Analysis of age-associated mitochondrial DNA deletion breakpoint regions from mice suggests a novel model of deletion formation

Journal of the American Aging Association

Volumn 19, Issue 4, 1996, Pages 117-128

  Chung, Susan S ^a   Eimon, Peter M ^a   Weindruch, Richard ^b   Aiken, Judd M ^a,c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN   (United States)

^c NONE   (United States)

Author keywords

Aging; Mouse; mtDNA deletions; Replication jumping model

Indexed keywords

EID: 2842590500     PISSN: 01619152     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF02434081     Document Type: Article

References (83)

1. Agarwal S and Sohal RS DNA oxidative damage and life expectancy in houseflies. Proc. Natl. Acad. Sci. USA 91 (25):12332-12335, 1994.
2. Attardi G: The elucidation of the human mitochondrial genome: a historical perspective. Bioessays 5(1): 34-39, 1986.
3. Bandy B and Davison AJ: Mitochondrial mutations may increase oxidative stress: implications for carcinogenesis and aging. Free Radical Biol. Med. 8(6):523-539, 1990.
4. Baumer A, Zhang C, Linnane AW and Nagley, P: Age-related human mtDNA deletions: A heterogeneous set of deletions arising at a single pair of directly repeated sequences. Am. J. Hum. Genet. 54(4):618-630, 1994.
5. Bibb MJ, Van Etten RA, Wright CT, Walberg MW and Clayton DA: Sequence and gene organization of mouse mitochondrial DNA. Cell 26(2 Pt2):167-180, 1981.
6. Blok RB, Thorburn DR, Thompson GN and Dahl HHM: A topoisomerase II cleavage site is associated with a novel mitochondrial DNA deletion. Hum. Genet. 95(1):75-81, 1995.
7. Bogenhagen D and Clayton DA: Mechanism of mitochondrial DNA replication in mouse L-cells: Introduction of superhelical turns into newly replicated molecules J. Mol. Biol. 119(1):69-81, 1978.
8. Brossas JY, Barreau E, Courtois Y and Tréton J: Multiple deletions in mitochondrial DNA are present in senescent mouse brain. Biochem. Biophys. Res. Comm. 202(2):654-659, 1994.
9. Castora FJ and Simpson MV. Search for a DNA gyrase in mammalian mitochondria. J. Biol Chem. 254(22):11193-11195, 1979.
10. Castora FJ, Vissering FF and Simpson MV: The effect of bacterial DNA gyrase inhibitors on DNA synthesis in mammalian mitochondria. Biochim. Biophys. Acta 740(4):417-427, 1983.
11. Chung SS, Weindruch R, Schwarze SR, McKenzie DI and Aiken JM: Multiple age-associated mitochondrial DNA deletions in skeletal muscle of mice. Aging Clin. Exp. Res. 6(3):193-200, 1994.
12. Clayton DA: Replication of animal mitochondrial DNA. Cell 28(4):693-705, 1982
13. Corral-Debrinski M, HortonT, Lott MT, Shoffner JM, Beal MF and Wallace DC: Mitochondrial DNA deletions in human brain. regional variability and increase with advanced age. Nature Genet. 2(4):324-329, 1992.
14. Cortopassi GA and Arnheim N: Detection of a specific mitochondrial DNA deletion in tissues of older humans. Nucl Acids Res. 18(23):6927-6933, 1990.
15. Cortopassi GA, Shibata D, Soong NW and Arnheim N: A pattern of accumulation of a somatic deletion of mitochondrial DNA in aging human tissues. Proc. Natl. Acad. Sci. USA 89(16):7370-7374, 1992.
16. Degoul F, Nelson I, Amselem S, Romero N, Obermaier-Kusser B, Ponsot G, Marsac C and Lestienne P: Different mechanisms inferred from sequences of human mitochondrial DNA deletions in ocular myopathies. Nucl. Acids Res. 19(3):493-496, 1991.
17. Devereaux J, Haeberli P and Smithies O: A comprehensive set of sequence analysis programs for the VAX. Nucl Acids Res. 12(1Pt1):387-395, 1984.
18. Dizdaroglu M: Oxidative damage to DNA in mammalian chromatin. Mutat. Res. 275(3-6):331-342, 1992.
19. Douc-Rasy S, Kayser A, Riou JF, and Riou G: ATP-independent type II topoisomerase from trypanosomes. Proc. Natl. Acad. Sci. USA 83(19):7152-7156, 1986.
20. Edris W, Burgett B, Stine OC and Filburn CR: Detection and quantitation by competitive PCR of an age-associated increase in a 4.8-kb deletion in rat mitochondrial DNA. Mutat. Res. 316(2):69-78, 1994.
21. Eimon PM, Chung SS, Lee CM, Weindruch R and Aiken JM: Age-associated mitochondrial DNA deletions in mouse skeletal muscle: comparison of different regions of the mitochondrial genome. Dev. Genet. 18(2) 107-113, 1996.
22. Fleming JE, Miquel J, Cottrell SF, Yengoyan LS and Economos AC: Is cell aging caused by respiration-dependent injury to the mitochondrial genome? Gerontology 28(1):44-53, 1982.
23. Fraga CG, Shigenaga MK, Park JW, Degan P and Ames BN: Oxidative damage to DNA during aging: 8-hydroxy-2′-deoxyguanosine in rat organ DNA and urine. Proc. Natl. Acad. Sci. USA 87(12):4533-4537, 1990.
24. Fragoso SP and Goldenberg S: Cloning and characterization of the gene encoding Trypanosoma cruzi DNA topoisomerase II. Mol. Biochem. Parasitol. 55(1-2):127-134, 1992.
25. Gadaleta MN, Rainaldi G, Lezza AMS. Milella F, Fracasso F and Cantatore P: Mitochondrial DNA copy number and mitochondrial DNA deletions in adult and senescent rats. Mutat. Res. 275(3-6):181-193, 1992.
26. Gudikote JP and Van Tuyle GC: Rearrangements in the shorter arc of rat mitochondrial DNA involving the region of the heavy and light strand promoters. Mutat. Res. 356 (2): 275-286, 1996.
27. Harman, D: Free radical theory of aging: consequences of mitochondrial aging. Age 6(3).86-94, 1983
28. Hattori K, Tanaka M, Sugiyama S, Obayashi T, Ito T, Satake T, Hanaki Y, Asai J, Nagano M and Ozawa T: Age-dependent increase in deleted mitochondrial DNA in the human heart: possible contributory factor to presbycardia. Am. Heart J. 121(6):1735-1742, 1991.
29. Hayakawa M, Torri K, Sugiyama S, Tanaka M and Ozawa T: Age-associated accumulation of 8-hydroxydeoxyguanosine in mitochondrial DNA of human diaphragm. Biochem. Biophys. Res. Comm. 179(2):1023-1029, 1991.
30. Hayakawa M, Hattori K, Sugiyama S and Ozawa T: Age-associated oxygen damage and mutations in mitochondrial DNA in human hearts. Biochem. Biophys. Res. Comm. 189(2):979-985, 1992.
31. Hayakawa M, Sugiyama S, Hattori K, Takasawa M and Ozawa T: Age-associated damage in mitochondrial DNA in human hearts. Mol. Cell Biochem. 119(1-2):95-103, 1993.
32. Holt IJ, Harding AE and Morgan-Hughes JA: Deletions of muscle mitochondrial DNA in mitochondrial myopathies. sequence analysis and possible mechanisms. Nucl. Acids Res 17(12):4465-4469, 1989.
33. Katayama M, Tanaka M, Yamamoto H, Ohbayashi T. Nimura Y and Ozawa T: Deleted mitochondrial DNA in the skeletal muscle of aged individuals. Biochem. Int. 25(1):47-56, 1991.
34. Keefe DL, Niven-Fairchild T, Powell S and Buradagunta S: Mitochondrial deoxyribonucleic acid deletions in oocytes and reproductive aging in women Fertil. Steril. 64(3):577-583, 1995.
35. King SR, Krolewski MA, Marvo SL, Lipson PJ, Pogue-Geile KL, Chung JH and Jaskunas R: Nucleotide sequence analysis of in vivo recombinants between bateriophage λ DNA and pBR322. Mol. Gen. Genet. 186(4):548-557, 1982.
36. Kitagawa T, Suganuma N, Nawa A, Kikkawa F, Tanaka M, Ozawa T and Tomoda Y: Rapid accumulation of deleted mitochondrial deoxyribonucleic acid in postmenopausal women. Biol Reprod. 49(4):730-736, 1993.
37. Kuchino Y, Mori F, Kasai H, Inoue H, Iwai S, Miura K, Ohtsuka E and Nishimura S: Misreading of DNA templates containing 8-hydroxydeoxyguanosine at the modified base and at adjacent residues. Nature 327(6117):77-79, 1987.
38. Kunkel TA and Mosbaugh DW: Exonucleolytic proofreading by a mammalian DNA polymerase g. Biochem. 28(3):988-995, 1989.
39. Lee CM, Chung SS, Kaczkowski JM, Weindruch R and Aiken JM: Multiple mitochondrial DNA deletions associated with age in skeletal muscle of rhesus monkeys. J. Gerontol 48(6):B201-B205, 1993.
40. Lee CM, Eimon P, Weindruch R and Aiken JM: Direct repeat sequences are not required at the breakpoints of age-associated mitochondrial DNA deletions in rhesus monkeys. Mech. Ageing Dev. 75(1):69-79, 1994.
41. Lee HC, Pang CY, Hsu HS and Wei YH. Differential accumulation of 4,977 bp deletion in mitochondrial DNA of various tissues in human ageing. Biochim. Biophys. Acta 1226(1):37-43, 1994.
42. Linnane AW, Marzuki S, Ozawa T and Tanaka M: Mitochondrial DNA mutations as an important contributor to ageing and degenerative diseases. Lancet i (8639):642-645, 1989.
43. Linnane AW, Baumer A, Maxwell RJ, Preston H, Zhang CF and Marzuki S: Mitochondrial gene mutation: the aging process and degenerative diseases. Biochem. Int. 22(6):1067-1076, 1990.
44. Mecocci P, MacGarvey U, Kaufman AE, Koontz D, Shoffner JM, Wallace DC and Beal MF: Oxidative damage to mitochondrial DNA shows marked age-dependent increases in human brain. Ann. Neurol. 34(4):609-616, 1993.
45. Melendy T and Ray DS: Novobiovin affinity purification of a mitochondrial type II topoisomerase from the typanosomatid Crithidia fasciculata. J. Biol. Chem. 264(3):1870-1876, 1989.
46. Melov S, Hertz GZ, Stormo GD and Johnson TE: Detection of deletions in the mitochondrial genome of Caenorhabditis elegans. Nucl. Acids Res. 22(6): 1075-1078, 1994.
47. Melov S, Lithgow GJ, Fischer DR, Tedesco PM and Johnson TE: Increased frequency of deletions in the mitochondrial genomes with age of Caenorhabditis elegans. Nucl. Acids Res. 23(8):1419-1425, 1995.
48. Miquel J and Fleming JE: Theoretical and experimental support for an "oxygen radical-mitochondrial injury" hypothesis of cell aging in Free Radicals, Aging and Degenerative Diseases, edited by Johnson JE, Walford R, Harman D, Miquel J, New York, Liss, 1986, p.p. 51-74.
49. Mita S, Rizzuto R, Moraes C, Shanske S, Arnaudo E, Fabrizi GM, Koga Y, DiMauro S and Schon EA: Recombination via flanking direct repeats is a major cause of large-scale deletions of human mitochondrial DNA. Nucl. Acids Res. 18(3):561-567, 1990.
50. Naito A, Naito S and Ikeda H: Homology is not required for recombination mediated by DNA gyrase of Escherichia coli. Mol. Gen. Genet. 193(2):238-243, 1984.
51. Pang CY, Lee HC, Yang JH and Wei YH. Human skin mitochondrial DNA deletions associated with light exposure. Arch Biochem. Biophys. 312(2):534-538, 1994.
52. Pasion SG, Hines JC, Aebersold R and Ray DS: Molecular cloning and expression of the gene encoding the kinetoplast-associated type II topoisomerase of Crithidia fasciculata. Mol. Biochem. Parasitol. 50(1):57-68, 1992.
53. Richter C, Park PW and Ames BN: Normal damage to mitochondrial and nuclear DNA is extensive Proc Natl. Acad. Sci. USA. 85(17):6465-6467, 1988
54. Schon EA, Rizzuto R, Moraes CT, Nakase H, Zeviani M and DiMauro S: A direct repeat is a hotspot for large-scale deletion of human mitochondrial DNA. Science 244(4902):346-349, 1989.
55. Shibutani S, Takeshita M and Grollman AP: Insertions of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature 349(6308).431-434, 1991.
56. Shigenaga MK, Gimeno CJ and Ames BN: Urinary 8-hydroxy-2′-deoxyguanosine as a biological marker of in vivo oxidative DNA damage Proc. Natl. Acad. Sci. USA 86(24):9697-9701, 1989.
57. Shlomai J, Zadok A and Frank D. A unique ATP-dependent DNA topoisomerase from trypanosomatids. Adv. Exp. Med. Biol. 179.409-422, 1984.
58. Shoffner JM, Lott MT, Voliavec AS, Soueidan SA, Costigan DA and Wallace DC: Spontaneous Kearns-Sayre/chronic external opthalmoplegia plus syndrome associated with a mitochondrial DNA deletion: a slip-replication model and metabolic therapy. Proc. Natl. Acad. Sci. USA86(20):7952-7956, 1989.
59. Simonetti S, Chen X, DiMauro S and Schon EA: Accumulation of deletions in human mitochondrial DNA during normal aging: analysis by quantitative PCR. Biochim. Biophys. Acta 1180(2):113-122, 1992.
60. Sohal RS and Brunk UT: Mitochondrial production of pro-oxidants and cellular senescence. Mutat. Res. 275(3-6):295-304, 1992.
61. Sohal RS, Agarwal S, Candas M, Forster MJ and Lal H: Effect of age and caloric restriction on DNA oxidative damage in different tissues of C57BL/6 mice. Mech. Ageing Dev. 76(2-3):215-224, 1994.
62. Sohal RS and Weindruch R: Oxidative stress, caloric restriction, and aging. Science 273(5271):59-63, 1996.
63. Soong NW, Hinton DR. Cortopassi G and Arnheim N: Mosaicism for a specific somatic mitochondrial DNA mutation in adult human brain Nature Genet. 2(4):318-323, 1992.
64. Spitzner JR, Chung IK and Muller MT: Eukaryotic topoisomerase II preferentially cleaves alternating purine-pyrimidine repeats. Nucl Acids Res. 18(1).1-11, 1990.
65. Strauss PR, and Wang JC: The TOP2 gene of Trypanosoma brucei: a single-copy gene that shares extensive homology with other TOP2 genes encoding eukaryotic DNA topoisomerase II. Mol. Biochem. Parasitol. 38(1):141-150, 1990.
66. Suganuma N, Kitagawa T, Nawa A and Tomoda Y: Human ovarian aging and mitochondrial DNA deletion Horm. Res. 39(suppl. 1):16-21, 1993.
67. Sugiyama S, Hattori K, Hayakawa M and Ozawa T: Quantitative analysis of age-associated accumulation of mitochondrial DNA with deletion in human hearts. Biochem. Biophys. Res. Comm. 180(2):894-899, 1991.
68. Tanhauser SM and Laipis PJ: Multiple deletions are detectable in mitochondrial DNA of aging mice. J. Biol. Chem. 270(42):24769-24775, 1995
69. Torii K, Sugiyama S, Tanaka M, Takagi K, Hanaki Y, Iida K, Matsuyama M, Hirabayashi N, Uno Y and Ozawa T: Aging-associated deletion of human diaphragmatic mitochondrial DNA. Am. J. Respir. Cell Mol Biol. 6(5):543-549, 1992.
70. Tzagoloff A and Myers AM: Genetics of mitochondrial biogenesis. Annu. Rev. Biochem. 55:249-285, 1986.
71. Van Tuyle GC, Gudikote JP, Hurt VR, Miller BB and Moore CA: Multiple, large deletions in rat mitochondrial DNA: evidence for a major hot spot. Mutat. Res. 349(1):95-107, 1996.
72. Volk MJ, Pugh TD, Kim M, Frith CH, Daynes RA, Ershler WB and Weindruch R: Dietary restriction from middle age attenuates age-associated lymphoma development and interleukin 6 dysregulation in C57BL/6 mice. Cancer Res. 54(11):3054-3061, 1994.
73. von Zglinicki T and Bimmler M: Intercellular water and ionic shifts during growth and ageing of rats. Mech. Ageing Dev. 38(2): 179-187, 1987.
74. Vosberg HP: DNA topoisomerases: enzymes that control DNA conformation. Curr. Topics Microbiol. Immunol. 114:19-102, 1985.
75. Wagner JR, Hu CC and Ames BN: Endogenous oxidative damage of deoxycytidine in DNA. Proc. Natl. Acad. Sci. USA 89(8):3380-3384, 1992.
76. Wallace DC: Diseases of the mitochondrial DNA. Annu. Rev Biochem. 61:1175-1212, 1992.
77. Yamamoto H, Tanaka M, Katayama M, Obayashi T, Nimura Y and Ozawa T: Significant existence of deleted mitochondrial DNA in cirrhotic liver surrounding hepatic tumor. Biochem. Biophys. Res. Comm 182(2):913-920, 1992.
78. Yen TC, Su JH, King KL and Wei YH: Ageing-associated 5 Kb deletion in human liver mitochondrial DNA. Biochem. Biophys. Res. Comm. 178(1)L: 124-131, 1991.
79. Yen TC, Pang CY, Hsieh RH, Su CH, King KL and Wei YH: Age-dependent 6 Kb deletion in human liver mitochondrial DNA. Biochem. Int 26(3):457-468, 1992.
80. Yoneda M, Katsumata K, Hayakawa M, Tanaka M and Ozawa T: Oxygen stress induces an apoptotic cell death associated with fragmentation of mitochondrial genome. Biochem. Biophys. Res. Comm. 209(2):723-729, 1995.
81. Zeviani M, Servidei S, Gellera C, Bertini E, DiMauro S and DiDonato S: An autosomal dominant disorder with multiple deletions of mtDNA starting at the D-loop region. Nature 339(6222):309-311, 1989.
82. Zhang C, Baumer A, Maxwell RJ, Linnane AW and Nagiey P: Multiple mitochondrial DNA deletions in an elderly human individual. FEBS. 297(1, 2):34-38, 1992.
83. Zhang C, Baumer A, Mackay IR, Linnane AW and Nagley P: Unusual pattern of mitochondrial DNA deletions in skeletal muscle of an adult human with chronic fatigue syndrome. Hum. Mol. Genet. 4(4).751-754, 1995.