Examining the mechanisms responsible for lower ROS release rates in liver mitochondria from the long-lived house sparrow (Passer domesticus) and big brown bat (Eptesicus fuscus) compared to the short-lived mouse (Mus musculus)

Mechanisms of Ageing and Development

Volumn 130, Issue 8, 2009, Pages 467-476

  Brown, Jason C L ^a   McClelland, Grant B ^b   Faure, Paul A ^b   Klaiman, Jordan M ^a   Staples, James F ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

Aging; Hydrogen peroxide; Longevity; Spare capacity; Uncoupling to survive

Indexed keywords

HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE; UBIQUINOL CYTOCHROME C REDUCTASE;

ANIMAL TISSUE; ARTICLE; BAT; CONTROLLED STUDY; ENZYME ACTIVITY; LIVER MITOCHONDRION; LONGEVITY; METABOLIC RATE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTON TRANSPORT; RESPIRATORY CHAIN; SPARROW; SPECIES COMPARISON;

AGING; ANIMALS; CHIROPTERA; CYTOCHROMES C; HYDROGEN PEROXIDE; KINETICS; LONGEVITY; MEMBRANE POTENTIALS; MICE; MITOCHONDRIA, LIVER; MITOSIS; OXIDOREDUCTASES; REACTIVE OXYGEN SPECIES; SPARROWS; SUCCINIC ACID;

EPTESICUS; EPTESICUS FUSCUS; MUS; MUS MUSCULUS; PASSER DOMESTICUS; PASSERIDAE;

EID: 67650693720     PISSN: 00476374     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mad.2009.05.002     Document Type: Article

References (77)

1. Bains R., Moe M.C., Larsen G.A., Berg-Johnsen J., and Vinje M.L. Volatile anaesthetics depolarize neural mitochondria by inhibition of the electron transport. Acta Anaesthesiol. Scand. 50 (2006) 572-579
2. Barja G. Mitochondria free radical release and aging in mammals and birds. Ann. NY Acad. Sci. 854 (1998) 224-238
3. Barja G. Mitochondrial oxygen radical generation and leak: sites of release in states 4 and 3, organ specificity, and relation to aging and longevity. J. Bioenerg. Biomembr. 31 (1999) 347-366
4. Barja G. Mitochondrial oxygen consumption and reactive oxygen species release are independently modulated: implications for aging studies. Rejuv. Res. 10 (2007) 215-223
5. Barja G., and Herrero A. Localization at complex I and mechanism of the higher free radical release of brain nonsynaptic mitochondria in the short-lived rat than the longevous pigeon. J. Bioenerg. Biomembr. 30 (1998) 235-243
6. 2 consumption can explain the simultaneous presence of high longevity and high aerobic metabolic rate in birds. Free Radic. Res. 21 (1994) 317-328
7. Beer J.R., and Richards A.G. Hibernation of the big brown bat. J. Mammol. 37 (1956) 31-41
8. Brand M.D. Uncoupling to survive? The role of mitochondrial inefficiency in ageing. Exp. Gerontol. 35 (2000) 811-820
9. Brand M.D., Brindle K.M., Buckingham J.A., Harper J.A., Rolfe D.F.S., and Stuart J.A. The significance and mechanism of mitochondrial proton conductance. Int. J. Obesity 23 (1999) S4-S11
10. + leak and ROS generation: an add couple. Free Rad. Biol. Med. 38 (2005) 12-23
11. Brown J.C.L., Gerson A.R., and Staples J.F. Mitochondrial metabolism during daily torpor in the dwarf Siberian: role of active regulated changes and passive thermal effects. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293 (2007) R1833-R1845
12. Brunet-Rossinni A.K. Reduced free-radical release and extreme longevity in the little brown bat (Myotis lucifugus) versus two non-flying mammals. Mech. Ageing Dev. 125 (2004) 11-40
13. 2 release during aging in oxidative and glycolytic muscles in rats. Mech. Ageing Dev. 125 (2004) 367-373
14. Chappell M.A., Bech C., and Buttemer W.A. The relationship of central and peripheral organ masses to aerobic performance variation in house sparrows. J. Exp. Biol. 202 (1999) 2269-2279
15. Chen Q., Vazquez E.J., Moghaddas S., Hoppel C.L., and Lesnefsky E.J. Release of reactive oxygen species by mitochondria. Central role of complex III. J. Biol. Chem. 278 (2003) 36027-36031
16. Finkel T., and Holbrook N.J. Oxidants, oxidative stress and the biology of ageing. Nature 408 (2000) 239-247
17. Fridell Y.-W.C., Sanchez-Blanco A., Silvia B.A., and Helfand S.L. Targeted expression of the human uncoupling protein 2 (hUCP2) to adult neurons extends life span in the fly. Cell Metab. 1 (2005) 145-152
18. Graves J.L., Luckinbill L.S., and Nichols A. Flight duration and wing beat frequency in long- and short-lived Drosophila melanogaster. J. Insect Physiol. 34 (1988) 1021-1026
19. Green J.D., and Narahara H.T. Assay of succinate dehydrogenase activity by the tetrazolium method: evaluation of an improved technique in skeletal muscle fractions. J. Histochem. Cytochem. 28 (1980) 408-412
20. Hamilton M.L., Van Remmen H., Drake J.A., Yang H., Guo Z.M., Kewitt K., Walter C.A., and Richardson A. Does oxidative damage to DNA increase with age?. PNAS (2001) 10469-10474
21. Hanley J., Ray U., and Brandt J. Daut, Halothane, isoflurane and sevoflurane inhibit NADH:ubiquinone oxidoreductase (complex I) of cardiac mitochondria. J. Physiol. 544 (2002) 687-693
22. Harman D. Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 11 (1956) 298-300
23. Harman D. The biological clock: the mitochondria?. J. Am. Geriatr. Soc. 20 (1972) 145-147
24. Harper J.M., Durkee S.J., Dysko R.C., Austad S.N., and Miller R.A. Genetic modulation of hormone levels and life span in hybrids between laboratory and wild-derived mice. J. Gerontol. 61A (2006) 1019-1029
25. Herreid C.F., and Schmidt-Nielsen K. Oxygen consumption, temperature, and water loss in bats from different environments. Am. J. Physiol. 211 (1966) 1108-1112
26. Herrero A., and Barja G. Sites and mechanisms responsible for the low rate of free radical release of heart mitochondria in the long-lived pigeon. Mech. Ageing Dev. 98 (1997) 95-111
27. 2 release of heart mitochondria and aging rate are slower in canaries and parakeets than in mice: sites of free radical generation and mechanisms involved. Mech. Ageing Dev. 103 (1998) 133-146
28. Herrero A., and Barja G. Localization of the site of oxygen radical generation inside the complex I of heart and nonsynaptic brain mammalian mitochondria. J. Bioenerg. Biomembr. 32 (2000) 609-615
29. Jurgens K.D., and Prothero J.W. Scaling of maximal lifespan in bats. Comp. Biochem. Physiol. A 88 (1987) 361-367
30. Klimkiewicz M.K., and Futcher A.G. Longevity records of North American birds: Coerbinae through Estrildidae. J. Field Ornithol. 58 (1987) 318-333
31. Konarzewski M., and Diamond J. Evolution of basal metabolic rate and organ masses in laboratory mice. Evolution 49 (1995) 1239-1248
32. Ku H.-H., and Sohal R.S. Comparison of mitochondrial pro-oxidant generation and anti-oxidant defenses between rat and pigeon: possible basis of variation in longevity and metabolic potential. Mech. Ageing Dev. 72 (1993) 67-76
33. Ku H.-H., Brunk U.T., and Sohal R.S. Relationship between mitochondrial superoxide and hydrogen peroxide release and longevity of mammalian species. Free Rad. Biol. Med. 15 (1993) 621-627
34. + oxidation-reduction state. Biochem. J. 368 (2002) 545-553
35. Labinskyy N., Mukhopadhyay P., Toth J., Szalai G., Veres M., Losonczy G., Pinto J.T., Pacher P., Ballabh P., Podlutsky A., Austad S.N., Csiszar A., and Ungvari Z. Longevity is associated with increased vascular resistance to high glucose-induced oxidative stress and inflammatory gene expression in Peromyscus leucopus. Am. J. Physiol. Heart Circ. Physiol. 296 (2009) H946-H956
36. Lambert A.J., Boysen H.M., Buckingham J.A., Yang T., Podlutsky A., Austad S.N., Kunz T.H., Buffenstein R., and Brand M.D. Low rates of hydrogen peroxide release by isolated heart mitochondria associate with long maximum lifespan in vertebrate homeotherms. Ageing Cell 6 (2007) 607-618
37. Lane N. A unifying view of aging and disease: the double-agent theory. J. Theor. Biol. 225 (2003) 531-540
38. Lane N. Power, sex, suicide: mitochondria and the meaning of life (2005), Oxford University Press, New York pp. 306-311
39. Lasiewski R.C., and Dawson W.R. A re-examination of the relation between standard metabolic rate and body weight in birds. Condor 69 (1967) 12-23
40. Leary S.C., Lyons C.N., Rosenberger A.G., Ballantyne J.S., Stillman J., and Moyes C.D. Fibre-type differences in muscle mitochondrial profiles. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285 (2003) R817-R826
41. 13C NMR signal from glutamate and direct detection of tricarboxylic acid (TCA) cycle intermediates. Mag. Res. Med. 35 (1996) 149-154
42. Liu S. Generating, partitioning, targeting and functioning of superoxide in mitochondria. Biosci. Rep. 17 (1997) 259-272
43. Liu Y., Fiskum G., and Schubert D. Generation of reactive oxygen species by the mitochondria electron transport chain. J. Neurochem. 80 (2002) 780-787
44. 2, and basal and maximum aerobic capacity. Mech. Ageing Dev. 70 (1993) 177-199
45. Martin A.W., and Fuhrman F.A. The relationship between summated tissue respiration and metabolic rate in the mouse and dog. Physiol. Zool. 28 (1955) 18-34
46. McCord J.M., and Fridovich I. Superoxide dismutase. An enzymatic function for erythrocuprein (hemocuprein). J. Biol. Chem. 244 (1969) 6049-6055
47. Miller R.A., Harper J.M., Dysko R.C., Durkee S.J., and Austad S.N. Longer life spans and delayed maturation in wild-derived mice. Exp. Biol. Med. 227 (2002) 500-508
48. Miwa S., and Brand M.D. Mitochondrial matrix reactive oxygen species release is very sensitive to mild uncoupling. Biochem. Soc. Trans. 31 (2003) 1300-1301
49. Mori A., Utsumi K., Liu J., and Hosokawa M. Oxidative damage in the senescence-accelerated mouse. Ann. NY Acad. Sci. 854 (2006) 239-250
50. Nohl H., and Jordan W. The metabolic fate of mitochondrial hydrogen peroxide. Eur. J. Biochem. 111 (1980) 203-210
51. Pamploma R., Portero-Otin M., Requena J.R., Thorpe S.R., Herrero A., and Barja G. A low degree of fatty acid unsaturation leads to lower lipid peroxidation and lipoxidation-derived protein modification in heart mitochondria of the longevous pigeon than in the short-lived rat. Mech. Ageing Dev. 106 (1999) 283-296
52. Perez V.I., Van Remmen H., Bokov A., Epstein C.J., Vijg J., and Richardson A. The overexpression of major antioxidant enzymes does not extend the lifespan of mice. Aging Cell 8 (2009) 73-75
53. Perez-Campo R., Lopez-Torres M., Cadenas S., Roja C., and Barja G. The rate of free radical release as a determinant of the rate of aging: evidence from the comparative approach. J. Comp. Physiol. B 168 (1998) 149-158
54. 2 release in liver. Comp. Biochem. Physiol. B 140 (2005) 99-108
55. 2 solubility in aqueous media determined by a kinetic method. Anal. Biochem. 145 (1985) 406-418
56. Rottenberg H. Exceptional longevity in songbirds is associated with high rates of evolution of Cytochrome b, suggesting selection for reduced generation of free radicals. J. Exp. Biol. 210 (2007) 2170-2180
57. Rottenberg H. Coevolution of exceptional longevity, exceptionally high metabolic rates, and mitochondrial DNA-coded proteins in mammals. Exp. Gerontol. 42 (2007) 364-373
58. 2 release by macrophages and neutrophils with homovanillic acid and horse-radish peroxidase. J. Immunol. Meth. 63 (1983) 347-357
59. Sanz A., Pamploma R., and Barja G. Is the mitochondrial free radical theory of aging intact?. Antioxid. Redox Signal. 8 (2006) 582-599
60. 2 release by subsarcolemmal and intermyofibrilar mitochondria. Free Rad. Biol. Med. 35 (2003) 24-32
61. Speakman J.R. Oxidative phosphorylation, mitochondrial proton cycling, free-radical release and aging. Adv. Cell Aging Gerontol. 14 (2003) 35-68
62. Speakman J.R., Talbot D.A., Selman C., Snart S., McLaren J.S., Redman P., Krol E., Jackson D.M., Johnson M.S., and Brand M.D. Uncoupled and surviving: individual mice with high metabolism have greater mitochondria uncoupling and live longer. Aging Cell 3 (2004) 87-95
63. St. Pierre J., Buckingham J.A., Roebuck S.J., and Brand M.D. Topology of superoxide release from different sites in the mitochondrial electron transport chain. J. Biol. Chem. 277 (2002) 44784-44790
64. Stahl W.R. Organ weights in primates and other mammals. Science 150 (1965) 1039-1042
65. 2 release by membrane potential and NAD(P)H redox state. J. Neurochem. 86 (2003) 1101-1107
66. Suarez R.K., Brownsey R.W., Vogl W., Brown G.S., and Hochachka P.W. Biosynthetic capacity of hummingbird liver. Am. J. Physiol. Regul. Integr. Comp. Physiol. 255 (1988) R699-R702
67. Sutherland B.A., Shaw O.M., Clarkson A.N., Jackson D.M., Sammut I.A., and Appleton I. Neuroprotective effects of (-)-epigallocatechin gallate after hypoxia-ischemia-induced brain damage: novel mechanisms of action. FASEB J. 19 (2005) 258-260
68. Takaki M., Nakahara H., Kawatani Y., Utsumi K., and Suga H. No suppression of respiratory function of mitochondria isolated from the hearts of anesthetized rats with high-dose pentobarbital sodium. Jpn. J. Physiol. 47 (1997) 87-92
69. Trounce I.A., Kim Y.L., Jun A.S., and Wallace D.C. Assessment of mitochondrial oxidative phosphorylation in patient muscle biopsies, lymphoblasts, and transmitochondrial cell lines. Methods Enzymol. 264 (1996) 484-509
70. Turrens J.F. Superoxide release by the mitochondrial respiratory chain. Biosci. Rep. 17 (1997) 3-8
71. Ungvari Z., Buffenstein R., Austad S.N., Podlutsky A., Kaley G., and Csiszar A. Oxidative stress in vascular senescence: lessons from successfully aging species. Front. Biosci. 13 (2008) 5056-5070
72. 2 release by rat liver mitochondria. Mol. Cell. Endocrinol. 205 (2003) 185-192
73. 2 release by mitochondria from rat skeletal muscle. Arch. Biochem. Biophys. 372 (1999) 315-320
74. Wilkinson G.S., and South J.M. Life history, ecology and longevity in bats. Aging Cell 1 (2002) 124-131
75. Willis C.K.R., Lane J.E., Liknes E.T., Swanson D.L., and Brigham R.M. Thermal energetics of female big brown bats (Eptesicus fuscus). Can. J. Zool. 83 (2005) 871-879
76. Winter Y., and von Helversen O. The energy cost of flight: do small bats fly more cheaply than birds?. J. Comp. Physiol. B 168 (1998) 105-111
77. Young T.A., Cunningham C.C., and Bailey S.M. Reactive oxygen species release by the mitochondrial respiratory chain in isolated rat hepatocytes and liver mitochondria: studies using myxothiazol. Arch. Biochem. Biophys. 405 (2002) 65-72