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. 2016 Aug 9;17:583.
doi: 10.1186/s12864-016-2892-y.

When the Brain Goes Diving: Transcriptome Analysis Reveals a Reduced Aerobic Energy Metabolism and Increased Stress Proteins in the Seal Brain

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Free PMC article

When the Brain Goes Diving: Transcriptome Analysis Reveals a Reduced Aerobic Energy Metabolism and Increased Stress Proteins in the Seal Brain

Andrej Fabrizius et al. BMC Genomics. .
Free PMC article

Abstract

Background: During long dives, the brain of whales and seals experiences a reduced supply of oxygen (hypoxia). The brain neurons of the hooded seal (Cystophora cristata) are more tolerant towards low-oxygen conditions than those of mice, and also better survive other hypoxia-related stress conditions like a reduction in glucose supply and high concentrations of lactate. Little is known about the molecular mechanisms that support the hypoxia tolerance of the diving brain.

Results: Here we employed RNA-seq to approach the molecular basis of the unusual stress tolerance of the seal brain. An Illumina-generated transcriptome of the visual cortex of the hooded seal was compared with that of the ferret (Mustela putorius furo), which served as a terrestrial relative. Gene ontology analyses showed a significant enrichment of transcripts related to translation and aerobic energy production in the ferret but not in the seal brain. Clusterin, an extracellular chaperone, is the most highly expressed gene in the seal brain and fourfold higher than in the ferret or any other mammalian brain transcriptome. The largest difference was found for S100B, a calcium-binding stress protein with pleiotropic function, which was 38-fold enriched in the seal brain. Notably, significant enrichment of S100B mRNA was also found in the transcriptomes of whale brains, but not in the brains of terrestrial mammals.

Conclusion: Comparative transcriptomics indicates a lower aerobic capacity of the seal brain, which may be interpreted as a general energy saving strategy. Elevated expression of stress-related genes, such as clusterin and S100B, possibly contributes to the remarkable hypoxia tolerance of the brain of the hooded seal. Moreover, high levels of S100B that possibly protect the brain appear to be the result of the convergent adaptation of diving mammals.

Keywords: Brain; Calcium; Diving; Glucose; Hooded seal; Hypoxia; Marine mammals; Stress.

Figures

Fig. 1
Fig. 1
Gene ontology (GO) analyses of the differentially expressed genes in the seal (blue) and ferret (red). Only genes with an at least twofold difference in expression levels and RPKM >5 in both species were considered. a GO terms in the PANTHER Annotation Data Set “Molecular Function”. b GO terms in the PANTHER Annotation Data Set “Biological Process”
Fig. 2
Fig. 2
Expression levels of Clu (blue) and S100B (green) in brain tissues of diving and non-diving mammals a The specific brain regions and the species are indicated. b S100B expression was normalised according to the neuron/glia ratio

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References

    1. Peers C, Pearson HA, Boyle JP. Hypoxia and Alzheimer’s disease. Essays Biochem. 2007;43:153–164. doi: 10.1042/bse0430153. - DOI - PubMed
    1. Speer RE, Karuppagounder SS, Basso M, Sleiman SF, Kumar A, Brand D, Smirnova N, Gazaryan I, Khim SJ, Ratan RR. Hypoxia-inducible factor prolyl hydroxylases as targets for neuroprotection by “antioxidant” metal chelators: From ferroptosis to stroke. Free Radic. Biol. Med. 2013;62:26–36. doi: 10.1016/j.freeradbiomed.2013.01.026. - DOI - PMC - PubMed
    1. Dirnagl U, Iadecola C, Moskowitz MA. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 1999;22(9):391–397. doi: 10.1016/S0166-2236(99)01401-0. - DOI - PubMed
    1. Haddad GG, Jiang C. O2 deprivation in the central nervous system: on mechanisms of neuronal response, differential sensitivity and injury. Prog. Neurobiol. 1993;40(3):277–318. doi: 10.1016/0301-0082(93)90014-J. - DOI - PubMed
    1. Hansen AJ. Effect of anoxia on ion distribution in the brain. Physiol. Rev. 1985;65(1):101–148. - PubMed

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