When the brain goes diving: glial oxidative metabolism may confer hypoxia tolerance to the seal brain |
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Authors: | SA Mitz S Reuss LP Folkow AS Blix J-M Ramirez T Hankeln T Burmester |
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Institution: | 1. Institute of Zoology and Zoological Museum, University of Hamburg, Germany;2. Department of Anatomy and Cell Biology, University Medical Center, Mainz, Germany;3. Department of Arctic Biology, University of Tromsø, Tromsø, Norway;4. Center for Neuroscience, Seattle Children''s Research Institute, Seattle, WA, USA;5. Institute of Molecular Genetics, University of Mainz, Germany |
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Abstract: | Deep diving mammals have developed strategies to cope with limited oxygen availability when submerged. These adaptations are associated with an increased neuronal hypoxia tolerance. Brain neurons of the hooded seal Cystophora cristata remain much longer active in hypoxic conditions than those of mice. To understand the cellular basis of neuronal hypoxia tolerance, we studied neuroglobin and cytochrome c in C. cristata brain. Neuroglobin, a respiratory protein typically found in vertebrate neurons, displays three unique amino acid substitutions in hooded seal. However, these substitutions unlikely contribute to a modulation of O2 affinity. Moreover, there is no significant difference in total neuroglobin protein levels in mouse, rat and seal brains. However, in terrestrial mammals neuroglobin resided exclusively in neurons, whereas in seals neuroglobin is mainly located in astrocytes. This unusual localization of neuroglobin is accompanied by a shift in the distribution of cytochrome c. In seals, this marker for oxidative metabolism is mainly localized in astrocytes, whereas in terrestrial mammals it is essentially found in neurons. Our results indicate that in seals aerobic ATP production depends significantly on astrocytes, while neurons rely less on aerobic energy metabolism. This adaptation may imbue seal neurons with an increased tolerance to hypoxia and potentially also to reactive oxygen species, and may explain in part the ability of deep diving mammals to sustain neuronal activity during prolonged dives. |
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Keywords: | astrocytes cytochrome c deep diving lactate shuttle neuroglobin seal |
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