Daily Torpor Alters Multiple Gene Expression in the Suprachiasmatic Nucleus and Pineal Gland of the Djungarian Hamster (Phodopus sungorus)

Circadian rhythms are still expressed in animals that display daily torpor, implying a temperature compensation of the pacemaker. Nevertheless, it remains unclear how the clock works in hypothermic states and whether torpor itself, as a temperature pulse, affects the circadian system. To reveal changes in the clockwork during torpor, we compared clock gene and neuropeptide expression by in situ hybridization in the suprachiasmatic nucleus (SCN) and pineal gland of normothermic and torpid Djungarian hamsters (Phodopus sungorus). Animals from light‐dark (LD) 8∶16 were sacrificed at 8 time points throughout 24 h. To investigate the effect of a previous torpor episode on the clock, we sacrificed a group of normothermic hamsters 1 day after torpor. In normothermic animals, Per1 peaked at zeitgeber time (ZT)4; whereas, Bmal1 reached maximal expression between ZT16 and ZT19. AVP mRNA in the SCN showed highest levels at ZT7. On the day of torpor, the levels of all mRNAs investigated, except for AVP mRNA, were increased during the torpor bout. Moreover, the Bmal1 rhythm was advanced. On the day after the hypothermia, Bmal1 and AVP rhythms showed severely depressed amplitude. Those distinct amplitude changes of Bmal1 and AVP on the day after a torpor episode expression suggests that torpor affects the circadian system, probably by altered translational processes that might lead to a modified protein feedback on gene expression. In the pineal gland, an important clock output, Aanat expression, peaked between ZT16 and ZT22 in normothermic animals. Aanat levels were significantly advanced on the day of hypothermia, an effect which was still visible 1 day afterward. In summary, this study showed that daily torpor affects the phase and amplitude of rhythmic clock gene and clock‐controlled gene expression in the SCN. Furthermore, the rhythmic gene expression in a peripheral oscillator, the pineal gland, is also affected.

[1]  I. Zucker,et al.  Torpor shortens the period of Siberian hamster circadian rhythms. , 1993, The American journal of physiology.

[2]  I. Zucker,et al.  Melatonin Production Accompanies Arousal from Daily Torpor in Siberian Hamsters , 2003, Physiological and Biochemical Zoology.

[3]  P. Pévet,et al.  Daily torpor in the Djungarian hamster (Phodopus sungorus): photoperiodic regulation, characteristics and circadian organization , 2004, Journal of Comparative Physiology A.

[4]  A. R. French Periodicity of recurrent hypothermia during hibernation in the pocket mouse,Perognathus longimembris , 2004, Journal of comparative physiology.

[5]  J. Aschoff,et al.  Circadian rhythms: influences of internal and external factors on the period measured in constant conditions. , 2010 .

[6]  C. Graff,et al.  Feeding Cues Alter Clock Gene Oscillations and Photic Responses in the Suprachiasmatic Nuclei of Mice Exposed to a Light/Dark Cycle , 2005, The Journal of Neuroscience.

[7]  I. Zucker,et al.  Daily torpor in the absence of the suprachiasmatic nucleus in Siberian hamsters. , 1992, The American journal of physiology.

[8]  C S Pittendrigh,et al.  ON TEMPERATURE INDEPENDENCE IN THE CLOCK SYSTEM CONTROLLING EMERGENCE TIME IN DROSOPHILA. , 1954, Proceedings of the National Academy of Sciences of the United States of America.

[9]  J. Knight,et al.  mRNA Stability and Polysome Loss in Hibernating Arctic Ground Squirrels (Spermophilus parryii) , 2000, Molecular and Cellular Biology.

[10]  U. Albrecht,et al.  Robust Circadian Rhythmicity of Per1 and Per2 Mutant Mice in Constant Light, and Dynamics of Per1 and Per2 Gene Expression under Long and Short Photoperiods , 2002, Journal of biological rhythms.

[11]  J. W. Hastings,et al.  Effects of temperature upon diurnal rhythms. , 1960, Cold Spring Harbor symposia on quantitative biology.

[12]  P. Pévet,et al.  Photoperiod differentially regulates clock genes’ expression in the suprachiasmatic nucleus of Syrian hamster , 2003, Neuroscience.

[13]  A. Loudon,et al.  Photoperiod Differentially Regulates Circadian Oscillators in Central and Peripheral Tissues of the Syrian Hamster , 2003, Current Biology.

[14]  T. Bartness,et al.  Mammalian pineal melatonin: A clock for all seasons , 1989, Experientia.

[15]  E. Maywood,et al.  Regional Distribution of Iodomelatonin Binding Sites within the Suprachiasmatic Nucleus of the Syrian Hamster and the Siberian Hamster , 1995, Journal of neuroendocrinology.

[16]  I. Zucker,et al.  Temperature Dependence of Circadian Rhythms in Golden-Mantled Ground Squirrels , 1990, Journal of biological rhythms.

[17]  P. Pévet The role of the pineal gland in the photoperiodic control of reproduction in different hamster species. , 1988, Reproduction, nutrition, developpement.

[18]  L. Rensing,et al.  Ethical Principles and Standards for the Conduct of Human and Animal Biological Rhythm Research , 2004, Chronobiology international.

[19]  A. Kalsbeek,et al.  Interindividual differences in the pattern of melatonin secretion of the Wistar rat , 1999, Journal of pineal research.

[20]  B. Goldman Mammalian Photoperiodic System: Formal Properties and Neuroendocrine Mechanisms of Photoperiodic Time Measurement , 2001, Journal of biological rhythms.

[21]  G. Krause,et al.  Suppression of protein synthesis in brain during hibernation involves inhibition of protein initiation and elongation. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Hastings Jw,et al.  Effects of Temperature upon Diurnal Rhythms , 1960 .

[23]  G. Heldmaier,et al.  Photoperiodic control and effects of melatonin on nonshivering thermogenesis and brown adipose tissue. , 1981, Science.

[24]  G. Heldmaier,et al.  Reduced locomotor activity following daily torpor in the djungarian hamster: recovery from hypothermia? , 1992, Naturwissenschaften.

[25]  J. Vanecek,et al.  Effect of photoperiod and of one minute light at night-time on the pineal rhythm on N-acetyltransferase activity in the Djungarian hamster Phodopus sungorus. , 1981, Biology of reproduction.

[26]  H. Heller,et al.  Circadian Rhythms in the Suprachiasmatic Nucleus are Temperature-Compensated and Phase-Shifted by Heat Pulses In Vitro , 1999, The Journal of Neuroscience.

[27]  M. Sládek,et al.  Clock Gene Daily Profiles and Their Phase Relationship in the Rat Suprachiasmatic Nucleus Are Affected by Photoperiod , 2003, Journal of biological rhythms.

[28]  D. Hazlerigg,et al.  Photoperiod regulates multiple gene expression in the suprachiasmatic nuclei and pars tuberalis of the Siberian hamster (Phodopus sungorus) , 2005, The European journal of neuroscience.