Potentiation of transmitter release from NMB human neuroblastoma cells by kappa-opioids is mediated by N-type voltage-dependent calcium channels

doi:10.1016/S0006-8993(99)01904-6

Brain Research

Volume 843, Issues 1–2, 2 October 1999, Pages 193-198

https://doi.org/10.1016/S0006-8993(99)01904-6 Get rights and content

Abstract

The selective kappa-opioid agonist trans-(±)-3,4-dichloro-N-methyl-N-[2-(1-pyrrolidinyl) cyclohexyl] benzenacetamidemethansulfonate (U50,488) potentiates both basal and depolarization-evoked $[^{3} H]$ dopamine release from NMB cells. The potentiation of dopamine release by U50,488 is mediated by N-type voltage-dependent calcium channels since it is blocked by omega-conotoxin, and is resistant to pertussis toxin (PTX)-treatment. When the stimulation of release by U50,488 is blocked by the N-channel antagonist omega-conotoxin, an inhibitory effect on dopamine release is revealed, suggesting that stimulatory and inhibitory effects of U50,488 are exerted in parallel.

Section snippets

Acknowledgements

This study was supported by a grant from the Anti-Drug Authority of Israel.

References (43)

Y. Baumhaker et al.
Characterization of a triple opioid system in the human neuroblastoma NMB cell line
Brain Res.
(1994)
S.M. Crain et al.
Opioids can evoke direct receptor-mediated excitatory effects on sensory neurons
Trends Pharmacol. Sci.
(1990)
T. Endoh et al.
The regulating manner of opioid receptors on distinct types of calcium channels in hamster submandibular ganglion cells
Arch. Oral Biol.
(1998)
P.S. Eriksson et al.
Kappa-opioid receptors on astrocytes stimulate L-type Ca²⁺ channels
Neuroscience
(1993)
S.F. Fan et al.
Opioids at low concentration decrease openings of K⁺ channels in sensory ganglion neurons
Brain Res.
(1991)
S.F. Fan et al.
Dual regulation by mu, delta and kappa opioid receptor agonists of K⁺ conductance of DRG neurons and neuroblastoma×DRG neuron hybrid F11 cells
Brain Res.
(1995)
A. Fields et al.
Multiple effects of opiates on intracellular calcium level and on calcium uptake in three neuronal cell lines
Brain Res.
(1995)
A. Fields et al.
The stimulatory effect of opioids on cyclic AMP production in SK-N-SH cells is mediated by calcium ions
Life Sci.
(1997)
K. Hirai et al.
Methionine enkephalin presynaptically facilitates and inhibits bullfrog sympathetic ganglionic transmission
Brain Res.
(1988)
O. Keren et al.
Dual regulation by opioids of $[^{3} H]$ norepinephrine release in the human neuroblastoma cell line SK-N-SH
Brain Res.
(1994)

O. Keren et al.

Opioids potentiate transmitter release from SK-N-SH human neuroblastoma cells by modulating N-type calcium channels

Brain Res.

(1997)

R.J. Knox et al.

Effects of selective and non-selective kappa-opioid receptor agonists on cutaneous C-fibre-evoked responses of rat dorsal horn neurons

Brain Res.

(1987)

M.H. Makman et al.

Modulation of adenylate cyclase activity of mouse spinal cord-ganglion explants by opioids, serotonin and pertussis toxin

Brain Res.

(1988)

L. Oron et al.

Effect of opioid peptides on electrically evoked acetylcholine release from Torpedo electromotor neurons

Neurosci. Lett.

(1991)

Y. Sarne et al.

Dissociation between the inhibitory and stimulatory effects of opioid peptides on cAMP formation in SK-N-SH neuroblastoma cells

Biochem. Biophys. Res. Commun.

(1998)

K.F. Shen et al.

Dual opioid modulation of the action potential duration of mouse dorsal root ganglion neurons in culture

Brain Res.

(1989)

K.F. Shen et al.

Cholera toxin-A subunit blocks opioid excitatory effects on sensory neuron action potentials indicating mediation by Gs-linked opioid receptors

Brain Res.

(1990)

D. Smart et al.

The stimulatory effects of opioids and their possible role in the development of tolerance

Trends Pharmacol. Sci.

(1996)

H. Tomura et al.

Enkephalin induces Ca²⁺ mobilization in single cells of bradykinin-sensitized differentiated neuroblastoma hybridoma (NG108-15) cells

Neurosci. Lett.

(1992)

L.L. Werling et al.

Opioid receptor regulation of the release of norepinephrine in brain

Neuropharmacology

(1987)

H. Xu et al.

Opioids can enhance and inhibit the electrically evoked release of methionine-enkephalin

Brain Res.

(1989)

Cited by (8)

Contribution of G inhibitory protein alpha subunits in paradoxical hyperalgesia elicited by exceedingly low doses of morphine in mice
2011, Life Sciences
Citation Excerpt :
Depending on the type of cell used and dose applied, opioids can induce hyperpolarization or depolarization and either inhibit or stimulate neuronal cells. On the basis of electrophysiological studies, it was suggested that either stimulatory or inhibitory influence on neurones by opioid agonists depends on the dose applied (North and Uchimura, 1989; Crain and Shen, 1990; Smart and Lambert, 1996; Keren et al., 1999). Studies in primary dorsal root ganglion cultures showed that neuronal stimulation occurred at nanomolar concentrations of opioids whereas inhibition occurred at micromolar concentrations.
Although morphine, at higher doses, induces analgesia, it may also enhance sensitivity to pain at extremely low doses as shown in studies for testing an animal's sensitivity to pain. We used an antisense approach capable of selectively down-regulating in vivo G_i(G inhibitory protein),G_o and G_s members of the G_α sub-family protein subunits in order to establish if these proteins might be implicated in the effects induced by extremely low morphine doses on acute thermonociception.
Mice pretreated with a morphine hyperalgesic dose (1 μg/kg) were submitted to hot plate test after pre-treatment with antisense oligodeoxynucleotides (aODNs) targeting G_iα, G_oα and G_sα regulatory proteins. The association of G-protein (guanine nucleotide-binding regulatory protein) coupled receptors with G protein was investigated using co-immunoprecipitation procedure.
The downregulation of the G_iα1–3 and G_oα1 proteins reversed the licking latency responses induced by 1 μg/kg morphine administration toward the basal value whereas downregulation of the G_oα2 and G_sα proteins did not significantly modify the hyperalgesic response.
These results suggest that G inhibitory proteins play a role in the production of low dose evoked morphine hyperalgesia in mouse. Immunoprecipitation studies revealed that both μ opioid receptor (μOR) and α₂ adrenoreceptor (α₂ AR) are bound to G inhibitory proteins in hyperalgesic response to morphine extremely low dose. Both μOR and α₂ AR appear to be necessary for low morphine dose induced hyperalgesic response through G inhibitory proteins.
G-protein-independent modulation of P-type calcium channels by μ-opioids in Purkinje neurons of rat
2010, Neuroscience Letters
P-type calcium channels play a key role in the synaptic transmission between mammalian central neurons since a major part of calcium entering pre-synaptic terminals is delivered via these channels. Using conventional whole-cell patch clamp techniques we have studied the effect of μ-opioids on P-type calcium channels in acutely isolated Purkinje neurons from rat cerebellum. The selective μ-opioid agonist DAMGO (10 nM) produced a small, but consistent facilitation of current through P-type calcium channels (10 ± 1%, n = 27, p < 0.001). The effect of DAMGO was rapid (less than 10 s) and fully reversible. This effect was both concentration and voltage-dependent. The EC₅₀ for the effect of DAMGO was 1.3 ± 0.4 nM and the saturating concentration was 100 nM. The endogenous selective agonist of μ-opioid receptors, endomorphin-1 demonstrated similar action. Intracellular perfusion of Purkinje neurons with GTPγS (0.5 mM) or GDPβS (0.5 mM), as well as strong depolarizing pre-pulses (+50 mV), did not eliminate facilitatory action of DAMGO on P-channels indicating that this effect is not mediated by G-proteins. Furthermore, the effect of DAMGO was preserved in the presence of a non-specific inhibitor of PKA and PKC (H7, 10 μM) inside the cell. DAMGO-induced facilitation of P-current was almost completely abolished by the selective μ-opioid antagonist CTOP (100 nM). These observations indicate that μ-type opioid receptors modulate P-type calcium channels in Purkinje neurons via G-protein-independent mechanism.
Different stimulatory opioid effects on intracellular Ca<sup>2+</sup> in SH-SY5Y cells
2000, Brain Research
Citation Excerpt :
However, from the middle of the 1970s, experiments began to show opioid might also take excitatory roles as well. For example, opiate were found to increase cAMP production [8,25], to enhance both L- and N-typed VOC channel [7,20], to elevate [Ca2+]i in NG108-15 cells (either through mobilization of Ca2+ store or through membrane depolarization) [10,11,30,36], to prolong action potential duration of DRG neuron [3,27–29], and finally to enhance transmitter release from SK-N-SH and NMB cells [15,16,23]. Some of the stimulatory effects are pertussis toxin (PTX) sensitive while others are cholera toxin (CTX) sensitive [3,28,29].
Present study revealed the stimulatory effects of δ opioid receptor on intracellular Ca²⁺ concentration ([Ca²⁺]_i) in SH-SY5Y cells. Fura-2 based single cell fluorescence ratio (F345/F380) was used to monitor the fluctuation of [Ca²⁺]_i. Application of the selective delta-opioid receptor agonist alone, [D-Pen^2,5]-enkephalin (DPDPE), hardly had any effects on cells cultivated for 3–10 days. However, after the cells had been pre-stimulated with cholinoceptor agonist, carbachol, variable calcium elevation was found in 59% of the cultures. The response was naltridole-reversible and dose-dependent, and was abolished completely by thapsigargin (TG) treatment but not by administration of CdCl₂ or 0-Ca²⁺ bath solutions. DPDPE-mediated [Ca²⁺]_i elevation was abolished by pertussis toxin (PTX) pretreatment but not cholera toxin (CTX), indicating coupling via G proteins of G_i/G_o subfamily. In 17.5% of the responding cells, biphase response was found which may be due to both the stimulatory and the inhibitory effects of opioid. On the other hand, in acutely dissociated cells, DPPDE alone induced [Ca²⁺]_i increase in 50% of the cultures. The probability and the amplitude of the elevation were decreased considerably by application of nifedipine or 0-Ca²⁺ bath solution and was little affected by application of TG. DPDPE activated [Ca²⁺]_i increase via a PTX-insensitive and CTX-sensitive pathway suggesting coupling through G_s subunit. All these indicated the opioid modulated the intracellular Ca²⁺ regulation system through different pathways. SH-SY5Y cell line might be a suitable model for the investigation of the complex mechanism which underlies opioid function.
Endogenous opiates: 1999
2000, Peptides
This paper is the twenty-second installment of the annual review of research concerning the opiate system. It summarizes papers published during 1999 that studied the behavioral effects of the opiate peptides and antagonists, excluding the purely analgesic effects, although stress-induced analgesia is included. The specific topics covered this year include stress; tolerance and dependence; learning, memory, and reward; eating and drinking; alcohol and other drugs of abuse; sexual activity, pregnancy, and development; mental illness and mood; seizures and other neurologic disorders; electrical-related activity; general activity and locomotion; gastrointestinal, renal, and hepatic function; cardiovascular responses; respiration and thermoregulation; and immunologic responses.
Mechanisms Underlying Positive Modulation of a Current through P-Type Calcium Channels in Purkinje Neurons by an Agonist of Opioid Receptors
2016, Neurophysiology
Neurotransmitter Modulation of Neuronal Calcium Channels
2003, Journal of Bioenergetics and Biomembranes

View all citing articles on Scopus

View full text

Short communicationPotentiation of transmitter release from NMB human neuroblastoma cells by kappa-opioids is mediated by N-type voltage-dependent calcium channels

Abstract

Section snippets

Acknowledgements

Brain Res.

Trends Pharmacol. Sci.

Arch. Oral Biol.

Neuroscience

Brain Res.

Brain Res.

Brain Res.

Life Sci.

Brain Res.

Brain Res.

Brain Res.

Brain Res.

Brain Res.

Neurosci. Lett.

Biochem. Biophys. Res. Commun.

Brain Res.

Brain Res.

Trends Pharmacol. Sci.

Neurosci. Lett.

Neuropharmacology

Brain Res.

Short communication
Potentiation of transmitter release from NMB human neuroblastoma cells by kappa-opioids is mediated by N-type voltage-dependent calcium channels