Adaptation of peroxisome proliferator-activated receptor alpha to hibernation in bats

Han, Yong‐Jian; Zheng, Guantao; Yang, Tianxiao; Zhang, Shuyi; Dong, Dong; Pan, Yi-Hsuan

doi:10.1186/s12862-015-0373-6

Cited by 15 publications

(13 citation statements)

References 75 publications

(85 reference statements)

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“…4e, the levels of ATF4 were found to be increased during torpor. These findings suggest that the PERK/ EIF2/ATF4 signal transduction pathway is activated in torpid bats and that these bats selectively produce some proteins to cope with endoplasmic reticulum stress as seen in many hibernating mammals 51,52 . Since the levels of several UPR ER makers, such as ATF4, PERK, and GRP78, are increased in various tissues (e.g., brain, liver, and muscle) of different mammalian species (e.g., ground squirrels, hamsters, and bats) during hibernation 26,29,[53][54][55] , these findings also support our hypothesis that UPR ER is a common stress response in bats.…”

Section: Discussionmentioning

confidence: 87%

Co-activation of Akt, Nrf2, and NF-κB signals under UPRER in torpid Myotis ricketti bats for survival

Huang

Liao²,

Han

et al. 2020

Commun Biol

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Bats hibernate to survive stressful conditions. Examination of whole cell and mitochondrial proteomes of the liver of Myotis ricketti revealed that torpid bats had endoplasmic reticulum unfolded protein response (UPRER), global reduction in glycolysis, enhancement of lipolysis, and selective amino acid metabolism. Compared to active bats, torpid bats had higher amounts of phosphorylated serine/threonine kinase (p-Akt) and UPRER markers such as PKR-like endoplasmic reticulum kinase (PERK) and activating transcription factor 4 (ATF4). Torpid bats also had lower amounts of the complex of Kelch-like ECH-associated protein 1 (Keap1), nuclear factor erythroid 2-related factor 2 (Nrf2), and nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB) (p65)/I-κBα. Cellular redistribution of 78 kDa glucose-regulated protein (GRP78) and reduced binding between PERK and GRP78 were also seen in torpid bats. Evidence of such was not observed in fasted, cold-treated, or normal mice. These data indicated that bats activate Akt, Nrf2, and NF-κB via the PERK-ATF4 regulatory axis against endoplasmic reticulum stresses during hibernation.

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Section: Discussionmentioning

confidence: 87%

Co-activation of Akt, Nrf2, and NF-κB signals under UPRER in torpid Myotis ricketti bats for survival

Huang

Liao²,

Han

et al. 2020

Commun Biol

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“…Indeed, NFYA, a known regulator of HSP 70/90 and a TF expressed higher in bats (Fig. 4d ), has also been implicated in torpor (Han et al 2015 ). Other additional elements compared to human included GATA, NFAT, ELK1/Ets and MYB binding sites, though these had lower binding scores.…”

Section: Discussionmentioning

confidence: 97%

High basal heat-shock protein expression in bats confers resistance to cellular heat/oxidative stress

Chionh

Cui

Koh

et al. 2019

Cell Stress and Chaperones

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Bats, unique among mammals with powered flight, have many species with the longest size-proportionate lifespan of all mammals. Evolutionary adaptations would have been required to survive the elevated body temperatures during flight. Heat shock protein (HSP), highly conserved master regulators of cell stress, expression was examined across tissues and various cell lines in bats. Basal expression level of major HSPs (HSP70 and HSP90) is significantly higher in two different bat species compared to other mammals. This HSP expression could be a bat-unique, key factor to modulate cellular stress and death. Consequently, bat cells survive prolonged heat treatment, along with other stress stimuli, in a HSP-dependent manner, whereas other mammalian cells succumbed. This suggests HSP expression in bats could be an important adaption to intrinsic metabolic stresses like flight and therefore an important model to study stress resilience and longevity in general.

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“…Studies of transcriptomes in small hibernating mammals have revealed that many genes involved in metabolism are differentially expressed during hibernation. Specifically, the genes involved in carbohydrate catabolism are downregulated during hibernation, while genes responsible for lipid catabolism are upregulated (Carey et al, 2013; Stevenson et al, 2014; Han et al, 2015; Xiao et al, 2015; Sommer et al, 2016). We also found that the relative abundance of functional categories associated with amino acid metabolism increased in the early winter compared with the late summer, consistent with other studies showing that hibernating bats have elevated levels of amino acid metabolism during hibernation (Pan et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

Seasonal Changes in Gut Microbiota Diversity and Composition in the Greater Horseshoe Bat

et al. 2019

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A large number of microorganisms colonize the intestines of animals. The gut microbiota plays an important role in nutrient metabolism and affects a number of physiological mechanisms in the host. Studies have shown that seasonal changes occur in the intestinal microbes of mammals that hibernate seasonally. However, these studies only focused on ground squirrels and bears. It remains unclear how hibernation might affect the intestinal microbes of bats. In this study, we measured microbial diversity and composition in the gut of Rhinolophus ferrumequinum in different periods (early spring, early summer, late summer, torpor, and interbout arousal) using 16S ribosomal RNA gene amplicon sequencing and PICRUSt to predict functional profiles. We found seasonal changes in the diversity and composition of the gut microbes in R. ferrumequinum. The diversity of gut microbiota was highest in the late summer and lowest in the early summer. The relative abundance of Proteobacteria was highest in the early summer and significantly lower in other periods. The relative abundance of Firmicutes was lowest in the early summer and significantly increased in the late summer, followed by a significant decrease in the early winter and early spring. The relative abundance of Tenericutes was significantly higher in the early spring compared with other periods. The results of functional prediction by PICRUSt showed seasonal variations in the relative abundance of metabolism-related pathways, including lipid metabolism, carbohydrate metabolism, and energy metabolism. Functional categories for carbohydrate metabolism had significantly lower relative abundance in early winter-torpor compared with late summer, while those associated with lipid metabolism had significantly higher relative abundance in the early winter compared with late summer. Overall, our results show that seasonal physiological changes associated with hibernation alter the gut microbial community of R. ferrumequinum. Hibernation may also alter the metabolic function of intestinal microbes, possibly by converting the gut microflora from carbohydrate-related to lipid-related functional categories. This study deepens our understanding of the symbiosis between hibernating mammals and gut microbes.

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Adaptation of peroxisome proliferator-activated receptor alpha to hibernation in bats

Cited by 15 publications

References 75 publications

Co-activation of Akt, Nrf2, and NF-κB signals under UPRER in torpid Myotis ricketti bats for survival

Co-activation of Akt, Nrf2, and NF-κB signals under UPRER in torpid Myotis ricketti bats for survival

High basal heat-shock protein expression in bats confers resistance to cellular heat/oxidative stress

Seasonal Changes in Gut Microbiota Diversity and Composition in the Greater Horseshoe Bat

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