Genetically controlled mtDNA deletions prevent ROS damage by arresting oxidative phosphorylation

Deletion of mitochondrial DNA in eukaryotes is currently attributed to rare accidental events associated with mitochondrial replication or repair of double-strand breaks. We report the discovery that yeast cells arrest harmful intramitochondrial superoxide production by shutting down respiration thr...

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Published in:	eLife Vol. 11
Main Authors:	Stenberg, Simon, Li, Jing, Gjuvsland, Arne B, Persson, Karl, Demitz-Helin, Erik, González Peña, Carles, Yue, Jia-Xing, Gilchrist, Ciaran, Ärengård, Timmy, Ghiaci, Payam, Larsson-Berglund, Lisa, Zackrisson, Martin, Smits, Silvana, Hallin, Johan, Höög, Johanna L, Molin, Mikael, Liti, Gianni, Omholt, Stig W, Warringer, Jonas
Format:	Journal Article
Language:	English
Published:	England eLife Science Publications, Ltd 08-07-2022 eLife Sciences Publications, Ltd eLife Sciences Publications Ltd
Subjects:	Cell Biology Cellbiologi Cells DNA DNA Damage DNA, Mitochondrial - genetics DNA, Mitochondrial - metabolism Enzymes Evolutionary Biology Evolutionsbiologi Genes Genetics Genetics and Genomics Genetik genome editing genome stability Humans metabolism Mitochondria Mitochondria - metabolism Mitochondrial Mitochondrial DNA mitochondrial impairment mtDNA Oxidative Phosphorylation Oxidative Stress Oxidative Stress - genetics Reactive Oxygen Species Reactive Oxygen Species - metabolism Superoxide Superoxides Superoxides - metabolism genome editing genome stability cell biology genetics mitochondrial DNA mitochondrial impairment genomics oxidative stress S. cerevisiae
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Abstract	Deletion of mitochondrial DNA in eukaryotes is currently attributed to rare accidental events associated with mitochondrial replication or repair of double-strand breaks. We report the discovery that yeast cells arrest harmful intramitochondrial superoxide production by shutting down respiration through genetically controlled deletion of mitochondrial oxidative phosphorylation genes. We show that this process critically involves the antioxidant enzyme superoxide dismutase 2 and two-way mitochondrial-nuclear communication through Rtg2 and Rtg3. While mitochondrial DNA homeostasis is rapidly restored after cessation of a short-term superoxide stress, long-term stress causes maladaptive persistence of the deletion process, leading to complete annihilation of the cellular pool of intact mitochondrial genomes and irrevocable loss of respiratory ability. This shows that oxidative stress-induced mitochondrial impairment may be under strict regulatory control. If the results extend to human cells, the results may prove to be of etiological as well as therapeutic importance with regard to age-related mitochondrial impairment and disease.
AbstractList	Deletion of mitochondrial DNA in eukaryotes is currently attributed to rare accidental events associated with mitochondrial replication or repair of double-strand breaks. We report the discovery that yeast cells arrest harmful intramitochondrial superoxide production by shutting down respiration through genetically controlled deletion of mitochondrial oxidative phosphorylation genes. We show that this process critically involves the antioxidant enzyme superoxide dismutase 2 and two-way mitochondrial-nuclear communication through Rtg2 and Rtg3. While mitochondrial DNA homeostasis is rapidly restored after cessation of a short-term superoxide stress, long-term stress causes maladaptive persistence of the deletion process, leading to complete annihilation of the cellular pool of intact mitochondrial genomes and irrevocable loss of respiratory ability. This shows that oxidative stress-induced mitochondrial impairment may be under strict regulatory control. If the results extend to human cells, the results may prove to be of etiological as well as therapeutic importance with regard to age-related mitochondrial impairment and disease. Deletion of mitochondrial DNA in eukaryotes is currently attributed to rare accidental events associated with mitochondrial replication or repair of double-strand breaks. We report the discovery that yeast cells arrest harmful intramitochondrial superoxide production by shutting down respiration through genetically controlled deletion of mitochondrial oxidative phosphorylation genes. We show that this process critically involves the antioxidant enzyme superoxide dismutase 2 and two-way mitochondrial-nuclear communication through Rtg2 and Rtg3. While mitochondrial DNA homeostasis is rapidly restored after cessation of a short-term superoxide stress, long-term stress causes maladaptive persistence of the deletion process, leading to complete annihilation of the cellular pool of intact mitochondrial genomes and irrevocable loss of respiratory ability. This shows that oxidative stress-induced mitochondrial impairment may be under strict regulatory control. If the results extend to human cells, the results may prove to be of etiological as well as therapeutic importance with regard to age-related mitochondrial impairment and disease.Deletion of mitochondrial DNA in eukaryotes is currently attributed to rare accidental events associated with mitochondrial replication or repair of double-strand breaks. We report the discovery that yeast cells arrest harmful intramitochondrial superoxide production by shutting down respiration through genetically controlled deletion of mitochondrial oxidative phosphorylation genes. We show that this process critically involves the antioxidant enzyme superoxide dismutase 2 and two-way mitochondrial-nuclear communication through Rtg2 and Rtg3. While mitochondrial DNA homeostasis is rapidly restored after cessation of a short-term superoxide stress, long-term stress causes maladaptive persistence of the deletion process, leading to complete annihilation of the cellular pool of intact mitochondrial genomes and irrevocable loss of respiratory ability. This shows that oxidative stress-induced mitochondrial impairment may be under strict regulatory control. If the results extend to human cells, the results may prove to be of etiological as well as therapeutic importance with regard to age-related mitochondrial impairment and disease.
Audience	Academic
Author	Ärengård, Timmy Smits, Silvana Yue, Jia-Xing Persson, Karl Larsson-Berglund, Lisa Zackrisson, Martin Omholt, Stig W Li, Jing Liti, Gianni Gilchrist, Ciaran Molin, Mikael Stenberg, Simon González Peña, Carles Höög, Johanna L Warringer, Jonas Ghiaci, Payam Hallin, Johan Demitz-Helin, Erik Gjuvsland, Arne B
Author_xml	– sequence: 1 givenname: Simon orcidid: 0000-0003-0300-1730 surname: Stenberg fullname: Stenberg, Simon organization: Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden – sequence: 2 givenname: Jing surname: Li fullname: Li, Jing organization: Université Côte d'Azur, CNRS, INSERM, IRCAN, Nice, France – sequence: 3 givenname: Arne B surname: Gjuvsland fullname: Gjuvsland, Arne B organization: Centre for Integrative Genetics, Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, Ås, Norway – sequence: 4 givenname: Karl surname: Persson fullname: Persson, Karl organization: Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden – sequence: 5 givenname: Erik surname: Demitz-Helin fullname: Demitz-Helin, Erik organization: Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden – sequence: 6 givenname: Carles orcidid: 0000-0002-7771-7988 surname: González Peña fullname: González Peña, Carles organization: Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden – sequence: 7 givenname: Jia-Xing orcidid: 0000-0002-2122-9221 surname: Yue fullname: Yue, Jia-Xing organization: Université Côte d'Azur, CNRS, INSERM, IRCAN, Nice, France – sequence: 8 givenname: Ciaran surname: Gilchrist fullname: Gilchrist, Ciaran organization: Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden – sequence: 9 givenname: Timmy surname: Ärengård fullname: Ärengård, Timmy organization: Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden – sequence: 10 givenname: Payam surname: Ghiaci fullname: Ghiaci, Payam organization: Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden – sequence: 11 givenname: Lisa surname: Larsson-Berglund fullname: Larsson-Berglund, Lisa organization: Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden – sequence: 12 givenname: Martin surname: Zackrisson fullname: Zackrisson, Martin organization: Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden – sequence: 13 givenname: Silvana surname: Smits fullname: Smits, Silvana organization: Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden – sequence: 14 givenname: Johan surname: Hallin fullname: Hallin, Johan organization: Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden – sequence: 15 givenname: Johanna L orcidid: 0000-0003-2162-3816 surname: Höög fullname: Höög, Johanna L organization: Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden – sequence: 16 givenname: Mikael orcidid: 0000-0002-3903-8503 surname: Molin fullname: Molin, Mikael organization: Department of Biology and Biological Engineering, Chalmers University of Technology, Gothenburg, Sweden – sequence: 17 givenname: Gianni orcidid: 0000-0002-2318-0775 surname: Liti fullname: Liti, Gianni organization: Université Côte d'Azur, CNRS, INSERM, IRCAN, Nice, France – sequence: 18 givenname: Stig W orcidid: 0000-0002-8320-4337 surname: Omholt fullname: Omholt, Stig W organization: Department of Circulation and Medical Imaging, Cardiac Exercise Research Group, Norwegian University of Science and Technology, Trondheim, Norway – sequence: 19 givenname: Jonas orcidid: 0000-0001-6144-2740 surname: Warringer fullname: Warringer, Jonas organization: Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
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Keywords	genome editing genome stability cell biology genetics mitochondrial DNA mitochondrial impairment genomics oxidative stress S. cerevisiae
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SubjectTerms	Cell Biology Cellbiologi Cells DNA DNA Damage DNA, Mitochondrial - genetics DNA, Mitochondrial - metabolism Enzymes Evolutionary Biology Evolutionsbiologi Genes Genetics Genetics and Genomics Genetik genome editing genome stability Humans metabolism Mitochondria Mitochondria - metabolism Mitochondrial Mitochondrial DNA mitochondrial impairment mtDNA Oxidative Phosphorylation Oxidative Stress Oxidative Stress - genetics Reactive Oxygen Species Reactive Oxygen Species - metabolism Superoxide Superoxides Superoxides - metabolism
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Title	Genetically controlled mtDNA deletions prevent ROS damage by arresting oxidative phosphorylation
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