Relationship between mitochondrial superoxide and hydrogen peroxide production and longevity of mammalian species

Ku, Hung Hai; Brunk, Ulf T.; Sohal, Rajindar S.

doi:10.1016/0891-5849(93)90165-q

Cited by 444 publications

(214 citation statements)

References 27 publications

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“…Control oligo is THF control (Table 2) Tables 1 and 4 FIC analysis in many instances. Nonetheless, this negative correlation is consistent with four related observations from multi-species comparisons: (1) cellular respiration rates (e.g., liver hepatocytes, Porter and Brand 1995) and the corresponding proportion of cell volume occupied by mitochondria (multiple cell types, Else and Hulbert 1985;Porter and Brand 1995) are greater in smaller species; (2) ROS production per mitochondrion (multiple tissues; Sohal et al 1989;Sohal et al 1990;Ku et al 1993;Barja 1998;Wright et al 2004;Lambert et al 2007) is generally greater in smaller, shorter-lived species (Fig. 5a); (3) steady-state levels of nuclear DNA oxidative damage are greater in some tissues of smaller species (see Fig.…”

Section: Discussionsupporting

confidence: 89%

Activities of DNA base excision repair enzymes in liver and brain correlate with body mass, but not lifespan

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Stuart

2011

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Accumulation of DNA lesions compromises replication and transcription and is thus toxic to cells. DNA repair deficiencies are generally associated with cellular replicative senescence and premature aging syndromes, suggesting that efficient DNA repair is required for normal longevity. It follows that the evolution of increasing lifespan amongst animal species should be associated with enhanced DNA repair capacities. Although UV damage repair has been shown to correlate positively with mammalian species lifespan, we lack similar insight into many other DNA repair pathways, including base excision repair (BER). DNA is continuously exposed to reactive oxygen species produced during aerobic metabolism, resulting in the occurrence of oxidative damage within DNA. Shortpatch BER plays an important role in repairing the resultant oxidative lesions. We therefore tested whether an enhancement of BER enzyme activities has occurred concomitantly with the evolution of increased maximum lifespan (MLSP). We collected brain and liver tissue from 15 vertebrate endotherm species ranging in MLSP over an order of magnitude. We measured apurinic/ apyrimidinic (AP) endonuclease activity, as well as the rates of nucleotide incorporation into an oligonucleotide containing a single nucleotide gap (catalyzed by BER polymerase β) and subsequent ligation of the oligonucleotide. None of these activities correlated positively with species MLSP. Rather, nucleotide incorporation and oligonucleotide ligation activities appeared to be primarily (and negatively) correlated with species body mass.

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Section: Discussionsupporting

confidence: 89%

Activities of DNA base excision repair enzymes in liver and brain correlate with body mass, but not lifespan

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Stuart

2011

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“…Previous studies have suggested that the relationship between energy expenditure and lifespan is a consequence of the association of high mass-specific levels of DEE and RMR with high production of mitochondrial reactive oxygen species (ROS). Consistent with this idea, an inverse relationship between ROS production in various tissues and life span has been found in several species (Sohal et al 1989(Sohal et al , 1990Ku et al 1993;Barja et al 1994). In our analysis, however, DEE and RMR were not significantly related to MLSP in birds after the effects of body mass and phylogeny were accounted for.…”

Section: Discussionsupporting

confidence: 56%

Energetics and longevity in birds

Furness

Speakman

2008

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The links between energy expenditure and ageing are different at different levels of enquiry. When studies have examined the relationships between different species within a given class the association is generally negative-animals with greater metabolism per gram of tissue live shorter lives. Within species, or between classes (e.g. between birds and mammals) the association is the opposite-animals with higher metabolic rates live longer. We have previously shown in mammals that the negative association between lifespan and metabolic rate is in fact an artefact of using resting rather than daily energy expenditure, and of failing to adequately take into account the confounding effects of body size and the lack of phylogenetic independence of species data. When these factors are accounted for, across species of mammals, the ones with higher metabolism also have the largest lifetime expenditures of energy-consistent with the inter-class and intra-specific data. A previous analysis in birds did not yield the same pattern, but this may have been due to a lack of sufficient power in the analysis. Here we present an analysis of a much enlarged data set (>300 species) for metabolic and longevity traits in birds. These data show very similar patterns to those in mammals. Larger individuals have longer lives and lower per-gram resting and daily energy expenditures, hence there is a strong negative relationship between longevity and mass-specific metabolism. This relationship disappears when the confounding effects of body mass and phylogeny are accounted for. Across species of birds, lifetime expenditure of energy per gram of tissue based on both daily and resting energy expenditure is positively related to metabolic intensity, mirroring these statistical relationships in mammals and synergising with the positive associations of metabolism with lifespan within species and between vertebrate classes.

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“…To validate the use of LSP as a surrogate for mitochondrial RONS production [16][17][18] , we plotted published rates of RONS formation in 11 species and 4 postmitotic tissues (kidney, heart, brain and liver) [22][23][24][25][26] to show that a strong (r 2 = 0.71 ± 0.15) inverse relationship exists with LSP, with a mean allometric exponent of -0.84 ± 0.34 (Fig. 2).…”

Section: Measuring Rates Of Degenerationmentioning

confidence: 99%

Lifespan and mitochondrial control of neurodegeneration

et al. 2004

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We examine the allometric (comparative scaling) relationships between rates of neurodegeneration resulting from equivalent mutations in a diverse group of genes from five mammalian species with different maximum lifespan potentials. In both retina and brain, rates of neurodegeneration vary by as much as two orders of magnitude and are strongly correlated with maximum lifespan potential and rates of formation of mitochondrial reactive oxygen and nitrogen species (RONS). Cell death in these disorders is directly or indirectly regulated by the intrinsic mitochondrial cell death pathway. Mitochondria are the main source of RONS production and integrate cellular stress signals to coordinate the intrinsic pathway. We propose that these two functions are intimately related and that steadystate RONS-mediated signaling or damage to the mitochondrial stress-integration machinery is the principal factor setting the probability of cell death in response to a diverse range of cellular stressors. This provides a new and unifying framework for investigating neurodegenerative disorders.Cell death in inherited neurodegenerative disorders most commonly occurs by apoptosis 1-4 . The evidence is often indirect and inferred on the basis of characteristic morphological changes, such as chromatin compaction and cell shrinkage, or evidence of caspase activation, but in many cases it is more reliably based on multiple lines of evidence [1][2][3][4] . Caspase-independent cell death also occurs, although the precise mechanisms are less well understood and evidence that this occurs in inherited neurodegenerations is sparse. In these disorders, cell death occurs with a probability that is constant through part or all of the adult lifespan, consistent with a steady-state (one-hit or exponential kinetics) rather than a cumulative damage model 5,6 . The retina is a particularly well understood model of neurodegeneration. Mutations in more than 100 genes are known to cause neurodegeneration of retinal photoreceptors (RetNet; see URL below); these affect virtually all areas of metabolism and all parts of the cell 7-9 .Two main pathways lead to the activation of cysteine proteases or caspases that execute the apoptotic death program [10][11][12] . The extrinsic pathway involves cell-surface signaling complexes (e.g., Fas or FasL), which trigger the cell death cascade by activating caspase 8 and downstream caspases. The intrinsic, or mitochondrial, pathway controls activation of caspase 9, through the adaptor molecule Apaf-1, by regulating release of cytochrome c from mitochondria. Proapoptotic and antiapoptotic members of the Bcl-2 family and various stress and survival signals regulate the release of cytochrome c. Proapoptotic signals can also release proteins such as Smac and Omi, which antagonize IAP (inhibitor of apoptosis) proteins to activate cell death caspases, from the mitochondrial intermembrane space.Evidence from animal models of human photoreceptor degeneration suggests that the mitochondrial, rather than the extrinsic, cell death pa...

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Relationship between mitochondrial superoxide and hydrogen peroxide production and longevity of mammalian species

Cited by 444 publications

References 27 publications

Activities of DNA base excision repair enzymes in liver and brain correlate with body mass, but not lifespan

Activities of DNA base excision repair enzymes in liver and brain correlate with body mass, but not lifespan

Energetics and longevity in birds

Lifespan and mitochondrial control of neurodegeneration

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