Seasonal protein changes support rapid energy production in hibernator brainstem

Epperson, L. Elaine; Rose, James C.; Russell, Rae L.; Nikrad, Mrinalini P.; Carey, Hannah V.; Martin, Sandra L.

doi:10.1007/s00360-009-0422-9

Cited by 31 publications

(35 citation statements)

References 47 publications

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“…In addition, the same mechanism might also serve for a lower vulnerability to excitotoxic insults observed during hibernation (95,179,223). Still our knowledge on regulation of synaptic plasticity during hibernation and the role of tau protein in this process is very limited, and further candidates might be involved, including tau-interacting proteins, such as 14 -3-3 protein gamma, as recently identified by a proteomic approach (49).…”

Section: Is Phospho-tau a Central Regulator Of Brain Plasticity And Smentioning

confidence: 96%

Neuronal plasticity in hibernation and the proposed role of the microtubule-associated protein tau as a “master switch” regulating synaptic gain in neuronal networks

Arendt

Bullmann

2013

American Journal of Physiology-Regulatory, Integrative and Comp

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Arendt T, Bullmann T. Neuronal plasticity in hibernation and the proposed role of the microtubule-associated protein tau as a "master switch" regulating synaptic gain in neuronal networks. Am J Physiol Regul Integr Comp Physiol 305: R478 -R489, 2013. First published July 13, 2013 doi:10.1152/ajpregu.00117.2013.-The present paper provides an overview of adaptive changes in brain structure and learning abilities during hibernation as a behavioral strategy used by several mammalian species to minimize energy expenditure under current or anticipated inhospitable environmental conditions. One cellular mechanism that contributes to the regulated suppression of metabolism and thermogenesis during hibernation is reversible phosphorylation of enzymes and proteins, which limits rates of flux through metabolic pathways. Reversible phosphorylation during hibernation also affects synaptic membrane proteins, a process known to be involved in synaptic plasticity. This mechanism of reversible protein phosphorylation also affects the microtubule-associated protein tau, thereby generating a condition that in the adult human brain is associated with aggregation of tau protein to paired helical filaments (PHFs), as observed in Alzheimer's disease. Here, we put forward the concept that phosphorylation of tau is a neuroprotective mechanism to escape NMDA-mediated hyperexcitability of neurons that would otherwise occur during slow gradual cooling of the brain. Phosphorylation of tau and its subsequent targeting to subsynaptic sites might, thus, work as a kind of "master switch," regulating NMDA receptor-mediated synaptic gain in a wide array of neuronal networks, thereby enabling entry into torpor. If this condition lasts too long, however, it may eventually turn into a pathological trigger, driving a cascade of events leading to neurodegeneration, as in Alzheimer's disease or other "tauopathies".Alzheimer's disease; neurodegeneration; neuroprotection; neuronal plasticity; protein phosphorylation; tauopathies Seasonal Brain Plasticity Might Be a Widespread PhenomenonANIMALS LIVING IN ENVIRONMENTS with daily or seasonal rhythms have developed different strategies to coordinate endogenous processes with ambient conditions. To optimize their energy balance under conditions of restricted availability of food and increased costs for temperature regulation, animals can either reduce the expense for foraging or the need of foraging (96). The expense for foraging can be reduced by food storing or escaping a cold climate by migration. Alternatively, hibernation is a powerful strategy to reduce the metabolic costs of daily activity. All of these aforementioned strategies to optimize energy expenditure are associated with plastic adaptive changes both at the level of behavior and brain structure.The seasonal modulation of food-storing behavior (33,177,178,182) or migration (17) in birds has been shown to require special spatial learning abilities, which are paralleled by seasonal changes in neuronal structure. These cyclic changes in size and mo...

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Section: Is Phospho-tau a Central Regulator Of Brain Plasticity And Smentioning

confidence: 96%

Neuronal plasticity in hibernation and the proposed role of the microtubule-associated protein tau as a “master switch” regulating synaptic gain in neuronal networks

Arendt

Bullmann

2013

American Journal of Physiology-Regulatory, Integrative and Comp

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“…Use of two dimensional gel electrophoresis and mass spectrometry has uncovered changes in the proteome of hibernating thirteen-lined ground squirrels (Russeth et al, 2006; Epperson et al, 2010a; Epperson et al, 2010b). An in vivo approach employing proton magnetic resonance spectroscopy ( 1 H MRS) was used to measure brain metabolites during hibernation in ground squirrels (Henry et al, 2007).…”

Section: Recent Advances In Circannual Timing Researchmentioning

confidence: 99%

Circannual Transitions in Gene Expression

Schwartz

Andrews

2013

Current Topics in Developmental Biology

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Circannual timing is important for the coordination of seasonal activities, particularly promoting survival of individuals in adverse conditions through adaptive physiological and behavioral changes. This includes optimizing survival of offspring by coordinating reproductive efforts at appropriate times. Thus timing is very important for overall fitness. In this review, we provide several examples of circannually timed events, discussing the physiological changes that accompany these events, and some of the known genes and pathways underlying these changes. We then describe five candidate systems, including mammalian hibernation, that are potentially involved in circannual timing. Finally, we discuss several recent advances in molecular biology and animal husbandry that have made the use of non-model organisms for research more feasible, which will hopefully promote and encourage further advancement in the knowledge of circannual timing.

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“…The spectral data were then analyzed with Spectrum Mill as described above. All of the resulting peptide data were combined to account for multiple MS/MS runs and orthologous identifications using an in-house program, ExtracTags (23). Spots were considered unambiguously identified if they returned an overall score Ն30 and contained Ն2 peptides for only one protein.…”

Section: D Digementioning

confidence: 99%

Multistate proteomics analysis reveals novel strategies used by a hibernator to precondition the heart and conserve ATP for winter heterothermy

Grabek

Karimpour-Fard

Epperson³

et al. 2011

Physiological Genomics

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SL. Multistate proteomics analysis reveals novel strategies used by a hibernator to precondition the heart and conserve ATP for winter heterothermy. Physiol Genomics 43: 1263-1275. First published September 13, 2011 doi:10.1152/physiolgenomics.00125.2011.-The hibernator's heart functions continuously and avoids damage across the wide temperature range of winter heterothermy. To define the molecular basis of this phenotype, we quantified proteomic changes in the 13-lined ground squirrel heart among eight distinct physiological states encompassing the hibernator's year. Unsupervised clustering revealed a prominent seasonal separation between the summer homeotherms and winter heterotherms, whereas within-season state separation was limited. Further, animals torpid in the fall were intermediate to summer and winter, consistent with the transitional nature of this phase. A seasonal analysis revealed that the relative abundances of protein spots were mainly winter-increased. The winter-elevated proteins were involved in fatty acid catabolism and protein folding, whereas the winter-depleted proteins included those that degrade branched-chain amino acids. To identify further statedependent changes, protein spots were re-evaluated with respect to specific physiological state, confirming the predominance of seasonal differences. Additionally, chaperone and heat shock proteins increased in winter, including HSPA4, HSPB6, and HSP90AB1, which have known roles in protecting against ischemia-reperfusion injury and apoptosis. The most significant and greatest fold change observed was a disappearance of phospho-cofilin 2 at low body temperature, likely a strategy to preserve ATP. The robust summer-to-winter seasonal proteomic shift implies that a winter-protected state is orchestrated before prolonged torpor ensues. Additionally, the general preservation of the proteome during winter hibernation and an increase of stress response proteins, together with dephosphorylation of cofilin 2, highlight the importance of ATP-conserving mechanisms for winter cardioprotection. 2D DiGE; CFL2; hibernating; Ictidomys (spermophilus) tridecemlineatus; mass spectrometry HIBERNATION IN MAMMALS IS characterized by dramatic, but reversible, reductions in body temperature (T b ) and metabolic rate. During this torpid phase, respiration and heart rate also decline to 1-4% of their euthermic values (for review, see Ref. 11). Torpor bouts are punctuated by interbout arousals (54), when physiological rates are restored to or even surpass euthermic levels (11). For circannual hibernators such as 13-lined ground squirrels, Ictidomys tridecemlineatus, the ability to orchestrate reversible metabolic depression exists only in winter (reviewed in Ref. 38). This heterothermic winter phenotype contrasts markedly with summer, when animals remain homeotherms. A "two-switch" mechanism in which animals first switch from summer homeothermy to a state that is permissive for winter heterothermy (switch 1), and then cycle between periods of torpor and arousal in winte...

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Seasonal protein changes support rapid energy production in hibernator brainstem

Cited by 31 publications

References 47 publications

Neuronal plasticity in hibernation and the proposed role of the microtubule-associated protein tau as a “master switch” regulating synaptic gain in neuronal networks

Neuronal plasticity in hibernation and the proposed role of the microtubule-associated protein tau as a “master switch” regulating synaptic gain in neuronal networks

Circannual Transitions in Gene Expression

Multistate proteomics analysis reveals novel strategies used by a hibernator to precondition the heart and conserve ATP for winter heterothermy

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