Depression of transcription and translation during daily torpor in the Djungarian hamster (Phodopus sungorus)

During daily torpor, Djungarian hamsters reduce their metabolic rate by more than 70% below their resting metabolic rate for several hours per day. We investigated whether this depression of metabolism is associated with a reduction in transcription and translation. Liver tissue was sampled in defined metabolic states: during normometabolism, in the torpid state and after arousal from torpor. Nuclei were isolated from liver tissue and subjected to nuclear run-on assays at an assay temperature of 25 °C. We observed a ~40% decrease in transcriptional initiation in liver nuclei of hamsters which had attained minimal metabolic rate during torpor as compared to nuclei from normometabolic hamsters. During arousal from torpor, the transcriptional run-on activity recovered to the normometabolic level. Polysome profile analysis of liver tissue was used to determine the proportion of actively translating polysomes. Profiles of liver samples from torpid animals show a disaggregation of polysomes compared to profiles from normometabolic hamsters, which indicates that, in addition to transcription, protein synthesis decreases during torpor. These results indicate that during torpor a specific inhibition of the energetically costly processes of RNA and protein synthesis contributes to the overall metabolic depression.

[1]  M. Katze,et al.  Molecular Mechanisms Responsible for Malignant Transformation by Regulatory and Catalytic Domain Variants of the Interferon-induced Enzyme RNA-dependent Protein Kinase (*) , 1995, The Journal of Biological Chemistry.

[2]  F. Geiser,et al.  Reduction of metabolism during hibernation and daily torpor in mammals and birds: temperature effect or physiological inhibition? , 2004, Journal of Comparative Physiology B.

[3]  Sandra L. Martin,et al.  Translational initiation is uncoupled from elongation at 18°C during mammalian hibernation , 2001 .

[4]  G. Heldmaier,et al.  Photoperiod and Thermoregulation in Vertebrates: Body Temperature Rhythms and Thermogenic Acclimation , 1989, Journal of biological rhythms.

[5]  G. Heldmaier,et al.  Body temperature and metabolic rate during natural hypothermia in endotherms , 2004, Journal of Comparative Physiology B.

[6]  K. Storey,et al.  Metabolic Rate Depression and Biochemical Adaptation in Anaerobiosis, Hibernation and Estivation , 1990, The Quarterly Review of Biology.

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

[8]  G. Heldmaier,et al.  Role of Photoperiod During Seasonal Acclimation in Winter-Active Small Mammals , 2003 .

[9]  James E. Darnell,et al.  The definition of a large viral transcription unit late in Ad2 infection of HeLa cells: Mapping of nascent RNA molecular labeled in isolated nuclei , 1977, Cell.

[10]  J. Goodman,et al.  RNA synthesis and RNA polymerase activity in hepatic nuclei isolated from rats fed the carcinogen 2-acetylaminofluorene. , 1976, Biochemical and biophysical research communications.

[11]  G. Brown,et al.  Cellular energy utilization and molecular origin of standard metabolic rate in mammals. , 1997, Physiological reviews.

[12]  B. K. Whitten,et al.  Protein metabolism in hepatic tissue of hibernating and arousing ground squirrels. , 1968, The American journal of physiology.

[13]  B. L. Jones,et al.  Use of monoclonal antibodies to study the structure and function of eukaryotic protein synthesis initiation factor eIF-2B. , 1994, European journal of biochemistry.

[14]  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.

[15]  J. R. Nestler,et al.  Relationships between body temperature, thermal conductance,Q10 and energy metabolism during daily torpor and hibernation in rodents , 2004, Journal of Comparative Physiology B.

[16]  R. Capparelli,et al.  DNA content differences in laboratory mouse strains determined by flow cytometry. , 1997, Cytometry.

[17]  K. Storey,et al.  Metabolic adjustments during daily torpor in the Djungarian hamster. , 1999, The American journal of physiology.

[18]  K. Storey,et al.  Metabolic regulation in mammalian hibernation: enzyme and protein adaptations. , 1997, Comparative biochemistry and physiology. Part A, Physiology.

[19]  S. Martin,et al.  Reversible depression of transcription during hibernation , 2002, Journal of Comparative Physiology B.

[20]  V. I. Grischenko,et al.  Peculiarities of functioning of protein-synthesizing apparatus of the hibernator (Citellus undulatus). , 1992, Cryobiology.

[21]  K. Seifart,et al.  Synthesis of ribosomal 5S RNA by isolated nuclei from HeLa cells in vitro. , 1977, Biochemistry.

[22]  G. Heldmaier,et al.  Seasonal pattern and energetics of short daily torpor in the Djungarian hamster, Phodopus sungorus , 1981, Oecologia.