Mitochondrial abnormalities in muscle and other aging cells: Classification, causes, and effects

Muscle and Nerve

Volumn 26, Issue 5, 2002, Pages 597-607

  DiMauro, Salvatore ^a   Tanji, Kurenai ^a   Bonilla, Eduardo ^a   Pallotti, Francesco ^a   Schon, Eric A ^a  

^a Department of Neurology and the Taub Institute for Research on Alzheimer's Disease and the Aging Brain   (United States)

Author keywords

Aging; Amyotrophic lateral sclerosis; Brain; Mitochondrial DNA (mtDNA); mtDNA deletions; Muscle; Oxidative damage; Reactive oxygen species (ROS)

Indexed keywords

MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE;

AGING; BASAL GANGLION; DEGENERATIVE DISEASE; DISEASE CLASSIFICATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GENE MUTATION; MITOCHONDRION; MUSCLE DISEASE; PRIORITY JOURNAL; RESPIRATORY CHAIN; REVIEW;

ANIMALS; CELL AGING; DNA, MITOCHONDRIAL; HUMANS; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL DISEASES; MUSCULAR DISEASES; MUTATION; NEURODEGENERATIVE DISEASES; OXIDATIVE STRESS;

EID: 0036843935     PISSN: 0148639X     EISSN: None     Source Type: Journal    
DOI: 10.1002/mus.10194     Document Type: Review

References (100)

1. Andreu AL, Arbos MA, Perez-Martos A, Lopez-Perez MJ, Asin J, Lopez N, Montoya J, Schwartz S. Reduced mitochondrial DNA transcription in senescent rat heart. Biochem Biophys Res Commun 1998;252:577-581.
2. Askanas V, McFerrin J, Baque S, Alvarez RB, Sarkozi E, Engel WK. Transfer of β-amyloid precursor protein gene using adenovirus vector causes mitochondrial abnormalities in cultured normal human muscle. Proc Natl Acad Sci USA 1996; 93:1314-1319.
3. Barrientos A, CasademontJ, Cardellach F, Ardite E, Estivill X, Urbano-Marquez A, Fernandez-Checa JC, Nunes V. Qualitative and quantitative changes in skeletal muscle mtDNA and expression of mitochondrial-encoded genes in the human aging process. Biochem Mol Med 1997;62:165-171.
4. Beal F. Aging, energy, and oxidative stress in neurodegenerative diseases. Ann Neurol 1995;38:357-366.
5. Boffoli D, Scacco SC, Vergari R, Solarino G, Santacroce G, Papa S. Decline with age of the respiratory chain activity in human skeletal muscle. Biochim Biophys Acta 1994;1236: 73-82.
6. Bonilla E, Tanji K, Hirano M, Vu TH, DiMauro S, Schon EA. Mitochondrial involvement in Alzheimer's disease. Biochim Biophys Acta 1999;1410:171-182.
7. Borthwick GM, Johnson MA, Ince PG, Shaw PJ, Turnbull DM. Mitochondrial enzyme activity in amyotrophic lateral sclerosis: Implications for the role of mitochondria in neuronal cell death. Ann Neurol 1999;46:787-790.
8. Bowling AC, Mutisya EM, Walker LC, Price DL, Cork LC, Beal MF. Age-dependent impairment of mitochondrial function in primate brain. J Neurochem 1993;60:1964-1967.
9. Brierley EJ, Johnson MA, Bowman A, Ford GA, Sbhan F, Reed JW, Turnbull DM. Mitochondrial function in muscle of elderly athletes. Ann Neurol 1997;41:114-116.
10. Brierly EJ,Johnson MA, Lightowlers RN, James OF, Turnbull DM. Role of mitochondrial DNA mutations in human aging: Implications for the central nervous system and muscle. Ann Neurol 1998;43:217-223.
11. Byrne E, Dennett X, Trounce I. Oxidative energy failure in post-mitotic cells: A major factor in senescence. Rev Neurol 1991;147:532-535.
12. Cardellach F, Galofre J, Cusso R. Decline in skeletal muscle mitochondrial respiratory chain function with ageing. Lancet 1989;2:637-639.
13. Castelluccio C, Baracca A, Fato R, Pallotti F, Maranesi M, Barzanti V, Gorini A, Villa RF, Parenti-Castelli G, Marchetti M. Mitochondrial activities of rat heart during aging. Mech Aging Devel 1995;84:139-150.
14. Chen X, Prosser R, Simonetti S, Sadlock J, Jagiello G, Schon EA. Rearranged mitochondrial genomes are present in human oocytes. Am J Hum Genet 1995;57:239-247.
15. Chen X, Simonetti S, DiMauro S, Schon EA. Accumulations of mitochondrial DNA deletions in organisms with various lifespans. Bull Mol Biol Med 1993;18:57-66.
16. Chinnery PF, Taylor DJ, Brown DT, Manners D, Styles P, Lodi R. Very low levels of the mtDNA A3243G mutation associated with mitochondrial dysfunction in vivo. Ann Neurol 2000;47:381-384.
17. Chomyn A, Martinuzzi A, Yoneda M, Daga A, Hurko O, Johns D, Lai ST, Nonaka I, Angelini C, Attardi G. MELAS mutation in mtDNA binding site for transcription termination factor causes defects in protein synthesis and in respiration but no change in levels of upstream and downstream mature transcripts. Proc Natl Acad Sci USA 1992;89: 4221-4225.
18. Chretien D, Gallego J, Barrientos A, Casademont J, Cardellach F, Munnich A, Rotig A, Rustin P. Biochemical parameters for the diagnosis of mitochondrial respiratory chain deficiency in humans and their lack of age-related changes. Biochem J 1998;329:249-254.
19. Clayton DA, Doda JN, Friedberg EC. The absence of a pyrimidine dimer repair mechanism in mammalian mitochondria. Proc Natl Acad Sci USA 1974;71:2777-2781.
20. Comi GP, Bordoni A, Salani S, Franceschina L, Sciacco M, Prelle A, Fortunato F, Zeviani M, Napoli L, Bresolin N, Moggio M, Ausenda CD, Taanman J-W, Scarlato G. Cytochrome c oxidase subunit I microdeletion in a patient with motor neuron disease. Ann Neurol 1998;43:110-116.
21. Cooper JM, Mann VM, Schapira AH. Analysis of mitochondrial respiratory chain function and mitochondrial DNA deletion in human skeletal muscle: Effect of ageing. J Neurol Sci 1992;113:91-98.
22. Corral Debrinski M, Stepien G, Shoffner JM, Lott MT, Kanter K, Wallace DC. Hypoxemia is associated with mitochondrial DNA damage and gene induction. Implications for cardiac disease. JAMA 1991;266:1812-1816.
23. Corral-Debrinski M, Horton T, Lott MT, Shoffner JM, Flint Beal M, Wallace DC. Mitochondrial DNA deletions in human brain: Regional variability and increase with advanced age. Nat Genet 1992;2:324-329.
24. Cortopassi GA, Arnheim N. Detection of a specific mitochondrial DNA deletion in tissues of older humans. Nucleic Acids Res 1990;18:6927-6933.
25. Cortopassi GA, Shibata D, Soong NW, Arnheim N. A pattern of accumulation of a somatic deletion of mitochondrial DNA in aging human tissues. Proc Natl Acad Sci USA 1992;89: 7370-7374.
26. Davis RE, Miller S, Herrnstadt C, Ghosh SS, Fahy E, Shinobu LA, Galasko D, Thal LJ, Beal MF, Howell N, Parker WD. Mutations in mitochondrial cytochrome c oxidase genes segregate with late-onset Alzheimer disease. Proc Natl Acad Sci USA 1997;94:4526-4531.
27. DiMauro S. Mitochondrial involvement in Parkinson's disease: The controversy continues. Neurology 1993;43: 2170-2172.
28. DiMauro S, Kulikova R, Tanji K, Bonilla E, Hirano M. Mitochondrial genes for generalized epilepsies. In: Delgado-Escueta AV, Wilson WA, Olsen RW, Porter RJ. Mitochondrial Genes for Generalized Epilepsies. Philadelphia: Lippincott Williams & Wilkins; 1999. p 411-419.
29. Dubeau F, De Stefano N, Zifkin BG, Arnold DL, Shoubridge EA. Oxidative phosphorylation defect in the brains of carriers of the tRNAleu (UUR) A3243G mutation in a MELAS pedigree. Ann Neurol 2000;47:179-185.
30. Fayet G, Jansson M, Sternberg D, Lombes A, Moslemi A-R, Fardeau M, Oldfors A. Mitochondrial DNA mutations in cytochrome c oxidase deficient muscle fibers associated with aging. Neuromuscul Disord 2000;10:346.
31. Gu M, Cooper JM, Schapira AHV. Mitochondrial DNA transmission of the mitochondrial defect in Parkinson's disease. Ann Neurol 1998;44:177-186.
32. Hand CK, Rouleau GA. Familial amyotrophic lateral sclerosis. Muscle Nerve 2002;24:135-159.
33. Harding AE. Growing old: The most common mitochondrial disease of all? Nat Genet 1992;2:251-252.
34. Harman D. The aging process. Proc Natl Acad Sci USA 1981; 78:7124-7128.
35. Harman D. Free radical theory of aging: Consequences of mitochondrial aging. Age 1983;6:86-94.
36. Hattori K, Tanaka M, Sugiyama S, Obayashi T, Ito T, Satake T, Hanaki Y, Asai J, Nagano M, Ozawa T. Age-dependent increase in deleted mitochondrial DNA in the human heart: Possible contributory factor to presbycardia. Am Heart J 1991;121:1735-1742.
37. Hayakawa M, Torii K, Sugiyama S, Tanaka M, Ozawa T. Age-associated accumulation of 8-hydroxy-2-deoxyguanosine in mitochondrial DNA of human diaphragm. Biochem Biophys Res Commun 1991;179:1023-1029.
38. Hayashi J, Ohta S, Kagawa Y, Kondo H, Kaneda H, Yonekawa H, Takai D, Miyabayashi S. Nuclear but not mitochondrial genome involvement in human age-related mitochondrial dysfunction. Functional integrity of mitochondrial DNA from aged subjects. J Biol Chem 1994;269:6878-6883.
39. Hirano M, Shtilbans A, Mayeux R, Davidson MM, DiMauro S, Knowles JA, Schon EA. Apparent mtDNA heteroplasmy in Alzheimer's disease patients and in normals due to PCR amplification of nucleus-embedded mtDNA pseudogenes. Proc Natl Acad Sci USA 1997;94:14894-14899.
40. Holt IJ, Dunbar DR, Jacobs HT. Behavior of a population of partially duplicated mitochondrial DNA molecules in cell culture: Segregation, maintenance and recombination dependent upon nuclear background. Hum Mol Genet 1997; 6:1251-1260.
41. Holt IJ, Harding AE, Morgan Hughes JA. Deletions of muscle mitochondrial DNA in patients with mitochondrial myopathies. Nature 1988;331:717-719.
42. Hseih RH, HouJH, Hsu HS, Wei YH. Age-dependent respiratory function decline and DNA deletions in human muscle mitochondria. Biochem Mol Biol Intern 1994;32:1009-1022.
43. Johnston W, Karpati G, Carpenter S, Arnold D, Shoubridge EA. Late-onset mitochondrial myopathy. Ann Neurol 1995; 37:16-23.
44. King MP, Attardi G. Human cells lacking mtDNA: Repopulation with exogenous mitochondria by complementation. Science 1989;246:500-503.
45. LeDoux SP, Wilson GL, Beecham EJ, Stevnsner T, Wassermann K, Bohr VA. Repair of mitochondrial DNA after various types of DNA damage in Chinese hamster ovary cells. Carcinogenesis 1992;13:1967-1973.
46. Lin FH, Lin R, Wisniewski HM, Hwang YW, Grundke-Iqbal I, Healy-Louie G, Iqbal K. Detection of point mutations in codon 331 of mitochondrial NADH dehydrogenase subunit 2 in Alzheimer's brains. Biochem Biophys Res Commun 1992;182:238-246.
47. Linnane AW, Marzuki S, Ozawa T, Tanaka M. Mitochondrial DNA mutations as an important contributor to ageing and degenerative diseases. Lancet 1989;1:642-645.
48. Mecocci P, MacGarvey U, Beal MF. Oxidative damage to mitochondrial DNA is increased in Alzheimer's disease. Ann Neurol 1994;36:747-751.
49. Mecocci P, MacGarvey U, Kaufman AE, Koontz D, Shoffner JM, Wallace DC, Beal MF. Oxidative damage to mitochondrial DNA shows marked age-dependent increases in human brain. Ann Neurol 1993;34:609-616.
50. Melov S, Hinerfeld D, Esposito L, Wallace DC. Multi-organ characterization of mitochondrial genomic rearrangements in ad libitum and caloric restricted mice show striking somatic mitochondrial DNA rearrangements with age. Nucleic Acid Res 1997;25:974-982.
51. Melov S, RavenscroftJ, Malik S, Gill MS, Walker DW, Clayton PE, Wallace DC, Malfroy B, Doctrow SR, Lithgow GJ. Extension of life-span with superoxide dismutase/catalase mimetics. Science 2000;289:1567-1569.
52. Melov S, Shoffner JM, Kaufman A, Wallace DC. Marked increase in the number and variety of mitochondrial DNA rearrangements in aging human skeletal muscle. Nucleic Acid Res 1995;23:4122-4126.
53. Mendell JR. Mitochondrial myopathy in the elderly: Exaggerated aging in the pathogenesis of disease. Ann Neurol 1995;37:3-4.
54. Michikawa Y, Mazzucchelli F, Bresolin N, Scarlato G, Attardi G. Aging-dependent large accumulation of point mutations in the human mtDNA control region for replication. Science 1999;286:774-779.
55. Miquel J. An integrated theory of aging as the result of mitochondrial-DNA mutation in different cells. Arch Gerontol Geriatr 1991;12:99-117.
56. Miquel J, Fleming J. Theoretical and experimental support for an "oxygen radical-mitochondrial injury" hypothesis of cell aging. In: Johnson JE, Walford R, Harmon D, Miquel J, editors. Free Radicals, Aging, and Degenerative Diseases. New York: AR Liss; 1986. p 51-84.
57. Mita S, Schmidt B, Schon EA, DiMauro S, Bonilla E. Detection of "deleted" mitochondrial genomes in cytochrome-coxidase-deficient muscle fibers of a patient with Kearns-Sayre syndrome. Proc Natl Acad Sci USA 1989;86: 9509-9513.
58. Moraes CT, DiMauro S, Zeviani M, Lombes A, Shanske S, Miranda AF, Nakase H, Bonilla E, Werneck LC, Servidei S, Nonaka I, Koga Y, Spiro AJ, Brownnel A, Schmidt B, Schotland DL, Zupanc M, DeVivo DC, Schon EA, Rowland LP. Mitochondrial DNA deletions in progressive external ophthalmoplegia and Kearns-Sayre syndrome. N Engl J Med 1989;320:1293-1299.
59. Muller-Hocker J. Mitochondria and ageing. Brain Pathol 1992;2:149-158.
60. Munscher C, Muller-Hocker J, Kadenbach B. Human aging is associated with various point mutations in tRNA genes of mitochondrial DNA. Biol Chem 1993;374:1099-1104.
61. Munscher C, Rieger T, Muller-Hocker J, Kadenbach B. The point mutation of mitochondrial DNA characteristic for MERRF disease is found also in healthy people of different ages. FEBS Lett 1993;317:27-30.
62. Mutisya EM, Bowling AC, Beal MF. Cortical cytochrome oxidase activity is reduced in Alzheimer's disease. J Neurochem 1994;63:2179-2184.
63. Ojaimi J, Masters CL, McLean C, Opeskin K, McKelvie P, Byrne E. Irregular distribution of cytochrome c oxidase protein subunits in aging and Alzheimer's disease. Ann Neurol 1999;46:656-660.
64. Ojaimi J, Masters CL, Opeskin K, McKelvie P, Byrne E. Mitochondrial respiratory chain activity in the human brain as a function of age. Mech Aging Devel 1999;111:39-47.
65. Orr WC, Sohal RS. Extension of life-span by overexpression of superoxide dismutase and catalase in Drosophila melanogaster. Science 1994;263:1128-1130.
66. Ozawa T, Tanaka M, Ikebe S, Ohno K, Kondo T, Mizuno Y. Quantitative determination of deleted mitochondrial DNA relative to normal DNA in parkinsonian striatum by a kinetic PCR analysis. Biochem Biophys Res Comm 1990;172: 483-489.
67. Ozawa T, Tanaka M, Sugiyama S, Hattori K, Ito T, Ohno K, Takahashi A, Sato W, Takada G, Mayumi B, Yamamoto K, Adachi K, Koga Y, Toshima H. Multiple mitochondrial DNA deletions exist in cardiomyocytes of patients with hypertrophic or dilated cardiomyopathy. Biochem Biophys Res Commun 1990;170:830-836.
68. Pallotti F, Chen X, Bonilla E, Schon EA. Evidence that specific mtDNA point mutations may not accumulate in skeletal muscle during normal human aging. Am J Hum Genet 1996; 59:591-602.
69. Papa S. Mitochondrial oxidative phosphorylation changes in the life span. Molecular aspects and physiopathological implications. Biochem Biophys Acta 1996;1276:87-105.
70. Parker WD, Filley CM, Parks JK. Cytochrome oxidase deficiency in Alzheimer's disease. Neurology 1990;40: 1302-1303.
71. Parker WD, Parks JK. Cytochrome c oxidase in Alzheimer's disease brain: Purification and characterization. Neurology 1995;45:482-486.
72. Pedersen WA, Fu W, Keller JN, Markesbery WR, Appel S, Smith RG, Kasarskis E, Mattson MP. Protein modification by the lipid peroxidation product 4-hydroxynonenal in the spinal cords of amyotrophic lateral sclerosis patients. Ann Neurol 1998;44:819-824.
73. Pennisi E. Do mitochondrial mutations dim the fire of life? Science 1999;286:664.
74. Petruzzella V, Chen X, Schon EA. Is a point mutation in the mitochondrial ND2 gene associated with Alzheimer's disease? Biochem Biophys Res Commun 1992;186:491-497.
75. Richter C, Park J-W, Ames BN. Normal oxidative damage to mitochondrial and nuclear DNA is extensive. Proc Natl Acad Sci USA 1988;85:6465-6467.
76. Schlame M, Rua D, Greenberg ML. The biosynthesis and functional role of cardiolipin. Prog Lipid Res 2000;39: 257-288.
77. Schon EA, Rizzuto R, Moraes CT, Nakase H, Zeviani M, DiMauro S. A direct repeat is a hotspot for large-scale deletions of human mitochondrial DNA. Science 1989;244: 346-349.
78. Servidei S. Mitochondrial encephalomyopathies: Gene mutation. Neuromuscul Disord 2002;12:101-110.
79. Shaw PJ, Ince PG, Falkous G, Mantle D. Oxidative damage to protein in sporadic motor neuron disease spinal cord. Ann Neurol 1995;38:691-695.
80. Shigenaga MK, Hagen TM, Ames BN. Oxidative damage and mitochondrial decay in aging. Proc Natl Acad Sci USA 1994; 91:10771-10778.
81. Shungu DC, Sano M, Millar WS, Polanco Y, Kaufmann P, DeLaPaz RL, DiMauro S, De Vivo DC. Metabolic, structural and neuropsychological deficits in mitochondrial encephalomyopathies assessed by 1H MRSI, MRI and neuropsychological testing. Proc Int Soc Magn Reson Med 1999;7:49.
82. Simonetti S, Chen X, DiMauro S, Schon EA. Accumulation of deletions in human mitochondrial DNA during normal aging: Analysis by quantitative PCR. Biochim Biophys Acta 1992;1180:113-122.
83. Soong NW, Hinton DR, Cortopassi G, Arnheim N. Mosaicism for a specific mitochondrial DNA mutation in adult human brain. Nat Genet 1992;2:318-323.
84. Sue CM, Schon EA. Mitochondrial respiratory chain diseases and mutations in nuclear DNA: A promising start? Brain Pathol 2000;10:442-450.
85. Sugiyama S, Hattori K, Ozawa T. Quantitative analysis of age-associated accumulation of mitochondrial with deletions in human hearts. Biochem Biophys Res Commun 1991;180: 894-899.
86. Suomalainen A, Kaukonen J. Diseases caused by nuclear genes affecting mtDNA stability. Am J Med Genet 2001;106: 53-61.
87. Swerdlow RH, Parks JK, Cassarino DS, Trimmer PA, Miller SW, Maguire DJ, Dheehan JP, Maguire RS, Pattee G, Juel VC, Phillips LH, Tuttle JB, Bennett JP, Davis RE, Parker WD. Mitochondria in sporadic amyotrophic lateral sclerosis. Exp Neurol 1998;153:135-142.
88. Tabrizi SJ, Schapira AHV. Mitochondrial abnormalities in neurodegenerative disorders. In: Schapira AHV, DiMauro S, editors. Mitochondrial Abnormalities in Neurodegenerative Disorders. Boston: Butterworth-Heinemann; 2002. p 143-174.
89. Tang Y, Manfredi G, Hirano M, Schon EA. Maintenance of human rearranged mitochondrial DNAs in long-term cultured transmitochondrial cell lines. Mol Biol Cell 2000;11: 2349-2358.
90. Tanji K, Vu TH, Schon EA, DiMauro S, Bonilla E. Kearns-Sayre syndrome: Unusual pattern of expression of subunits of the respiratory chain in the cerebellar system. Ann Neurol 1999;45:377-383.
91. Torii K, Sugiyama S, Tanaka M, Takagi K, Hanaki Y, Iida KI, Matsuyama M, Hirabayashi N, Uno Y, Ozawa T. Agingassociated deletions of human diaphragmatic mitochondrial DNA. Am J Respir Cell Mol Biol 1992;6:543-549.
92. Trounce I, Byrne E, Marzuki S. Decline in skeletal muscle mitochondrial respiratory chain function: Possible factor in ageing. Lancet 1989;1:637-639.
93. Vielhaber S, Winkler K, Kirches E, Kunz D, Buchner M, Feistner H, Elger CE, Ludolph AC, Riepe MW, Kunz WS. Visualization of defective mitochondrial function in skeletal muscle fibers of patients with sporadic amyotrophic lateral sclerosis. J Neurol Sci 1999;169:133-139.
94. Wallace DC, Singh G, Lott MT, Hodge JA, Schurr TG, Lezza A, Elsas LJ, Nikoskelainen EK. Mitochondrial DNA mutation associated with Leber's hereditary optic neuropathy. Science 1988;242:1427-1430.
95. Wallace DC, Stugard C, Murdock D, Schurr T, Brown MD. Ancient mtDNA sequences in the human nuclear genome: a potential source of errors in identifying pathogenic mutations. Proc Natl Acad Sci USA 1997;94:14900-14905.
96. Weindruch R, Sohal RS. Caloric intake and aging. N Engl J Med 1997;337:986-994.
97. Wiedemann FR, Winkler K, Kuznetsov AV, Bartels C, Vielhaber S, Feistner H, Kunz WS. Impairment of mitochondrial function in skeletal muscle of patients with amyotrophic lateral sclerosis. J Neurol Sci 1998;156:65-72.
98. Yen TC, Su JH, King KL, Wei YH. Ageing-associated 5 kb deletion in human liver mitochondrial DNA. Biochem Biophys Res Commun 1991;178:124-131.
99. Zhang C, Baumer A, Maxwell RJ, Linnane AW, Nagley P. Multiple mitochondrial DNA deletions in an elderly human individual. FEBS Lett 1992;297:34-38.
100. Zhang C, Linnane AW, Nagley P. Occurrence of a particular base substitution (3243 A to G) in mitochondrial DNA of tissues of aging humans. Biochem Biophys Res Commun 1993;195:1104-1110.