Patch- and voltage-clamp analysis of cyclic AMP-stimulated inward current underlying neurone bursting

Green, Daniel; Gillette, Rhanor

doi:10.1038/306784a0

Cited by 81 publications

(51 citation statements)

References 21 publications

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“…Analogous to this logic, it is interesting to speculate if 5-HT sulfate, but not 5-HT, regulates ApC/EBP diurnal expression in the eye (Hattar et al 2002). 5-HT neuromodulation in gastropod mollusks is mediated, in part, through the activation of slow, depolarizing ion currents readily observable in voltage clamp recordings of Aplysia and Pleurobranchaea MCC, buccal, and pedal G neurons (Green and Gillette 1983). Investigation of the electrogenic effects of 5-HT sulfate has so far not shown any of the excitatory effects exhibited by native 5-HT.…”

Section: Discussionmentioning

confidence: 99%

Systemic serotonin sulfate in opisthobranch mollusks

Stuart¹,

Ebaugh²,

Copes³

et al. 2004

Journal of Neurochemistry

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Serotonin (5-hydroxytryptamine, 5-HT) is a ubiquitous modulatory neurotransmitter with roles as a neurohormone and neurotransmitter. However, few studies have been performed characterizing this molecule and its related metabolites in circulating fluids. Here, we demonstrate native 5-HT sulfate, but much lower levels of 5-HT, in hemolymph of the marine mollusk Pleurobranchaea californica. The metabolite 5-HT sulfate forms from 5-HT uptake and metabolism in central ganglia of Aplysia californica and in the visceral nerve and eye of Pleurobranchaea, but not in hemolymph itself. In addition, 5-hydroxyindole acetic acid (5-HIAA), while not detected in hemolymph, forms in higher quantities than does 5-HT sulfate in the eye and visceral nerve, and c-glu-5-HT is also observed in this area but never in hemolymph. As systemic 5-HT sulfate appears not to originate from the optic region or from systemic 5-HT, 5-HT sulfate likely derives from the nervous system. Circulating 5-HT sulfate is at least 10-fold higher during the light portion of a 12 : 12-h light/dark cycle than during the dark portion (p < 0.0007), but there is no obvious trend for free systemic tryptophan (Trp) (p > 0.3) in Pleurobranchaea. 5-HT in mollusks is associated with general arousal state; thus, diurnal systemic changes in a 5-HT catabolite may reflect a regulatory role for indole catabolism in behavioral rhythms. Keywords: capillary electrophoresis, hemolymph, marine mollusk, serotonin, sulfation. Serotonin (5-hydroxytryptamine, 5-HT) is a biogenic amine responsible for a variety of tasks in the nervous system. For instance, 5-HT is implicated in learning and memory in the central nervous system (CNS) and emesis and peristaltic reflex in the enteric nervous system (ENS) (Bartsch et al. 2000;Buhot et al. 2000;Endo et al. 2000). Several organs serve as targets for 5-HT, but the fate of 5-HT in target tissues, let alone the physiological effects of the resulting metabolites, has not been fully ascertained. Knowledge of the products of transformed 5-HT, as well as their distribution patterns, will assist in illuminating the processes leading to impaired neurotransmission and eventually aid in designing compounds that could potentially inhibit disease in neural and surrounding tissues.Marine mollusks present an excellent model for the study of the nervous system because of their large cell somata and well-characterized neural networks. In gastropod mollusks, 5-HT is involved in many neurophysiological processes, including sensitization and facilitation of withdrawal reflexes (Hawkins et al. 1993), feeding behavior (Gillette and Davis 1977) and locomotion (McPherson and Blankenship 1991). However, 5-HT-related metabolites have received considerably less attention.Our laboratory recently demonstrated that 5-HT metabolism in Aplysia californica involves sulfation and c-glutamylation with trace amounts of monoamine oxidase activity present in the form of 5-hydroxyindole acetic acid (5-HIAA) (Stuart et al. 2003). In particular, 5-HT sulfate is present ...

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Section: Discussionmentioning

confidence: 99%

Systemic serotonin sulfate in opisthobranch mollusks

Stuart¹,

Ebaugh²,

Copes³

et al. 2004

Journal of Neurochemistry

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“…An increased K+-current has been observed in response to bath and intracellularly applied cAMP or its analogs to molluscan neurons (TREISTMAN, 1981;EWALD and ECKERT, 1983). On the other hand, several investigators have reported that intracellular injections of cAMP cause either an increase in inward current (PELLMAR, 1981;ALDENHOFF et al, 1983;GREEN and GILLETTE, 1983;KONO-NENKO et al, 1983;CONNOR and HOCKBERGER, 1984), or a decrease in outward current (KLEIN and KANDEL, 1980;DETERRE et al, 1982;KACZMAREK and STRUMWASSER, 1984) across the molluscan neuronal membranes.…”

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confidence: 99%

Influences of pressure-injected cyclic AMP on the membrane current and characteristics of an identified neuron of Aplysia kurodai.

1985

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The ionic mechanism of the effect of intracellularly injected adenosine 3',5'-cyclic monophosphate (CAMP) on the membrane of identified neuron L5 of Apl ysia kurodai was investigated with conventional voltage-clamp and ion-substitution techniques. The intracellular elevation of CAMP caused an inward current ('CAMP), which was not accompanied by a significant change in membrane conductance at potentials more hyperpolarized than -60 mV. The current increased over the voltage range (-50 to -30 mV) associated with a conductance decrease and decreased at potentials more hyperpolarized than -60 mV. Elevated intracellular CAMP was found to enhance a region of negative slope resistance in steady-state I -V relations. Duration of the 'CAMP was greatly prolonged by bath-applied isobutylmethylxanthine (50 ,uM), but imidazole (10 mM) had an opposite effect on the 'CAMP. Tolbutamide (5 mM), a protein kinase inhibitor, reduced the DAMP. The current was not affected by the presence of bath-applied TTX (50 µM), ouabain (50 /LM), or triaminopyrimidine (5 mM). Reduction of [Na+]o reversibly decreased the DAMP. Li+ could largely substitute for Nat Alterations of [K+]o, and bath application of 4-AP (5 mM) and TEA (30 mM) did not affect the DAMP, In the presence of Nat, Cl-, and divalent cations such as Ca2+ and Ba2+ inhibited the DAMP. These results suggest that fast elevation of intracellular cAMP induces a TTX-resistant slow Na+ inward current, and the current might be due to activation of CAMP-dependent protein kinase.

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“…The permeant, cyclic AMP analogue CPT-cyclic AMP has been shown to imitate the effects of intracellularly applied cyclic AMP in a number of preparations (see Gillette, 1983, andEwald &Eckert, 1983 for recent examples in molluscan neurones). This analogue, applied to the bathing medium at a 10/M concentration, caused an immediate and marked reduction in the K-dependent response to an ionophoretic application of carbachol (Fig.…”

Section: Effects Of Cholinergic Antagonists On the K Conductance And mentioning

confidence: 99%

“…14-2 elicits an inward current (see also Kononenko, Kostyuk & Scherbatko, 1983;Aldenhoff, Hofmeier, Lux & Swandulla, 1983b;Green & Gillette, 1983;Swandulla & Lux, 1984;Connor & Hockburger, 1984a). This inward current can be almost completely eliminated by increasing the Ca content of the sea water from 10 to 60 mM or by replacing the Na in the sea water by mannitol (see Fig.…”

Section: Effects Of Cholinergic Antagonists On the K Conductance And mentioning

confidence: 99%

Synaptic block of a transmitter‐induced potassium conductance in Aplysia neurones.

Kehoe¹

1985

The Journal of Physiology

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A voltage‐clamp study was made of a slow excitatory post‐synaptic potential (slow e.p.s.p.) that can be elicited in the medial cells of the left pleural ganglion of Aplysia californica by the firing of at least three different presynaptic neurones (labelled I, II and III). Each of these three neurones elicits other permeability changes in addition to the slow e.p.s.p., and all elements of these synaptic responses were shown to be mediated monosynaptically. The slow e.p.s.p., associated with an increase in membrane resistance, was shown to be due to a decrease in K permeability. When the slow e.p.s.p. was present spontaneously, it could be blocked by three compounds (tetraethylammonium (TEA), phenyltrimethylammonium (PTMA), or methylxylocholine (beta‐TM 10], all previously shown to block the cholinergic receptor that mediates an increase in K conductance in the medial cells (see Kehoe, 1972b). Furthermore, in ganglia in which no slow e.p.s.p. was seen in response to firing of the neurones I, II, and III, such a response became manifest when agonists capable of activating the cholinergic receptor were applied (e.g. acetylcholine (ACh), carbachol, arecoline, or F2268). The slow e.p.s.p. thus appears to result from the reduction, induced by any one of three 'blocking neurones', of a cholinergically controlled K conductance. Finally, when presynaptic neurone I (the only neurone tested) was fired shortly before or during the activation of presynaptic neurone IV, previously shown to be cholinergic (Kehoe, 1972b), the K component of the cholinergic post‐synaptic inhibitory potential was markedly reduced. The concentration at which a given agonist caused the manifestation of the synaptic diminution in K conductance (i.e. the slow e.p.s.p.) was found to be the same as that at which it caused a reduction in the synaptically activated, cholinergic, K‐dependent conductance elicited by presynaptic neurone IV. Intracellularly injected adenosine 3',5'‐cyclic monophosphate (cyclic AMP) imitated the effect of the 'blocking neurones' on the K conductance activated by bath‐applied cholinomimetics. This effect was superimposed on a cyclic‐AMP‐induced, voltage‐dependent inward current that disappeared when the cell was bathed in Na‐free sea water, or when the extracellular Ca concentration was increased to 60 mM. The effect of cyclic AMP on the cholinergic K conductance remained even after this cyclic‐AMP‐activated inward current was eliminated.(ABSTRACT TRUNCATED AT 400 WORDS)

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Patch- and voltage-clamp analysis of cyclic AMP-stimulated inward current underlying neurone bursting

Cited by 81 publications

References 21 publications

Systemic serotonin sulfate in opisthobranch mollusks

Systemic serotonin sulfate in opisthobranch mollusks

Influences of pressure-injected cyclic AMP on the membrane current and characteristics of an identified neuron of Aplysia kurodai.

Synaptic block of a transmitter‐induced potassium conductance in Aplysia neurones.

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