Germline mitochondrial DNA mutations aggravate ageing and can impair brain development

Nature

Volumn 501, Issue 7467, 2013, Pages 412-415

  Ross, Jaime M ^a   Stewart, James B ^b   Hagström, Erik ^a   Brené, Stefan ^a   Mourier, Arnaud ^b   Coppotelli, Giuseppe ^a   Freyer, Christoph ^a,b   Lagouge, Marie ^b   Hoffer, Barry J ^c   Olson, Lars ^a   Larsson, Nils Göran ^a,b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b MAX PLANCK INSTITUTE FOR BIOLOGY OF AGEING   (Germany)

^c UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA;

ACCUMULATION; ALLELE; BRAIN; FERTILITY; GENOME; MITOCHONDRIAL DNA; MUTATION;

AGING; ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEVELOPMENT; BRAIN MALFORMATION; CELL DENSITY; CONTROLLED STUDY; FEMALE; FEMALE SUBFERTILITY; GERM LINE; MOLECULAR CLONING; MOUSE; MUTAGENESIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RESPIRATORY CHAIN; SOMATIC MUTATION; STOCHASTIC MODEL;

AGING; ALLELES; ANIMALS; BRAIN; CELL NUCLEUS; DNA, MITOCHONDRIAL; EXTRACHROMOSOMAL INHERITANCE; FEMALE; GENOME; HETEROZYGOTE; LITTER SIZE; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MUTAGENESIS; MUTATION; PHENOTYPE; REPRODUCTION; STOCHASTIC PROCESSES;

MAMMALIA; MUS;

EID: 84884416043     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12474     Document Type: Article

References (33)

1. Szilard, L. On the nature of the aging process. Proc. Natl Acad. Sci. USA 45, 30-45 (1959)
2. Kirkwood,T.B. L.Understanding theoddscience of aging.Cell120,437- 447(2005)
3. Ernster, L., Löw, H., Nordenbrand, K. & Ernster, B. A component promoting oxidative phosphorylation, released frommitochondria during aging. Exp. Cell Res. 9, 348-349 (1955)
4. Miquel, J., Economos, A. C., Fleming, J. & Johnson, J. E. Mitochondrial role in cell aging. Exp. Gerontol. 15, 575-591 (1980)
5. Pikó, L., Hougham, A. J. & Bulpitt, K. J. Studies of sequence heterogeneity of mitochondrial DNA from rat andmouse tissues: evidence for an increased frequency ofdeletions/additionswithaging.Mech.AgeingDev.43,279- 293(1988)
6. Müller-Höcker, J. Cytochrome-c-oxidase deficient cardiomyocytes in the human heart-an age-related phenomenon. Am. J. Pathol. 134, 1167-1173 (1989)
7. Cortopassi, G. A. & Arnheim, N. Detection of a specific mitochondrial DNAdeletion in tissues of older humans. Nucleic Acids Res. 18, 6927-6933 (1990)
8. Corral-Debrinski, M. et al. Mitochondrial DNA deletions in human brain: regional variability and increase with advanced age. Nature Genet. 2, 324-329 (1992)
9. Pakendorf, B.&Stoneking, M. MitochondrialDNAandhumanevolution. Annu. Rev. Genomics Hum. Genet. 6, 165-183 (2005)
10. Krakauer, D. C.&Mira, A. Mitochondria and germ-cell death. Nature 400, 125-126 (1999)
11. Stewart, J. B. et al. Strong purifying selection in transmission of mammalian mitochondrial DNA. PLoS Biol. 6, e10 (2008)
12. Fan, W. et al. A mouse model of mitochondrial disease reveals germline selection against severe mtDNA mutations. Science 319, 958-962 (2008)
13. Freyer, C. et al. Variation in germline mtDNA heteroplasmy is determined prenatally but modified during subsequent transmission. Nature Genet. 44, 1282-1285 (2012)
14. Stewart, J. B., Freyer, C., Elson, J. L. & Larsson, N.-G. Purifying selection of mtDNA and its implications for understanding evolution and mitochondrial disease. Nature Rev. Genet. 9, 657-662 (2008)
15. Li, M. et al. Detecting heteroplasmy fromhigh-throughput sequencing of complete human mitochondrial DNA genomes. Am. J. Hum. Genet. 87, 237-249 (2010)
16. Payne, B. A. I. et al. Universal heteroplasmy of human mitochondrial DNA. Hum. Mol. Genet. 22, 384-390 (2013)
17. Payne,B.A. I. et al.Mitochondrialagingisacceleratedbyanti-retroviral therapy through the clonal expansion of mtDNAmutations. Nature Genet. 43, 806-810 (2011)
18. Greaves, L. C.& Turnbull, D. M. MitochondrialDNAmutations and ageing. Biochim. Biophys. Acta 1790, 1015-1020 (2009)
19. Larsson, N. G. Somatic mitochondrial DNA mutations in mammalian aging. Annu. Rev. Biochem. 79, 683-706 (2010)
20. Ameur, A. et al. Ultra-deep sequencing of mouse mitochondrial DNA: mutational patterns and their origins. PLoS Genet. 7, e1002028 (2011)
21. Trifunovic, A. et al. Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 429, 417-423 (2004)
22. Kujoth, G. C. et al. MitochondrialDNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 309, 481-484 (2005)
23. Hance, N., Ekstrand, M. I. & Trifunovic, A. Mitochondrial DNA polymerase gamma is essential for mammalian embryogenesis. Hum. Mol. Genet. 14, 1775-1783 (2005)
24. Kraytsberg, Y. & Khrapko, K. Single-molecule PCR: an artifact-free PCR approach for the analysis of somatic mutations. Expert Rev. Mol. Diagn. 5, 809-815 (2005)
25. Greaves, L. C. et al. Quantification of mitochondrial DNA mutation load. Aging Cell 8, 566-572 (2009)
26. Greaves, L. C., Elson, J. L., Nooteboom, M. & Grady, J. P. Comparison of mitochondrialmutation spectra in ageing human colonic epitheliumand disease: absence of evidence for purifying selection in somatic mitochondrial DNA point mutations. PLoS Genet. 8, e1003082 (2012)
27. Taylor, R. W. et al. MitochondrialDNAmutations in human colonic crypt stemcells. J. Clin. Invest. 112, 1351-1360 (2003)
28. Ahlqvist, K. J. et al. Somatic progenitor cell vulnerability to mitochondrial DNA mutagenesis underlies progeroid phenotypes in Polg mutator mice. Cell Metab. 15, 100-109 (2012)
29. Norddahl, G. L. et al. Accumulating mitochondrialDNAmutations drive premature hematopoietic aging phenotypes distinct fromphysiological stemcell aging. Stem Cells 8, 499-510 (2011)
30. Chen, M. L. et al. Erythroid dysplasia, megaloblastic anemia, and impaired lymphopoiesis arising from mitochondrial dysfunction. Blood 114, 4045-4053 (2009)
31. Hancock, D. K., Tully, L. A. & Levin, B. C. A Standard Reference Material to determine the sensitivity of techniques for detecting low-frequency mutations, SNPs, and heteroplasmies in mitochondrial DNA. Genomics 86, 446-461 (2005)
32. Wanrooij, S. et al. In vivo mutagenesis reveals that OriL is essential for mitochondrial DNA replication. EMBO Rep. 13, 1130-1137 (2012)
33. Ross, J. M. et al. High brain lactate is a hallmark of aging and caused by a shift in the lactate dehydrogenase A/B ratio. Proc. Natl Acad. Sci. USA 107, 20087-20092 (2010).