Endothelin-1, superoxide and adeninediphosphate ribose cyclase in shark vascular smooth muscle
1 Mount Desert Island Biological Laboratory, Salisbury Maine 04672
USA
2 Department of Cell and Molecular Physiology, University of North Carolina
at Chapel Hill, Chapel Hill, NC 27599-7545, USA
* Author for correspondence (e-mail: sfellner{at}med.unc.edu)
Accepted 24 January 2005
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Summary |
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Key words: NAD(P)H oxidase, nicotinamide, CICR, ryanodine, calcium, shark, Squalus acanthias
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Introduction |
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Evidence for the presence of an ADPR cyclase and for a role of cADPR in
Ca2+ signaling has been established in a large number of mammalian
cell types (Guse, 1999;
Lee, 2001
). There are only two
reports of cADPR activity in fish, both in oocytes
(Polzonetti et al., 2002
;
Fluck et al., 1999
). Recently
we demonstrated a role for cADPR in endothelin B receptor
(ETBR)-mediated Ca2+ signaling in the anterior
mesenteric artery of Squalus acanthias
(Fellner and Parker, 2004
).
Participation of cADPR in Ca2+ signaling has been demonstrated from
a variety of mammalian vascular smooth muscle (VSM) sources: membrane
preparations of rat aorta (Yusufi et al.,
2002
; de Toledo et al.,
2000
), renal microvessels (Li
et al., 2000
), bovine and porcine coronary arteries
(Zhang et al., 2004
;
Yu et al., 2000
;
Kannan et al., 1996
), and
pulmonary artery (Wilson et al.,
2001
). The VSM ADPR cyclase has several unique properties that
distinguish it from CD38. In contrast to the ADPR cyclase of sea urchin eggs,
Aplysia and HL-60 cells, in which Zn2+ enhances the activity of the
enzyme, Zn2+ inhibits the cyclase of rat aortic VSM cells
(de Toledo et al., 2000
).
Furthermore, the VSM cyclase has a specific activity 20-fold greater than the
CD38 of HL 60 cells (de Toledo et al.,
2000
), suggesting that the enzyme may play an important role in
normal vascular physiology. Recently, it has been shown that oxidative stress
increases [Ca2+]i in fresh bovine coronary VSM cells
(Zhang et al., 2004
) and that
nitric oxide (NO) inhibits ADPR cyclase in bovine coronary artery. These
findings contrast with the stimulatory effect of NO in non-vascular cells such
as macrophages, pancreatic cells, neurons and sea urchin eggs
(Yu et al., 2000
).
Evidence for participation of cADPR in endothelin-1 (ET-1) Ca2+
signaling has been demonstrated in porcine airway smooth muscle
(White et al., 2003), rat
seminiferous peritubular smooth muscle
(Barone et al., 2002
), rat
mesenteric artery (Giulumian et al.,
2000
) and shark mesenteric artery VSM
(Fellner and Parker, 2004
).
None of these studies has explored the mechanism(s) by which ET-1 might
activate the ADPR cyclase. A link between ET-1 and the generation of
superoxide (O2.-) has been demonstrated in cultured A-10
cells (Sedeek et al., 2003
)
and human gluteal arterial VSM cells
(Touyz et al., 2004
). We
hypothesized that ET-1 might activate VSM NAD(P)H oxidases (NOX) causing the
generation of O2.- leading to the activation of the VSM
ADPR cyclase. Therefore, in the current study we utilized inhibitors of the
ADPR cyclase, an inhibitor of NOX and a superoxide dismutase mimetic to
investigate how ET-1 might activate the cyclase to generate cADPR. Because our
previous investigations of Ca2+ signaling pathways in shark VSM
have demonstrated remarkable concordance with those of mammalian VSM
(Fellner and Parker, 2004
), we
believe that the current study can give insight into the role of superoxide,
preserved during evolution, in the responses of VSM to peptide agonists.
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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 Ringers, 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; Hepes, 5, and
trimethylamine oxide (TMAO), 72 (Fellner
and Parker, 2002
). Calcium buffer contained 2.5 mmol
l-1 calcium (normal concentration in the shark;
Prosser and Kirschner, 1973
),
whereas no CaCl2 was added to the calcium-free buffer. The anterior
mesenteric artery was minced into pieces <0.5 mm in size and then loaded
with the Ca2+-sensitive fluorescent dye, fura-2AM at 13°C for
30 min in the dark in Ca2+-Ringers containing 0.5% bovine serum
albumin (BSA); the sample was washes three times with Ca2+-free
buffer and incubated for another 30 min at 18°C. Subsequent experiments
were conducted in a temperature-controlled room kept at 18°C.
Measurement of cytosolic free calcium concentration
[Ca2+]i was measured as previously described
(Fellner and Parker, 2004;
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 oil-immersion fluorescence
objective of an inverted microscope (Olympus IX70). All experiments were
conducted in a room maintained at 18°C. Approximately 5-6 typical
elongated vascular smooth muscle cells were selected for analysis. There were
no visible endothelial cells in the study sample. 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 (PTI), New Jersey, 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 with a calibration kit purchased from
Molecular Probes (Eugene, OR, USA).
Experimental protocol
The concentrations of ET-1 that we employed in each experiment was
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 also chosen on the basis of values reported
in the literature: Zn2+ (3 mmol l-1)
(de Toledo et al., 2000
),
nicotinamide (3 mmol l-1)
(Sethi et al., 1996
),
4-hydroxy-2,2,6,6-tetramethyl piperidinoxyl (TEMPOL; 1 mmol l-1)
(Zhang et al., 2004
;
Touyz et al., 2004
) and
diphenyl iodonium (DPI; 1 µmol l-1)
(Touyz et al., 2004
;
Rodriguez-Puyol et al., 2002
).
Tissue was preincubated with antagonists for at least 2 min before adding
ET-1.
Mesenteric VSM cells were analyzed only once and then discarded. All
experiments were conducted initially in Ca2+-free Ringers. After
responses to ET-1 in the presence or absence of inhibitors had concluded, we
added Ca2+ (final concentration, 2.5 mmol l-1), to
confirm tissue viability. Calcium entry via store-operated channels
or voltage-gated channels as well as operation of the calcium sensing receptor
(Fellner and Parker, 2002)
should increase [Ca2+]i. In the case of the
Zn2+ experiments however, because Zn2+ inhibits
voltage-gated Ca2+ entry
(Kerchner et al., 2000
) and
possibly store-operated Ca2+ entry
(Uehara et al., 2002
), the
effect of adding Ca2+ was markedly diminished. If there was no
Ca2+ response, that sample was discarded.
Reagents
Trimethylamine oxide (TMAO), nicotinamide, DPI, 2-aminoethoxy diphenyl
borate (2-APB) and TEMPOL were purchased from Sigma (St Louis, MO, USA),
endothelin-1 from California Peptide Research, Inc (Napa, CA, USA), fura-2-AM
from Teflab (Austin, TX, USA) and 3,4,5-trimethoxybenzoic
acid-8-(diethylamino) octyl ester (TMB-8; CalBiochem, La Jolla, CA, USA).
Statistics and graphics
The data are presented as means ±
S.E.M. Each data set is derived from tissue
originating from at least three different sharks. For representative tracings
of original data with ET-1 and antagonists, we selected data pairs from the
same experimental day. Paired data sets were tested with Student's paired
t-test. Multiple comparisons were analyzed using one-way analysis of
variance 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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Inhibitors of the ADPR cyclase
A major question is what is the relationship between agonist stimulation of
a G-protein-coupled receptor to initiate the sequence of IP3
generation, activation of the IP3R, release of Ca2+ from
the SR and participation of the RyR to augment the Ca2+ signal? And
further, what is the communication between ET-1 and the membrane ADPR cyclase
to direct formation of cADPR? If inhibitors of the ADPR cyclase diminish the
response of VSM cells to ET-1, one might infer that ET-1 is somehow sending a
message to the cyclase to increase the formation of cADPR. Both nicotinamide
and Zn2+ are well-studied inhibitors of the ADPR cyclase in
vascular smooth muscle (de Toledo et al.,
2000; Sethi et al.,
1996
). Neither of these antagonists is known to have an effect on
the IP3 receptor (IP3R). Nicotinamide (3 mmol
l-1) pretreatment of arterioles reduced the
[Ca2+]i response to ET-1 by 62% (40±6 nmol
l-1; N=15, P<0.01 for ET-1 alone vs
ET-1 + nicotinamide; Fig.
2A,C). In the presence of Zn2+ (3 mmol l-1),
the net response to ET-1 was decreased to 30±3 nmol l-1 (72%
inhibition; N=11, P<0.01;
Fig. 2B,C). Together, the
nicotinamide and Zn2+ experimental data suggest that there is a
pathway utilized by ET-1 that increases the activity of the ADPR cyclase and
that is independent of the IP3 pathway.
|
Blockade of superoxide generation or effect
To address the question of whether there is a connection between ET-1,
O2.- generation and ET-1-induced elevation of
[Ca2+]i, we employed the NOX inhibitor DPI
(Babior, 1999;
Touyz et al., 2004
). In the
presence of DPI (1 µmol l-1), the increase in
[Ca2+]i following addition of ET-1 was 39±7
(N=19, P<0.01 for ET-1 + DPI vs baseline, and
0.05 for ET alone vs ET + DPI;
Fig. 3A,C). To further examine
the role of O2.- in ET-1-mediated Ca2+
signaling in shark VSM, we utilized TEMPOL, a superoxide dismutase mimetic
(Evans et al., 2004
;
Sedeek et al., 2003
). When the
VSM was preincubated with TEMPOL (1 mmol l-1), the increase in
[Ca2+]i was 38±3 (N=19,
P<0.05 for ET-1 + TEMPOL vs baseline, and <0.01 for
ET-1 vs ET-1 + TEMPOL; Fig.
3B,C). These data, showing 63% inhibition of the ET-1-induced
[Ca2+]i response by DPI and TEMPOL, suggest that when
the production or duration of elevated O2.- is
diminished, the ability of ET-1 to mobilize Ca2+ from the SR and
increase [Ca2+]i is markedly reduced.
|
Simultaneous blockade of the IP3R and O2.- generation or effect
To substantiate the premise that ET-1 signals via two independent
pathways, namely the classic IP3 pathway and perhaps a NOX,
O2.-, ADPR cyclase pathway, we measured the
[Ca2+]i response to ET-1 in the presence of added TEMPOL
or of DPI plus 2-APB (33 µmol l-1) or DPI plus TMB-8 (1 µmol
l-1). We were unable to test TEMPOL plus TMB-8 because of
precipitation when the two reagents were combined. The
[Ca2+]i response to ET-1 in the presence of TEMPOL plus
2-APB was 19±6 nmol l-1 (82% inhibition, N=6,
P<0.01 vs TEMPOL alone). For DPI plus 2-APB, the
[Ca2+]i response was 17±6 nmol l-1
(84% inhibition, N=8, P=0.02 vs DPI alone). For DPI
plus TMB-8, the response was 18±4 nmol l-1 (83% inhibition,
N=9, P=0.01 vs DPI alone;
Fig. 4).
|
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Discussion |
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An enzyme capable of forming cADPR was first described in homogenates of
sea urchin eggs (Lee et al.,
1989) and subsequently has been shown to be present in a wide
variety of cell types (Lee,
1997
; Guse, 1999
,
2004
). In mammals, a single
bifunctional protein, CD38, can act as a cyclase or hydrolase for cADPR
(Lee et al., 1997
; reviewed by
Schuber and Lund, 2004
). This
unusual membrane-bound enzyme is stimulated by a number of different agonists
in specific mammalian cell types: for example, estrogen in myometrium
(Barata et al., 2004
); glucose
in pancreatic beta cells (Takasawa et al.,
1993
); retinoic acid and triiodothyronine (T3) in
aortic VSM cells (de Toledo et al.,
1997
); reactive oxygen species (ROS) in bovine coronary VSM
(Zhang et al., 2004
);
angiotensin II in neonatal cardiac myocytes
(Higashida et al., 2000
),
tumor necrosis factor-
and interleukin 1-ß in glomerular mesangial
cell (Yusufi et al., 2001
),
and acetylcholine and ET-1 in airway smooth muscle
(White et al., 2003
). How this
structurally diverse group of molecules mediates the same process, namely
activation of the ADPR cyclase, has not yet been elucidated with
certainty.
NAD(P)H oxidases are plasmalemmal enzymes that catalyze the production of
(O2.-) from two molecules of O2 (reviewed by
Babior, 1999). Although widely
studied in phagocytic cells, NOX has been more recently found to be present in
VSM and to be activated by peptide agonists such as angiotensin II
(Rajagopalan et al., 1996
).
There is now evidence for ET-1-induced activation of NOX and formation of
superoxide (O2.-) and reactive oxygen species (ROS) in
VSM (Sedeek et al., 2003
;
Touyz et al., 2004
;
Li et al., 2003
;
Galle et al., 2000
;
Wedgwood et al., 2001
). In
cultured rat aortic VSM cells, ET-1 dose dependently (10-8 to
10-6 mol l-1) increased the formation of
O2.- (Sedeek et al.,
2003
) and, in human gluteal VSM cells, similar results were noted
(Touyz et al., 2004
). DPI, an
inhibitor of NOX, diminished the ET-1-induced production of
O2.- only at high concentrations of ET (10-6
mol l-1) whereas thenotrifluoroacetone (TIFT), a mitochondrial
electron chain inhibitor, reduced the production of O2.-
at concentrations of ET-1 between 10-9 and 10-6 mol
l-1 (Touyz et al.,
2004
). To our knowledge, there have been no reports of a vascular
smooth muscle NOX, or NOX of any non-phagocytic cell origin, in fish. Our
finding of inhibition of the [Ca2+]i response to ET-1 by
the NOX inhibitor DPI and by the superoxide dismutase mimetic, TEMPOL, lends
support to the presence of generation of O2.- by NOX on
VSM of S. acanthias.
Recent studies have investigated a possible linkage between
O2.- generation, cADPR and changes in
[Ca2+]i, and vascular contraction in small bovine
coronary arteries (Zhang et al.,
2004). Xanthine/xanthine oxidase (X/XO), a
O2.- generating system, increased the activity of ADPR
cyclase and increased [Ca2+]i in fresh coronary artery
VSM cells. The elevation in [Ca2+]i was partially
blocked by 8-Br cADPR, nicotinamide, high concentrations of ryanodine and
tetracaine (Zhang et al.,
2004
). Other studies have likewise suggested that
O2.- increases that activity of ADPR cyclases
(Xie et al., 2003
;
Okabe et al., 2000
). In
cardiac myocytes, nearly nanomolar concentrations of
O2.- stimulated the synthesis of cADPR and
Ca2+ release (Okabe et al.,
2000
). Oxidation of cysteine residues of the cyclase results in
the formation of disulfide bond and dimers of the enzyme, which have much
greater activity than the monomer (Tohgo
et al., 1994
; Chidambaram et
al., 1998
). Taken together, these studies suggest that
ET-1-induced formation of O2.- may acutely increase the
activity of ADPR cyclase, possibly via dimerization of the
enzyme.
Superoxide generation may have other effects on
[Ca2+]i and the activity of ADPR cyclase. Superoxide
rapidly combines with nitric oxide (NO) to form peroxynitrate
(Gryglewski et al., 1986).
Nitric oxide has been shown to inhibit the ADPR cyclase of bovine coronary
arterial VSM cells (Yu et al.,
2000
). Thus, ET-1-stimulated O2.- production
may diminish available NO, thereby abolishing the usual inhibitory effect of
NO on the cyclase, and increasing both the ability of the cyclase to form
cADPR and its participation in CICR. There are vascular effects of
O2.- that are independent of cADPR. Nitrosylation of
tyrosine residues may impair the synthesis of prostacyclin, which is
vasodilatory (Zou et al.,
1997
). Superoxide may combine non-enzymatically with arachidonate,
generating isoprostanes, which can then activate thromboxane receptors
(Seshiah et al., 2002
). Thus
there are several possible mechanisms by which ET-1 stimulated
O2.- formation could have an effect on Ca2+
in VSM.
Our finding that DPI or TEMPOL plus 2-APB or TMB-8 inhibited the [Ca2+]i response to ET-1 in afferent arterioles by 83% raises the question of why there was not 100% inhibition. It is possible that neither the IP3R nor O2.- blockers were given at maximal inhibitory concentrations. There may be other pathways of ET-1-induced calcium signaling such as receptor-operated mechanisms, working through diacyl glycerol rather than IP3. Our data suggest that blockade of the IP3R represents the sum of IP3R-mediated release of Ca2+ from the SR and that obtained from CICR. Anything that interferes with generation or disposition of O2.-, will reduce activation of the ADPR cyclase, production of cADPR and sensitization of the RyR to Ca2+. The inhibitors of the ADPR cyclase, nicotinamide and Zn2+, diminished the [Ca2+]i response to ET-1 by two thirds. Similarly, both DPI and TEMPOL reduced the response by about two thirds, suggesting that the effect of cADPR on the RyR is a major component of the global response of afferent arteriolar VSM to ET-1.
Complex control systems have developed in animals to ensure homeostasis in
response to intermittent feeding conditions and to environmental changes. The
well-known initiating event in contraction of vascular smooth muscle is a
change in [Ca2+]i caused by hormones, autocrine or
paracrine substances or stretch of the vascular wall. Endothelin-1, which is
produced by the vascular endothelium, acts locally to cause vasoconstriction.
In all animals, the ability to regulate systemic blood flow in the face of
environmental stresses has great survival benefit. The elasmobranch,
Squalus acanthias, controls plasma osmolality and blood volume by
secreting hypertonic fluid from its rectal gland. We have previously proposed
that changes in blood flow to the rectal gland are important modulators of
salt excretion from the rectal gland
(Fellner and Parker, 2002). As
well, ET-1 is thought to have an important role in influencing gill function
in the shark (Evans and Gunderson,
1999
).
In summary, we have shown that ET-1 stimulation of the anterior mesenteric artery VSM of the shark increases [Ca2+]i via several distinct pathways. The classic G-protein-coupled receptor activation that results in IP3 generation and release of [Ca2+]i from the SR probably provides an initial increase of [Ca2+]i. The IP3R-stimulated increase in [Ca2+]i can initiate CICR. Our data suggest that in S. acanthias, ET-1 activates NOX to produce O2.- which, in turn, activates VSM ADPR cyclase to increase the formation of cADPR. cADPR, with its interaction with the RyRs, further amplifies the Ca2+ signal. These findings demonstrate that vascular NOX and ADPR cyclase are enzymes that have been preserved for millions of years during evolution.
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Acknowledgments |
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