Nitric oxide control of the dorsal aorta and the intestinal vein of the Australian short-finned eel Anguilla australis
School of Biological and Chemical Sciences, Deakin University, Geelong, Victoria, Australia, 3217
* Author for correspondence (e-mail: brettj{at}deakin.edu.au)
Accepted 19 January 2004
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Summary |
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Key words: nitric oxide, neural nitric oxide synthase, soluble guanylyl cyclase, vasodilation, nicotine, Anguilla australis, prostaglandin
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Introduction |
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The role of NO in the control of vascular tone in non-mammalian vertebrates
has received less attention. Early comparative studies in avian
(Hasegawa and Nishimura,
1991), reptilian (Knight and
Burnstock, 1993
), and amphibian
(Rumbaut et al., 1995
;
Knight and Burnstock, 1996
)
species provided evidence that an endothelial NO system was present.
Furthermore, there is evidence for endothelial NO signalling in teleost fish,
which was obtained in perfused vascular beds in which vascular resistance was
affected by the NO precursor L-arginine, and inhibition of NO
synthase, the enzyme that generates NO
(Nilsson and Söderström,
1997
; Mustafa et al.,
1997
; Mustafa and Agnisola,
1998
). The only study in teleost fish that has shown anatomically
that an endothelial NO synthase is present is that of Fritsche et al.
(2000
), who showed
immunoreactivity to endothelial NOS in developing zebrafish blood vessels.
However, in some species of teleost fish, there is now convincing evidence
that vasodilatory signalling molecules released by the endothelium are
prostaglandins, rather than NO (Olson and
Villa, 1991
;
Kågström and Holmgren,
1997
; Park et al.,
2000
).
Recently, we demonstrated in the cane toad Bufo marinus that NO
control of the large central arteries was mediated by NO generated from neural
NOS that was located in the perivascular nerves
(Broughton and Donald, 2002).
Furthermore, no evidence for an endothelial NO system was found in B.
marinus (Broughton and Donald,
2002
). In the present study we use anatomical and physiological
approaches to demonstrate that NO control of two blood vessels of the eel
Anguilla australis is mediated by neural NOS in perivascular
nerves.
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Materials and methods |
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NADPH diaphorase histochemistry
The dorsal aorta, the intestinal vein and the gut were dissected free and
immersed in phosphate-buffered saline (PBS; 0.01 mol l1
phosphate buffer, 0.15 mol l1 NaCl, pH 7.4) at 4°C. Each
vessel was opened and pinned out endothelium side up on dental wax, prior to
fixing for 2 h in 4% formaldehyde (pH 7.4) at 4°C. The blood vessels were
washed in 0.01 mol l1 PBS (3x10 min) and removed from
the dental wax. They were then stained in a NADPH diaphorase mixture
containing 1 mg ml1 ß-NADPH, 0.25 mg
ml1 Nitroblue Tetrazolium (NBT), 1% Triton X-100 in 0.1 mol
l1 Tris buffer, pH 8, for periods ranging from 15 to 60 min
at room temperature. This mixture was kept in the dark, as it is light
sensitive. The vessels were then washed in 0.01 mol l1 PBS
and mounted on slides in buffered glycerol (0.5 mol l1
Na2CO3 added dropwise to 0.5 mol l1
NaHCO3 to pH 8.6, combined 1:1 with glycerol). Blood vessels were
observed under a light microscope (Axioskop 20, Zeiss, Germany) and
photographed with a digital colour system (Spot 35 Camera System, Diagnostic
Instruments, USA). Control experiments were performed on the myenteric plexus
of the gut of A. australis, because positive NADPH diaphorase
staining has been previously demonstrated in the myenteric plexus of fish
(Li et al., 1993).
Immunohistochemistry
Blood vessels were fixed as described above. They were unpinned, washed in
0.01 mol l1 PBS (3x10 min), incubated in dimethyl
sulphoxide (3x10 min) and washed in 0.01 mol l1 PBS
(5x2 min). The vessels were then incubated in either sheep anti-neural
NOS (1:4000; Anderson et al.,
1995) or mouse anti-endothelial NOS (1:1000;
O'Brien et al., 1995
) for 24 h
at room temperature in a humid box. The following day, tissues were washed in
0.01 mol l1 PBS (3x10 min) to remove any excess
antibody and incubated in FITC-conjugated goat anti-sheep IgG (1:200) or
FITC-conjugated goat anti-mouse IgG (1:200) (Zymed Laboratories, San
Francisco, USA) for 34 h at room temperature in a humid box. The blood
vessels were then washed in 0.01 mol l1 PBS (3x10
min), and mounted in buffered glycerol. Blood vessels were observed under a
fluorescence microscope (Zeiss) using a FITC filter and photographed as
above.
Organ bath physiology
After decapitation, the dorsal aorta and the intestinal vein were excised
and placed in Cortland's ringer solution (124.1 mmol l1
NaCl, 5.1 mmol l1 KCl, 12 mmol l1
NaHCO3, 0.41 mmol l1 NaH2
PO4, 0.29 mmol l1 MgSO4, 7.8 mmol
l1 D[+]glucose and 2.5 mmol l1
CaCl2, pH 7.2). Individual rings of approximately 45 mm in
length were mounted horizontally between two hooks for the measurement of
isometric force, and placed in an organ bath. The rings were bathed in 15 ml
of Cortland's ringer solution, which was maintained at 19°C and aerated
with air. The force transducer (FT03, Grass Instruments, USA) was linked to a
PowerLabTM data collection system and a personal computer, which recorded
data for further analysis. An initial tension of 0.5 g was applied to the
blood vessels, and they were allowed to equilibrate for 30 min. In some
experiments, the endothelium was removed by a pin, and the extent of removal
was determined using NADPH histochemistry. The extent of removal was also
substantiated by the use of the calcium ionophore, A23187, which mediates
vasodilation in the presence of an intact endothelium, but has no effect when
the endothelium is disrupted. Prior to administering various vasodilatory
substances, each vessel was pre-constricted with endothelin-1
(108 mol l1), and vasoconstriction was
allowed to reach its maximum. Previous studies have demonstrated that
endothelin-1 at 108 mol l1 elicits an
appropriate vasoconstriction for studies of vasodilatory mechanisms
(Minerds and Donald, 2001;
Broughton and Donald, 2002
).
The extent of vasodilation was determined for each vasodilator, by scoring the
degree of relaxation as a ratio, having assigned relaxation to
pre-constriction levels at 100%. In experiments, matched controls were used
from the same animal for comparison of drug effects. Data are expressed as
mean ± one standard error (S.E.M.) of
five or more experiments, and statistical analysis was performed by
independent t-tests using the SPSS (11.5) statistical package; a
P value
0.05 was considered significant.
Materials
Sodium nitroprusside (SNP), acetylcholine (ACh),
N-nitro-L-arginine (L-NNA),
indomethacin, calcium ionophore A23187, ß-nicotinamide adenine
dinucleotide phosphate, reduced form (ß-NADPH), NBT and Triton X-100 were
obtained from Sigma (St Louis, USA). Endothelin-1 (ET-1) and rat atrial
natriuretic peptide (rANP) were purchased from Auspep (Melbourne, Australia),
and oxadiazole quinoxalin-1 (ODQ) was obtained from Alexis (San Diego, USA).
Nicotine was purchased from BDH chemicals and
N
-propyl-L-arginine was obtained from
Cayman chemicals. The NOS antibodies were obtained from Chemicon (Melbourne,
Australia).
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Results |
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Endothelial and neural NOS immunohistochemistry
To specifically identify the types of NOS present in the blood vessels,
eNOS and neural NOS (nNOS) antibodies were used (N=3). In the dorsal
aorta and the intestinal vein, no eNOS immunoreactivity was found
(Fig. 1C), but it could be
readily demonstrated in endothelial cells of the rat aorta
(Fig. 1D). In both the dorsal
aorta (Fig. 2C) and intestinal
vein (Fig. 2D), nNOS
immunoreactivity was observed in nerve bundles and single fibres in a similar
pattern to that observed using NADPH diaphorase histochemistry. In addition,
NADPH diaphorase staining and specific nNOS immunoreactivity were colocalised
in the same neural structures, demonstrating that the NADPH diaphorase
reaction was staining positively for nNOS.
In vitro organ bath physiology
Blood vessels were preconstricted with ET-1 (108 mol
l1), which induced a potent and long-lasting effect that was
allowed to reach its maximum. Following this, various substances associated
with vasodilator mechanisms were added to the baths. In tetrapods, ACh has
been used to indirectly activate NOS to generate a NO-mediated vasodilation;
however, in fish, ACh generally causes vasoconstriction in peripheral blood
vessels. This was verified in A. australis in which ACh always caused
vasoconstriction regardless of whether or not the vessel had been
preconstricted with ET-1 (108 mol l1)
(N=5, results not shown). In the dorsal aorta and the intestinal
vein, the NO donor, SNP (104 mol l1),
induced a dilation of 52.27±9.43% and 94.12±8.79%, respectively
(N=5, Fig. 3). In
addition, the application of nicotine (3x10-4 mol
l1) mediated a vasodilation in the dorsal aorta
(73.86±14.84%) and intestinal vein (70.09±6.24%; N=5;
Fig. 4). Preincubation of the
vessels with the soluble GC inhibitor, ODQ (105 mol
l1), blocked the dilation induced by both SNP
(104 mol l1) and nicotine
(3x104 mol l1). However, the
addition of rat ANP (108 mol l1), which
mediates dilation through a particulate GC, caused a marked vasodilation
(N=5, Fig. 5B). This
indicates that both SNP and nicotine mediate vasodilation via a
soluble GC.
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The addition of the non-specific NOS inhibitor, L-NNA (104 mol l1), abolished the vasodilatory effect of nicotine (3x104 mol l1) in the aorta and the vein (N=5). However, when SNP (104 mol l1) was applied to the vessels in the presence of L-NNA a marked vasodilation was observed (Fig. 5C). This result was expected as SNP is a NO donor, and does not require NOS for the production of NO.
In the next series of experiments, the endothelium was removed from the
blood vessels, and was verified by subsequent NADPH staining. In
endothelium-denuded dorsal aortae, the application of nicotine
(3x104 mol l1) caused a similar
dilation (76.22±7.42%) to that observed in control vessels with an
intact endothelium (76.95±12.01%; P=0.94, N=5;
Fig. 6). Similar results were
observed in the intestinal vein (endothelium denuded 77.35±12.50%;
endothelium intact 74.50±12.10%; P=0.90, N=5;
Fig. 6C). These results
indicate that removal of the endothelium does not significantly affect the
nicotine-mediated vasodilation in the dorsal aorta and the intestinal vein. In
the dorsal aorta incubated with
N-propyl-L-arginine (PLA,
105 mol l1), a specific nNOS inhibitor
(Zhang et al., 1997
), the
vasodilatory effect of nicotine (3x104 mol
l1) was significantly reduced compared to control blood
vessels (PLA 27.80±11.25%; control 72.36±11.23%;
P<0.05, N=5; Fig.
7). A similar result was obtained in endothelium-denuded dorsal
aortae (P<0.05, N=5; not shown). Furthermore, incubation
of the intestinal vein with PLA (105 mol
l1) significantly reduced the nicotine-mediated vasodilation
(PLA 45.89±13.76%; control 80.11±16.81%; P<0.05,
N=5; Fig. 7). A
similar result was obtained in endothelium-denuded intestinal vein
(P<0.05, N=5; not shown). These results suggest that PLA
significantly inhibits the nicotine-mediated vasodilation in the dorsal aorta
and the intestinal vein with or without an intact endothelium.
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In the dorsal aorta, preincubation with the cyclo-oxygenase inhibitor, indomethacin (105 mol l1), did not significantly reduce the vasodilation to nicotine (indomethacin 71.49±9.41%; control 66.55±7.40; P=0.63, N=5; Fig. 8). Similar results were also observed in the intestinal vein (indomethacin 70.68±10.97; control 82.88±5.70; P=0.20, N=5; Fig. 8). These results suggest that nicotine is not stimulating the production of cyclo-oxygenase metabolites to mediate vasodilation in the dorsal aorta and the intestinal vein.
|
In the dorsal aorta and the intestinal vein, the calcium ionophore, A23187 (3x106 mol l1), mediated a significant dilation (N=3; Fig. 9A). In both vessels, pre-incubation with indomethacin (105 mol l1) significantly reduced the dilation induced by the calcium ionophore (P<0.05, N=3; Fig. 9B); in fact a vasoconstriction was now observed. In addition, removal of the endothelium in both blood vessels abolished the dilation induced by the calcium ionophore (P<0.05, N=3; Fig. 9C). These results suggest that the calcium ionophore stimulates the production of endothelium dependent, cyclo-oxygenase derived metabolites to induce vasodilation in the dorsal aorta and intestinal vein of A. australis.
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Discussion |
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The current study demonstrated the absence of an endothelial NO system in
A. australis, which is in accordance with a number of previous
studies in teleost fishes. These studies have proposed that prostaglandins
released from the endothelium are responsible for mediating vasodilation
(Olson and Villa, 1991;
Sverdrup et al., 1994
;
Farrell and Johansen, 1995
;
Kågström and Holmgren,
1997
; Miller and Vanhoutte,
2000
; Park et al.,
2000
). However, the presence of an endothelial NO system in fish
vasculature remains controversial because it has been reported that some
vascular beds are dilated by NO purportedly released by the endothelium
(Nilsson and Söderström,
1997
; Mustafa et al.,
1997
; Mustafa and Agnisola,
1998
). Furthermore, it has been demonstrated that elasmobranchs
lack a NO system and instead it is proposed that prostaglandins are the
endothelium-dependent vasodilators in this group
(Evans and Gunderson, 1998
;
Evans, 2000
).
NADPH diaphorase histochemistry and immunohistochemistry are two anatomical
techniques that have been used previously to identify eNOS in the vasculature
of mammals (Beesley, 1995). In
the present study, these techniques demonstrated an absence of NOS in the
endothelium in both the dorsal aorta and intestinal vein of A.
australis. However, in the endothelium of the rat aorta (used as a
control), perinuclear staining was observed as previously demonstrated in
mammals (O'Brien et al.,
1995
). This suggests that the dorsal aorta and intestinal vein of
A. australis do in fact lack an eNOS. The only study to report the
presence of eNOS in teleost blood vessels is that of Fritsche et al.
(2000
), who demonstrated using
immunohistochemistry and a different eNOS antibody to that used in this study,
that eNOS immunoreactivity was present in the dorsal vein of the developing
zebrafish. Thus, there seems to be conflicting data on the presence of eNOS
that could reflect a dichotomy between developing and adult fish. In contrast
to the endothelium, NADPH diaphorase histochemistry readily demonstrated NOS
staining in the perivascular nerves of the dorsal aorta and intestinal vein of
A. australis, which was supported by the use of immunohistochemistry
and a mammalian nNOS antibody. The staining patterns of the two techniques
were identical, revealing both nerve bundles and single, varicose nerve fibres
in the blood vessels. It has been previously reported that nNOS is located
within autonomic nerves that innervate peripheral blood vessels of a number of
species of teleost fishes (Brunning et al.,
1996
; Esteban et al.,
1998
; Jiminez et al.,
2001
). Taken together, our data suggest that the vascular
endothelium of A. australis is incapable of synthesising NO, but that
NO may be released from perivascular nerves to regulate vascular tone in
eels.
The presence of nitrergic nerves in the dorsal aorta and intestinal vein
suggested that NO is a key regulator of vascular tone, but it was important to
determine physiologically whether the nerves provide NO control of the blood
vessels. Donald et al. (2003)
demonstrated the presence of nitrergic nerves in the vasculature of the giant
shovelnose ray Rhinobatus typus, but they could not stimulate the
production of NO, nor could they demonstrate the presence of a NO receptor
via use of the NO donor, SNP. These data indicated that despite the
presence of nitrergic nerves, NO does not contribute to the maintenance of
vascular tone in R. typus. The present study, however, demonstrates
that SNP mediated a dilation in both the dorsal aorta and intestinal vein that
could be blocked by ODQ, suggesting that NO stimulates the production of cGMP
via a soluble GC. This observation is consistent with a number of
previous studies that have shown that the vascular smooth muscle of teleost
fish contains a NO receptor that mediates vasodilation
(Small et al., 1990
;
Small and Farrell, 1990
;
Olson and Villa, 1991
;
Hylland and Nilsson, 1995
;
Kågström and Holmgren, 1996;
McGeer and Eddy, 1996
;
Mustafa et al., 1997
;
Miller and Vanhoutte, 2000
).
In contrast to these studies, Pellegrino et al.
(2002
) reported a
vasoconstrictive effect of NO in the branchial circulation of A.
anguilla using the NO donors, SNP and SIN-1, at a range of
concentrations. These authors also demonstrated that the vasoconstriction was
due to the activation of soluble GC, as pre-incubation with ODQ prevented the
constriction induced by the NO donors. This result was substantiated with the
use of the cGMP analog 8-bromo cGMP, which caused a dose-dependent
vasoconstriction. This was the first study in fish to suggest that NO
stimulates the production of cGMP, and elicits a subsequent vasoconstriction.
In addition, a vasoconstrictory effect of NO has been shown in the dogfish
shark Squalus acanthias (Evans
and Gunderson, 1998
; Evans,
2000
). Interestingly, a vasoconstriction mediated by cGMP
signalling has recently been demonstrated in murine splenic vessels
(Andrews and Kaufman,
2003
).
Acetylcholine has been used as a pharmacological tool to indirectly
stimulate the production of NO via nNOS in mammals
(Meng et al., 1998) and
amphibians (Broughton and Donald,
2002
). However, it is clear that ACh generally causes
vasoconstriction in peripheral blood vessels of fish, and a similar result was
observed in this study. Previously, it has been suggested in mammals that
nicotine can specifically stimulate nitrergic nerves to produce NO
(Toda and Okamura, 1990
; Toda
et al., 1997
,
1998
), but it is apparent that
the action of nicotine is more complex than initially thought. Recently, it
has been shown that in mammalian cerebral blood vessels, the nicotine-induced
NO-mediated vasodilation is dependent on an intact sympathetic innervation
(Zhang et al., 1998
;
Lee et al., 2000
;
Si and Lee, 2001
). These
authors proposed that nicotine does not directly stimulate the production of
NO from nitrergic nerves, but instead, it binds to nicotinic receptors on
sympathetic nerves to release noradrenaline. Noradrenaline then binds to
adrenoceptors situated on neighbouring nitrergic nerves, which stimulates the
production and release of NO from these nerves. In A. australis, it
was demonstrated that nicotine induced a vasodilation that was mediated
via a soluble GC, as ODQ completely abolished the dilation.
Subsequently, it was then shown that nicotine was stimulating the production
of NO via NOS, as the NOS inhibitor, L-NNA, abolished or
significantly inhibited the dilation. In addition, pre-incubation with the
specific nNOS inhibitor, PLA, significantly inhibited the vasodilation caused
by the application of nicotine, which provided evidence that nNOS was
generating NO. Thus, it was demonstrated that in A. australis
nicotine can be used to stimulate the production of NO from nitrergic nerves
of blood vessels, but the exact mechanism of nicotine-mediated vasodilation is
not known and warrants further study.
We also demonstrated that the endothelium did not contribute to the
nicotine-mediated vasodilation, as disruption of the endothelium did not alter
the effect of nicotine. Recently, Donald et al.
(2003) demonstrated that in
R. typus nicotine induced an endothelium-dependent vasodilation due
to the production of prostaglandins, because it was inhibited by the
cyclo-oxygenase inhibitor, indomethacin. However, preincubation of the blood
vessels from A. australis with indomethacin did not affect the
nicotine-mediated vasodilation. This study also looked at the possible role of
endothelium-dependent vasodilation due to the release of prostaglandins. Our
results demonstrated that vessels preconstricted with ET-1, dilated after the
addition of the calcium ionophore, A23187. In addition, it was shown that the
vasodilation was due to the production of cyclo-oxygenase derived products, as
pre-incubation of the blood vessels with indomethacin significantly inhibited
the vasodilatory response to A23187. Subsequently, it was demonstrated that
the dilation was endothelium-dependent, as removal of the endothelium
abolished the response. These results demonstrate that cyclooxygenase derived
products are endothelium-dependent vasodilators in A. australis.
The demonstration of NO control of vascular smooth muscle of A.
australis by nitrergic nerves is consistent with a recent study that
demonstrated a similar mechanism in the toad, B. marinus
(Broughton and Donald, 2002).
Furthermore, in both species, an endothelial NO system could not be
demonstrated. In light of the findings in other species it seems that there
has been a clear evolutionary progression in NO control of vertebrate blood
vessels. The elasmobranch vasculature contains nitrergic nerves but not
endothelial NOS, and the vascular smooth muscle apparently lacks a soluble GC
that mediates vasodilation (Evans and
Gunderson, 1998
; Evans,
2000
; Donald et al.,
2003
). In most teleost fish and amphibians, a soluble GC that
mediates vasodilation is present in the vascular smooth muscle. We have
provided evidence that the source of NO for the soluble GC in specific blood
vessels of A. australis and B. marinus is the perivascular
nitrergic nerves. Future work will be directed towards determining how general
the mechanism of vascular regulation by nitrergic nerves is in teleost fish
and amphibians.
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List of abbreviations |
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Acknowledgments |
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References |
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