Home LiteratureArticle Details
PMID: 11710804 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Effect of short-term caloric restriction on H2O2 production and oxidative DNA damage in rat liver mitochondria and location of the free radical source.

Journal of bioenergetics and biomembranes ·Vol. 33 ·No. 4 ·2001-08-00 ·Pages 279-87

Gredilla R, Barja G, López-Torres M

Abstract

Oxygen free radicals (ROS) of mitochondrial origin seem to be involved in aging. Whereas in other tissues complexes I or III of the respiratory chain contain the ROS generators, in this study we find that rat liver mitochondria generate oxygen radicals at complexes I, II, and III. Short-term (6 weeks) caloric restriction significantly decreased H2O2 production in rat liver mitochondria. This decrease in ROS production was located at complex I because it occurred with complex I-linked substrates (pyruvate/malate), but did not reach statistical significance with the complex II-linked substrate succinate. The mechanism responsible for the lowered ROS production was not a decrease in oxygen consumption. Instead, the mitochondria of caloric-restricted animals released less ROS per unit electron flow. This was due to a decrease in the degree of reduction of the complex I generator. Furthermore, oxidative damage to mitochondrial and nuclear DNA was also decreased in the liver by short-term caloric restriction. The results agree with the idea that caloric restriction delays aging, at least in part, by decreasing the rate of mitochondrial ROS generation and thus the rate of attack to molecules, like DNA, highly relevant for the accumulation of age-dependent changes.

MeSH Terms
Animals DNA Damage/physiology Diet Electron Transport Complex I Hydrogen Peroxide/metabolism Male Mitochondria, Liver/metabolism NADH, NADPH Oxidoreductases/metabolism Oxidants/metabolism Oxidation-Reduction Rats Rats, Wistar Reactive Oxygen Species/metabolism Time Factors
Chemicals
Oxidants Reactive Oxygen Species Hydrogen Peroxide NADH, NADPH Oxidoreductases Electron Transport Complex I
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Gredilla R
Department of Animal Biology II (Animal Physiology), Faculty of Biology, Complutense University, Madrid, Spain.
Barja G
López-Torres M
References (35)
35 references, click to expand
  1. Generation of superoxide anion by succinate-cytochrome c reductase from bovine heart mitochondria.
    J Biol Chem. 1998 Dec 18;273(51):33972-6 PMID: 9852050
  2. 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.
    J Bioenerg Biomembr. 1998 Jun;30(3):235-43 PMID: 9733090
  3. Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria.
    Biochem J. 1980 Nov 1;191(2):421-7 PMID: 6263247
  4. Aging: a theory based on free radical and radiation chemistry.
    J Gerontol. 1956 Jul;11(3):298-300 PMID: 13332224
  5. Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria.
    Arch Biochem Biophys. 1985 Mar;237(2):408-14 PMID: 2983613
  6. Dependence of H2O2 formation by rat heart mitochondria on substrate availability and donor age.
    J Bioenerg Biomembr. 1997 Feb;29(1):89-95 PMID: 9067806
  7. Effect of age and caloric restriction on DNA oxidative damage in different tissues of C57BL/6 mice.
    Mech Ageing Dev. 1994 Oct 20;76(2-3):215-24 PMID: 7885066
  8. Mitochondrial oxygen radical generation and leak: sites of production in states 4 and 3, organ specificity, and relation to aging and longevity.
    J Bioenerg Biomembr. 1999 Aug;31(4):347-66 PMID: 10665525
  9. Sites and mechanisms responsible for the low rate of free radical production of heart mitochondria in the long-lived pigeon.
    Mech Ageing Dev. 1997 Nov;98(2):95-111 PMID: 9379714
  10. Does food restriction retard aging by reducing the metabolic rate?
    Am J Physiol. 1985 Apr;248(4 Pt 1):E488-90 PMID: 3157325
  11. Relationship between mitochondrial superoxide and hydrogen peroxide production and longevity of mammalian species.
    Free Radic Biol Med. 1993 Dec;15(6):621-7 PMID: 8138188
  12. Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammals.
    FASEB J. 2000 Feb;14(2):312-8 PMID: 10657987
  13. Retarding effect of dietary restriction on the accumulation of 8-hydroxy-2'-deoxyguanosine in organs of Fischer 344 rats during aging.
    Free Radic Biol Med. 1997;23(1):76-81 PMID: 9165299
  14. ADP-regulation of mitochondrial free radical production is different with complex I- or complex II-linked substrates: implications for the exercise paradox and brain hypermetabolism.
    J Bioenerg Biomembr. 1997 Jun;29(3):241-9 PMID: 9298709
  15. H2O2 production 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. 1998 Jun 15;103(2):133-46 PMID: 9701767
  16. Mitochondrial free radical production and aging in mammals and birds.
    Ann N Y Acad Sci. 1998 Nov 20;854:224-38 PMID: 9928433
  17. Oxidative DNA damage levels in rats fed low-fat, high-fat, or calorie-restricted diets.
    Toxicol Appl Pharmacol. 1992 Aug;115(2):156-60 PMID: 1641849
  18. 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 Oct;21(5):317-27 PMID: 7842141
  19. Protection of DNA damage by dietary restriction.
    Free Radic Biol Med. 1992;12(6):523-5 PMID: 1601327
  20. NADH- and NADPH-dependent formation of superoxide anions by bovine heart submitochondrial particles and NADH-ubiquinone reductase preparation.
    Biochem J. 1979 Apr 15;180(1):129-35 PMID: 39543
  21. Metabolic mass, metabolic rate, caloric restriction, and aging in male Fischer 344 rats.
    Mech Ageing Dev. 2000 Jan 24;113(1):37-48 PMID: 10708248
  22. Assay of H2O2 production by macrophages and neutrophils with homovanillic acid and horse-radish peroxidase.
    J Immunol Methods. 1983 Oct 28;63(3):347-57 PMID: 6631014
  23. Oxidative damage, mitochondrial oxidant generation and antioxidant defenses during aging and in response to food restriction in the mouse.
    Mech Ageing Dev. 1994 May;74(1-2):121-33 PMID: 7934203
  24. Mitochondrial glutathione oxidation correlates with age-associated oxidative damage to mitochondrial DNA.
    FASEB J. 1996 Feb;10(2):333-8 PMID: 8641567
  25. The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen.
    Biochem J. 1973 Jul;134(3):707-16 PMID: 4749271
  26. Caloric intake and aging: mechanisms in rodents and a study in nonhuman primates.
    Toxicol Sci. 1999 Dec;52(2 Suppl):35-40 PMID: 10630588
  27. Hydrogen peroxide production by liver mitochondria in different species.
    Mech Ageing Dev. 1990 Apr 30;53(3):209-15 PMID: 2115947
  28. Age-related mitochondrial DNA deletions: effect of dietary restriction.
    Free Radic Biol Med. 1998 Jan 1;24(1):148-54 PMID: 9436624
  29. Conditions allowing redox-cycling ubisemiquinone in mitochondria to establish a direct redox couple with molecular oxygen.
    Free Radic Biol Med. 1996;20(2):207-13 PMID: 8746441
  30. Oxidative stress, caloric restriction, and aging.
    Science. 1996 Jul 5;273(5271):59-63 PMID: 8658196
  31. The free radical theory of aging matures.
    Physiol Rev. 1998 Apr;78(2):547-81 PMID: 9562038
  32. Detection and quantification of oxidative adducts of mitochondrial DNA.
    Methods Enzymol. 1996;264:442-53 PMID: 8965717
  33. Evolution of mitochondrial DNA in Drosophila subobscura.
    Proc Natl Acad Sci U S A. 1986 Nov;83(22):8649-53 PMID: 16578796
  34. Markers of oxidative damage to DNA: antioxidants and molecular damage.
    Methods Enzymol. 1999;300:166-84 PMID: 9919520
  35. Role of ubiquinone in the mitochondrial generation of hydrogen peroxide.
    Biochem J. 1976 May 15;156(2):435-44 PMID: 182149
Article Info
Journal
Journal of bioenergetics and biomembranes
Abbr.
J Bioenerg Biomembr
ISSN
0145-479X
Published
2001-08-00
Pages
279-87
Language
English
Region
United States
NLM ID
7701859
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com