Glucocorticoids Inhibit Glucose Transport in Cultured Hippocampal Neurons and Glia
Abstract
A classical action of glucocorticoids (GCs) is to inhibit glucose uptake into various peripheral tissues. Two recent reports suggest that GCs do the same in the brain. Because of the in vivo nature of those studies, it was impossible to determine whether this inhibition occurred at the blood-brain barrier, and/or within neurons and glia themselves. In order to answer this and other mechanistic questions, we examined the effects of GCs on glucose transport in primary brain cultures. We established that uptake of 14C-2-deoxyglucose into hippocampal cultures was linear over a 15-min period and was inhibited by D-glucose and the uptake inhibitor cytochalasin B. Using this system, we found the following. (1) Both corticosterone and dexamethasone inhibited uptake into cultures containing both neurons and glia. (2) The effect was dose-dependent; steroid concentrations in the nanomolar range inhibited uptake from 20 to 33%. The effect was time-dependent, with more than 4 h of steroid exposure needed for inhibition. (3) Non-GC steroids did not inhibit uptake. (4) The GC inhibition seemed to be mediated by the type II (glucocorticoid) corticosteroid receptor. The effect was blocked by a type II, but not a type I (mineralocorticoid) receptor antagonist. Moreover, corticosterone inhibited only at concentrations well above the K d for the type I receptor. Finally, aldosterone inhibited transport when applied at concentrations that bound heavily to type II receptors. (5) Corticosterone did not inhibit uptake in hypothalamic, cerebellar or cortical cultures, despite the presence of corticosteroid receptors in these cultures. (6) GCs inhibited uptake in both neuron- and glia-enriched hippocampal cultures.
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Cortisol administration reduces glucose transport into neurons.
“Cortisol administration reduces glucose transport into neurons (18)”
From Reduced glucose tolerance is associated with poor memory performance and hippocampal atrophy among normal elderly (2003) · cites this paper as [18]
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Sapolsky, R. M. (1993) · Behavioural Brain Research · doi:10.1016/0166-4328(93)90133-b · Cited by 103 · see citing works
Self-citationImpact of aging on stress-responsive neuroendocrine systems
Pedersen, W. A. (2001) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(01)00250-0 · Cited by 104 · see citing works
Chapter 26 Re-examination of the glucocorticoid hypothesis of stress and aging
McEwen, B. S. (1992) · Progress in brain research · doi:10.1016/s0079-6123(08)64585-9 · Cited by 104 · see citing works
Mifepristone protects CA1 hippocampal neurons following traumatic brain injury in rat
McCullers, D. L., Sullivan, P. G., Scheff, S. W., & Herman, J. P. (2002) · Neuroscience · doi:10.1016/s0306-4522(01)00477-8 · Cited by 103 · see citing works
Meaney, M. J., O’Donnell, D., Rowe, W. B., Tannenbaum, B. M., Steverman, A., Walker, M., Nair, N. P. V., & LUPIEN, S. J. (1995) · Experimental Gerontology · doi:10.1016/0531-5565(94)00065-b · Cited by 103 · see citing works
Cognitive dysfunction associated with metabolic syndrome
Taylor, V. H., & MacQUEEN, G. M. (2007) · Obesity Reviews · doi:10.1111/j.1467-789x.2007.00401.x · Cited by 102 · see citing works
“In animal studies, glucocorticoid exposure inhibits glucose transport into hippocampal neurones and glia (70), perhaps because”
BackgroundDoes fluorine-18 fluorodeoxyglucose metabolic imaging of tumours benefit oncology?
Brock, C., Meikle, S. R., & Price, P. (1997) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/bf00841411 · Cited by 96 · see citing works
“It is known that glucose utilisation by brain is affected by exogenous corticosteroid ingestion, and in vitro it has been demonstrated that corticosteroids inhibit the glucose uptake by glial cells and neurons of hippocampus in a dose-dependent receptor-mediated manner [ 106 ].”
BackgroundSocial Stress Exacerbates Focal Cerebral Ischemia in Mice
Sugo, N., Hurn, P. D., Morahan, M., Hattori, K., Traystman, R. J., & DeVries, A. C. (2002) · Stroke · doi:10.1161/01.str.0000016967.76805.bf · Cited by 94 · see citing works
Glucocorticoids may alter antioxidant enzyme capacity in the brain: kainic acid studies
McIntosh, L. J., Cortopassi, K. M., & Sapolsky, R. M. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00104-8 · Cited by 94 · see citing works
Self-citationCorticosterone Enhances Kainic Acid‐Induced Calcium Elevation in Cultured Hippocampal Neurons
Elliott, E. M., & Sapolsky, R. M. (1992) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1992.tb08345.x · Cited by 90 · see citing works
“GCs appear to endanger hippocampal neurons by impairing glucose uptake, and thus inducing a state of metabolic vulnerability (Phillips et al., 1987; Kadekaro et al., 1988; Horner et al., 1990).”
BackgroundMethodInfluentialSelf-citationDexamethasone blocks sleep induced improvement of declarative memory
Plihal, W., Pietrowsky, R., & Born, J. (1999) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(98)00080-8 · Cited by 90 · see citing works
“, 1992) and a site-specific inhibition of glucose transport into hippocampal neurons and glia (Horner et al., 1990).”
BackgroundGarcía‐Bueno, B., Caso, J. R., Perez‐Nievas, B. G., Lorenzo, P. L., & Leza, J. C. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301252 · Cited by 90 · see citing works
“Studies have shown that in hippocampal cell cultures glucocorticoids significantly inhibit glucose transport and glutamate uptake by both neurons and astrocytes (Horner et al, 1990; Virgin et al, 1991).”
Background
- Authors
- Homer, H. C., Packan, D. R., & Sapolsky, R. M.
- Affiliations
- Stanford University (US)
- ORCID
- Sapolsky, Robert M.
- Venue
- Neuroendocrinology
- Publisher
- S. Karger AG
- Published
- 2008-04-03
- Volume
- 52
- Issue
- 1
- Pages
- 57-64
- ISSN
- 0028-3835 (ISSN-L)
- 1423-0194
- OpenAlex
- W2056408203
- Cited by
- 331
- References
- 0
- Citations by year
- 2025: 1 · 2024: 2 · 2023: 4 · 2022: 1 · 2021: 4 · 2020: 1 · 2019: 2 · 2018: 5 · 2017: 2 · 2016: 3 · 2015: 3 · 2014: 5 · 2013: 7 · 2012: 7
- FWCI
- 4.91
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01ag006633-08)
- National Institute on Aging (AG-06633)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- glucocorticoids, glucose transport, glucose uptake, hippocampal neurons, glia, corticosterone, dexamethasone, aldosterone, mineralocorticoid receptor, 2-deoxyglucose, cytochalasin B, brain glucose metabolism
- MeSH terms
- Analysis of Variance, Animals, Biological Transport, Carbon Radioisotopes, Cells, Cultured, Deoxyglucose, Glucocorticoids, Glucose, Hippocampus, Immunohistochemistry, Neuroglia, Neurons, Rats, Inbred Strains, Receptors, Glucocorticoid, Rats
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