Characterization of Pardaxin-Induced Dopamine
Release from Pheochromocytoma Cells: Role of
Calcium and Eicosanoids
SALEH ABU-RAYA, EUGENIA BLOCH-SHILDERMAN, PETER I. LELKES, VICTORIA TREMBOVLER, ESTHER SHOHAMI,
YEHUDA GUTMAN and PHILIP LAZAROVICI
1
Department of Pharmacology and Experimental Therapeutics, School of Pharmacy, Faculty of Medicine, The Hebrew University of Jerusalem,
Jerusalem 91120, Israel (S.A.-R., E.B.-S., V.T., E.S., Y.G., P.L.); and Laboratory of Cell Biology, University of Wisconsin, Medical School,
Milwaukee Clinical Campus, Milwaukee, Wisconsin (P.I.L)
Accepted for publication August 5, 1998 This paper is available online at http://www.jpet.org
ABSTRACT
Pardaxin, an excitatory neurotoxin, induced dopamine release
from pheochromocytoma (PC12) cells both in the presence and
absence of extracellular calcium ([Ca]
o
). In the presence of
extracellular calcium, nifedipine, an L-type calcium channel
blocker, did not affect dopamine release, whereas 1,2-bis (2-
aminophenoxy) ethane N,N, N'N'-tetra-acetic acid (BAPTA), a
chelator of cytosolic calcium, and dantrolene, a blocker of
calcium release from intracellular stores, inhibited only partially
(30 – 40%) pardaxin-induced dopamine release. In the absence
of [Ca]
o
, BAPTA and dantrolene were ineffective. Pardaxin stim-
ulated the arachidonic acid (AA) cascade in PC12 cells inde-
pendently of [Ca]
o
. The phospholipase inhibitors mepacrine
and bromophenacyl bromide inhibited both pardaxin-induced
AA release and pardaxin-induced dopamine release. Dopamine
release induced by pardaxin also was blocked by the lipoxy-
genase inhibitors nordihydroguaiaretic acid, esculetin, and
2-(12-hydroxydodeca-5,10-diynyl)-3,5,6-trimethyl-1,4-benzo-
quinone. Under these conditions, a parallel reduction in 5-hy-
droxyeicosatetranoic acid release also was observed. Suppres-
sion of pardaxin-induced dopamine release by inhibitors of
phospholipase A
2
and lipoxygenase was more pronounced in
calcium-free medium. These results indicate the involvement of
the lipoxygenase pathway in pardaxin-induced dopamine re-
lease and suggest the use of this toxin as a novel pharmaco-
logical tool for investigating the mechanism of calcium-inde-
pendent neurotransmitter release.
Neurotransmitter release from the synaptic terminal oc-
curs via regulated secretion (exocytosis) as synaptic vesicles
fuse with the neuronal plasma membrane and release their
contents into the synaptic cleft. Regulated exocytosis of cat-
echolamines has been largely investigated in bovine adrenal
chromaffin cells (Burgoyne, 1991) and in rat pheochromocy-
toma (PC12) cells (Ahnert-Hilger et al., 1985). The secretory
vesicles of these cells, the chromaffin granules, store dopa-
mine, norepinephrine, ATP, and various proteins. The essen-
tial role of calcium in catecholamine secretion from chromaf-
fin cells has been well established (Burgoyne, 1991). The
concentration of cytosolic calcium ([Ca]
i
) is strictly regulated,
and it is thought that the increase in calcium concentration
within the microdomain of the active exocytotic zone allows
vesicles to fuse and release their catecholamines content
(Burgoyne and Morgan, 1995). [Ca]
i
can be increased because
of membrane depolarization, opening of receptor-operated
channels, or release of calcium from intracellular stores (Bur-
goyne, 1991).
In PC12 cells, membrane depolarization by KCl (Greene
and Rein, 1977a; DiVirgilio et al., 1987) resulted in an influx
of Ca
++
through depolarization-induced activation of volt-
age-sensitive calcium channels, thereby triggering exocytosis
(DiVirgilio et al., 1987). One of the secretagogues largely
investigated in PC12 cells is acetylcholine. Acetylcholine-
induced catecholamine release in PC12 cells is mediated both
by nicotinic and muscarinic receptors (Zerby and Ewing,
1996). Stimulation of nicotinic receptor in PC12 cells induced
catecholamine release (Greene and Rein, 1977b) by mem-
brane depolarization, which triggers the influx of extracellu-
lar calcium through voltage-dependent calcium channels
(Zerby and Ewing., 1996). Muscarinic agonists such as
Received for publication October 1, 1997.
1
Affiliated with the David R. Bloom Center for Pharmacy at the Hebrew
University.
ABBREVIATIONS: PX, pardaxin; BPB, 4-bromophenacyl bromide; CCH, carbachol; [Ca]
o
, extracellular calcium; [Ca]
i
, cytosolic-free calcium; Dan,
dantrolene; NDGA, nordihydroguaiaretic acid; AA861, 2-(12-hydroxydodeca-5,10-diynyl)-3,5,6-trimethyl-1,4-benzoquinone; AA, arachidonic acid;
5-HETE, 5-hydroxyeicosatetranoic acid; Fura-2-AM, acetoxymethyl ester of Fura-2; DMEM, Dulbecco’s modified Eagle’s medium; PC12,
pheochromocytoma cells; BAPTA, 1,2-bis(2-aminophenoxy)ethane-N,N,N'N'-tetra-acetic acid; PLA
2
, phospholipase A
2
; IP
3
, inositol 1,4,5-
trisphosphate.
0022-3565/99/2882-0399$03.00/0
THE JOURNAL OF PHARMACOLOGY AND EXPERIMENTAL THERAPEUTICS Vol. 288, No. 2
Copyright © 1999 by The American Society for Pharmacology and Experimental Therapeutics Printed in U.S.A.
JPET 288:399 –406, 1999
399