Protein stability and resistance to oxidative stress are determinants of longevity in the longest-living rodent, the naked mole-rat
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The widely accepted oxidative stress theory of aging postulates that aging results from accumulation of oxidative damage. Surprisingly, data from the longest-living rodent known, naked mole-rats [MRs; mass 35 g; maximum lifespan (MLSP) > 28.3 years], when compared with mice (MLSP 3.5 years) exhibit higher levels of lipid peroxidation, protein carbonylation, and DNA oxidative damage even at a young age. We hypothesize that age-related changes in protein structural stability, oxidation, and degradation are abrogated over the lifespan of the MR. We performed a comprehensive study of oxidation states of protein cysteines [both reversible (sulfenic, disulfide) and indirectly irreversible (sulfinic/sulfonic acids)] in liver from young and old C57BL/6 mice (6 and 28 months) and MRs (2 and >24 years). Furthermore, we compared interspecific differences in urea-induced protein unfolding and ubiquitination and proteasomal activity. Compared with data from young mice, young MRs have 1.6 times as much free protein thiol groups and similar amounts of reversible oxidative damage to cysteine. In addition, they show less urea-induced protein unfolding, less protein ubiquitination, and higher proteasome activity. Mice show a significant age-related increase in cysteine oxidation and higher levels of ubiquitination. In contrast, none of these parameters were significantly altered over 2 decades in MRs. Clearly MRs have markedly attenuated age-related accrual of oxidation damage to thiol groups and age-associated up-regulation of homeostatic proteolytic activity. These pivotal mechanistic interspecies differences may contribute to the divergent aging profiles and strongly implicate maintenance of protein stability and integrity in successful aging.
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Long-lived animals including naked mole-rats, calorie-restricted/intermittent-fasting rodents, and long-lived daf-2 mutant worms have decreased oxidative damage and greater resistance to oxidative stress.
“Accordingly, long-lived animals, including the naked mole-rat, rodents maintained on calorie restricted (CR) and intermittent fasting (IF) diets, and long-lived daf-2 mutant worms exhibit decreased levels of oxidative damage and are more resistant to oxidative stress (Fontana and Partridge, 2015; Guarente and Kenyon, 2000; Pérez et al., 2009).”
From NAD+ in Brain Aging and Neurodegenerative Disorders (2019) · cites this paper as Pérez et al., 2009
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- Authors
- Pérez, V. I., Buffenstein, R., Masamsetti, V., Leonard, S., Salmon, A. B., Mele, J., Andziak, B., Yang, T., Edrey, Y., Friguet, B., Ward, W., Richardson, A., & Chaudhuri, A.
- Affiliations
- The University of Texas at San Antonio Health Science Center (US)
- City University of New York (US)
- Université Paris Diderot (FR)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2009-03-03
- Volume
- 106
- Issue
- 9
- Pages
- 3059-3064
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2651236
- OpenAlex
- W2155933519
- Cited by
- 418
- References
- 44
- Citations by year
- 2026: 13 · 2025: 8 · 2024: 11 · 2023: 21 · 2022: 17 · 2021: 34 · 2020: 28 · 2019: 38 · 2018: 26 · 2017: 21 · 2016: 16 · 2015: 29 · 2014: 27 · 2013: 27 · 2012: 24
- FWCI
- 10.24
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5k07ag025063-05)
- National Institute on Aging (R01AG023843, R01AG022891, AG022891, R37 AG26557, R01AG025362, R37AG026557, AG025362, K07 AG02506304, K07-AG-025063)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Keywords
- naked mole-rat, protein stability, protein oxidation, cysteine oxidation, protein thiol groups, protein unfolding, ubiquitination, proteasome activity, protein degradation, longevity, cross-species comparison, mice, liver
- MeSH terms
- Animals, Cysteine, Longevity, Oxidation-Reduction, Protein Folding, Oxidative Stress, Mole Rats, Mice, Rats, Ubiquitination, Protein Stability
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