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Eur J Cardiothorac Surg 2000;17:175-181
© 2000 Elsevier Science NL

Natriuretic peptides stimulate cyclic guanosine monophosphate production in human saphenous vein and internal mammary artery

Johannes Bonattia, Wolfgang Dichtla, Angelika Lercherb, Bernd Puschendorfb

a Division of Surgery/Cardiac Surgery, Innsbruck University Hospital, University of Innsbruck, Innsbruck, Austria
b Institute for Medical Chemistry and Biochemistry, University of Innsbruck, Innsbruck, Austria

Corresponding author. Tel.: +43-512-504-3806/2529; fax: +43-512-504-2528
e-mail: johannes.o.bonatti{at}uibk.ac.at


   Abstract
Top
 Abstract
1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 
Objective: It has been shown previously that the internal mammary artery releases more cyclic guanosine monophosphate after stimulation with atrial natriuretic peptide than the saphenous vein, and that C-type natriuretic peptide possesses a cyclic guanosine monophosphate stimulating potential on saphenous vein bypass grafts. The present study was undertaken to investigate intracellular content and extracellular release of cyclic guanosine monophosphate, by the internal mammary artery and saphenous vein, after challenge with further members of the natriuretic peptide family. Methods: Specimens of human internal mammary artery and saphenous vein from 29 patients were cut into segments and stimulated with 10-6 M concentrations of atrial natriuretic peptide (internal mammary artery n=8, saphenous vein n=10), brain natriuretic peptide (internal mammary artery n=9, saphenous vein n=13), C-type natriuretic peptide (internal mammary artery n=12, saphenous vein n=15), and urodilatin (internal mammary artery n=8, saphenous vein n=12). Intracellular content and extracellular release of cyclic guanosine monophosphate were determined using an 125I radioimmunoassay. Results: The following median stimulated intracellular cyclic guanosine monophosphate concentrations were measured in the internal mammary artery and saphenous vein: 35358 and 8672 fmol/cm2 (P<0.001) after atrial natriuretic peptide, 45632 and 7830 fmol/cm2 (P=0.003) after brain natriuretic peptide, 10144 and 13216 fmol/cm2 (P=NS for intergraft comparison) after C-type natriuretic peptide, and 20949 and 6690 fmol/cm2 (P=0.001) after urodilatin. Stimulation with atrial natriuretic peptide, brain natriuretic peptide and urodilation also led to a significant increase of extracellular cyclic guanosine monophosphate release by the internal mammary artery. Conclusion: We conclude that brain natriuretic peptide and urodilatin exhibit a similarly effective cyclic guanosine monophosphate-stimulating potential on the internal mammary artery as atrial natriuretic peptide. In contrast, C-type natriuretic peptide shows comparable effects on the internal mammary artery and saphenous vein.

Key Words: Coronary artery bypass • Internal mammary artery • Saphenous vein • Natriuretic peptides


   1. Introduction
Top
 Abstract
 1. Introduction
2. Material and methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 
Vasospasm, local thrombosis, and development of neointimal hyperplasia, as well as atherosclerotic lesions, are the main problems jeopardizing a coronary artery bypass graft [1]. Different protecting systems such as the nitric oxide [2] and prostacyclin pathways [3], which exhibit vasodilating and platelet inhibiting actions seem to provide local resistance against these events. Natriuretic peptides due to vasodilating and antiproliferative properties, might provide protective action for coronary artery bypass grafts as well [4–7]. Atrial natriuretic peptide (ANP), brain natriuretic peptide (BNP), and C-type natriuretic peptide (CNP) are the main representatives of the natriuretic peptide family. Their effects are mediated via cyclic guanosine monophosphate (cGMP), which is generated by the intrinsic guanylyl cyclase activity of the type A and type B natriuretic peptide receptor.

We have recently been able to demonstrate superior cGMP production by the internal mammary artery in reponse to ANP, as compared to the right gastroepiploic artery and the saphenous vein [7]. It has been shown by others that the two members of the natriuretic peptide family, ANP and CNP, seem to have different effects on cGMP production in human coronary artery bypass grafts [5,6]. The aim of the present study was to further investigate these variations in cGMP release and to assess the reactions of the internal mammary artery and saphenous vein to stimulation by BNP and the stable natriuretic peptide urodilatin, a substance that could potentially be applied in the clinical setting [8].


   2. Material and methods
Top
 Abstract
 1. Introduction
 2. Material and methods
3. Results
 4. Discussion
 5. Conclusions
 References
 
2.1. Specimens
The study protocol received approval from the Institutional Review Board and written informed consent was obtained from all patients studied. Remnants of IMA and SV were obtained from 29 patients undergoing CABG procedures and transported to the laboratory in HEPES–RPMI 1640 medium (Sigma Aldrich Co. Ltd, UK) at room temperature. Adherent tissue was carefully dissected from the vessel, which was opened longitudinally in order to expose the endothelium. The vessels were then cut into segments, one for control measurements and the others for stimulation with different natriuretic peptides. The number of specimens investigated are shown in Figs. 1–4. From the majority of patients both internal mammary artery and saphenous vein were obtained. In several cases, however, due to inadequate length of internal mammary artery only saphenous vein could be taken for investigation. Control vessels and corresponding stimulated vessels were always obtained from the same patient.



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  		Fig. 1. After stimulation with 10-6 M ANP solution, there was a significant increase of intracellular cGMP-production in both IMA and SV. (* P<0.05 ** P<0.01 vs. control). Stimulated intracellular cGMP content was significantly more pronounced in the internal mammary artery than in the saphenous vein (## P<0.01 IMA vs. SV). ANP, atrial natriuretic peptide; cGMP, cylic guanosine monophosphate; IMA, internal mammary artery; SV, saphenous vein.

 
Small tubes were filled with 450 µl of HEPES–RPMI 1640 medium containing 0.7426 mmol/l of the phosphordiesterase-inhibitor 3-isobutyl-1-methyl-xanthine (IBMX) and 50 µl of ANP (9128, Peninsula, St. Helens, UK), BNP (H 9060, Bachem, Bubendorf, Switzerland), CNP (9030, Peninsula, St. Helens, UK) and Urodilatin (H 3046, Bachem, Bubendorf, Switzerland), respectively. The natriuretic peptide concentration thus was 10-6 M. The intact vascular segments were placed in the solution and incubated for 10 min at 37°C with 5% CO2 and 95% air. Control vessels remained unstimulated in 500 µl HEPES–RPMI 1640 medium. Aliquots were taken from the supernatants and stored at -20°C, until determination of cGMP. For measurement of intracellular cGMP, the IMA and SV pieces were shock frozen in liquid nitrogen and stored at -80°C. They were homogenized in liquid nitrogen and solved in 1 ml of 0.01 M HCl for douncing. After centrifugation at 2200xg for 15 min at 4°C, the supernatant was stored in aliquots at -20°C.

2.2. Determination of cGMP
Cyclic GMP release was measured in the supernatants using an 125I Biotrak Amersham RIA (Amersham International, Buckinghamshire, UK). Aliquots were thawed and acetylated with a solution of acetic anhydride and triethylamine. They were then incubated for 24 h with a fixed quantity of antiserum and a fixed quantity of 125I marked cGMP at 4°C. The antibody-bound cGMP was then reacted with the Amerlex-MTM second antibody reagent, which contains second antibody that is bound to magnetizable polymer particles. The antibody-bound fraction was magnetically separated and then analyzed by a gamma counter. The concentration of unlabelled cGMP in the sample was determined by interpolation from a standard curve.

2.3. Statistical analysis
Statistical analysis was performed on the SPSS for Windows statistical software package. Results are expressed as median plus range. Stimulated vs. control values were compared with the non-parametric Wilcoxon-test for two related samples, comparisons between internal mammary artery and saphenous vein were carried out using the nonparametric Mann–Whitney U-test.


   3. Results
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
4. Discussion
 5. Conclusions
 References
 
3.1. Intracellular cGMP content
There were no statistical differences between internal mammary artery and saphenous vein concerning control levels of intracellular cGMP. ANP led to a more pronounced cGMP stimulating effect in the IMA as compared with the SV (Fig. 1). ANP induced intracellular cGMP concentrations were 35 358 (16 582–81 096) fmol/cm2 and 8672 (3184–19 318) fmol/cm2, respectively (P<0.001). BNP also showed a more pronounced cGMP increasing effect on the IMA than on the SV (Fig. 2). Stimulated concentrations reached 45 632 (3851–127 223) fmol/cm2 and 7830 (75–40 740) fmol/cm2 (P=0.003). Intracellular cGMP content after CNP incubation was significantly increased in both internal mammary artery and saphenous vein and amounted to 10 144 (611–44 545) fmol/cm2 and 13 216 (1220–52 989) fmol/cm2, respectively (P=NS for intergraft comparison) (Fig. 3). Urodilatin was more effective on the IMA than on the SV (Fig. 4). Intracellular cGMP concentrations after incubation with urodilatin were 20 949 (17 648–95 352) fmol/cm2 and 6690 (309–17 325) fmol/cm2 (P=0.001).



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  		Fig. 2. After stimulation with 10-6 M BNP solution, there was a significant increase of intracellular cGMP-production in the IMA (** P<0.01 vs. control), whereas the response of the saphenous vein was not significant. Stimulated intracellular cGMP levels were significantly more pronounced in the internal mammary artery than in the saphenous vein (## P<0.01 IMA vs. SV). BNP, brain natriuretic peptide; cGMP, cylic guanosine monophosphate; IMA, internal mammary artery; SV, saphenous vein.

 


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  		Fig. 3. 10-6 M CNP solution elevated intracellular cGMP in both the IMA and the saphenous vein (** P<0.01 vs. control) with a trend toward higher values in the saphenous vein. CNP, C-type natriuretic peptide; cGMP, cylic guanosine monophosphate; IMA, internal mammary artery; SV, saphenous vein.

 


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  		Fig. 4. After stimulation with 10-6 M urodilatin solution there was a statistically insignificant increase of intracellular cGMP content in IMA and SV. The difference of stimulated values was statistically significant in favour of the internal mammary artery (## P<0.05 IMA vs. SV). cGMP, cylic guanosine monophosphate; IMA, internal mammary artery, SV, saphenous vein.

 
3.2. Extracellular cGMP release
Baseline extracellular cGMP release was significantly higher in IMA vs. SV and showed lower absolute values than intracellular content (Table 1). ANP, BNP, and urodilatin significantly stimulated cGMP release in both internal mammary artery and the saphenous vein, but effects were more pronounced in the former vessel. The influence of CNP on the IMA was considerably less accentuated than the influence of ANP, BNP, and urodilatin. ANP, BNP and CNP were able to significantly increase the extracellular cGMP release from the saphenous vein.


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  		Table 1. Extracellular cGMP release after NP-stimulationa

 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
5. Conclusions
 References
 
4.1. The natriuretic peptide family
Atrial natriuretic peptide and brain natriuretic peptide are produced in atrial and ventricular cardiac myocytes, respectively and predominantely exhibit diuretic, natriuretic, and vasorelaxant actions [9,10]. C-type natriuretic peptide is distinct from A- and B-type natriuretic peptides in both structure and function. It is abundantly produced in the brain, where it acts as a neurotransmitter [11]. Another site of production is the vascular endothelium, and as a local mediator CNP shows vasodilating properties. A potent antigrowth effect has been demonstrated on cultured smooth muscle cells [12] and on neointima formation in a carotid artery injury model [13]. Due to the local vascular actions of CNP, the term ‘vascular natriuretic peptide’ has been created [14].

Urodilatin was first purified by Schulz–Knappe and Forssmann [15], and is produced in the kidney where it causes natriuresis and diuresis in a paracrine fashion. Urodilatin exhibits an N-terminal extension of four amino acids in comparison to circulating ANP. This additional amino acid sequence seems to be responsible for the high resistance of urodilatin to enzymatic degradation by the neutral endopeptidase (NEP). Due to its biochemical stability the substance has already been used as a diuretic and natriuretic substance in clinical studies during the post-operative phase in heart and liver transplantation [8].

4.2. Vascular effects of natriuretic peptides
In general, natriuretic peptides seem to counteract actions of the renin–angiotensin–aldosterone system and the endothelin system, which both cause vasoconstriction and promote vascular growth [16]. ANP and BNP predominantly bind to the guanylyl cyclase receptor type A, and can thereby effectively stimulate the release of cyclic guanosine monophosphate. The cGMP generated by guanylyl cyclase receptors leads to the relaxation of vascular smooth muscle [17].

4.3. Natriuretic peptides in coronary artery disease and coronary artery surgery
What is the importance of the natriuretic peptide system in coronary artery disease and coronary artery surgery? Both ANP and BNP are known to increase coronary blood flow [18]. A study by Honkonen [19] has shown that especially significant stenosis of the right coronary artery leads to high levels of ANP. Elevated plasma levels of ANP can be detected during the course of coronary artery bypass grafting (CABG) procedures [20], an important fact regarding potential intra-operative protection of coronary artery bypass conduits. Nevertheless, CABG seems to have a less pronounced ANP stimulating action than valve replacement [21].

4.4. Natriuretic peptide effects on coronary bypass grafts
It is well known that ANP and BNP show more predominant actions on arteries than on veins. A vasodilating effect of ANP on several human arteries was demonstrated by Hughes [22], whereas a vasodilating effect was absent in human saphenous vein. These findings are well in accordance with results of a study by Aardal, who demonstrated vasodilating properties of ANP on human internal mammary artery specimens in comparison to saphenous vein [4]. A stronger release of the vasodilating second messenger cGMP by the IMA in comparison to the SV was shown in by Zhang [6] and by our research group [7]. Vasodilating properties of BNP on endothelin-1 and phenylephrine precontracted pieces of IMA were demonstrated by Protter and coworkers [23].

In our experiments, we have used micromolar natriuretic peptide concentrations, a level at which others have also found a significant effect on coronary artery bypass grafts [4,5]. Concerning the clinical relevance of our findings, we would like to note that nanomolar concentrations of ANP have been demonstrated for the post-cardiopulmonary bypass period, and in a variety of cardiac dysfunctions [4,24].

One interesting finding in our study is that there seem to be no clear differences in baseline intracellular cGMP content of the internal mammary artery and saphenous vein. Ikeda and Itoh [5] also showed that endothelially denuded and homogenized samples of these two coronary bypass grafts showed about the same baseline content of cyclic GMP. Baseline cGMP release into the medium in our experiments was three to four times higher in the internal mammary artery. This confirms the results of our previous studies [7], which revealed higher basal extracellular release of cGMP by the internal mammary artery as compared with both the saphenous vein and right gastroepiploic artery. Whether the IMA is supplied with a more effective cGMP transport system into the extracellular space has, to our knowledge, not been investigated.

4.5. Effects of different members of the natriuretic peptide family
4.5.1. ANP, BNP
Our study revealed that ANP and BNP show about the same cGMP stimulating pattern on the internal mammary artery and on the saphenous vein. Both natriuretic peptides stimulated intra-and extracellular cGMP production significantly more pronounced in the internal mammary artery. Concerning ANP this is well in accordance with our previous findings [7].

4.5.2. CNP
In contrast to the marked and comparable effects of ANP, BNP, and urodilatin on the IMA and SV, CNP in our study showed only weak cGMP-stimulating action on the internal mammary artery. Similar intracellular levels of cyclic guanosine monophosphate after CNP application were found in the internal mammary artery and saphenous vein. This phenomenon has already been described: Ikeda and coworkers found that CNP, in comparison to ANP, increases the cGMP content of human saphenous vein and internal mammary artery to about the same extent [5]. They provided further explanations for this fact by showing that in the internal mammary artery, significantly more natriuretic peptide receptor type A (NPR-A) gene transcript can be identified than in the saphenous vein. Natriuretic peptide receptor type B (NPR-B) gene transcript, however, was detectable in saphenous vein specimen. Since NPR-B is the main receptor for CNP, this might be another explanation why CNP can stimulate cGMP production in the saphenous vein to a higher extent than other natriuretic peptides. Our results concerning CNP actions on IMA and SV are also well in accordance with findings on isolated canine vessels, which clearly revealed that CNP seems to be a more potent venodilator than ANP [25].

4.5.3. Urodilatin
To our knowledge, no data on the action of urodilatin on coronary artery bypass grafts has been published so far. As our results show, urodilatin seems to stimulate cGMP production by coronary bypass grafts to a similar extent as ANP and BNP, a fact which might be important if natriuretic peptides are considered as potential therapeutic agents. The excellent tolerance in clinical studies during the post-transplant period [8] speaks for functional and clinical testing of urodilatin.


   5. Conclusions
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 5. Conclusions
References
 
According to the findings in this study no clear differences between internal mammary artery and the saphenous vein can be found concerning baseline intracellular content of cyclic guanosine monophosphate. Extracellular cGMP release, however, seems to be more pronounced in the internal mammary artery than in the saphenous vein. ANP, BNP, and urodilatin are able to stimulate intracellular cGMP production and extracellular release of cGMP in both the IMA and the SV but effects on the IMA are much more pronounced. C-type or vascular natriuretic peptide exhibits less pronounced effects on the internal mammary artery and saphenous vein than cardial and renal natriuretic peptides. The cGMP stimulating effect on both coronary bypass grafts is comparable. Urodilatin, as a stable, clinically well tolerated natriuretic peptide, has a potential as a therapeutic agent.


   Acknowledgments
 
The authors wish to thank Dr Hanno Ulmer from the Institute of Biostatistics at Innsbruck University for his assistance in the statistical analysis.


   References
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 

  1. Yang Z., Oemar B., Luscher T.F. Mechanism of coronary bypass graft disease. Schweiz Med Wochenschr 1993;123:422-427.[Medline]
  2. Luscher T.F., Diederich D., Siebenmann R., Lehmann K., Stulz P., von Segesser L., Yang Z.H., Turina M., Gradel E., Weber E., Buhler F.R. Difference between endothelium-dependent relaxation in arterial and in venous coronary bypass grafts. N Engl J Med 1988;319:462-467.[Abstract]
  3. Chaikhouni A., Crawford F.A., Kochel P.J., Olanoff L.S., Halushka P.V. Human internal mammary artery produces more prostacyclin than saphenous vein. J Thorac Cardiovasc Surg 1986;92:88-91.[Abstract]
  4. Aardal S., Helle K.B., Svendsen E. In vitro responses to atrial natriuretic polypeptide in human vessels commonly used as aortocoronary bypass grafts. Scand J Thorac Cardiovasc Surg 1992;26:135-141.[Medline]
  5. Ikeda T., Itoh H., Komatsu Y., Hanyu M., Yoshimasa T., Matsuda K., Nakao K., Ban T. Natriuretic peptide receptors in human artery and vein and rabbit vein graft. Hypertension 1996;27:833-837.[Abstract/Free Full Text]
  6. Zhang L.M., Castresana M.R., McDonald M.H., Johnson J.H., Newman W.H. Response of human artery, vein, and cultured smooth muscle cells to atrial and C-type natriuretic peptides. Crit Care Med 1996;24:306-310.[Medline]
  7. Bonatti J., Dichtl W., Dworzak E.A., Antretter H., Unger F., Puschendorf B., Dapunt O.E. Atrial natriuretic peptide-induced release of cyclic guanosine monophosphate by coronary bypass grafts. Ann Thorac Surg 1998;65:1621-1624.[Abstract/Free Full Text]
  8. Meyer M., Richter R., Forssmann W.G. Urodilatin, a natriuretic peptide with clinical implications. Eur J Med Res 1998;3:103-110.[Medline]
  9. de Bold A.J., Borenstein H.B., Veress A.T., Sonnenberg H. A rapid and potent natriuretic response to intravenous injection of atrial myocardial extract in rats. Life Sci 1981;28:89-94.[Medline]
  10. Flynn T.G., Davies P.L. The biochemistry and molecular biology of atrial natriuretic factor. Biochem J 1985;232:313-321.[Medline]
  11. Kaneko T., Shirakami G., Nakao K., Nagata I., Nakagawa O., Hama N., Suga S., Miyamoto S., Kubo H., Hirai O., Kikuchi H., Imura H. C-type natriuretic peptide (CNP) is the major natriuretic peptide in human cerebrospinal fluid. Brain Res 1993;612:104-109.[Medline]
  12. 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]
  13. Furuya M., Miyazaki T., Honbou N., Kawashima K., Ohno T., Tanaka S., Kangawa K., Matsuo H. C-type natriuretic peptide inhibits intimal thickening after vascular injury. Ann N Y Acad Sci 1995;748:517-523.[Medline]
  14. 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-beta. Possible existence of ‘vascular natriuretic peptide system’. J Clin Invest 1992;90:1145-1149.
  15. Schulz Knappe P., Forssmann K., Herbst F., Hock D., Pipkorn R., Forssmann W.G. Isolation and structural analysis of ‘urodilatin’, a new peptide of the cardiodilatin-(ANP)-family, extracted from human urine. Klin Wochenschr 1988;66:752-759.[Medline]
  16. Brandt R.R., Heublein D.M., Mattingly M.T., Pittelkow M.R., Burnett J.C., Jr Presence and secretion of atrial natriuretic peptide from cultured human aortic endothelial cells. Am J Physiol 1995;268:H921-H925.[Abstract/Free Full Text]
  17. Drewett J.G., Garbers D.L. The family of guanylyl cyclase receptors and their ligands. Endocr Rev 1994;15:135-162.[Abstract/Free Full Text]
  18. Okumura K., Yasue H., Fujii H., Kugiyama K., Matsuyama K., Yoshimura M., Jougasaki M., Kikuta K., Kato H., Tanaka H., Sumida H., Nakao K. Effects of brain (B-type) natriuretic peptide on coronary artery diameter and coronary hemodynamic variables in humans: comparison with effects on systemic hemodynamic variables. J Am Coll Cardiol 1995;25:342-348.[Abstract]
  19. Honkonen E.L., Kaukinen L., Pehkonen E.J., Kaukinen S. Atrial natriuretic peptide and N-terminal atrial natriuretic peptide in plasma reflect right ventricular volumes following coronary artery surgery. Acta Anaesthesiol Scand 1997;41:685-693.[Medline]
  20. Hedner J., Towle A., Saltzman L., Mueller R.A., Norfleet E.A., Watson C.B., Hedner T. Changes in plasma atrial natriuretic peptide-immunoreactivity in patients undergoing coronary artery bypass graft placements. Regul Pept 1987;17:151-157.[Medline]
  21. Wambach G., Hannekum A., Schmidt S., Kaufmann W., Dalichau H. Increased concentrations of atrial natriuretic peptide in the plasma and heart atrium of patients with aortic and mitral valve diseases compared to patients with coronary heart disease. Z Kardiol 1987;76:76-80.[Medline]
  22. Hughes A.D., Thom S.A., Martin G.N., Nielsen H., Hair W.M., Schachter M., Sever P.S., Hughes A., Thom S. Size and site-dependent heterogeneity of human vascular responses in vitro. Direct effect of alpha-human atrial natriuretic peptide on human vasculature in vivo and in vitro. J Hypertens 1988;74(Suppl):207-211.
  23. Protter A.A., Wallace A.M., Ferraris V.A., Weishaar R.E. Relaxant effect of human brain natriuretic peptide on human artery and vein tissue. Am J Hypertens 1996;9:432-436.[Medline]
  24. Oie B.K., Myking O., Hoff P.I., Ohm O.J. The acute effects of induced tachycardia on coronary sinus and arterial plasma levels of atrial natriuretic peptide and on arterial catecholamines. Scand J Clin Lab Invest 1994;54:155-159.[Medline]
  25. Wei C.M., Aarhus L.L., Miller V.M., Burnett J.C., Jr Action of C-type natriuretic peptide in isolated canine arteries and veins. Am J Physiol 1993;264:H71-H73.[Abstract/Free Full Text]
Received June 21, 1999; received in revised form October 27, 1999; accepted November 2, 1999.




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