(Hypertension. 1996;27:833-837.)
© 1996 American Heart Association, Inc.
Articles |
Natriuretic Peptide Receptors in Human Artery and Vein and Rabbit Vein Graft
From the Department of Medicine and Clinical Science (H.I., Y.K., T.Y., K.N.) and the Department of Cardiovascular Surgery (T.I., M.H., K.M., T.B.), Kyoto (Japan) University Graduate School of Medicine.
Correspondence to Katsuhiko Matsuda, MD, Department of Cardiovascular Surgery, Kyoto University Graduate School of Medicine, 54 Shogoin Kawahara-cho, Sakyo-ku, Kyoto 606-01, Japan.
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Abstract |
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 Top Abstract IntroductionMethods Results Discussion References |
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Abstract Natriuretic peptides elicit their biological effects by elevation of cGMP through activation of two biologically active receptors: natriuretic peptide A receptor, which shows high affinity to atrial and brain natriuretic peptides, and natriuretic peptide B receptor, which is specific to C-type natriuretic peptide. To elucidate the implications of the natriuretic peptide system in arteries and veins, we examined the cGMP production in response to atrial and C-type natriuretic peptides and gene expressions of biologically active natriuretic peptide receptors in human gastroepiploic artery, internal mammary artery, and saphenous vein. Atrial natriuretic peptide augmented cGMP production more potently by one order of magnitude in arteries than in veins. C-type natriuretic peptide stimulated cGMP production weakly and equally in these vessels. Analyzed by reverse transcription–polymerase chain reaction, gene expression of natriuretic peptide A receptor was four times more abundant in arteries than in veins. Gene expression of natriuretic peptide B receptor was approximately the same between these vessels. We also studied the responsiveness to atrial and C-type natriuretic peptide in rabbit jugular vein grafted into carotid artery. In arterialized vein grafts 4 weeks after operation, the effects of atrial and C-type natriuretic peptides on cGMP production did not change from those in jugular veins. In conclusion, atrial natriuretic peptide stimulates cGMP production more potently in arteries than in veins due to the preferential expression of natriuretic peptide A receptor in arteries. These observations support the distinct roles of natriuretic peptides in cardiovascular homeostasis.
Key Words: natriuretic peptide • natriuretic peptide receptor • vein graft • cyclic GMP
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Introduction |
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TopAbstractIntroductionMethods Results Discussion References |
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The natriuretic peptide family consists of at least three distinct peptides: ANP, BNP, and CNP. We and others have demonstrated that ANP and BNP are circulating hormones secreted mainly from the atrium and the ventricle, respectively.1 Although CNP was originally considered to serve as a neuropeptide,2 we recently reported that CNP is produced by vascular endothelial cells3 and that CNP is detected in human circulation.4 Thus, CNP can be considered to be a novel endothelium-derived relaxing peptide.
Natriuretic peptides elicit their pharmacological actions via activation of two subtypes of the biologically active receptor, NPR-A and NPR-B, which are the particulate guanylate cyclase itself, to elevate intracellular cGMP.5 We and others have demonstrated that ANP and, to a lesser extent, BNP potently activate NPR-A, whereas CNP selectively activates NPR-B.6 7 Several studies, including ours, demonstrated that CNP infused into healthy humans has weaker vasodepressor and natriuretic effects than ANP or BNP, suggesting a difference of expression of natriuretic peptide receptors in humans and distinct roles of these natriuretic peptides in cardiovascular homeostasis.8 9 10
In the present study, to elucidate the possible differential implications of the natriuretic peptide system in human artery and vein, we examined the cGMP production in response to ANP and CNP and gene expressions of biologically active natriuretic peptide receptors in human GEA, IMA, and SV. In addition, using a rabbit model of arterialized vein graft, we further studied the alteration of the responsiveness to ANP and CNP in the jugular vein grafted into the arterial circulation by the process of arterialization.
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Methods |
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TopAbstractIntroductionMethods Results Discussion References |
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Preparation of Human Tissues
Segments of GEA, IMA, and SV were obtained from 13 patients with ischemic heart disease undergoing coronary artery bypass surgery (11 men, 47 to 70 years old; average, 61.1 years). Segments of GEA were also obtained from 2 patients with gastric cancer undergoing total gastrectomy (2 men, 66 and 70 years old, respectively). For cGMP production assay, the segments of the vessels were stored in ice-cold phosphate-buffered saline and used within 6 hours after sampling. For RNA preparation, the segments of vessels were immediately frozen by liquid nitrogen and stored at -70°C until RNA preparation. Informed consent was obtained from each patient. This study was approved by the ethical committee on human research of Kyoto University.
Animals
Sixteen male Japanese White rabbits weighing 2.5 to
3.0 kg were
used. Rabbits were maintained under a 12-hour light schedule and were
fed regular rabbit chow diet. All animals used in this study received
humane care in compliance with the Principles of Laboratory
Animal Care formulated by the National Society for Medical
Research and the Guide for the Care and Use of Laboratory
Animals prepared by the National Academy of Sciences and published
by the National Institutes of Health (NIH publication 85-23, revised
1985).
Surgical Technique of Rabbit Vein Graft Operation
The
operative procedures were performed under aseptic
conditions. Anesthesia was achieved by administration of 25
mg/kg pentobarbital sodium IV and 50 mg lidocaine hydrochloride SC. The
right carotid artery and jugular vein were exposed through a vertical
neck incision. After the animals were given 100 U/kg heparin sodium IV,
a 15- to 20-mm segment of the artery was isolated with vascular forceps
and removed. A 15- to 20-mm segment of the jugular vein was reversed
and interposed in the carotid artery in an end-to-end fashion.
Anastomoses were created with 10-0 nylon continuous suture at x20
magnification. After 4 weeks of observation, the vein graft, left
carotid artery, and left jugular vein were harvested from each rabbit,
and cGMP production in response to ANP and CNP in these three
vessels was examined. For histological examination,
animals were killed by an overdose of pentobarbital sodium, and neck
vessels were harvested after fixation in situ by perfusion of 10%
phosphate-buffered formalin into the ascending aorta through a
median sternotomy. Harvested arteries were subjected to usual
histological examination, and vascular wall thickness,
defined as the distance between external elastic lamina and
endothelium, was measured in at least five sections
from each vessel. Of 16 grafts, 14 were patent after 4 weeks of
observation (patency rate, 0.875); the occluded grafts were excluded
from the study.
Peptides
-Human ANP and human CNP were purchased from
the Peptide
Institute.
Determination of cGMP Production
The effects of ANP and CNP
on cGMP production in each
vessel were examined as we previously described.7 Each of
the vessel segments was cleaned of surrounding tissue and was cut
longitudinally on ice. Endothelial cells were denuded
by gentle scraping with the blade of scalpel. Then each vessel segment
was cut into fragments of approximately the same size and was subjected
to cGMP production assay for either ANP or CNP and for vehicle,
each in duplicate. Examined concentrations of the peptides were 10
nmol/L, 100 nmol/L, and 1 µmol/L in humans and 1 nmol/L, 10 nmol/L,
100 nmol/L, and 1 µmol/L in rabbits. Each fragment was preincubated
for 30 minutes at 37°C in 250 µL Dulbecco's modified
Eagle's
medium containing 0.5% fetal calf serum and 0.5 mmol/L
isobutylmethylxanthine. ANP or CNP was added to
the medium and incubated for another 30 minutes at 37°C. After the
incubation, trichloroacetic acid was added to a final concentration of
6% and the tissue fragments were mechanically homogenized
in the medium by a Teflon homogenizer. After the
trichloroacetic acid was removed by extraction three times with
water-saturated ether, the amount of cGMP in the sample was
determined by radioimmunoassay after succinylation as described
elsewhere.11 The production of cGMP was expressed
on a molar basis and was normalized by wet weight of the tissue
fragments.
Characterization of Gene Expressions of Biologically Active
Natriuretic Peptide Receptors
Gene expressions of NPR-A and NPR-B were
characterized by
the RT-PCR method. Total RNA was extracted by the guanidinium
thiocyanate–CsCl method from GEA, IMA, and SV pooled from at least
three patients. The specific primers for PCR were synthesized with an
Applied Biosystems 381A DNA Synthesizer according to the
nucleotide sequence of each receptor in humans (NPR-A:
sense, 5'-GGGGATGTAGAAATGAAGGGC-3' and antisense,
5'-TCATGGTAGAAGCAAGGCATACAGG-3'; NPR-B: sense,
5'-TGACCAGCTGAGGCTACGCA-3' and antisense,
5'-CTACAACTTCCATATAAGGT-3').5 12 cDNA was
synthesized from
1 µg of total RNA by oligo (dT) priming with Molony murine leukemia
virus reverse transcriptase (Life Technologies Inc) and was subjected
to PCR using Taq DNA polymerase (Takara Shuzo). After 30
cycles of PCR, aliquots of the PCR products were
size-fractionated by agarose gel electrophoresis, and then gels
were subjected to ethidium bromide staining and Southern blot
analysis. For Southern blot analysis,
32P-labeled synthetic oligomer was used as a probe. The
nucleotide sequences of the probes were
5'-GAGCTTACAGGCTGAGCCAA-3' for NPR-A and
5'-GGTGGTAGAGGAGACATGGAT-3' for NPR-B. As an
internal control, Southern blotting of RT-PCR product for G3PDH was
also done by specific primers and oligoprobe (sense,
5'-TCAAGGCTGAGAACGGGAAGC-3'; antisense,
5'-CTTCACCACCTTCTTGATGTC-3';
oligoprobe, 5'-CTCATGACCACAGTCCAT-3').13 Every blot
was
quantified by NIH Image 1.52 software after being scanned by an HP
ScanJet 3c flatbed scanner (Hewlett-Packard) and was presented
in arbitrary units such that 1 unit equaled the intensity of blot for
G3PDH in each vessel.
To confirm the quantification by RT-PCR, we also performed PCR for NPR-A, NPR-B, and G3PDH using 0.25, 0.5, and 2 times the amount of cDNA and examined whether the intensity of blots increased according to the amount of cDNA.
Statistical Analysis
All values were expressed as
mean±SEM. When two mean values
between different groups were compared, a two-sided unpaired
Student's t test was performed. When mean values between
more than three groups were compared, factorial ANOVA followed by
Fisher's protected least significant difference was performed.
Statistical significance was defined as a value of
P<.05.
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Results |
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TopAbstractIntroductionMethods Results Discussion References |
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Effects of ANP and CNP on cGMP Production in Human GEA, IMA, and SV
Fig 1
shows the effects of ANP and CNP on
cGMP
production in GEA, IMA, and SV segments. Basal cGMP
production (vehicle) in GEA (n=3), IMA (n=6), and SV
(n=7) was
22.6±6.1, 8.2±1.8, and 4.9±1.7 fmol/mg wet tissue,
respectively (GEA
versus IMA, P=.004; GEA versus SV, P=.0007;
IMA
versus SV, P=.32). In all three vessels, ANP and CNP
exhibited significant augmentation of cGMP production. ANP
stimulated cGMP production more potently in GEA and IMA than in
SV. ANP at a concentration of 1 µmol/L augmented cGMP
production by 23.3-fold in GEA and 27.4-fold in IMA but only
4.2-fold in SV. In contrast, the effect of CNP on cGMP
production did not differ significantly between GEA, IMA, and
SV at any concentration. CNP 1 µmol/L elevated cGMP
production by 3.0-fold in GEA, 2.7-fold in IMA, and 3.2-fold in
SV. Therefore, the effect of ANP was more potent by at least one order
of magnitude in GEA and IMA than in SV. The effect of CNP on cGMP
production was almost equipotent in GEA, IMA, and SV and was
almost equivalent to the effect of ANP in SV.
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P<.01, 
P<.005 by Fisher's
protected least
significant difference.
Gene Expressions of Biologically Active Natriuretic
Peptide Receptors in GEA, IMA, and SV
Fig 2A shows the
results of Southern blot
analysis on PCR-amplified products of the transcripts for
two subtypes of the biologically active natriuretic peptide
receptor in GEA (n=3, pooled), IMA (n=3, pooled), and SV
(n=4, pooled).
As shown in the figure, specific signal for NPR-A gene transcript in
GEA or IMA was about four times more intense than that in SV. In
contrast, the intensity of the specific signal for NPR-B gene
transcript was approximately the same in GEA, IMA, and SV. Fig
2B shows
the results of Southern blot analysis for NPR-A, NPR-B, and
G3PDH gene transcripts using 0.25, 0.5, 1, and 2 times the amount of
cDNA from GEA used in the analysis shown in Fig 2A. The
intensities of blots for PCR-amplified products of NPR-A, NPR-B,
and G3PDH transcripts increased in an almost linear relation to the
amounts of cDNA used (Fig 2B).
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Effects of ANP and CNP on cGMP Production in Rabbit Carotid
Artery, Jugular Vein, and Arterialized Vein
Graft
As shown in Fig 3, in the arterialized
vein grafts 4 weeks after operation, wall thickness measured in
histological sections was 116±20 µm (n=5). This was
significantly greater than wall thickness of intact jugular veins
(21±1 µm, n=5, P<.0001) and comparable to that
of intact
carotid arteries (108±6 µm, n=5, P=.71).
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The effects of ANP and CNP on cGMP production in rabbit vessels
are shown in Fig 4. Basal production of cGMP was
36.6±3.7 fmol/mg wet tissue in carotid arteries (n=15),
16.2±2.5
fmol/mg wet tissue in jugular veins (n=9), and 13.8±2.0 fmol/mg
wet
tissue in arterialized vein grafts (n=9) (carotid artery
versus jugular vein, P=.0001; carotid artery versus vein
graft, P<.0001; jugular vein versus vein graft,
P=.64). ANP stimulated cGMP production more potently
in carotid arteries than in jugular veins, but the difference of
responsiveness to ANP between the artery and the vein was smaller than
that in humans. ANP at a concentration of 1 µmol/L augmented cGMP
production by 12.6-fold in carotid arteries but 6.9-fold in
jugular veins. In arterialized vein grafts, ANP at a
concentration of 1 µmol/L caused only a 3.6-fold increase of cGMP
production. The effect of CNP on cGMP production did
not differ significantly between carotid arteries, jugular veins, and
arterialized vein grafts at any concentration. CNP 1
µmol/L elevated cGMP production by 6.0-fold in carotid
arteries, 4.9-fold in jugular veins, and 5.0-fold in
arterialized vein grafts.
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Discussion |
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TopAbstractIntroductionMethods Results Discussion References |
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The present study demonstrates that in humans, ANP augments cGMP production more potently in GEA and IMA than in SV, and CNP exerts weak stimulatory action on cGMP production similarly in GEA, IMA, and SV. In rabbit vessels, similar effects of ANP and CNP on cGMP production were observed; the stimulatory effect of ANP on cGMP production was more potent in carotid arteries than in jugular veins; and the effect of CNP was weak and almost the same in carotid arteries and in jugular veins. Most of the biological activities of natriuretic peptides are thought to be mediated by intracellular elevation of cGMP through the activation of the particulate guanylate cyclases (NPR-A and NPR-B).14 Therefore, our results suggest that ANP can elicit its vasodilating effect preferentially in arteries compared with veins. Actually, Hughes et al15 reported that ANP produced concentration-dependent relaxation in isolated human arteries, including pulmonary, brachial, uterine, and saphenous arteries, but not in saphenous veins. Wei et al16 reported that ANP but not CNP caused vasorelaxation in isolated canine renal arteries. Our results in human and rabbit arteries and veins were consistent with those results. However, Wei et al16 also reported that CNP but not ANP was a relaxing factor of isolated canine renal, saphenous, and femoral veins. We did not observe the difference in the responsiveness to CNP and ANP of human saphenous and rabbit jugular veins. The differences in the response to ANP and CNP in the veins between our results and theirs might be due to the difference in the vessels examined or the species.
Augmentation of cGMP production in response to ANP and CNP was considered to reflect the expression of biologically active natriuretic peptide receptors in the vessel. As we have reported previously, in cultured PC12 cells, which express only NPR-A, ANP and BNP at concentrations >10 nmol/L significantly increased cGMP production and 1 µmol/L of ANP caused a 20-fold increase of cGMP generation, whereas CNP exerted almost no effect even at a concentration of 1 µmol/L.7 In contrast, in cultured rat aortic smooth muscle cells with a synthetic phenotype, which express predominantly NPR-B, CNP at concentrations >100 nmol/L significantly increased cGMP production, whereas ANP and BNP slightly increased cGMP production at a concentration of 1 µmol/L.7 From these results, it is obvious that cGMP production in response to ANP reflects the amount of NPR-A and that cGMP production in response to CNP reflects the amount of NPR-B. Therefore, the differential effects of ANP and CNP on cGMP production in human and rabbit arteries and veins suggest that NPR-B is expressed almost equally in arteries and veins in low quantity, whereas NPR-A is expressed as much as NPR-B in veins but is expressed more abundantly by one or two orders of magnitude in arteries. Indeed, the results of Southern blot analysis demonstrated that NPR-B mRNA expression was about the same in human IMA, GEA, and SV, whereas the gene expression of NPR-A was more abundant in GEA and IMA than in SV.
Another important finding in the present study is that the effects of ANP and CNP on cGMP production in the rabbit jugular veins did not change when the vein was incorporated into the arterial circulation. Although the wall thicknesses of the arterialized vein grafts were comparable to those of carotid arteries, basal cGMP production of the arterialized vein grafts was significantly lower than that of carotid arteries and almost the same as that of jugular veins. From these results, it is suggested that there are some differences in characteristics between VSMCs in intact arteries and VSMCs in neointima occurring in veins. Otherwise, it is possible that 4 weeks of observation was too short for VSMCs to alter their phenotype from the "venous" to the "arterial" type.
In the present study, the concentrations of ANP and CNP necessary to augment cGMP production in isolated vessels exceeded the levels of ANP and CNP detected in human circulation under physiological and pathophysiological conditions (at most 300 pmol/L and 50 pmol/L, respectively), as we and others previously reported.1 4 17 But we have demonstrated that the elevated plasma cGMP level of stroke-prone spontaneously hypertensive rats with a plasma ANP level of 300 pmol/L was significantly reduced by the intravenous administration of our monoclonal antibody against ANP.18 Furthermore, in our recent observations, when the CNP gene was overexpressed by adenovirus-mediated gene transfer in cultured VSMCs that expressed predominantly NPR-B, the VSMCs exhibited enhanced cGMP production and a significantly lower growth rate (unpublished observations). In this system, the CNP concentration in the culture medium was about 100 pmol/L. Exogenously administered CNP at that concentration exerts no effects on cGMP production in cultured VSMCs.19 20 Therefore, a difference exists in the effective concentration of exogenously administered natriuretic peptides and endogenously produced natriuretic peptides. It is thus possible that GEA and IMA produce more cGMP than SV in vivo in response to circulating ANP and BNP at the enhanced level.
The stimulating effect of exogenous CNP on cGMP production was not as prominent as that of ANP and was almost equal in GEA, IMA, and SV. As we and others have demonstrated, CNP is produced by vascular endothelial cells and is suggested to be a local regulator of vascular tone and growth rather than a circulating hormone.3 21 We also reported that the endothelial production of CNP is markedly augmented by several growth factors and cytokines.3 22 Therefore, the possibility still remains that CNP at the enhanced level activates NPR-B in an autocrine and paracrine manner in atherosclerotic vessels.
In conclusion, the present study demonstrated that ANP stimulates cGMP production more potently in IMA and GEA than SV in humans and in the carotid artery more than the jugular vein and the arterialized vein graft in rabbits. This is due to the preferential expression of NPR-A in these arteries. Circulating ANP thus can elicit more prominent vasodilating and antiproliferative effects in arteries than in veins. CNP is considered to exert less effect than ANP on either arteries or veins. These observations support the distinct roles of natriuretic peptides in cardiovascular homeostasis: ANP as a circulating hormone and CNP as a local regulator of vascular tone and remodeling.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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This work was supported in part by research grants from the Japanese Ministry of Education, Science, and Culture. We thank Dr Ario Yamazato of Kyoto Takeda Hospital, Dr Jun-ichi Soneda of Takeda General Hospital, Dr Toshifumi Takeuchi of Mitsubishi Kyoto Hospital, and Dr Teiji Oda of Otowa Hospital for their assistance in tissue samplings.
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Footnotes |
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1 The first two authors contributed equally to this study.
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References |
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TopAbstractIntroductionMethods Results Discussion References |
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1. Mukoyama M, Nakao K, Hosoda K, Suga S, Saito Y, Ogawa Y, Shirakami G, Jougasaki M, Obata K, Yasue H, Kambayashi Y, Inouye K, Imura H. Brain natriuretic peptide as a novel cardiac hormone in humans: evidence for an exquisite dual natriuretic peptide system, atrial natriuretic peptide and brain natriuretic peptide. J Clin Invest.. 1991;87:1402-1412.
2.
Komatsu Y, Nakao K, Suga S, Ogawa Y, Mukoyama M, Arai
H, Shirakami G, Hosoda K, Nakagawa O, Hama N, Kishimoto I, Imura H.
C-type natriuretic peptide (CNP) in rats and
humans. Endocrinology.. 1991;129:1104-1106.
3. Suga S, Nakao K, Itoh H, Komatsu Y, Ogawa Y, Hama N, Imura H. Endothelial production of C-type natriuretic peptide and its marked augmentation by transforming growth factor-ß: possible existence of `vascular natriuretic peptide system.' J Clin Invest.. 1992;90:1145-1149.
4. Hama N, Itoh H, Shirakami G, Suga S, Komatsu Y, Yoshimasa T, Tanaka I, Mori K, Nakao K. Detection of C-type natriuretic peptide in human circulation and marked increase of plasma CNP level in septic shock patients. Biochem Biophys Res Commun.. 1994;198:1177-1182. [Medline] [Order article via Infotrieve]
5. Chang MS, Lowe DG, Lewis M, Hellmiss R, Chen E, Goeddel DV. Differential activation by atrial and brain natriuretic peptides of two different receptor guanylate cyclases. Nature.. 1989;341:68-72. [Medline] [Order article via Infotrieve]
6.
Koller KJ, Lowe DG, Bennett GL, Minamino N, Kangawa K,
Matsuo H, Goeddel DV. Selective activation of the B
natriuretic peptide receptor by C-type
natriuretic peptide (CNP). Science.. 1991;252:120-123.
7.
Suga S, Nakao K, Hosoda K, Mukoyama M, Ogawa Y,
Shirakami G, Arai H, Saito Y, Kambayashi Y, Inouye K, Imura H.
Receptor selectivity of natriuretic peptide family,
atrial natriuretic peptide, brain natriuretic
peptide, and C-type natriuretic peptide.
Endocrinology.. 1992;130:229-239.
8. Hunt PJ, Richards AM, Espiner EA, Nicholls MG, Yandle TG. Bioactivity and metabolism of C-type natriuretic peptide in normal man. J Clin Endocrinol Metab.. 1994;78:1428-1435. [Abstract]
9. Cargill RI, Struthers AD, Lipworth BJ. Human C-type natriuretic peptide: effects on the haemodynamic and endocrine responses to angiotensin II. Cardiovasc Res.. 1995;29:108-111. [Medline] [Order article via Infotrieve]
10. Igaki T, Itoh H, Suga S, Hama N, Ogawa Y, Komatsu Y, Mukoyama M, Sugawara A, Yoshimasa T, Tanaka I, Nakao K. C-type natriuretic peptide in chronic renal failure and its action in humans. Kidney Int. In press.
11. Honma M, Satoh T, Takezawa J, Ui M. An ultrasensitive method for the simultaneous determination of cyclic AMP and cyclic GMP in small volume samples from blood and tissue. Biochem Med.. 1977;18:257-273. [Medline] [Order article via Infotrieve]
12. Lowe DG, Chang MS, Hellmiss R, Chen E, Singh S, Garbers DL, Goeddel DV. Human atrial natriuretic peptide receptor defines a new paradigm for second messenger signal transduction. EMBO J.. 1989;8:1377-1384. [Medline] [Order article via Infotrieve]
13.
Tso JY, Sun XH, Kao TH, Reece KS, Wu R.
Isolation and characterization of rat and human
glyceraldehyde-3-phosphate dehydrogenase cDNAs: genomic
complexity and molecular evolution of the gene. Nucleic
Acids Res.. 1985;13:2485-2502.
14. Chinkers M, Garbers DL, Chang MS, Lowe DG, Chin HM, Goeddel DV, Schulz S. A membrane form of guanylate cyclase is an atrial natriuretic peptide receptor. Nature.. 1989;338:78-83. [Medline] [Order article via Infotrieve]
15.
Hughes A, Thom S, Goldberg P, Martin G, Sever P.
Direct effect of -human atrial natriuretic
peptide on human vasculature in vivo and in
vitro. Clin Sci.. 1988;74:207-211.
16.
Wei CM, Aarhus LL, Miller VM, Burnett JC Jr.
Action of C-type natriuretic peptide in isolated
canine arteries and veins. Am J Physiol.. 1993;264:H71-H73.
17.
Burnett JC Jr, Kao PC, Hu DC, Heser DW, Heublein D,
Granger JP, Opgenorth TJ, Reeder GS. Atrial
natriuretic peptide elevation in congestive heart failure
in the human. Science.. 1986;231:1145-1147.
18. Itoh H, Nakao K, Mukoyama M, Yamada T, Hosoda K, Shirakami G, Morii N, Sugawara A, Saito Y, Shiono S, Arai H, Yoshida I, Imura H. Chronic blockade of endogenous atrial natriuretic polypeptide (ANP) by monoclonal antibody against ANP accelerates the development of hypertension in spontaneously hypertensive and deoxycorticosterone acetate-salt-hypertensive rats. J Clin Invest.. 1989;84:145-154.
19. Furuya M, Takehisa M, Minamitake Y, Kitajima Y, Hayashi Y, Ohnuma N, Ishihara T, Minamino N, Kangawa K, Matsuo H. Novel natriuretic peptide, CNP, potently stimulates cyclic GMP production in rat cultured vascular smooth muscle cells. Biochem Biophys Res Commun.. 1990;170:201-208. [Medline] [Order article via Infotrieve]
20. Furuya M, Yoshida M, Hayashi Y, Ohnuma N, Minamino N, Kangawa K, Matsuo H. C-type natriuretic peptide is a growth inhibitor of rat vascular smooth muscle cells. Biochem Biophys Res Commun.. 1991;177:927-931. [Medline] [Order article via Infotrieve]
21.
Stingo AJ, Clavell AL, Heublein DM, Wei CM, Pittelkow
MR, Burnett JC Jr. Presence of C-type natriuretic
peptide in cultured human endothelial cells and
plasma. Am J Physiol.. 1992;263:H1318-H1321.
22.
Suga S, Itoh H, Komatsu Y, Ogawa Y, Hama N, Yoshimasa
T, Nakao K. Cytokine-induced C-type
natriuretic peptide (CNP) secretion from vascular
endothelial cells: evidence for CNP as a novel
autocrine/paracrine regulator from endothelial
cells. Endocrinology.. 1993;133:3038-3041.
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