Journal of Comparative Physiology B

, Volume 160, Issue 6, pp 655–661 | Cite as

Effect of natural ageing and antioxidant inhibition on liver antioxidant enzymes, glutathione system, peroxidation, and oxygen consumption inRana perezi

  • M. López-Torres
  • R. Pérez-Campo
  • G. Barja de Quiroga
Article
Accepted:

Summary

A study of the physiological role of oxygen free radicals in relation to the ageing process was performed using the liver ofRana perezi, an animal with a moderate rate of oxygen consumption and a life span substantially longer than that of laboratory rodents.

Among the five different antioxidant enzymes only superoxide dismutase (SOD) showed an age-dependent decrease. Cytochrome oxidase (COX), glutathione status, in vivo and in vitro liver peroxidation, and metabolic rate did not vary as a function of age.

Long-term (2.5 months) treatment with aminotriazole and diethyldithiocarbamate depleted catalase (CAT) activity and did not change both glutathione peroxidases (GPx), COX, reduced (GSH) and oxidized (GSSG) glutathione, or metabolic rate. This treatment resulted in great compensatory increases in SOD (to 250–460% of controls) and glutathione reductase (GR) (to 200%) which are possibly responsible for the lack of increase of in vivo and in vitro liver peroxidation and for the absence of changes in survival rate.

The comparison of these results with previous data from other species suggests the possibility that decreases in antioxidant capacity in old age are restricted to animal species with high metabolic rates. Nevertheless, ageing can still be due to the continuous presence of small concentrations of O2 radicals in the tissues throughout life in animals with either high or low metabolic rates, because radical scavenging can not be 100% effective. Compensatory homeostasis among antioxidants seems to be a general phenomenon in different species.

Key words

Ageing Radicals Peroxidation Superoxide dismutase Glutathione peroxidase 

Abbreviations

AT

3-amino-1,2,4 triazole

CAT

catalase

COX

cytochrome c oxidase

DDC

diethyldithiocarbamate

GPx

glutathione peroxidase

GR

glutathione reductase

GSH

reduced glutathione

GSSG

oxidized glutathione

MDA

malondialdehyde

SOD

superoxide dismutase

TBA-RS

thiobarbituric acid-reacting substances

VO2

oxygen consumption

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References

  1. Allen RG, Farmer KJ, Sohal RS (1983) Effect of catalase inactivation on levels of inorganic peroxides, superoxide dismutase, glutathione, oxygen consumption and life span in adult houseflies (Musca domestica). Biochem J 216:503–506Google Scholar
  2. Baird MB, Samis HV (1971) Regulation of catalase activity in mice of different ages. Gerontologia (Basel) 17:105–115Google Scholar
  3. Barja de Quiroga G, Gil P, López-Torres M (1988) Physiological significance of catalase and glutathione peroxidases, and in vivo peroxidation, in selected tissues of the toadDiscoglossus pictus (Amphibia) during acclimation to normobaric hyperoxia. J Comp Physiol B 158:583–590Google Scholar
  4. Cand F, Verdetti J (1989) Superoxide dismutase, glutathione peroxidase, catalase, and lipid peroxidation in the major organs of the aging rats. Free Rad Biol Med 7:59–63Google Scholar
  5. Carrillo MC, Kitani K, Kanai S, Sato Y, Nokubo M, Ohta M, Otsubo K (1989) Differences in the influence of diet on the hepatic glutathione S-transferase activity and glutathione content between young and old C57 black female mice. Mech Ageing Dev 47:1–15Google Scholar
  6. Chance B, Sies H, Boveris A (1979) Hydroperoxide metabolism in mammalian organs. Physiol Rev 59:527–605Google Scholar
  7. Chatterjee SN, Agarwal S (1988) Liposomes as membrane model for study of lipid peroxidation. Free Rad Biol Med 4:51–72Google Scholar
  8. Cutler RG (1984) Antioxidants aging and longevity. In: Pryor WA (ed) Free radicals in biology. vol. VI, Chap. 11. Academic Press, New York, pp 371–428Google Scholar
  9. Devasagayam TPA (1986) Senescence-associated decrease of NADPH-induced lipid peroxidation in rat liver microsomes. FEBS Letters 205:246–250Google Scholar
  10. Devasagayam TPA, Pushpendran CK (1986) Changes in ascorbate-induced lipid peroxidation of hepatic rough and smooth microsomes during postnatal development and ageing of rats. Mech Ageing Dev 34:13–21Google Scholar
  11. Farmer KJ, Sohal RS (1989) Relationship between superoxide anion radical generation and aging in the housefly,Musca domestica. Free Rad Biol Med 7:23–29Google Scholar
  12. Gee DL, Tappel AL (1981) Production of volatile hydrocarbons by isolated hepatocytes: an in vitro model for lipid peroxidation studies. Toxicol Appl Pharmacol 60:112–120Google Scholar
  13. Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207–212Google Scholar
  14. Gutteridge JMC (1982) Free-radical damage to lipids, aminoacids, carbohydrates, and nucleic acids determined by thiobarbituric acid reactivity. Int J Biochem 14:649–653Google Scholar
  15. Hazelton A, Lang CA (1980) Glutathione contents of tissues in the aging mouse. Biochem J 188:25–30Google Scholar
  16. Hazelton GA, Lang CA (1985) Glutathione peroxidase and reductase activities in the aging mouse. Mech Ageing Dev 29:71–81Google Scholar
  17. Kappus H (1985) Lipid peroxidation: mechanisms, analysis, enzymology, and biological relevance. In: Sies H (ed) Oxidative stress. Academic Press, London, pp 273–310Google Scholar
  18. Kellogg EW III, Fridovich I (1976) Superoxide dismutase in the rat and mouse as a function of age and longevity. J Gerontol 31:405–408Google Scholar
  19. Koizumi A, Weindruch R, Walford RL (1987) Influences of dietary restriction and age on liver enzyme activities and lipid peroxidation in mice. J Nutr 117:361–367Google Scholar
  20. Lammi-Keefe CJ, Swan PB, Hegarty PVJ (1984) Copper-zinc and manganese superoxide dismutase activities in cardiac and skeletal muscles during aging in male rats. Gerontology 30:153–158Google Scholar
  21. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275Google Scholar
  22. Massey V, Williams CH (1965) On the reaction mechanism of yeast glutathione reductase. J Biol Chem 240:4470–4481Google Scholar
  23. Müller D, Kretzschmar M, Marin E, Hübscher J (1989) Influence of training and acute physical exercise on glutathione and lipid peroxides in plasma. Proceedings of the IUBS-XVII. XXXI International Congress of Physiological Sciences. Symposium S3086, Helsinki, Finland, pp 244Google Scholar
  24. Paoletti F, Aldinucci D, Mocali A, Caparrini A (1986) A sensitive spectrophotometric method for the determination of superoxide dismutase activity in tissue extracts. Anal Biochem 154:536–541Google Scholar
  25. Player TJ, Mills DJ, Horton AA (1977) Age-dependent changes in rat liver microsomal and mitochondrial NADPH-dependent lipid peroxidation. Biochem Biophys Res Com 78:1397–1402Google Scholar
  26. Pompella A, Maellaro E, Casini AF, Ferrali M, Ciccoli L, Comporti M (1987) Measurement of lipid peroxidation in vivo: a comparison of different procedures. Lipids 22:206–211Google Scholar
  27. Reiss U, Gershon D (1976) Comparison of cytoplasmic superoxide dismutase in liver, heart, and brain of aging rats and mice. Biochem Biophys Res Com 73:255–262Google Scholar
  28. Richie JP, Lang CA (1988) A decrease in cysteine levels causes the glutathione deficiency of aging in the mosquito. Proc Soc Exp Biol and Med 187:235–240Google Scholar
  29. Rikans LE, Moore R (1988) Effect of aging on aqueous phase antioxidants in tissues of male Fisher rats. Biochim Biophys Acta 966:269–275Google Scholar
  30. Ross MH (1969) Aging, nutrition and hepatic enzyme activity pattern in the rat. J Nutr 97:563–602Google Scholar
  31. Sawada M, Carlson JC (1987) Changes in superoxide radical and lipid peroxide formation in the brain, heart and liver during the lifetime of the rat. Mech Ageing Dev 41:125–137Google Scholar
  32. Smith L (1955) Spectrophotometric assay of cytochrome c oxidase. In: Gick D (ed) Methods of biochemical analysis. vol. 2, Wiley-Interscience, New York, pp 427–434Google Scholar
  33. Sohal RS, Farmer KJ, Allen RG, Cohen NR (1983) Effect of age on oxygen consumption, superoxide dismutase, catalase, glutathione, inorganic peroxides and chloroform-soluble antioxidants in the adult male housefly,Musca domestica. Mech Ageing Dev 24:185–195Google Scholar
  34. Sohal RS, Farmer KJ, Allen RG, Ragland SS (1984) Effects of diethyldithiocarbamate on lifespan, metabolic rate, superoxide dismutase, catalase, inorganic peroxides and glutathione in the adult male housefly,Musca domestica. Mech Ageing Dev 24:175–183Google Scholar
  35. Sohal RS, Müller A, Koletzko B, Sies H (1985) Effect of age and ambient temperature on n-pentane production in adult housefly,Musca domestica. Mech Ageing Dev 29:317–326Google Scholar
  36. Sohal RS, Allen RG (1986) Relationship between oxygen metabolism aging and development. Adv in Free Rad Biol Med 2:117–160Google Scholar
  37. Sohal RS (1988) Effect of hydrogen peroxide administration on life span, superoxide dismutase, catalase, and glutathione in the adult housefly,Musca domestica. Exp Gerontol 23:211–216Google Scholar
  38. Sohal RS, Svensson I, Sohal BH, Brunk UT (1989) Superoxide anion radical production in different animal species. Mech Ageing Dev 49:129–135Google Scholar
  39. Starke PE, Farber JL (1985) Endogenous defenses against the cytotoxicity of hydrogen peroxide in cultured rat hepatocytes. J Biol Chem 260:86–92Google Scholar
  40. Stohs SJ, Lawson T (1986) The role of glutathione and its metabolism in aging. In: Kitani K (ed) Liver and brain. Elsevier, Amsterdam, pp 59–70Google Scholar
  41. Sunderman FW, Zaharia O, Reid MC, Bellibeau JF, O'leary GP Griffin H (1984) Effects of diethyldithiocarbamate and nickel chloride on glutathione and trace metal concentrations in rat liver. Toxicology 32:11–21Google Scholar
  42. Thayer WS (1986) Role of catalase in metabolism of hydrogen peroxide by the perfused rat heart. FEBS Letters 202:137–140Google Scholar
  43. Tietze F (1969) Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal Biochem 27:502–522Google Scholar

Copyright information

© Springer-Verlag 1991

Authors and Affiliations

  • M. López-Torres
    • 1
  • R. Pérez-Campo
    • 1
  • G. Barja de Quiroga
    • 1
  1. 1.Department of Animal Biology-II, Animal Physiology, Faculty of BiologyComplutense UniversityMadridSpain

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