Abstract
Djungarian hamsters are able to use spontaneous daily torpor (SDT) during the winter season as well as fasting-induced torpor (FIT) at any time of the year to cope with energetically challenging environmental conditions. Torpor is a state of severely reduced metabolism with a pronounced decrease in body temperature, which enables animals to decrease their individual energy requirements. Despite sharing common characteristics, such as reduced body mass before first torpor expression and depressed metabolism and body temperature during the torpid state, FIT and SDT differ in several physiological properties including torpor bout duration, minimal body temperature, fuel utilization and circadian organization. It remains unclear, whether SDT and FIT reflect the same phenomenon or two different physiological states. The hypothalamus has been suggested to play a key role in regulating energy balance and torpor. To uncover differences in molecular control mechanisms of torpor expression, we set out to investigate hypothalamic gene expression profiles of genes related to orexigenic (Agrp/Npy), circadian clock (Bmal1/Per1) and thyroid hormone (Dio2/Mct8) systems of animals undergoing SDT and FIT during different torpor stages. Orexigenic genes were mainly regulated during FIT and remained largely unaffected by SDT. Expression patterns of clock genes showed disturbed circadian clock rhythmicity in animals undergoing FIT, but not in animals undergoing SDT. During both, SDT and FIT, decreased Dio2 expression was detected, indicating reduced hypothalamic T3 availability in both types of torpor. Taken together, our results provide evidence that SDT and FIT also differ in certain central control mechanisms and support the observation that animals undergoing SDT are in energetical balance, whereas animals undergoing FIT display a negative energy balance. This should be carefully taken into account when interpreting data in torpor research, especially from animal models of fasting-induced hypometabolism such as mice.
Highlights
The use of torpor in times of energetically challenging environmental conditions is a common strategy, which has been identified in most orders of mammals
We investigated differences between spontaneous daily torpor and fastinginduced torpor on the physiological and molecular levels in the Djungarian hamster
fasting-induced torpor (FIT)-long day conditions (LD) bouts differed from spontaneous daily torpor (SDT) in depth and duration
Summary
The use of torpor in times of energetically challenging environmental conditions is a common strategy, which has been identified in most orders of mammals. Reduction of metabolic rate and body temperature (Tb), the two main characteristics of torpor, enable the animal to reduce energy expenditure and lower energy requirements with almost no evidence of tissue or organ damage after rewarming from the torpid state [1,2,3,4,5,6,7]. The Djungarian hamster (Phodopus sungorus, known as Siberian hamster) uses spontaneous daily torpor (SDT) to save energy during the harsh winters of Central Asian steppes. SDT in Djungarian hamsters is the final trait of various adaptions (severe body weight loss, molt to white winter fur, gonadal regression) to the winter season [8,9]. When SDT is used frequently, Djungarian hamsters are able to save up to 65% of total energy requirements during the winter season [15]
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