented in this thesis shows that mitochondrial gene expression is a highly organized and regulated process. The concepts and technical innovations will facilitate the elucidation of many additional and important aspects and therefore contribute to the general understanding of how proteins are synthesized in mitochondria.

  • 5.
    Kehrein, Kirsten
    et al.
    Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics.
    Bonnefoy, Nathalie
    Ott, Martin
    Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics.
    Mitochondrial Protein Synthesis: Efficiency and Accuracy2013In: Antioxidants and Redox Signaling, ISSN 1523-0864, E-ISSN 1557-7716, Vol. 19, no 16, p. 1928-1939Article, review/survey (Refereed)
    Abstract [en]

    Significance: The mitochondrial genetic system is responsible for the production of a few core-subunits of the respiratory chain and ATP synthase, the membrane protein complexes driving oxidative phosphorylation (OXPHOS). Efficiency and accuracy of mitochondrial protein synthesis determines how efficiently new OXPHOS complexes can be made. Recent Advances: The system responsible for expression of the mitochondrial-encoded subunits developed from that of the bacterial ancestor of mitochondria. Importantly, many aspects of genome organization, transcription, and translation have diverged during evolution. Recent research has provided new insights into the architecture, regulation, and organelle-specific features of mitochondrial translation. Mitochondrial ribosomes contain a number of proteins absent from prokaryotic ribosomes, implying that in mitochondria, ribosomes were tailored to fit the requirements of the organelle. In addition, mitochondrial gene expression is regulated post-transcriptionally by a number of mRNA-specific translational activators. At least in yeast, these factors can regulate translation in respect to OXPHOS complex assembly to adjust the level of newly synthesized proteins to amounts that can be successfully assembled into respiratory chain complexes. Critical Issues: Mitochondrial gene expression is determining aging in eukaryotes, and a number of recent reports indicate that efficiency of translation directly influences this process. Future Directions: Here we will summarize recent advances in our understanding of mitochondrial protein synthesis by comparing the knowledge acquired in the systems most commonly used to study mitochondrial biogenesis. However, many steps have not been understood mechanistically. Innovative biochemical and genetic approaches have to be elaborated to shed light on these important processes. Antioxid. Redox Signal. 19, 1928-1939.

  • 6.
    Kehrein, Kirsten
    et al.
    Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics.
    Ott, Martin
    Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics.
    Conserved and Organelle-Specific Molecular Mechanisms of Translation in Mitochondria2012In: Organelle Genetics: Evolution of Organelle Genomes and Gene Expression, New York: Springer, 2012, p. 401-429Chapter in book (Refereed)
  • 7.
    Kehrein, Kirsten
    et al.
    Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics.
    Schilling, Ramon
    Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics.
    Vargas Möller-Hergt, Braulio
    Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics.
    Wurm, Christian A.
    Jakobs, Stefan
    Lamkemeyer, Tobias
    Langer, Thomas
    Ott, Martin
    Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics.
    Organization of Mitochondrial Gene Expression in Two Distinct Ribosome-Containing Assemblies2015In: Cell reports, ISSN 2211-1247, E-ISSN 2211-1247, Vol. 10, no 6, p. 843-853Article in journal (Refereed)
    Abstract [en]

    Mitochondria contain their own genetic system that provides subunits of the complexes driving oxidative phosphorylation. A quarter of the mitochondrial proteome participates in gene expression, but how all these factors are orchestrated and spatially organized is currently unknown. Here, we established a method to purify and analyze native and intact complexes of mitochondrial ribosomes. Quantitative mass spectrometry revealed extensive interactions of ribosomes with factors involved in all the steps of posttranscriptional gene expression. These interactions result in large expressosome-like assemblies that we termed mitochondrial organization of gene expression (MIOREX) complexes. Superresolution microscopy revealed that most MIOREX complexes are evenly distributed throughout the mitochondrial network, whereas a subset is present as nucleoid-MIOREX complexes that unite the whole spectrum of organellar gene expression. Our work therefore provides a conceptual framework for the spatial organization of mitochondrial protein synthesis that likely developed to facilitate gene expression in the organelle.

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