Hypersensitivity of the hippocampal CA3 region to stress-induced neurodegeneration and amyloidogenesis in a rat model of surgical menopause
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Females who enter menopause prematurely via bilateral ovariectomy (surgical menopause) have a significantly increased risk for cognitive decline and dementia. To help elucidate the mechanisms underlying this phenomenon, we used an animal model of surgical menopause, long-term (10-week) bilateral ovariectomy in female rats. Herein, we demonstrate that long-term oestrogen deprivation dramatically increases sensitivity of the normally resistant hippocampal CA3 region to ischaemic stress, an effect that was gender-specific, as it was not observed in long-term orchiectomized males. Furthermore, the enhanced damage to the CA3 region correlated with a worse cognitive outcome after ischaemic stress. Long-term ovariectomized rats also displayed a robust hyperinduction of Alzheimer's disease-related proteins in the CA3 region and a switch in amyloid precursor protein processing from non-amyloidogenic to amyloidogenic following ischaemic stress CA3 hypersensitivity also extended to an Alzheimer's disease-relevant insult, as the CA3 region of long-term ovariectomized rats was profoundly hypersensitive to the neurotoxic effects of amyloid-β1-42, the most amyloidogenic form of the amyloid-β peptide. Additional studies revealed that CA3 region hypersensitivity, Alzheimer's disease-related protein induction, and amyloidogenesis are mediated by a NADPH oxidase/superoxide/c-Jun N-terminal kinase/c-Jun signalling pathway, involving both transcriptional and post-translational mechanisms. In addition, while 17β-oestradiol replacement at the end of the long-term oestrogen deprivation period could not prevent CA3 hypersensitivity and amyloidogenesis, if 17β-oestradiol was initiated at the time of ovariectomy and maintained throughout the 10-week oestrogen deprivation period, it completely prevented these events, providing support for the 'critical window' hypothesis for oestrogen replacement therapy benefit. Collectively, these findings may help explain the increased risk of cognitive decline and dementia observed in women following surgical menopause, and they provide increased support that early 17β-oestradiol replacement is critical in preventing the negative neural effects associated with bilateral ovariectomy.
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In animal experiments, bilaterally ovariectomized rats developed Aβ 1−42 in the hippocampus after exposure to stress.
“In animal experiments, bilaterally ovariectomized rats developed Aβ 1 −42 in the hippocampus after exposure to stress, a finding which corroborate with our finding of more Aβ in women with surgical menopause at young ages [59,66].”
From Sex differences in Alzheimer’s disease and common neuropathologies of aging (2018) · cites this paper as [66]
The CA3 field of the hippocampus has been implicated as one of the first sites of neuronal dysfunction and neuronal death in Alzheimer's disease.
“This region has been implicated as one of the first sites of neuronal dysfunction and neuronal death in AD (Belvindrah et al., 2014; Padurariu et al., 2012; Zhang et al., 2013).”
From LC3-Associated Endocytosis Facilitates β-Amyloid Clearance and Mitigates Neurodegeneration in Murine Alzheimer’s Disease (2019) · cites this paper as Zhang et al., 2013
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Radix Achyranthis Bidentatae improves learning and memory capabilities in ovariectomized rats.
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Estetrol and Its Effects on the Damaged Brain
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Surgical menopause enhances hippocampal amyloidogenesis following global cerebral ischemia
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Self-citationEstrogen Neuroprotection and Anti-Inflammation Actions in the Hippocampus
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- Authors
- Zhang, Q.-G., Wang, R.-M., Scott, E., Han, D., Dong, Y., Tu, J.-Y., Yang, F., Reddy Sareddy, G., Vadlamudi, R. K., & Brann, D. W.
- Affiliations
- Augusta University (US)
- North China University of Science and Technology (CN)
- The University of Texas at San Antonio Health Science Center (US)
- Venue
- Brain
- Publisher
- Oxford University Press (OUP)
- Published
- 2013-03-09
- Volume
- 136
- Issue
- 5
- Pages
- 1432-1445
- ISSN
- 0006-8950 (ISSN-L)
- 1460-2156
- PMC
- PMC3634196
- OpenAlex
- W2081861881
- Cited by
- 50
- References
- 49
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 2 · 2023: 2 · 2022: 2 · 2021: 2 · 2020: 5 · 2019: 7 · 2018: 6 · 2017: 5 · 2016: 5 · 2015: 4 · 2014: 6 · 2013: 1
- FWCI
- 3.71
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Brain (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- American Heart Association (10SDG256009)
- National Institutes of Health (NS050730)
- National Institute of Neurological Disorders and Stroke (NS050730, R01NS050730)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
- Keywords
- surgical menopause, bilateral oophorectomy, estrogen deprivation, hippocampal CA3, stress-induced neurodegeneration, amyloidogenesis, amyloid-beta 42, Alzheimer's disease, NADPH oxidase, superoxide, c-Jun N-terminal kinase, estrogen replacement therapy, sex differences, cognitive decline
- MeSH terms
- Animals, Female, Male, Menopause, Nerve Degeneration, Ovariectomy, Peptide Fragments, Stress, Physiological, Amyloid beta-Peptides, Rats, Sprague-Dawley, Models, Animal, Rats, CA3 Region, Hippocampal
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