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Antioxidant enzyme activities are not broadly correlated with longevity in 14 vertebrate endotherm species

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Abstract

The free radical theory of ageing posits that accrual of oxidative damage underlies the increased cellular, tissue and organ dysfunction and failure associated with advanced age. In support of this theory, cellular resistance to oxidative stress is highly correlated with life span, suggesting that prevention or repair of oxidative damage might indeed be essential for longevity. To test the hypothesis that the prevention of oxidative damage underlies longevity, we measured the activities of the five major intracellular antioxidant enzymes in brain, heart and liver tissue of 14 mammalian and avian species with maximum life spans (MLSPs) ranging from 3 years to over 100 years. Our data set included Snell dwarf mice in which life span is increased by ∼50% compared to their normal littermates. We found that CuZn superoxide dismutase, the major cytosolic superoxide dismutase, showed no correlation with MLSP in any of the three organs. Similarly, neither glutathione peroxidase nor glutathione reductase activities correlated with MLSP. MnSOD, the sole mitochondrial superoxide dismutase in mammals and birds, was positively correlated with MLSP only for brain tissue. This same trend was observed for catalase. For all correlational data, effects of body mass and phylogenetic relatedness were removed using residual analysis and Felsenstein’s phylogenetically independent contrasts. Our results are not consistent with a causal role for intracellular antioxidant enzymes in longevity, similar to recent reports from studies utilising genetic modifications of mice (Pérez et al., Biochim Biophys Acta 1790:1005–1014, 2009). However, our results indicate a specific augmentation of reactive oxygen species neutralising activities in brain associated with longevity.

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Acknowledgements

MMP was supported by an Ontario Graduate Scholarship. Work at Brock University was supported by the Natural Sciences and Engineering Research Council (NSERC), the Canada Foundation for Innovation (CFI) and an Early Researcher Award from the Ontario Ministry of Research and Innovation (OMRI) to JAS. The bat colony at McMaster University is supported by NSERC, CFI and OMRI grants to PAF. The bird colonies at Trent University have been supported by NSERC.

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Authors and Affiliations

  1. Department of Biological Sciences, Brock University, 500 Glenridge Ave., St. Catharines, ON, Canada, L2S 3A1

    Melissa M. Page, Brent E. Wiens, Esther Tiedtke, Craig W. Peters & Jeffrey A. Stuart

  2. Department of Biology, University of Victoria, P.O. Box 3020 STN CSC, Victoria, BC, Canada, V8W 3N5

    Jean Richardson

  3. Department of Psychology, Neuroscience & Behaviour, McMaster University, 1280 Main St. W, Hamilton, ON, Canada, L8S 4K1

    Paul A. Faure

  4. Department of Biology, Trent University, Peterborough, ON, Canada, K9J 7B8

    Gary Burness

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  1. Melissa M. Page
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Correspondence to Jeffrey A. Stuart.

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Fig. S1

Correlations between MnSOD activity and species MLSP. a Residual analysis of liver MnSOD activity with the inclusion of the human data point (t value significant at the 0.025 level). b FIC analysis of liver MnSOD with the inclusion of the human data point. c Residual analysis of liver MnSOD activity following the removal of the human data point. d FIC analysis of liver MnSOD activity following the removal of the human data point. All values are natural log-transformed and each data point consists of measurements from three to eight individuals of each species (PPT 122 kb)

Fig. S2

Activity of brain and heart CAT. a Brain CAT activity is not significantly correlated with species body mass. b FIC analysis of heart CAT activity and species MLSP. All values are natural log-transformed and each data point consists of measurements from three to eight individuals of each species (PPT 94 kb)

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Page, M.M., Richardson, J., Wiens, B.E. et al. Antioxidant enzyme activities are not broadly correlated with longevity in 14 vertebrate endotherm species. AGE 32, 255–270 (2010). https://doi.org/10.1007/s11357-010-9131-2

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