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Surviving winter on the Qinghai-Xizang Plateau:Extensive reversible protein phosphorylation plays a dominant role in regulating hypometabolism in hibernating Nanorana parkeri

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Zoological Research 2024年第1期45卷 1-12页

作者： Yong-Gang Niu Deng-bang Wei Xue-Jing Zhang Ti-Sen Xu Xiang-Yong Li Hai-Ying Zhang Zhi-Fang An kenneth b.storey Qiang Chen Department of Life Sciences Dezhou UniversityDezhouShandong 253023China State Key Laboratory of Plateau Ecology and Agriculture Qinghai UniversityXiningQinghai 810016China School of Life Sciences Lanzhou UniversityLanzhouGansu 730000China Department of biology Carleton UniversityOttawaON K1S 5B6Canada

Changes in protein abundance and reversible protein phosphorylation(RPP)play important roles in regulating hypometabolism but have never been documented in overwintering frogs at high altitudes.To test the hypothesis that protein abundance and phosphorylation change in response to winter hibernation,we conducted a comprehensive and quantitative proteomic and phosphoproteomic analysis of the liver of the Xizang plateau frog,Nanorana parkeri,living on the Qinghai-Xizang Plateau.In total,5170 proteins and 5695 phosphorylation sites in 1938 proteins were quantified.based on proteomic analysis,674 differentially expressed proteins(438 up-regulated,236 down-regulated)were screened in hibernating N.parkeri versus summer individuals.Functional enrichment analysis revealed that higher expressed proteins in winter were significantly enriched in immune-related signaling pathways,whereas lower expressed proteins were mainly involved in metabolic processes.A total of 4251 modified sites(4147 up-regulated,104 down-regulated)belonging to 1638 phosphoproteins(1555 up-regulated,83 down-regulated)were significantly changed in the liver.During hibernation,RPP regulated a diverse array of proteins involved in multiple functions,including metabolic enzymatic activity,ion transport,protein turnover,signal transduction,and alternative splicing.These changes contribute to enhancing protection,suppressing energy-consuming processes,and inducing metabolic depression.Moreover,the activities of phosphofructokinase,glutamate dehydrogenase,and ATPase were all significantly lower in winter compared to summer.In conclusion,our results support the hypothesis and demonstrate the importance of RPP as a regulatory mechanism when animals transition into a hypometabolic state.

关键词： Nanorana parkeri Proteomic Phosphoproteomic Hibernation Reversible protein phosphorylation Metabolism

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The Gray Mouse Lemur: A Model for Studies of Primate Metabolic Rate Depression

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Genomics, Proteomics & bioinformatics 2015年第2期13卷 77-80页

作者： kenneth b.storey Institute of biochemistry and Department of biology Carleton University

The use of daily torpor and/or of multi-day torpor bouts during a hibernation season are energy-saving survival strategies that have been well-studied for many years,particularly for small mammals living in seasonally... 详细信息

关键词： Depression physiological suppression season environments Mouse perfusion intestine winter breeding

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The emerging roles of microRNAs in the molecular responses of metabolic rate depression

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分子细胞生物学报:英文版 2011年第3期3卷 167-175页

作者： Kyle K.biggar kenneth b.storey Institute of biochemistry and Department of biology Carleton University1125 Colonel By DriveOttawaONCanada K1S 5B6

Metabolic rate depression is an important survival strategy for many animal species and a common element of hibernation,torpor,estivation,anoxia and diapause.Studies of the molecular mechanisms that regulate reversible transitions to and from hypometabolic states have identified principles of regulatory control.These control mechanisms are conserved among biologically diverse organisms and include the coordinated reduction of specific groups of key regulatory enzymes or proteins in the cell,a process likely driven by microRNA target repression/degradation.The present review focuses on a growing area of research in hypometabolism and mechanisms involving the rapid and reversible control of translation facilitated by microRNAs.The analysis draws primarily from current research on three animal models:hibernating mammals,anoxic turtles and freeze-tolerant frogs(with selected examples from multiple other sources).Here,we demonstrate a link between metabolic rate depression,a well-documented response to periods of environmental stress,and microRNA expression.Microarray-based expression profiles and PCR-driven studies have revealed that specific microRNAs are induced in response to environmental stress.Selected members of this group decrease pro-apoptotic signaling,reduce muscle wasting and reduce protein translation,whereas other members contribute to cell cycle arrest and mitogen-activated protein kinase signaling.Many of the same microRNAs are frequently deregulated in numerous disease pathologies and,hence,the hypometabolism model could provide a novel approach for the treatment of stroke and heart attack in humans.

关键词： microRNA metabolism metabolic rate depression protein translation muscle atrophy cell cycle apoptosis

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Regrowth and neuronal protection are key for mammalian hibernation:roles for metabolic suppression

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Neural Regeneration Research 2020年第11期15卷 2027-2028页

作者： Samantha M.Logan kenneth b.storey Institute of biochemistry Departments of Biology and ChemistryCarleton UniversityOttawaONCanada

Thought experiment:you're starving,huddled in the fetal position in a hole in the ground,with no sense of the world around you,except that you are really,really cold.In fact,your internal temperature can go as low as... 详细信息

关键词： really fetal suppression

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Cytokine and Antioxidant Regulation in the Intestine of the Gray Mouse Lemur (Microcebus murinus) During Torpor

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Genomics, Proteomics & bioinformatics 2015年第2期13卷 127-135页

作者： Shannon N.Tessier barbara A.Katzenback Fabien Pifferi Martine Perret kenneth b.storey Institute of biochemistry & Department of biology Carleton University Department of Surgery & Center for Engineering in Medicine Massachusetts General Hospital & Harvard Medical School Department of biology University of Waterloo UMR 7179 Centre National de la Recherche Scientifique Muse'um National d'Histoire Naturelle

During food shortages, the gray mouse lemur（Microcebus murinus） of Madagascar experiences daily torpor thereby reducing energy expenditures. The present study aimed to understand the impacts of torpor on the immune system and antioxidant response in the gut of these animals.This interaction may be of critical importance given the trade-off between the energetically costly immune response and the need to defend against pathogen entry during hypometabolism. The protein levels of cytokines and antioxidants were measured in the small intestine（duodenum, jejunum,and ileum） and large intestine of aroused and torpid lemurs. While there was a significant decrease of some pro-inflammatory cytokines（IL-6 and TNF-a） in the duodenum and jejunum during torpor as compared to aroused animals, there was no change in anti-inflammatory cytokines. We observed decreased levels of cytokines（IL-12p70 and M-CSF）, and several chemokines（MCP-1and MIP-2） but an increase in MIP-1a in the jejunum of the torpid animals. In addition, we evaluated antioxidant response by examining the protein levels of antioxidant enzymes and total antioxidant capacity provided by metabolites such as glutathione（and others）. Our results indicatedthat levels of antioxidant enzymes did not change between torpor and aroused states, although antioxidant capacity was significantly higher in the ileum during torpor. These data suggest a suppression of the immune response, likely as an energy conservation measure, and a limited role of antioxidant defenses in supporting torpor in lemur intestine.

关键词： Primate torpor Cytokines Chemokines Antioxidant enzymes Gut immunology

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Expression Profiling and Structural Characterization of Micro RNAs in Adipose Tissues of Hibernating Ground Squirrels

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Genomics, Proteomics & bioinformatics 2014年第6期12卷 284-291页

作者： Cheng-Wei Wu Kyle K.biggar kenneth b.storey Department of biology Carleton University biochemistry Department Schulich School of Medicine and DentistryWestern University

Micro RNAs（mi RNAs） are small non-coding RNAs that are important in regulating metabolic stress. In this study, we determined the expression and structural characteristics of 20 mi RNAs in brown（bAT） and white adipose tissue（WAT） during torpor in thirteen-lined ground squirrels. Using a modified stem-loop technique, we found that during torpor, expression of six mi RNAs including let-7a, let-7b, mi R-107, mi R-150, mi R-222 and mi R-31 was significantly downregulated in WAT（P 〈 0.05）, which was 16%–54% of euthermic non-torpid control squirrels,whereas expression of three mi RNAs including mi R-143, mi R-200 a and mi R-519 d was found to be upregulated by 1.32–2.34-fold. Similarly, expression of more mi RNAs was downregulated in bAT during torpor. We detected reduced expression of 6 mi RNAs including mi R-103 a, mi R-107, mi R-125 b, mi R-21, mi R-221 and mi R-31（48%–70% of control）, while only expression of mi R-138 was significantly upregulated（2.91 ± 0.8-fold of the control, P 〈 0.05）. Interestingly,mi RNAs found to be downregulated in WAT during torpor were similar to those dysregulated in obese humans for increased adipogenesis, whereas mi RNAs with altered expression in bAT during torpor were linked to mitochondrial b-oxidation. mi RPath target prediction analysis showed that mi RNAs downregulated in both WAT and bAT were associated with the regulation of mitogen-activated protein kinase（MAPK） signaling, while the mi RNAs upregulated in WAT were linked to transforming growth factor b（TGFb） signaling. Compared to mouse sequences, no unique nucleotide substitutions within the stem-loop region were discovered for the associated pre-mi RNAs for the mi RNAs used in this study, suggesting no structure-influenced changes in pre-mi RNA processing efficiency in the squirrel. As well, the expression of mi RNA processingenzyme Dicer remained unchanged in both tissues during torpor. Overall, our findings suggest that changes of mi RNA expression in adipose tissues may be linked to distinct biological roles in WAT and bA

关键词： Non-coding RNA Dicer Ground squirrel Stress adaptation Hypometabolism

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Differential Expression of Mature MicroRNAs Involved in Muscle Maintenance of Hibernating Little brown bats, Myotis lucifugus: A Model of Muscle Atrophy Resistance

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Genomics, Proteomics & bioinformatics 2012年第5期10卷 295-301页

作者： Samantha F.Kornfeld Kyle K.biggar kenneth b.storey Institute of biochemistry&Department of biology Carleton University

Muscle wasting is common in mammals during extended periods of immobility. However, many small hibernating mammals manage to avoid muscle atrophy despite remaining stationary for long periods during hibernation. Recent research has highlighted roles for short non-coding microRNAs （miRNAs） in the regulation of stress tolerance. We proposed that they could also play an important role in muscle maintenance during hibernation. To explore this possibility, a group of 10 miRNAs known to be normally expressed in skeletal muscle of non-hibernating mammals were analyzed by RT-PCR in hibernating little brown bats, Myotis lucifugus. We then compared the expression of these miRNAs in euthermic control bats and bats in torpor. Our results showed that compared to euthermic controls, sig- nificant, albeit modest （1.2-1.6 fold）, increases in transcript expression were observed for eight mature miRNAs, including miR-la-1, miR-29b, miR-181b, miR-15a, miR-20a, miR-206 and miR-128-1, in the pectoral muscle of torpid bats. Conversely, expression of miR-21 decreased by 80% during torpor, while expression of miR-107 remained unaffected. Interestingly, these miRNAs have been either validated or predicted to affect multiple muscle-specific factors, including myostatin, FoxO3a, HDAC4 and SMADT, and are likely involved in the preservation of pectoral muscle mass and functionality during bat hibernation.

关键词： MlicroRNA Hibernation Metabolic rate depression Atrophy Dicer Myostatin

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MicroRNA Regulation in Extreme Environments: Differential Expression of MicroRNAs in the Intertidal Snail Littorina littorea During Extended Periods of Freezing and Anoxia

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Genomics, Proteomics & bioinformatics 2012年第5期10卷 302-309页

作者： Kyle K.biggar Samantha F.Kornfeld Yulia Maistrovski kenneth b.storey Institute of biochemistry&Department of biology Carleton University

Several recent studies of vertebrate adaptation to environmental stress have suggested roles for microRNAs （miRNAs） in regulating glo- bal suppression of protein synthesis and/or restructuring protein expression patterns. The present study is the first to characterize stress- responsive alterations in the expression of miRNAs during natural freezing or anoxia exposures in an invertebrate species, the intertidal gastropod Littorina littorea. These snails are exposed to anoxia and freezing conditions as their environment constantly fluctuates on both a tidal and seasonal basis. The expression of selected miRNAs that are known to influence the cell cycle, cellular signaling pathways, carbohydrate metabolism and apoptosis was evaluated using RT-PCR. Compared to controls, significant changes in expression were observed for miR-la-1, miR-34a and miR-29b in hepatopancreas and for miR-la-1, miR-34a, miR-133a, miR-125b, miR-29b and miR-2a in foot muscle after freezing exposure at -6 ~C for 24 h （P 〈 0.05）. In addition, in response to anoxia stress for 24 h, significant changes in expression were also observed for miR-la-1, miR-210 and miR-29b in hepatopancreas and for miR-1 a-1, miR-34a, miR-133a, miR-29b and miR-2a in foot muscle （P 〈 0.05）. Moreover, protein expression of Dicer, an enzyme responsible for mature microRNA processing, was increased in foot muscle during freezing and anoxia and in hepatopancreas during freezing. Alterations in expression of these miRNAs in L. littorea tissues may contribute to organismal survival under freezing and anoxia.

关键词： Freeze tolerance Anaerobiosis Metabolic rate depression Periwinkle Marine mollusk

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Modulation of Gene Expression in Key Survival Pathways During Daily Torpor in the Gray Mouse Lemur, Microcebus murinus

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Genomics, Proteomics & bioinformatics 2015年第2期13卷 111-118页

作者： Kyle K.biggar Cheng-Wei Wu Shannon N.Tessier Jing Zhang Fabien Pifferi Martine Perret kenneth b.storey Institute of biochemistry & Department of biology Carleton University biochemistry Department Schulich School of Medicine and Dentistry Western University Department of biology Genetics Institute University of Florida Department of Surgery & Center for Engineering in Medicine Massachusetts General Hospital & Harvard Medical School Chemistry and Chemical Engineering Department Royal Military College of Canada UMR 7179 Centre National de la Recherche Scientifique Muse'um National d'Histoire Naturelle

A variety of mammals employ torpor as an energy-saving strategy in environments of marginal or severe stress either on a daily basis during their inactive period or on a seasonal basis during prolonged multi-day hibernation. Recently, a few Madagascar lemur species have been identified as the only primates that exhibit torpor; one of these is the gray mouse lemur（Microcebus murinus）. To explore the regulatory mechanisms that underlie daily torpor in a primate, we analyzed the expression of 28 selected genes that represent crucial survival pathways known to be involved in squirrel and bat hibernation. Array-based real-time PCR was used to compare gene expression in control（aroused） versus torpid lemurs in five tissues including the liver, kidney,skeletal muscle, heart, and brown adipose tissue. Significant differences in gene expression during torpor were revealed among genes involved in glycolysis, fatty acid metabolism, antioxidant defense, apoptosis, hypoxia signaling, and protein protection. The results showed upregulation of select genes primarily in liver and brown adipose tissue. For instance, both tissues showed elevated gene expression of peroxisome proliferator activated receptor gamma（ppargc）, ferritin（fth1）, and protein chaperones during torpor. Overall, the data show that the expression of only a few genes changed during lemur daily torpor, as compared with the broader expression changes reported for hibernation in ground squirrels. These results provide an indication that the alterations in gene expression required for torpor in lemurs are not as extensive as those needed for winter hibernation in squirrel models. However, identification of crucial genes with altered expression that support lemur torpor provides key targets to be explored and manipulated toward a goal of translational applications of inducible torpor as a treatment option in human biomedicine.

关键词： Daily torpor Primate hypometabolism PPAR gamma coactivator Ferritin Chaperone proteins

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Regulation of Torpor in the Gray Mouse Lemur:Transcriptional and Translational Controls and Role of AMPK Signaling

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Genomics, Proteomics & bioinformatics 2015年第2期13卷 103-110页

作者： Jing Zhang Shannon N.Tessier Kyle K.biggar Cheng-Wei Wu Fabien Pifferi Martine Perret kenneth b.storey Institute of biochemistry & Department of biology Carleton University Chemistry and Chemical Engineering Department Royal Military College of Canada Department of Surgery & Center for Engineering in Medicine Massachusetts General Hospital & Harvard Medical School biochemistry Department Schulich School of Medicine and Dentistry Western University Department of biology Genetics Institute University of Florida UMR 7179 Centre National de la Recherche Scientifique Muse'um National d'Histoire Naturelle

The gray mouse lemur（Microcebus murinus） is one of few primate species that is able to enter daily torpor or prolonged hibernation in response to environmental stresses. With an emerging significance to human health research, lemurs present an optimal model for exploring molecular adaptations that regulate primate hypometabolism. A fundamental challenge is how to effectively regulate energy expensive cellular processes（e.g., transcription and translation） during transitionsto/from torpor without disrupting cellular homeostasis. One such regulatory mechanism is reversible posttranslational modification of selected protein targets that offers fine cellular control without the energetic burden. This study investigates the role of phosphorylation and/or acetylation in regulating key factors involved in energy homeostasis（AMP-activated protein kinase, or AMPK, signaling pathway）, m RNA translation（eukaryotic initiation factor 2a or e IF2 a, eukaryotic initiation factor 4E or e IF4 E, and initiation factor 4E binding protein or 4EbP）, and gene transcription（histone H3） in six tissues of torpid and aroused gray mouse lemurs. Our results indicated selective tissue-specific changes of these regulatory proteins. The relative level of Thr172-phosphorylated AMPKa was significantly elevated in the heart but reduced in brown adipose tissue during daily torpor, as compared to the aroused lemurs, implicating the regulation of AMPK activity during daily torpor in these tissues. Interestingly, the levels of the phosphorylated e IFs were largely unaltered between aroused and torpid animals. Phosphorylation and acetylation of histone H3 were examined as a marker for transcriptional regulation. Compared to the aroused lemurs, level of Ser10-phosphorylated histone H3 decreased significantly in white adipose tissue during torpor, suggesting global suppression of gene transcription. However, a significant increase in acetyl-histone H3 in the heart of torpid lemurs indicated a possible stimulation of transcriptional activity of this tiss

关键词： Posttranslational modification Histone H3 Ribosomal initiation factorsMetabolic rate depression AMP-activated protein kinase

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