The long lifespan of two bat species is correlated with resistance to protein oxidation and enhanced protein homeostasis

Abstract

Altered structure, and hence function, of cellular macromolecules caused by oxidation can contribute to loss of physiological function with age. Here, we tested whether the lifespan of bats, which generally live far longer than predicted by their size, could be explained by reduced protein damage relative to short-lived mice. We show significantly lower protein oxidation (carbonylation) in Mexican free-tailed bats (Tadarida brasiliensis) relative to mice, and a trend for lower oxidation in samples from cave myotis bats (Myotis velifer) relative to mice. Both species of bat show in vivo and in vitro resistance to protein oxidation under conditions of acute oxidative stress. These bat species also show low levels of protein ubiquitination in total protein lysates along with reduced proteasome activity, suggesting diminished protein damage and removal in bats. Lastly, we show that bat-derived protein fractions are resistant to urea-induced protein unfolding relative to the level of unfolding detected in fractions from mice. Together, these data suggest that long lifespan in some bat species might be regulated by very efficient maintenance of protein homeostasis.

Lifespan of mice and primates correlates with immunoproteasome expression

“…In addition, fibroblasts from long-lived rodent and bird species require higher doses of a range of oxidants to cause lethality than do fibroblasts from shorter-lived species (2,3). Similar findings have been made by other studies using smaller sets of animals (4)(5)(6). It has also been shown that telomerase activity is higher in larger longer-lived species, though this association was found to be more closely linked with body mass than with lifespan (7).…”

Age-related cellular changes in the long-lived bivalve A. islandica

“…Differences in A. islandica protein stability may be due to posttranslational modifications, chaperone compositions, and chaperone activities (Pride et al 2015). Relatively high protein stability in the gills of long-lived A. islandica is consistent with previous observations of high protein stability in A. islandica foot and adductor muscle compared to other clams, and higher protein stability in long-lived than short-lived vertebrates (Pérez et al 2009;Salmon et al 2009;Treaster et al 2014). However, protein stability does not change over the lifetime of either A. islandica population.…”

Enhanced protein repair and recycling are not correlated with longevity in 15 vertebrate endotherm species

“…Indeed, bat liver 20S/26S proteasome activities were in the mid-range of all species values, whereas heart and brain proteasome activities were actually in the high end of the species range. There are numerous possible reasons for the differences between the present study and Salmon et al (2009), including the use of different bat species. However, these contrasting results highlight the importance of using as many species as possible in such studies to avoid biasing conclusions.…”

“…This conclusion is consistent with two recent reports of proteasome activity in the context of mammalian species lifespan. Salmon et al (2009) also reported significantly lower 20S proteasome activity in livers of two long-lived bat species, Tadarida brasiliensis and Myotis velifer, compared to mice. Interestingly, we did not find that liver 20S and 26S proteasome activities in our bat Table 3 Statistical analysis of enzyme activities as correlates of body mass species, Eptesicus fuscus, were lower than those in mice.…”

“…Similarly, proteins of naked mole rats actually have higher cysteine content than shorter-lived mice (Perez et al 2009a). On the other hand, proteins in crude liver homogenates of some long-lived species, such as bats or naked mole rats, have been shown to resist urea-induced denaturation, which suggests some inherent stabilizing property (Perez et al 2009a;Salmon et al 2009). Perez et al (2009a) report that this is not attributable to differences in heat shock protein-70 levels.…”