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. 2006 Feb 17;27(4):267–280. doi: 10.1007/s11357-005-4562-x

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

Reinald Pamplona 1,✉, Manuel Portero-Otín 1, Alberto Sanz 2, Victoria Ayala 1, Ekaterina Vasileva 1, Gustavo Barja 2,✉
PMCID: PMC3455889  PMID: 23598660

Abstract

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), Nɛ-(carboxyethyl)lysine (CEL), Nɛ-(carboxymethyl)lysine (CML), and Nɛ-(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 ‘parakeets’ (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.

Key words: Aminoadipic semialdehyde, complex I, glutamic semialdehyde, lipid peroxidation, Maillard reaction, malondialdehyde, maximum life span, Nɛ-(carboxyethyl)lysine, Nɛ-(carboxymethyl)lysine, Nɛ-(malondialdehyde)lysine, peroxidizability index, protein carbonyls, protein oxidation

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Abbreviations

AASA

aminoadipic semialdehyde

CEL

Nɛ-(carboxyethyl)lysine

CML

Nɛ-(carboxymethyl)lysine

DBI

double bond index

GSA

glutamic semialdehyde

MDAL

Nɛ-(malondialdehyde)lysine

MLSP

maximum life span

PI

peroxidizability index

PUFA

polyunsaturated fatty acids

ROS

reactive oxygen species

SFA

saturated fatty acids

UFA

unsaturated fatty acids

Contributor Information

Reinald Pamplona, FAX: +34-973702426, Email: reinald.pamplona@cmb.udl.es.

Gustavo Barja, FAX: +34-913944935, Email: gbarja@bio.ucm.es.

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