Angiotensin II blockade of long-term potentiation at the perforant path-granule cell synapse in vitro

doi:10.1016/0196-9781(96)00030-7

Peptides

Volume 17, Issue 4, 1996, Pages 689-693

https://doi.org/10.1016/0196-9781(96)00030-7 Get rights and content

Abstract

Field recordings of evoked excitatory postsynaptic potentials (pEPSPs) were carried out in the granule cell stratum moleculare following stimulation of the perforant path in rat hippocampal slices. Under control conditions tetanic stimulation produced long-term potentiation (LTP) as measured by an increase in the initial slope of the pEPSPs that lasted for at least 1 h. LTP experiments were repeated with 0.5, 5.0, 50, or 500 nM angiotensin II (AII) present in the bath at the time of tetanization. Induction of LTP was blocked by 50 nM AII; however, normal baseline responses were not affected. At the highest dose tested, 500 nM, a decrease in the amplitude and slope of baseline pEPSPs was observed. When the AII AT₁ receptor antagonist losartan was present in the bath AII inhibition of LTP was blocked. The application of losartan alone had no effect on LTP expression. These findings support previous results from in vivo studies demonstrating that activation of AT₁ receptors in the dentate gyrus blocks the induction of LTP at the perforant path-granule cell synapse.

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Transient Global Amnesia (TGA) is an enigmatic amnestic syndrome. We conducted a systematic review to investigate the relationship between the conventional cardiovascular risk factors and TGA. MEDLINE, CENTRAL, EMBASE and PsycINFO were comprehensively searched and 23 controlled observational studies were retrieved. The prevalence of hypertension, diabetes mellitus, dyslipidemia and smoking was lower among patients with TGA compared to Transient Ischemic Attack. Regarding the comparison of TGA with healthy individuals, there was strong evidence suggesting a protective effect of diabetes mellitus on TGA and weaker evidence for a protective effect of smoking. Hypertension was associated with TGA only in more severe stages, while dyslipidemia was not related. In view of these findings, a novel pathophysiological hypothesis is proposed, in which the functional interactions of Angiotensin-II type-1 and N-methyl-D-aspartate receptors are of pivotal importance. The whole body of clinical evidence (nature of precipitating events, associations with migraine, gender-based association patterns) was integrated.
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The activation of the angiotensin (Ang) II after acute kidney injury (AKI) triggers oxidative stress and inflammatory cascade which involved not only the kidneys but also the brain. Ang II through the Ang II type 1 receptor (AT1R) may have deleterious effects on hippocampal synaptic transmission and cognitive functions under uremic encephalopathy. The present study was conducted to examine the effects of AT1R antagonist on AKI-induced cognitive and synaptic plasticity impairment.
Here, we investigated the effect of AKI and possible pathophysiological roles of AT1R with the selective AT1R antagonist losartan (10 mg/kg/day for consecutive 9 days) on cognitive performance using passive avoidance and Morris water maze tests. In order to understand the synaptic transmission, in vivo short and long-term plasticity were evaluated at the Schaffer collateral-CA1 synapse. Biochemical analysis was also performed to detect possible hippocampal nitric oxide and oxidative stress mechanisms.
Our data provide evidence of hippocampal complication following AKI with increased level of nitrite (P < 0.01 vs. sham) as well as oxidative stress (P < 0.01 vs. sham) that may be responsible for behavioral dysfunction under uremia (spatial memory, P < 0.001; passive avoidance P < 0.01 vs. sham). Losartan treatment effectively protects against cognitive (spatial memory, P < 0.01; passive avoidance P < 0.05 vs. AKI-veh) and synaptic plasticity impairments induced by AKI possibly via modulation of oxidative stress in the hippocampus (P < 0.01 vs. AKI-veh).
The present study conclusively demonstrated a protective role of AT1R antagonist losartan in hippocampal complication and neurocognitive dysfunction after AKI via modulating oxidative stress.
Short-term Heat Exposure Promotes Hippocampal Neurogenesis via Activation of Angiotensin II Type 1 Receptor in Adult Rats
2018, Neuroscience
Angiotensin II (Ang II) synthesized in response to body fluid loss caused by actions such as sweating and breathing is today considered as one of the essential factors for promoting hippocampal neurogenesis. Because heat stimuli, along with exercise, increase systemic levels of Ang II, the effects of short-term heat exposure on hippocampal neurogenesis were examined in adult male rats. When rats were exposed daily to a 1-h heat treatment (36.0 ± 0.1 °C) during a 7-d experimental period, the number of doublecortin-immunoreactive newborn cells in the hippocampal dentate gyrus was increased approximately 1.4-fold compared with that in controls that were exposed to a normothermic environment (25.0 ± 0.8 °C). No significant change was observed in the number of Ki-67-immunoreactive stem cells. Western blot and immunohistochemical analyses revealed an enhancement of vascular endothelial growth factor (VEGF) expression in hippocampal astrocytes following short-term heat exposure. These beneficial effects of short-term heat exposure were prevented when an antagonist for Ang II type 1 receptor (AT1R), candesartan, was given orally. These results indicate that short-term heat exposure enhances adult neurogenesis via activation of AT1R in the hippocampal dentate gyrus, in which VEGF may participate by promoting cell proliferation and/or newborn neuron survival.
Long-term intracerebroventricular infusion of angiotensin II after kainate-induced status epilepticus: Effects on epileptogenesis, brain damage, and diurnal behavioral changes
2015, Epilepsy and Behavior
Citation Excerpt :
However, they are reported to be upregulated under pathological conditions in the hippocampus of a rat model of epilepsy [13] as well as in patients with TLE [12]. The other explanation might be that the exogenous Ang II exerts an indirect modulatory effect on inhibitory neurotransmission [26–29]. The KA–sham rats exhibited impaired spatial learning over the whole testing period of 18 days which is in agreement with our previous data with epileptic rats [30].
Our previous studies revealed that Angiotensin (Ang) II has anticonvulsant effects in acute seizure models. However, data on its role in experimental models of epilepsy are missing. In the present study, we tested whether posttreatment with Ang II after kainate (KA)-induced status epilepticus (SE) can affect epileptogenesis, concomitant behavioral changes, and brain damage. The Wistar rats were intracerebroventricularly infused via osmotic mini-pumps with Ang II (1.52 μg/μl/day for 28 days) after SE. Spontaneous motor seizures (SMS) were video-recorded for up to three months. Locomotor activity, anxiety, and depression-like behavior were evaluated during the last week of drug infusion, while spatial memory was assessed during the 3rd month after SE. Angiotensin II decreased the latency for onset of the first SMS and increased the frequency of SMS two months after SE. The continuous peptide infusion exacerbated the KA-induced hyperactivity and caused depression-like behavior. The reduced anxiety of KA-treated rats was alleviated by Ang II exposure. The KA-induced deficit in the hippocampal-dependent spatial memory was not influenced by Ang II. However, Ang II partially prevented the neuronal damage in the hippocampus, specifically in the CA1 area. The role of AT₁ and AT₂ receptor activation in the effects of the octapeptide is discussed.
Inhibition of central angiotensin II enhances memory function and reduces oxidative stress status in rat hippocampus
2013, Progress in Neuro-Psychopharmacology and Biological Psychiatry
While it is now well established that the independent brain renin–angiotensin system (RAS) has some important central functions besides the vascular ones, the relevance of its main bioactive peptide angiotensin II (Ang II) on the memory processes, as well as on oxidative stress status is not completely understood.
The purpose of the present work was to evaluate the effects of central Ang II administration, as well as the effects of Ang II inhibition with either AT1 and AT 2 receptor specific blockers (losartan and PD-123177, respectively) or an angiotensin-converting enzyme (ACE) inhibitor (captopril). These effects were studied on the short-term memory (assessed through Y-maze) or long-term memory (as determined in passive avoidance) and on the oxidative stress status of the hippocampus.
Our results demonstrate memory deficits induced by the administration of Ang II, as showed by the significant decrease of the spontaneous alternation in Y-maze (p = 0.015) and latency-time in passive avoidance task (p = 0.001) when compared to saline. On the other side, the administration of all the aforementioned Ang II blockers significantly improved the spontaneous alternation in Y-maze task, while losartan also increased the latency time as compared to saline in step-through passive avoidance (p = 0.042).
Also, increased oxidative stress status was induced in the hippocampus by the administration of Ang II, as demonstrated by increased levels of lipid peroxidation markers (malondialdehyde-MDA concentration) (p < 0.0001) and a decrease in both antioxidant enzymes determined: superoxide dismutase-SOD (p < 0.0001) and glutathione peroxidase-GPX (p = 0.01), as compared to saline. Additionally, the administration of captopril resulted in an increase of both antioxidant enzymes and decreased levels of lipid peroxidation (p = 0.001), while PD-123177 significantly decreased MDA concentration (p > 0.0001) vs. saline.
Moreover, significant correlations were found between all of the memory related behavioral parameters and the main oxidative stress markers from the hippocampus, which is known for its implication in the processes of memory and also where RAS components are well expressed.
This could be relevant for the complex interactions between Ang II, behavioral processes and neuronal oxidative stress, and could generate important therapeutic approaches.
Angiotensin-(1-7) central administration induces anxiolytic-like effects in elevated plus maze and decreased oxidative stress in the amygdala
2013, Journal of Affective Disorders
Citation Excerpt :
In this way, regarding Ang-(1–7), it has been shown that this heptapeptide could counterbalance most of the pressor and angiogenic actions of Ang II (Tallant et al., 2005; Machado et al., 2000). These effects were also observed at the behavioral and higher functions level, considering that for instance Ang II is known to block long-term potentiation (LTP) in both hippocampus (Armstrong et al., 1996) and amygdala (von Bohlen und Halbach, Albrecht, 1998), while Ang-(1–7) appears to enhance it (Hellner et al., 2005). While our group previously confirmed that RAS is implicated in anxiety processes (Gard, 2004) and reported anxiety-like effects for angiotensin II administration (Ciobica et al., 2011), to our knowledge, no data are available concerning the role of Ang-(1–7) alone administration in the mechanisms of anxiety behavior, except from some studies regarding the relevance of Mas receptor deletion (Walther et al., 1998), which was only later on identified as Ang-(1–7) receptor (Santos et al., 2003).
There is increasing evidence that besides the well-known angiotensin (Ang) II, other renin–angiotensin system (RAS) peptides, including Ang-(1–7), could have important effects at the central level.
However, very few things are known about the central actions of Ang-(1–7), while the effects of its administration alone on anxiety have not been tested to date, to the best of our knowledge. In this way, we were interested in studying the effects of Ang-(1–7) intracerebroventricular administration on anxiety levels, as studied through some main behavioral parameters in the elevated plus maze, as well as the importance of Ang-(1–7) in the oxidative stress status from the amygdala, which is one of the key brain regions involved in mediating anxiety.
We report here a possible anxiolytic-like effect of Ang-(1–7) administration, as demonstrated by the increased percentage of time spent and frequency of entries in the open arms of the elevated plus maze, as well as increased head-dipping behavior in the open arms and decreased stretching in closed arms. Also some antioxidant effects of Ang-(1–7) are suggested since a significant increase of GPX specific activity and a decrease of the main peroxidation marker MDA were observed in the amygdala. Moreover, we found a significant correlation between most of the behavioral parameters in the elevated plus maze and the levels of the oxidative stress markers.
However, further studies are necessary in order to elucidate the effects of Ang-(1–7) administration on anxiety and oxidative stress status and also on the possible correlation that might exists between these aspects.

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ArticleAngiotensin II blockade of long-term potentiation at the perforant path-granule cell synapse in vitro

Abstract

Eur. J. Pharmacol.

Biochem. Biophys. Res. Commun.

Biochem. Biophys. Res. Commun.

Pharmacol. Biochem. Behav.

Brain Res.

Brain Res.

Neuroscience

Brain Res.

Trends Neurosci.

Brain Res.

Brain Res.

Neuron

Neuron

Pharmacol. Biochem. Behav.

Brain Res. Rev.

Dual effects of angiotensin II on calcium currents in neonatal rat nodose neurons

J. Neurosci.

Article
Angiotensin II blockade of long-term potentiation at the perforant path-granule cell synapse in vitro