Inflammatory challenge increases measures of oxidative stress in a free-ranging, long-lived mammal

Abstract

SUMMARYOxidative stress -the imbalance between reactive oxygen species (ROS) and neutralising antioxidants -has been under debate as the main cause of ageing in aerobial organisms. The level of ROS should increase during infection as part of the activation of an immune response, leading to oxidative damage to proteins, lipids and DNA. Yet, it is unknown how long-lived organisms, especially mammals, cope with oxidative stress. Bats are known to carry a variety of zoonotic pathogens and at the same time are, despite their high mass-specific basal metabolic rate, unusually long lived, which may be partly the result of low oxidative damage of organs. Here, we asked whether an immune challenge causes oxidative stress in free-ranging bats, measuring two oxidative stress markers. We injected 20 short-tailed fruit bats (Carollia perspicillata) with bacterially derived lipopolysaccharide (LPS) and 20 individuals with phosphate-buffered saline solution (PBS) as a control. Individuals injected with LPS showed an immune reaction by increased white blood cell count after 24 h, whereas there was no significant change in leukocyte count in control animals. The biological antioxidant potential (BAP) remained the same in both groups, but reactive oxygen metabolites (ROMs) increased after treatment with LPS, indicating a significant increase in oxidative stress in animals when mounting an immune reaction toward the inflammatory challenge. Control individuals did not show a change in oxidative stress markers. We conclude that in a long-lived mammal, even high concentrations of antioxidants do not immediately neutralise free radicals produced during a cellular immune response. Thus, fighting an infection may lead to oxidative stress in bats.

Immune Profile Predicts Survival and Reflects Senescence in a Small, Long-Lived Mammal, the Greater Sac-Winged Bat (Saccopteryx bilineata)

“…Therefore, high WBC count may be associated with increased oxidative stress and oxidative damage. In a previous experiment, we showed that a cellular immune response causes an increase in concentration of damaging pro-oxidants in blood of the Neotropical short-tailed fruit bat, Carollia perspicillata , and that the number of immune cells is positively correlated with measures of oxidative stress [60]. Given that cells become less resistant to oxidative stress with increasing age [61], older individuals may be more affected by oxidative stress induced by WBCs.…”

A Potent Anti-Inflammatory Response in Bat Macrophages May Be Linked to Extended Longevity and Viral Tolerance

“…Interestingly, wild caught Molossus molossus bats injected with LPS showed no leucocytosis or fever (Stockmaier et al, 2015), which could be hypotheticaly explained by increased levels of antipyretic Il-10. However this observation might be speciesor experimental set-up-specific, as LPS induced fever was observed in Myotis vivesi (Otálora-Ardila et al, 2016) and leukocytosis occurred in challenged Carollia perspicillata (Schneeberger et al, 2013); therefore the LPS induced systemic responses in bats require further investigation. The proposed link between bat longevity, viral tolerance and antiinflammatory response is certainly plausible also in the light of available evidence from other species.…”

Angelica Sinensis Polysaccharide Prevents Hematopoietic Stem Cells Senescence in D-Galactose-Induced Aging Mouse Model

“…An imbalance between ROS production and degradation results in oxidative stress, leading primarily to peroxidation of membrane fatty acid chains, modification of DNA, loss of sulfhydryl and carbonylation in proteins, and higher cell apoptosis rates [31, 32]. Oxidative stress ultimately causes cellular senescence and is closely correlated to life-history in vertebrates [33]. Specifically, it has been reported that aberrant increases in ROS can disrupt HSC quiescence by stimulating entry into the cell cycle, which comprises the ability of the HSCs to self-renew and leads to premature exhaustion [34–36].…”