Substance P modulates the sensitivity of the nicotinic receptor in amphibian cholinergic transmission

Akasu, Takashi; Kojima, Masayasu; Koketsu, K.

doi:10.1111/j.1476-5381.1983.tb11057.x

Cited by 61 publications

(27 citation statements)

References 31 publications

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“…These results are different from a recent report on bullfrog sympathetic ganglia in which, after a 2-to 3-min bath application of substance P, the peptide apparently decreased the peak current response to iontophoretically applied AcCho by =40% with no effect on the time course of current decay (14). The discrepancy between the results is difficult to resolve given the different preparations studied.…”

Section: Discussioncontrasting

confidence: 99%

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Substance P modulation of acetylcholine-induced currents in embryonic chicken sympathetic and ciliary ganglion neurons.

Role¹

1984

Proc. Natl. Acad. Sci. U.S.A.

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Substance P has been identified by combined immunohistochemical and radioimmunological techniqueslto be present in preganglionic cholinergic and sensory nerve fibers of amphibian, mammalian, and avian autonomic ganglia. The peptide has been shown to depolarize sympathetic neurons of frog and guinea pig and to decrease the cholinergic activation of Na' influx and catecholamine release from chromaffin cells. The aim of this study was to examine the interaction of acetylcholine and substance P on autonomic neurons. This report demonstrates a direct effect of substance P on acetylcholine-induced inward currents in both sympathetic and parasympathetic neurons clamped near resting membrane potential. Under these conditions, substance P dramatically enhances the rate of decay of the inward current in the continued presence of agonist without substantially affecting peak inward current. This effect is consistent with an enhancement of acetylcholine-receptor desensitization. Since substance P-containing cell bodies have been demonstrated in the avian (preganglionic) column of Terni as well as in fibers from the nucleus of Edinger-Westphal, the observed peptide inhibition of cholinergic activation of the neurons may function physiologically to modulate synaptic function in autonomic ganglia.Over the last 10 years, more than 30 peptides have been found in mammalian nervous tissue. The further demonstration that many of these peptides coexist with more "classical" neurotransmitters underscores the enormous potential for diversity of chemical signaling in the nervous system. The functional roles so far elucidated for various peptides are quite diverse. Perhaps most intriguing, however, in light of peptide-transmitter coexistence, are the modulatory actions of peptides on the effects of classical neurotransmitters. Among these are potentiation by vasoactive intestinal polypeptide of acetylcholine (AcCho)-induced secretion from acinar cells (1), inhibition by substance P of AcCho activation of the Renshaw cell (2) and the chromaffin cell (3-5), and potentiation by substance P and somatostatin of f3 adrenergic activation of astrocytes (6).In the avian nervous system, immunohistochemical techniques have demonstrated substance P in preganglionic cell bodies within both the column of Terni and the nerve fibers from the Edinger-Westphal nucleus (7-9). In the ciliary ganglion, substance P-containing terminals from these preganglionic neurons contact most of the postganglionic cells (7,8). The presence of substance P in both sympathetic and parasympathetic ganglia of many species (7,8,(10)(11)(12)(13) This paper reports that substance P selectively modulates AcCho-induced depolarization and inward current in chicken sympathetic and parasympathetic neurons. The observed increase in the rate of decay of the AcCho-induced current by substance P occurs immediately and in the absence of substantial effects on peak current. Furthermore, substance P has no direct effect on membrane potential or resting membrane resistance. These re...

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Section: Discussioncontrasting

confidence: 99%

“…ref. 14), although several studies have demonstrated a direct depolarization of mammalian and amphibian sympathetic neurons by the peptide (15)(16)(17)(18).…”

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confidence: 99%

Substance P modulation of acetylcholine-induced currents in embryonic chicken sympathetic and ciliary ganglion neurons.

Role¹

1984

Proc. Natl. Acad. Sci. U.S.A.

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“…This inhibitory action of SP was markedly enhanced by pre-exposure to SP for 10min before nicotine (Figure 4). Inhibitory effects of SP on the nicotinic responses have been described for a number of different preparations including cat spinal Renshaw cells (Belcher & Ryall, 1977;Krnjevic & Lekic, 1977), bovine isolated chromaffin cells (Livett et al, 1979;Role et al, 1981;Boksa & Livett, 1984b), frog sympathetic ganglia and skeletal muscle endplates (Akasu et al, 1983), (Stallcup & Patrick, 1980;Simasko et al, 1985;Boyd & Leeman, 1987), BC3H1 cells (Simasko et al, 1985) and rat adrenal gland slices (Nieber & Oehme, 1987). This action which is Ca2"-dependent and specific to nicotinic receptor function (Boksa & Livett, 1984b;Role et al, 1981) has an IC50 for SP of about 10-6M (Boksa & Livett, 1984b;Simasko et al, 1987).…”

Section: Discussionmentioning

confidence: 99%

Substance P modulates the time course of nicotinic but not muscarinic catecholamine secretion from perfused adrenal glands of rat

Zhou

Marley

Livett

1991

British J Pharmacology

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1 Substance P (SP) and acetylcholine (ACh) are contained within the splanchnic nerve terminals in the adrenal gland and can be released in response to stress. In the rat, the release of ACh brings about secretion of catecholamines (CA) by acting on nicotinic and muscarinic receptors on the adrenal chromaffin cells. 2 In the present study, we have used a rat isolated adrenal gland preparation to investigate the effects of SP, perfused at different concentrations, on CA secretion evoked by 10-sM nicotine and 10-M muscarine. 3 In the first 10min stimulation period (Si), in the absence of SP, nicotine (10-sM) evoked substantial and equal secretion of noradrenaline (NA) and adrenaline (Ad). In a second 10min stimulation period (S2), carried out 18 min after SI, the nicotinic response was desensitized. In contrast, the muscarinic response, which preferentially evoked Ad secretion in Si (Ad/NA: 8.7/1), was well maintained in S2. 4 SP present in SI had no effect on desensitization of the subsequent nicotinic response in S2.5 At low concentrations (10--10-'0M), SP changed the time course of nicotine-induced CA secretion during SI by enhancing CA secretion in the first 4min and inhibiting CA secretion thereafter. The maximal effect occurred at 10-M SP. 6 At a higher concentration (10 5 M), SP inhibited total nicotinic CA secretion throughout SI and produced a biphasic secretion of CA (depressed in the presence of SP and enhanced after wash out of SP).Pre-exposure of adrenal glands to SP (10-' to 10-M) for 10min produced marked inhibition of the nicotine-induced CA secretion. 7 In contrast to the effect of SP on the nicotinic response, SP from 10-to 10-SM had no effect on muscarinic CA secretion. 8 This difference in sensitivity of the nicotinic and muscarinic responses to SP points to a diversity of mechanisms available for control of adrenal catecholamine secretion. In addition to the ability of SP to increase or decrease the total amount of adrenal CA secretion, dependent on the concentration of SP, the present study shows that SP can change the time-course of nicotinic CA secretion. These results with the rat adrenal gland perfused in vitro suggests both a quantitative and temporal role for SP as a novel modulator of adrenal CA secretion.

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“…None of these substances alter the equilibrium potential [7,8,9,17,43]. The time constant of the falling phase of the end-plate current is not decreased by catecholamines [43] and polypeptides [8,9], suggesting that these transmitters change the conductance of the single channel. One interesting characteristic of the nicotinic ACh-receptor is desensitization.…”

Section: A) Experimental Evidencementioning

confidence: 99%

“…AKASU et al [9] reported that substance-P decreased the sensitivity of the nicotinic ACh-receptor in bullfrog sympathetic ganglion cells and at frog skeletal muscle endplates. Analyses of the effects of substance-P on the dose-response relationship for the ACh-current indicated that the action of substance-P is similar to that of LH-RH [8].…”

Section: A) Experimental Evidencementioning

confidence: 99%

Modulation of receptor sensitivity and action potentials by transmitters in vertebrate neurones.

Koketsu

1984

Jpn.J.Physiol

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According to the classical concept of synaptic transmission, it occurs at a synapse where a presynaptic nerve terminal (synaptic knob) comes in close contact with the subsynaptic membrane of a postsynaptic neurone. A very narrow gap,, called the synaptic cleft, separates the pre-and subsynaptic membranes. Transmitters released from presynaptic nerve terminals diffuse across the synaptic cleft andd interact with receptors which are located at the subsynaptic membrane. The action of the transmitter is very rapid and powerful. The interaction of the transmitter with receptors results in the generation of a postsynaptic potential. The size of the postsynaptic potential is indicative of the efficiency of synaptic transmission. The postsynaptic potential (PSP) can be either an excitatory postsynaptic potential (EPSP) or an inhibitory postsynaptic potential (IPSP). When the EPSP depolarizes the postsynaptic membrane to a critical membrane potential, an action potential is produced which propagates along the membrane of the postsynaptic neurone.Such a typical transmission does not always occur. In many cases, a neurone which releases a transmitter does not make close contact with its target neurones. In general, endogenous substances, such as transmitters or hormones, reach the membranes of their target neurones via many different routes after they are released. Thus the actions of endogenous substances reaching remote target neurones should be relatively weak and slow, but sustained. This is different from the typical synaptic transmission. Furthermore, the mode of action of these substances may be more complex. The combination of these substances with their target receptors changes the physiological state of target neurones in a variety of ways. These actions of endogenous substances are considered to be modulatory on the target neurones.There appear to be at least four different types of modulatory actions by transmitters. In type 1 modulation, a transmitter acts on the membrane of a target neurone and changes the amount of transmitter or hormone released from the target neurone. Much research has been devoted to this type of modulatory action of transmitters, especially in connection with presynaptic inhibition. In type 2 modulation, the transmitter changes the sensitivity of a receptor located on

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Substance P modulates the sensitivity of the nicotinic receptor in amphibian cholinergic transmission

Cited by 61 publications

References 31 publications

Substance P modulation of acetylcholine-induced currents in embryonic chicken sympathetic and ciliary ganglion neurons.

Substance P modulation of acetylcholine-induced currents in embryonic chicken sympathetic and ciliary ganglion neurons.

Substance P modulates the time course of nicotinic but not muscarinic catecholamine secretion from perfused adrenal glands of rat

Modulation of receptor sensitivity and action potentials by transmitters in vertebrate neurones.

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