The road to rack and ruin: Selecting deleterious mitochondrial DNA variants

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1646, 2014, Pages

  Holt, Ian J ^a   Speijer, Dave ^b   Kirkwood, Thomas B L ^c  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

DNA; Mitochondria; Mutation

Indexed keywords

DISEASE; EUKARYOTE; MITOCHONDRIAL DNA; MITOCHONDRION; MUTATION; SELECTION;

MITOCHONDRIAL DNA;

AGING; DNA REPLICATION; GENETIC SELECTION; GENETIC VARIATION; GENETICS; HUMAN; MITOCHONDRION; MUTATION;

AGING; DNA REPLICATION; DNA, MITOCHONDRIAL; GENETIC VARIATION; HUMANS; MITOCHONDRIA; MUTATION; SELECTION, GENETIC;

EID: 84988799879     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2013.0451     Document Type: Article

References (67)

1. Holt IJ, Harding AE, Morgan-Hughes JA. 1988 Deletions of muscle mitochondrial DNA in patients with mitochondrial myopathies. Nature 331, 717-719. (doi:10.1038/331717a0)
2. Herbst A, Pak JW, McKenzie D, Bua E, Bassiouni M, Aiken JM. 2007 Accumulation of mitochondrial DNA deletion mutations in aged muscle fibers: evidence for a causal role in muscle fiber loss. J. Gerontol. A 62, 235-245. (doi:10.1093/gerona/62.3.235)
3. Moraes CT, Schon EA, DiMauro S, Miranda AF. 1989 Heteroplasmy of mitochondrial genomes in clonal cultures from patients with Kearns-Sayre syndrome. Biochem. Biophys. Res. Commun. 160, 765-771. (doi:10.1016/0006-291X(89)92499-6)
4. Taylor RW et al. 2003 Mitochondrial DNA mutations in human colonic crypt stem cells. J. Clin. Invest. 112, 1351-1360. (doi:10.1172/JCI19435)
5. Nooteboom M, Johnson R, Taylor RW, Wright NA, Lightowlers RN, Kirkwood TB, Mathers JC, Turnbull DM, Greaves LC. 2010 Age-associated mitochondrial DNA mutations lead to small but significant changes in cell proliferation and apoptosis in human colonic crypts. Aging Cell 9, 96-99. (doi:10. 1111/j.1474-9726.2009.00531.x)
6. Larsson NG, Wang J, Wilhelmsson H, Oldfors A, Rustin P, Lewandoski M, Barsh GS, Clayton DA. 1998 Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat. Genet. 18, 231-236. (doi:10.1038/ng0398-231)
7. King MP, Attardi G. 1989 Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science 246, 500-503. (doi:10.1126/science.2814477)
8. Kowald A, Dawson M, Kirkwood TB. 2014 Mitochondrial mutations and ageing: can mitochondrial deletion mutants accumulate via a size based replication advantage? J. Theor. Biol. 340, 111-118. (doi:10.1016/j.jtbi.2013.09.009)
9. Kowald A, Kirkwood TB. 2013 Mitochondrial mutations and aging: random drift is insufficient to explain the accumulation of mitochondrial deletion mutants in short-lived animals. Aging Cell 12, 728-731. (doi:10.1111/acel.12098)
10. Poulton J, Deadman ME, Gardiner RM. 1989 Duplications of mitochondrial DNA in mitochondrial myopathy. Lancet 1, 236-240. (doi:10.1016/S0140-6736(89)91256-7)
11. Poulton J, Holt IJ. 1994 Mitochondrial DNA: does more lead to less? Nat. Genet. 8, 313-315. (doi:10. 1038/ng1294-313)
12. Bender A et al. 2006 High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease. Nat. Genet. 38, 515-517. (doi:10.1038/ng1769)
13. Kraytsberg Y, Kudryavtseva E, McKee AC, Geula C, Kowall NW, Khrapko K. 2006 Mitochondrial DNA deletions are abundant and cause functional impairment in aged human substantia nigra neurons. Nat. Genet. 38, 518-520. (doi:10.1038/ng1778)
14. Trifunovic A et al. 2005 Somatic mtDNA mutations cause aging phenotypes without affecting reactive oxygen species production. Proc. Natl Acad. Sci. USA 102, 17 993-17 998. (doi:10.1073/pnas. 0508886102)
15. Zweifel SG, Fangman WL. 1991 A nuclear mutation reversing a biased transmission of yeast mitochondrial DNA. Genetics 128, 241-249.
16. Holt IJ, Dunbar DR, Jacobs HT. 1997 Behaviour of a population of partially duplicated mitochondrial DNA molecules in cell culture: segregation, maintenance and recombination dependent upon nuclear background. Hum. Mol. Genet. 6, 1251-1260. (doi:10.1093/hmg/6.8.1251)
17. Samuels DC et al. 2013 Recurrent tissue-specific mtDNA mutations are common in humans. PLoS Genet. 9, e1003929. (doi:10.1371/journal.pgen. 1003929)
18. Bowmaker M, Yang MY, Yasukawa T, Reyes A, Jacobs HT, Huberman JA, Holt IJ. 2003 Mammalian mitochondrial DNA replicates bidirectionally from an initiation zone. J. Biol. Chem. 278, 50 961-50 969. (doi:10.1074/jbc.M308028200)
19. Reyes A, Yang MY, Bowmaker M, Holt IJ. 2005 Bidirectional replication initiates at sites throughout the mitochondrial genome of birds. J. Biol. Chem. 280, 3242-3250. (doi:10.1074/jbc.M411916200)
20. Yasukawa T, Yang MY, Jacobs HT, Holt IJ. 2005 A bidirectional origin of replication maps to the major noncoding region of human mitochondrial DNA. Mol. Cell 18, 651-662. (doi:10.1016/j.molcel.2005. 05.002)
21. Diaz F, Bayona-Bafaluy MP, Rana M, Mora M, Hao H, Moraes CT. 2002 Human mitochondrial DNA with large deletions repopulates organelles faster than full-length genomes under relaxed copy number control. Nucleic Acids Res. 30, 4626-4633. (doi:10.1093/nar/gkf602)
22. He J et al. 2007 The AAA+ protein ATAD3 has displacement loop binding properties and is involved in mitochondrial nucleoid organization. J. Cell Biol. 176, 141-146. (doi:10.1083/jcb. 200609158)
23. Rajala N, Gerhold JM, Martinsson P, Klymov A, Spelbrink JN. 2013 Replication factors transiently associate with mtDNA at the mitochondrial inner membrane to facilitate replication. Nucleic Acids Res. 42, 952-967. (doi:10.1093/nar/gkt988)
24. Holt IJ. 2009 Mitochondrial DNA replication and repair: all a flap. Trends Biochem. Sci. 34, 358-365. (doi:10.1016/j.tibs.2009.03.007)
25. Kowald A, Kirkwood TB. 2014 Transcription could be the key to the selection advantage of mitochondrial deletion mutants in aging. Proc. Natl Acad. Sci. USA 111, 2972-2977. (doi:10.1073/pnas.1314970111)
26. Twig G et al. 2008 Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 27, 433-446. (doi:10.1038/ sj.emboj.7601963)
27. Kowald A, Kirkwood TB. 2011 The evolution and role of mitochondrial fusion and fission in aging and disease. Commun. Integr. Biol. 4, 627-629.
28. Kim TY et al. 2012 Metabolic labeling reveals proteome dynamics of mouse mitochondria. Mol. Cell Proteomics 11, 1586-1594. (doi:10.1074/mcp. M112.021162)
29. Hamalainen RH, Manninen T, Koivumaki H, Kislin M, Otonkoski T, Suomalainen A. 2013 Tissue-and celltype-specific manifestations of heteroplasmic mtDNA 3243A. G mutation in human induced pluripotent stem cell-derived disease model. Proc. Natl Acad. Sci. USA 110, E3622-E3630. (doi:10. 1073/pnas.1311660110)
30. Malena A, Loro E, Di Re M, Holt IJ, Vergani L. 2009 Inhibition of mitochondrial fission favours mutant over wild-type mitochondrial DNA. Hum. Mol. Genet. 18, 3407-3416. (doi:10.1093/hmg/ddp281)
31. Dai Y, Zheng K, Clark J, Swerdlow RH, Pulst SM, Sutton JP, Shinobu LA, Simon DK. 2013 Rapamycin drives selection against a pathogenic heteroplasmic mitochondrial DNA mutation. Hum. Mol. Genet. 23, 637-647. (doi:10.1093/hmg/ddt450)
32. Suen DF, Narendra DP, Tanaka A, Manfredi G, Youle RJ. 2010 Parkin overexpression selects against a deleterious mtDNA mutation in heteroplasmic cybrid cells. Proc. Natl Acad. Sci. USA 107, 11 835-11 840. (doi:10.1073/pnas.0914569107)
33. Stewart JB, Freyer C, Elson JL, Wredenberg A, Cansu Z, Trifunovic A, Larsson NG. 2008 Strong purifying selection in transmission of mammalian mitochondrial DNA. PLoS Biol. 6, e10. (doi:10.1371/ journal.pbio.0060010)
34. Lehtinen SK, Hance N, El Meziane A, Juhola MK, Juhola KM, Karhu R, Spelbrink JN, Holt IJ, Jacobs HT. 2000 Genotypic stability, segregation and selection in heteroplasmic human cell lines containing np 3243 mutant mtDNA. Genetics 154, 363-380.
35. Yoneda M, Chomyn A, Martinuzzi A, Hurko O, Attardi G. 1992 Marked replicative advantage of human mtDNA carrying a point mutation that causes the MELAS encephalomyopathy. Proc. Natl Acad. Sci. USA 89, 11 164-11 168. (doi:10.1073/ pnas.89.23.11164)
36. He J et al. 2012 Mitochondrial nucleoid interacting proteins support mitochondrial protein synthesis. Nucleic Acids Res. 40, 6109-6121. (doi:10.1093/ nar/gks266)
37. Gilkerson RW, Schon EA, Hernandez E, Davidson MM. 2008 Mitochondrial nucleoids maintain genetic autonomy but allow for functional complementation. J. Cell Biol. 181, 1117-1128. (doi:10.1083/jcb. 200712101)
38. Raap AK et al. 2012 Non-random mtDNA segregation patterns indicate a metastable heteroplasmic segregation unit in m.3243A. G cybrid cells. PLoS ONE 7, e52080. (doi:10.1371/ journal.pone.0052080)
39. Kleff S, Kemper B, Sternglanz R. 1992 Identification and characterization of yeast mutants and the gene for a cruciform cutting endonuclease. EMBO J. 11, 699-704.
40. Lockshon D, Zweifel SG, Freeman-Cook LL, Lorimer HE, Brewer BJ, Fangman WL. 1995 A role for recombination junctions in the segregation of mitochondrial DNA in yeast. Cell 81, 947-955. (doi:10.1016/0092-8674(95)90014-4)
41. Minczuk M, He J, Duch AM, Ettema TJ, Chlebowski A, Dzionek K, Nijtmans LG, Huynen MA, Holt IJ. 2011 TEFM (c17orf42) is necessary for transcription of human mtDNA. Nucleic Acids Res. 39, 4284-4299. (doi:10.1093/nar/gkq1224)
42. Hagstrom E, Freyer C, Battersby BJ, Stewart JB, Larsson NG. 2013 No recombination of mtDNA after heteroplasmy for 50 generations in the mouse maternal germline. Nucleic Acids Res. 42, 1111-1116. (doi:10.1093/nar/gkt969)
43. Reyes-Lamothe R, Nicolas E, Sherratt DJ. 2012 Chromosome replication and segregation in bacteria. Annu. Rev. Genet. 46, 121-143. (doi:10.1146/ annurev-genet-110711-155421)
44. Pohjoismaki JL et al. 2009 Human heart mitochondrial DNA is organized in complex catenated networks containing abundant four-way junctions and replication forks. J. Biol. Chem. 284, 21 446-21 457. (doi:10.1074/jbc.M109.016600)
45. D'Aurelio M, Gajewski CD, Lin MT, Mauck WM, Shao LZ, Lenaz G, Moraes CT, Manfredi G. 2004 Heterologous mitochondrial DNA recombination in human cells. Hum. Mol. Genet. 13, 3171-3179. (doi:10.1093/hmg/ddh326)
46. Poulton J, Deadman ME, Bindoff L, Morten K, Land J, Brown G. 1993 Families of mtDNA rearrangements can be detected in patients with mtDNA deletions: duplications may be a transient intermediate form. Hum. Mol. Genet. 2, 23-30. (doi:10.1093/hmg/2.1.23)
47. Sembongi H, Di Re M, Bokori-Brown M, Holt IJ. 2007 The yeast Holliday junction resolvase, CCE1, can restore wild-type mitochondrial DNA to human cells carrying rearranged mitochondrial DNA. Hum. Mol. Genet. 16, 2306-2314. (doi:10.1093/hmg/ ddm182)
48. Holzmann J, Frank P, Loffler E, Bennett KL, Gerner C, Rossmanith W. 2008 RNase P without RNA: identification and functional reconstitution of the human mitochondrial tRNA processing enzyme. Cell 135, 462-474. (doi:10.1016/j.cell.2008.09.013)
49. Hyvarinen AK, Pohjoismaki JL, Holt IJ, Jacobs HT. 2011 Overexpression of MTERFD1 or MTERFD3 impairs the completion of mitochondrial DNA replication. Mol. Biol. Rep. 38, 1321-1328. (doi:10. 1007/s11033-010-0233-9)
50. Hess JF, Parisi MA, Bennett JL, Clayton DA. 1991 Impairment of mitochondrial transcription termination by a point mutation associated with the MELAS subgroup of mitochondrial encephalomyopathies. Nature 351, 236-239. (doi:10.1038/351236a0)
51. Hyvarinen AK, Pohjoismaki JL, Reyes A, Wanrooij S, Yasukawa T, Karhunen PJ, Spelbrink JN, Holt IJ, Jacobs HT. 2007 The mitochondrial transcription termination factor mTERF modulates replication pausing in human mitochondrial DNA. Nucleic Acids Res. 35, 6458-6474. (doi:10.1093/nar/gkm676)
52. Holt IJ, He J, Mao CC, Boyd-Kirkup JD, Martinsson P, Sembongi H, Reyes A, Spelbrink JN. 2007 Mammalian mitochondrial nucleoids: organizing an independently minded genome. Mitochondrion 7, 311-321. (doi:10.1016/j.mito.2007.06.004)
53. Busch KB, Kowald A, Spelbrink JN. 2014 Quality matters: how does mitochondrial network dynamics and quality control impact on mtDNA integrity? Phil. Trans. R. Soc. B 369, 20130442. (doi:10.1098/ rstb.2013.0442)
54. Lim SE, Longley MJ, Copeland WC. 1999 The mitochondrial p55 accessory subunit of human DNA polymerase gamma enhances DNA binding, promotes processive DNA synthesis, and confers N-ethylmaleimide resistance. J. Biol. Chem. 274, 38 197-38 203. (doi:10.1074/jbc.274.53.38197)
55. Di Re M et al. 2009 The accessory subunit of mitochondrial DNA polymerase gamma determines the DNA content of mitochondrial nucleoids in human cultured cells. Nucleic Acids Res. 37, 5701-5713. (doi:10.1093/nar/gkp614)
56. Durham SE, Samuels DC, Chinnery PF. 2006 Is selection required for the accumulation of somatic mitochondrial DNA mutations in post-mitotic cells? Neuromuscul. Disord. 16, 381-386. (doi:10.1016/j. nmd.2006.03.012)
57. Goto Y, Nonaka I, Horai S. 1990 A mutation in the tRNA(Leu)(UUR) gene associated with the MELAS subgroup of mitochondrial encephalomyopathies. Nature 348, 651-653. (doi:10.1038/348651a0)
58. van den Ouweland JM, Lemkes HH, Ruitenbeek W, Sandkuijl LA, de Vijlder MF, Struyvenberg PA, van de Kamp JJ, Maassen JA. 1992 Mutation in mitochondrial tRNA(Leu)(UUR) gene in a large pedigree with maternally transmitted type II diabetes mellitus and deafness. Nat. Genet. 1, 368-371. (doi:10.1038/ng0892-368)
59. Jenuth JP, Peterson AC, Shoubridge EA. 1997 Tissuespecific selection for different mtDNA genotypes in heteroplasmic mice. Nat. Genet. 16, 93-95. (doi:10.1038/ng0597-93)
60. Li Y et al. 1995 Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat. Genet. 11, 376-381. (doi:10.1038/ng1295-376)
61. McFadden SL, Ding D, Burkard RF, Jiang H, Reaume AG, Flood DG, Salvi RJ. 1999 Cu/Zn SOD deficiency potentiates hearing loss and cochlear pathology in aged 129, CD-1 mice. J. Comp. Neurol. 413, 101-112. (doi:10.1002/(SICI)1096-9861(19991011) 413:1,101::AID-CNE7.3.0.CO;2-L)
62. de Vries RL, Gilkerson RW, Przedborski S, Schon EA. 2012 Mitophagy in cells with mtDNA mutations: being sick is not enough. Autophagy 8, 699-700. (doi:10.4161/auto.19470)
63. Fukui H, Moraes CT. 2008 The mitochondrial impairment, oxidative stress and neurodegeneration connection: reality or just an attractive hypothesis? Trends Neurosci. 31, 251-256. (doi:10.1016/j.tins. 2008.02.008)
64. Moreno-Loshuertos R, Acin-Perez R, Fernandez-Silva P, Movilla N, Perez-Martos A, Rodriguez de Cordoba S, Gallardo ME, Enriquez JA. 2006 Differences in reactive oxygen species production explain the phenotypes associated with common mouse mitochondrial DNA variants. Nat. Genet. 38, 1261-1268. (doi:10.1038/ng1897)
65. Hori A, Yoshida M, Shibata T, Ling F. 2009 Reactive oxygen species regulate DNA copy number in isolated yeast mitochondria by triggering recombination-mediated replication. Nucleic Acids Res. 37, 749-761. (doi:10.1093/ nar/gkn993)
66. de Grey AD. 1997 A proposed refinement of the mitochondrial free radical theory of aging. Bioessays 19, 161-166. (doi:10.1002/bies. 950190211)
67. Kim I, Lemasters JJ. 2011 Mitophagy selectively degrades individual damaged mitochondria after photoirradiation. Antioxidants Redox Signal. 14, 1919-1928. (doi:10.1089/ars.2010.3768)