Effect of Acute Stress on Hippocampal Glutamate Levels and Spectrin Proteolysis in Young and Aged Rats

Lowy, Martin T.; Wittenberg, Lee; Yamamoto, Bryan K.

doi:10.1046/j.1471-4159.1995.65010268.x

Cited by 201 publications

(100 citation statements)

References 43 publications

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“…IL-1␤ is reported to enhance the death of human fetal brain cells and rat oligodendrocyte progenitor cells, but only when combined with TNF-␣ or INF-␥ (39,40). In the present study, there was no evidence from TUNEL staining that IL-1␤ and/or acute stress elicit hippocampal cell death either in vitro or in vivo, which is consistent with previous studies (40)(41)(42), although there is one report that severe acute stress increases apoptosis (43). In contrast, we found that incubation of AHPs with IL-1␤ induces a dramatic decline in levels of cyclin D1, a cell cycle regulatory protein that controls specific cyclin-dependent kinases such as cdk4 (31).…”

Section: Discussionsupporting

confidence: 93%

IL-1β is an essential mediator of the antineurogenic and anhedonic effects of stress

Koo

Duman

2008

Proc. Natl. Acad. Sci. U.S.A.

775

564

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Stress decreases neurogenesis in the adult hippocampus, and blockade of this effect is required for the actions of antidepressants in behavioral models of depression. However, the mechanisms underlying these effects of stress have not been identified. Here, we demonstrate an essential role for the proinflammatory cytokine IL-1␤. Administration of IL-1␤ or acute stress suppressed hippocampal cell proliferation. Blockade of the IL-1␤ receptor, IL-1RI, by using either an inhibitor or IL-1RI null mice blocks the antineurogenic effect of stress and blocks the anhedonic behavior caused by chronic stress exposure. In vivo and in vitro studies demonstrate that hippocampal neural progenitor cells express IL-1RI and that activation of this receptor decreases cell proliferation via the nuclear factor-B signaling pathway. These findings demonstrate that IL-1␤ is a critical mediator of the antineurogenic and depressive-like behavior caused by acute and chronic stress.cytokine ͉ depression ͉ neurogenesis T he profound consequences of stress exposure, defined as disturbances of physiological homeostasis, include a detrimental impact on certain aspects of brain function (1, 2). In particular, uncontrollable stress is a major contributing factor for neuropsychiatric disorders such as major depression and posttraumatic stress disorders (3, 4). Alterations at the cellular level in the hippocampus have been linked to the pathophysiology of stress-related mood disorders (5-7). Many studies demonstrate that stressful experiences suppress hippocampal neurogenesis, which could contribute to the hippocampal atrophy observed in depressed patients (8-10). In contrast, antidepressant treatment increases hippocampal neurogenesis, blocks the antineurogenic effects of stress (11,12), and reduces or even reverses hippocampal atrophy (9, 11). Recent studies demonstrate that new hippocampal neurons are required for the actions of antidepressants in behavioral models of depression and anxiety (13, 14) with some exceptions (15,16).Despite this progress, the mechanisms underlying the antineurogenic and behavioral actions of stress remain ill defined. One possibility is that excessive proinflammatory cytokines, particularly IL-1␤, contribute to the actions of stress. Animal studies demonstrate that exposure to stress increases IL-1␤ in several brain areas, including the hippocampus (17-20), and central administration of IL-1␤ produces several stress-like effects, including activation of the hypothalamic-pituitary-adrenal (HPA) axis (17, 21), inhibition of hippocampal long-term potentiation (22), down-regulation of hippocampal brain-derived neurotrophic factor (23), and impaired hippocampal-dependent contextual fear conditioning (24). In contrast, blockade of the receptor, IL-1RI that mediates the actions of IL-1␤ (25) inhibits these stress-like effects (23, 24) and blocks the antiproliferative effects of INF-␣ in the hippocampus (26).Based on this evidence, the current study was undertaken to test the hypothesis that the antineurogenic and depressiv...

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Section: Discussionsupporting

confidence: 93%

IL-1β is an essential mediator of the antineurogenic and anhedonic effects of stress

Koo

Duman

2008

Proc. Natl. Acad. Sci. U.S.A.

775

564

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“…We have observed that CRS increases GLT-1 mRNA in the DG and Ammon's horn and GLT-1 protein levels in the CA3c region, increases that were reportedly (18) prevented by chronic treatment with the antidepressant tianeptine. The CRS-induced increase in GLT-1 protein expression in the CA3 suggests that the increase in extracellular concentrations of glutamate observed during stress (19,42) may elicit a compensatory increase in GLT-1 expression. The ability of lithium to prevent this stress-induced increase is likely due to its ability to stabilize glutamate activity, including changes in transporter activity.…”

Section: The Effect Of Chronic Stress and Lithium On Glutamate Transpmentioning

confidence: 99%

Stress-induced structural remodeling in hippocampus: Prevention by lithium treatment

Wood

Young²,

Reagan³

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

183

121

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Chronic restraint stress, psychosocial stress, as well as systemic or oral administration of the stress-hormone corticosterone induces a morphological reorganization in the rat hippocampus, in which adrenal steroids and excitatory amino acids mediate a reversible remodeling of apical dendrites on CA3 pyramidal cell neurons of the hippocampus. This stress-induced neuronal remodeling is accompanied also by behavioral changes, some of which can be prevented with selective antidepressant and anticonvulsive drug treatments. Lithium is an effective treatment for mood disorders and has neuroprotective effects, which may contribute to its therapeutic properties. Thus, we wanted to determine whether lithium treatment could prevent the effects of chronic stress on CA3 pyramidal cell neuroarchitecture and the associated molecular and behavioral measures. Chronic lithium treatment prevented the stress-induced decrease in dendritic length, as well as the stressinduced increase in glial glutamate transporter 1 (GLT-1) mRNA expression and the phosphorylation of cAMP-response element binding in the hippocampus. Lithium treatment, however, did not prevent stress effects on behavior in the open field or the plusmaze. These data demonstrate that chronic treatment with lithium can protect the hippocampus from potentially deleterious effects of chronic stress on glutamatergic activation, which may be relevant to its therapeutic efficacy in the treatment of major depressive disorder and bipolar disorder.

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“…29,30 Glucocorticoids and stress enhance glutamatergic transmission in the hippocampus. 31,32 Glucocorticoids, through increased glutamatergic signaling, elicit structural remodeling in the hippocampus such as dendritic atrophy, 33,34 an effect that can be prevented by lithium treatment. 35 Notably, chronic treatment with lithium stabilizes glutamate uptake in presynaptic nerve endings over a narrow range 36 and produces a robust neuroprotective effect against excitotoxicity.…”

Section: Introductionmentioning

confidence: 99%

Glutamate as a spectroscopic marker of hippocampal structural plasticity is elevated in long-term euthymic bipolar patients on chronic lithium therapy and correlates inversely with diurnal cortisol

et al. 2008

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While an excess of glucocorticoids is associated with hippocampal pathology in mood disorders, lithium exerts robust neuroprotective and neurotrophic effects. Here, 21 stably remitted bipolar I patients who had been on chronic lithium maintenance therapy, on average, for more than a decade, and 19 carefully matched healthy controls were studied using 3 T 1 Hmagnetic resonance spectroscopy of left and right hippocampus. Salivary cortisol samples were obtained to assess activity of the hypothalamus-pituitary-adrenal system. Absolute concentrations of N-acetylaspartate (NAA), choline-containing compounds and total creatine were similar in euthymic bipolar patients and healthy controls. Hippocampal glutamate concentrations were significantly increased as an effect of patient status (patients > controls) and laterality (left hippocampus > right hippocampus). Hippocampal glutamate content (Glu) was strongly correlated with NAA. Across groups and within the patient group, diurnal saliva cortisol levels showed a significant inverse relationship with both Glu and NAA. Taken together, these results add to the concept of bipolar disorder as an illness involving disturbed hippocampal structural plasticity under the opposing influences of lithium and glucocorticoids.

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Effect of Acute Stress on Hippocampal Glutamate Levels and Spectrin Proteolysis in Young and Aged Rats

Cited by 201 publications

References 43 publications

IL-1β is an essential mediator of the antineurogenic and anhedonic effects of stress

IL-1β is an essential mediator of the antineurogenic and anhedonic effects of stress

Stress-induced structural remodeling in hippocampus: Prevention by lithium treatment

Glutamate as a spectroscopic marker of hippocampal structural plasticity is elevated in long-term euthymic bipolar patients on chronic lithium therapy and correlates inversely with diurnal cortisol

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