Ultra-deep sequencing of mouse mitochondrial DNA: Mutational patterns and their origins

PLoS Genetics

Volumn 7, Issue 3, 2011, Pages

  Ameur, Adam ^a   Stewart, James B ^b   Freyer, Christoph ^b   Hagström, Erik ^c   Ingman, Max ^a   Larsson, Nils Göran ^b,c   Gyllensten, Ulf ^a  

^a UPPSALA UNIVERSITY   (Sweden)

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

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; MITOCHONDRIAL DNA;

AGING; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION ORIGIN; DNA SEQUENCE; GENE DELETION; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENE INSERTION; GENE LOCATION; GENETIC ASSOCIATION; GENETIC VARIABILITY; GERM LINE; HETEROZYGOSITY; LIVER PARENCHYMA; MALE; MITOCHONDRIAL DNA REPLICATION; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PHENOTYPIC VARIATION; POINT MUTATION; PROMOTER REGION; WILD TYPE; ANIMAL; C57BL MOUSE; ELECTRON TRANSPORT; GENETICS; HIGH THROUGHPUT SEQUENCING; METABOLISM; MUTATION;

MUS;

ANIMALS; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MALE; MICE; MICE, INBRED C57BL; MUTATION;

EID: 79953735503     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002028     Document Type: Article

References (39)

1. Harman D, (1972) The biologic clock: the mitochondria? J Am Geriatr Soc 20: 145-147.
2. Miquel J, Economos AC, Fleming J, Johnson JE Jr, (1980) Mitochondrial role in cell aging. Exp Gerontol 15: 575-591.
3. Krishnan KJ, Greaves LC, Reeve AK, Turnbull D, (2007) The ageing mitochondrial genome. Nucleic Acids Res 35: 7399-7405.
4. Larsson NG, (2010) Somatic mitochondrial DNA mutations in mammalian aging. Annu Rev Biochem 79: 683-706.
5. Cortopassi GA, Arnheim N, (1990) Detection of a specific mitochondrial DNA deletion in tissues of older humans. Nucleic Acids Res 18: 6927-6933.
6. Ikebe S, Tanaka M, Ohno K, Sato W, Hattori K, et al. (1990) Increase of deleted mitochondrial DNA in the striatum in Parkinson's disease and senescence. Biochem Biophys Res Commun 170: 1044-1048.
7. Katayama M, Tanaka M, Yamamoto H, Ohbayashi T, Nimura Y, et al. (1991) Deleted mitochondrial DNA in the skeletal muscle of aged individuals. Biochem Int 25: 47-56.
8. Yen TC, Su JH, King KL, Wei YH, (1991) Ageing-associated 5 kb deletion in human liver mitochondrial DNA. Biochem Biophys Res Commun 178: 124-131.
9. Hattori K, Tanaka M, Sugiyama S, Obayashi T, Ito T, et al. (1991) Age-dependent increase in deleted mitochondrial DNA in the human heart: possible contributory factor to presbycardia. Am Heart J 121: 1735-1742.
10. Schwarze SR, Lee CM, Chung SS, Roecker EB, Weindruch R, et al. (1995) High levels of mitochondrial DNA deletions in skeletal muscle of old rhesus monkeys. Mech Ageing Dev 83: 91-101.
11. Piko L, (1992) Accumulation of mtDNA defects and changes in mtDNA content in mouse and rat tissues with aging. Ann N Y Acad Sci 663: 450-452.
12. Trifunovic A, Hansson A, Wredenberg A, Rovio AT, Dufour E, et al. (2005) Somatic mtDNA mutations cause aging phenotypes without affecting reactive oxygen species production. Proc Natl Acad Sci U S A 102: 17993-17998.
13. Trifunovic A, Wredenberg A, Falkenberg M, Spelbrink JN, Rovio AT, et al. (2004) Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 429: 417-423.
14. Kujoth GC, Hiona A, Pugh TD, Someya S, Panzer K, et al. (2005) Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 309: 481-484.
15. Edgar D, Shabalina I, Camara Y, Wredenberg A, Calvaruso MA, et al. (2009) Random point mutations with major effects on protein-coding genes are the driving force behind premature aging in mtDNA mutator mice. Cell Metab 10: 131-138.
16. Vermulst M, Wanagat J, Kujoth GC, Bielas JH, Rabinovitch PS, et al. (2008) DNA deletions and clonal mutations drive premature aging in mitochondrial mutator mice. Nat Genet 40: 392-394.
17. Vermulst M, Wanagat J, Loeb LA, (2009) On mitochondria, mutations, and methodology. Cell Metab 10: 437.
18. Edgar D, Larsson NG, Trifunovic A, (2010) Response: Point Mutations Are Causing Progeroid Phenotypes in the mtDNA Mutator Mouse. Cell Metab 11: 93.
19. Bailey LJ, Cluett TJ, Reyes A, Prolla TA, Poulton J, et al. (2009) Mice expressing an error-prone DNA polymerase in mitochondria display elevated replication pausing and chromosomal breakage at fragile sites of mitochondrial DNA. Nucleic Acids Res 37: 2327-2335.
20. Kraytsberg Y, Simon DK, Turnbull DM, Khrapko K, (2009) Do mtDNA deletions drive premature aging in mtDNA mutator mice? Aging Cell 8: 502-506.
21. Williams SL, Huang J, Edwards YJ, Ulloa RH, Dillon LM, et al. (2010) The mtDNA mutation spectrum of the progeroid Polg mutator mouse includes abundant control region multimers. Cell Metab 12: 675-682.
22. He Y, Wu J, Dressman DC, Iacobuzio-Donahue C, Markowitz SD, et al. (2010) Heteroplasmic mitochondrial DNA mutations in normal and tumour cells. Nature 464: 610-614.
23. Li M, Schonberg A, Schaefer M, Schroeder R, Nasidze I, et al. (2010) Detecting heteroplasmy from high-throughput sequencing of complete human mitochondrial DNA genomes. Am J Hum Genet 87: 237-249.
24. Stewart JB, Freyer C, Elson JL, Wredenberg A, Cansu Z, et al. (2008) Strong Purifying Selection in Transmission of Mammalian Mitochondrial DNA. PLoS Biol 6: e10 doi:10.1371/journal.pbio.0060010.
25. Khrapko K, Coller HA, Andre PC, Li XC, Hanekamp JS, et al. (1997) Mitochondrial mutational spectra in human cells and tissues. Proc Natl Acad Sci U S A 94: 13798-13803.
26. Zheng W, Khrapko K, Coller HA, Thilly WG, Copeland WC, (2006) Origins of human mitochondrial point mutations as DNA polymerase gamma-mediated errors. Mutat Res 599: 11-20.
27. Elliott HR, Samuels DC, Eden JA, Relton CL, Chinnery PF, (2008) Pathogenic mitochondrial DNA mutations are common in the general population. Am J Hum Genet 83: 254-260.
28. Ameur A, Wetterbom A, Feuk L, Gyllensten U, (2010) Global and unbiased detection of splice junctions from RNA-seq data. Genome Biol 11: R34.
29. Rovio AT, (2006) DNA Polymerase Gamma Mutaions in Male Infertility and Ageing. Tampere University of Tampere.
30. Vermulst M, Bielas JH, Kujoth GC, Ladiges WC, Rabinovitch PS, et al. (2007) Mitochondrial point mutations do not limit the natural lifespan of mice. Nat Genet 39: 540-543.
31. Falkenberg M, Larsson NG, Gustafsson CM, (2007) DNA replication and transcription in mammalian mitochondria. Annu Rev Biochem 76: 679-699.
32. Holt IJ, Harding AE, Morgan-Hughes JA, (1988) Deletions of muscle mitochondrial DNA in patients with mitochondrial myopathies. Nature 331: 717-719.
33. Inoue K, Nakada K, Ogura A, Isobe K, Goto Y, et al. (2000) Generation of mice with mitochondrial dysfunction by introducing mouse mtDNA carrying a deletion into zygotes. Nat Genet 26: 176-181.
34. Tyynismaa H, Mjosund KP, Wanrooij S, Lappalainen I, Ylikallio E, et al. (2005) Mutant mitochondrial helicase Twinkle causes multiple mtDNA deletions and a late-onset mitochondrial disease in mice. Proc Natl Acad Sci U S A 102: 17687-17692.
35. Nakase H, Moraes CT, Rizzuto R, Lombes A, DiMauro S, et al. (1990) Transcription and translation of deleted mitochondrial genomes in Kearns-Sayre syndrome: implications for pathogenesis. Am J Hum Genet 46: 418-427.
36. Chen H, Vermulst M, Wang YE, Chomyn A, Prolla TA, et al. (2010) Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 141: 280-289.
37. Kukat A, Trifunovic A, (2009) Somatic mtDNA mutations and aging-facts and fancies. Exp Gerontol 44: 101-105.
38. Jensen-Seaman MI, Wildschutte JH, Soto-Calderon ID, Anthony NM, (2009) A comparative approach shows differences in patterns of numt insertion during hominoid evolution. J Mol Evol 68: 688-699.
39. Bayona-Bafaluy MP, Acin-Perez R, Mullikin JC, Park JS, Moreno-Loshuertos R, et al. (2003) Revisiting the mouse mitochondrial DNA sequence. Nucleic Acids Res 31: 5349-5355.