Endothelin B receptor Ca2+ signaling in shark vascular smooth muscle: participation of inositol trisphosphate and ryanodine receptors
1 Department of Cell and Molecular Physiology, University of North Carolina
at Chapel Hill, Chapel Hill, NC 27599, USA
2 Mount Desert Island Biological laboratory, Salisbury Cove, ME 04672,
USA
* Author for correspondence (e-mail: sfellner{at}med.unc.edu)
Accepted 10 June 1004
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Summary |
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Key words: calcium signaling, elasmobranch, cADPR, ryanodine, IP3, dogfish shark, Squalus acanthias
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Introduction |
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Endothelin is considered to be among the most potent initiators of vascular
contraction in mammalian species
(Yanagisawa et al., 1988); its
receptors are sub-classified into ETAR and ETBR. In
mammals, activation of the ETAR on VSM is purely constrictive,
whereas stimulation of ETBR may cause either dilatation, by
promoting the release of nitric oxide (NO) and sometimes prostacyclin from
endothelial cells, or constriction of VSM
(D'Orleans-Juste et al., 2002
).
In S. acanthias, VSM of the ventral aorta and anterior mesenteric
artery appears to respond to ETBR but not ETAR agonist
stimulation (Evans, 2001
). The
ETBR-specific agonist sarafotoxin S6c (SRX) was as constrictive as
endothelin-1 (ET-1) to arterial rings.
In mammals, ET-1 has been shown to mobilize Ca2+ from the
endoplasmic (ER) or sarcoplasmic reticulum (SR) via activation of
both the IP3R and RyR (Shimoda
et al., 2000). Cyclic ADP-ribose (cADPR) is synthesized from
nicotinamide adenine dinucleotide (NAD) following ET-1 stimulated ADP-ribosyl
cyclase activity. Then cADPR activates the RyR, causing a release of
Ca2+ from the endoplasmic or sarcoplasmic reticulum. Involvement of
cADPR in ET-1 induced contraction has been demonstrated in rat mesenteric
small arteries (Giulumian et al.,
2000
). However, whether both ETAR and ETBR
activation signals involve both IP3R and RyR activation in VSM is
unknown. In rat peritubular smooth muscle of seminiferous tubules,
ETAR activation involves both IP3R and RyR whereas
ETBR works exclusively through the RyR via formation of
cADPR (Barone et al., 2002
).
That the dogfish shark appears to have only ETBR on VSM of the
aorta and anterior mesenteric artery raises the question of whether
ETBR signals through both IP3R and RyR or exclusively
through RyR. Thus investigating the participation of these SR receptors in
shark may answer important questions applicable to all vertebrate VSM. We have
utilized the specific ETBR agonists IRL-1620 and SRX to explore the
involvement of IP3R and RyR activation in the anterior mesenteric
artery of S. acanthias.
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Materials and methods |
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The anterior mesenteric artery was dissected and placed in ice-cold
Ca2+-free shark Ringer (pH 7.7) containing, in mmol l-1,
NaCl, 275; KCl, 4; MgCl2, 3; Na2SO4, 0.5;
KH2PO4, 1.0; NaHCO3, 8; urea, 350;
D-glucose, 5; and trimethylamine oxide (TMAO), 72
(Fellner and Parker, 2002).
The complete buffer contained 2.5 mmol l-1 calcium (normal
concentration in the shark), whereas no CaCl2 was added to the
nominally calcium-free buffer. Unless otherwise specified, the Ca2+
concentration in the buffer was 2.5 mmol l-1. The anterior
mesenteric artery was minced into pieces <0.5 mm in size and then loaded
with the Ca2+-sensitive fluorescent dye, fura-2AM. Cytosolic
[Ca2+]i was measured as previously described (Fellner
and Arendshorst, 2000
,
2002
;
Fellner and Parker, 2002
).
Arterial tissue was placed in an open static chamber and examined in a small
window of the optical field of a x40 oilimmersion fluorescence objective
of an inverted microscope (Olympus IX70, Tokyo, Japan). Approximately 5-6
typical elongated vascular smooth muscle cells were selected for analysis. The
tissue was excited alternately with light of 340 and 380 nm wavelengths from a
dual-excitation wavelength Delta-Scan equipped with dual monochronometers and
a chopper (Photon Technology International, NJ, USA). After passing signals
through a barrier filter (510 nm), fluorescence was detected by a
photomultiplier tube. The calibration of [Ca2+]i was
based on the signal ratio at 340/380 nm and known concentrations of
Ca2+ (Grynkiewicz et al.,
1985
) and was performed prior to initiating the experimental
protocol.
The concentrations of ET-1, IRL 1620 and SRX that we employed in each
experiment were 2x10-7 mol l-1, a concentration at
least twice the maximal stimulatory concentrations reported in the literature
(Just et al., 2004;
Touyz et al., 1995
;
Shimoda et al., 2000
;
Yanagisawa et al., 1988
;
Cavarape et al., 2003
;
Batra et al., 1993
). The
concentrations of antagonists were at least tenfold greater than that of the
agonists and were also chosen on the basis of values reported in the
literature.
Reagents
TMAO, Ruthenium Red, 8-Br cADPR, 8-(N,N-diethylamino) octyl
3,4,5-trimethoxybenzoate (TMB-8) and 2-aminoethyl diphenyl borate (2-APB) were
purchased from Sigma (St Louis, MO, USA), ET-1 and IRL-1620 from California
Peptide Research (Napa, CA, USA), ryanodine from Calbiochem (San Diego, CA,
USA), sarafotoxin S6c from American Peptide (Sunnyvale, CA, USA) and fura-2AM
from Teflab (Austin, TX, USA).
Statistics
The data are presented as means ± standard error of the mean
(S.E.M.). Each data set is derived from
tissue originating from at least three different sharks. Paired data sets were
tested using Student's paired t-test. Multiple comparisons were
analyzed using one-way analysis of variance (ANOVA) for repeated measures
followed by Student-Neuman-Kuels post hoc test. P<0.05
was considered statistically significant.
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Results |
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In VSM known to have both ETAR and ETBR, stimulation
first by IRL 1620 produces a peak response similar to that in shark mesenteric
artery; however, subsequent addition of ET-1 causes a second peak, which is
about twice the magnitude of the IRL 1620-induced peak
(Fellner and Arendshorst,
2004), showing that initial application of ETBR
agonists does not cause ETAR desensitization, at least in rat VSM.
It is conceivable that substantial differences exist between mammalian and
fish VSM. To further demonstrate that ET-1 activates ETBR but not
ETAR in shark VSM, we treated the VSM with IRL 1620; at the nadir
of the response we added ET-1. Fig.
1B, a representative tracing of the response of mesenteric artery
VSM to IRL 1620, illustrates the typical pattern in the shark mesenteric
artery VSM of a rise to a peak over a 10-20 s period and an unusually long
peak duration of nearly 100 s. When ET-1 was added at the nadir of the
[Ca2+]i response to IRL 1620, there was no further
significant increase in [Ca2+]i; the absolute value of
the IRL 1620 peak was 366±22, the nadir was 270±31 and that of
the subsequent ET-1 peak 282±30 nmol l-1 (N=8,
P=0.78 for ET-1 vs IRL 1620 nadir). These results suggest
but do not prove with certainty that ETBR is the exclusive ET-1
receptor in S. acanthias.
Response to IRL-1620 and endothelin-1 in Ca2+-Ringer
To confirm that the [Ca2+]i responses to IRL 1620 and
ET-1 were not different in Ringer containing Ca2+
(Ca2+-Ringer) compared to Ca2+-free Ringer, that is,
both in the presence of Ca2+ mobilization and entry and without the
possibility that SR depletion of Ca2+ was an issue, we performed
experiments in Ca2+-Ringer. The increase in
[Ca2+]i from baseline following IRL 1620 was
149±12 nmol l-1 (N=7) and that following ET-1 was
146±20 nmol l-1 (N=5), demonstrating again that
only ETB receptor activity is present in shark VSM (data not
shown).
Evidence for activation of the IP3 receptor
Having established that stimulation of ETBR but not
ETAR mobilized [Ca2+]i from the SR, we
investigated the mechanisms by which this occurs. To determine if
ETBR-coupled G protein activation results in formation of
IP3, activation of the IP3R and mobilization of
Ca2+ from the SR, we tested two inhibitors of the IP3R
in nominally Ca2+-free Ringer. In the presence of TMB-8
(10-5 mol l-1;
Palade et al., 1989), IRL 1620
increased [Ca2+]i by only 26.8±8 nmol
l-1 (N=8, P<0.01 vs IRL without
TMB-8). The compound 2-APB not only inhibits the IP3R but also
blocks Ca2+ entry via a store-operated Ca2+
entry channel in mammals (Broad et al.,
2001
; Maruyama et al.,
1997
) and in the dogfish shark
(Fellner and Parker, 2002
). In
Ca2+-free Ringer, only the effect on the IP3R can occur.
At concentrations of greater than 100 µmol l-1, 2-APB can
inhibit the SR/ER Ca2+-ATPase (SERCA), leading to a rise of
[Ca2+]i (Peppiatt et
al., 2003
). In the presence of 2-APB (50 µmol l-1)
there was no change in baseline [Ca2+]i
(P=0.88) and the [Ca2+]i response to IRL-1620
was reduced to 25.3±8 nmol l-1 (N=10,
P<0.01 vs IRL without 2-APB). Thus TMB-8 and 2-APB
inhibited the IRL 1620 response by 71%
(Fig. 2A,B).
|
Evidence for activation of the ryanodine receptor by cADPR
Cyclic ADP-ribose is synthesized from NAD by the action of cADPR, which
then stimulates the RyR to release Ca2+ from the
endoplasmic/sarcoplasmic reticulum in sea urchin eggs and a variety of
mammalian cell types (Guse,
2000; Lee, 2001
).
If the same systems operate in the shark, one might anticipate that
ETBR agonist stimulation of shark VSM would cause activation of the
ADPR cyclase, formation of cADPR and opening of the RyR to release
Ca2+ from the SR. To investigate this possibility, we treated VSM
with 8-Br cADPR (1 µmol l-1), a cell-permeant inhibitor of
activation of the RyR. The [Ca2+] response to IRL 1620 was reduced
to 53±8 nmol l-1 (N=16, P<0.01 for IRL
alone vs IRL with 8-Br cADPR). 8-Br cADPR alone caused an increase in
[Ca2+]i of 16±6 nmol l-1, which was
not different from baseline values. Fig.
3A is a representative tracing of the response of shark VSM to IRL
1620 in the presence of 8-Br cADPR.
|
To further address the participation of the RyR in the response to
activation of the ETBR, we treated shark VSM in
Ca2+-free Ringer with lower concentrations of ryanodine (5 µmol
l-1) to activate rather than close the RyR. This concentration of
ryanodine increased [Ca2+]i by 49±8 nmol
l-1 from baseline values (N=14, P<0.01).
Subsequent addition of IRL 1620 further increased
[Ca2+]i by only 28±6 nmol l-1
(Fig. 3B,C). This value is
significantly lower than that achieved by IRL 1620 following inhibition of the
RyR with 100 µmol l-1 ryanodine, Ruthenium Red (vide
infra) and 8-Br cADPR (P=0.02). Ryanodine at high concentrations
(>>10 µmol l-1) locks the RyR in a closed state
(Carroll et al., 1991).
Ryanodine (100 µmol l-1) did not change baseline values of
[Ca2+]i (N=11, P=0.47). Subsequent
addition of IRL 1620 increased [Ca2+]i by 54.3±5
nmol l-1 (N=11, P=0.01 vs IRL 1620
without ryanodine; Fig. 3B).
When shark anterior mesenteric artery VSM was pretreated with Ruthenium Red
(50 µmol l-1), an inhibitor of the RyR, basal
[Ca2+]i was unchanged and the addition of IRL 1620
caused an increase in [Ca2+]i of 57±5 nmol
l-1 (N=6, P<0.05 vs IRL 1620 without
Ruthenium Red). Taken together, the three inhibitors of the RyR diminished the
response of VSM to IRL 1620 by a mean of 39%
(Fig. 3D).
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Discussion |
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Having confirmed that ETBR and not ETAR seems to be
the ET-1 subtype responsible for stimulating a rise in
[Ca2+]i in the anterior mesenteric artery of the dogfish
VSM, we investigated the Ca2+ signaling pathways by which
ETBR activation elevates [Ca2+]i. To evaluate
the participation of IP3-mediated release of Ca2+ from
the SR, we employed two inhibitors of the IP3R, TMB-8 and 2-APB (50
µmol l-1). In Ca2+-free shark Ringer, these agents
inhibited the response to ETBR agonist stimulation by 71%. Although
2-APB has actions other than blockade of the IP3R, in
Ca2+-free Ringer, store-operated Ca2+ entry cannot
occur. While 2-APB can block SERCA Ca2+-ATPase, it is reported to
do so only at concentrations greater than 100 µmol l-1
(Peppiatt et al., 2003). TMB-8
has proven to be a reliable blocker of the IP3R in VSM in the rat
(Salomonsson and Arendshorst,
2001
; Purdy and Arendshorst,
2001
).
In mammalian VSM, the RyR participates in the process of Ca2+
mobilization following agonist stimulation of VSM. Stimulation of the RyR can
occur via several separate mechanisms: calcium-induced calcium
release (CICR) is a process by which an elevation of
[Ca2+]i (e.g. following activation of the
IP3R or entry through a voltage-gated Ca2+ channel) is
thought to stimulate the RyR, thereby augmenting the signal
(Galione and Churchill, 2002;
Lee, 1993
); alternatively,
IP3 may enhance ryanodine or cADPR binding to the RyR, creating a
site of crosstalk between the two signaling pathways
(Yusufi et al., 2002
). Another
mechanism involves the effect of cADPR on the RyR; cADPR-sensitive
Ca2+ stores have been described in a broad variety of cell types in
rat and mouse (Lee, 2001
). In
mammals, cADPR is both synthesized and hydrolyzed by the bifunctional protein
CD38 (White et al., 2003
).
There are only two reports of cADPR activity in fish, both in oocytes
(Fluck et al., 1999
;
Polzonetti et al., 2002
). The
current study is the first to demonstrate activity of cADPR in VSM of an
elasmobranch, S. acanthias. Utilizing three different inhibitors of
the RyR, including 8-Br cADPR, we found that the response to ETBR
agonist stimulation in Ca2+-free shark Ringer was inhibited by 39%.
These data are the first to demonstrate that the RyR participates in the
elevation of [Ca2+]i that is ultimately responsible for
vascular contraction in the dogfish shark. Whether endothelin-1 directly
activates the ADPR cyclase to form cADPR in the shark has not yet been studied
in VSM of any species.
That the sum of inhibition achieved by inhibitors of IP3R and
RyR was greater than 100% raises the question of whether there is
communication between the IP3R- and RyR-responsive compartments
within the SR. In canine pulmonary artery, for example, the SR of VSM appears
to have two spatially distinct compartments, whereas in renal artery they
communicate (Janiak et al.,
2001), demonstrating that there is heterogeneity of calcium stores
in vascular beds of a single species. Future studies will be required to
examine the compartmental organization of Ca2+ stores in the shark
SR.
The [Ca2+]i response of shark anterior mesenteric
artery VSM to ETBR stimulation in Ca2+-free Ringer was
characterized by a prolonged peak of approximately 100 s. This contrasts with
the short duration spike (<25 s) typical of the responses seen in mammalian
VSM (Schroeder et al., 2000).
The current studies were performed intentionally at 20-21°C, because shark
cells are accustomed to ambient temperatures of 13-17°C in the sea, and
our experience is that they lose viability at temperatures above 25°C. It
has previously been shown that the removal of Ca2+ from the cytosol
in mammalian cells is prolonged at reduced temperatures (13-27°C;
Shuttleworth and Thompson,
1991
), which may explain the long-duration peak response that we
observed.
Previous studies of dogfish ventral aorta demonstrated that acetylcholine
produced a concentration-dependent contraction of vascular rings whether or
not the endothelium was intact (Evans and
Gunderson, 1998). Furthermore, L-arginine, sodium
nitroprusside and nitric oxide (NO) produced significant contractions, a
finding opposite to that produced in mammalian VSM, in which dilation occurs
with these substances. More recently, it has been shown that there is evidence
for a vasodilatory effect of NO in S. acanthias in vivo, in animals
that were made severely hypoxic (E. Swenson, unpublished results). These
results suggest that under ordinary conditions, endothelial cell
ETBR has little or no role in vascular homeostasis in S.
acanthias.
One might ask if ETBR is the only ET-1 receptor type in
elasmobranchs. In shark rectal gland tubules, ET-1 regulates the xenobiotic
efflux pump multidrug resistance-associated protein iosform 2 (MRP2).
Inhibitors of ETBR but not ETAR prevented transport
(Miller et al., 2002). The
gill of the dogfish shark appears to express only ETBR; the
ETBR-specific agonists IRL 1620, SRX and BQ-3020 competed against
(125)IET-1 at a single site
(Evans and Gunderson, 1999
). A
band of muscle tissue has been identified on the periphery of the shark rectal
gland. ET-1 constricted the smooth muscle but the ETBR agonist SRX
did not, suggesting that ETAR might be the receptor involved
(Evans and Piermarini, 2001
).
Inhibitors of ETAR were not tried. It appears that ETBR
is an ancient receptor and that ETAR, now generally considered to
be the major vasoconstrictive sub-type of ET-1 in mammals, is a more recent
evolutionary event.
In summary, we have established for the first time in VSM of the elasmobranch Squalus acanthias that stimulation of the ETBR mobilizes Ca2+ from the SR via activation of both IP3R and RyR and that cADPR participates in the signaling process. We have confirmed that ETBR but not ETAR may be the exclusive receptor for the endothelin in shark VSM.
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List of abbreviations |
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Acknowledgments |
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References |
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