The Mechanism Enabling Hibernation in Mammals

Horii, Yuuki; Shiina, Takahiko; Shimizu, Yasutake

doi:10.1007/978-981-13-1244-1_3

Cited by 18 publications

(8 citation statements)

References 98 publications

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“…This is in contrast to non-hibernators, in which the heart cannot maintain beating in a deep hypothermic condition [ 126 ]. Therefore, the hearts of hibernating animals would possess a protective mechanism against the harmful effects of a low temperature [ 127 ]. The innate ability of the heart that is specific for hibernators definitely contributes to the cold-resistant nature.…”

Section: Temperature-dependent Regulation Of Alternative Splicing mentioning

confidence: 99%

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Temperature-Dependent Alternative Splicing of Precursor mRNAs and Its Biological Significance: A Review Focused on Post-Transcriptional Regulation of a Cold Shock Protein Gene in Hibernating Mammals

Shiina

Shimizu

2020

IJMS

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Multiple mRNA isoforms are often generated during processing such as alternative splicing of precursor mRNAs (pre-mRNA), resulting in a diversity of generated proteins. Alternative splicing is an essential mechanism for the functional complexity of eukaryotes. Temperature, which is involved in all life activities at various levels, is one of regulatory factors for controlling patterns of alternative splicing. Temperature-dependent alternative splicing is associated with various phenotypes such as flowering and circadian clock in plants and sex determination in poikilothermic animals. In some specific situations, temperature-dependent alternative splicing can be evoked even in homothermal animals. For example, the splicing pattern of mRNA for a cold shock protein, cold-inducible RNA-binding protein (CIRP or CIRBP), is changed in response to a marked drop in body temperature during hibernation of hamsters. In this review, we describe the current knowledge about mechanisms and functions of temperature-dependent alternative splicing in plants and animals. Then we discuss the physiological significance of hypothermia-induced alternative splicing of a cold shock protein gene in hibernating and non-hibernating animals.

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Section: Temperature-dependent Regulation Of Alternative Splicing mentioning

confidence: 99%

“… Post-transcriptional regulation of expression of the CIRP gene by alternative splicing in non-hibernating euthermic and hibernating hypothermic hamsters. The figure was modified from our published article [ 14 , 127 ]. …”

Section: Figurementioning

confidence: 99%

Temperature-Dependent Alternative Splicing of Precursor mRNAs and Its Biological Significance: A Review Focused on Post-Transcriptional Regulation of a Cold Shock Protein Gene in Hibernating Mammals

Shiina

Shimizu

2020

IJMS

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“…In relation to animal size and core body temperature of the hibernating animal, frequency of the heart beat decreases, but remains at a sufficient and constant rate although the body temperature can be low (< 10 °C). This is related to a “reduced Ca 2+ entry into the cell and concomitant enhancement of Ca 2+ release from and reuptake by the sarcoplasmic reticulum” as Horii et al [ 48 ] reviewed. A very recent controlled study on European ground squirrels quantified protein upregulations of antioxidant defense enzymes (e.g., manganese and copper/zinc superoxide dismutases) in the myocardium.…”

Section: Protective Effects Of Hypometabolismmentioning

confidence: 99%

“…A very recent controlled study on European ground squirrels quantified protein upregulations of antioxidant defense enzymes (e.g., manganese and copper/zinc superoxide dismutases) in the myocardium. Those hibernation-related phenotypes of the myocardium are hence characterized by changes in the Ca 2+ homeostasis and strong upregulation of antioxidant enzymes [ 48 , 97 ]. Moreover, unique expression pattern of cold-shock proteins can exert tissue protection during hibernation.…”

Section: Protective Effects Of Hypometabolismmentioning

confidence: 99%

“…Moreover, unique expression pattern of cold-shock proteins can exert tissue protection during hibernation. Cold-inducible RNA-binding proteins, so-called CIRP, have been reported by Horii et al [ 48 ] in the myocardium of hibernating hamsters, showing that CIRP expression in the hamster heart is “regulated at the level of alternative splicing, which would permit a rapid increment of functional CIRP when entering hibernation” [ 48 ]. Interestingly, CIRP also targets cancer-associated mRNAs and can modulate inflammation [ 63 ], which might both be of importance to other organs’ protection during hibernation.…”

Section: Protective Effects Of Hypometabolismmentioning

confidence: 99%

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Hibernating astronauts—science or fiction?

Choukèr

Bereiter‐Hahn

Singer

et al. 2018

Pflugers Arch - Eur J Physiol

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For long-duration manned space missions to Mars and beyond, reduction of astronaut metabolism by torpor, the metabolic state during hibernation of animals, would be a game changer: Water and food intake could be reduced by up to 75% and thus reducing payload of the spacecraft. Metabolic rate reduction in natural torpor is linked to profound changes in biochemical processes, i.e., shift from glycolysis to lipolysis and ketone utilization, intensive but reversible alterations in organs like the brain and kidney, and in heart rate control via Ca 2+. This state would prevent degenerative processes due to organ disuse and increase resistance against radiation defects. Neuro-endocrine factors have been identified as main targets to induce torpor although the exact mechanisms are not known yet. The widespread occurrence of torpor in mammals and examples of human hypometabolic states support the idea of human torpor and its beneficial applications in medicine and space exploration.

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Integrated transcriptomics and metabolomics reveal protective effects on heart of hibernating Daurian ground squirrels

Yang,

Hao,

et al. 2023

Journal Cellular Physiology

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Hibernating mammals are natural models of resistance to ischemia, hypoxia‐reperfusion injury, and hypothermia. Daurian ground squirrels (spermophilus dauricus) can adapt to endure multiple torpor‐arousal cycles without sustaining cardiac damage. However, the molecular regulatory mechanisms that underlie this adaptive response are not yet fully understood. This study investigates morphological, functional, genetic, and metabolic changes that occur in the heart of ground squirrels in three groups: summer active (SA), late torpor (LT), and interbout arousal (IBA). Morphological and functional changes in the heart were measured using hematoxylin‐eosin (HE) staining, Masson staining, echocardiography, and enzyme‐linked immunosorbent assay (ELISA). Results showed significant changes in cardiac function in the LT group as compared with SA or IBA groups, but no irreversible damage occurred. To understand the molecular mechanisms underlying these phenotypic changes, transcriptomic and metabolomic analyses were conducted to assess differential changes in gene expression and metabolite levels in the three groups of ground squirrels, with a focus on GO and KEGG pathway analysis. Transcriptomic analysis showed that differentially expressed genes were involved in the remodeling of cytoskeletal proteins, reduction in protein synthesis, and downregulation of the ubiquitin‐proteasome pathway during hibernation (including LT and IBA groups), as compared with the SA group. Metabolomic analysis revealed increased free amino acids, activation of the glutathione antioxidant system, altered cardiac fatty acid metabolic preferences, and enhanced pentose phosphate pathway activity during hibernation as compared with the SA group. Combining the transcriptomic and metabolomic data, active mitochondrial oxidative phosphorylation and creatine‐phosphocreatine energy shuttle systems were observed, as well as inhibition of ferroptosis signaling pathways during hibernation as compared with the SA group. In conclusion, these results provide new insights into cardio‐protection in hibernators from the perspective of gene and metabolite changes and deepen our understanding of adaptive cardio‐protection mechanisms in mammalian hibernators.

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The Mechanism Enabling Hibernation in Mammals

Cited by 18 publications

References 98 publications

Temperature-Dependent Alternative Splicing of Precursor mRNAs and Its Biological Significance: A Review Focused on Post-Transcriptional Regulation of a Cold Shock Protein Gene in Hibernating Mammals

Temperature-Dependent Alternative Splicing of Precursor mRNAs and Its Biological Significance: A Review Focused on Post-Transcriptional Regulation of a Cold Shock Protein Gene in Hibernating Mammals

Hibernating astronauts—science or fiction?

Integrated transcriptomics and metabolomics reveal protective effects on heart of hibernating Daurian ground squirrels

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