Greater glucocorticoid receptor activation in hippocampus of aged rats sensitizes microglia

Barrientos, Ruth M.; Thompson, Vanessa M.; Kitt, Meagan M.; Amat, Jose; Hale, Matthew W.; Frank, Matthew G.; Crysdale, Nicole Y.; Stamper, Christopher E.; Hennessey, Patrick A.; Watkins, Linda R.; Spencer, Robert L.; Lowry, Christopher A.; Maier, Steven F.

doi:10.1016/j.neurobiolaging.2014.12.003

Cited by 70Neuroinflammation and Neurodegeneration MechanismsStress Responses and CortisolTryptophan and brain disorders

Greater glucocorticoid receptor activation in hippocampus of aged rats sensitizes microglia

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Barrientos, Ruth M., Thompson, Vanessa M., Kitt, Meagan M., Amat, Jose, Hale, Matthew W., Frank, Matthew G., Crysdale, Nicole Y., Stamper, Christopher E. +5 more·2015·Neurobiology of Aging

DOI 10.1016/j.neurobiolaging.2014.12.003PMC PMC4346455

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Abstract

Healthy aging individuals are more likely to suffer profound memory impairments following an immune challenge than are younger adults. These challenges produce a brain inflammatory response that is exaggerated with age. Sensitized microglia found in the normal aging brain are responsible for this amplified response, which in turn interferes with processes involved in memory formation. Here, we examine factors that may lead aging to sensitize microglia. Aged rats exhibited higher corticosterone levels in the hippocampus, but not in plasma, throughout the daytime (diurnal inactive phase). These elevated hippocampal corticosterone levels were associated with increased hippocampal 11β-hydroxysteroid dehydrogenase type 1 protein expression, the enzyme that catalyzes glucocorticoid formation and greater hippocampal glucocorticoid receptor (GR) activation. Intracisternal administration of mifepristone, a GR antagonist, effectively reduced immune-activated proinflammatory responses, specifically from hippocampal microglia and prevented Escherichia coli-induced memory impairments in aged rats. Voluntary exercise as a therapeutic intervention significantly reduced total hippocampal GR expression. These data strongly suggest that increased GR activation in the aged hippocampus plays a critical role in sensitizing microglia.

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The enzyme 11β-hydroxysteroid dehydrogenase (11β-HSD1), involved in the conversion of the inactive corticosterone into its active form, was increased with aging.
“Indeed, the enzyme, 11β-hydroxysteroid dehydrogenase (11β-HSD1), involved in the conversion of the inactive corticosterone into its active form, was increased with aging (Barrientos et al, 2015), and aging-associated memory impairments were prevented in 11β-HSD1-knockout animals (Yau et al, 2015).”
From Microglia Priming with Aging and Stress (2017) · cites this paper as Barrientos et al, 2015
Hippocampal expression of nuclear GC receptors has been reported to increase with age in rats.
“Relevant to this, hippocampal expression of nuclear GC receptors has been reported to increase with age in rats (Barrientos et al, 2015).”
From Microglia Priming with Aging and Stress (2017) · cites this paper as Barrientos et al, 2015
Enhanced GC receptor activity in aging was associated with increased microglial expression of MHCII, which was reversed by GC receptor antagonist.
“Furthermore, enhanced GC receptor activity in aging was associated with increased microglial expression of MHCII, which was reversed by GC receptor antagonist (Barrientos et al, 2015).”
From Microglia Priming with Aging and Stress (2017) · cites this paper as Barrientos et al, 2015

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Authors: Barrientos, R. M., Thompson, V. M., Kitt, M. M., Amat, J., Hale, M. W., Frank, M. G., Crysdale, N. Y., Stamper, C. E., Hennessey, P. A., Watkins, L. R., Spencer, R. L., Lowry, C. A., & Maier, S. F.
Affiliations: University of Colorado Boulder (US)
ORCID: Barrientos, Ruth M.
Kitt, Meagan M.
Hale, Matthew W.
Frank, Matthew G.
Stamper, Christopher E.
Watkins, Linda R.
Spencer, Robert L.
Lowry, Christopher A.
Maier, Steven F.
Venue: Neurobiology of Aging
Publisher: Elsevier BV
Published: 2015-03
Volume: 36
Issue: 3
Pages: 1483-1495
ISSN: 0197-4580 (ISSN-L)
DOI: 10.1016/j.neurobiolaging.2014.12.003
PMC: PMC4346455
OpenAlex: W2166436861
Cited by: 70
References: 67
Citations by year: 2025: 1 · 2024: 5 · 2023: 5 · 2022: 3 · 2021: 6 · 2020: 12 · 2019: 3 · 2018: 8 · 2017: 12 · 2016: 13 · 2015: 2
FWCI: 4.67
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neurobiology of Aging (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute on Aging (R01AG028271)
NSF (No. 0921969)
Topics: Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Keywords: glucocorticoid receptor, hippocampus, brain aging, corticosterone, 11β-hydroxysteroid dehydrogenase type 1, mifepristone, immune challenge, memory impairment, neuroinflammation, voluntary exercise, Escherichia coli, diurnal variation
MeSH terms: Aging, Animals, Catalysis, Cells, Cultured, Corticosterone, Hippocampus, Inflammation, Male, Memory, Memory Disorders, Physical Conditioning, Animal, Rats, Inbred F344, Receptors, Glucocorticoid, Mifepristone, Microglia, 11-beta-Hydroxysteroid Dehydrogenase Type 1

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Greater glucocorticoid receptor activation in hippocampus of aged rats sensitizes microglia

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