Neuroglobin of seals and whales: evidence for a divergent role in the diving brain.

Abstract

Although many physiological adaptations of diving mammals have been reported, little is known about how their brains sustain the high demands for metabolic energy and thus O(2) when submerged. A recent study revealed in the deep-diving hooded seal (Cystophora cristata) a unique shift of the oxidative energy metabolism and neuroglobin, a respiratory protein that is involved in neuronal hypoxia tolerance, from neurons to astrocytes. Here we have investigated neuroglobin in another pinniped species, the harp seal (Pagophilus groenlandicus), and in two cetaceans, the harbor porpoise (Phocoena phocoena) and the minke whale (Balaenoptera acutorostrata). Neuroglobin sequences, expression levels and patterns were compared with those of terrestrial relatives, the ferret (Mustela putorius furo) and the cattle (Bos taurus), respectively. Neuroglobin sequences of whales and seals only differ in two or three amino acids from those of cattle and ferret, and are unlikely to confer functional differences, e.g. in O(2) affinity. Neuroglobin is expressed in the astrocytes also of P. groenlandicus, suggesting that the shift of neuroglobin and oxidative metabolism is a common adaptation in the brains of deep-diving phocid seals. In the cetacean brain neuroglobin resides in neurons, like in terrestrial mammals. However, neuroglobin mRNA expression levels were 4-15 times higher in the brains of harbor porpoises and minke whales than in terrestrial mammals or in seals. Thus neuroglobin appears to play a specific role in diving mammals, but seals and whales have evolved divergent strategies to cope with cerebral hypoxia. The specific function of neuroglobin that conveys hypoxia tolerance may either relate to oxygen supply or protection from reactive oxygen species. The different strategies in seals and whales resulted from a divergent evolution and an independent adaptation to diving.

• Authors: M Schneuer, S Flachsbarth, N U Czech-Damal, L P Folkow, U Siebert, T Burmester
• Journal: Neuroscience (Neuroscience) Vol. 223 Pg. 35-44 (Oct 25 2012) ISSN: 1873-7544 [Electronic] United States
• PMID: 22864183 (Publication Type: Journal Article, Research Support, Non-U.S. Gov't)
• Copyright: Copyright © 2012 IBRO. Published by Elsevier Ltd. All rights reserved.

Chemical References

• Glial Fibrillary Acidic Protein
• Nerve Tissue Proteins
• Neuroglobin
• RNA, Messenger
• Globins

Topics

• Animals
• Astrocytes (metabolism)
• Brain (anatomy & histology, metabolism)
• Cattle
• Cloning, Molecular
• Dogs
• Ferrets
• Glial Fibrillary Acidic Protein (metabolism)
• Globins (genetics, metabolism)
• Nerve Tissue Proteins (genetics, metabolism)
• Neuroglobin
• RNA, Messenger (metabolism)
• Seals, Earless (anatomy & histology, genetics, metabolism)
• Sequence Analysis, Protein
• Swine
• Whales (anatomy & histology, genetics, metabolism)