Presynaptic NK1 Receptor Activation by Substance P Suppresses EPSCs via Nitric Oxide Synthesis in the Rat Insular Cortex

Matsumura, Shigenobu; Yamamoto, Keiji; Nakaya, Yoshihiro; Ohashi, Kazunori; Kaneko, Katsuyoshi; Takei, Hiroki; Tsuda, Hiromasa; Shirakawa, Tetsuo; Kobayashi, Masayuki

doi:10.1016/j.neuroscience.2020.12.012

Cited by 5 publications

(5 citation statements)

References 48 publications

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“…The effect of SR140333 was reversible in some of the cases (not shown). In the presence of TTX (500 nM), blocking action potential generation, SP could not evoke EPSP number increase, excluding the possibility of activation of presynaptic NK1 receptors (He et al., 2019 ; Matsumura et al., 2021 ). Finally, when the ipsilateral DH was removed by performing a cut at the base of the DH, application of SP failed to raise the number of EPSPs registered from lamina VII neurons (Figure 7b,c ).…”

Section: Resultsmentioning

confidence: 99%

Quantitative spatial analysis reveals that the local axons of lamina I projection neurons and interneurons exhibit distributions that predict distinct roles in spinal sensory processing

Kókai

Luz

Fernandes

et al. 2022

J of Comparative Neurology

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Our knowledge about the detailed wiring of neuronal circuits in the spinal dorsal horn (DH), where initial sensory processing takes place, is still very sparse. While a substantial amount of data is available on the somatodendritic morphology of DH neurons, the laminar and segmental distribution patterns and consequential function of individual axons are much less characterized. In the present study, we fully reconstructed the axonal and dendritic processes of 10 projection neurons (PNs) and 15 interneurons (INs) in lamina I of the rat, to reveal quantitative differences in their distribution. We also performed whole‐cell patch‐clamp recordings to test the predicted function of certain axon collaterals. In line with our earlier qualitative description, we found that lamina I INs in the lateral aspect of the superficial DH send axon collaterals toward the medial part and occupy mostly laminae I–III, providing anatomical basis for a lateromedial flow of information within the DH. Local axon collaterals of PNs were more extensively distributed including dorsal commissural axon collaterals that might refer to those reported earlier linking the lateral aspect of the left and right DHs. PN collaterals dominated the dorsolateral funiculus and laminae IV–VI, suggesting propriospinal and ventral connections. Indeed, patch‐clamp recordings confirmed the existence of a dorsoventral excitatory drive upon activation of neurokinin‐1 receptors that, although being expressed in various lamina I neurons, are specifically enriched in PNs. In summary, lamina I PNs and INs have almost identical dendritic input fields, while their segmental axon collateral distribution patterns are distinct. INs, whose somata reside in lamina I, establish local connections, may show asymmetry, and contribute to bridging the medial and lateral halves of the DH. PNs, on the other hand, preferably relay their integrated dendritic input to deeper laminae of the spinal gray matter where it might be linked to other ascending pathways or the premotor network, resulting in a putative direct contribution to the nociceptive withdrawal reflex.

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Section: Resultsmentioning

confidence: 99%

Quantitative spatial analysis reveals that the local axons of lamina I projection neurons and interneurons exhibit distributions that predict distinct roles in spinal sensory processing

Kókai

Luz

Fernandes

et al. 2022

J of Comparative Neurology

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“…The commercialized NO-selective fluorescent probe, DAX-J2 Red, was used in subsequent bioimaging assays. 47,48 First, HeLa cells were treated with a near-infrared DAX-J2 probe alone, and the probe-loaded HeLa cells were treated with the Ru-NO complex in the dark. They showed almost no fluorescence.…”

Section: Resultsmentioning

confidence: 99%

“…To further investigate whether the complex could be transported into the cell and NO could be released upon photoirradiation, confocal fluorescence imaging assay for NO in living cells was conducted. The commercialized NO-selective fluorescent probe, DAX-J2 Red, was used in subsequent bioimaging assays. , First, HeLa cells were treated with a near-infrared DAX-J2 probe alone, and the probe-loaded HeLa cells were treated with the Ru-NO complex in the dark. They showed almost no fluorescence.…”

Section: Resultsmentioning

confidence: 99%

“…Cells were plated on the bottom of a cell culture dish (30 mm) and allowed to adhere for 12 h. Before experiments, cells were washed three times with phosphate buffer saline (PBS). For imaging of intracellular basal NO, cells were directly treated with commercialized fluorescent NO probes DAX-J2 Red (5 μM, 20 min). , For imaging of photoinduced NO release, the cells were pretreated with DAX-J2 Red (5 μM) in PBS for 20 min and then treated with the Ru-NO complex (20 μM, 20 min). After each treatment, the cells were washed three times with PBS, and then measurements were performed using a Zeiss LSM 880 confocal fluorescence microscope.…”

Section: Methodsmentioning

confidence: 99%

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Structural and Photodynamic Studies on Nitrosylruthenium-Complexed Serum Albumin as a Delivery System for Controlled Nitric Oxide Release

et al. 2021

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How to deliver nitric oxide (NO) to a physiological target and control its release quantitatively is a key issue for biomedical applications. Here, a water-soluble nitrosylruthenium complex, [(CH3)4N][RuCl3(5cqn)(NO)] (H5cqn = 5-chloro-8-quinoline), was synthesized, and its structure was confirmed with 1H NMR and X-ray crystal diffraction. Photoinduced NO release was investigated with time-resolved Fourier transform infrared and electron paramagnetic resonance (EPR) spectroscopies. The binding constant of the [RuCl3(5cqn)(NO)]− complex with human serum albumin (HSA) was determined by fluorescence spectroscopy, and the binding mode was identified by X-ray crystallography of the HSA and Ru-NO complex adduct. The crystal structure reveals that two molecules of the Ru-NO complex are located in the subdomain IB, which is one of the major drug binding regions of HSA. The chemical structures of the Ru complexes were [RuCl3(5cqn)(NO)]− and [RuCl3(Glycerin)NO]−, in which the electron densities for all ligands to Ru are unambiguously identified. EPR spin-trapping data showed that photoirradiation triggered NO radical generation from the HSA complex adduct. Moreover, the near-infrared image of exogenous NO from the nitrosylruthenium complex in living cells was observed using a NO-selective fluorescent probe. This study provides a strategy to design an appropriate delivery system to transport NO and metallodrugs in vivo for potential applications.

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“…The observed presynaptic depression of glutamatergic terminals could be accomplished via a heterosynaptic process involving acetylcholine release and presynaptically expressed Gi-coupled M2 receptors. Alternatively, presynaptic NK1R activation could trigger a NOS dependent LTD, as described for the cerebral cortex (Matsumura et al, 2021).…”

Section: Cell-type Specific Neuropeptide Signaling In the Ventral Pal...mentioning

confidence: 99%

Differential Modulation of GABAergic and Glutamatergic Neurons in the Ventral Pallidum by GABA and Neuropeptides

Neuhofer

Kalivas

2023

eNeuro

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The ventral pallidum (VP) is an integral locus in the reward circuitry and a major target of GABAergic innervation of both D1-medium spiny neurons (MSNs) and D2-MSNs from the nucleus accumbens (NAc). The VP contains populations of GABAergic (VPGABA, GAD2(+) or vGlut(-)) and glutamatergic (VPglutamate, GAD2(-) or vGlut(+)) cells that facilitate positive reinforcement and behavioral avoidance, respectively. MSN efferents to the VP exert opponent control over behavioral reinforcement with activation of D1-MSN afferents promoting and D2-MSN afferents inhibiting reward seeking. How this afferent-specific and cell type-specific control of reward-seeking is integrated remains largely unknown.Besides GABA, D1-MSNs co-release substance P to stimulate NK1 receptors and D2-MSNs co-release enkephalin to activate mu-opioid and delta-opioid receptors. These neuropeptides act in the VP to alter appetitive behavior and reward-seeking.Using a combination of optogenetics and patch-clamp electrophysiology in mice we found that GAD2(-) cells receive weaker GABA input from D1-MSN but GAD2(+) receive comparable GABAergic input from both afferents types. Pharmacological activation of µ-opioid receptors induced an equally strong presynaptic inhibition of GABA and glutamate transmission on both cell types. Interestingly, MOR activation hyperpolarized VPGABA but not vGlut(+). NK1R activation inhibited glutamatergic transmission only on vGlut(+) cells.Our results indicate that the afferent-specific release of GABA and neuropeptides from D1- and D2-MSNs can differentially influence VP neuronal subtypes.Significance StatementLittle is known about the cell type-specific modulation of neurotransmission by the neuropeptides co-released with GABA from striatal D1 and D2 synapses. We explored the differential micro-circuitry of the D1 and D2 inputs to the GABAergic and glutamatergic neuronal subpopulations in the ventral pallidum. Based on differential electrophysiological actions of D1 and D2 GABAergic and peptidergic inputs we propose a circuit-based model that partly explains the different actions of D1- and D2-MSN afferents in the ventral pallidum to regulate reward behaviors.

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Presynaptic NK1 Receptor Activation by Substance P Suppresses EPSCs via Nitric Oxide Synthesis in the Rat Insular Cortex

Cited by 5 publications

References 48 publications

Quantitative spatial analysis reveals that the local axons of lamina I projection neurons and interneurons exhibit distributions that predict distinct roles in spinal sensory processing

Quantitative spatial analysis reveals that the local axons of lamina I projection neurons and interneurons exhibit distributions that predict distinct roles in spinal sensory processing

Structural and Photodynamic Studies on Nitrosylruthenium-Complexed Serum Albumin as a Delivery System for Controlled Nitric Oxide Release

Differential Modulation of GABAergic and Glutamatergic Neurons in the Ventral Pallidum by GABA and Neuropeptides

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