Effect of Acute Stress on Hippocampal Glutamate Levels and Spectrin Proteolysis in Young and Aged Rats
Abstract
Abstract: Aging in rats is associated with a loss of hippocampal neurons, which may contribute to age‐related cognitive deficits. Several lines of evidence suggest that stress and glucocorticoids may contribute to age‐related declines in hippocampal neuronal number. Excitatory amino acids (EAAs) have been implicated in the glucocorticoid endangerment and stress‐induced morphological changes of hippocampal neurons of young rats. Previously, we have reported that acute immobilization stress can increase extracellular concentrations of the endogenous excitatory amino acid, glutamate, in the hippocampus. The present study examined the effect of an acute bout of immobilization stress on glutamate levels in the hippocampus and medial prefrontal cortex of young (3–4‐month) and aged (22–24‐month) Fischer 344 rats. In addition, the effect of stress on spectrin proteolysis in these two brain regions was also examined. Spectrin is a cytoskeleton protein that contributes to neuronal integrity and proteolysis of this protein has been proposed as an important component of EAA‐induced neuronal death. There was no difference in basal glutamate levels between young and old rats in the hippocampus or medial prefrontal cortex. During the period of restraint stress a modest increase in glutamate levels in the hippocampus of young and aged rats was observed. After the termination of the stress procedure, hippocampal glutamate concentrations continued to rise in the aged rats, reaching a level approximately five times higher than the young rats, and remained elevated for at least 2 h after the termination of the stress. A similar pattern was also observed in the medial prefrontal cortex with an augmented post‐stress‐induced glutamate response observed in the aged rats. There was no increase in spectrin proteolysis in the hippocampus or medial prefrontal cortex of young or aged rats after stress or under basal nonstress conditions. The enhanced poststress glutamate response in the aged rats may contribute to the increased sensitivity of aged rats to neurotoxic insults.
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There was no evidence from TUNEL staining that IL-1β and/or acute stress elicit hippocampal cell death either in vitro or in vivo.
“In the present study, there was no evidence from TUNEL staining that IL-1β and/or acute stress elicit hippocampal cell death either in vitro or in vivo, which is consistent with previous studies (40–42), although there is one report that severe acute stress increases apoptosis (43).”
From IL-1β is an essential mediator of the antineurogenic and anhedonic effects of stress (2008) · cites this paper as [42]
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Zoladz, P. R., Park, C. R., Halonen, J. D., Salim, S., Alzoubi, K. H., Srivareerat, M., Fleshner, M., Alkadhi, K. A., & Diamond, D. M. (2011) · Hippocampus · doi:10.1002/hipo.20922 · Cited by 79 · see citing works
“ticoid administration produces a rapid modulation of the hippocampal glutamatergic system (Lowy et al., 1993; Lowy et al., 1995; Raudensky and Yamamoto, 2007; Joels et al., 2008; Prager and Johnson, 2009; McEwen et al., 2010), which can ultimately result in an impairment of hippocampal synaptic plasticity (Diamond et…”
BackgroundNácher, J., Guirado, R., & Castillo-Gómez, E. (2013) · Neurochemical Research · doi:10.1007/s11064-013-0977-4 · Cited by 75 · see citing works
Repeated Restraint Stress Alters Hippocampal Glutamate Uptake and Release in the Rat
Fontella, F. U., Vendite, D., Tabajara, Â. S., Porciúncula, L. O., Torres, I. L. D. S., Jardim, F. M. A., Martini, L., Souza, D. O., Netto, C. A., & Dalmaz, C. (2004) · Neurochemical Research · doi:10.1023/b:nere.0000035805.46592.6c · Cited by 74 · see citing works
“Evidence from the literature suggests that different types of stress, including restraint and ether exposure, or increased glucocorticoid concentrations, may increase extracellular glutamate levels in the hippocampus, and this effect occurs in parallel with a rise in corticosterone in this brain structure (16,27,37,38…”
BackgroundZoladz, P. R., Fleshner, M., & Diamond, D. M. (2013) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2013.01.001 · Cited by 73 · see citing works
“Preclinical studies have shown that stress significantly increases glutamate levels (Bagley and Moghaddam, 1997; Lowy et al., 1993, 1995; Moghaddam, 1993; Reznikov et al., 2007), inhibits glutamate uptake (Yang et al., 2005), increases the expression and binding of glutamate receptors (Bartanusz et…”
Repurposing of the β-Lactam Antibiotic, Ceftriaxone for Neurological Disorders: A Review
Yimer, E. M., Hishe, H. Z., & Tuem, K. B. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00236 · Cited by 72 · see citing works
“In such cases increased extracellular concentrations of glutamate were observed in several brain regions (Lowy et al., 2002).”
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Dackis, M. N., Rogosch, F. A., Oshri, A., & Cicchetti, D. (2012) · Development and Psychopathology · doi:10.1017/s0954579412000673 · Cited by 71 · see citing works
Marsden, W. N. (2011) · Medical Hypotheses · doi:10.1016/j.mehy.2011.06.021 · Cited by 63 · see citing works
“In support of this, stress and glucocorticoids have been shown to increase extracellular glutamate release in the hippocampus, prefrontal cortex and other regions [219–224], and hippocampal stress-induced LTD has been shown to be dependent upon extrasynaptic NMDAR activity [161]; which may become activated due to gluc…”
BackgroundHotsenpiller, G., & Wolf, M. E. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00951-x · Cited by 63 · see citing works
Ketamine regulates the presynaptic release machinery in the hippocampus
Müller, H. K., Wegener, G., Liebenberg, N., Zarate, C. A., Popoli, M., & Elfving, B. (2013) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2013.03.008 · Cited by 61 · see citing works
“Both stress and glucocorticoids have been shown by microdialysis to increase extracellular glutamate levels in the hippocampus (Bagley and Moghaddam, 1997; Gilad et al., 1990; Lowy et al., 1995; Moghaddam et al., 1994) and enhancement of presynaptic glutamate release by stress/glucocorticoids has been shown by differe…”
BackgroundMethodAging and stress: past hypotheses, present approaches and perspectives.
Garrido, P. (2011) · Europe PMC (PubMed Central) · Cited by 59 · see citing works
Bettio, L. E. B., Freitas, A. E., Neis, V. B., Santos, D. B., Ribeiro, C. M., da Rosa, P. B., Farina, M., & Rodrigues, A. L. S. (2014) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2014.10.002 · Cited by 59 · see citing works
“evoked glutamate release in cortical and limbic regions (Lowy et al., Pharmacology, Biochemistry and Behavior 127 (2014) 7–14”
Wang, C., & Wang, S. (2009) · Synapse · doi:10.1002/syn.20654 · Cited by 59 · see citing works
“administration of CORT can enhance the release of glutamate from the hippocampus (Bagley and Moghaddam, 1997; Lowy et al., 1995; Skorzewska et al., 2007; Venero and Borrell, 1999).”
BackgroundResultMolecular Basis of Late-Life Depression
Kuo, C.-Y., Lin, C., & Lane, H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147421 · Cited by 58 · see citing works
Bambico, F. R., & Belzung, C. (2012) · Current topics in behavioral neurosciences · doi:10.1007/7854_2012_234 · Cited by 57 · see citing works
McEwen, B. S. (2004) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2004.6.2/bmcewen · Cited by 54 · see citing works
“When that does not happen, however, there is allostatic load and the brain is at increased risk for damage.(115,116) The processes of allostasis and allostatic load have been described and measured for metabolic and cardiovascular changes that are associated with obesity, type 2 diabetes, and cardiovascular disease.”
Background
- Authors
- Lowy, M. T., Wittenberg, L., & Yamamoto, B. K.
- Affiliations
- Case Western Reserve University (US)
- Corresponding author
- Lowy, Martin T.
- ORCID
- Yamamoto, Bryan K.
- Venue
- Journal of Neurochemistry
- Publisher
- Wiley
- Published
- 1995-07
- Volume
- 65
- Issue
- 1
- Pages
- 268-274
- ISSN
- 0022-3042 (ISSN-L)
- 1471-4159
- OpenAlex
- W2119257185
- Cited by
- 217
- References
- 0
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 4 · 2023: 5 · 2022: 3 · 2021: 8 · 2020: 5 · 2019: 7 · 2018: 6 · 2017: 3 · 2016: 5 · 2015: 3 · 2014: 4 · 2013: 10 · 2012: 9
- FWCI
- 2.64
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neurochemistry (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Drug Abuse (DA-07606, R01DA007606)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- acute stress, restraint stress, hippocampus, glutamate, aging, age-related cognitive decline, excitatory amino acids, neuronal cell death, medial prefrontal cortex, glucocorticoids, F344 rats
- MeSH terms
- Aging, Animals, Extracellular Space, Hippocampus, Male, Peptide Hydrolases, Rats, Inbred F344, Spectrin, Stress, Physiological, Prefrontal Cortex, Glutamic Acid, Rats
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