Dopamine suppresses neuronal activity of Helisoma B5 neurons via a D2-like receptor, activating PLC and K channels

Zhong, Lei; Artinian, Liana; Rehder, Vincent

doi:10.1016/j.neuroscience.2012.10.005

Cited by 10 publications

(9 citation statements)

References 40 publications

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“…CORM-2 was bath applied to isolated B5 neurons while their electrical activity was recorded using a whole-cell current clamp configuration. Prior to CO treatment, B5 neurons had resting membrane potentials (RMP) of -45.1 ± 0.8 mV (n = 25) and were spontaneously active producing a range of firing frequencies from 0.4 to 1.6 Hz, similar to our previous findings (Artinian et al, 2010, Zhong et al, 2013a. Following treatment with CORM-2 (5, 50, or 100 µM), all neurons showed hyperpolarization of the RMP and a decrease in firing frequency [ Fig (Ai and B)], which was statistically significant when compared with the solvent control DMSO (-0.27 ± 1.7 mV, n = 7, MWU, U = 0, p = 0.004).…”

Section: Carbon Monoxide Hyperpolarizes V M and Silences Spontaneous supporting

confidence: 85%

“…To study total calcium currents, membrane potential was held at -68.6 mV and stepped from -68.6 mV to + 68.6 mV for 500 ms by increments of +10 mV, as previously shown (Artinian et al, 2012, Zhong et al, 2013a. To characterize high VGCC currents, the membrane potential was first stepped to -28.6 mV for 200 ms to fully inactivate the low VGCC currents, followed by stepping the membrane potential from -68.6 to +68.6 mV for 500 ms. Low VGCC currents were calculated by subtraction of high VGCC currents from total calcium currents (Haydon and Man-Son-Hing, 1988).…”

Section: Measurement Of Voltage-gated Calcium Currentsmentioning

confidence: 99%

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Regulation of electrical activity and neuronal excitability in Helisoma trivolvis by carbon monoxide

et al. 2015

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Carbon monoxide (CO), like other gaseous neuromodulators, has a dual nature as both a toxic gas and a physiologically relevant signaling molecule. In the nervous system, high concentrations of CO can lead to neuronal injury while lower concentrations are found to be neuroprotective. The number of cellular targets affected by physiological concentrations of CO is rapidly growing and includes ion channels in various cell types. The modulation of ion channels by CO in neurons, however, and the effect it has on neural activity are incompletely understood. Here, the well-characterized buccal neurons, B5 and B19, of the freshwater snail, Helisoma trivolvis, were used to investigate the role that CO plays in regulating spontaneous firing activity and neuronal excitability. Neurons were studied in single-cell culture, thereby removing other signals normally present in the intact nervous system and allowing for the optimal characterization of physiological effects of CO. We found that the CO donor molecule, carbon monoxide releasing molecule-2 (CORM-2), hyperpolarized the resting membrane potential of B5 neurons and silenced their spontaneous firing activity. These effects were mediated through the inhibition of a persistent sodium current. CORM-2 also inhibited neuronal excitability. This effect was mediated by the inhibition of voltage-gated calcium channels by CO. The general findings of CO acting as a hyperpolarizing signal and an inhibitor of neuronal excitability extended to B19 neurons. Taken together, these findings suggest that CO is a potent modulator of ion channels with broad implications for the modulation of neural activity in a wide range of neuron-types.

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Section: Carbon Monoxide Hyperpolarizes V M and Silences Spontaneous supporting

confidence: 85%

Section: Measurement Of Voltage-gated Calcium Currentsmentioning

confidence: 99%

Regulation of electrical activity and neuronal excitability in Helisoma trivolvis by carbon monoxide

et al. 2015

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“…Identified B5 and B19 neurons were dissected from the buccal ganglia of the adult freshwater pond snail, Helisoma trivolvis , and plated in isolation onto poly‐ l ‐lysine (hydrobromide; molecular weight of 70,000–150,000; 0.25 mg/mL; Sigma) coated glass coverslips glued to the bottom of 35 mm cell culture dishes (Falcon 1008), as previously described (Zhong et al, , c). Briefly, neurons were cultured in 2 mL of conditioned medium at room temperature and used for experiments 24–48 h after plating, at which time neurons had extended neurites tipped by growth cones which were at least 140–180 µm (two cell body diameters for B19 and B5, respectively) from the soma.…”

Section: Methodsmentioning

confidence: 99%

The role of action potentials in determining neuron‐type‐specific responses to nitric oxide

Estes

Zhong

Artinian

et al. 2014

Developmental Neurobiology

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The electrical activity in developing and mature neurons determines the intracellular calcium concentration ([Ca(2+)]i), which in turn is translated into biochemical activities through various signaling cascades. Electrical activity is under control of neuromodulators, which can alter neuronal responses to incoming signals and increase the fidelity of neuronal communication. Conversely, the effects of neuromodulators can depend on the ongoing electrical activity within target neurons; however, these activity-dependent effects of neuromodulators are less well understood. Here, we present evidence that the neuronal firing frequency and intrinsic properties of the action potential (AP) waveform set the [Ca(2+)]i in growth cones and determine how neurons respond to the neuromodulator nitric oxide (NO). We used two well-characterized neurons from the freshwater snail Helisoma trivolvis that show different growth cone morphological responses to NO: B5 neurons elongate filopodia, while those of B19 neurons do not. Combining whole-cell patch clamp recordings with simultaneous calcium imaging, we show that the duration of an AP contributes to neuron-specific differences in [Ca(2+)]i, with shorter APs in B19 neurons yielding lower growth cone [Ca(2+)]i. Through the partial inhibition of voltage-gated K(+) channels, we increased the B19 AP duration resulting in a significant increase in [Ca(2+)]i that was then sufficient to cause filopodial elongation following NO treatment. Our results demonstrate a neuron-type specific correlation between AP shape, [Ca(2+)]i, and growth cone motility, providing an explanation to how growth cone responses to guidance cues depend on intrinsic electrical properties and helping explain the diverse effects of NO across neuronal populations.

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“…It has indeed been shown to inhibit in vitro PI-PLCs either from animals (Bleasdale and Fisher, 1993; Wilsher et al, 2007) or from plants (Takahashi et al, 2001; Helling et al, 2006). It is widely used in animals to study PI-PLC roles (Romano and Lograno, 2013; Zhong et al, 2013). In plants, U73122 was shown to lead to an increase of PI-PLC substrates in tobacco plasma membrane (Van Leeuwen et al, 2007) and in pollen tube tip (Helling et al, 2006).…”

Section: Discussionmentioning

confidence: 99%

The Arabidopsis DREB2 genetic pathway is constitutively repressed by basal phosphoinositide-dependent phospholipase C coupled to diacylglycerol kinase

Djafi¹,

Vergnolle²,

Cantrel³

et al. 2013

Front. Plant Sci.

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Phosphoinositide-dependent phospholipases C (PI-PLCs) are activated in response to various stimuli. They utilize substrates provided by type III-Phosphatidylinositol-4 kinases (PI4KIII) to produce inositol triphosphate and diacylglycerol (DAG) that is phosphorylated into phosphatidic acid (PA) by DAG-kinases (DGKs). The roles of PI4KIIIs, PI-PLCs, and DGKs in basal signaling are poorly understood. We investigated the control of gene expression by basal PI-PLC pathway in Arabidopsis thaliana suspension cells. A transcriptome-wide analysis allowed the identification of genes whose expression was altered by edelfosine, 30 μM wortmannin, or R59022, inhibitors of PI-PLCs, PI4KIIIs, and DGKs, respectively. We found that a gene responsive to one of these molecules is more likely to be similarly regulated by the other two inhibitors. The common action of these agents is to inhibit PA formation, showing that basal PI-PLCs act, in part, on gene expression through their coupling to DGKs. Amongst the genes up-regulated in presence of the inhibitors, were some DREB2 genes, in suspension cells and in seedlings. The DREB2 genes encode transcription factors with major roles in responses to environmental stresses, including dehydration. They bind to C-repeat motifs, known as Drought-Responsive Elements that are indeed enriched in the promoters of genes up-regulated by PI-PLC pathway inhibitors. PA can also be produced by phospholipases D (PLDs). We show that the DREB2 genes that are up-regulated by PI-PLC inhibitors are positively or negatively regulated, or indifferent, to PLD basal activity. Our data show that the DREB2 genetic pathway is constitutively repressed in resting conditions and that DGK coupled to PI-PLC is active in this process, in suspension cells and seedlings. We discuss how this basal negative regulation of DREB2 genes is compatible with their stress-triggered positive regulation.

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Dopamine suppresses neuronal activity of Helisoma B5 neurons via a D2-like receptor, activating PLC and K channels

Cited by 10 publications

References 40 publications

Regulation of electrical activity and neuronal excitability in Helisoma trivolvis by carbon monoxide

Regulation of electrical activity and neuronal excitability in Helisoma trivolvis by carbon monoxide

The role of action potentials in determining neuron‐type‐specific responses to nitric oxide

The Arabidopsis DREB2 genetic pathway is constitutively repressed by basal phosphoinositide-dependent phospholipase C coupled to diacylglycerol kinase

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