Alzheimer's disease‐like neuropathology in three species of oceanic dolphin

Alzheimer's disease (AD) is the most common neurodegenerative disease and the primary cause of disability and dependency among elderly humans worldwide. AD is thought to be a disease unique to humans although several other animals develop some aspects of AD‐like pathology. Odontocetes (toothed...

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Published in:	The European journal of neuroscience Vol. 57; no. 7; pp. 1161 - 1179
Main Authors:	Vacher, Marissa C., Durrant, Claire S., Rose, Jamie, Hall, Ailsa J., Spires‐Jones, Tara L., Gunn‐Moore, Frank, Dagleish, Mark P.
Format:	Journal Article
Language:	English
Published:	France Wiley Subscription Services, Inc 01-04-2023 John Wiley and Sons Inc
Subjects:	Aged Alzheimer Disease - metabolism Alzheimer's disease Amyloid beta-Peptides - metabolism amyloid plaques Animals Astrocytes beta amyloid Brain - metabolism cetacean Clinical and Translational Neuroscience Conspecifics Cytology Dolphins - metabolism Gliosis Humans Immunohistochemistry Microglia Neurodegenerative diseases Neurodegenerative Diseases - metabolism neurofibrillary tangles Neurofibrillary Tangles - metabolism Neuropathology Neuropil odontocetes Odontoceti Pathology Plaque, Amyloid - metabolism Research Report Senile plaques Species Stranding tau Tau protein tau Proteins - metabolism beta amyloid neurofibrillary tangles odontocetes tau immunohistochemistry amyloid plaques cetacean
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Summary:	Alzheimer's disease (AD) is the most common neurodegenerative disease and the primary cause of disability and dependency among elderly humans worldwide. AD is thought to be a disease unique to humans although several other animals develop some aspects of AD‐like pathology. Odontocetes (toothed whales) share traits with humans that suggest they may be susceptible to AD. The brains of 22 stranded odontocetes of five different species were examined using immunohistochemistry to investigate the presence or absence of neuropathological hallmarks of AD: amyloid‐beta plaques, phospho‐tau accumulation and gliosis. Immunohistochemistry revealed that all aged animals accumulated amyloid plaque pathology. In three animals of three different species of odontocete, there was co‐occurrence of amyloid‐beta plaques, intraneuronal accumulation of hyperphosphorylated tau, neuropil threads and neuritic plaques. One animal showed well‐developed neuropil threads, phospho‐tau accumulation and neuritic plaques, but no amyloid plaques. Microglia and astrocytes were present as expected in all brain samples examined, but we observed differences in cell morphology and numbers between individual animals. The simultaneous occurrence of amyloid‐beta plaques and hyperphosphorylated tau pathology in the brains of odontocetes shows that these three species develop AD‐like neuropathology spontaneously. The significance of this pathology with respect to the health and, ultimately, death of the animals remains to be determined. However, it may contribute to the cause(s) of unexplained live‐stranding in some odontocete species and supports the ‘sick‐leader’ theory whereby healthy conspecifics in a pod mass strand due to high social cohesion. Vacher et al used immunohistochemistry to look for Alzheimer's‐like pathology in the brains of aged long‐finned pilot whales, white‐beaked dolphins, Risso's dolphins, harbour porpoises and a bottle‐nosed dolphin that were found beached on the shores of Scotland. All aged animals had amyloid plaque pathology, and three species exhibited both plaques and accumulation of phosphorylated tau in neurons. The simultaneous occurrence of amyloid‐beta plaques and hyperphosphorylated tau in the brains of odontocetes shows that these three species develop Alzheimer's‐like neuropathology spontaneously.
Bibliography:	Funding information This research did not receive any specific grant from funding agencies in the public, commercial or not‐for‐profit sectors. MCV was supported, in part, by the Erasmus+ mobility program. CD is a Race Against Dementia Dyson Fellow and Emerging Leader at the UK Dementia Research Institute. JR is supported by the UK Dementia Research Institute. AJH was funded by the Natural Environment Research Council (Grant No. NE/R015007/1). TS‐J is supported by the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation programme (Grant Agreement No. 681181) and the UK Dementia Research Institute, which receives its funding from DRI Ltd, funded by the UK Medical Research Council, Alzheimer's Society and Alzheimer's Research UK. FG‐M is supported by the RSMacDonald Charitable Trust, Rosetrees Trust and the Engineering and Physical Sciences Research Council programme grant EP/P030017/1. MPD was funded by the Scottish Government and undertakes the detailed histological examination of cetacean tissues for SMASS, which is supported by Marine Scotland, a division of the Scottish Government, and the Department for Environment, Food and Rural Affairs (defra), a department of the UK Government. ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 A Commentary on this Article is available here: https://doi.org/10.1111/ejn.15946
ISSN:	0953-816X 1460-9568
DOI:	10.1111/ejn.15900