A mitochondria-specific mutational signature of aging: increased rate of A > G substitutions on the heavy strand.


Journal

Nucleic acids research
ISSN: 1362-4962
Titre abrégé: Nucleic Acids Res
Pays: England
ID NLM: 0411011

Informations de publication

Date de publication:
14 10 2022
Historique:
accepted: 07 09 2022
revised: 02 08 2022
received: 28 04 2022
pubmed: 22 9 2022
medline: 18 10 2022
entrez: 21 9 2022
Statut: ppublish

Résumé

The mutational spectrum of the mitochondrial DNA (mtDNA) does not resemble any of the known mutational signatures of the nuclear genome and variation in mtDNA mutational spectra between different organisms is still incomprehensible. Since mitochondria are responsible for aerobic respiration, it is expected that mtDNA mutational spectrum is affected by oxidative damage. Assuming that oxidative damage increases with age, we analyse mtDNA mutagenesis of different species in regards to their generation length. Analysing, (i) dozens of thousands of somatic mtDNA mutations in samples of different ages (ii) 70053 polymorphic synonymous mtDNA substitutions reconstructed in 424 mammalian species with different generation lengths and (iii) synonymous nucleotide content of 650 complete mitochondrial genomes of mammalian species we observed that the frequency of AH > GH substitutions (H: heavy strand notation) is twice bigger in species with high versus low generation length making their mtDNA more AH poor and GH rich. Considering that AH > GH substitutions are also sensitive to the time spent single-stranded (TSSS) during asynchronous mtDNA replication we demonstrated that AH > GH substitution rate is a function of both species-specific generation length and position-specific TSSS. We propose that AH > GH is a mitochondria-specific signature of oxidative damage associated with both aging and TSSS.

Identifiants

pubmed: 36130228
pii: 6709245
doi: 10.1093/nar/gkac779
pmc: PMC9561281
doi:

Substances chimiques

DNA, Mitochondrial 0
Nucleotides 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

10264-10277

Subventions

Organisme : NICHD NIH HHS
ID : R01 HD091439
Pays : United States

Informations de copyright

© The Author(s) 2022. Published by Oxford University Press on behalf of Nucleic Acids Research.

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Auteurs

Alina G Mikhailova (AG)

Center for Mitochondrial Functional Genomics, Immanuel Kant Baltic Federal University, Kaliningrad, Russian Federation.
Vavilov Institute of General Genetics RAS, Moscow, Russia.

Alina A Mikhailova (AA)

Center for Mitochondrial Functional Genomics, Immanuel Kant Baltic Federal University, Kaliningrad, Russian Federation.

Kristina Ushakova (K)

Center for Mitochondrial Functional Genomics, Immanuel Kant Baltic Federal University, Kaliningrad, Russian Federation.

Evgeny O Tretiakov (EO)

Center for Mitochondrial Functional Genomics, Immanuel Kant Baltic Federal University, Kaliningrad, Russian Federation.
Department of Molecular Neurosciences, Center for Brain Research, Medical University of Vienna, Vienna, Austria.

Dmitrii Iliushchenko (D)

Center for Mitochondrial Functional Genomics, Immanuel Kant Baltic Federal University, Kaliningrad, Russian Federation.

Victor Shamansky (V)

Center for Mitochondrial Functional Genomics, Immanuel Kant Baltic Federal University, Kaliningrad, Russian Federation.

Valeria Lobanova (V)

Center for Mitochondrial Functional Genomics, Immanuel Kant Baltic Federal University, Kaliningrad, Russian Federation.

Ivan Kozenkov (I)

Center for Mitochondrial Functional Genomics, Immanuel Kant Baltic Federal University, Kaliningrad, Russian Federation.

Bogdan Efimenko (B)

Center for Mitochondrial Functional Genomics, Immanuel Kant Baltic Federal University, Kaliningrad, Russian Federation.

Andrey A Yurchenko (AA)

INSERM U981, Gustave Roussy Cancer Campus, Université Paris Saclay, Villejuif, France.

Elena Kozenkova (E)

Institute of Physics, Mathematics and Information Technology, Immanuel Kant Baltic Federal University, Kaliningrad, Russian Federation.

Evgeny M Zdobnov (EM)

Department of Genetic Medicine and Development, University of Geneva Medical School, Geneva, Switzerland.
Swiss Institute of Bioinformatics, Lausanne, Switzerland.

Vsevolod Makeev (V)

Vavilov Institute of General Genetics RAS, Moscow, Russia.
Moscow Institute of Physics and Technology, Moscow, Russian Federation.

Valerian Yurov (V)

Institute of Physics, Mathematics and Information Technology, Immanuel Kant Baltic Federal University, Kaliningrad, Russian Federation.

Masashi Tanaka (M)

Department of Neurology, Juntendo University Graduate School of Medicine, Tokyo, Japan.

Irina Gostimskaya (I)

Manchester Institute of Biotechnology, The University of Manchester, Manchester, United Kingdom.

Zoe Fleischmann (Z)

Department of Biology, Northeastern University, Boston, MA, USA.

Sofia Annis (S)

Department of Biology, Northeastern University, Boston, MA, USA.

Melissa Franco (M)

Department of Biology, Northeastern University, Boston, MA, USA.

Kevin Wasko (K)

Department of Biology, Northeastern University, Boston, MA, USA.

Stepan Denisov (S)

Center for Mitochondrial Functional Genomics, Immanuel Kant Baltic Federal University, Kaliningrad, Russian Federation.
School of Biological Sciences, Faculty of Biology, Medicine and Health, The University of Manchester, Manchester, United Kingdom.

Wolfram S Kunz (WS)

Department of Epileptology and Institute of Experimental Epileptology and Cognition Research, University Bonn, Bonn, Germany.

Dmitry Knorre (D)

The A.N. Belozersky Institute Of Physico-Chemical Biology, Moscow State University, Moscow, Russian Federation.

Ilya Mazunin (I)

Center for Molecular and Cellular Biology, Skolkovo Institute of Science and Technology (Skoltech), Skolkovo, Russian Federation.
Fomin Clinic, Moscow, Russian Federation.
Medical Genomics LLC, Moscow, Russian Federation.

Sergey Nikolaev (S)

INSERM U981, Gustave Roussy Cancer Campus, Université Paris Saclay, Villejuif, France.

Jacques Fellay (J)

Swiss Institute of Bioinformatics, Lausanne, Switzerland.
School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland.

Alexandre Reymond (A)

Center for Integrative Genomics, University of Lausanne, Lausanne, Switzerland.

Konstantin Khrapko (K)

Department of Biology, Northeastern University, Boston, MA, USA.

Konstantin Gunbin (K)

Center for Mitochondrial Functional Genomics, Immanuel Kant Baltic Federal University, Kaliningrad, Russian Federation.
Institute of Molecular and Cellular Biology SB RAS, Novosibirsk, Russian Federation.

Konstantin Popadin (K)

Center for Mitochondrial Functional Genomics, Immanuel Kant Baltic Federal University, Kaliningrad, Russian Federation.
Swiss Institute of Bioinformatics, Lausanne, Switzerland.
School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland.

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