bims-mitran Biomed News
on Mitochondrial Translation
Issue of 2023‒02‒26
fourteen papers selected by
Andreas Kohler



  1. Cell. 2023 Feb 17. pii: S0092-8674(23)00093-4. [Epub ahead of print]
      Mitochondrial activity differs markedly between organs, but it is not known how and when this arises. Here we show that cell lineage-specific expression profiles involving essential mitochondrial genes emerge at an early stage in mouse development, including tissue-specific isoforms present before organ formation. However, the nuclear transcriptional signatures were not independent of organelle function. Genetically disrupting intra-mitochondrial protein synthesis with two different mtDNA mutations induced cell lineage-specific compensatory responses, including molecular pathways not previously implicated in organellar maintenance. We saw downregulation of genes whose expression is known to exacerbate the effects of exogenous mitochondrial toxins, indicating a transcriptional adaptation to mitochondrial dysfunction during embryonic development. The compensatory pathways were both tissue and mutation specific and under the control of transcription factors which promote organelle resilience. These are likely to contribute to the tissue specificity which characterizes human mitochondrial diseases and are potential targets for organ-directed treatments.
    Keywords:  OXPHOS; RNA-seq; SCENIC; mitochondria; mt-Ta; mtDNA; organogenesis; single-cell
    DOI:  https://doi.org/10.1016/j.cell.2023.01.034
  2. bioRxiv. 2023 Feb 15. pii: 2023.02.09.527880. [Epub ahead of print]
      Mitochondria play critical roles in cellular metabolism, primarily by serving as the site of assembly and function of the oxidative phosphorylation (OXPHOS) machinery. The OXPHOS proteins are encoded by mitochondrial DNA (mtDNA) and nuclear DNA, which reside and are regulated within separate compartments. To unravel how the two gene expression systems collaborate to produce the OXPHOS complexes, the regulatory principles controlling the production of mtDNA-encoded proteins need to be elucidated. In this study, we performed a quantitative analysis of the mitochondrial messenger RNA (mt-mRNA) life cycle to determine which steps of gene expression experience strong regulatory control. Our analysis revealed that the high accumulation of mt-mRNA despite their rapid turnover was made possible by a 700-fold higher transcriptional output than nuclear-encoded OXPHOS genes. In addition, we observed that mt-mRNA processing and its association with the mitochondrial ribosome occur rapidly and that these processes are linked mechanistically. Based on these data, we developed a model of mtDNA expression that is predictive across human cell lines, revealing that differences in turnover and translation efficiency are the major contributors to mitochondrial-encoded protein synthesis. Applying this framework to a disease model of Leigh syndrome, French-Canadian type, we found that the disease-associated nuclear-encoded gene, LRPPRC , acts predominantly by stabilizing mt-mRNA. Our findings provide a comprehensive view of the intricate regulatory mechanisms governing mtDNA-encoded protein synthesis, highlighting the importance of quantitatively analyzing the mitochondrial RNA life cycle in order to decode the regulatory principles of mtDNA expression.
    DOI:  https://doi.org/10.1101/2023.02.09.527880
  3. Bio Protoc. 2023 Feb 05. pii: e4602. [Epub ahead of print]13(3):
      In addition to cytosolic protein synthesis, mitochondria also utilize another translation system that is tailored for mRNAs encoded in the mitochondrial genome. The importance of mitochondrial protein synthesis has been exemplified by the diverse diseases associated with in organello translation deficiencies. Various methods have been developed to monitor mitochondrial translation, such as the classic method of labeling newly synthesized proteins with radioisotopes and the more recent ribosome profiling. However, since these methods always assess the average cell population, measuring the mitochondrial translation capacity in individual cells has been challenging. To overcome this issue, we recently developed mito-fluorescent noncanonical amino acid tagging (FUNCAT) fluorescence-activated cell sorting (FACS), which labels nascent peptides generated by mitochondrial ribosomes with a methionine analog, L-homopropargylglycine (HPG), conjugates the peptides with fluorophores by an in situ click reaction, and detects the signal in individual cells by FACS equipment. With this methodology, the hidden heterogeneity of mitochondrial translation in cell populations can be addressed.
    Keywords:   FACS ; FUNCAT ; Mitochondria ; Mitoribosome ; Translation
    DOI:  https://doi.org/10.21769/BioProtoc.4602
  4. Autophagy. 2023 Feb 20.
      Mitochondrial DNA (mtDNA) is prone to the accumulation of mutations. To prevent harmful mtDNA mutations from being passed on to the next generation, the female germline, through which mtDNA is exclusively inherited, has evolved extensive mtDNA quality control. To dissect the molecular underpinnings of this process, we recently performed a large RNAi screen in Drosophila and uncovered a programmed germline mitophagy (PGM) that is essential for mtDNA quality control. We found that PGM begins as germ cells enter meiosis, induced, at least in part, by the inhibition of the mTor (mechanistic Target of rapamycin) complex 1 (mTorC1). Interestingly, PGM requires the general macroautophagy/autophagy machinery and the mitophagy adaptor BNIP3, but not the canonical mitophagy genes Pink1 and park (parkin), even though they are critical for germline mtDNA quality control. We also identified the RNA-binding protein Atx2 as a major regulator of PGM. This work is the first to identify and implicate a programmed mitophagy event in germline mtDNA quality control, and it highlights the utility of the Drosophila ovary for studying developmentally regulated mitophagy and autophagy in vivo.
    Keywords:  Drosophila; autophagy; germline; mitochondria; mitochondrial DNA; mitophagy; mtDNA; purifying selection
    DOI:  https://doi.org/10.1080/15548627.2023.2182595
  5. Methods Mol Biol. 2023 ;2615 219-228
      Mitochondria are eukaryotic organelles of endosymbiotic origin that contain their own genetic material, mitochondrial DNA (mtDNA), and dedicated systems for mtDNA maintenance and expression. MtDNA molecules encode a limited number of proteins that are nevertheless all essential subunits of the mitochondrial oxidative phosphorylation system. Here, we describe protocols to monitor DNA and RNA synthesis in intact, isolated mitochondria. These in organello synthesis protocols are valuable techniques for studying the mechanisms and regulation of mtDNA maintenance and expression.
    Keywords:  Mitochondria; Radioactive labeling of nucleic acids; in organello replication and transcription; mtDNA; mtDNA maintenance and expression
    DOI:  https://doi.org/10.1007/978-1-0716-2922-2_16
  6. Methods Mol Biol. 2023 ;2615 89-98
      Proper mitochondrial DNA (mtDNA) levels are critical for many cellular biological functions and are associated with aging and many mitochondria disorders. Defects in core subunits of the mtDNA replication machinery lead to decreased mtDNA levels. Other indirect mitochondrial contexts including ATP concentration, lipid composition, and nucleotide composition also contribute to mtDNA maintenance. Furthermore, mtDNA molecules are distributed evenly throughout the mitochondrial network. This uniform distribution pattern is required for oxidative phosphorylation and ATP production and has been linked to many diseases when perturbed. Thus, it is important to visualize mtDNA in the cellular context. Here we provide detailed protocols for cellular visualization of mtDNA using fluorescence in situ hybridization (FISH). The fluorescent signals are targeted to the mtDNA sequence directly, ensuring both sensitivity and specificity. This mtDNA FISH method can be combined with immunostaining and used for visualizing mtDNA-protein interactions and dynamics.
    Keywords:  FISH; Imaging; Microscopy; Mitochondria; Visualization; mtDNA
    DOI:  https://doi.org/10.1007/978-1-0716-2922-2_7
  7. Methods Mol Biol. 2023 ;2615 17-30
      Mitochondria are double membrane-bound eukaryotic organelles with roles in a range of cellular activities including energy conversion, apoptosis, cell signalling, and the biosynthesis of enzyme cofactors. Mitochondria contain their own genome, called mtDNA, which encodes subunits of the oxidative phosphorylation machinery as well as the rRNA and tRNA molecules required for their translation within mitochondria. The ability to isolate highly purified mitochondria from cells has been instrumental in a number of studies of mitochondrial function. Differential centrifugation is a long-established method for the isolation of mitochondria. Cells are subjected to osmotic swelling and disruption, followed by centrifugation in isotonic sucrose solutions to separate mitochondria from other cellular components. We present a method using this principle for the isolation of mitochondria from cultured mammalian cell lines. Mitochondria purified by this method can be further fractionated to investigate protein localization, or act as a starting point to purify mtDNA.
    Keywords:  DNA extraction; Mitochondria; Mitochondrial DNA; Mitochondrial isolation; Protein localization
    DOI:  https://doi.org/10.1007/978-1-0716-2922-2_2
  8. Mol Microbiol. 2023 Feb 24.
      Consistent with other eukaryotes, the Trypanosoma brucei mitochondrial genome encodes mainly hydrophobic core subunits of the oxidative phosphorylation system. These proteins must be co-translationally inserted into the inner mitochondrial membrane and are synthesized by the highly unique trypanosomal mitoribosomes, which have a much higher protein to RNA ratio than any other ribosome. Here, we show that the trypanosomal ortholog of the mitoribosome receptor Mba1 (TbMba1) is essential for normal growth of procyclic trypanosomes but redundant in the bloodstream form, which lacks an oxidative phosphorylation system. Proteomic analyses of TbMba1-depleted mitochondria from procyclic cells revealed reduced levels of many components of the oxidative phosphorylation system, most of which belong to the cytochrome c oxidase (Cox) complex, three subunits of which are mitochondrially encoded. However, the integrity of the mitoribosome and its interaction with the inner membrane were not affected. Pulldown experiments showed that TbMba1 forms a dynamic interaction network that includes the trypanosomal Mdm38/Letm1 ortholog and a trypanosome-specific factor that stabilizes the CoxI and CoxII mRNAs. In summary, our study suggests that the function of Mba1 in the biogenesis of membrane subunits of OXPHOS complexes is conserved among yeast, mammals, and trypanosomes, which belong to two eukaryotic supergroups.
    DOI:  https://doi.org/10.1111/mmi.15048
  9. Methods Mol Biol. 2023 ;2615 345-364
      Chlamydomonas reinhardtii and Saccharomyces cerevisiae are currently the two micro-organisms in which genetic transformation of mitochondria is routinely performed. The generation of a large variety of defined alterations as well as the insertion of ectopic genes in the mitochondrial genome (mtDNA) are possible, especially in yeast. Biolistic transformation of mitochondria is achieved through the bombardment of microprojectiles coated with DNA, which can be incorporated into mtDNA thanks to the highly efficient homologous recombination machinery present in S. cerevisiae and C. reinhardtii organelles. Despite a low frequency of transformation, the isolation of transformants in yeast is relatively quick and easy, since several natural or artificial selectable markers are available, while the selection in C. reinhardtii remains long and awaits new markers. Here, we describe the materials and techniques used to perform biolistic transformation, in order to mutagenize endogenous mitochondrial genes or insert novel markers into mtDNA. Although alternative strategies to edit mtDNA are being set up, so far, insertion of ectopic genes relies on the biolistic transformation techniques.
    Keywords:  Biolistic techniques; Chlamydomonas reinhardtii; Genetic transformation; Homologous recombination; Mitochondrial DNA; Mutagenesis and ectopic gene insertion; Saccharomyces cerevisiae
    DOI:  https://doi.org/10.1007/978-1-0716-2922-2_24
  10. Methods Mol Biol. 2023 ;2615 443-463
      Mitochondrial DNA (mtDNA) deletions underpin mitochondrial dysfunction in human tissues in aging and disease. The multicopy nature of the mitochondrial genome means these mtDNA deletions can occur in varying mutation loads. At low levels, these deletions have no impact, but once the proportion of molecules harbouring a deletion exceeds a threshold level, then dysfunction occurs. The location of the breakpoints and the size of the deletion impact upon the mutation threshold required to cause deficiency of an oxidative phosphorylation complex, and this varies for each of the different complexes. Furthermore, mutation load and deletion species can vary between adjacent cells in a tissue, with a mosaic pattern of mitochondrial dysfunction observed. As such, it is often important for understanding human aging and disease to be able to characterise the mutation load, breakpoints and size of deletion(s) from a single human cell. Here, we detail protocols for laser micro-dissection and single cell lysis from tissues, and the subsequent analysis of deletion size, breakpoints and mutation load using long-range PCR, mtDNA sequencing and real-time PCR, respectively.
    Keywords:  Breakpoint; Heteroplasmy; Mutation load; mtDNA deletion
    DOI:  https://doi.org/10.1007/978-1-0716-2922-2_29
  11. Methods Mol Biol. 2023 ;2615 241-266
      Two-dimensional neutral/neutral agarose gel electrophoresis (2D-AGE) has been employed for nearly two decades in the analysis of replication and maintenance processes of animal mitochondrial DNA, but the method's potential has not been fully exploited. Here, we describe the various steps involved in this technique, from DNA isolation, to two-dimensional neutral/neutral agarose gel electrophoresis (2D-AGE), Southern hybridization and interpretation. We also provide examples of the applicability of 2D-AGE to investigate the different features of mtDNA maintenance and regulation.
    Keywords:  2D-AGE; Gel electrophoresis; Mitochondrial DNA; Recombination; Replication intermediates; Replication mechanism; Replication pausing
    DOI:  https://doi.org/10.1007/978-1-0716-2922-2_18
  12. Methods Mol Biol. 2023 ;2615 79-88
      Mitochondrial DNA (mtDNA) encodes a variety of rRNAs, tRNAs, and respiratory chain complex proteins. The integrity of mtDNA supports the mitochondrial functions and plays an essential role in numerous physiological and pathological processes. Mutations in mtDNA cause metabolic diseases and aging. The mtDNA within the human cells are packaged into hundreds of nucleoids within the mitochondrial matrix. Knowledge of how the nucleoids are dynamically distributed and organized within mitochondria is key to understanding mtDNA structure and functions. Therefore, visualizing the distribution and dynamics of mtDNA within mitochondria is a powerful approach to gain insights into the regulation of mtDNA replication and transcription. In this chapter, we describe the methods of observing mtDNA and its replication with fluorescence microscopy in both fixed and live cells using different labeling strategies.
    Keywords:  BrdU; EdU; Mitochondrial DNA (mtDNA); POLG2; PdG; TFAM
    DOI:  https://doi.org/10.1007/978-1-0716-2922-2_6
  13. Methods Mol Biol. 2023 ;2615 203-217
      Faithful mitochondrial DNA (mtDNA) replication is critical for the proper function of the oxidative phosphorylation system. Problems with mtDNA maintenance, such as replication stalling upon encountering DNA damage, impair this vital function and can potentially lead to disease. An in vitro reconstituted mtDNA replication system can be used to investigate how the mtDNA replisome deals with, for example, oxidatively or UV-damaged DNA. In this chapter, we provide a detailed protocol on how to study the bypass of different types of DNA damage using a rolling circle replication assay. The assay takes advantage of purified recombinant proteins and can be adapted to the examination of various aspects of mtDNA maintenance.
    Keywords:  DNA damage; DNA polymerase; DNA replication; Mitochondrial DNA; Rolling circle
    DOI:  https://doi.org/10.1007/978-1-0716-2922-2_15
  14. Methods Mol Biol. 2023 ;2615 229-240
      The manipulation of mitochondrial DNA (mtDNA) copy number in cultured cells, using substances that interfere with DNA replication, is a useful tool to investigate various aspects of mtDNA maintenance. Here we describe the use of 2',3'-dideoxycytidine (ddC) to induce a reversible reduction of mtDNA copy number in human primary fibroblasts and human embryonic kidney (HEK293) cells. Once the application of ddC is stopped, cells depleted for mtDNA attempt to recover normal mtDNA copy numbers. The dynamics of repopulation of mtDNA provide a valuable measure for the enzymatic activity of the mtDNA replication machinery.
    Keywords:  DNA polymerase γ (POLG); Nucleoside reverse transcriptase inhibitor (NRTI); Quantitative PCR; Replication of mtDNA; Zalcitabine; mtDNA copy number
    DOI:  https://doi.org/10.1007/978-1-0716-2922-2_17