Histamine H3 Receptor Activation Modulates Glutamate Release in the Corticostriatal Synapse by Acting at CaV2.1 (P/Q-Type) Calcium Channels and GIRK (KIR3) Potassium Channels

Vázquez-Vázquez, Héctor; Gónzalez-Sandoval, Carolina; Vega, Alberto; Arias‐Montaño, José‐Antonio; Barral, Jaime

doi:10.1007/s10571-020-00980-6

Cited by 9 publications

(6 citation statements)

References 62 publications

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“…To better understand the mechanism underlying the inhibitory effect of PD on 4-AP-induced glutamate release and increase in Ca 2+ influx, Ca 2+ -channel antagonists were used in this study. Previous studies have suggested that glutamate release is mainly dependent on Ca 2+ influx through N- and P/Q-type VDCCs [ 28 , 29 ]. In rat cortical synaptosomes, control glutamate release evoked by 4-AP was 7.4 ± 0.3 nmol mg of protein −1 5 min −1 .…”

Section: Resultsmentioning

confidence: 99%

Plantainoside D Reduces Depolarization-Evoked Glutamate Release from Rat Cerebral Cortical Synaptosomes

Chiu

Lee

et al. 2023

Molecules

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Inhibiting the excessive release of glutamate in the brain is emerging as a promising therapeutic option and is efficient for treating neurodegenerative disorders. The aim of this study is to investigate the effect and mechanism of plantainoside D (PD), a phenylenthanoid glycoside isolated from Plantago asiatica L., on glutamate release in rat cerebral cortical nerve terminals (synaptosomes). We observed that PD inhibited the potassium channel blocker 4-aminopyridine (4-AP)-evoked release of glutamate and elevated concentration of cytosolic Ca2+. Using bafilomycin A1 to block glutamate uptake into synaptic vesicles and EDTA to chelate extracellular Ca2+, the inhibitory effect of PD on 4-AP-evoked glutamate release was prevented. In contrast, the action of PD on the 4-AP-evoked release of glutamate in the presence of dl-TBOA, a potent nontransportable inhibitor of glutamate transporters, was unaffected. PD does not alter the 4-AP-mediated depolarization of the synaptosomal membrane potential, suggesting that the inhibitory effect of PD on glutamate release is associated with voltage-dependent Ca2+ channels (VDCCs) but not the modulation of plasma membrane potential. Pretreatment with the Ca2+ channel blocker (N-type) ω-conotoxin GVIA abolished the inhibitory effect of PD on the evoked glutamate release, as did pretreatment with the protein kinase C inhibitor GF109203x. However, the PD-mediated inhibition of glutamate release was eliminated by applying the mitochondrial Na+/Ca2+ exchanger inhibitor CGP37157 or dantrolene, which inhibits Ca2+ release through ryanodine receptor channels. These data suggest that PD mediates the inhibition of evoked glutamate release from synaptosomes primarily by reducing the influx of Ca2+ through N-type Ca2+ channels, subsequently reducing the protein kinase C cascade.

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Section: Resultsmentioning

confidence: 99%

Plantainoside D Reduces Depolarization-Evoked Glutamate Release from Rat Cerebral Cortical Synaptosomes

Chiu

Lee

et al. 2023

Molecules

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“…GIRK channel blocker tertiapin-Q (100 nM) had no effect on the parameters of evoked ACh release ( Figure 5B ), but it completely prevented the decrease in the amplitude and quantal content of EPPs caused by BDNF prodomain (1 nM) in mature NMJs ( Figure 5C ). Apparently, GIRK channels, known as modulators of presynaptic RMP and action potential of nerve terminals in CNS ( Meneses et al, 2015 ; Vázquez-Vázquez et al, 2020 ), may be downstream targets of BDNF prodomain and mediate its inhibitory effects on evoked ACh release in mouse motor synapses.…”

Section: Resultsmentioning

confidence: 99%

“…Another new and unexpected fact is the relation of the TrkB-mediated proBDNF-induced inhibitory effect on the frequency of MEPPs and an increase in muscle fiber RMP with the activity of GIRK channels in newly formed NMJs. Examples are known in CNS, when the activation of GIRK in nerve terminals leads to downregulation of neurotransmitter release ( Meneses et al, 2015 ; Vázquez-Vázquez et al, 2020 ). However, the specific signaling mechanism of proBDNF-induced inhibition of spontaneous ACh release involving GIRK activation in newly formed NMJs remains to be discovered in further experiments.…”

Section: Discussionmentioning

confidence: 99%

ProBDNF and Brain-Derived Neurotrophic Factor Prodomain Differently Modulate Acetylcholine Release in Regenerating and Mature Mouse Motor Synapses

Bogacheva

Молчанова

Pravdivceva

et al. 2022

Front. Cell. Neurosci.

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The effects of brain-derived neurotrophic factor (BDNF) processing by-products (proBDNF and BDNF prodomain) on the activity of mouse neuromuscular junctions (NMJs) were studied in synapses formed during the reinnervation of extensor digitorum longus muscle (m. EDL) and mature synapses of the diaphragm. The parameters of spontaneous miniature endplate potentials (MEPPs) and evoked endplate potentials (EPPs) were analyzed in presence of each of the BDNF maturation products (both – 1 nM). In newly formed NMJs, proBDNF caused an increase in the resting membrane potential of muscle fibers and a decrease in the frequency of MEPPs, which was prevented by tertiapin-Q, a G-protein-coupled inwardly rectifying potassium channels (GIRK) blocker but not by p75 receptor signaling inhibitor TAT-Pep5. proBDNF had no effect on the parameters of EPPs. BDNF prodomain in newly formed synapses had effects different from those of proBDNF: it increased the amplitude of MEPPs, which was prevented by vesamicol, an inhibitor of vesicular acetylcholine (ACh) transporter; and reduced the quantal content of EPPs. In mature NMJs, proBDNF did not influence MEPPs parameters, but BDNF prodomain suppressed both spontaneous and evoked ACh release: decreased the frequency and amplitude of MEPPs, and the amplitude and quantal content of EPPs. This effect of the BDNF prodomain was prevented by blocking GIRK channels, by TAT-Pep5 or by Rho-associated protein kinase (ROCK) inhibitor Y-27632. At the same time, the BDNF prodomain did not show any inhibitory effects in diaphragm motor synapses of pannexin 1 knockout mice, which have impaired purinergic regulation of neuromuscular transmission. The data obtained suggest that there is a previously unknown mechanism for the acute suppression of spontaneous and evoked ACh release in mature motor synapses, which involves the activation of p75 receptors, ROCK and GIRK channels by BDNF prodomain and requires interaction with metabotropic purinoreceptors. In general, our results show that both the precursor of BDNF and the product of its maturation have predominantly inhibitory effects on spontaneous and evoked ACh release in newly formed or functionally mature neuromuscular junctions, which are mainly opposite to the effects of BDNF. The inhibitory influences of both proteins related to brain neurotrophin are mediated via GIRK channels of mouse NMJs.

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“…Following 28-days abstinence, evoked field potentials were significantly decreased in both the CeA and BLA with the latter accompanied by an increase in PPR. While many factors may underly an increased response to a second test stimulus, the increase in PPR suggests that neuroadaptations in BLA, but not CeA, are connected to a reduced probability of transmitter release (Morales, McGinnis et al 2018, Vázquez-Vázquez, Gonzalez-Sandoval et al 2022, Vestin, Lagström et al 2022.…”

Section: Abstinence-induced Amygdalo-striatal Neuroadaptationsmentioning

confidence: 99%

“…Decreased excitatory neurotransmission in the striatum is most likely of clinical relevance as the inability to disengage from habitual associations when the contingency is disrupted has been shown to be related to a significant reduction in glutamate concentration in the putamen in cocaine addicted patients (Ersche, Lim et al 2021). While recordings performed in striatal subregions primarily supported nicotine-induced transformations in postsynaptic neurons, PPR was significantly increased in the DMS after 14-days abstinence, indicative of a reduced probability of transmitter release (Meneses, Mateos et al 2015, Vázquez-Vázquez, Gonzalez-Sandoval et al 2022. It is relevant to note the PPR is measured at around half max of the response amplitude.…”

Section: Abstinence-induced Amygdalo-striatal Neuroadaptationsmentioning

confidence: 99%

Abstinence-Induced Nicotine Seeking Relays on a Persistent Hypoglutamatergic State within the Amygdalo-Striatal Neurocircuitry

Domi

Lagström

et al. 2023

eNeuro

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Nicotine robustly sustains smoking behavior by acting as a primer reinforcer and by enhancing the incentive salience of the nicotine associated stimuli. The motivational effects produced by environmental cues associated with nicotine delivery can progressively manifest during abstinence resulting in reinstatement of nicotine seeking. However, how the activity in reward neuronal circuits is transformed during abstinence-induced nicotine seeking is not yet fully understood. In here we used a contingent nicotine and saline control self-administration model to disentangle the contribution of cue-elicited seeking responding for nicotine after drug abstinence in male Wistar rats. Using ex vivo electrophysiological recordings and a network analysis approach, we defined temporal and brain-region specific amygdalo-striatal glutamatergic alterations that occur during nicotine abstinence. The results from this study provide critical evidence indicating a persistent hypoglutamatergic state within the amygdalo-striatal neurocircuitry over protracted nicotine abstinence. During abstinence-induced nicotine seeking, electrophysiological recordings showed progressive neuroadaptations in dorsal and ventral striatum already at 14-days abstinence while neuroadaptations in subregions of the amygdala emerged only after 28-days abstinence. The observed neuroadaptations pointed to a brain network involving the amygdala and the dorsolateral striatum (DLS) to be implied in cue-induced reinstatement of nicotine seeking. Together these data suggest long-lasting neuroadaptations that might reflect neuroplastic changes responsible to abstinence-induced nicotine craving. Neurophysiological transformations were detected within a time window that allows therapeutic intervention advancing clinical development of preventive strategies in nicotine addiction.SIGNIFICANT STATEMENTMost people attempting to quit smoking, experience multiple periods of remission and relapse within the first month of abstinence. Our results provide evidence of a persistent hypoglutamatergic state over four weeks of nicotine abstinence when assessing parallel changes in evoked glutamate transmission in multiple amygdalo-striatal subregions at once. The observed neuroadaptations pointed to a brain network involving the amygdala and the dorsolateral striatum that correlated with cue-induced reinstatement of nicotine seeking. The importance of these findings resides in an improved picture when capturing a single frame of the amygdalo-striatal circuitry in abstinence-induced nicotine craving. The neurophysiological transformations were detected within a time window that allows therapeutic intervention advancing clinical development of preventive strategies in nicotine addiction.

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Histamine H3 Receptor Activation Modulates Glutamate Release in the Corticostriatal Synapse by Acting at CaV2.1 (P/Q-Type) Calcium Channels and GIRK (KIR3) Potassium Channels

Cited by 9 publications

References 62 publications

Plantainoside D Reduces Depolarization-Evoked Glutamate Release from Rat Cerebral Cortical Synaptosomes

Plantainoside D Reduces Depolarization-Evoked Glutamate Release from Rat Cerebral Cortical Synaptosomes

ProBDNF and Brain-Derived Neurotrophic Factor Prodomain Differently Modulate Acetylcholine Release in Regenerating and Mature Mouse Motor Synapses

Abstinence-Induced Nicotine Seeking Relays on a Persistent Hypoglutamatergic State within the Amygdalo-Striatal Neurocircuitry

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