Experimental evidence against the mitochondrial theory of aging A study of isolated human skeletal muscle mitochondria

Experimental Gerontology

Volumn 38, Issue 8, 2003, Pages 877-886

  Rasmussen, Ulla F ^a   Krustrup, Peter ^b   Kjær, Michael ^c   Rasmussen, Hans N ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c BISPEBJERG HOSPITAL   (Denmark)

Author keywords

Age effects; ATP formation; BSA effects; Collagen content; Cytochromes; Low temperature spectroscopy; Oxygen uptakes; Quadriceps muscle; Respiration; Specific enzyme activities

Indexed keywords

ADENOSINE TRIPHOSPHATE; CITRATE SYNTHASE; CYTOCHROME; FATTY ACID; MITOCHONDRIAL PROTEIN; PYRUVATE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; TRICARBOXYLIC ACID;

ADULT; AGE DISTRIBUTION; AGED; ARTICLE; CELL AGING; CELL ISOLATION; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; HEALTH STATUS; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; MUSCLE MITOCHONDRION; NORMAL HUMAN; OXIDATION; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN SYNTHESIS; QUADRICEPS FEMORIS MUSCLE; SARCOPLASM;

EID: 0042707789     PISSN: 05315565     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0531-5565(03)00092-5     Document Type: Article

References (54)

1. Ames B.N., Shigenaga M.K., Hagen T.M. Mitochondrial decay in aging. Biochim. Biophys. Acta. 1271:1995;165-170.
2. Anson R.M., Bohr V.A. Mitochondria, oxidative damage, and aging. J. Am. Aging Assoc. 23:2000;199-218.
3. Atamna H., Walter P.B., Ames B.N. The role of heme and iron-sulfur clusters in mitochondrial biogenesis, maintenance, and decay with age. Arch. Biochem. Biophys. 397:2002;345-353.
4. Barrientos A., Casademont J., Rötig A., Miró Ò., Urbano-Márquez A., Rustin P., Cardellach F. Absence of relationship between the level of electron transport chain activities and aging in human skeletal muscle. Biochem. Biophys. Res. Commun. 229:1996;536-539.
5. Beckman K.B., Ames B.N. The free radical theory of aging matures. Physiol. Rev. 78:1998;547-581.
6. Berg R.A. Determination of 3- and 4-hydroxyproline. Methods Enzymol. 82:1982;372-394.
7. Boffoli D., Scacco S.C., Vergari R., Solarino G., Santacroce G., Papa S. Decline with age of the respiratory chain activity in human skeletal muscle. Biochim. Biophys. Acta. 1226:1994;73-82.
8. 1 complex in skeletal muscle mitochondria. Biochim. Biophys. Acta. 1315:1996;66-72.
9. Bohr V.A., Stevnsner T., de Souza-Pinto N.C. Mitochondrial DNA repair of oxidative damage in mammalian cells. Gene. 286:2002;127-134.
10. Brierley E.J., Johnson M.A., James O.F.W., Turnbull D.M. Effects of physical activity and age on mitochondrial function. Q. J. Med. 89:1996;251-258.
11. Brierley E.J., Johnson M.A., Lightowlers R.N., James O.F.W., Turnbull D.M. Role of mitochondrial DNA mutations in human aging: implications for the central nervous system and muscle. Ann. Neurol. 43:1998;217-223.
12. Byrne E., Trounce I. Oxygen electrode studies with human skeletal muscle mitochondria in vitro. J. Neurol. Sci. 69:1985;319-333.
13. Calabrese V., Scapagnini G., Giuffrida Stella A.M., Bates T.E., Clark J.B. Mitochondrial involvement in brain function and dysfunction: relevance to aging, neurodegerative disorders and longevity. Neurochem. Res. 26:2001;739-764.
14. Chretien D., Gallego J., Barrientos A., Casademont J., Cardellach F., Munnich A., Rötic A., Rustin P. Biochemical parameters for the diagnosis of mitochondrial respiratory chain deficiency in humans, and their lack of age-related changes. Biochem. J. 329:1998;249-254.
15. Coggan A.R., Spina R.J., Rogers M.A., King D.S., Brown M., Nemeth P.M., Holloszy J.O. Histochemical and enzymatic characteristics of skeletal muscle in master athletes. J. Appl. Physiol. 68:1990;1896-1901.
16. Coggan A.R., Spina R.J., King D.S., Rogers M.A., Brown M., Nemeth P.M., Holloszy J.O. Histochemical and enzymatic comparison of the gastrocnemius muscle of young and elderly men and women. J. Gerontol. Biol. Sci. 47:1992;B71-B76.
17. Cooper J.M., Mann V.M., Schapira A.H.V. Analyses of respiratory chain function and mitochondrial DNA deletion in human skeletal muscle: effect of ageing. J. Neurol. Sci. 113:1992;91-98.
18. De Grey A.D.N. A proposed refinement of the mitochondrial free radical theory of aging. BioEssays. 19:1997;161-167.
19. De Grey A.D.N. The reductive hotspot hypothesis of mammalian aging. Membrane metabolism magnifies mutant mitochondrial mischief. Eur. J. Biochem. 269:2002;2003-2009.
20. Fujii H., Miwa S. Pyruvate kinase assay in serum and erythrocytes. Bergmeyer H.U. Methods in Enzymatic Analysis. vol. 3:1983;496-501 Verlag Chemie, Weinheim.
21. Hansford R.G. Bioenergetics in aging. Biochim. Biophys. Acta. 726:1983;41-80.
22. Hartree E.F. Haematin compounds. Paech K., Tracey M.W. Modern Methods in Plant Analysis. vol. 4:1955;208-210 Springer, Berlin.
23. Jackman M.R., Willis W.T. Characteristics of mitochondria isolated from type I and type IIb skeletal muscle. Am. J. Physiol. 270:1996;C673-C678.
24. Jezek P. Possible physiological roles of mitochondrial uncoupling proteins - UCPn. Int. J. Biochem. Cell Biol. 34:2002;1190-1206.
25. Kivirikko K.I., Laitinen O., Prockop D.J. Modifications of a specific assay for hydroxyproline in urine. Anal. Biochem. 19:1967;249-255.
26. Kovanen V., Suominen H., Risteli J., Risteli L. Type IV collagen and laminin in slow and fast skeletal muscle in rats - effects of age and life-time endurance training. Collagen Rel. Res. 8:1998;145-153.
27. Kowald A. The mitochondrial theory of aging. Biol. Signals Recept. 10:2001;162-175.
28. Lexell J. Human aging, muscle mass, and fiber type composition. J. Gerontol. 50A:1995;11-16.
29. Lightowlers R.N., Jacobs H.T., Kajander O.A. Mitochondrial DNA - all things bad. Trends Genet. 15:1999;91-93.
30. Meredith C.N., Frontera W.R., Fisher E.C., Hughes V.A., Herland J.C., Edwards J., Ewans W.J. Peripheral effects of endurance training in young and old subjects. J. Appl. Physiol. 66:1989;2844-2849.
31. Miró Ò., Casademont J., Casals E., Perea M., Urbano-Márquez Á., Rustin P., Cardellach F. Aging is associated with increased lipid peroxidation in human hearts, but not with mitochondrial respiratory chain defects. Cardiovasc. Res. 47:2000;624-631.
32. Ozawa T. Genetic and functional changes in mitochondria associated with aging. Physiol. Rev. 77:1997;425-464.
33. Pesce V., Cormio A., Fracasso F., Vecchiet J., Felzani G., Lezza A.M.S., Cantatore P., Gadaleta M.N. Age-related mitochondrial genotypic and phenotypic alterations in human skeletal muscle. Free Rad. Biol. Med. 30:2001;1223-1233.
34. O2-max in trained older subjects. J. Appl. Physiol. 82:1997;1411-1415.
35. Proctor D.N., Sinning W.E., Walro J.M., Sieck G.C., Lemon P.W.R. Oxidative capacity of human muscle fiber types: effects of age and training status. J. Appl. Physiol. 78:1995;2033-2038.
36. Rasmussen H.N., Rasmussen U.F. Respiration measurements in small scale. Anal. Biochem. 208:1993;244-248.
37. Rasmussen H.N., Rasmussen U.F. Small scale preparation of skeletal muscle mitochondria, criteria of integrity, and assays with reference to tissue function. Mol. Cell. Biochem. 174:1997;55-60.
38. Rasmussen H.N., Andersen A.J., Rasmussen U.F. Optimization of preparation of mitochondria from 25-100 mg skeletal muscle. Anal. Biochem. 252:1997;153-159.
39. Rasmussen U.F., Rasmussen H.N. Human quadriceps muscle mitochondria: a functional characterization. Mol. Cell. Biochem. 208:2000;37-44.
40. Rasmussen U.F., Rasmussen H.N. Human skeletal muscle mitochondrial capacity. Acta Physiol. Scand. 168:2000;473-480.
41. Rasmussen U.F., Rasmussen H.N., Jørgensen B.M. Three functionally different cytochrome b redox centres in pigeon heart mitochondria. Biochem. J. 201:1982;311-320.
42. Rasmussen U.F., Krustrup P., Bangsbo J., Rasmussen H.N. The effect of high-intensity exhaustive exercise studied in isolated mitochondria from human skeletal muscle. Pflügers Arch. 443:2001;180-187.
43. Rasmussen U.F., Rasmussen H.N., Krustrup P., Quistorff B., Saltin B., Bangsbo J. Aerobic metabolism of human quadriceps muscle: in vivo data parallel measurements on isolated mitochondria. Am. J. Physiol. 280:2001;E301-E307.
44. Rasmussen U.F., Krustrup P., Kjaer M., Rasmussen H.N. Human skeletal muscle mitochondrial metabolism in youth and senescence: no signs of functional changes in ATP formation and mitochondrial oxidative capacity. Pflügers Arch. 2003;. DOI 10.1007/s00424-003-1022-2.
45. Rifai Z., Welle S., Kamp C., Thornton C.A. Ragged red fibers in normal aging and inflammatory myopathy. Ann. Neurol. 37:1995;24-29.
46. Schaffner W., Weissmann C. A rapid, sensitive, and specific method for the determination of protein in dilute solution. Anal. Biochem. 56:1973;502-514.
47. Shepherd D., Garland P.G. Citrate synthase from rat liver. Methods Enzymol. 13:1969;11-16.
48. Sial S., Coggan A.R., Carroll R., Goodwin J., Klein S. Fat and carbohydrate metabolism during exercise in elderly and young subjects. Am. J. Physiol. 271:1996;E983-E989.
49. Srere P.A., Sherry A.D., Malloy C.R., Sumegi B. Channelling in the Krebs tricarboxylic acid cycle. Agius L., Sherratt H.S.A. Channelling in Intermediary Metabolism. 1997;201-217 Portland Press, London.
50. Trounce I., Byrne E., Marzuki S. Decline in skeletal muscle mitochondrial respiratory chain function: possible factor in ageing. Lancet. 25:1989;637-639.
51. Van Remmen H., Richardson A. Oxidative damage to mitochondria and aging. Exp. Gerontol. 36:2001;957-968.
52. Wallace D.C. Mitochondrial diseases in man and mouse. Science. 283:1999;1482-1488.
53. Wei Y.-H., Lee H.-C. Oxidative stress, mitochondrial DNA mutation, and impairment of antioxidant enzymes in aging. Exp. Biol. Med. 227:2002;671-682.
54. Wibom R., Hagenfeldt L., von Döbeln U. Measurement of ATP production and respiratory chain enzyme activities in mitochondria isolated from small muscle biopsy samples. Anal. Biochem. 311:2002;139-151.