The 4977 bp deletion of mitochondrial DNA in human skeletal muscle, heart and different areas of the brain: A useful biomarker or more?

Experimental Gerontology

Volumn 43, Issue 7, 2008, Pages 645-652

  Meissner, Christoph ^a   Bruse, Petra ^a   Mohamed, Salaheldien Ali ^a   Schulz, Anja ^a   Warnk, Hanne ^a   Storm, Thilo ^b   Oehmichen, Manfred ^a  

^a UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

4977 bp deletion; Ageing; Human brain; Human heart; Human skeletal muscle; Mitochondrial DNA

Indexed keywords

MITOCHONDRIAL DNA;

AGE; AGING; APOPTOSIS; ARTICLE; BASAL GANGLION; BRAIN; BRAIN TISSUE; CEREBELLAR TISSUE; DNA DAMAGE; GENE DELETION; HEART; HEART LEFT VENTRICLE; HEART MUSCLE; HUMAN; HUMAN TISSUE; ILIOPSOAS MUSCLE; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; SKELETAL MUSCLE; SUBSTANTIA NIGRA;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; AGING; BRAIN CHEMISTRY; CHILD; CHILD, PRESCHOOL; DNA, MITOCHONDRIAL; GENETIC MARKERS; HUMANS; INFANT; MIDDLE AGED; MITOCHONDRIA, HEART; MITOCHONDRIA, MUSCLE; MUSCLE, SKELETAL; MYOCARDIUM; POLYMERASE CHAIN REACTION; SEQUENCE DELETION;

EID: 46749100918     PISSN: 05315565     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exger.2008.03.004     Document Type: Article

References (76)

1. Ames B.N. Endogenous oxidative DNA damage, aging, and cancer. Free Radic. Res. Commun. 7 (1989) 121-128
2. Bagenholm R., Nilsson U.A., Gotborg C.W., and Kjellmer I. Free radicals are formed in the brain of fetal sheep during reperfusion after cerebral ischema. Pediatr. Res. 43 (1998) 271-275
3. Ballard J.W., and Dean M.D. The mitochondrial genome: mutation, selection and recombination. Curr. Opin. Genet. Dev. 11 (2001) 667-672
4. Ballinger S.W., Bouder T.G., Davis G.S., Judice S.A., Nicklas J.A., and Albertini R.J. Mitochondrial genome damage associated with cigarette smoking. Cancer Res. 56 (1996) 5692-5697
5. Bank C., Soulimane T., Schröder M., Buse G., and Zassen S. Multiple deletions of mtDNA remove the light strand origin of replication. Biochem. Biophys. Res. Commun. 279 (2000) 595-601
6. Bender A., Krishnan K.J., Morris C.M., Taylor G.A., Reeve A.K., Perry R.H., Jaros E., Hersheson J.S., Betts J., Kloppstock T., Taylor R.W., and Turnbull D.M. High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease. Nat. Genet. 38 (2006) 515-517
7. Berneburg M., Grether-Beck S., Kurten V., Ruzicka T., Briviba K., Sies H., and Krutmann J. Singlet oxygen mediates the UVA-induced generation of the photoaging-associated mitochondrial common deletion. J. Biol. Chem. 274 (1999) 15345-15349
8. Berneburg M., Plettenberg H., Medve-König K., Pfahlberg A., Gers-Barlag H., Gefeller O., and Krutmann J. Induction of the photoaging-associated mitochondrial common deletion in vivo in normal human skin. J. Invest. Dermatol. 122 (2004) 1277-1283
9. Bodyak N.D., Nekhaeva E., Wei J.Y., and Khrapko K. Quantification and sequencing of somatic deleted mtDNA in single cells: evidence for partially duplicated mtDNA in aged human tissues. Hum. Mol. Genet. 10 (2001) 17-24
10. Bua E.A., Johnson J., Herbst A., Delong B., McKenzie D., Salamat S., and Aiken J.M. Mitochondrial DNA-deletion mutations accumulate intracellularly to detrimental levels in aged human skeletal muscle fibres. Am. J. Hum. Genet. 79 (2006) 469-480
11. Chabi B., de Camaret B.M., Chevrollier A., Boisgard S., and Stepien G. Random mtDNA deletions and functional consequence in aged human skeletal muscle. Biochem. Biophys. Res. Commun. 332 (2005) 542-549
12. Chan C.C., Liu V.W., Lau E.Y., Yeung W.S., Ng E.H., and Ho P.C. Mitochondrial DNA content and 4977 bp deletion in unfertilized oocytes. Mol. Hum. Reprod. 11 (2005) 843-846
13. Chen X.J., and Butow R.A. The organization and inheritance of the mitochondrial genome. Nat. Rev. Genet. 6 (2005) 815-825
14. Corral-Debrinski M., Horton T., Lott M.T., Shoffner J.M., Beals M.F., and Wallace D.C. Mitochondrial DNA deletions in human brain: regional variability and increase with advanced age. Nat. Genet. 2 (1992) 324-329
15. Corral-Debrinski M., Shoffner J.M., Lott M.T., and Wallace D.C. Association of mitochondrial DNA damage with aging and coronary atherosclerotic heart disease. Mutat. Res. 275 (1992) 169-180
16. Cortopassi G.A., Shibata D., Soong N.W., and Arnheim N. A pattern of accumulation of a somatic deletion of mitochondrial DNA in aging human tissues. Proc. Natl. Acad. Sci. USA 89 (1992) 7370-7374
17. Dai J.G., Xiao Y.B., Min J.X., Zhang G.Q., Yao K., and Zhou R.J. Mitochondrial DNA 4977 BP deletion mutations in lung carcinoma. Indian J. Cancer 43 (2006) 20-25
18. Dani M.A., Dani S.U., Lima S.P., Martinez A., Rossi B.M., Soares F., Zago M.A., and Simpson A.J. Less DeltamtDNA4977 than normal in various types of tumors suggests that cancer cells are essentially free of this mutation. Genet. Mol. Res. 3 (2004) 395-409
19. Elson J.L., Samuels D.C., Turnbull D.M., and Chinnery P.F. Random intracellular drift explains the clonal expansion of mitochondrial DNA mutations with age. Am. J. Hum. Genet. 68 (2001) 802-806
20. Eshaghian A., Vleugels R.A., Canter J.A., McDonald M.A., Stasko T., and Sligh J.E. Mitochondrial DNA deletions serve as biomarkers of aging in the skin, but are typically absent in nonmelanoma skin cancers. J. Invest. Dermatol. 126 (2006) 336-344
21. Fukushima K., and Fiocchi C. Paradoxical decrease of mitochondrial DNA deletions in epithelial cells of active ulcerative colitis patients. Am. J. Physiol. Gastrointest. Liver Physiol. 286 (2004) G804-G813
22. Gershon D. The mitochondrial theory of aging: is the culprit a faulty disposal system rather than indigenous mitochondrial alterations?. Exp. Gerontol. 34 (1999) 613-619
23. Gokey N.G., Cao Z., Pak J.W., Lee D., McKiernan S.H., McKenzie D., Weindruch R., and Aiken J.M. Molecular analyses of mtDNA deletion mutations in microdissected skeletal muscle fibers from aged rhesus monkeys. Aging Cell 3 (2004) 319-326
24. Goldstein M., and Lieberman A. The role of the regulatory enzymes of catecholamine synthesis in Parkinson's disease. Neurology 42 (1992) 8-12
25. Graeber M.B., Grasbon-Frodl E., Eitzen U.V., and Kösel S. Neurodegeneration and aging: role of the second genome. J. Neurosci. Res. 52 (1998) 1-6
26. Griffiths P.D., Dobson B.R., Jones G.R., and Clarke D.T. Iron in the basal ganglia in Parkinson's disease. Brain 122 (1999) 667-673
27. Gross N.J., Getz G.S., and Rabinowitz M. Apparent turnover of mitochondrial deoxyribonucleic acid and mitochondrial phospholipids in the tissues of the rat. J. Biol. Chem. 244 (1969) 1552-1562
28. Harman D. The aging process. Proc. Natl. Acad. Sci. USA 78 (1981) 7124-7128
29. Hayakawa M., Katsumata K., Yoneda M., Tanaka M., Sugiyama S., and Ozawa T. Age-related extensive fragmentation of mitochondrial DNA into minicircles. Biochem. Biophys. Res. Commun. 226 (1996) 369-377
30. Holt I.J., He J., Mao C.C., Boyd-Kirkup J.D., Martinsson P., Sembongi H., Reyes A., and Spelbrink J.N. Mammalian mitochondrial nucleoids: organizing an independently minded genome. Mitochondrion 7 (2007) 311-321
31. Indo H.P., Davidson M., Yen H.-C., Suenaga S., Tomita K., Nishii T., Higuchi M., Koga Y., Ozawa T., and Majima H.J. Evidence of ROS generation by mitochondria in cells with impaired electron transport chain and mitochondrial DNA damage. Mitochondrion 7 (2007) 106-118
32. Kajander O.A., Rovio A.T., Majamaa K., Poulton J., Spelbrink J.N., Holt I.J., Karhunen P.J., and Jacobs H.T. Human mtDNA sublimons resemble rearranged mitochondrial genomes found in pathological states. Hum. Mol. Genet. 9 (2000) 2821-2835
33. Kao S., Chao H.T., and Wei Y.H. Mitochondrial deoxyribonucleic acid 4977-bp deletion is associated with diminished fertility and motility of human sperm. Biol. Reprod. 52 (1995) 729-736
34. Khrapko K., Nekhaeva E., Kratysberg Y., and Kunz W. Clonal expansions of mitochondrial genomes: implications for in vivo mutational spectra. Mutat. Res. 522 (2003) 13-19
35. Koch H., Wittern K.P., and Bergemann J. In human keratinocytes the common deletion reflects donor variabilities rather than chronologic aging and can be induced by ultraviolet A irradiation. J. Invest. Dermatol. 117 (2001) 892-897
36. Kopsidas G., Zhang C., Yarovaya N., Kovalenko S., Graves S., Richardson M., and Linnane A.W. Stochastic mitochondrial DNA changes: bioenergy decline in type I skeletal muscle fibres correlates with a decline in the amount of amplifiable full-length mtDNA. Free Radic. Res. 36 (2002) 445-453
37. Korr H., Kurz C., Seidler T.O., Sommer D., and Schmitz C. Mitochondrial DNA synthesis studied autoradiographically in various cell types in vivo. Braz. J. Med. Biol. Res. 32 (1998) 289-298
38. Kovalenko S.A., Kopsidas G., Kelso J.M., and Linnane A.W. Deltoid human muscle mtDNA is extensively rearranged in old age subjects. Biochem. Biophys. Res. Commun. 232 (1997) 147-152
39. Kraytsberg Y., Kudryavtseva E., McKee A.C., Geula C., Kowall N.W., and Khrapko K. Mitochondrial DNA deletions are abundant and cause functional impairment in aged human substantia nigra neurons. Nat. Genet. 38 (2006) 518-520
40. Kujoth G.C., Bradshaw P.C., Haroon S., and Prolla T.A. The role of mitochondrial DNA mutations in mammalian aging. PLoS Genet 3 (2007) e24
41. Kujoth G.C., Hiona A., Pugh T.D., Someya S., Panzer K., Wohlgemuth S.E., Hofer T., Seo A.Y., Sullivan R., Jobling W.A., Morrow J.D., van Remmen H., Sedivy J.M., Yamasoba T., Tanokura M., Weindruch R., Leeuwenburgh C., and Prolla T.A. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 309 (2005) 481-484
42. Lezza A.M., Mecocci P., Cormio A., Beal M.F., Cherubini A., Cantatore P., Senin U., and Gadaleta M.N. Mitochondrial DNA 4977 bp deletion and OH8dG levels correlate in the brain of aged subjects but not Alzheimeŕs disease patients. FASEB J. 13 (1999) 1083-1088
43. Lee H.C., Pang C.Y., Hsu H.S., and Wei Y.H. Differential accumulations of 4977 bp deletion in mitochondrial DNA of various tissues in human ageing. Biochim. Biophys. Acta 1226 (1994) 37-43
44. Lim P.S., Cheng Y.M., and Wei Y.H. Large-scale mitochondrial DNA deletions in skeletal muscle of patients with end-stage renal disease. Free Radic. Biol. Med. 29 (2000) 454-463
45. Liu C.Y., Lee C.F., and Wei Y.H. Quantitative effect of 4977 bp deletion of mitochondrial DNA on the susceptibility of human cells to UV-induced apoptosis. Mitochondrion 7 (2007) 89-95
46. Liu V.W., Zhang C., and Nagley P. Mutations in mitochondrial DNA accumulate differentially in three different human tissues during ageing. Nucleic Acids Res. 26 (1998) 1268-1275
47. Mansouri A., Fromenty B., Berson A., Robin M.A., Grimbert S., Beaugrand M., Erlinger S., and Pessayre D. Multiple hepatic mitochondrial DNA deletions suggest premature oxidative aging in alcoholic patients. J. Hepatol. 27 (1997) 96-102
48. Meissner C. Mutations of mitochondrial DNA-cause or consequence of the ageing process?. Z. Gerontol. Geriatr. 40 (2007) 325-333
49. Meissner C., Bruse P., and Oehmichen M. Tissue-specific deletion patterns of the mitochondrial genome with advancing age. Exp. Gerontol. 41 (2006) 508-524
50. Meissner C., Mohamed S.A., Klueter H., Hamann K., von Wurmb N., and Oehmichen M. Quantification of mitochondrial DNA in human blood cells using an automated detection system. Forensic Sci. Int. 113 (2000) 109-112
51. Meissner C., Schwark T., von Wurmb N., and Oehmichen M. Cerebellar mitochondrial DNA deletion associated with survival of prolonged ischemia. In: Oehmichen M. (Ed). Brain Hypoxia and Ischemia. Research in Legal Medicine vol. 24 (2000), Schmidt-Römhild, Luebeck 179-192
52. Merril C.R., Zullo S., Ghanbari H., Herman M.M., Kleinman J.E., Bigelow L.B., Bartko J.J., and Sabourin D.J. Possible relationships between conditions associated with chronic hypoxia and brain mitochondrial DNA deletions. Arch. Biochem. Biophys. 326 (1996) 172-177
53. Miquel J., Economos A.C., Fleming J., and Johnson Jr. J.E. Mitochondrial role in cell aging. Exp. Gerontol. 15 (1980) 575-591
54. Mita S., Schmidt B., Schon E.A., DiMauro S., and Bonilla E. Detection of "deleted" mitochondrial genomes in cytochrome- c oxidase-deficient muscle fibers of a patient with Kearns-Sayre syndrome. Proc. Natl. Acad. Sci USA 86 (1989) 9509-9513
55. Mohamed S.A., Wesch D., Blumenthal A., Bruse P., Windler K., Ernst M., Kabelitz D., Oehmichen M., and Meissner C. Detection of the 4977 bp deletion of mitochondrial DNA in different human blood cells. Exp. Gerontol. 39 (2004) 181-188
56. Papiha S.S., Rathod H., Briceno I., Pooley J., and Datta H.K. Age related somatic mitochondrial DNA deletions in bone. J. Clin. Pathol. 51 (1998) 117-120
57. Peng T.I., Yu P.R., Chen J.Y., Wang H.L., Wu H.Y., Wei Y.H., and Jou M.J. Visualizing common deletion of mitochondrial DNA-augmented mitochondrial reactive oxygen species generation and apoptosis upon oxidative stress. Biochim. Biophys. Acta 1762 (2006) 241-255
58. Phadnis N., Sia R.A., and Sia E.A. Analysis of repeat-mediated deletions in the mitochondrial genome of Saccharomyces cerevisiae. Genetics 171 (2005) 1549-1559
59. Prigione A., and Cortopassi G. Mitochondrial DNA deletions and chloramphenicol treatment stimulate the autophagic transcript ATG12. Autophagy 3 (2007) 377-380
60. Prithivirajsingh S., Story M.D., Berg S.A., Geara F.B., Ang K.K., Ismail S.M., Stevens C.W., Buchholz T.A., and Brock W.A. Accumulation of the common mitochondrial DNA deletion induced by ionizing radiation. FEBS Lett. 571 (2004) 227-232
61. Rasmussen U.F., Krustrup P., Kjaer M., and Rasmussen H.N. Experimental evidence against the mitochondrial theory of aging. A study of isolated human skeletal muscle mitochondria. Exp. Gerontol. 38 (2003) 877-886
62. Ray A.J., Turner R., Nikaido O., Rees J.L., and Birch-Machin M.A. The spectrum of mitochondrial DNA deletions is a ubiquitous marker of ultraviolet radiation exposure in human skin. J. Invest. Dermatol. 115 (2000) 674-679
63. Ross O.A., Hyland P., Curran M.D., McIlhatton B.P., Wikby A., Johansson B., Tompa A., Pawelec G., Barnett C.R., Middleton D., and Barnett Y.A. Mitochondrial DNA damage in lymphocytes: a role in immunosenescence?. Exp. Gerontol. 37 (2002) 329-340
64. Schoeler S., Szibor R., Gellerich F.N., Wartmann T., Mawrin C., Dietzmann K., and Kirches E. Mitochondrial DNA deletions sensitize cells to apoptosis at low heteroplasmy levels. Biochem. Biophys. Res. Commun. 332 (2005) 43-49
65. Shoffner J.M., Lott M.T., Voljavec A.S., Soueidan S.A., Costigan D.A., and Wallace D.C. 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 (1989) 952-7956
66. Simonetti S., Chen X., DiMauro S., and Schon E.A. Accumulation of deletions in human mitochondrial DNA during normal aging: analysis by quantitative PCR. Biochim. Biophys. Acta 1180 (1992) 113-122
67. Soong N.W., Hinton D.R., Cortopassi G., and Arnheim N. Mosaicism for a specific somatic mitochondrial DNA mutation in adult human brain. Nat. Genet. 2 (1992) 318-323
68. Srivastava S., and Moraes C.T. Double-strand breaks of mouse muscle mtDNA promote large deletions similar to multiple mtDNA deletions in humans. Hum. Mol. Genet. 14 (2005) 893-902
69. Steuerwald N., Barrit J.A., Adler R., Malter H., Schimmel T., Cohen J., and Brenner C.A. Quantification of mtDNA in single oocytes, polar bodies and subcellular components by real-time rapid cycle fluorescence monitored PCR. Zygote 8 (2000) 209-215
70. Stevnsner T., Thorslund T., de Souza-Pinto N., and Bohr V.A. Mitochondrial repair of 8-oxoguanine and changes with aging. Exp. Gerontol. 37 (2002) 1189-1196
71. Storm T., Rath S., Mohamed S.A., Bruse P., Kowald A., Oehmichen M., and Meissner C. Mitotic brain cells are just as prone to mitochondrial deletions as neurons: a large-scale single-cell PCR study of the human caudate nucleus. Exp. Gerontol. 37 (2002) 1387-1398
72. St-Pierre J., Buckingham J.A., Roebuck S.J., and Brand M.D. Topology of superoxide production from different sites in the mitochondrial electron transport chain. J. Biol. Chem. 277 (2002) 44784-44790
73. Zeviani M., Spinazzola A., and Carelli V. Nuclear genes in mitochondrial disorders. Curr. Opin. Genet. Dev. 13 (2003) 262-270
74. Zhang C., Lee A., Liu V.W., Pepe S., Rosenfeldt F., and Nagley P. Mitochondrial DNA deletions in human cardiac tissue show a gross mosaic distribution. Biochem. Biophys. Res. Commun. 254 (1999) 152-157
75. Zhang C., Liu V.W., Addessi C.L., Sheffield D.A., Linnane A.W., and Nagley P. Differential occurrence of mutations in mitochondrial DNA of human skeletal muscle during aging. Hum. Mutat. 11 (1998) 360-371
76. Ye, C., Shu, X.O., Wen, W., Pierce, L., Courtney, R., Gao, Y.T., Zheng, W., Cai, Q., 2007. Quantitative analysis of mitochondrial DNA 4977-bp deletion in sporadic breast cancer and benign breast diseases. Breast Cancer Res. Treat. May 31; [Epub ahead of print].