Heart fatty acid unsaturation and lipid peroxidation, and aging rate, are lower in the canary and the parakeet than in the mouse

Pamplona, Reinald; Portero‐Otín, Manuel; Riba, D.; Ledo, Fran; Gredilla, Ricardo; Herrero, A.; Barja, Gustavo

doi:10.1007/bf03399636

Cited by 61 publications

(42 citation statements)

References 22 publications

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“…Thus the novel and unexpected finding that the composition of membrane bilayers varies systematically in mammals provided a link between metabolic rate and maximum life span of mammalian species. In agreement with this, it was demonstrated that in long-lived mammals, the low degree of membrane fatty acid unsaturation was accompanied by a low sensitivity to in vivo and in vitro lipid peroxidation (269,272,(275)(276)(277) and a low steady-state level of lipoxidation-derived adducts in both tissue and mitochondrial proteins of skeletal muscle, heart, liver, and brain (267,268,274,277,292,307). These findings were consistent with the negative correlation between MLSP and the sensitivity to lipid autoxidation of mammalian kidney and brain homogenates that had been described some years earlier (72).…”

Section: Membrane Composition Lipid Peroxidation Body Size and supporting

confidence: 62%

“…At the same time that the fatty acid composition of membranes from a variety of mammalian tissues was related to variation in BMR (69,158,159), Pamplona and colleagues (266,271,272,(275)(276)(277) also measured the membrane fatty acid composition of a number of mammalian tissues and related it to MLSP of the particular species. Thus the novel and unexpected finding that the composition of membrane bilayers varies systematically in mammals provided a link between metabolic rate and maximum life span of mammalian species.…”

Section: Membrane Composition Lipid Peroxidation Body Size and mentioning

confidence: 99%

“…In addition to low rates of mitochondrial ROS formation, these bird species were shown to also have a membrane fatty acid composition that is considerably more METABOLIC RATE, MEMBRANE COMPOSITION, AND LIFE SPAN resistant to peroxidation than equivalent membranes from the mammals and also to have low levels of lipid peroxidation products in their tissues compared with mammals (275)(276)(277). That the mammal-bird difference in membrane fatty acid composition was an important determinant of this low level of lipid peroxidation in bird tissues was demonstrated by the dramatic reduction in MDA produced by avian mitochondria compared with mammalian mitochondria when both were subjected to an in vitro free radical generation system (276,277).…”

Section: Insights From Bird-mammal Comparisonsmentioning

confidence: 99%

“…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: 98%

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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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Section: Membrane Composition Lipid Peroxidation Body Size and supporting

confidence: 62%

Section: Membrane Composition Lipid Peroxidation Body Size and mentioning

confidence: 99%

Section: Insights From Bird-mammal Comparisonsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 98%

See 2 more Smart Citations

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

Hulbert¹,

Pamplona²,

Buffenstein

et al. 2007

Physiological Reviews

765

725

View full text Add to dashboard Cite

show abstract

“…This lack of consensus has led some to conclude that progressive accrual of oxidative damage is not an integral component of organismal aging, but rather that species-specific steady state levels of oxidative damage are important determinants of aging (Rikans and Hornbrook 1997). Some comparative studies show an inverse relationship between oxidative damage and longevity, already evident in young adults of a species (Pamplona et al 1999). While data from many longer-living species across a wide range of phyla concur with predictions based on this theory (Barja 2002b), exceptions have been reported; for example within flies, the longer-lived Drosophila spp.…”

Section: Do Levels Of Oxidative Damage Correlate With Mls?mentioning

confidence: 99%

The oxidative stress theory of aging: embattled or invincible? Insights from non-traditional model organisms

Buffenstein

Edrey

Yang

et al. 2008

AGE

162

131

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Reactive oxygen species (ROS), inevitable byproducts of aerobic metabolism, are known to cause oxidative damage to cells and molecules. This, in turn, is widely accepted as a pivotal determinant of both lifespan and health span. While studies in a wide range of species support the role of ROS in many agerelated diseases, its role in aging per se is questioned. Comparative data from a wide range of endotherms offer equivocal support for this theory, with many exceptions and inconclusive findings as to whether or not oxidative stress is either a correlate or a determinant of maximum species lifespan. Available data do not support the premise that metabolic rate and in vivo ROS production are determinants of lifespan, or that superior antioxidant defense contributes to species longevity. Rather, published studies often show either a negative associate or lack of correlation with species longevity. Furthermore, many long-living species such as birds, bats and mole-rats exhibit high levels of oxidative damage even at young ages. Similarly genetic manipulations altering expression of key antioxidants do not necessarily show an impact on lifespan, even though oxidative damage levels may be affected. While it is possible that these multiple exceptions to straightforward predictions of the free radical theory of aging all reflect speciesspecific, "private" mechanisms of aging, the preponderance of contrary data nevertheless present a challenge to this august theory. Therefore, contrary to accepted dogma, the role of oxidative stress as a determinant of longevity is still open to question.

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The Modulation of Lifespan by Natural Selection

Holliday¹

2003

Modulating Aging and Longevity

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Heart fatty acid unsaturation and lipid peroxidation, and aging rate, are lower in the canary and the parakeet than in the mouse

Cited by 61 publications

References 22 publications

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

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

The oxidative stress theory of aging: embattled or invincible? Insights from non-traditional model organisms

The Modulation of Lifespan by Natural Selection

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