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Journal of Neuroscience, Vol 14, 1920-1929, Copyright © 1994 by Society for Neuroscience
Opioids mobilize calcium from inositol 1,4,5-trisphosphate-sensitive stores in NG108-15 cells
W Jin, NM Lee, HH Loh and SA Thayer
Department of Pharmacology, University of Minnesota Medical School, Minneapolis 55455.
Opioids elicit an increase in the intracellular free Ca2+ concentration
([Ca2+]i) in neuroblastoma x glioma hybrid NG108-15 cells, which, depending
upon growth conditions, results from either Ca2+ influx in differentiated
cells or Ca2+ release from internal stores in undifferentiated cells (Jin
et al., 1992). In this report we describe fura-2-based digital imaging
studies that demonstrate that opioid- evoked Ca2+ release in these cells
results from the activation of phospholipase C (PLC) and subsequent
mobilization of the inositol 1,4,5- trisphosphate (IP3)-sensitive store.
D-Ala2-D-Leu5-enkephalin (DA-DLE) evoked concentration-dependent increases
in [Ca2+]i (EC50 approximately equal to 4 nM). The response was blocked by
naloxone (1 microM). In single cells, sequential application of selective
opioid agonists (10 nM) evoked responses of the rank order DADLE = D-Pen2,
D-Pen5- enkephalin (DPDPE) > trans-(+/-) 3,4-dichloro-N-methyl-N-(2-[1-
pyrrolidinyl]cyclohexyl) benzeneacetamide (U50488) > D-ala2, N-Me-Phe4,
Gly5-ol-enkephalin (DAMGO), consistent with activation of a delta- opioid
receptor. Forty percent (n = 198) of the cells responded to 100 nM DADLE
with a net [Ca2+]i increase of 483 +/- 40 nM. Bradykinin (100 nM) elicited
a response in 91% of the cells with a mean net amplitude of 707 +/- 36 nM.
The DADLE-evoked responses were not blocked by removal of extracellular
Ca2+; instead, they were abolished by treatment with 10 nM thapsigargin, an
agent that depletes and prevents refilling of IP3-sensitive Ca2+ stores. A
1 microM concentration of U73122, an aminosteroid inhibitor of PLC,
completely blocked the DADLE- evoked [Ca2+]i increase, while an inactive
analog, U73433, was without effect. To explore the possible role of
G-proteins in mediating opioid- induced [Ca2+]i increases in NG108-15
cells, we pretreated cells with pertussis or cholera toxin; pertussis toxin
blocked the opioid-induced response while cholera toxin was without effect,
consistent with a Gi- or Go-mediated effect. Activation of the opioid
inhibitory pathway previously described for these cells appears to
stimulate the phosphoinositide (PI) cascade as well. Including the PI
cascade among the multiple second messenger systems modulated by opioids
may be key to understanding the biochemical events that underlie acute and
chronic opioid action.
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