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First published online December 14, 2006
Journal of Experimental Biology 210, 129-137 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02620
Dual mechanisms for nitric oxide control of large arteries in the estuarine crocodile Crocodylus porosus
School of Life and Environmental Sciences, Deakin University, Geelong, Victoria, 3217, Australia
* Author for correspondence at present address: Department of Cell Biology and Physiology, University of New Mexico Health Sciences Center, MSC 08-4750, 1 University of New Mexico, Albuquerque, NM 87131-0001, USA (e-mail: bbroughton{at}salud.unm.edu)
Accepted 26 October 2006
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Summary |
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Key words: nitric oxide, nitric oxide synthase, endothelium, nitrergic nerves, blood vessel, vasodilation
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionList of abbreviationsReferences |
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). NO derived from the vascular endothelium provides
vasodilator tone that is important in the control of blood pressure
(Moncada et al., 1991). In
addition, blood vessels in the cranial, pelvic and gut regions are innervated
by nitrergic nerves that mediate vasodilation via NO
neurotransmission (Young et al.,
2000), and in combination with the endothelium, nitrergic nerves
provide a second means of NO control of vascular tone
(Toda and Okamura, 2003).
Many studies in non-mammalian vertebrates (birds, reptiles, amphibians and
teleost fishes) have shown that NO mediates vasorelaxation
(Olson and Villa, 1991;
Knight and Burnstock, 1993;
Knight and Burnstock, 1996;
Nilsson and Soderstrom, 1997;
Martinez-Lemus et al., 1999;
Crossley et al., 2000;
Axelsson et al., 2001;
Broughton and Donald, 2002;
Jennings et al., 2004;
Broughton and Donald, 2005;
Galli et al., 2005;
Skovgaard et al., 2005), but
there is some controversy as to whether the vascular endothelium synthesises
and releases NO in fishes and amphibians. A number of studies have provided
evidence that endothelial NO signalling is present in the vasculature of
fishes (Mustafa and Agnisola,
1998; Fritsche et al.,
2000; Pellegrino et al.,
2002) and amphibians (Rumbaut
et al., 1995; Knight and
Burnstock, 1996). In contrast, in many species of teleost and
elasmobranch fishes, there is physiological and anatomical evidence that an
endothelial NO system is absent from the vasculature, and that the
endothelium-derived relaxing factor is in fact a prostaglandin
(Olson and Villa, 1991;
Evans and Gunderson, 1998;
Miller and Vanhoutte, 2000;
Park et al., 2000;
Donald et al., 2004;
Jennings et al., 2004).
Furthermore, it was found in the Australian short-finned eel Anguilla
australis that NO control of the dorsal aorta and the intestinal veins
was provided by nitrergic nerves and that there was no evidence for
endothelial NOS or endothelial NO signalling
(Jennings et al., 2004).
Similarly, we have shown that the large blood vessels of the cane toad
Bufo marinus are regulated by NO that is derived from perivascular
nerves and not the vascular endothelium
(Broughton and Donald, 2002;
Broughton and Donald, 2005),
and that NOS is present in the perivascular nerves, but not the vascular
endothelium of the American bullfrog Rana catesbeiana
(Donald and Broughton, 2005).
Thus, we proposed that perivascular nerves may be the primary means for
providing NO regulation of blood vessels in teleost fishes and amphibians.
The question then arises as to when vascular endothelial NO signalling
first appeared in vertebrate evolution. In 1986 (prior to the discovery of
biological NO), it was demonstrated that the acetylcholine (ACh)-mediated
relaxation in the descending aorta of the spectacled caiman Caiman
crocodylus was endothelium-dependent, which suggested that an
endothelialderived relaxing factor was involved in regulating vascular tone in
reptiles (Miller and Vanhoutte,
1986). More recently, it was found that the ACh-mediated
relaxation in isolated, pre-constricted aortic rings of the garter snake
Thamnophis sirtalis parietalis was abolished or greatly reduced by
the NOS inhibitor, N
-nitro-L-arginine
methyl ester (L-NAME), or when the endothelium was removed
(Knight and Burnstock, 1993).
It was thus concluded that ACh was mediating vasorelaxation following the
synthesis of NO by an endothelial NOS. Furthermore, endothelial NO signalling
has been clearly demonstrated in the arteries of chickens (see
Hasegawa and Nishimura, 1991;
Martinez-Lemus et al., 1999;
Le Noble et al., 2000).
Similarly to amphibians (Broughton and
Donald, 2002; Broughton and
Donald, 2005) and teleost fish
(Jennings et al., 2004),
neural NOS immunoreactivity (IR) has also been found in the perivascular
nerves of reptilian blood vessels, including the estuarine crocodile
Crocodylus porosus (Karila et
al., 1995; Olsson and Gibbins,
1999; Axelsson et al.,
2001; Donald and Broughton,
2005). Therefore, there is the potential for vascular control by
NO derived from the endothelium and perivascular nerves of reptiles. A number
of studies have shown that a NO tonus is present in the circulation of various
reptilian species (see Skovgaard et al.,
2005).
This study investigated the NO control of the large arteries of the crocodile, C. porosus. We used both NADPH-d histochemistry and immunohistochemistry (IHC) to determine whether endothelial and/or neural NOS are present in the large arteries, and in vitro organ bath physiology to examine the mechanism of NO control. Our findings show, for the first time, both endothelial and neural NO control of systemic blood vessels in a non-mammalian vertebrate.
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Materials and methods |
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NADPH-d histochemistry
The right aorta, dorsal aorta, aortic anastomosis and vena cava were
dissected free and immersed in phosphate buffered saline (PBS, 0.01 mol
l-1 phosphate buffer and 0.15 mol l-1 NaCl; pH 7.4) at
4°C. Prior to fixation, the blood vessels that were prepared as
whole-mounts were opened and pinned out on dental wax, endothelium side up.
All blood vessels were fixed in 4% formaldehyde (pH 7.4) at 4°C for 1 h.
They were then washed in 0.01 mol l-1 PBS (3x10 min) and
either removed from the dental wax (whole-mounts) or cryoprotected overnight
in a solution of 0.01 mol l-1 PBS containing 30% sucrose for
cryostat sectioning. The cryoprotected tissues were mounted in an OCT
Tissue-Tek (Bayer Diagnostics, Puteaux, France) mould and frozen in liquid
nitrogen. Sections were then cut at 12 µm on a Reichardt-Jung cryostat
(Heidelberg, Germany, and thaw-mounted onto 0.1% gelatinised slides. The
sectioned blood vessels and whole-mounts were stained in a NADPH-d mixture
containing 1 mg ml-1 ß-NADPH, 0.25 mg ml-1
nitroblue tetrazolium (NBT), 1% Triton X-100 in 0.1 mol l-1 Tris
buffer (pH 8), at room temperature, for 15 min at 37°C; this mixture was
kept in the dark as it is light sensitive
(Beesley, 1995). The tissues
were then washed in 0.01 mol l-1 PBS (3x 2 min) and mounted
in buffered glycerol (0.5 mol l-1 Na2CO3
added dropwise to 0.5 mol l-1 NaHCO3 to pH 8.6, combined
1:1 with glycerol). Both tissue sections and whole-mounts were observed under
a light microscope (Zeiss, Oberkochen, Germany) and were photographed with a
digital colour system (Spot 35 Camera System, USA).
Endothelial and neural NOS immunohistochemistry
The right aorta, dorsal aorta and aortic anastomosis were fixed as
whole-mount preparations, as described above. The blood vessels were unpinned,
washed in 0.01 mol l-1 PBS (3x10 min), incubated in DMSO
(3x10 min) and washed in 0.01 mol l-1 PBS (5x2 min).
The blood vessels were then incubated in a polyclonal antibody raised against
mouse endothelial NOS (1:1000) (O'Brien et
al., 1995), or a polyclonal antibody raised against sheep neural
NOS (1:4000) (Anderson et al.,
1995), for 24 h at room temperature in a humid box. The following
day, the tissues were washed in 0.01 mol l-1 PBS (3x10 min)
to remove any excess antibody, and were incubated in a fluorescein
isothiocyanate (FITC)-conjugated goat anti-mouse IgG or FITC-conjugated goat
antisheep IgG (1:200) (Zymed Labratories, San Francisco, CA, USA) for 3-4 h at
room temperature in a humid box. The blood vessels were then washed in 0.01
mol l-1 PBS (3x10 min), mounted in buffered glycerol, and
observed under a fluorescence microscope (Zeiss) using a FITC filter, and
photographed as above.
In vitro organ bath physiology
After sacrifice, segments of the right aorta and dorsal aorta were excised
and placed in Mackenzie's balanced salt solution (115 mmol l-1
NaCl, 3.2 mmol l-1 KCl, 20 mmol l-1 NaHCO3,
3.1 mmol l-1 NaH2PO4, 1.4 mmol l-1
MgSO4, 16.7 mmol l-1 D[+] glucose and 1.3 mmol
l-1 CaCl2; pH 7.2-7.3), which was maintained at
30°C. Individual rings of approximately 4-5 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 Mackenzie's
balanced salt solution, which was aerated with 95% O2 and 5%
CO2. Tension was recorded by force transducers (Grass-FT03, West
Warwick, USA) connected through a PowerLabTM (ADI Instruments, Castle
Hill, Australia) data acquisition system to a PC computer. 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 deliberately
removed by gently rotating the blood vessel on a fine toothpick, and the
extent of removal was determined using Haematoxylin and Eosin staining (see
below). Prior to administering various vasorelaxant substances, each vessel
was pre-contracted with endothelin 1 (ET-1, 10-8 mol
l-1), and vasocontraction was allowed to reach its maximum. The
extent of vasorelaxation was determined for each relaxant by scoring the
degree of relaxation as a ratio by assigning a relaxation to pre-contraction
levels as 100%. In all experiments from the one animal, an additional ring
from the same blood vessel was used as a matched control for the comparison of
drug effects. Data are expressed as mean ± 1 standard error (s.e.m.) of
five experiments from five animals, and statistical analysis was performed
with paired t-tests using the SPSS (10.0) statistical package;
P
0.05 was considered significant.
Haematoxylin and Eosin staining
After in vitro organ bath physiology, the aortic rings from C.
porosus with the endothelium removed and the matched controls with the
endothelium intact were fixed and sectioned as described above. The vessel
sections were stained with Haematoxylin and Eosin to verify the presence or
absence of the endothelium.
Materials
Sodium nitroprusside, ACh, L-NNA, atropine, ß-NADPH, NBT
and Triton X-100 were obtained from Sigma (St Louis, MO, USA). Nicotine was
purchased from BDH chemicals (Melbourne, Australia) and ET-1 and rat atrial
natriuretic peptide (rANP) were obtained from Auspep (Melbourne, Australia).
Oxadiazole quinoxalin-1 was purchased from Alexis (San Diego, CA, USA), and
the NOS antibodies were obtained from Chemicon (Melbourne, Australia).
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionList of abbreviationsReferences |
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). The
frequency and staining intensity of the patches was less in the vena cava in
comparison to the large arteries and the aortic anastomosis
(Fig. 1B). Furthermore, in the
dorsal aorta and the aortic anastomosis, a similar pattern of staining was
observed in the endothelial cells following endothelial NOS IHC (N=3;
Fig. 1D).
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Upon scanning through the various layers of the blood vessels following NADPH-d histochemistry, positive staining was also observed in the perivascular nerve fibres (N=5; Fig. 2A,B). This observation was confirmed with IHC, which showed specific neural NOS-IR in the perivascular nerves of each blood vessel (N=5; Fig. 2C,D); the neural NOS-IR showed the same distribution pattern as that of the NADPH-d staining. Therefore, a single description is provided for the observations made using both techniques. A moderate to dense plexus of neural NOS-positive nerves was observed in all blood vessels. All vessels contained neural NOS-positive nerve bundles (arrowhead, Fig. 2A) and single, varicose nerve fibres (arrows, Fig. 2A-D), although there was no distinct pattern in the distribution of perivascular nerves.
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In vitro organ bath physiology
The right aorta and dorsal aorta were pre-contracted with ET-1
(10-8 mol l-1). At the peak of contraction various
chemicals associated with the relaxation mechanisms of NO were added. A
summary of the data for all in vitro organ bath experiments is given
in Table 1.
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In the right and dorsal aortae, the NO donor, SNP (10-4 mol
l-1), induced a potent relaxation (N=5,
Fig. 3A,D). To activate a
putative endothelial NO system, ACh was used as an agonist because previous
studies in mammals (see Moncada et al.,
1991) and reptiles (see Knight
and Burnstock, 1993) have shown that ACh indirectly stimulates the
release of NO from endothelial NOS. In contrast, nicotine was used to
stimulate the release of NO from nitrergic nerves, because previous studies in
mammals (see Toda and Okamura,
2003), amphibians (Donald and
Broughton, 2005) and teleost fish
(Jennings et al., 2004) have
shown that nicotine indirectly stimulates the release of NO from perivascular
nerves. In the right and dorsal aortae, both applied ACh (10-5 mol
l-1; Fig. 3B,D) and
nicotine (3x10-4 mol l-1;
Fig. 3C,D) produced a
relaxation (N=5). In both aortae, the addition of the soluble
guanylyl cyclase inhibitor, ODQ (10-5 mol l-1),
completely abolished the relaxation effect of SNP (10-4 mol
l-1; Fig. 4B),
applied ACh (10-5 mol l-1;
Fig. 4B) and nicotine
(3x10-4 mol l-1;
Fig. 5B), in comparison to the
control vessels (N=5; Fig.
4A and Fig. 5A);
ACh now caused a contraction, whereas SNP and nicotine had no effect. Rat ANP
(10-8 mol l-1), which mediates vasodilation via
a particulate guanylyl cyclase (Winquist
et al., 1984), caused a potent vasodilation in the presence of ODQ
(rANP was only added to the vessels with ODQ;
Fig. 4B,
Fig. 5B).
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To determine if both the ACh- and nicotine-mediated vasodilations were via NOS, the vessels were pre-treated with L-NNA. The addition of L-NNA caused a constriction in the aortic rings with or without the endothelium, although the constriction was more potent in the vascular rings with the endothelium present (data not shown). The vasodilation induced by ACh (10-5 mol l-1) was abolished by L-NNA (10-4 mol l-1) in both the right and dorsal aortae with an intact endothelium; however, SNP produced a potent vasodilatory response (N=5; Fig. 4C). Furthermore, in the endothelium-denuded right and dorsal aortae, the vasodilation induced by nicotine (3x10-4 mol l-1) was abolished in the presence of L-NNA (10-4 mol l-1; N=5; Fig. 5C).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionList of abbreviationsReferences |
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; Crossley et
al., 2000; Skovgaard et al.,
2005), little is understood as to whether NO is generated by an
endothelial and/or neural NOS. Interestingly, the present study demonstrates,
using both anatomical and physiological approaches, that both NO signalling
mechanisms are capable of regulating the large arteries of the estuarine
crocodile C. porosus.
NADPH-d histochemistry revealed punctate, perinuclear staining in the
endothelial cells of the right and dorsal aortae, aortic anastomosis, and vena
cava of C. porosus, which was similar to the NADPH-d staining
observed in the endothelial cells of mammalian blood vessels (see
O'Brien et al., 1995) and the
pigeon dorsal aorta (Donald and Broughton,
2005). More specifically, similar staining was observed in the
dorsal aorta and aortic anastomosis following endothelial NOS IHC. These
findings indicated that the large blood vessels of C. porosus are
potentially regulated by NO synthesised and released from an endothelial NOS
located in the endothelial cells. The lower frequency of stained patches in
the vena cava compared to the arteries may be due to different characteristics
of endothelial cells in veins compared to arteries, which would be consistent
with observations in the mammalian circulation
(Isogai et al., 1991).
Furthermore, NADPH-d staining was observed in nerve bundles and single
varicose fibres, which indicated that the nerves were NOS positive. The
staining pattern using a specific antibody to neural NOS was identical to that
obtained using NADPH-d histochemistry, which indicated that the NADPH-d
staining was specific for neural NOS. In C. porosus, the presence of
neural NOS in perivascular nerves was previously reported in the
gastrointestinal vasculature (Karila et
al., 1995; Olsson and Gibbins,
1999). Moreover, Axelsson et al.
(Axelsson et al., 2001)
demonstrated that NOS was present in the perivascular nerves of the aortic
anastomosis, but the distribution of NOS was diffuse and difficult to
interpret in the photomicrographs of the tissue sections. In contrast, the use
of tissue whole-mounts in the present study demonstrated that a
moderate-to-dense plexus of perivascular nitrergic nerves is present in the
vasculature of C. porosus. Therefore, the systemic vasculature of
C. porosus is potentially modulated by NO derived from both
endothelial and neural NOS. To the best of our knowledge, this is the first
study to show that both endothelial and neural NOS are present in the same
blood vessel in a non-mammalian vertebrate.
Although the anatomical findings indicated that both an endothelial and
neural NO system are present in the large arteries of C. porosus, it
was imperative to determine whether NO derived from endothelial and/or neural
NOS was involved in regulating vascular tone. Two different pharmacological
tools were used to stimulate the release of endothelially and/or neurally
derived NO. Acetylcholine was used as an agonist for activating the
endothelial NO system, as it is well-documented in mammals that ACh activates
endothelial NOS to produce NO (see Moncada
et al., 1991). The nicotinic receptor agonist, nicotine was used
to stimulate the release of NO from perivascular, nitrergic nerves.
Previously, nicotine has been shown to specifically cause the release of NO
from nerves in the vasculature of various mammals (see
Toda and Okamura, 2003) and
non-mammalian vertebrates (Jennings et
al., 2004; Donald and
Broughton, 2005).
In the right and dorsal aortae of C. porosus, the ACh-mediated
relaxation was endothelium-dependent and abolished in the presence of
atropine, L-NNA and ODQ. These data indicated that ACh mediates
relaxation by activating a similar endothelial NO signalling cascade to that
found in mammalian blood vessels (Moncada
et al., 1991). These findings are consistent with those reported
by Knight and Burnstock (Knight and
Burnstock, 1993), who demonstrated that the ACh-mediated
relaxation in the dorsal aorta of T. sirtalis parietalis was
abolished or significantly reduced in the presence of L-NNA, or
when the endothelium was removed. Furthermore, ACh-mediated relaxation that is
probably due to NO was reported in isolated, vascular rings of the chicken
aorta (Hasegawa and Nishimura,
1991) and pulmonary artery
(Martinez-Lemus et al., 1999).
The presence of an endothelial NO system in the vasculature of both C.
porosus and birds is to be expected because it is thought that birds
evolved from a crocodilian-like ancestor
(Hedges, 1994). Overall, it
appears that NO derived from endothelial NOS plays an important role in
maintaining tone in the large arteries of C. porosus. Interestingly,
when the endothelium was removed from the vasculature of C. porosus,
ACh induced a contraction even though nitrergic nerves had been shown to be
present in these vessels. This is in contrast to our previous findings in the
toad B. marinus, in which ACh induced a relaxation in the
endothelium-denuded central aortae
(Broughton and Donald, 2002).
One possible explanation for this difference is that the muscarinic receptors
are only located on the endothelial cells in C. porosus, whereas in
B. marinus, it is likely that they are located on the perivascular,
nitrergic nerves.
The presence of nitrergic nerves in the large arteries of C.
porosus suggested that neurally derived NO was involved in regulating
vascular tone, in addition to that derived from the endothelium. In the right
and dorsal aortae, the nicotine-mediated relaxation was abolished by ODQ and
L-NNA, but the removal of the endothelium had no significant
effect. This suggested that nicotine, acting independently of the endothelium,
activated neural NOS to synthesise and release NO. This subsequently induced a
relaxation via a soluble guanylyl cyclase, which is the first
demonstration of neurally based NO signalling in reptilian blood vessels. The
findings are similar to those previously reported in the large systemic blood
vessels of B. marinus (Broughton
and Donald, 2002; Broughton and
Donald, 2005) and A. australis
(Jennings et al., 2004), which
suggests that nitrergic nerves may play a significant role in regulating the
large blood vessels of lower vertebrates. This is the first study to
demonstrate both endothelial and neural NO control of large systemic blood
vessels in any non-mammalian vertebrate species. However, it remains to be
determined how the dual NO systems contribute to vascular control in
vivo in C. porosus.
It is well documented that NO contributes to basal tone in the circulation
of mammals (Moncada et al.,
1991). In the present study, L-NNA increased the basal
tonus in both the right and dorsal aortae with or without the endothelium
being present; however, the response was less in endothelium-denuded vessels
than when the endothelium was intact. This suggested that in the absence of an
endothelial NO system, NO-derived from another source, which is likely to be
from neural NOS located in perivascular nerves, is also able to contribute to
basal tone. The presence of a basal NO tonus has also been reported in the
dorsal aorta of T. sirtalis parietalis
(Knight and Burnstock, 1993)
and in the aortic anastomosis of C. porosus
(Axelsson et al., 2001), but
not in isolated coeliac or mesenteric arteries of the latter species
(Kågström et al.,
1998). Furthermore, in vivo injection of the NOS
inhibitor, L-NAME, caused an elevation in blood pressure in American alligator
Alligator mississippiensis
(Platzack et al., 2002), the
varanid lizard Varanus exanthematicus, ball python Python
regius, and turtle Trachemys scripta, but not the rattlesnake
Crotalus durissis (see Skovgaard
et al., 2005). Thus, it appears that there is a tonic release of
NO from endothelial and/or neural NOS in the circulation of some reptiles.
Skovgaard et al. have proposed that the NO regulation of the reptilian
circulation is correlated with circulatory anatomy and lung complexity, where
it is more developed in species with separated systemic and pulmonary
circulation (Skovgaard et al.,
2005). Accordingly, it would be intriguing to examine the in
vitro mechanism of NO control of blood vessels in the different reptilian
groups.
The discovery that NO is derived from the endothelium and nitrergic nerves
in the large arteries of C. porosus is important for our
understanding of vascular NO control in this species; however, further studies
are required to determine if endothelial and/or neural NO signalling
mechanisms are present in smaller resistance vessels that control blood flow
distribution and overall blood pressure. Nitric oxide is clearly an important
regulator of the crocodilian circulation since in C. porosus it was
found to regulate vascular tone in the aortic anastomosis
(Axelsson et al., 2001) and
play an important role in buffering blood pressure against changes in heart
rate during cooling (Seebacher and
Franklin, 2004). However, in both studies the source from which NO
was produced and released was not determined. Therefore, future studies of
cardiovascular regulation in C. porosus will need to consider that NO
regulation could be provided by both endothelial and/or neural NOS
systems.
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List of abbreviations |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionList of abbreviationsReferences |
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-nitro-L-arginine methyl
ester
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Acknowledgments |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionList of abbreviationsReferences |
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