Mitochondrial DNA mutations in aging

Progress in Molecular Biology and Translational Science

Volumn 127, Issue , 2014, Pages 29-62

  Khrapko, Konstantin ^a   Turnbull, Doug ^b  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Aging; Clonal expansion; Evolution of aging; Mitochondrial DNA; Mutations

Indexed keywords

MITOCHONDRIAL DNA; MUTAGENIC AGENT;

AGING; ARTICLE; CELL FUNCTION; CLONE; COLON; CYTOLOGY; EVOLUTION; FEEDBACK SYSTEM; GENE MUTATION; GENE SEQUENCE; GENETIC DRIFT; HUMAN; LIFE EXPECTANCY; LIFESPAN; LONGEVITY; MITOCHONDRIAL DNA DISORDER; MITOCHONDRIAL GENOME; MITOCHONDRION; MOLECULE; MUSCLE CELL; NERVE CELL; NONHUMAN; PHENOTYPE; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; RESPIRATORY CHAIN; RESPIRATORY FAILURE; SOMATIC MUTATION; SPECIES COMPARISON; SUBSTANTIA NIGRA; ANIMAL; ANTIBODY SPECIFICITY; GENETICS; MUTATION; SPECIES DIFFERENCE;

AGING; ANIMALS; BIOLOGICAL EVOLUTION; DNA, MITOCHONDRIAL; HUMANS; MUTATION; ORGAN SPECIFICITY; SPECIES SPECIFICITY;

EID: 84906663913     PISSN: 18771173     EISSN: 18780814     Source Type: Book Series    
DOI: 10.1016/B978-0-12-394625-6.00002-7     Document Type: Chapter

References (78)

1. D. Harman The biologic clock: the mitochondria? J Am Geriatr Soc 20 4 1972 145 147
2. A.W. Linnane, S. Marzuki, T. Ozawa, and M. Tanaka Mitochondrial DNA mutations as an important contributor to ageing and degenerative diseases Lancet 1 8639 1989 642 645 (Pubitemid 19078788)
3. A. Terman, B. Gustafsson, and U.T. Brunk Autophagy, organelles and ageing J Pathol 211 2 2007 134 143 (Pubitemid 46195512)
4. M. Vermulst, J.H. Bielas, and G.C. Kujoth et al. Mitochondrial point mutations do not limit the natural lifespan of mice Nat Genet 39 4 2007 540 543 (Pubitemid 46514771)
5. S. DiMauro, M. Hirano, and E.A. Schon Approaches to the treatment of mitochondrial diseases - invited review Muscle Nerve 34 3 2006 265 283 (Pubitemid 44300157)
6. S.L. Archer Mitochondrial dynamics - mitochondrial fission and fusion in human diseases N Engl J Med 369 23 2013 2236 2251
7. D.L. Longo, and S.L. Archer Mitochondrial dynamics - mitochondrial fission and fusion in human diseases N Engl J Med 369 23 2013 2236 2251
8. J.L. Boore Animal mitochondrial genomes Nucleic Acids Res 27 8 1999 1767 1780 (Pubitemid 29209617)
9. K.L. Adams, and J.D. Palmer Evolution of mitochondrial gene content: gene loss and transfer to the nucleus Mol Phylogenet Evol 29 3 2003 380 395 (Pubitemid 37491885)
10. C. Kukat, C.A. Wurm, H. Spåhr, M. Falkenberg, N.-G. Larsson, and S. Jakobs Super-resolution microscopy reveals that mammalian mitochondrial nucleoids have a uniform size and frequently contain a single copy of mtDNA Proc Natl Sci U S A 108 33 2011 13534 13539
11. W. Zheng, K. Khrapko, H.A. Coller, W.G. Thilly, and W.C. Copeland Origins of human mitochondrial point mutations as DNA polymerase gamma-mediated errors Mutat Res 599 1-2 2006 11 20 (Pubitemid 44043167)
12. L.A. Marcelino, P.C. Andre, K. Khrapko, H.A. Coller, J. Griffith, and W.G. Thilly Chemically induced mutations in mitochondrial DNA of human cells: mutational spectrum of N-methyl-N'-nitro-N-nitrosoguanidine Cancer Res 58 13 1998 2857 2862 (Pubitemid 28311919)
13. K.J. Krishnan, A.K. Reeve, and D.C. Samuels et al. What causes mitochondrial DNA deletions in human cells? Nat Genet 40 3 2008 275 279 (Pubitemid 351311775)
14. H. Fukui, and C.T. Moraes Mechanisms of formation and accumulation of mitochondrial DNA deletions in aging neurons Hum Mol Genet 18 6 2009 1028 1036
15. X. Guo, K. Popadin, and N. Markuzon et al. Repeats, longevity and the sources of mtDNA deletions: evidence from "deletional spectra" Trends Genet 26 8 2010 340 343
16. D.A. Kreutzer, and J.M. Essigmann Oxidized, deaminated cytosines are a source of C → T transitions in vivo Proc Natl Acad Sci U S A 95 7 1998 3578 3582 (Pubitemid 28173170)
17. Y. Kraytsberg, E. Kudryavtseva, A.C. McKee, C. Geula, N.W. Kowall, and K. Khrapko Mitochondrial DNA deletions are abundant and cause functional impairment in aged human substantia nigra neurons Nat Genet 38 5 2006 518 520
18. Y. Kraytsberg, E. Nekhaeva, N.B. Bodyak, and K. Khrapko Mutation and intracellular clonal expansion of mitochondrial genomes: two synergistic components of the aging process? Mech Ageing Dev 124 1 2003 49 53 (Pubitemid 36266683)
19. K. Nakada, K. Inoue, and T. Ono et al. Inter-mitochondrial complementation: mitochondria-specific system preventing mice from expression of disease phenotypes by mutant mtDNA Nat Med 7 8 2001 934 940 (Pubitemid 32756431)
20. C.T. Moraes, and E.A. Schon + Detection and analysis of mitochondrial DNA and RNA in muscle by in situ hybridization and single-fiber PCR "Met Enzymol" Methods Enzymol 264 1996 522 540 (Pubitemid 26089335)
21. R. Rossignol, B. Faustin, C. Rocher, M. Malgat, J.P. Mazat, and T. Letellier Mitochondrial threshold effects Biochem J 370 Pt 3 2003 751 762 (Pubitemid 36399067)
22. R.W. Gilkerson, E.A. Schon, E. Hernandez, and M.M. Davidson Mitochondrial nucleoids maintain genetic autonomy but allow for functional complementation J Cell Biol 181 7 2008 1117 1128 10.1083/jcb.200712101 (Pubitemid 351915487)
23. A. Herbst, J.W. Pak, D. McKenzie, E. Bua, M. Bassiouni, and J.M. Aiken Accumulation of mitochondrial DNA deletion mutations in aged muscle fibers: evidence for a causal role in muscle fiber loss J Gerontol A Biol Sci Med Sci 62 3 2007 235 245 (Pubitemid 47065720)
24. S. Sacconi, L. Salviati, and Y. Nishigaki et al. A functionally dominant mitochondrial DNA mutation Hum Mol Genet 17 12 2008 1814 1820 10.1093/hmg/ddn073 (Pubitemid 351791508)
25. Y. Bai, and G. Attardi The mtDNA-encoded ND6 subunit of mitochondrial NADH dehydrogenase is essential for the assembly of the membrane arm and the respiratory function of the enzyme EMBO J 17 16 1998 4848 4858 (Pubitemid 28377185)
26. W. Fan, K.G. Waymire, and N. Narula et al. A mouse model of mitochondrial disease reveals germline selection against severe mtDNA mutations Science 319 5865 2008 958 962 (Pubitemid 351263767)
27. S.J. Dubec, R. Aurora, and H.P. Zassenhaus Mitochondrial DNA mutations may contribute to aging via cell death caused by peptides that induce cytochrome c release Rejuvenation Res 11 3 2008 611 619 (Pubitemid 351931466)
28. S.R. Schwarze, C.M. Lee, S.S. Chung, E.B. Roecker, R. Weindruch, and J.M. Aiken High levels of mitochondrial DNA deletions in skeletal muscle of old rhesus monkeys Mech Ageing Dev 83 2 1995 91 101
29. W. Johnston, G. Karpati, S. Carpenter, D. Arnold, and E.A. Shoubridge Late-onset mitochondrial myopathy Ann Neurol 37 1 1995 16 23
30. K. Khrapko Two ways to make an mtDNA bottleneck Nat Genet 40 2 2008 134 135 (Pubitemid 351171411)
31. N.J. Gross, G.S. Getz, and M. Rabinowitz Apparent turnover of mitochondrial DNA and mitochondrial phospholipids in the tissues of the rat J Biol Chem 244 6 1969 1552 1562
32. Y. Michikawa, F. Mazzucchelli, N. Bresolin, G. Scarlato, and G. Attardi Aging-dependent large accumulation of point mutations in the human mtDNA control region for replication Science 286 5440 1999 774 779
33. Y. Wang, Y. Michikawa, and C. Mallidis et al. Muscle-specific mutations accumulate with aging in critical human mtDNA control sites for replication Proc Natl Acad Sci U S A 98 7 2001 4022 4027 (Pubitemid 32249891)
34. A. Kowald, M. Dawson, and T.B.L. Kirkwood Mitochondrial mutations and ageing: can mitochondrial deletion mutants accumulate via a size based replication advantage? J Theor Biol 340 2014 111 118 10.1016/j.jtbi.2013.09.009
35. A. Bender, K.J. Krishnan, and C.M. Morris et al. High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease Nat Genet 38 5 2006 515 517
36. G. Campbell, K.J. Krishnan, M. Deschauer, R.W. Taylor, and D.M. Turnbull Dissecting the mechanisms underlying the accumulation of mitochondrial DNA deletions in human skeletal muscle Hum Mol Genet 2014 10.1093/hmg/ddu176
37. A. Kowald, and T.B.L. Kirkwood Transcription could be the key to the selection advantage of mitochondrial deletion mutants in aging Proc Natl Acad Sci U S A 111 8 2014 2972 2977
38. A. Kowald, and T.B.L. Kirkwood Evolution of the mitochondrial fusion-fission cycle and its role in aging Proc Natl Acad Sci U S A 108 25 2011 10237 10242
39. J. Avise, J. Neigel, and J. Arnold Demographic influences on mitochondrial DNA lineage survivorship in animal populations J Mol Evol 20 2 1984 99 105 (Pubitemid 14058162)
40. H.A. Coller, N.D. Bodyak, and K. Khrapko Frequent intracellular clonal expansions of somatic mtDNA mutations: significance and mechanisms Ann N Y Acad Sci 959 2002 434 447 (Pubitemid 34457582)
41. H. Jacobs Dinosaurs, dementia and cancer Trends Genet 16 2000 295 (Pubitemid 30389599)
42. E. Nekhaeva, N.D. Bodyak, and Y. Kraytsberg et al. Clonally expanded mtDNA point mutations are abundant in individual cells of human tissues Proc Natl Acad Sci U S A 99 8 2002 5521 5526 (Pubitemid 34411581)
43. R.W. Taylor, M.J. Barron, and G.M. Borthwick et al. Mitochondrial DNA mutations in human colonic crypt stem cells J Clin Invest 112 9 2003 1351 1360 (Pubitemid 38057689)
44. P.F. Chinnery, and D.C. Samuels Relaxed replication of mtDNA: a model with implications for the expression of disease Am J Hum Genet 64 4 1999 1158 1165 (Pubitemid 30463047)
45. K. Inoue, K. Nakada, and A. Ogura et al. Generation of mice with mitochondrial dysfunction by introducing mouse mtDNA carrying a deletion into zygotes Nat Genet 26 2 2000 176 181
46. J. Wanagat, Z. Cao, P. Pathare, and J.M. Aiken Mitochondrial DNA deletion mutations colocalize with segmental electron transport system abnormalities, muscle fiber atrophy, fiber splitting, and oxidative damage in sarcopenia FASEB J 15 2 2001 322 332 (Pubitemid 32141424)
47. J.N. Guzman, J. Sanchez-Padilla, and D. Wokosin et al. Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1 Nature 468 7324 2010 696 700
48. P. Luoma, A. Melberg, and J.O. Rinne et al. Parkinsonism, premature menopause, and mitochondrial DNA polymerase gamma mutations: clinical and molecular genetic study Lancet 364 9437 2004 875 882 (Pubitemid 39221065)
49. D.A. Bennett, L.A. Beckett, and A.M. Murray et al. Prevalence of parkinsonian signs and associated mortality in a community population of older people N Engl J Med 334 2 1996 71 76 (Pubitemid 26017932)
50. L.C. Greaves, S.L. Preston, and P.J. Tadrous et al. Mitochondrial DNA mutations are established in human colonic stem cells, and mutated clones expand by crypt fission Proc Natl Acad Sci U S A 103 3 2006 714 719 (Pubitemid 43153091)
51. M. Rera, S. Bahadorani, and J. Cho et al. Modulation of longevity and tissue homeostasis by the Drosophila PGC-1 homolog Cell Metab 14 5 2011 623 634
52. J. Elson, D. Samuels, D. Turnbull, and P. Chinnery Random intracellular drift explains the clonal expansion of mitochondrial DNA mutations with age Am J Hum Genet 68 3 2001 802 806 (Pubitemid 32202775)
53. K. Khrapko, E. Nekhaeva, Y. Kraytsberg, and W. Kunz Clonal expansions of mitochondrial genomes: implications for in vivo mutational spectra Mutat Res 522 1-2 2003 13 19 (Pubitemid 36216297)
54. S.D. Taylor, N.G. Ericson, and J.N. Burton et al. Targeted enrichment and high-resolution digital profiling of mitochondrial DNA deletions in human brain Aging Cell 13 1 2014 29 38
55. K. Popadin, A. Safdar, Y. Kraytsberg, and K. Khrapko When man got his mtDNA deletions? Aging Cell 2014 10.1111/acel.12231
56. K. Khrapko The timing of mitochondrial DNA mutations in aging Nat Genet 43 8 2011 726 727
57. B. Bandy, and A.J. Davison Mitochondrial mutations may increase oxidative stress: implications for carcinogenesis and aging? Free Radic Biol Med 8 6 1990 523 539 (Pubitemid 20204417)
58. A. Nicholas, Y. Kraytsberg, X. Guo, and K. Khrapko On the timing and the extent of clonal expansion of mtDNA deletions: evidence from single-molecule PCR Exp Neurol 218 2 2009 316 319
59. G.C. Kujoth, A. Hiona, and T.D. Pugh et al. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging Science 309 5733 2005 481 484 (Pubitemid 40994689)
60. A. Hiona, and C. Leeuwenburgh The role of mitochondrial DNA mutations in aging and sarcopenia: implications for the mitochondrial vicious cycle theory of aging Exp Gerontol 43 1 2008 24 33 (Pubitemid 350245432)
61. L. Weissman, N.C. de Souza-Pinto, T. Stevnsner, and V.A. Bohr DNA repair, mitochondria, and neurodegeneration Neuroscience 145 4 2007 1318 1329 (Pubitemid 46602727)
62. E.S. Lander, and H. Lodish Mitochondrial diseases: gene mapping and gene therapy Cell 61 6 1990 925 926
63. K.L. Adams, D.O. Daley, Y.L. Qiu, J. Whelan, and J.D. Palmer Repeated, recent and diverse transfers of a mitochondrial gene to the nucleus in flowering plants Nature 408 6810 2000 354 357
64. D. Zhang, J.L. Mott, S.W. Chang, G. Denniger, Z. Feng, and H.P. Zassenhaus Construction of transgenic mice with tissue-specific acceleration of mitochondrial DNA mutagenesis Genomics 69 2 2000 151 161
65. A. Trifunovic, A. Wredenberg, and M. Falkenberg et al. Premature ageing in mice expressing defective mitochondrial DNA polymerase Nature 429 6990 2004 417 423 (Pubitemid 38715133)
66. K. Khrapko, Y. Kraytsberg, A.D.N.J. de Grey, J. Vijg, and E.A. Schon Does premature aging of the mtDNA mutator mouse prove that mtDNA mutations are involved in natural aging? Aging Cell 5 3 2006 279 282 (Pubitemid 43805618)
67. M. Vermulst, J. Wanagat, and G.C. Kujoth et al. DNA deletions and clonal mutations drive premature aging in mitochondrial mutator mice Nat Genet 40 4 2008 392 394 (Pubitemid 351450885)
68. L.C. Greaves, M.J. Barron, G. Campbell-Shiel, T.B. Kirkwood, and D.M. Turnbull Differences in the accumulation of mitochondrial defects with age in mice and humans Mech Ageing Dev 132 11-12 2011 588 591
69. X. Guo, E. Kudryavtseva, and N. Bodyak et al. Mitochondrial DNA deletions in mice in men: substantia nigra is much less affected in the mouse Biochim Biophys Acta 1797 6-7 2010 1159 1162
70. K. Khrapko, and J. Vijg Mitochondrial DNA mutations and aging: a case closed? Nat Genet 39 4 2007 445 446 (Pubitemid 46514762)
71. Y. Kraytsberg, D.K. Simon, D.M. Turnbull, and K. Khrapko Do mtDNA deletions drive premature aging in mtDNA mutator mice? Aging Cell 8 4 2009 502 506
72. D.C. Samuels Mitochondrial DNA, repeats constrain the life span of mammals Trends Genet 20 5 2004 226 229 (Pubitemid 38510433)
73. M. Khaidakov, E.R. Siegel, and R.J. Shmookler Reis Direct repeats in mitochondrial DNA and mammalian lifespan Mech Ageing Dev 127 10 2006 808 812 (Pubitemid 44374666)
74. J.-N. Yang, A. Seluanov, and V. Gorbunova Mitochondrial inverted repeats strongly correlate with lifespan: mtDNA inversions and aging PLoS One 8 9 2013 e73318
75. D.C. Samuels Life span is related to the free energy of mitochondrial DNA Mech Ageing Dev 126 10 2005 1123 1129 (Pubitemid 41253864)
76. G. Lehmann, E. Segal, K.K. Muradian, and V.E. Fraifeld Do mitochondrial DNA and metabolic rate complement each other in determination of the mammalian maximum longevity? Rejuvenation Res 11 2 2008 409 417 (Pubitemid 351601182)
77. Laura C Greaves, Marco Nooteboom, Joanna L Elson, Helen AL Tuppen, Geoffrey A Taylor, Daniel M Commane, Ramesh P Arasaradnam, Konstantin Khrapko, Robert W Taylor, Thomas BL Kirkwood, John C Mathers, Douglass M Turnbull. Clonal expansion of early to mid-life mitochondrial DNA point mutations drives mitochondrial dysfunction during human ageing. Under review in Plos Genetics.
78. K. Khrapko, and J. Vijg Mitochondrial DNA mutations in Aging: devils in the details Trends in Genet 25 2009 91 98