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Interspecies differences in proteome turnover kinetics are correlated with lifespans and energetic demands

Kyle Swovick, Denis Firsanov, Kevin A. Welle, Jennifer R. Hryhorenko, John P. Wise, Craig George, Todd L. Sformo, Andrei Seluanov, Vera Gorbunova, View ORCID ProfileSina Ghaemmaghami
doi: https://doi.org/10.1101/2020.04.25.061150
Kyle Swovick
1Department of Biology, University of Rochester, NY, 14627, USA
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Denis Firsanov
1Department of Biology, University of Rochester, NY, 14627, USA
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Kevin A. Welle
2University of Rochester Mass Spectrometry Resource Laboratory, NY, 14627, USA
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Jennifer R. Hryhorenko
2University of Rochester Mass Spectrometry Resource Laboratory, NY, 14627, USA
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John P. Wise
3Wise Laboratory for Environmental and genetic Toxicology, University of Louisville, Department of Pharmacology and Toxicology, Louisville, KY, 40292, USA
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Craig George
4North Slope Borough Department of Wildlife Management, Barrow, AK, 99723
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Todd L. Sformo
4North Slope Borough Department of Wildlife Management, Barrow, AK, 99723
5Institute of Arctic Biology, University of Alaska Fairbanks, Fairbanks, AK, 99775
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Andrei Seluanov
1Department of Biology, University of Rochester, NY, 14627, USA
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Vera Gorbunova
1Department of Biology, University of Rochester, NY, 14627, USA
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Sina Ghaemmaghami
1Department of Biology, University of Rochester, NY, 14627, USA
2University of Rochester Mass Spectrometry Resource Laboratory, NY, 14627, USA
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  • ORCID record for Sina Ghaemmaghami
  • For correspondence: sina.ghaemmaghami@rochester.edu
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Abstract

Cells continually degrade and replace damaged and old proteins. However, the high energetic demand of protein turnover generates reactive oxygen species (ROS) that compromise the long-term health of the proteome. Thus, the relationship between aging, protein turnover and energetic demand remains unclear. Here, we used a proteomic approach to measure rates of protein turnover within primary fibroblasts isolated from a number of species with diverse lifespans including the longest-lives rodent, the naked mole rat and the longest-lived mammal, the bowhead whale. We show that organismal lifespan is negatively correlated with turnover rates of highly abundant proteins. In comparison to mice, cells from long-lived naked mole rats have slower rates of protein turnover, lower levels of ATP production and reduced ROS levels. Despite having slower rates of protein turnover, naked mole rat cells tolerate protein misfolding stress more effectively than mouse cells. We suggest that in lieu of rapid constitutive turnover, long-lived species may have evolved more energetically efficient mechanisms for selective detection and clearance of damaged proteins.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted April 27, 2020.
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Interspecies differences in proteome turnover kinetics are correlated with lifespans and energetic demands
Kyle Swovick, Denis Firsanov, Kevin A. Welle, Jennifer R. Hryhorenko, John P. Wise, Craig George, Todd L. Sformo, Andrei Seluanov, Vera Gorbunova, Sina Ghaemmaghami
bioRxiv 2020.04.25.061150; doi: https://doi.org/10.1101/2020.04.25.061150
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Interspecies differences in proteome turnover kinetics are correlated with lifespans and energetic demands
Kyle Swovick, Denis Firsanov, Kevin A. Welle, Jennifer R. Hryhorenko, John P. Wise, Craig George, Todd L. Sformo, Andrei Seluanov, Vera Gorbunova, Sina Ghaemmaghami
bioRxiv 2020.04.25.061150; doi: https://doi.org/10.1101/2020.04.25.061150

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