The variability of the mitochondrial genome in human aging: A key for life and death?

International Journal of Biochemistry and Cell Biology

Volumn 34, Issue 11, 2002, Pages 1449-1460

  Rose, G ^a   Passarino, G ^a   Franceschi, C ^b   De Benedictis, G ^a  

^a UNIVERSITY OF CALABRIA   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Human aging; Longevity; MtDNA; Programmed death

Indexed keywords

MITOCHONDRIAL DNA;

APOPTOSIS; CELL AGING; CELL KINETICS; GENETIC VARIABILITY; GERM LINE; HUMAN; HUMAN GENETICS; MITOCHONDRIAL GENETICS; OXIDATIVE PHOSPHORYLATION; QUALITATIVE ANALYSIS; REVIEW;

AGING; APOPTOSIS; DNA, MITOCHONDRIAL; HUMANS; MITOCHONDRIA; MODELS, BIOLOGICAL; OXIDATIVE PHOSPHORYLATION; PHYLOGENY; VARIATION (GENETICS);

EID: 0036829697     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1357-2725(02)00042-0     Document Type: Review

References (79)

1. Anderson S., Bakier A.T., Barrel B.G., de Bruijin M.L.H., Coulson A.R., Drouin J., Eperon I.C., Nierlich D.P., Roe A., Sanger F., Schreier P., Smith A.J.H., Staden R., Young I.G. Sequence and organization of the human mitochondrial genome. Nature. 290:1981;457-465.
2. Andrews R.M., Kubacka I., Chinnery P.F., Lightowlers R.N., Turnbull D.M., Howell N. Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nat. Genet. 23:1999;147.
3. Kasamatsu H., Vinograd J. Unidirectionality of replication in mouse mitochondrial DNA. Nat. New Biol. 241:1973;103-105.
4. Clayton D.A. Nuclear gene products that function in mitochondrial DNA replication. Philos. Trans. R. Soc. Lond. B Biol. Sci. 317:1987;473-482.
5. Montoya J., Christianson T., Levens D., Rabinowitz M., Attardi G. Identification of initiation sites for heavy-strand and light-strand transcription in human mitochondrial DNA. Proc. Natl. Acad. Sci. U.S.A. 79:1982;7195-7199.
6. Montoya J., Gaines G.L., Attardi G The pattern of transcription of the human mitochondrial rRNA genes reveals two overlapping transcription units. Cell. 34:1983;151-159.
7. Garesse R., Vallejo C.G. Animal mitochondrial biogenesis and function: a regulatory cross-talk between two genomes. Gene. 263:2001;1-16.
8. Turrens J.F., Alexandre A., Lehninger A.L. Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Arch. Biochem. Biophys. 237:1985;408-414.
9. Harman D. The biologic clock: the mitochondria? J. Am. Geriatr. Soc. 20:1972;145-147.
10. Bertoni-Freddari C., Fattoretti P., Casoli T., Spagna C., Meier-Ruge W. Morphological plasticity of synaptic mitochondria during aging. Brain Res. 628:1993;193-200.
11. Barazzoni R., Short K.R., Nair K.S. Effects of aging on mitochondrial DNA copy number and cytochrome c oxidase gene expression in rat skeletal muscle, liver, and heart. J. Biol. Chem. 275:2000;3343-3347.
12. Cortopassi G.A., Shibata D., Soong N.W., Arnheim N. A pattern of accumulation of a somatic deletion of mitochondrial DNA in aging human tissues. Proc. Natl. Acad. Sci. U.S.A. 89:1992;7370-7374.
13. de Grey A.D. A proposed refinement of the mitochondrial free radical theory of aging. Bioessays. 19:1997;161-166.
14. 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. 286:1999;774-779.
15. Drouet M., Lauthier F., Charmes J.P., Sauvage P., Ratinaud M.H. Age-associated changes in mitochondrial parameters on peripheral human lymphocytes. Exp. Gerontol. 34:1999;843-852.
16. Fannin S.W., Lesnefsky E.J., Slabe T.J., Hassan M.O., Hoppel C.L. Aging selectively decreases oxidative capacity in rat heart interfibrillar mitochondria. Arch. Biochem. Biophys. 372:1999;399-407.
17. Esposito L.A., Melov S., Papov A., Cottrell B.A., Wallace D.C. Mitochondrial disease in mouse results in increased oxidative stress. Proc. Natl. Acad. Sci. U.S.A. 96:1999;4820-4825.
18. Lee A.C., Fenster B.E., Ito H., Takeda K., Bae N.S., Hirai T., Yu Z.X., Ferrans V.J., Howard B.H., Finkel T. Ras proteins induce senescence by altering the intracellular levels of reactive oxygen species. J. Biol. Chem. 274:1999;7936-7940.
19. S. Melov, J. Ravenscroft, S. Malik, M.S. Gill, D.W. Walker, P.E. Clayton, D.C. Wallace, B. Malfroy, S.R. Doctrow, G.J. Lithgow, Extension of life-span with superoxide dismutase/catalase mimetics, Science 289 (2000) 1567-1569.
20. Sohal R.S. The free-radical hypothesis of aging: an appraisal of the current status. Aging. 5:1993;3-17.
21. Le Bourg E. Oxidative stress, aging and longevity in Drosophila melanogaster. FEBS Lett. 498:2001;183-186.
22. Rustin P., von Kleist-Retzow J.C., Vajo Z., Rotig A., Munnich A. For debate: defective mitochondria, free-radicals, cell death, aging-reality or myth-ochondria? Mech. Ageing Dev. 114:2000;201-206.
23. Kurland C.G. Evolution of mitochondrial genomes and the genetic code. Bioessays. 14:1992;709-714.
24. Allen J.F. Control of gene expression by redox potential and the requirement for chloroplast and mitochondrial genomes. J. Theor. Biol. 165:1993;609-631.
25. Race H.L., Herrmann R.G., Martin W. Why have organelles retained genomes? Trends Genet. 15:1999;364-370.
26. Zoratti M., Szabo I. The mitochondrial permeability transition. Biochim. Biophys. Acta. 1241:1995;139-176.
27. Petit P.X., Susin S.A., Zamzami N., Mignotte B., Kroemer G. Mitochondria and programmed cell death: back to the future. FEBS Lett. 396:1996;7-13.
28. Green D.R., Reed J.C. Mitochondria and apoptosis. Science. 281:1998;1309-1312.
29. Hengartner M.O. The biochemistry of apoptosis. Nature. 407:2000;770-776.
30. +/- mouse results in the age-related decline of mitochondrial function culminating in increased apoptosis. Proc. Natl. Acad. Sci. U.S.A. 98:2001;2278-2283.
31. A. Rebollo, D. Perez-Sala, C. Martinez-A, Bcl-2 differentially targets K-, N-, and H-Ras to mitochondria in IL-2 supplemented or deprived cells: Implications in prevention of apoptosis, Oncogene 18 (1999) 4930-4939.
32. Wang H.G., Rapp U.R., Reed J.C. Bcl-2 targets the protein kinase Raf-1 to mitochondria. Cell. 87:1996;629-638.
33. Salomoni P., Wasik M.A., Riedel R.F., Reiss K., Choi J.K., Skorski T., Calabretta B. Expression of constitutively active Raf-1 in the mitochondria restores antiapoptotic and leukemogenic potential of a transformation-deficient BCR/ABL mutant. J. Exp. Med. 187:1998;1995-2007.
34. A. Nantel, M. Huber, D.Y. Thomas, Localization of endogenous Grb10 to the mitochondria and its interaction with the mitochondrial-associated Raf-1 pool, J. Biol. Chem. 274 (1999) 35719-35724.
35. Kolch W. Meaningful relationships: the regulation of the Ras/Raf/MEK/ERK pathway by protein interactions. Biochem. J. 351:2000;289-305.
36. Migliaccio E., Giorgio M., Mele S., Pelicci G., Reboldi P., Pandolfi P.P., Lanfrancone L., Pelicci P.G. The p66shc adaptor protein controls oxidative stress response and life span in mammals. Nature. 402:1999;309-313.
37. Salvioli S., Bonafe M., Capri M M., Monti D., Franceschi C. Mitochondria, aging and longevity: a new perspective. FEBS Lett. 492:2001;9-13.
38. Skulachev V.P. The programmed death phenomena, aging and the Samurai law of biology. Exp. Gerontol. 36:2001;995-1024.
39. A. Weissman, Essays upon Heredity and Kindred Biological Problems, Claderon Press, Oxford, 1889.
40. B.P. Medawar, An Unsolved Problem of Biology, H.K. Lewis, London, 1952.
41. Polla B.S., Kantengwa S., Francois D., Salvioli S., Franceschi C., Marsac C., Cossarizza A. Mitochondria are selective targets for the protective effects of heat shock against oxidative injury. Proc. Natl. Acad. Sci. U.S.A. 93:1996;6458-6463.
42. Yashin A.I., Ukraintseva S.V., De Benedictis G., Anisimov V.N., Butov A.A., Arbeev K., Jdanov D.A., Boiko S.I., Begun A.S., Bonafè M., Franceschi C. Have the oldest old adults ever been frail in the past? A hypothesis that explains modern trends in survival. J. Geront. A Biol. Sci. Med. Sci. 56:2001;B432-442.
43. De Benedictis G., Franceschi C. The genetics of successful aging. Aging Clin. Exp. Res. 10:1998;147-148.
44. Elson J.L., M Andrews R., Chinnery P.F., Lightowlers R.N., Tumbull D.M., Howell N. Analysis of European mtDNAs for recombination. Am. J. Hum. Genet. 68:2001;145-153.
45. Johnson M.J., Wallace D.C., Ferris S.D., Rattazzi M.C., Cavalli-Sforza L.L. Radiation of human mitochondria DNA types analyzed by restriction endonuclease cleavage patterns. J. Mol. Evol. 19:1983;255-271.
46. Cann R.L., Stoneking M., Wilson A.C. Mitochondrial DNA and human evolution. Nature. 325:1987;31-36.
47. Ballinger S.W., Schurr T.G., Torroni A., Gan Y.Y., Hodge J.A., Hassan K., Chen K.M., Wallace D.C. South-east Asian mitochondrial DNA analysis reveals genetic continuity of ancient Mongoloid migrations. Genetics. 130:1992;139-152.
48. Vigilant L., Stoneking M., Harpending H., Hawkes K., Wilson A.C. African populations and the evolution of human mitochondrial DNA. Science. 253:1991;1503-1507.
49. Graven L., Passarino G., Semino O., Boursot P., Santachiara-Benerecetti A.S., Langaney A., Excoffier L. Evolutionary correlation between control region sequence and restriction polymorphisms in the mitochondrial genome of a large Senegalese mandenka. Mol. Biol. Evol. 12:1995;334-345.
50. Richards M.B., Macaulay V.A., Bandelt H.J., Sykes B.C. Phylogeography of mitochondrial DNA in western Europe. Ann. Hum. Genet. 62:1998;241-260.
51. Ingman M., Kaessmann H., Paabo S., Gyllensten U. Mitochondrial genome variation and the origin of modern humans. Nature. 408:2000;708-713.
52. Rose G., Passarino G., Carrieri G., Altomare K., Greco V., Bertolini S., Bonafè M., Franceschi C., De Benedictis G. Paradoxes in longevity: sequence analysis of mtDNA haplogroup J in centenarians. Eur. J. Hum. Genet. 9:2001;701-707.
53. Finnila S., Lehtonen M.S., Majamaa K. Related articles phylogenetic network for European mtDNA. Am. J. Hum. Genet. 68:2001;1475-1484.
54. L.L. Cavalli-Sforza, P. Menozzi, A. Piazza, History and Geography of Human Genes, Princeton University Press, Princeton, 1994.
55. Underhill P.A., Passarino G., Lin A.A., Shen P., Mirazon Lahr M., Foley R.A., Oefner P.J., Cavalli-Sforza L.L. The phylogeography of Y chromosome binary haplotypes and the origins of modern human populations. Ann. Hum. Genet. 65:2001;43-62.
56. Torroni A., Huoponen K., Francalacci P., Petrozzi M., Morelli L., Scozzari R., Obinu D., Savontaus M.L., Wallace D.C. Classification of European mtDNAs from an analysis of three European populations. Genetics. 144:1996;1835-1850.
57. Passarino G., Semino O., Bernini L.F., Santachiara-Benerecetti A.S. Pre-Caucasoid and Caucasoid genetic features of the Indian population, revealed by mtDNA polymorphisms. Am. J. Hum. Genet. 59:1996;927-934.
58. Macaulay V., Richards M., Hickey E., Vega E., Cruciani F., Guida V., Scozzari R., Bonne-Tamir B., Sykes B., Torroni A. The emerging tree of West Eurasian mtDNAs: a synthesis of control-region sequences and RFLPs. Am. J. Hum. Genet. 64:1999;232-249.
59. Quintana-Murci L., Semino O., Bandelt H.J., Passarino G., McElreavey K., Santachiara-Benerecetti A.S. Genetic evidence of an early exit of Homo sapiens sapiens from Africa through eastern Africa. Nat. Genet. 23:1999;437-441.
60. Richards M., Macaulay V., Hickey E., Vega E., Sykes B., Guida V., Rengo C., Sellitto D., Cruciani F., Kivisild T., Villems R., Thomas M., Rychkov S., Rychkov O., Rychkov Y., Golge M., Dimitrov D., Hill E., Bradley D., Romano V., Cali F., Vona G., Demaine A., Papiha S., Triantaphyllidis C., Stefanescu G. Tracing European founder lineages in the near eastern mtDNA pool. Am. J. Hum. Genet. 67:2000;1251-1276.
61. Wallace D.C., Singh C., Lott M.T., Hodge J.A., Schurr T.G., Lezza A.M., Elsas L.J. II, Nikoskelainen E.K. Mitochondrial DNA mutation associated with Leber's hereditary optic neuropathy. Science. 242:1988;1427-1430.
62. Holt I.J., Harding A.E., Morgan-Hughes J.A. Deletions of muscle mitochondrial DNA in patients with mitochondrial myopathies. Nature. 331:1988;717-719.
63. Ruiz Pesini E., Lapena A.C., Diez-Sanchez A.C., Perez-Martos A., Montoya J., Alvarez E., Diaz M., Urries A., Montoro L., Lopez-Perez M.J., Enriquez J.A. Human mtDNA haplogroups associated with huge or reduced spermatozoa motility. Am. J. Hum. Genet. 67:2000;682-696.
64. De Benedictis G., Rose G., Carrieri G., De Luca M., Falcone E., Passarino G., Bonafè M., Monti D., Baggio G., Bertolini S., Mari D., Mattace R., Franceschi C. Mitochondrial DNA inherited variants are associated with successful aging and longevity in humans. FASEB J. 13:1999;1532-1536.
65. Ross O.A., McCormack R., Curran M.D., Duguid A.R., Barnett Y.A., Rea I.M., Middleton D. Mitochondrial DNA polymorphism: its role in longevity of the Irish population. Exp. Gerontol. 36:2001;1161-1178.
66. Torroni A., Petrozzi M., D'Urbano L., Sellitto D., Zeviani M., Carrara F., Carducci C., Leuzi V., Barboni P., De Negri A., Scozzari R. Haplotype and phylogenetic analyses suggest that one European-specific mtDNA background plays a role in the expression of Leber's hereditary optic neuropathy by increasing the penetrance of the primary mutations 11778 and 14484. Am. J. Hum. Genet. 60:1997;1107-1121.
67. Chagnon P., Gee M., Filion M., Robitaille Y., Belouchi M., Gauvreau D. Phylogenetic analysis of the mitochondrial genome indicates significant difference between patients with Alzheimer's disease and controls in a French-Canadian founder population. Am. J. Med. Genet. 85:1999;20-30.
68. Kirchman P.A., Kim S., Lai C.Y., Jazwinski M.S. Interorganelle signaling is a determinant of longevity in Saccharomyces cerevisae. Genetics. 152:1999;179-190.
69. Tanaka M., Gong J.S., Zhang J., Yoneda M., Yagi K. Mitochondrial genotype associated with longevity. Lancet. 351:1998;185-186.
70. De Benedictis G., Carrieri G., Garasto S., Rose G., Varcasia O., Bonafe M., Franceschi C., Jazwinski S.M. Does a retrograde response in human aging and longevity exist? Exp. Gerontol. 35:2000;795-801.
71. De Benedictis G., Carotenuto L., Carrieri G., De Luca M., Falcone E., Rose G., Cavalcanti S., Corsonello F., Feraco E., Baggio G., Bertolini S., Mari D., Mattace R., Yashin A.I., Bonafe M., Franceschi C. Gene/longevity association studies at four autosomal loci (REN, THO, PARP, SOD2). Eur. J. Hum. Genet. 6:1998;534-541.
72. Meloni R., Albanese V., Ravassard P., Treilhou F., Mallet J. A tetranucleotide polymorphic microsatellite, located in the first intron of the tyrosine hydroxylase gene, acts as a transcription regulatory element in vitro. Hum. Mol. Genet. 7:1998;423-428.
73. Franceschi C., Bonafè M., Valensin S., Olivieri F., De Luca M., Ottaviani E., De Benedictis G., An evolutionary perspective on immunosenescence Ann. N. Y. Acad. Sci. 908:2000;244-254.
74. Carrieri G., Bonafè M., De Luca M., Rose G., Varcasia O., Bruni A., Maletta R., Nacmias B., Sorbi S., Corsonello F., Feraco E., Andreev K.A., Yashin A., Franceschi C., De Benedictis G. Mitochondrial DNA haplogroups and APOEe4 allele are non-independent variables in sporadic Alzheimer's disease. Hum. Genet. 108:2001;194-198.
75. M.N. Gadaleta, B. Kadenbach, A.M.S. Lezza, A. Reith, P. Cantatore, D. Boffoli, S. Papa, Aged-linked changes in the genotype and phenotype of mitochondria, in: S. Papa, et al. (Eds.), Frontiers in Cellular Bionergetics, Plenum Press, New York, 1999, pp. 693-727.
76. Wang Y., Michikawa Y., Mallidis C., Woodhouse L., Yarasheski K.E., Miller C.A., Askanas V., Engel W.K., Bhasin S., Attardi G. Muscle-specific mutations accumulate with aging in critical human mtDNA control sites for replication. Proc. Natl. Acad. Sci. U.S.A. 98:2001;4022-4027.
77. Tanaka M., Gong J., Zhang J., Yamada Y., Borgeld H.J., Yagi K. Mitochondrial genotype associated with longevity and its inhibitory effect on mutagenesis. Mech. Ageing Dev. 116:2000;65-76.
78. Rattan S.I.S. I no longer believe that cell death is programmed, an interview with Vincent Cristofalo. Biogerontology. 2:2001;283-290.
79. Brown M.D., Hosseini S.H., Torroni A., Bandelt H.J., Allen J.C., Schurr T.G., Scozzari R., Cruciani F., Wallace D.C. mtDNA haplogroup X: an ancient link between Europe/western Asia and North America? Am. J. Hum. Genet. 63:1998;1852-1861.