© 1997 American Heart Association, Inc.
Articles |
Effect of Natriuretic Peptide Family on the Oxidized LDL–Induced Migration of Human Coronary Artery Smooth Muscle Cells
From the First Department of Internal Medicine (M.K., K. Yokokawa, K. Yasunari, H.K., M.M., J.Y.) and the First Department of Pathology (M.U.), Osaka (Japan) City University Medical School.
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 The migration of medial smooth muscle cells (SMCs) into the intima is proposed to be an important process of intimal thickening in atherosclerotic lesions. The present study examined the possible effect of a novel endothelium-derived relaxing peptide, C-type natriuretic peptide (CNP), on oxidized low-density lipoprotein (LDL)–induced migration of cultured human coronary artery SMCs by the Boyden's chamber method. The effect of CNP was compared with that of atrial and brain natriuretic peptides (ANP and BNP, respectively). Oxidized LDL stimulates SMC migration in a concentration-dependent manner between 20 and 200 µg/mL. This stimulation was chemotactic in nature but was not chemokinetic. By contrast, native LDL was without significant activity. CNP-22 clearly inhibited SMC migration stimulated with 200 µg/mL oxidized LDL in a concentration-dependent manner between 10-9 and 10-6 mol/L. ANP-(1-28) and BNP-32 also inhibited oxidized LDL–induced SMC migration at concentrations of 10-7 and 10-6 mol/L, but these effects were weaker than the effect of CNP-22. Such inhibition by these natriuretic peptides was paralleled by an increase in the cellular level of cGMP. Oxidized LDL–induced migration was significantly inhibited by a stable analogue of cGMP, 8-bromo-cGMP, or an activator of the cytosolic guanylate cyclase, sodium nitroprusside. These natriuretic peptides did not suppress the cell adhesion either in the absence or presence of oxidized LDL. These data indicate that oxidized LDL stimulates migration of human coronary artery SMCs and that natriuretic peptides, especially CNP, inhibit this stimulated SMC migration, at least in part, through a cGMP-dependent process. Taken together with the finding that oxidized LDL is present in the intima, CNP may play a role as a local antimigration factor during the process of intimal thickening in hypercholesterolemia-induced coronary atherosclerosis.
Key Words: natriuretic peptide • oxidized low-density lipoprotein • migration • smooth muscle cell • human coronary artery
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Introduction |
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Elevated levels of LDL cholesterol are an important risk factor for coronary atherosclerosis and cardiovascular morbidity.1 2 3 4 LDL is considered to be the main atherogenic class of lipoproteins. However, recent evidence strongly suggests that oxidatively modified LDL possesses more atherogenic properties than does native LDL.5 Actually, oxidized LDL is shown to contribute to the migration of bovine aortic medial SMCs into the intima,6 which is an important process of the initiation and/or the progression of atherosclerosis.7 8
Natriuretic peptides are a family of hormones involved in the control of fluid balance. ANP and BNP are two members of this family9 10 11 that are both secreted through the coronary sinus from the heart.12 13 14 15 CNP is the most recently identified member of this family, which was first identified in the porcine brain.16 Subsequently, CNP is shown to be present in cultured human endothelial cells and plasma.17 Furthermore, Suga et al18 have demonstrated that CNP is produced by cultured bovine vascular endothelial cells, and this production is markedly augmented by transforming growth factor-ß. In addition to its vasorelaxant and natriuretic effects, CNP is shown to be able to inhibit the serum- and PDGF-induced mitogenesis.19 However, the effect of CNP on the oxidized LDL–induced human coronary artery SMC migration and the mechanisms of this effect remain to be clarified.
The objectives of the present study were (1) to determine whether oxidized LDL stimulates migration of cultured SMCs derived from human coronary artery and, if so, (2) to examine the possible effect of human CNP-22 on oxidized LDL–induced migration and (3) to investigate the mechanism of this effect in these cells. In addition, we examined in these cells the effects of human ANP-(1-28) and human BNP-32, the major circulating forms of ANP and BNP in humans, on oxidized LDL–induced migration.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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Materials
SMC basal medium (SmBM) and human coronary artery SMCs were purchased from Clonetics Corp. Trypsin and Versine were purchased from GIBCO Laboratories. Synthetic human ANP-(1-28), human BNP-32, and human CNP-22 were purchased from the Peptide Institute. 8-Bromo-cGMP, sodium nitroprusside, IBMX, human LDL, and BSA were purchased from Sigma Chemical Co. Flasks and multiwell plates were purchased from Becton Dickinson & Co.. The cGMP assay kit was purchased from Yamasa Shoyu Co, Ltd. Diff-Quick staining solution was purchased from Green-cross Corp.
Oxidation of LDL
Before oxidation, LDL was dialyzed against three changes of PBS
to remove EDTA. Then LDL was oxidized at a concentration of 500
µg/mL by exposure to 10 µmol/L CuSO4
for 24 hours at room temperature, followed by dialysis at 4°C for 24
hours against three changes of PBS.20 21 The extent of
lipid peroxidation was estimated as for thiobarbituric acid–reactive
substances. Tetramethoxypropane was used as a standard, and results are
expressed as nanomoles of malondialdehyde equivalents per 100 µg
protein. The average degree of oxidation for native LDL and oxidized
LDL were 0.3±0.1 and 4.1±0.4 nmol malondialdehyde equivalents per 100
µg protein, respectively.
Culture of SMCs
Human coronary artery SMCs were cultured in SmBM
containing human epidermal growth factor (0.5 ng/mL), human
fibroblast growth factor (2 ng/mL), insulin (5 µg/mL),
5% FBS, 50 µg/mL gentamicin sulfate, and 50 µg/mL
amphotericin B. Cells were identified as SMCs according to their
morphological and growth characteristics.22 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 4th and 8th passages were used for
the experiments.
Migration Assay
Migration of SMCs was assayed by a modification of the Boyden's
chamber method using microchemotaxis chambers (Neuro Probe Inc) and
polycarbonate filters (Nucleopore Corp), as previously
reported.23
In this experiment, polycarbonate filters with pores of 12 µm in
diameter were used. In all experiments, collagen-coated filters were
used. Briefly, the membranes were treated with 0.5N acetic acid and
then incubated for 48 to 72 hours at 25°C in a collagen solution (100
µg/mL type I collagen in 0.5N acetic acid).24
They were then air-dried. Cultured SMCs were trypsinized and suspended
at a concentration of 
5.0x105 cells/mL in SmBM
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 medium/0.4% BSA containing oxidized LDL or native LDL was placed in
the lower chamber. The chamber was incubated at 37°C under 5%
CO2 in air for 3, 6, and 9 hours. 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 quantification of
SMC migration. Migration activity is calculated as the mean number of
migrated cells observed in 4HPF and is given as the mean value of four
measurements. In experiments to determine the effect of native LDL or
oxidized LDL on SMC migration, 20, 50, 100, and 200 µg/mL of
these lipoproteins were added to the lower chamber.
Oxidized LDL–induced migration may be separated into chemotactic and chemokinetic components. The chemotactic component was determined by the addition of 200 µg/mL oxidized LDL to the lower chamber only, whereas the chemokinetic component was determined with 200 µg/mL oxidized LDL added to either the upper chamber only or to the upper and lower chamber.6
In experiments to determine the effects of human ANP-(1-28), human BNP-32, and human CNP-22 on oxidized LDL–induced SMC migration, various concentrations (10-9, 10-8, 10-7, and 10-6 mol/L) of these natriuretic peptides were added to the lower chamber in addition to 200 µg/mL oxidized LDL.
In separate experiments, to determine the effects of 8-bromo-cGMP or sodium nitroprusside on oxidized LDL–stimulated SMC migration, these agents were added to the lower chamber in addition to 200 µg/mL oxidized LDL.
Adhesion Assay
SMC adhesion to the filter was assayed under conditions
identical to the SMC migration assay by using microchemotaxis chamber
and polycarbonate filters with pores of 12-µm diameter that had been
precoated with type I collagen as previously described.24
Cultured SMCs were trypsinized and suspended at a concentration of
5.0x105 cells per milliliter in SmBM supplemented with
0.4% BSA. A 200-µL volume of SMC suspension was placed in the upper
chamber, and 40 µL of medium/0.4% BSA containing oxidized LDL, ANP,
BNP, CNP, or a combination of these factors was placed in the lower
chamber. The chamber was incubated at 37°C under 5% CO2
in air for 6 hours. After incubation, the filter was removed and gently
washed to remove nonattached cells. The adherent SMCs on both upper and
lower sides of the filter were fixed in ethanol, stained with
Diff-Quick staining solution, and counted under a microscope (x400)
for quantification of SMC adhesion.
cGMP Measurement
The cell monolayers were washed twice with PBS and then
stimulated for 2, 5, 10, 30, 60, 180, and 360 minutes with different
concentrations of human ANP-(1-28), human BNP-32, or human CNP-22
dissolved in SmBM 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.25 After evaporation by a centrifugal
evaporator, the dry residue was dissolved in an assay buffer. cGMP
levels were determined by radioimmunoassay performed with the cGMP
assay kit, as previously described.26
NO Measurement
We examined whether oxidized LDL increases the
production of NO in cultured human coronary artery SMCs
and, if so, whether natriuretic peptides augment this
production. Cultured SMCs were assayed for NO
production by measuring the stable end product of NO,
NO2, and NO3, as previously
reported.27 Cultured SMCs were incubated for 6 hours in
the absence or presence of 200 µg/mL oxidized LDL or
10-6 mol/L CNP-22.
NO2/NO3 concentrations were expressed as
nanomoles per 107 cells per 6 hours.
Calculations and Analysis
The statistical significance of differences in the results was
evaluated using an unpaired ANOVA, and probability values were
calculated by Scheffé's method.28 All values were
expressed as the mean±SD.
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Results |
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Effect of Oxidized LDL on SMC Migration
Fig 1A
shows time-dependent effects
of various concentrations (20, 50, 100, and 200 µg/mL) of
oxidized LDL on human coronary artery SMC migration. Oxidized
LDL stimulated cell migration in a concentration-dependent manner. SMC
migration increased during the initial 6 hours of incubation, after
which the rate of increase slightly declined. Therefore, subsequent
studies on SMC migration were done with cells incubated for 6 hours. By
contrast, native LDL was without significant activity even after 9
hours.
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Fig 1B
shows the checkerboard analysis of migration activity of
oxidized LDL. The chemotactic component was determined by the addition
of oxidized LDL to the lower chamber only, whereas the chemokinetic
effect was determined with oxidized LDL added to either the upper
chamber only or to both the upper and lower chamber. The presence of
positive concentration gradients of the oxidized LDL across the filter
rather than equal concentration indicates that the
migration-stimulatory effect of this lipoprotein is chemotactic in
nature for human coronary artery SMCs (Fig 1B).
Effects of Natriuretic Peptides on Oxidized LDL–
Induced SMC Migration and cGMP Level
Fig 2 shows effects of various
concentrations (10-9,
10-8, 10-7, and
10-6 mol/L) of human ANP-(1-28), human
BNP-32, and human CNP-22 on SMC migration after stimulation with 200
µg/mL oxidized LDL. ANP-(1-28) and BNP-32 significantly
inhibited oxidized LDL–induced migration at concentrations of
10-7 and 10-6
mol/L. CNP-22 significantly inhibited the oxidized LDL effect
between 10-9 and 10-6
mol/L. The potency of CNP-22 was significantly greater than that
of ANP-(1-28) or BNP-32 (P<.05).
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P<.05 versus human ANP-(1-28) at the
respective concentration.
Effects of natriuretic peptides on cellular cGMP
level in cells treated with 200 µg/mL oxidized LDL are shown
in Fig 3. Cellular cGMP levels rapidly
increased after treatment of the cells with natriuretic
peptides, and the increased cGMP levels were sustained over 6 hours
(Fig 3A). The increase in cellular cGMP levels induced by
natriuretic peptides for 30 minutes was concentration
dependent (Fig 3B). In parallel with the inhibition by ANP-(1-28),
BNP-32, and CNP-22 on oxidized LDL–induced SMC migration, cellular
cGMP increased after treatment with these natriuretic
peptides (Figs 2 and 3B). Actually, CNP-22 was stronger than ANP-(1-28)
or BNP-32 in inhibiting SMC migration and increasing cGMP levels.
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The effects of ANP, BNP, and CNP on the adhesion of SMCs to the filter in the absence or presence of oxidized LDL are also examined. ANP, BNP, and CNP (10-6 mol/L) had no significant effect on cell adhesion, either in the absence or presence of 200 µg/mL oxidized LDL (data not shown).
Effects of 8-Bromo-cGMP and Sodium Nitroprusside on SMC
Migration
To determine whether the inhibitory effects of
natriuretic peptides on SMC migration after stimulation
with oxidized LDL are causally linked to the increase in cellular cGMP,
we examined the effect of a cGMP analogue, 8-bromo-cGMP, on 200
µg/mL oxidized LDL–stimulated SMC migration. 8-Bromo-cGMP
inhibited oxidized LDL–stimulated migration in a
concentration-dependent manner between 10-6
and 10-4 mol/L (Fig 4A).
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Approaching the issue from another point of view, the effect of an
activator of the cytosolic guanylate cyclase,
sodium nitroprusside, on 200 µg/mL oxidized LDL–induced
migration was examined. Sodium nitroprusside inhibited oxidized
LDL–induced migration in a concentration-dependent manner between
10-7 and 10-5
mol/L (Fig 4B).
Effects of Natriuretic Peptides and 8-Bromo-cGMP on the
Basal Migration Activity of Nonstimulated SMCs
Effects of natriuretic peptides and 8-bromo-cGMP on
the basal migration activity of nonstimulated SMCs were examined.
Neither natriuretic peptides (10-6
mol/L) nor 8-bromo-cGMP (10-4
mol/L) inhibited this basal activity (baseline, 5.4±3.2
cells/4HPF; ANP, 5.3±2.7 cells/4HPF; BNP, 5.7±3.1 cells/4HPF; CNP,
5.3±3.0 cells/4HPF; and 8-bromo-cGMP, 5.2±2.8 cells/4HPF).
Effects of Oxidized LDL and CNP on NO Production
Fig 5 shows effects of oxidized LDL
and CNP on NO production in cultured human coronary
artery SMCs. Oxidized LDL (200 µg/mL) slightly but
significantly increased NO production by 6 hours in these
cells. However, CNP did not augment NO production by 6 hours
either in the absence or presence of oxidized LDL.
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Discussion |
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In the present study, we showed that native LDL elicited no effects on the migration of human coronary artery SMCs, whereas oxidized LDL stimulated this migration. Furthermore, evaluation of oxidized LDL–induced migration showed that the migration-stimulatory effect of oxidized LDL was chemotactic in nature for cultured human coronary artery SMCs but was not chemokinetic. This finding seems to be compatible with the study by Autio et al,6 who reported that oxidized LDL stimulates the migration of bovine aortic SMCs. Recent evidence29 suggests that oxidized LDL is present in the intima. Therefore, these observations may raise the hypothesis that oxidation of LDL in the intima may render it chemotactic for medial SMCs, thus contributing to plaque formation and atherogenesis in the coronary artery, although we have no direct evidence in vivo at this time.
We were concerned that LDL oxidized by Cu2+ incubation may interact differently with the arterial wall than does LDL that has been oxidized in vivo.30 However, the Cu2+/oxidized LDL used in the present study shares physical and chemical characteristics with LDL oxidized in vivo, ie, an increased electrophoretic mobility on agarose gels, a high density, and a slightly greater size than native LDL.29 31 32 These observations suggest that Cu2+/oxidized LDL in the present study to a large extent mimics the biological effect of LDL oxidized in vivo. However, the present study cannot conclusively exclude the possibility that Cu2+/oxidized LDL may behave differently in vivo compared with LDL oxidized in vivo.
We have shown for the first time that human CNP-22 strongly
inhibits oxidized LDL–induced migration of human coronary
artery SMCs in a concentration-dependent manner. Actually, 200
µg/mL oxidized LDL–induced SMC migration was significantly
inhibited by human CNP-22 at concentrations of
10-9 to 10-6
mol/L. Percent inhibition by 10-6
mol/L CNP-22 of SMC migration stimulated with 200 µg/mL
oxidized LDL was 60%. Human ANP-(1-28) and human BNP-32 also
inhibited oxidized LDL–induced SMC migration at concentrations of
10-7 and 10-6
mol/L, but these effects were weaker than that of human CNP-22.
Although ANP-(1-28), BNP-32, and CNP-22 are the respective major
circulating forms of ANP, BNP, and CNP in
humans,12 14 15 17 the normal plasma concentrations
(10-10 to 10-11
mol/L) are lower than those of synthetic natriuretic
peptides that inhibited SMC migration in our in vitro study. However,
plasma concentrations of ANP and BNP are found to be markedly high in
patients with severe hypertension,13 15 congestive heart
failure,13 and acute myocardial infarction.33
In addition, vascular SMCs are shown to express a large number of
biologically active receptors of ANP and BNP.34 In
addition, local levels of CNP in coronary vascular tissues may
be much higher than plasma concentration
(10-12 mol/L) of CNP,17
because it has recently been shown that a considerable amount of CNP is
synthesized in and secreted from vascular endothelial
cells.18 In addition, CNP is shown to be the specific
ligand for a guanylate cyclase–linked receptor, termed the
ANP-B receptor, which is separated for the receptor that binds ANP and
BNP and is highly expressed in vascular SMCs.34 35 Taking
the matter into account, our results suggest that CNP-22, by acting
locally as a paracrine, inhibits the migration of human
coronary artery SMCs after stimulation with oxidized LDL. It
has been reported that CNP, as well as ANP and BNP, inhibits the
proliferation of SMCs stimulated with FCS and PDGF.19
Consequently, the natriuretic peptide family, especially
CNP, may antagonize the development of coronary atherosclerotic
vascular lesions in hypercholesterolemic patients.
However, this experiment was performed on cultured vascular SMCs. It
has been demonstrated34 that in intact aortic media, mRNA
of the ANP-A receptor and ANP-B receptor is detected and that the
potency of cGMP 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.36 Therefore, any extrapolation from the
present experiment on cultured SMCs to in vivo conditions should be
carefully performed.
Recently, Sugiyama et al37 have demonstrated that oxidized LDL actually decreases spontaneous and transforming growth factor-ß1–stimulated secretion of CNP from cultured vascular endothelial cells. This finding raises the hypothesis that in the in vivo condition, oxidized LDL in atherosclerotic arterial wall may suppress CNP synthesis and that this may weaken the net antiatherogenic action of CNP. However, our recent study38 using immunohistochemical staining has shown that CNP-positive endothelial cells, SMCs, and macrophages are present in early human coronary atherosclerotic lesions. Therefore, CNP, not only in vascular endothelial cells but also in SMCs and macrophages, may play a role as a local antiatherogenic factor through the inhibition of medial SMC migration into the intima in the initial phase of coronary atherosclerosis, although we have no direct evidence at this time.
In the present study, natriuretic peptides and 8-bromo-cGMP did not inhibit the basal migration activity of nonstimulated SMCs. In addition, natriuretic peptides did not suppress the cell adhesion either in the absence or presence of oxidized LDL. Furthermore, in a trypan blue exclusion test, dead cells stained with trypan blue were not found 6 hours after treatment with 10-6 mol/L natriuretic peptides. Therefore, it is likely that the observed migration-inhibitory effects of natriuretic peptides were not due to their cytotoxicity or their suppression on cell viability.
We have obtained some evidence for a causal link between cGMP production and inhibition of SMC migration after stimulation with oxidized LDL. First, human ANP-(1-28), human BNP-32, and human CNP-22 increased cGMP levels, and these effects paralleled the inhibition of migration. Second, a cGMP analogue, 8-bromo-cGMP, and an activator of the cytosolic guanylate cyclase, sodium nitroprusside, significantly inhibited oxidized LDL–stimulated migration. These results suggest that the natriuretic peptide family, especially CNP-22, inhibits oxidized LDL–stimulated migration, at least in part, through a cGMP-dependent process. Very recently, NO is shown to inhibit angiotensin II–induced migration of rat aortic SMCs in part via a cGMP-dependent mechanism.39 This finding may support our hypothesis. However, further studies are necessary to elucidate the involvement of cGMP and its related systems in the inhibition by natriuretic peptides of oxidized LDL–induced migration of coronary artery SMCs.
Finally, we examined whether oxidized LDL or CNP augments NO release in cultured coronary artery SMCs and whether the observed inhibition by CNP of SMC migration is mediated via released NO. Oxidized LDL slightly but significantly increased NO production in these cells. However, CNP did not augment NO production either in the absence or presence of oxidized LDL. Therefore, it seems to be unlikely, at least in our experimental conditions, that the inhibition of SMC migration and elevation of cGMP by natriuretic peptides are mediated via induction of NO.
Overall, the present work suggests that oxidized LDL stimulates human coronary artery SMCs and that the natriuretic peptide family, especially CNP, inhibits this stimulation. The increase in cellular cGMP levels is likely to be involved in this inhibition. Taken together with two findings that CNP potently suppresses SMC proliferation19 and that oxidized LDL is present in the intima,30 CNP in coronary vascular tissues may antagonize the development of coronary atherosclerosis as a paracrine in hypercholesterolemic patients. However, further in vivo studies will be necessary to elucidate the exact role of endogenous CNP on the initiation or development of hypercholesterolemia-induced coronary atherosclerosis.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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This study was supported by a grant-in-aid for scientific research from the Ministry of Education, Science, and Culture, Japan (572-690-231-646) and a grant from Osaka Heart Club. The authors thank Atsumi Ohnishi and Yuka Inoshita (Division of Hypertension and Atherosclerosis, Osaka City University Medical School) and Hiroyuki Sano (Sumitomo Pharmaceuticals, Osaka) for their technical assistance and Dr Mayumi Furuya (Suntory Institute for Biomedical Research, Osaka) and Dr Naoki Tohdoh (Discovery Research Laboratories III, Sumitomo Pharmaceuticals Research Center, Osaka) for their helpful advice.
Received February 14, 1997; accepted June 6, 1997.
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