Hibernation: A Natural Model of Tolerance to Cerebral Ischemia/Reperfusion

Drew, Kelly L.; Zuckerman, Jeffrey A.; Shenk, Phillip E.; Bogren, Lori K.; Jinka, Tulasi R.; Moore, Jeanette T.

doi:10.1007/978-1-4419-9695-4_3

Cited by 8 publications

(7 citation statements)

References 60 publications

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“…Although ID is delayed in AGS, once it occurs glutamate efflux approximates efflux seen in rat hippocampal slices, but with minimal evidence of cell death in AGS (Drew et al, 2012). Thus, glutamate released during OGD in AGS hippocampal slices is not excitotoxic.…”

Section: Resistance To Ischemia/reperfusion In the Euthermic State Inmentioning

confidence: 80%

“…Studies show that resistance to I/R injury in the brain is independent of the hibernation season or the hibernation state (Christian et al, 2008;Dave et al, 2006;Dave et al, 2009). In hippocampal slices from AGS, oxygen and glucose deprivation produces an overflow of glutamate but dramatically less cell death than in slices from rat (Drew et al, 2012). AGS hippocampal slices also resist NMDAinduced excitotoxicity and demonstrate smaller increases in intracellular calcium following bath application of glutamate Zhao et al, 2006).…”

Section: Agss Do Not Rely On Glycogen or Oxidative Phosphorylation Fomentioning

confidence: 99%

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No oxygen? No problem! Intrinsic brain tolerance to hypoxia in vertebrates

Larson

Drew

Folkow

et al. 2014

Journal of Experimental Biology

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134

102

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Many vertebrates are challenged by either chronic or acute episodes of low oxygen availability in their natural environments. Brain function is especially vulnerable to the effects of hypoxia and can be irreversibly impaired by even brief periods of low oxygen supply. This review describes recent research on physiological mechanisms that have evolved in certain vertebrate species to cope with brain hypoxia. Four model systems are considered: freshwater turtles that can survive for months trapped in frozen-over lakes, arctic ground squirrels that respire at extremely low rates during winter hibernation, seals and whales that undertake breath-hold dives lasting minutes to hours, and naked mole-rats that live in crowded burrows completely underground for their entire lives. These species exhibit remarkable specializations of brain physiology that adapt them for acute or chronic episodes of hypoxia. These specializations may be reactive in nature, involving modifications to the catastrophic sequelae of oxygen deprivation that occur in non-tolerant species, or preparatory in nature, preventing the activation of those sequelae altogether. Better understanding of the mechanisms used by these hypoxiatolerant vertebrates will increase appreciation of how nervous systems are adapted for life in specific ecological niches as well as inform advances in therapy for neurological conditions such as stroke and epilepsy.KEY WORDS: Arctic ground squirrel, Cetacean, Hypoxia, Naked mole-rat, Seal, Turtle IntroductionEnvironmental conditions vary enormously for vertebrates, both with respect to the extreme conditions tolerated by a given species at different times and with respect to average living conditions tolerated by different species. Temperature is perhaps the most obvious example: from the poles to the equator, average ambient temperatures vary widely and have been accompanied by physiological adaptations appropriate to resident species; seasonal variations in temperature and resource variability can induce dramatic changes in physiological and/or behavioral patterns including migration and hibernation. Oxygen levels also vary widely, with animals adapted to sea level, high-altitude, underground and aquatic habitats. Oxygen levels can also change dramatically on a shorter-term basis, as can occur in tidal pools or in breath-hold divers. Approximately 20% of the oxygen consumed by the human body is used by the brain. The greater part of this oxygen is used to produce the ATP required to maintain the membrane potentials necessary for electrical signaling with synaptic and action potentials (Harris et al., 2012). In many vertebrates, including adult humans, interruption of the oxygen supply to the brain for more than a few minutes leads to irreversible neurological damage, including neuronal death. Without oxidative phosphorylation, ATP-dependent neuronal processes including ion transport and neurotransmitter reuptake decline sharply. Without pumping, ion gradients fail and neurons depolarize, releasing excessive levels...

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Section: Resistance To Ischemia/reperfusion In the Euthermic State Inmentioning

confidence: 80%

Section: Agss Do Not Rely On Glycogen or Oxidative Phosphorylation Fomentioning

confidence: 99%

No oxygen? No problem! Intrinsic brain tolerance to hypoxia in vertebrates

Larson

Drew

Folkow

et al. 2014

Journal of Experimental Biology

Self Cite

134

102

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“…Based on these findings, we suggest that mouse-tailed bats do not perform arousals, or that they perform unusual, extremely long torpor bouts for hibernation in high ambient temperatures. Except for the energy saving, reducing arousal frequency can reduce possible oxidative stress or other damage to the brain and other tissues due to hypoxia during arousals (reviewed by [37,38]). …”

Section: Discussionmentioning

confidence: 99%

Subtropical mouse-tailed bats use geothermally heated caves for winter hibernation

et al. 2015

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We report that two species of mouse-tailed bats (Rhinopoma microphyllum and R. cystops) hibernate for five months during winter in geothermally heated caves with stable high temperature (208C). While hibernating, these bats do not feed or drink, even on warm nights when other bat species are active. We used thermo-sensitive transmitters to measure the bats' skin temperature in the natural hibernacula and open flow respirometry to measure torpid metabolic rate at different ambient temperatures (T a , 16-358C) and evaporative water loss (EWL) in the laboratory. Bats average skin temperature at the natural hibernacula was 21.7 + 0.88C, and no arousals were recorded. Both species reached the lowest metabolic rates around natural hibernacula temperatures (208C, average of 0.14 + 0.01 and 0.16 + 0.04 ml O 2 g 21 h 21 for R. microphyllum and R. cystops, respectively) and aroused from torpor when T a fell below 168C. During torpor the bats performed long apnoeas (14 + 1.6 and 16 + 1.5 min, respectively) and had a very low EWL. We hypothesize that the particular diet of these bats is an adaptation to hibernation at high temperatures and that caves featuring high temperature and humidity during winter enable these species to survive this season on the northern edge of their world distribution.

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“…By comparing similarities and differences, general properties of cell resistance could be discovered [81,105]. Understanding these properties could have direct applications to human health, as similar protective mechanisms could be harnessed to cure or prevent human pathologies [106,107,108]. …”

Section: Hibernation: Who How and Why Is It Interesting?mentioning

confidence: 99%

Calcium-Binding Proteins in the Nervous System during Hibernation: Neuroprotective Strategies in Hypometabolic Conditions?

Gattoni

Bernocchi

2019

IJMS

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Calcium-binding proteins (CBPs) can influence and react to Ca2+ transients and modulate the activity of proteins involved in both maintaining homeostatic conditions and protecting cells in harsh environmental conditions. Hibernation is a strategy that evolved in vertebrate and invertebrate species to survive in cold environments; it relies on molecular, cellular, and behavioral adaptations guided by the neuroendocrine system that together ensure unmatched tolerance to hypothermia, hypometabolism, and hypoxia. Therefore, hibernation is a useful model to study molecular neuroprotective adaptations to extreme conditions, and can reveal useful applications to human pathological conditions. In this review, we describe the known changes in Ca2+-signaling and the detection and activity of CBPs in the nervous system of vertebrate and invertebrate models during hibernation, focusing on cytosolic Ca2+ buffers and calmodulin. Then, we discuss these findings in the context of the neuroprotective and neural plasticity mechanisms in the central nervous system: in particular, those associated with cytoskeletal proteins. Finally, we compare the expression of CBPs in the hibernating nervous system with two different conditions of neurodegeneration, i.e., platinum-induced neurotoxicity and Alzheimer’s disease, to highlight the similarities and differences and demonstrate the potential of hibernation to shed light into part of the molecular mechanisms behind neurodegenerative diseases.

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Hibernation: A Natural Model of Tolerance to Cerebral Ischemia/Reperfusion

Cited by 8 publications

References 60 publications

No oxygen? No problem! Intrinsic brain tolerance to hypoxia in vertebrates

No oxygen? No problem! Intrinsic brain tolerance to hypoxia in vertebrates

Subtropical mouse-tailed bats use geothermally heated caves for winter hibernation

Calcium-Binding Proteins in the Nervous System during Hibernation: Neuroprotective Strategies in Hypometabolic Conditions?

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