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The Mechanism Enabling Hibernation in Mammals 3 The Mechanism Enabling Hibernation in Mammals 3 Yuuki Horii, Takahiko Shiina, and Yasutake Shimizu Abstract (CIRP) in the hearts of hibernating hamsters. Some rodents including squirrels and ham- The CIRP mRNA is constitutively expressed sters undergo hibernation. During hibernation, in the heart of a nonhibernating euthermic body temperature drops to only a few degrees hamster with several different forms probably above ambient temperature. The suppression due to alternative splicing. The short product of whole-body energy expenditure is associ- contained the complete open reading frame ated with regulated, but not passive, reduction for full-length CIRP, while the long product of cellular metabolism. The heart retains the had inserted sequences containing a stop ability to beat constantly, although body tem- codon, suggesting production of a C-terminal perature drops to less than 10 °C during hiber- deletion isoform of CIRP. In contrast to nonhi- nation. Cardiac myocytes of hibernating bernating hamsters, only the short product mammals are characterized by reduced Ca2+ was found in hibernating animals. Thus, these entry into the cell membrane and a concomi- results indicate that CIRP expression in the tant enhancement of Ca2+ release from and hamster heart is regulated at the level of alter- reuptake by the sarcoplasmic reticulum. These native splicing, which would permit a rapid adaptive changes would help in preventing increment of functional CIRP when entering excessive Ca2+ entry and its overload and in hibernation. We will summarize the current maintaining the resting levels of intracellular understanding of the cold-resistant property of Ca2+. Adaptive changes in gene expression in the heart in hibernating animals. the heart prior to hibernation may be indis- pensable for acquiring cold resistance. In Keywords addition, protective effects of cold-shock pro- Hibernation · Cold-shock protein · teins are thought to have an important role. We Hypothermia recently reported the unique expression pat- tern of cold-inducible RNA-binding protein Abbreviations Y. Horii · T. Shiina · Y. Shimizu (*) CIRP Cold-inducing RNA-binding protein Department of Basic Veterinary Science, Laboratory CNS The central nervous system of Physiology, The United Graduate School of Veterinary Sciences, Gifu University, Gifu, Japan ECG Electrocardiograms e-mail: [email protected] HNF Hepatocyte nuclear factor © Springer Nature Singapore Pte Ltd. 2018 45 M. Iwaya-Inoue et al. (eds.), Survival Strategies in Extreme Cold and Desiccation, Advances in Experimental Medicine and Biology 1081, https://doi.org/10.1007/978-981-13-1244-1_3 46 Y. Horii et al. HP Hibernation-specific protein Table 3.1 Hibernating mammals ICV Intracerebroventricular Body RBM3 RNA-binding motif 3 temperature in SERCA2 asarco(endo)plasmic reticulum Ca2+- hibernation Order Species (°C) ATPase 2a Monotremata Echidna 4 Marsupialia Pygmy possum, 1.3–7.1 feathertail glider, Chiloe opossum 3.1 Hibernation of Mammals Eulipotyphla Hedgehog 1–9.7 Afrosoricida Tenrec 8.6–15 Chiroptera Bat Most mammals have the ability to maintain their −2 to 13.9 Primates Lemur 6.5–9.3 body temperature within a narrow range even in a Carnivora Badger, bear 28–32.5 cold environment. In a cold environment, ther- Rodentia Prairie dog, marmot, −2.9 to 15 moregulatory responses to minimize heat loss woodchuck, ground (e.g., peripheral vasoconstriction and piloerec- squirrel, chipmunk, tion) are evoked (Tansey and Johnson 2015). In pocket mouse, kangaroo mouse, addition, heat-producing responses in skeletal hamster, jerboa, muscles (shivering thermogenesis) and in brown dormouse adipose tissue (non-shivering or metabolic ther- Ruf and Geiser (2015) mogenesis) are activated, and thereby a drop in body temperature is prevented (Tansey and Johnson 2015). If the body temperature of homo- contrast, mammalian hibernators possess a ther- therms drops extremely, they cannot survive moregulatory mechanism similar to that of non- because the heart cannot keep beating, and organs hibernators, and they can control their body fall into ischemia (Ivanov 2000). temperature in a nonhibernating state despite On the other hand, several mammalian species exposure to a wide range of surrounding temper- undergo hibernation (Carey et al. 2003; Ruf and atures (Carey et al. 2003; Ruf and Geiser 2015). Geiser 2015) (see Table 3.1). During hibernation, Even in an extremely cold environment, they do body temperature drops to only a few degrees not necessarily undergo hibernation if enough above ambient temperature (Carey et al. 2003; food is available. Furthermore, mammalian Ruf and Geiser 2015). Hibernating animals stay hibernators do not always continue in a hibernat- unmoving and usually show a curly shape to min- ing condition throughout winter; they sometimes imize heat dissipation from the body surface interrupt hibernation and spontaneously recover (Fig. 3.1). The hypothermic condition of mam- their body temperature even though they are con- malian hibernators is fundamentally different sistently exposed to a cold environment (Carey from that of poikilotherms (amphibians and rep- et al. 2003). This behavior provides further evi- tiles). The body temperature of poikilothermic dence for the notion that hypothermia during animals directly correlates with changes in ambi- mammalian hibernation is actively induced, since ent temperature due to a lack of efficacious passively induced hypothermia may not recover mechanisms for maintaining body temperature unless ambient temperature is increased. Thus, (Jackson and Ultsch 2010; Malan 2014). As a hibernation of mammals is considered to be an result, body temperature drops passively in adaptive strategy to survive in a severe environ- response to a decrease in ambient temperature. In ment during winter. 3 The Mechanism Enabling Hibernation in Mammals 47 Fig. 3.1 Hibernating hamster. Pictures show curly shape that is usually observed during hibernation in Syrian hamsters Fig. 3.2 A schema of body temperature during hibernation 3.2 Variation of Hibernation (Elephantulus myurus) reached 5–10 °C during daily torpor (Mzilikazi et al. 2002). Some species During hibernation, the degree of body tempera- including tenrec and mouse lemurs adopt either ture reduction and duration of the hypothermic daily torpor or hibernation depending on the state vary widely among animal species (Carey ambient temperature (Lovegrove and Génin et al. 2003; Ruf and Geiser 2015). In black bears, 2008; Kobbe and Dausmann 2009; Kobbe et al. the body temperature during hibernation is 2011). A typical deep hibernation is character- around 33 °C, which is much higher than that in ized by extended duration of torpor bouts. As small hibernators (Carey et al. 2003; Ruf and shown in Fig. 3.2, the hypothermic state during Geiser 2015). In contrast, the body temperature deep hibernation is interrupted by periods of of arctic ground squirrels drops to as low as arousals to euthermia, so-called interbout arous- −3 °C during hibernation (Barnes 1989). Several als. The duration of torpor bouts is from a few mammalian species undergo daily torpor, in days to up to 5 weeks. The interbout arousals are which duration of the hypothermic state is less maintained for 12–24 h before reentry into torpor than 24 h (Breukelen and Martin 2015). In daily (Carey et al. 2003). The periodic hibernation- torpor, reduction of body temperature is rela- arousal cycles suggest that the central nervous tively moderate compared with that in deep system (CNS) is continuously operated even at a hibernation. Exceptionally, it has been reported low temperature during hibernation. that body temperature of the rock elephant shrew 48 Y. Horii et al. Table 3.2 Physiological parameters in active and hiber- metabolic rate of the hibernating ground squirrel nating hamsters (n = 6) is reduced to less than 5% of that observed in the Active Hibernation Hibernation nonhibernating euthermic counterpart (Wang and control in summer in winter Lee 1996). The suppression of whole-body Body 35.2 ± 0.6 5.0 ± 0.9 5.5 ± 0.3 temperature energy expenditure is associated with regulated, (°C) but not passive, reduction of cellular metabolism. Heart rate 369 ± 13 15.8 ± 3.1 15.0 ± 2.7 It has been demonstrated that a serine/threonine (beats/min) protein kinase, Akt (also known as protein kinase Respiratory 92.2 ± 8.5 2.3 ± 1.7 3.0 ± 1.4 B), is inactivated by dephosphorylation in hiber- rate (breaths/ min) nating animal organs, typically in skeletal mus- cles and the liver (Abnous et al. 2008). Considering that Akt activation plays an impor- It is known that seasonal hibernators, e.g., tant role in anabolic and catabolic responses in Richardson’s ground squirrel (Spermophilus various cells, the dephosphorylation of Akt in richardsonii) and Siberian chipmunk (Tamias hibernating animal cells would be suitable for a sibiricus asiatics), rarely hibernate in summer decrease in metabolic activity. Interestingly, the even if they are placed in a cold condition (Kondo dephosphorylation is promoted immediately 1987). This suggests that the endogenous circan- prior to entering hibernation (Hoehn et al. 2004). nual rhythm plays a critical role in the induction Accordingly, the reduction of cellular metabo- of hibernation in seasonal hibernators. In con- lism during hibernation does not arise as a conse- trast, hamsters hibernated even in summer when quence of lowered temperature (i.e., general they were placed in a condition suitable for suppression of enzyme activity). Rather, cellular induction
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