Voluntary locomotor activity mitigates oxidative damage associated with isolation stress in the prairie vole (<i>Microtus ochrogaster</i>)

Fletcher, Kelsey L.; Whitley, Brittany N.; Treidel, Lisa A.; Thompson, David M.; Williams, A. J.; Noguera, José C.; Stevenson, Jennie R.; Haussmann, Mark F.

doi:10.1098/rsbl.2015.0178

Cited by 11 publications

(8 citation statements)

References 17 publications

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“…Long-term physical inactivity has been shown to activate endothelial NADPH oxidase, resulting in cerebral vascular dysfunction in mice (25). On the other hand, routine locomotor activity reduces brain oxidative stress (26). Adding to this knowledge about redox regulation of brain function, the current study showed that the normal aging process is associated with a massive increase in brain Nox2-dependent ROS production, together with a reduction in locomotor function, including voluntary wheel running activity in aging WT but not Nox2KO mice.…”

Section: Discussionmentioning

confidence: 99%

Nox2 contributes to age-related oxidative damage to neurons and the cerebral vasculature

Fan

Geng

Cahill-Smith

et al. 2019

Journal of Clinical Investigation

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Oxidative stress plays an important role in aging-related neurodegeneration. This study used littermates of WT and Nox2-knockout (Nox2KO) mice plus endothelial cell–specific human Nox2 overexpression–transgenic (HuNox2Tg) mice to investigate Nox2-derived ROS in brain aging. Compared with young WT mice (3–4 months), aging WT mice (20–22 months) had obvious metabolic disorders and loss of locomotor activity. Aging WT brains had high levels of angiotensin II (Ang II) and ROS production; activation of ERK1/2, p53, and γH2AX; and losses of capillaries and neurons. However, these abnormalities were markedly reduced in aging Nox2KO brains. HuNox2Tg brains at middle age (11–12 months) already had high levels of ROS production and activation of stress signaling pathways similar to those found in aging WT brains. The mechanism of Ang II–induced endothelial Nox2 activation in capillary damage was examined using primary brain microvascular endothelial cells. The clinical significance of Nox2-derived ROS in aging-related loss of cerebral capillaries and neurons was investigated using postmortem midbrain tissues of young (25–38 years) and elderly (61–85 years) adults. In conclusion, Nox2 activation is an important mechanism in aging-related cerebral capillary rarefaction and reduced brain function, with the possibility of a key role for endothelial cells.

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Section: Discussionmentioning

confidence: 99%

Nox2 contributes to age-related oxidative damage to neurons and the cerebral vasculature

Fan

Geng

Cahill-Smith

et al. 2019

Journal of Clinical Investigation

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“…However, the house sparrow, as a species, might be unique in terms of how it deals with oxidative damage during inflammation. Compared with domestic chickens (Gallus gallus) (Treidel et al, 2013) and prairie voles (Microtus ochrogaster) (Fletcher et al, 2015), two species measured in the same lab as the birds here, TAC was 10 times higher and ROM was 2 times lower prior to LPS challenge in Kenyan house sparrows. Thus, an alternative explanation for the pattern observed in Kenya is that there was strong selection for oxidative damage mitigation at the time of the initial introduction to Mombasa, and only those birds with robust TAC and/or modest ROM responses persist today.…”

Section: Population Differences In Inflammation Costsmentioning

confidence: 98%

Costs of immunity and their role in the range expansion of the house sparrow in Kenya

Martin

Kilvitis

Brace

et al. 2017

Journal of Experimental Biology

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There are at least two reasons to study traits that mediate successful range expansions. First, dispersers will found new populations and thus impact the distribution and evolution of species. Second, organisms moving into new areas will influence the fate of resident communities, directly competing with or indirectly affecting residents by spreading non-native or spilling-back native parasites. The success of invaders in new areas is likely mediated by a counterbalancing of costly traits. In new areas where threats are comparatively rare, individuals that grow rapidly and breed prolifically should be at an advantage. High investment in defenses should thus be disfavored. In the present study, we compared the energetic, nutritional and collateral damage costs of an inflammatory response among Kenyan house sparrow (Passer domesticus) populations of different ages, asking whether costs were related to traits of individuals from three different capture sites. Kenya is among the world's most recent range expansions for this species, and we recently found that the expression of Toll-like receptors (TLRs), leukocyte receptors that instigate inflammatory responses when bound to microbial elements, was related to the range expansion across the country. Here, we found (contrary to our expectations) that energetic and nutritional costs of inflammation were higher, but damage costs were lower, in range-edge compared with core birds. Moreover, at the individual level, TLR-4 expression was negatively related to commodity costs (energy and a critical amino acid) of inflammation. Our data thus suggest that costs of inflammation, perhaps mediated by TLR expression, might mitigate successful range expansions.

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“…We assessed reactive oxygen metabolites (ROMs) and total antioxidant capacity (TAC), using the D-ROMs and OXY-adsorbent tests (Diacron International, Grosseto, Italy), respectively, in all blood samples as described previously ( Fletcher et al, 2015 ). The D -ROMs test measures intermediate oxidative damage compounds, mostly represented by hydroperoxides, derived from lipids, proteins and nucleotides.…”

Section: Methodsmentioning

confidence: 99%

Oxytocin administration prevents cellular aging caused by social isolation

Stevenson

McMahon

Boner

et al. 2019

Psychoneuroendocrinology

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Chronic stressors, such as chronic isolation in social mammals, can elevate glucocorticoids, which can affect cellular mechanisms of aging, including increased levels of oxidative stress and shortened telomere lengths. Recent work in the selectively social prairie vole ( Microtus ochrogaster ) suggests that oxytocin and social support may mitigate some of the negative consequences of social isolation, possibly by reducing glucocorticoid levels. We investigated the influences of isolation, social support, and daily oxytocin injections in female prairie voles. Glucocorticoid levels, oxidative damage, telomere length, and anhedonia, a behavioral index of depression, were measured throughout the study. We found that six weeks of chronic isolation led to increased glucocorticoid levels, oxidative damage, telomere degradation and anhedonia. However, daily oxytocin injections in isolated voles prevented these negative consequences. These findings demonstrate that chronic social isolation in female prairie voles is a potent stressor that results in depression-like behavior and accelerated cellular aging. Importantly, oxytocin can completely prevent the negative consequences of social isolation.

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Voluntary locomotor activity mitigates oxidative damage associated with isolation stress in the prairie vole (Microtus ochrogaster)

Cited by 11 publications

References 17 publications

Nox2 contributes to age-related oxidative damage to neurons and the cerebral vasculature

Nox2 contributes to age-related oxidative damage to neurons and the cerebral vasculature

Costs of immunity and their role in the range expansion of the house sparrow in Kenya

Oxytocin administration prevents cellular aging caused by social isolation

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