The “hibernation induction trigger”: Specificity and validity of bioassay using the 13-lined ground squirrel

Wang, Lawrence C.H.; Belke, Darrell D.; Jourdan, M.L.; Lee, T.F.; Westly, J.; Nürnberger, F.

doi:10.1016/0011-2240(88)90043-0

Cited by 25 publications

(9 citation statements)

References 10 publications

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“…A subsequent study (295) that employed careful controls found that plasma from hibernating Richardson's ground squirrels induced summer hibernation when infused into thirteen lined ground squirrels, but not when injected into Richardson's ground squirrels. Moreover infusions of saline were at least as effective as hibernating plasma at inducing summer hibernation in thirteen lined ground squirrels (295). Such results do not support the existence a blood-borne HIT, but rather suggest that thirteen lined grounds squirrels are a poor bioassay model for evaluating potential HIT.…”

Section: How Is Torpor Induced?mentioning

confidence: 96%

“…Sometimes, however this induction required several days after infusion while the animals were housed in winter-like, cold and dark conditions (77,244). A subsequent study (295) that employed careful controls found that plasma from hibernating Richardson's ground squirrels induced summer hibernation when infused into thirteen lined ground squirrels, but not when injected into Richardson's ground squirrels. Moreover infusions of saline were at least as effective as hibernating plasma at inducing summer hibernation in thirteen lined ground squirrels (295).…”

Section: How Is Torpor Induced?mentioning

confidence: 96%

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Metabolic Flexibility: Hibernation, Torpor, and Estivation

Staples

2016

Comprehensive Physiology

136

116

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Many environmental conditions can constrain the ability of animals to obtain sufficient food energy, or transform that food energy into useful chemical forms. To survive extended periods under such conditions animals must suppress metabolic rate to conserve energy, water, or oxygen. Amongst small endotherms, this metabolic suppression is accompanied by and, in some cases, facilitated by a decrease in core body temperature-hibernation or daily torpor-though significant metabolic suppression can be achieved even with only modest cooling. Within some ectotherms, winter metabolic suppression exceeds the passive effects of cooling. During dry seasons, estivating ectotherms can reduce metabolism without changes in body temperature, conserving energy reserves, and reducing gas exchange and its inevitable loss of water vapor. This overview explores the similarities and differences of metabolic suppression among these states within adult animals (excluding developmental diapause), and integrates levels of organization from the whole animal to the genome, where possible. Several similarities among these states are highlighted, including patterns and regulation of metabolic balance, fuel use, and mitochondrial metabolism. Differences among models are also apparent, particularly in whether the metabolic suppression is intrinsic to the tissue or depends on the whole-animal response. While in these hypometabolic states, tissues from many animals are tolerant of hypoxia/anoxia, ischemia/reperfusion, and disuse. These natural models may, therefore, serve as valuable and instructive models for biomedical research.

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Section: How Is Torpor Induced?mentioning

confidence: 96%

Section: How Is Torpor Induced?mentioning

confidence: 96%

Metabolic Flexibility: Hibernation, Torpor, and Estivation

Staples

2016

Comprehensive Physiology

136

116

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“…3 will clarify how complex adaptive behaviors arise during evolution. In addition, it may be possible to work backwards from the hibernationinduced differential expression of liver genes, such as that of a2-macroglobulin, demonstrated here, to the putative master controller-i.e., the elusive (27,28) trigger molecule (29)--of hibernation.…”

Section: Resultsmentioning

confidence: 99%

Central role for differential gene expression in mammalian hibernation.

Srere

Wang

Martin

1992

Proc. Natl. Acad. Sci. U.S.A.

144

105

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Mammalian hibernators experience dramatic reductions in body temperature, metabolic rate, respiratory rate, and heart rate during hibernation. These changes are precisely controlled and reversible with only internally driven mechanisms, suggesting specific biochemical regulation. We present a model that integrates our observations of differential liver gene expression during preparation for, and maintenance of, the hibernating state, with the known phylogenetic interspersion of hibernating species in several major mammalian lineages. This model predicts a major role for the differential expression of existing mammalian genes in the biochemical regulation of hibernation.Hibernation is an adaptive strategy that is used by species in several mammalian orders to conserve energy in cold or inhospitable environments. During hibernation, these mammals dramatically lower their metabolic, heart, and respiratory rates as well as their body temperature in a precisely controlled manner. This strategy helps some, particularly small, mammals to survive cold winter conditions in temperate climates when food and water are scarce yet the demand for metabolic heat generation is high. Hibernating species are frequently closely related to nonhibernating species and are found in five orders of eutherian mammals as well as in a few species of marsupials and monotremes (ref. 1 and Fig. 1). The adaptive significance of hibernation, coupled with the interspersed phylogenetic distribution of hibernating species among mammals, makes hibernation an ideal model system to test the hypothesis that the molecular basis of important adaptive events during evolution involves mechanisms that lead to the differential regulation of existing genes and not the invention of new genes (reviewed in ref.3).The evolutionary origin of hibernation is unknown; either of two hypotheses can explain the interspersed nature of the distribution of extant hibernating species throughout Mammalia. One postulates that the common ancestor of all mammals was a hibernator, but the ability to hibernate was lost independently along multiple lineages. The alternative proposes that the common ancestor of all mammals was not a hibernator, and the ability to hibernate has been gained independently along multiple lineages (Fig. 1). With either scenario, we predict that a small number of regulatory changes determine the phenotype of hibernation, rather than the de novo creation or loss of numerous hibernation-specific biochemical functions, encoded by a collection of hibernation-specific genes. Thus, hibernation must be the result of a reprogramming of existing mammalian biochemical capabilities through the differential expression of existing genes.There is little evidence in the literature for differential gene expression during hibernation, although there are a few reports that demonstrate increases or decreases (4) in the amount of specific proteins relative to the active state. Mitochondrial uncoupling protein (thermogenin) is an example of a protein that increases i...

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“…The original bioassay for HIT was the induction of hibernation in summer-active 13-lined ground squirrels by intravenous injection of an albumin-containing plasma fraction from torpid hibernators such as woodchucks and black bears. At least part of the problem in purifying the HIT appears to stem from the use of this difficult and unreliable bioassay to measure the hibernation-inducing activity (167,245,248). A series of investigations have linked the "HIT" to a ␦-opioid activity (132), although at this time it is not justified to consider this activity a trigger that induces hibernation.…”

Section: A Initiation and Reversal Of Torpormentioning

confidence: 98%

Mammalian Hibernation: Cellular and Molecular Responses to Depressed Metabolism and Low Temperature

Carey

Andrews

Martin

2003

Physiological Reviews

996

955

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Mammalian hibernators undergo a remarkable phenotypic switch that involves profound changes in physiology, morphology, and behavior in response to periods of unfavorable environmental conditions. The ability to hibernate is found throughout the class Mammalia and appears to involve differential expression of genes common to all mammals, rather than the induction of novel gene products unique to the hibernating state. The hibernation season is characterized by extended bouts of torpor, during which minimal body temperature (Tb) can fall as low as -2.9 degrees C and metabolism can be reduced to 1% of euthermic rates. Many global biochemical and physiological processes exploit low temperatures to lower reaction rates but retain the ability to resume full activity upon rewarming. Other critical functions must continue at physiologically relevant levels during torpor and be precisely regulated even at Tb values near 0 degrees C. Research using new tools of molecular and cellular biology is beginning to reveal how hibernators survive repeated cycles of torpor and arousal during the hibernation season. Comprehensive approaches that exploit advances in genomic and proteomic technologies are needed to further define the differentially expressed genes that distinguish the summer euthermic from winter hibernating states. Detailed understanding of hibernation from the molecular to organismal levels should enable the translation of this information to the development of a variety of hypothermic and hypometabolic strategies to improve outcomes for human and animal health.

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The “hibernation induction trigger”: Specificity and validity of bioassay using the 13-lined ground squirrel

Cited by 25 publications

References 10 publications

Metabolic Flexibility: Hibernation, Torpor, and Estivation

Metabolic Flexibility: Hibernation, Torpor, and Estivation

Central role for differential gene expression in mammalian hibernation.

Mammalian Hibernation: Cellular and Molecular Responses to Depressed Metabolism and Low Temperature

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