Localization at Complex I and Mechanism of the Higher Free Radical Production of Brain Nonsynaptic Mitochondria in the Short-lived Rat Than in the Longevous Pigeon

Overview

Journal J Bioenerg Biomembr

Publisher Springer

Specialties Biochemistry
Biology
Endocrinology

Date 1998 Sep 11

PMID 9733090

Citations 56

Authors

G Barja

A Herrero

Affiliations

Soon will be listed here.

Abstract

Free radical production and leak of brain nonsynaptic mitochondria were higher with pyruvate/malate than with succinate in rats and pigeons. Rotenone, antimycin A, and myxothiazol maximally stimulated free radical production with pyruvate/malate but not with succinate. Simultaneous treatment with myxothiazol plus antimycin A did not decrease the stimulated rate of free radical production brought about independently by any of these two inhibitors with pyruvate/malate. Thenoyltrifluoroacetone did not increase free radical production with succinate. No free radical production was detected at Complex IV. Free radical production and leak with pyruvate/malate were higher in the rat (maximum longevity 4 years) than in the pigeon (maximum longevity 35 years). These differences between species disappeared in the presence of rotenone. The results localize the main free radical production site of nonsynaptic brain mitochondria at Complex I. They also suggest that the low free radical production of pigeon brain mitochondria is due to a low degree of reduction of Complex I in the steady state in this highly longevous species.

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References

Nohl H . Generation of superoxide radicals as byproduct of cellular respiration. Ann Biol Clin (Paris). 1994; 52(3):199-204. View

Turrens J, Boveris A . Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem J. 1980; 191(2):421-7. PMC: 1162232. DOI: 10.1042/bj1910421. View

Hansford R, Hogue B, Mildaziene V . Dependence of H2O2 formation by rat heart mitochondria on substrate availability and donor age. J Bioenerg Biomembr. 1997; 29(1):89-95. DOI: 10.1023/a:1022420007908. View

Cino M, Del Maestro R . Generation of hydrogen peroxide by brain mitochondria: the effect of reoxygenation following postdecapitative ischemia. Arch Biochem Biophys. 1989; 269(2):623-38. DOI: 10.1016/0003-9861(89)90148-3. View

Herrero A, Barja G . Sites and mechanisms responsible for the low rate of free radical production of heart mitochondria in the long-lived pigeon. Mech Ageing Dev. 1997; 98(2):95-111. DOI: 10.1016/s0047-6374(97)00076-6. View

Ku H, Brunk U, Sohal R . Relationship between mitochondrial superoxide and hydrogen peroxide production and longevity of mammalian species. Free Radic Biol Med. 1993; 15(6):621-7. DOI: 10.1016/0891-5849(93)90165-q. View

Sohal R, Svensson I, Sohal B, Brunk U . Superoxide anion radical production in different animal species. Mech Ageing Dev. 1989; 49(2):129-35. DOI: 10.1016/0047-6374(89)90096-1. View

Sorgato M, SARTORELLI L, Loschen G, Azzi A . Oxygen radicals and hydrogen peroxide in rat brain mitochondria. FEBS Lett. 1974; 45(1):92-5. DOI: 10.1016/0014-5793(74)80818-5. View

Nohl H, Jordan W . The mitochondrial site of superoxide formation. Biochem Biophys Res Commun. 1986; 138(2):533-9. DOI: 10.1016/s0006-291x(86)80529-0. View

10.

Barja G, Cadenas S, Rojas C, Lopez-Torres M . Low mitochondrial free radical production per unit O2 consumption can explain the simultaneous presence of high longevity and high aerobic metabolic rate in birds. Free Radic Res. 1994; 21(5):317-27. DOI: 10.3109/10715769409056584. View

11.

Takeshige K, MINAKAMI S . NADH- and NADPH-dependent formation of superoxide anions by bovine heart submitochondrial particles and NADH-ubiquinone reductase preparation. Biochem J. 1979; 180(1):129-35. PMC: 1161027. DOI: 10.1042/bj1800129. View

12.

Lass A, Agarwal S, Sohal R . Mitochondrial ubiquinone homologues, superoxide radical generation, and longevity in different mammalian species. J Biol Chem. 1997; 272(31):19199-204. PMC: 2839905. DOI: 10.1074/jbc.272.31.19199. View

13.

de la Asuncion J, Millan A, Pla R, Bruseghini L, Esteras A, Pallardo F . Mitochondrial glutathione oxidation correlates with age-associated oxidative damage to mitochondrial DNA. FASEB J. 1996; 10(2):333-8. DOI: 10.1096/fasebj.10.2.8641567. View

14.

Reynolds I, Hastings T . Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation. J Neurosci. 1995; 15(5 Pt 1):3318-27. PMC: 6578215. View

15.

Sohal R, Svensson I, Brunk U . Hydrogen peroxide production by liver mitochondria in different species. Mech Ageing Dev. 1990; 53(3):209-15. DOI: 10.1016/0047-6374(90)90039-i. View

16.

Ozawa T . Mitochondrial DNA mutations associated with aging and degenerative diseases. Exp Gerontol. 1995; 30(3-4):269-90. DOI: 10.1016/0531-5565(94)00057-a. View

17.

Calder 3rd W . The comparative biology of longevity and lifetime energetics. Exp Gerontol. 1985; 20(3-4):161-70. DOI: 10.1016/0531-5565(85)90033-6. View

18.

HATEFI Y . Ubiquinol-cytochrome c oxidoreductase. The redox reactions of the bis-heme cytochrome b in ubiquinone-sufficient and ubiquinone-deficient systems. J Biol Chem. 1996; 271(11):6164-71. DOI: 10.1074/jbc.271.11.6164. View

19.

Schapira A . Evidence for mitochondrial dysfunction in Parkinson's disease--a critical appraisal. Mov Disord. 1994; 9(2):125-38. DOI: 10.1002/mds.870090202. View

20.

Cadenas E, Boveris A . Enhancement of hydrogen peroxide formation by protophores and ionophores in antimycin-supplemented mitochondria. Biochem J. 1980; 188(1):31-7. PMC: 1162533. DOI: 10.1042/bj1880031. View