Heat dissipation does not suppress an immune response in laboratory mice divergently selected for basal metabolic rate (BMR)

Książek, Aneta; Konarzewski, Marek

doi:10.1242/jeb.129312

Cited by 5 publications

(3 citation statements)

References 88 publications

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“…Here, we cannot exclude that the H-BMR mice are more effective in using these physiological mechanisms than the L-BMR line. Irrespective of the responsible mechanisms, our results clearly show that even though SPA was indeed reduced by high ambient temperature, any potential heat stress did not preclude the H-BMR mice from expressing their genetically based higher SPA (this conclusion agrees with the results of earlier experiments on other costly traits in the same lines of mice (Książek and Konarzewski 2016;Sadowska et al 2019). Furthermore, our results suggest that the between-strain differences in SPA are not affected by thermal preferences of mice that can vary during the day (Keijer et al 2019).…”

Section: Discussionsupporting

confidence: 89%

Significance of variation in basal metabolic rate in laboratory mice for translational experiments

et al. 2021

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The basal metabolic rate (BMR) accounts for 60–70% of the daily energy expenditure (DEE) in sedentary humans and at least 50% of the DEE in laboratory mice in the thermoneutral zone. Surprisingly, however, the significance of the variation in the BMR is largely overlooked in translational research using such indices as physical activity level (PAL), i.e., the ratio of DEE/BMR. In particular, it is unclear whether emulation of human PAL in mouse models should be carried out within or below the thermoneutral zone. It is also unclear whether physical activity within the thermoneutral zone is limited by the capacity to dissipate heat generated by exercise and obligatory metabolic processes contributing to BMR. We measured PAL and spontaneous physical activity (SPA) in laboratory mice from two lines, divergently selected towards either high or low level of BMR, and acclimated to 30 °C (i.e., the thermoneutral zone), 23 or 4 °C. The mean PAL did not differ between both lines in the mice acclimated to 30 °C but became significantly higher in the low BMR mouse line at the lower ambient temperatures. Acclimation to 30 °C reduced the mean locomotor activity but did not affect the significant difference observed between the selected lines. We conclude that carrying out experiments within the thermoneutral zone can increase the consistency of translational studies aimed at the emulation of human energetics, without affecting the variation in physical activity correlated with BMR.

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Section: Discussionsupporting

confidence: 89%

Significance of variation in basal metabolic rate in laboratory mice for translational experiments

et al. 2021

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“…Artificial selection experiments using rodents provide some of the most compelling evidence that individuals with high EE also sustain high immune function. For example, mice selected for high resting EE had enhanced immune function and larger lymph node mass and spleen than mice selected for low resting EE, indicating that elevated energy capacity (reflected by high resting EE, see Box 1) permits greater immune response, while also permitting greater sustained activity rates [ 54 ]. In another example, rats selected for low and for high EE were exposed to breast cancer cells, and while high EE rats effectively resisted the spread of cancer, low-EE rats did not and, additionally, lost weight over time [ 42 ].…”

Section: Literature Support For Hypothesismentioning

confidence: 99%

A novel perspective suggesting high sustained energy expenditure may be net protective against cancer

Biro

Thomas

Újvári

et al. 2022

Evolution, Medicine, and Public Health

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Energy expenditure (EE) is generally viewed as tumorigenic, due to production of reactive oxygen species (ROS) that can damage cells and DNA. On this basis, individuals within a species that sustain high EE should be more likely to develop cancer. Here, we argue the opposite, that high EE may be net protective effect against cancer, despite high ROS production. This is possible because individuals that sustain high EE have a greater energetic capacity (= greater energy acquisition, expenditure, and ability to upregulate output), and can therefore allocate energy to multiple cancer-fighting mechanisms with minimal energetic tradeoffs. Our review finds that individuals sustaining high EE have greater anti-oxidant production, lower oxidative stress, greater immune function and lower cancer incidence. Our hypothesis and literature review suggest that EE may indeed be net protective against cancer, and that individual variation in energetic capacity may be a key mechanism to understand the highly individual nature of cancer risk.

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“… b M1: Varkoohi et al (2010); M2: Bordas et al (1992), Gabarrou et al (1998), Morisson et al (1997), Zerjal et al (2021); M3: Johnson and McLaury (1973), McLaury and Johnson (1972); M4: Pym and Nicholls (1979); M5: Brien et al (1984), Brien and Hill (1986); M5: Brien et al (1984), Brien nad Hill (1986); M6: Al Jothery et al (2016), Hastings et al (1997), Selman et al (2001); M7: Bhatnagar and Nielsen (2014), Nielsen et al (1997); M8: Książek and Konarzewski (2016), Sadowska et al (2013); M9: Downs et al (2013); M10: Clapperton et al (2006), Kerr and Cameron (1995); M11: Chatelet et al (2018), Gilbert et al (2017); M12: Boddicker et al (2011), Cai et al (2008), Grubbs et al (2013), Young et al (2016), and M13: Arthur et al (2005), Richardson and Herd (2004). …”

Section: Survey Of Breed Comparisons and Selection Experimentsmentioning

confidence: 99%

How much energetic trade‐offs limit selection? Insights from livestock and related laboratory model species

Douhard

Gilbert

et al. 2021

Evolutionary Applications

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Trade-offs between life history traits are expected to occur due to the limited amount of resources that organisms can obtain and share among biological functions, but are of least concern for selection responses in nutrientrich or benign environments. In domestic animals, selection limits have not yet been reached despite strong selection for higher meat, milk or egg yields. Yet, negative genetic correlations between productivity traits and health or fertility traits have often been reported, supporting the view that trade-offs do occur in the context of nonlimiting resources. The importance of allocation mechanisms in limiting genetic changes can thus be questioned when animals are mostly constrained by their time to acquire and process energy rather than by feed availability. Selection for high productivity traits early in life should promote a fast metabolism with less energy allocated to self-maintenance (contributing to soma preservation and repair). Consequently, the capacity to breed shortly after an intensive period of production or to remain healthy should be compromised. We assessed those predictions in mammalian and avian livestock and related laboratory model species. First, we surveyed studies that compared energy allocation to maintenance between breeds or lines of contrasting productivity but found little support for the occurrence of an energy allocation tradeoff. Second, selection experiments for lower feed intake per unit of product (i.e. higher feed efficiency) generally resulted in reduced allocation to maintenance, but this did not entail fitness costs in terms of survival or future reproduction. These findings indicate that the consequences of a particular selection in domestic animals are much more difficult to predict than one could anticipate from the energy allocation framework alone. Future developments to predict the contribution of time constraints and tradeoffs to selection limits will be insightful to breed livestock in increasingly challenging environments.This is an open access article under the terms of the Creat ive Commo ns Attri bution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

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Heat dissipation does not suppress an immune response in laboratory mice divergently selected for basal metabolic rate (BMR)

Cited by 5 publications

References 88 publications

Significance of variation in basal metabolic rate in laboratory mice for translational experiments

Significance of variation in basal metabolic rate in laboratory mice for translational experiments

A novel perspective suggesting high sustained energy expenditure may be net protective against cancer

How much energetic trade‐offs limit selection? Insights from livestock and related laboratory model species

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