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Comparative biology of mammalian telomeres: hypotheses on ancestral states and the roles of telomeres in longevity determination
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Summary: Progressive telomere shortening from cell division (replicative aging) provides a barrier for human tumor progression. This program is not conserved in laboratory mice, which have longer telomeres and constitutive telomerase. Wild species that do/do not use replicative aging have been reported, but the evolution of different phenotypes and a conceptual framework for understanding their uses of telomeres is lacking. We examined telomeres/telomerase in cultured cells from > 60 mammalian species to place different uses of telomeres in a broad mammalian context. Phylogeny‐based statistical analysis reconstructed ancestral states. Our analysis suggested that the ancestral mammalian phenotype included short telomeres (< 20 kb, as we now see in humans) and repressed telomerase. We argue that the repressed telomerase was a response to a higher mutation load brought on by the evolution of homeothermy. With telomerase repressed, we then see the evolution of replicative aging. Telomere length inversely correlated with lifespan, while telomerase expression co‐evolved with body size. Multiple independent times smaller, shorter‐lived species changed to having longer telomeres and expressing telomerase. Trade‐offs involving reducing the energetic/cellular costs of specific oxidative protection mechanisms (needed to protect < 20 kb telomeres in the absence of telomerase) could explain this abandonment of replicative aging. These observations provide a conceptual framework for understanding different uses of telomeres in mammals, support a role for human‐like telomeres in allowing longer lifespans to evolve, demonstrate the need to include telomere length in the analysis of comparative studies of oxidative protection in the biology of aging, and identify which mammals can be used as appropriate model organisms for the study of the role of telomeres in human cancer and aging.
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“The programmed silencing of TERT, loss of telomerase activity and the resulting shortening of telomeres is not a universal phenomenon in mammals. Apparently, this tumour suppressor pathway is restricted to large animals with a reproductive strategy that requires a long lifespan28.”
From Telomeres in cancer: tumour suppression and genome instability (2017) · cites this paper as [28]
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“Taken together, it seems that the evolution of large body sizes and longevity is strongly associated with the evolution of short telomeres and telomerase suppression, presumably for tumour suppression (de Magalhaes, 2013; Gomes et al., 2011).”
From Stress, cell senescence and organismal ageing (2018) · cites this paper as Gomes et al., 2011
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Metadata
- Authors
- Gomes, N. M. V., Ryder, O. A., Houck, M. L., Charter, S. J., Walker, W., Forsyth, N. R., Austad, S. N., Venditti, C., Pagel, M., Shay, J. W., & Wright, W. E.
- Affiliations
- University of Lisbon (PT)
- The University of Texas Southwestern Medical Center (US)
- Keele University (GB)
- University of Hull (GB)
- Santa Fe Institute (US)
- Corresponding author
- Wright, Woodring E.
- ORCID
- Venue
- Aging Cell
- Publisher
- Wiley
- Published
- 2011-06
- Volume
- 10
- Issue
- 5
- Pages
- 761-768
- ISSN
- 1474-9718 (ISSN-L)
- 1474-9726
- PMC
- PMC3387546
- OpenAlex
- W1483456062
- Cited by
- 464
- References
- 63
- Citations by year
- 2026: 18 · 2025: 33 · 2024: 34 · 2023: 33 · 2022: 36 · 2021: 41 · 2020: 40 · 2019: 39 · 2018: 39 · 2017: 30 · 2016: 24 · 2015: 26 · 2014: 19 · 2013: 24 · 2012: 24
- FWCI
- 15.26
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Aging Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- CentAUR (University of Reading) (acceptedVersion)
- Funders
- W. M. Keck Foundation
- National Marine Sanctuary Foundation
- European Commission
- Engineering and Physical Sciences Research Council (EP/H028277/1)
- Natural Environment Research Council (NE/C51992X/1)
- National Institute on Aging (AG 01228, R01AG001228)
- National Cancer Institute (P50CA070907)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Telomeres, Telomerase, and Senescence
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
- Keywords
- telomeres, telomerase, mammalian evolution, ancestral states, replicative senescence, lifespan, telomere length, homeothermy, mutational burden, body size, cancer, comparative biology, phylogenetic analysis
- MeSH terms
- Aging, Animals, Cell Division, Cell Line, Enzyme Repression, Fibroblasts, Genetic Vectors, Humans, Longevity, Mammals, Oxidation-Reduction, Phenotype, Phylogeny, Regression Analysis, Transfection, Telomere, Telomerase, Evolution, Molecular, Body Size, Cell Cycle Checkpoints, Telomere Shortening
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