© 1997 American Heart Association, Inc.
Articles |
Natriuretic Peptide Family as a Novel Antimigration Factor of Vascular Smooth Muscle Cells
From the First Department of Internal Medicine (M.I., M.K., K. Yasunari, K. Yokokawa, T.H., J.Y.) and the First Department of Pathology (M.U.), Osaka City University Medical School, and the Second Department of Internal Medicine, School of Medicine, Chiba University (N.M.), Japan.
Correspondence to Masakazu Kohno, MD, First Department of Internal Medicine, Osaka City University Medical School, 1-5-7 Asahi-machi, Abeno-ku, Osaka 545, Japan.
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Abstract |
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Abstract Vascular smooth muscle cell (SMC) migration is proposed to be an important process in the initiation and/or progression of atherosclerosis. The present study examined the effects of the natriuretic peptide family (atrial, brain, and C-type natriuretic peptides; ANP, BNP, and CNP) on the migration of cultured rat SMCs, using Boyden's chamber methods. Fetal calf serum (FCS) and platelet-derived growth factor (PDGF)-BB potently stimulated SMC migration. Rat ANP(1-28), rat BNP-45, and rat CNP-22 clearly inhibited SMC migration stimulated with FCS or PDGF-BB in a concentration-dependent manner. CNP-22 had the most potent inhibitory effect compared with other natriuretic peptides. When PDGF-BB–induced migration was separated into chemotactic and chemokinetic activities, the chemotactic component was strongly inhibited by these natriuretic peptides. Such inhibition by these natriuretic peptides was paralleled by an increase in the cellular level of cyclic GMP. The addition of a cyclic GMP analogue, 8-bromo cyclic GMP, and an activator of the cytosolic guanylate cyclase, sodium nitroprusside, significantly inhibited FCS- and PDGF-BB–stimulated migration in a concentration-dependent manner. These results suggest that natriuretic peptides, especially CNP-22, inhibit FCS- or PDGF-BB–stimulated SMC migration at least in part through a cyclic GMP–dependent process. Thus, the natriuretic peptide family may play a role as an antimigration factor of SMCs under certain circumstances.
Key Words: natriuretic peptide, atrial, brain, and C-type • migration • smooth muscle cells
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Introduction |
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Vascular SMCs play an important role in atherogenesis. Migration of arterial medial SMCs into the intimal layer is a key process in intimal thickening in atherosclerotic lesions.1 2 A number of factors are known to stimulate SMC migration, such as PDGF,3 transforming growth factor-ß,4 fibronectin,5 fibrinogen,6 and oxidized low-density lipoprotein.7
Natriuretic peptides are a family of hormones involved in the control of fluid balance.8 9 10 ANP and BNP are two members of this family that are both secreted through the coronary sinus from the heart.11 12 13 14 These hormones have peripheral effects on the vasculature and kidney, resulting in vasorelaxation and natriuresis and diuresis.8 9
CNP, which was first identified in the porcine brain, is the most recently identified member of the natriuretic peptide family.15 Subsequently, CNP has been shown to be present in cultured human endothelial cells and plasma.16 Furthermore, Suga et al17 have demonstrated that CNP is produced by cultured bovine vascular endothelial cells. In addition to their vasorelaxant and natriuretic effects, these natriuretic peptides have previously been shown to be able to inhibit serum- and PDGF-induced mitogenesis.18 19 20 21 22 However, the role of the natriuretic peptide family on SMC migration remains to be clarified.
Accordingly, the present study was designed to examine the possible effects of rat ANP(1-28), rat BNP-45, and rat CNP-22 on rat SMC migration after stimulation with FCS and PDGF. In addition, the effect of rat ANP(5-25), which is much weaker (2%) in vasorelaxant and natriuretic-diuretic potency than rat ANP(1-28), on SMC migration was also examined.
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Methods |
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Materials
DMEM, FCS, trypsin, Versine, penicillin, and streptomycin were purchased from GIBCO Laboratories. Synthetic rat ANP(1-28), rat BNP-45, and rat CNP-22 were purchased from Peptide Institute. Synthetic ANP(5-25) was purchased from Peninsula Laboratories, Inc. 8-Bromo cyclic GMP, sodium nitroprusside, IBMX, and BSA were purchased from Sigma Chemical Company. Flasks and multiwell plates were purchased from Becton Dickinson. The cyclic GMP assay kit was purchased from Yamasa Shoyu Co, Ltd. Diff-Quick staining solution was purchased from Green-Cross Corp.
Culture of SMCs
Rat vascular SMCs were grown from the aortic explants of Sprague-Dawley rats and were cultured in DMEM containing 10% FCS, penicillin (50 U/mL), and streptomycin (50 µg/mL) as previously described.23 Cells were identified as SMCs according to their morphological and growth characteristics.24 Cultures were maintained at 37°C with atmospheric air and 5% CO2. Cells were subcultured after treatment with 0.25% trypsin and 0.02% EDTA. Subconfluent SMCs between the 5th and 15th passages were used for the experiments.
Migration Assay
Migration of SMCs was assayed by a modification of Boyden's chamber method using microchemotaxis chambers (Neuro Probe Inc) and polycarbonate filters (Nucleopore Corp) with pores of 5.0 µm in diameter, as previously reported.25 Cultured SMCs were trypsinized and suspended at a concentration of 
5.0x105/mL in DMEM supplemented with 0.4% BSA. The cell number was counted with an electronic cell counter (Model ZB1; Coulter Electronics). A volume of 200 µL of SMC suspension was placed in the upper chamber, and 40 µL of DMEM/0.4% BSA containing a migration factor such as FCS or PDGF was placed in the lower chamber. The chamber was incubated at 37°C under 5% CO2 in air for 4 hours, as previously described.25 After incubation, SMCs on the upper side of the filter were scraped off and the filter was removed. The SMCs that had migrated to the lower side of the filter were fixed in ethanol, stained with Diff-Quick staining solution, and counted under a microscope (magnification x400) for quantitation of SMC migration. Migration activity is calculated as the mean number of migrated cells observed in four high-power fields and is given as the mean value of four measurements.
In experiments to determine the effects of ANP, BNP, CNP, 8-bromo cyclic GMP, and sodium nitroprusside on FCS- and PDGF-BB–induced SMC migration, these agents were added to the lower chamber in addition to 20% FCS or 20 ng/mL PDGF-BB.
PDGF-BB–induced migration was separated into two components: chemotaxis and chemokinesis. The chemotactic component was determined by the addition of PDGF-BB (20 ng/mL) to the lower chamber only, whereas the chemokinetic effect was measured with PDGF-BB (20 ng/mL) added to either the upper chamber only or to both the upper and lower chambers. In addition, to determine whether natriuretic peptides affect chemotactic or chemokinetic activity of PDGF-BB, natriuretic peptides (10-6 mol/L) were added to the upper chamber, lower chamber, or both, in addition to 20 ng/mL PDGF-BB.
Cyclic GMP Measurement
After preincubation, the cell monolayers were washed twice with phosphate buffered saline and then stimulated for 30 minutes with different concentrations of rat ANP(1-28), rat BNP-45, rat ANP(5-25), or rat CNP-22 dissolved in DMEM that contained 5x10-4 mol/L IBMX. The reaction was stopped by rapid aspiration and the addition of 2 mL of ice-cold 65% ethanol, as previously described.26 After evaporation by a centrifugal evaporator, the dry residue was dissolved in an assay buffer. Cyclic GMP levels were determined by radioimmunoassay done with the cyclic GMP assay kit, as previously described.27
Calculations and Analysis
The statistical significance of differences in the results was evaluated using an unpaired analysis of variance, and probability values were calculated by Scheffé's method.28 The relation between the percent increase in cellular cyclic GMP and the percent decrease in migration activity was evaluated using linear regression analysis. All values were expressed as the mean±SD.
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Results |
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Effects of Natriuretic Peptides on FCS-Stimulated SMC Migration
Effects of various concentrations (10-10, 10-9, 10-8, 10-7, and 10-6 mol/L) of rat ANP(1-28), rat BNP-45, rat CNP-22, and rat ANP(5-25) on SMC migration after stimulation with 20% FCS are shown in Fig 1A
. FCS potently stimulated SMC migration. Rat ANP(1-28) significantly inhibited FCS-stimulated migration at concentrations of 10-7 and 10-6 mol/L. Rat BNP-45 and rat CNP-22 significantly inhibited the FCS effect between 10-9 and 10-6 mol/L. The potency of CNP-22 was significantly greater than that of ANP(1-28) at concentrations of 10-6, 10-7, and 10-9 mol/L (P<.05).
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P<.05 versus rat ANP(5-25).
Effects of natriuretic peptides on cellular cyclic GMP level in cells treated with 20% FCS are shown in Fig 1B
. In parallel with the inhibition by ANP(1-28), BNP-45, and CNP-22 on FCS-stimulated SMC migration, cellular cyclic GMP increased after treatment with ANP(1-28), BNP-45, and CNP-22 (Fig 1A and 1B). Actually, rat CNP-22 was stronger than rat ANP(1-28) in inhibiting SMC migration and increasing cyclic GMP levels.
On the other hand, rat ANP(5-25) was much less effective than rat ANP(1-28), rat BNP-45, or rat CNP-22 with respect to inhibiting SMC migration and increasing cyclic GMP levels in cells treated with 20% FCS (Fig 1A and 1B). Rat ANP(5-25) significantly inhibited FCS-stimulated migration only at the highest concentration (10-6 mol/L).
There was a significant correlation between the percent increase in cellular cyclic GMP level and the percent decrease in migration activity in cells treated with 20% FCS (Fig 2).
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Effects of Natriuretic Peptides on PDGF-BB–Stimulated SMC Migration
The effects of natriuretic peptides on SMC migration after stimulation with PDGF-BB (20 ng/mL) were essentially the same as after stimulation with 20% FCS (Fig 3A). PDGF-BB potently stimulated SMC migration. Rat ANP(1-28), rat BNP-45, and rat CNP-22 clearly inhibited PDGF-BB–stimulated SMC migration in a concentration-dependent manner. Rat BNP-45 and CNP-22 significantly inhibited the PDGF effect between 10-10 and 10-6 mol/L. In parallel with the inhibition by ANP(1-28), BNP-45, and CNP-22 of PDGF-stimulated SMC migration, cellular cyclic GMP increased after treatment with ANP(1-28), BNP-45, and CNP-22 (Fig 3A and 3B).
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Rat ANP(5-25) was much less effective than rat ANP(1-28), rat BNP-45, or rat CNP-22 with respect to inhibiting migration and increasing cyclic levels in cells treated with 20 ng/mL PDGF-BB (Fig 3A and 3B). Rat ANP(5-25) significantly inhibited the PDGF effect only at the concentration of 10-6 mol/L.
There was a significant correlation between the percent increase in cellular cyclic GMP level and the percent decrease in migration activity in cells treated with 20 ng/mL PDGF-BB (Fig 4).
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Evaluation of PDGF-BB–induced SMC migration showed that chemotaxis and chemokinesis accounted for 80% and 20%, respectively, of the migration activity observed (Table 1, experiment A). To determine whether the inhibitory activity of natriuretic peptides on cell migration was due to inhibition of chemotaxis or chemokinesis, we added natriuretic peptides with or without PDGF-BB to either the upper chamber only or to both the upper and lower chambers. Natriuretic peptides significantly inhibited the chemotactic activity of PDGF-BB when these natriuretic peptides were added to the upper chamber, the lower chamber, or both (Table 1, experiments B, C, and D). In particular, CNP strongly inhibited the chemotactic activity of PDGF-BB. Natriuretic peptides also had a modestly inhibitory effect on the chemokinetic activity of PDGF-BB (Table 2, experiments A and B). These results indicate that natriuretic peptides strongly suppress the chemotactic effect of PDGF-BB and modestly suppress the chemokinetic effect of PDGF-BB.
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Effect of 8-Bromo Cyclic GMP and Sodium Nitroprusside on SMC Migration
To determine whether the inhibitory effects of natriuretic peptides on SMC migration after stimulation with FCS or PDGF are causally linked to the increase in cellular cyclic GMP, we examined the effect of a cyclic GMP analogue, 8-bromo cyclic GMP, on 20% FCS– and 20 ng/mL PDGF-BB–stimulated SMC migration. 8-Bromo cyclic GMP inhibited FCS- and PDGF-BB–stimulated migration in a concentration-dependent manner between 10-7 and 10-5 mol/L (Fig 5A).
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) or PDGF-BB (). Various kinds of 8-bromo cyclic GMP were added to the lower chamber in addition to 20% FCS or 20 ng/mL PDGF-BB. Migration activities were assayed in quadruplicate, and values are expressed as the mean±SD for the number of cells observed in four high-power fields. B, Effect of sodium nitroprusside on the migration of cultured vascular SMCs stimulated with FCS (
Approaching the issue from another point of view, the effect of an activator of the cytosolic guanylate cyclase, sodium nitroprusside, on 20% FCS– and 20 ng/mL PDGF-BB–stimulated migration was examined. Sodium nitroprusside inhibited FCS- and PDGF-BB–induced migration in a concentration-dependent manner between 10-10 and 10-6 mol/L (Fig 5B).
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Discussion |
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We have shown by Boyden's chamber method that FCS and PDGF-BB potently stimulate the migration of SMCs. It appears reasonable that FCS induces SMC migration, since blood serum contains numerous growth and migration factors for vascular cells.29 30 Among these factors in serum, PDGF is known to have important roles in the development of atherosclerosis not only as a mitogen but also as a chemoattractant.2 We have confirmed the previous reports3 31 that PDGF-BB, as well as FCS, potently stimulates the migration of SMCs.
Second, we have shown that the natriuretic peptide family, especially CNP, inhibits the migration of SMCs stimulated with FCS and PDGF-BB in a concentration-dependent manner. In addition, when PDGF-BB–induced migration was separated into chemotactic and chemokinetic activities,32 natriuretic peptides strongly suppressed the chemotactic effect of PDGF-BB and modestly suppressed the chemokinetic effect of PDGF-BB. The suppression of the chemotactic effect of PDGF-BB by CNP-22 was most potent. To our knowledge, this is the first demonstration concerning the relationship of natriuretic peptides and SMC migration. Actually, 20% FCS–induced SMC migration was significantly inhibited by rat ANP(1-28) at concentrations of 10-7 and 10-6 mol/L and by rat BNP-45 and rat CNP-22 at concentrations of 10-9 to 10-6 mol/L. Inhibition by 10-6 mol/L ANP(1-28), BNP-45, and CNP-22 of SMC migration stimulated with 20% FCS was 70% to 80%. Furthermore, 20 ng/mL PDGF-BB–stimulated SMC migration was significantly inhibited by rat ANP(1-28) at concentrations between 10-9 and 10-6 mol/L and by rat BNP-45 and rat CNP-22 at concentrations between 10-10 and 10-6 mol/L. Inhibition by 10-6 mol/L ANP(1-28), BNP-45, and CNP-22 of SMC migration stimulated with 20 ng/mL PDGF-BB was 40% to 45%. Although ANP(1-28), BNP-45, and CNP-22 are the respective major circulating forms of ANP, BNP, and CNP, the normal plasma concentrations13 14 16 33 34 (10-12 to 10-11 mol/L) are lower than those of synthetic natriuretic peptides, which inhibited SMC migration in our in vitro study. However, several investigators, including our group, have previously shown that these natriuretic peptide levels are markedly high in the malignant or severe stage of rat and human hypertension,12 14 in severe congestive heart failure,12 and in acute myocardial infarction.35 ANP and BNP are secreted through the coronary sinus from the heart,13 14 but ANP is secreted mainly from the atria, and BNP is secreted predominantly from the ventricles.33 34 36 Furthermore, vascular SMCs are shown to express a large number of biologically active receptors of ANP and BNP as well as clearance receptors.37 Taken together with these observations, our data raise the possibility that ANP and BNP secreted from the heart circulate into the general circulation and bind natriuretic peptide receptors in vascular SMCs, thereby inhibiting migration of these cells in a certain pathological condition.
On the other hand, CNP may act as a local antimigration factor in vascular tissues. Actually, levels of CNP in vascular tissues may be much higher than plasma concentration of CNP (10-12 mol/L),16 since it has recently been shown that a considerable amount of CNP is synthesized in and secreted from vascular endothelial cells.17 In addition, CNP is shown to be the specific ligand for a guanylate cyclase–linked receptor termed the ANP-B receptor, which is separate from the receptor that binds ANP and BNP and is highly expressed in vascular SMCs.37 38 Our results suggest that CNP-22, by acting locally as a paracrine, inhibits the migration of SMCs after stimulation with atherogenic factors such as PDGF-BB. However, this study was done on cultured vascular SMCs. It has been demonstrated39 that in intact aortic media, messenger RNA of ANP-A receptor and ANP-B receptor are detected, and the potency of cyclic GMP production by ANP is at least two orders of magnitude stronger than that of CNP. By contrast, in cultured aortic SMCs the ANP-B receptor and the clearance receptor are abundantly expressed, whereas the ANP-A receptor is minimally expressed.39 Therefore, any extrapolation from the present experiment on cultured SMCs to in vivo conditions should be carefully performed.
It has been reported that CNP, as well as ANP and BNP, also inhibits the proliferation of SMCs stimulated with FCS and PDGF.18 19 20 21 22 Furthermore, Furuya et al40 have shown that CNP-22 treatment (1 µg/kg body weight per minute, intravenous infusion) for either 14 or 15 days resulted in 71% and 60% reduction, respectively, of intimal cross-section area 14 days after air-drying injury in rat common carotid arteries in vivo. The migration of arterial medial SMCs into the intima and their proliferation there are important processes of intimal thickening not only in atherosclerotic lesions but also in restenosis after angioplasty.2 41 Consequently, it is possible that natriuretic peptides, especially CNP, antagonize the development of atherosclerotic vascular lesions as an antimigratory and antiproliferative factor for SMCs.
We have obtained some evidence for a causal link between cyclic GMP production and inhibition of SMC migration after stimulation with FCS or PDGF-BB. First, rat ANP(1-28), rat BNP-45, and rat CNP-22 increased cyclic GMP levels, and these effects paralleled the inhibition of migration. Second, rat ANP(5-25) had much weaker effects than other natriuretic peptides with respect to inhibiting SMC migration and increasing cyclic GMP in cells stimulated with FCS and PDGF-BB. Third, a cyclic GMP analogue, 8-bromo cyclic GMP, and an activator of the cytosolic guanylate cyclase, sodium nitroprusside, significantly inhibited FCS- and PDGF-BB–stimulated migration. These results suggest that the natriuretic peptide family inhibits FCS- and PDGF-BB–stimulated migration at least in part through a cyclic GMP–dependent process. Very recently, nitric oxide is shown to inhibit angiotensin II–induced migration of rat aortic SMCs, in part via a cyclic GMP–dependent mechanism.42 This finding may support our hypothesis.
Overall, the present work suggests that natriuretic peptides, especially CNP, inhibit SMC migration and that the increase in cellular cyclic GMP levels is likely to be partially involved in this inhibition. This action may be added to diuresis, natriuresis, vasodilation, and antiproliferation as yet another effect of the natriuretic peptide family.
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Acknowledgments |
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This work was supported by a grant-in-aid for Scientific Research from the Ministry of Education, Science, and Culture of Japan (572-690-231-646) and a grant from Osaka Heart Club. The authors thank Atsumi Ohnishi and Yuka Inoshita for their technical assistance and Dr Mayumi Furuya (Suntory Institute for Biomedical Research, Osaka) for her helpful advice on our work.
Received April 2, 1996; accepted July 19, 1996.
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  M. C. Mendonca, S. Q. Doi, S. Glerum, and D. F. Sellitti Increase of C-Type Natriuretic Peptide Expression by Serum and Platelet-Derived Growth Factor-BB in Human Aortic Smooth Muscle Cells Is Dependent on Protein Kinase C Activation Endocrinology, September 1, 2006; 147(9): 4169 - 4178. [Abstract] [Full Text] [PDF]
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 J.-Y. Qian, A. Leung, P. Harding, and M. C. LaPointe PGE2 stimulates human brain natriuretic peptide expression via EP4 and p42/44 MAPK Am J Physiol Heart Circ Physiol, May 1, 2006; 290(5): H1740 - H1746. [Abstract] [Full Text] [PDF]
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 E. M. Kairuz, M. N. Barber, C. R. Anderson, M. Kanagasundaram, G. R. Drummond, and R. L. Woods C-type natriuretic peptide (CNP) suppresses plasminogen activator inhibitor-1 (PAI-1) in vivo Cardiovasc Res, June 1, 2005; 66(3): 574 - 582. [Abstract] [Full Text] [PDF]
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 M. R. Alexander, J. W. Knowles, T. Nishikimi, and N. Maeda Increased Atherosclerosis and Smooth Muscle Cell Hypertrophy in Natriuretic Peptide Receptor A-/-Apolipoprotein E-/- Mice Arterioscler Thromb Vasc Biol, June 1, 2003; 23(6): 1077 - 1082. [Abstract] [Full Text] [PDF]
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H. Takeuchi, K. Ohmori, I. Kondo, A. Oshita, K. Shinomiya, Y. Yu, Y. Takagi, K. Mizushige, K. Kangawa, and M. Kohno Potentiation of C-type natriuretic peptide with ultrasound and microbubbles to prevent neointimal formation after vascular injury in rats Cardiovasc Res, April 1, 2003; 58(1): 231 - 238. [Abstract] [Full Text] [PDF]
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 K. Morishige, H. Shimokawa, T. Yamawaki, K. Miyata, Y. Eto, T. Kandabashi, K. Yogo, T. Higo, K. Egashira, H. Ueno, et al. Local adenovirus-mediated transfer of C-type natriuretic peptide suppresses vascular remodeling in porcine coronary arteries in vivo J. Am. Coll. Cardiol., March 15, 2000; 35(4): 1040 - 1047. [Abstract] [Full Text] [PDF]
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J. L. Bouchie, H. Hansen, and E. P. Feener Natriuretic Factors and Nitric Oxide Suppress Plasminogen Activator Inhibitor-1 Expression in Vascular Smooth Muscle Cells : Role of cGMP in the Regulation of the Plasminogen System Arterioscler Thromb Vasc Biol, November 1, 1998; 18(11): 1771 - 1779. [Abstract] [Full Text] [PDF]
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