Distribution of NMDA receptor subunit NR1 in Arctic ground squirrel central nervous system

Zhao, Hongbin; Christian, Sherri L.; Castillo, Marina; Bult‐Ito, Abel; Drew, Kelly L.

doi:10.1016/j.jchemneu.2006.09.002

Cited by 14 publications

(9 citation statements)

References 37 publications

(61 reference statements)

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“…Similar regressive adaptive changes during torpor in cell body area, dendritic arbor complexity, spine density, synaptic ultrastructure, presynaptic and postsynaptic proteins and its quick regrowth to euthermic values after arousal have been observed in brain areas other than the hippocampus, such as neocortex and thalamus, suggesting a global phenomenon (168,203,204,221,222). affect mechanisms of learning and memory during hibernation.…”

Section: Neuronal Plasticity During Hibernationsupporting

confidence: 56%

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: Neuronal Plasticity During Hibernationsupporting

confidence: 56%

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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“…Protective and functional alterations in the brain are likely to manifest themselves in large part at the protein level in a manner that is dependent on hibernation season (Epperson and Martin 2002; Martin and Epperson 2008; von der Ohe et al 2007; Zhao et al 2006). Evidence from previous two-dimensional gel electrophoresis (2DE) studies suggests a loss of protein quality during torpor that is corrected during interbout arousal (Epperson et al 2004; Martin et al 2004).…”

Section: Resultsmentioning

confidence: 99%

Seasonal protein changes support rapid energy production in hibernator brainstem

et al. 2009

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During the torpor phase of mammalian hibernation when core body temperature is near 4°C, the autonomic system continues to maintain respiration, blood pressure and heartbeat despite drastic reductions in brain activity. Additionally, the hibernator’s neuronal tissues enter into a protected state in which the potential for ischemia-reperfusion injury is markedly minimized. Evolutionary adaptations for continued function and neuroprotection throughout cycles of torpor and euthermia in winter are predicted to manifest themselves partly in changes in the brainstem proteome. Here we compare the soluble brainstem protein complement from six summer active ground squirrels and six in the early torpor phase of hibernation. Thirteen percent of the ~1500 quantifiable 2D gel spots alter significantly from summer to early torpor; the proteins identified in these differing spots are known to play roles in energy homeostasis via the tricarboxylic acid cycle (eight proteins), cytoarchitecture and cell motility (14 proteins), anabolic protein processes (13 proteins), redox control (11 proteins) and numerous other categories including protein catabolism, oxidative phosphorylation, signal transduction, glycolysis, intracellular protein trafficking and antiapoptotic function. These protein changes represent, at least in part, the molecular bases for restructuring of cells in the brainstem, a shift away from glucose as the primary fuel source for brain in the winter, and the generation of a streamlined mechanism capable of efficient and rapid energy production and utilization during the torpor and arousal cycles of hibernation.

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“…Tolerance in ibeAGS appears to involve channel arrest, but of a more limited scope than the channel arrest that occurs during torpor in hAGS. Relative to rat, glutamate-induced Ca 2+ influx is suppressed in both hAGS and ibeAGS and membrane expression of the essential NR1 subunit for NMDAR is lower in hAGS and ibeAGS than in rat (Zhao et al, 2006a). …”

Section: Euthermic Phasementioning

confidence: 99%

Neuroprotection: Lessons from hibernators

Dave

Christian

Pérez-Pinzón

et al. 2012

Comparative Biochemistry and Physiology Part B: Biochemistry an

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102

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Mammals that hibernate experience extreme metabolic states and body temperatures as they transition between euthermia, a state resembling typical warm blooded mammals, and prolonged torpor, a state of suspended animation where the brain receives as low as 10% of normal cerebral blood flow. Transitions into and out of torpor are more physiologically challenging than the extreme metabolic suppression and cold body temperatures of torpor per se. Mammals that hibernate show unprecedented capacities to tolerate cerebral ischemia, a decrease in blood flow to the brain caused by stroke, cardiac arrest or brain trauma. While cerebral ischemia often leads to death or disability in humans and most other mammals, hibernating mammals suffer no ill effects when blood flow to the brain is dramatically decreased during torpor or experimentally induced during euthermia. These animals, as adults, also display rapid and pronounced synaptic flexibility where synapses retract during torpor and rapidly re-emerge upon arousal. A variety of coordinated adaptations contribute to tolerance of cerebral ischemia in these animals. In this review we discuss adaptations in heterothermic mammals that may suggest novel therapeutic targets and strategies to protect the human brain against cerebral ischemic damage and neurodegenerative disease.

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Distribution of NMDA receptor subunit NR1 in Arctic ground squirrel central nervous system

Cited by 14 publications

References 37 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

Seasonal protein changes support rapid energy production in hibernator brainstem

Neuroprotection: Lessons from hibernators

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