Low fatty acid unsaturation protects against lipid peroxidation in liver mitochondria from long-lived species: the pigeon and human case

Pamplona, Reinald; Prat, J.; Cadenas, Susana; Rojas, C.; Pérez‐Campo, R.; Torres, M.; Barja, Gustavo

doi:10.1016/0047-6374(95)01673-2

Cited by 130 publications

(110 citation statements)

References 28 publications

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“…Variations in the steadystate levels of oxidatively modified proteins in vivo can be due to differences in rates of oxidant generation, antioxidative defenses, protein repair and degradative capacity, or susceptibility of proteins to oxidative modifications, and all these are tissue-or species-dependent. Thus, while in the present study it was clearly observed that brain of bugerigar parakeets and canaries has a lower degree of protein oxidation (specific protein carbonyls GSA and AASA) than that of mice, protein carbonyl contents are similar in pigeon and rat liver mitochondria (Pamplona et al 1996) and even higher in the skeletal muscle of pigeons compared to rats (Portero-Otin et al 2004). Further investigation is needed to establish the relationship between protein oxidation and longevity in mammals and birds.…”

Section: Discussionmentioning

confidence: 43%

“…Unsaturated fatty acids (UFAs) are extremely sensitive to oxidation, their sensitivity to oxidation exponentially increasing as a function of the number of double bonds per fatty acid molecule (Bielski et al 1983). We have found that the degree of unsaturation of membrane fatty acids is systematically lower in longlived than in short-lived species, both when comparing mammals (rats or mice) with birds (pigeons, parakeets or canaries) as well as when comparing mammals of different longevities (see Pamplona et al 2002;Pamplona and Barja 2003;, for a review). This has held true in a variety of investigations performed on liver mitochondrial phospholipids, total heart, liver and skeletal muscle phospholipids, heart mitochondria, and skeletal muscle.…”

Section: Discussionmentioning

confidence: 99%

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Protein and lipid oxidative damage and complex I content are lower in the brain of budgerigar and canaries than in mice. Relation to aging rate

Pamplona

Portero‐Otín

Sanz

et al. 2005

AGE

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What are the mechanisms determining the rate of animal aging? Of the two major classes of endothermic animals, bird species are strikingly long-lived compared to mammals of similar body size and metabolic rate. Thus, they are ideal models to identify longevity-related characteristics not linked to body size or low metabolic rates. Since oxidative stress seems to be related to the basic aging process, we measured specific markers of different kinds of oxidative damage to proteins, like glutamic and aminoadipic semialdehydes (GSA and AASA, specific protein carbonyls), N(-(carboxyethyl)lysine (CEL), N(-(carboxymethyl)lysine (CML), and N(-(malondialdehyde)lysine (MDAL), as well as mitochondrial Complex I content and amino acid and membrane fatty acyl composition, in the brain of short-lived mice (maximum life span [MLSP] 3.5 years) compared with those of long-lived budgerigar Fparakeets_ (MLSP, 21 years) and canaries (MLSP, 24 years). The brains of both bird species had significantly lower levels of compounds formed as a result of oxidative (GSA and AASA), glycoxidative (CEL and CML), and lipoxidative (CML and MDAL) protein modifications, as well as a lower levels of mitochondrial complex I protein. Although it is known that fatty acid unsaturation is lower in many tissues of long-lived compared to short-lived mammals, this is not true in the particular case of brain. In agreement with this, we also found that the brain tissue of bugerigars and canaries contains no fewer double bonds than that of mice. Amino acid composition analyses revealed that bird proteins have a significantly lower content of His, Leu and Phe, as well as, interestingly, of methionine, whereas Asp, Glu, Ala, Val, and Lys contents were higher than in the mammals. These results, together with those previously described in other tissues of pigeons (MLSP, 35 years) compared to rats (MLSP, 4 years), indicate that oxidative damage to proteins, lipids and mitochondrial DNA are lower in birds (very long-lived species) than in short-lived mammals of similar body size. The lower degree of oxidative modification of bird brain proteins was not due to decreases in the target amino acids (lysine for CEL, CML, MDAL, and AASA; and arg and pro for GSA), since these were present in bird brain proteins at higher or similar levels than in those of mice. These results are consistent with the possibility that decreases in oxidative protein modification are caused at least in part by the low rate of mitochondrial oxygen radical generation in these birds, as in all long-lived homeothermic vertebrates investigated so far.

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Section: Discussionmentioning

confidence: 43%

Section: Discussionmentioning

confidence: 99%

Protein and lipid oxidative damage and complex I content are lower in the brain of budgerigar and canaries than in mice. Relation to aging rate

Pamplona

Portero‐Otín

Sanz

et al. 2005

AGE

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“…However, recently it has been shown that one aspect of cell composition, namely, membrane fatty acid composition, does vary in a systematic manner with body size in mammals (69,164) and in birds (37,162). It has also been shown that membrane fatty acid composition is related to MLSP (266,271,272,(275)(276)(277). These observations, when combined with the long-known differences in susceptibility of different fatty acids to peroxidative damage (148), were seminal in the development of the "homeoviscouslongevity" membrane theory (267) and the later "membrane-pacemaker" theory of aging (155).…”

Section: Introductionmentioning

confidence: 82%

Life and Death: Metabolic Rate, Membrane Composition, and Life Span of Animals

Hulbert¹,

Pamplona²,

Buffenstein

et al. 2007

Physiological Reviews

765

725

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Maximum life span differences among animal species exceed life span variation achieved by experimental manipulation by orders of magnitude. The differences in the characteristic maximum life span of species was initially proposed to be due to variation in mass-specific rate of metabolism. This is called the rate-of-living theory of aging and lies at the base of the oxidative-stress theory of aging, currently the most generally accepted explanation of aging. However, the rate-of-living theory of aging while helpful is not completely adequate in explaining the maximum life span. Recently, it has been discovered that the fatty acid composition of cell membranes varies systematically between species, and this underlies the variation in their metabolic rate. When combined with the fact that 1) the products of lipid peroxidation are powerful reactive molecular species, and 2) that fatty acids differ dramatically in their susceptibility to peroxidation, membrane fatty acid composition provides a mechanistic explanation of the variation in maximum life span among animal species. When the connection between metabolic rate and life span was first proposed a century ago, it was not known that membrane composition varies between species. Many of the exceptions to the rate-of-living theory appear explicable when the particular membrane fatty acid composition is considered for each case. Here we review the links between metabolic rate and maximum life span of mammals and birds as well as the linking role of membrane fatty acid composition in determining the maximum life span. The more limited information for ectothermic animals and treatments that extend life span (e.g., caloric restriction) are also reviewed.

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“…Unsaturated fatty acids are sensitive to free radical damage, thus low double bond content should be advantageous by decreasing the sensitivity of tissues to lipid peroxidation; this would be crucial in mitochondrial membranes as they are the major source of ROS (Pamplona et al, 1999). Pamplona et al noted that the degree of unsaturation of fatty acids and the sensitivity of lipid peroxidation of liver and heart mitochondria are lower in the long-lived pigeon than in the short-lived rat, although they have similar metabolic rates (Pamplona et al, 1996;Pamplona et al, 1999). The susceptibility of fatty acids to free radical damage increases exponentially as a function of the number of double bonds per fatty acid molecule.…”

Section: Discussionmentioning

confidence: 99%

Linkages between the life-history evolution of tropical and temperate birds and the resistance of their cells to oxidative and non-oxidative chemical injury

Jiménez

Harper

Queenborough

et al. 2012

Journal of Experimental Biology

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SUMMARYA fundamental challenge facing physiological ecologists is to understand how variation in life history at the whole-organism level might be linked to cellular function. Thus, because tropical birds have higher annual survival and lower rates of metabolism, we hypothesized that cells from tropical species would have greater cellular resistance to chemical injury than cells from temperate species. We cultured dermal fibroblasts from 26 tropical and 26 temperate species of birds and examined cellular resistance to cadmium, H 2 O 2 , paraquat, thapsigargin, tunicamycium, methane methylsulfonate (MMS) and UV light. Using ANCOVA, we found that the values for the dose that killed 50% of cells (LD 50 ) from tropical birds were significantly higher for H 2 O 2 and MMS. When we tested for significance using a generalized least squares approach accounting for phylogenetic relationships among species to model LD 50 , we found that cells from tropical birds had greater tolerance for Cd, H 2 O 2 , paraquat, tunicamycin and MMS than cells from temperate birds. In contrast, tropical birds showed either lower or no difference in tolerance to thapsigargin and UV light in comparison with temperate birds. These findings are consistent with the idea that natural selection has uniquely fashioned cells of long-lived tropical bird species to be more resistant to forms of oxidative and non-oxidative stress than cells from shorterlived temperate species.Supplementary material available online at

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Low fatty acid unsaturation protects against lipid peroxidation in liver mitochondria from long-lived species: the pigeon and human case

Cited by 130 publications

References 28 publications

Protein and lipid oxidative damage and complex I content are lower in the brain of budgerigar and canaries than in mice. Relation to aging rate

Protein and lipid oxidative damage and complex I content are lower in the brain of budgerigar and canaries than in mice. Relation to aging rate

Life and Death: Metabolic Rate, Membrane Composition, and Life Span of Animals

Linkages between the life-history evolution of tropical and temperate birds and the resistance of their cells to oxidative and non-oxidative chemical injury

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