What causes mitochondrial DNA deletions in human cells?

Nature Genetics

Volumn 40, Issue 3, 2008, Pages 275-279

  Krishnan, Kim J ^a,b   Reeve, Amy K ^a   Samuels, David C ^c   Chinnery, Patrick F ^a   Blackwood, John K ^a   Taylor, Robert W ^a   Wanrooij, Sjoerd ^d,e   Spelbrink, Johannes N ^d   Lightowlers, Robert N ^a   Turnbull, Doug M ^a,b  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c VIRGINIA BIOINFORMATICS INSTITUTE   (United States)

^d TAMPERE UNIVERSITY HOSPITAL   (Finland)

^e KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA;

AGING; CLONE; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; GENE DELETION; HUMAN; HUMAN CELL; MITOSIS; PRIORITY JOURNAL; REVIEW;

DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA, MITOCHONDRIAL; GENE DELETION; HUMANS; MITOCHONDRIAL DISEASES; MODELS, BIOLOGICAL; SUBSTANTIA NIGRA;

EID: 39749124232     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.f.94     Document Type: Review

References (48)

1. Holt, I.J., Harding, A.E. & Morgan-Hughes, J.A. Deletions of muscle mitochondrial DNA in patients with mitochondrial myopathies. Nature 331, 717-719 (1988).
2. Shoffner, J.M. et al. Spontaneous Kearns-Sayre/chronic external ophthalmoplegia plus syndrome associated with a mitochondrial DNA deletion: a slip-replication model and metabolic therapy. Proc. Natl. Acad. Sci. USA 86, 7952-7956 (1989).
3. Goto, Y., Nonaka, I. & Horai, S. A mutation in the tRNA(Leu)(UUR) gene associated with the MELAS subgroup of mitochondrial encephalomyopathies. Nature 348, 651-653 (1990).
4. Wallace, D.C. et al. Familial mitochondrial encephalomyopathy (MERRF): genetic, pathophysiological, and biochemical characterization of a mitochondrial DNA disease. Cell 55, 601-610 (1988).
5. Schaefer, A.M. et al. The prevalence of mitochondrial DNA disease in adults. Ann. Neurol. 63, 35-39 (2008).
6. Taylor, R.W. & Turnbull, D.M. Mitochondrial DNA mutations in human disease. Nat. Rev. Genet. 6, 389-402 (2005).
7. Hudson, G. & Chinnery, P.F. Mitochondrial DNA polymerase-gamma and human disease. Human Molecular Genetics 15 (Spec. No. 2), R244-252 (2006).
8. Bender, A. et al. High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease. Nat. Genet. 38, 515-517 (2006).
9. Kraytsberg, Y. et al. Mitochondrial DNA deletions are abundant and cause functional impairment in aged human substantia nigra neurons. Nat. Genet. 38, 518-520 (2006).
10. Sciacco, M., Bonilla, E., Schon, E.A., DiMauro, S. & Moraes, C.T. Distribution of wild-type and common deletion forms of mtDNA in normal and respiration-deficient muscle fibers from patients with mitochondrial myopathy. Hum. Mol. Genet. 3, 13-19 (1994).
11. Bua, E. et al. Mitochondrial DNA-deletion mutations accumulate intracellularly to detrimental levels in aged human skeletal muscle fibers. Am. J. Hum. Genet. 79, 469-480 (2006).
12. Samuels, D.C., Schon, E.A. & Chinnery, P.F. Two direct repeats cause most human mtDNA deletions. Trends Genet. 20, 393-398 (2004).
13. Reeve, A.K., Krishnan, K.J., Elson. J.L., Morris. C.M., Bender. A., Lightowlers. R.N. & Turnbull. D.M. Nature of mitochondrial DNA deletions in substantia nigra neurons. Am. J. Hum. Genet. 82, 228-235 (2008).
14. Robberson, D.L. & Clayton, D.A. Replication of mitochondrial DNA in mouse L cells and their thymidine kinase - derivatives: displacement replication on a covalently-closed circular template. Proc. Natl. Acad. Sci. USA 69, 3810-3814 (1972).
15. Yasukawa, T. et al. Replication of vertebrate mitochondrial DNA entails transient ribonucleotide incorporation throughout the lagging strand. EMBO J. 25, 5358-5371 (2006).
16. Holt, I.J., Lorimer, H.E. & Jacobs, H.T. Coupled leading- and lagging-strand synthesis of mammalian mitochondrial DNA. Cell 100, 515-524 (2000).
17. Yang, M.Y. et al. Biased incorporation of ribonucleotides on the mitochondrial L-strand accounts for apparent strand-asymmetric DNA replication. Cell 111, 495-505 (2002).
18. Wang, G.J., Nutter, L.M. & Thayer, S.A. Insensitivity of cultured rat cortical neurons to mitochondrial DNA synthesis inhibitors: evidence for a slow turnover of mitochondrial DNA. Biochem. Pharmacol. 54, 181-187 (1997).
19. Taylor, R.W. et al. Mitochondrial DNA mutations in human colonic crypt stem cells. J. Clin. Invest. 112, 1351-1360 (2003).
20. Haber, J.E. Partners and pathways repairing a double-strand break. Trends Genet. 16, 259-264 (2000).
21. Bowmaker, M. et al. Mammalian mitochondrial DNA replicates bidirectionally from an initiation zone. J. Biol. Chem. 278, 50961-50969 (2003). .
22. Wanrooij, S. et al. Twinkle and POLG defects enhance age-dependent accumulation of mutations in the control region of mtDNA. Nucleic Acids Res. 32, 3053-3064 (2004).
23. Nguyen, L.H., Erzberger, J.P., Root, J. & Wilson, D.M., III. The human homolog of Escherichia coli Orn degrades small single-stranded RNA and DNA oligomers. J. Biol. Chem. 275, 25900-25906 (2000).
24. Hanekamp, T. & Thorsness, P.E. YNT20, a bypass suppressor of yme1 yme2, encodes a putative 3′-5′ exonuclease localized in mitochondria of Saccharomyces cerevisiae. Curr. Genet. 34, 438-448 (1999).
25. Barnerias, C. et al. Respiratory chain deficiency in a female with Aicardi-Goutieres syndrome. Dev. Med. Child Neurol. 48, 227-230 (2006).
26. Crow, Y.J. et al. Mutations in the gene encoding the 3′-5′ DNA exonuclease TREX1 cause Aicardi-Goutieres syndrome at the AGS1 locus. Nat. Genet. 38, 917-920 (2006).
27. Horiguchi, M. et al. Molecular nature of ultraviolet B light-induced deletions in the murine epidermis. Cancer Res. 61, 3913-3918 (2001).
28. Sargentini, N.J. & Smith, K.C. Involvement of RecB-mediated (but not RecF-mediated) repair of DNA double-strand breaks in the gamma-radiation production of long deletions in Escherichia coli. Mutat. Res. 265, 83-101 (1992).
29. Thacker, J., Chalk, J., Ganesh, A. & North, P. A mechanism for deletion formation in DNA by human cell extracts: the involvement of short sequence repeats. Nucleic Acids Res. 20, 6183-6188 (1992).
30. Srivastava, S. & Moraes, C.T. Double-strand breaks of mouse muscle mtDNA promote large deletions similar to multiple mtDNA deletions in humans. Hum. Mol. Genet. 14, 893-902 (2005).
31. Wanrooij, S., Goffart, S., Pohjoismaki, J.L., Yasukawa, T. & Spelbrink, J.N. Expression of catalytic mutants of the mtDNA helicase Twinkle and polymerase POLG causes distinct replication stalling phenotypes. Nucleic Acids Res. 35, 3238-3251 (2007).
32. Van Goethem, G. et al. Unusual presentation and clinical variability in Belgian pedigrees with progressive external ophthalmoplegia and multiple deletions of mitochondrial DNA. Eur. J. Neurol. 4, 476-484 (1997).
33. Esposito, L.A., Melov, S., Panov, A., Cottrell, B.A. & Wallace, D.C. Mitochondrial disease in mouse results in increased oxidative stress. Proc. Natl. Acad. Sci. USA 96, 4820-4825 (1999).
34. Berneburg, M. et al. Singlet oxygen mediates the UVA-induced generation of the photoaging-associated mitochondrial common deletion. J. Biol. Chem. 274, 15345-15349 (1999).
35. Krishnan, K.J., Harbottle, A. & Birch-Machin, M.A. The use of a 3895 bp mitochondrial DNA deletion as a marker for sunlight exposure in human skin. J. Invest. Dermatol. 123, 1020-1024 (2004).
36. Murphy, J.E., Nugent, S., Seymour, C. & Mothersill, C. Mitochondrial DNA point mutations and a novel deletion induced by direct low-LET radiation and by medium from irradiated cells. Mutat. Res. 585, 127-136 (2005).
37. Prithivirajsingh, S. et al. Accumulation of the common mitochondrial DNA deletion induced by ionizing radiation. FEBS Lett. 571, 227-232 (2004).
38. Halliwell, B. Reactive oxygen species and the central nervous system. J. Neurochem. 59, 1609-1623 (1992).
39. Arai, T. et al. Up-regulation of hMUTYH, a DNA repair enzyme, in the mitochondria of substantia nigra in Parkinson's disease. Acta Neuropathol. (Berl.) 112, 139-145 (2006).
40. DeGrey, A.D. A proposed refinement of the mitochondrial free radical theory of aging. Bioessays 19, 161-166 (1997).
41. Elson, J.L., Samuels, D.C., Turnbull, D.M. & Chinnery, P.F. Random intracellular drift explains the clonal expansion of mitochondrial DNA mutations with age. Am. J. Hum. Genet. 68, 802-806 (2001).
42. Wallace, D.C. Mitochondrial genetics: a paradigm for aging and degenerative diseases? Science 256, 628-632 (1992).
43. Yoneda, M., Chomyn, A., Martinuzzi, A., Hurko, O. & Attardi, G. Marked replicative advantage of human mtDNA carrying a point mutation that causes the MELAS encephalomyopathy. Proc. Natl. Acad. Sci. USA 89, 11164-11168 (1992).
44. . Chinnery, P.F. et al. Risk of developing a mitochondrial DNA deletion disorder. Lancet 364, 592-596 (2004).
45. Blakely, E.L. et al. Mitochondrial DNA deletion in "identical" twin brothers. J. Med. Genet. 41, e19 (2004).
46. Barritt, J.A., Brenner, C.A., Cohen, J. & Matt, D.W. Mitochondrial DNA rearrangements in human oocytes and embryos. Mol. Hum. Reprod. 5, 927-933 (1999).
47. Chan, C.C. et al. Mitochondrial DNA content and 4977 bp deletion in unfertilized oocytes. Mol. Hum. Reprod. 11, 843-846 (2005).
48. Chen, X. et al. Rearranged mitochondrial genomes are present in human oocytes. Am. J. Hum. Genet. 57, 239-247 (1995).