(Hypertension. 2000;35:971.)
© 2000 American Heart Association, Inc.
Scientific Contributions |
Effects of Cardiac Natriuretic Peptides on Oxidized Low-Density Lipoprotein– and Lysophosphatidylcholine-Induced Human Mesangial Cell Migration
From The First Department of Internal Medicine, Osaka City University Medical School, Abeno-ku, Osaka, Japan.
Correspondence to Masakazu Kohno, MD, The First Department of Internal Medicine, Osaka City University Medical School, 1-5-7 Asahi-machi, Abeno-ku, Osaka 545-8586, Japan.
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Abstract |
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Abstract—The objectives of the present study were (1) to determine whether oxidized LDL and lysophosphatidylcholine (lyso-PtdCho), a major phospholipid component of oxidized LDL, stimulate the migration of cultured human mesangial cells and (2) to investigate the possible effects on mesangial cell migration of the cardiac natriuretic peptides atrial and brain natriuretic peptide (ANP and BNP). Oxidized LDL (10 and 100 µg/mL) and lyso-PtdCho (10-7 to 10-5 mol/L) stimulated migration in a concentration-dependent manner. In contrast, the effects of native LDL and phosphatidylcholine were modest or nonexistent. Protein kinase C (PKC) inhibitor and downregulation of PKC activity by phorbol ester inhibited oxidized LDL– and lyso-PtdCho–induced migration. Human ANP(1-28) and human BNP-32 significantly inhibited oxidized LDL– and lyso-PtdCho–induced migration in a concentration-dependent manner. C-ANF {des-[Glu18,Ser19,Gly20,Leu21,Gly22]ANP(4-23)}, a specific ligand for ANP clearance receptors, could not inhibit oxidized LDL– and lyso-PtdCho–induced migration. Inhibition by ANP and BNP of lyso-PtdCho–induced migration was paralleled by an increase in the cellular level of GMP. Oxidized LDL– and lyso-PtdCho–induced migrations were inhibited by 8-bromo-cGMP. The results suggest that oxidized LDL and lyso-PtdCho stimulate the migration of human mesangial cells, at least in part, through a PKC-dependent process and that ANP and BNP inhibit this stimulated migration, probably through a cGMP-dependent process.
Key Words: lysophosphatidylcholines • lipoproteins • atrial natriuretic factors • glomerular mesangium • natriuretic peptide, brain
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Introduction |
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Hyperlipidemia is associated with a variety of renal diseases, and experimental evidence suggests a role for hyperlipidemia in the progression of glomerular diseases.1 2 Dietary cholesterol supplementation has been shown to accelerate the development of sclerotic glomerular lesions in experimental models of renal disease and in normal animals.1 2 3 4 LDL has been shown to be mitogenic for mesangial cells.5 6 7 8 9 However, oxidized LDL has been shown to possess more atherogenic properties than native LDL.10 11 12 13 Lysophosphatidylcholine (lyso-PtdCho) is a prominent phospholipid component of oxidized LDL.11 In oxidized LDL particles, the content of lyso-PtdCho is found to be dramatically increased.11 12 Furthermore, recent evidence indicates that lyso-PtdCho possesses mitogenic and chemotactic properties for smooth muscle cells (SMCs),10 13 monocytes, and lymphocytes.14 15 However, the migration of mesangial cells, which are modified SMCs, is believed to play an important role in the pathogenesis of certain glomerular diseases,16 and SMC migration may play a role in the pathogenesis of atherosclerosis. The present study was designed to determine whether oxidized LDL and lyso-PtdCho stimulate the migration of cultured human mesangial cells and, if so, to clarify the mechanism.
Natriuretic peptides are a family of hormones that are involved in the control of fluid balance. Atrial and brain natriuretic peptides (ANP and BNP) are 2 members of this family17 18 19 20 that are secreted through the coronary sinus from the heart.21 22 These hormones have peripheral effects on the vasculature and kidney, resulting in vasorelaxation, natriuresis, and diuresis.23 24 25 26 In addition to their vasorelaxant and natriuretic effects, these cardiac peptides have been shown to inhibit proliferation in mesangial cells as well as in vascular SMCs.27 28 29 Furthermore, we have recently shown that natriuretic peptides inhibit oxidized LDL–induced migration of human coronary artery SMCs. However, it is still uncertain whether these natriuretic peptides inhibit oxidized LDL– and lyso-PtdCho–induced migration of mesangial cells.
Accordingly, a study was designed to examine the possible effects of human ANP(1-28) and human BNP-32, the major circulating forms of ANP and BNP,19 20 21 22 on oxidized LDL– and lyso-PtdCho–induced migration of human mesangial cells.
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Methods |
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Materials
Mesangial cell basal medium (MsGM) and human mesangial cells were purchased from Clonetics Corp. Synthetic human ANP(1-28), human BNP-32, and C-ANF {des-[Glu18,Ser19,Gly20,Leu21,Gly22]ANP(4-23)} were purchased from Peptide Institute. Lyso-PtdCho (palmitoyl), phosphatidylcholine (dipalmitoyl), lysophosphatidylinositol (palmitoyl), lysophosphatidylserine, human LDL, 3-isobutyl-1-methylxanthine, 8-bromo-cGMP, phorbol-12-myristate-13-acetate, and BSA were purchased from Sigma Chemical Co. Staurosporine was purchased from Calbiochem Corp. The protein kinase C (PKC) inhibitor H 7 was purchased from Seikagaku Kogyo Co Ltd.
Mesangial Cell Cultures
Human mesangial cells were cultured in MsGM
containing 5% FCS, 50 µg/mL gentamicin sulfate, and 50 µg/mL
amphotericin B. The mesangial cells were identified
according to the follow-ing criteria26 29 : (1)
morphology, (2) typical microfilaments seen with transmission
electron microscopy, (3) presence of receptors specific to
angiotensin II (Ang II) and contraction in response to Ang
II, and (4) absence of immunofluorescence with
factor VIII antibody. Cells after passages 3 to 7 were used for the
experiment.
Migration Assay
The migration of mesangial cells was assayed
according to a modification of Boyden’s chamber method with the use of
microchemotaxis chambers (Neuro Probe Inc) and polycarbonate filters
(Nucleopore Corp), as previously reported.13 30 In this
experiment, polycarbonate filters with 12-µm-diameter pores were
used. In all experiments, type IV collagen–coated filters were used.
Migration activity is calculated as the mean number of migrated cells
observed in 4 high-power fields (HPF) and is given as the mean value of
4 measurements.
cGMP Measurement
After preincubation, the cell monolayers were washed twice with
serum-free medium and then stimulated for 30 minutes with varying
concentrations (10-9,
10-8, and 10-7 mol/L) of
natriuretic peptides dissolved in medium that contained
5x10-1 mmol/L 3-isobutyl-1-methylxanthine.
cGMP levels were determined through radioimmunoassay with a cGMP kit,
as previously described.31
Measurement of Lactate Dehydrogenase and Assessment of
Cytotoxicity
The cytotoxic effects of high concentrations of lyso-PtdCho and
oxidized LDL on human mesangial cells were assessed on the
basis of lactate dehydrogenase (LDH) release according to a
commercially available method (Sigma Chemical Co) with the procedure
described by Wrobleski and LaDue.32 LDH was measured in
cell culture supernatants after 5 hours of incubation at 37°C in MsGM
with or without varying concentrations of lyso-PtdCho
(10-7, 10-6,
10-5, 10-4, and
5x10-4 mol/L) or oxidized LDL (1, 10, 50, 100,
and 200 µg/mL). Cytotoxicity was expressed as percent LDH activity
present in supernatants of cultured cells compared with total LDH
activity present in 5x105 cells/well
incubated with 1 mL of 1% Triton X-100 for 30
minutes33
Calculations and Statistical Analysis
The statistical significance of differences in the results was
evaluated with 1-way ANOVA, and probability values were obtained with
Scheffé’s method.34 Values are expressed as
mean±SD.
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Results |
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Effects of Oxidized LDL and Lyso-PtdCho on Human Mesangial Cell Migration
Figure 1 shows the concentration-dependent effects of native and oxidized LDL on human mesangial cell migration. Oxidized LDL significantly induced migration in a concentration-dependent manner between 10 and 100 µg/mL. On the other hand, the migration-stimulatory effects of native LDL were modest.
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Figure 2 shows the concentration- and time-dependent effects of lyso-PtdCho on human mesangial cell migration. Lyso-PtdCho significantly induced migration in a concentration- and time-dependent manner between 10-7 and 10-5 mol/L. In contrast, the migration-stimulatory effects of 10-4 and 5x10-4 mol/L lyso-PtdCho were nonexistent. Lyso-PtdCho at 10-4 and 5x10-4 mol/L appeared to be cytotoxic for human mesangial cells, because these concentrations of lyso-PtdCho clearly caused morphological injury or cell lysis (Figure 3) and a marked increase in LDH release from the cells (Figure 4, top). On the other hand, oxidized LDL did not cause clear morphological injury or cell lysis, at least not at the concentration used in the current experiment, and did not cause a significant increase in LDH release even at the concentration of 200 µg/mL (Figure 4, bottom).
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P<0.05 vs control level of 10-hour incubation.
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Table 1 shows the effects on mesangial cell migration of other lysophospholipids that are structurally similar to lyso-PtdCho. When these phospholipids were tested at 2 comparable concentrations, phosphatidylcholine had no significant activity, and lysophosphatidylinositol and lysophosphatidylserine appeared to be less effective than lyso-PtdCho.
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Effects of the PKC Inhibitors on Lyso-PtdCho– and
Oxidized LDL–Induced Human Mesangial Cell
Migration
The stimulatory effect of lyso-PtdCho (10-5
mol/L) on migration was significantly inhibited by the PKC
inhibitors H 7 and staurosporine (Figures 5A and 5B). These inhibitory
effects of H 7 and staurosporine were relatively
concentration dependent. On the other hand, the PKC
inhibitors did not affect the basal migration.
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The migration-stimulatory effect of oxidized LDL (50 µg/mL) was also significantly inhibited by H 7 (10-6 and 10-5 mol/L) (oxidized LDL alone, 38.2±5.7 cells/4 HPF; oxidized LDL+H 7 at 10-6 mol/L, 28.7±3.2 cells/4 HPF, P<0.05; oxidized LDL+H 7 at 10-5 mol/L, 23.1±2.5 cells/4 HPF, P<0.05) and staurosporine (10-8 and 10-7 mol/L) (oxidized LDL alone, 37.7±4.9 cells/4 HPF; oxidized LDL+staurosporine at 10-8 mol/L, 26.2±2.6 cells/4 HPF, P<0.05; oxidized LDL+staurosporine at 10-7 mol/L, 20.7±2.0 cells/4 HPF, P<0.05).
To confirm the importance of the PKC-dependent mechanism in the stimulation by lyso-PtdCho and oxidized LDL of migration activity, PKC depletion was generated through preincubation with a high dose of phorbol-12-myristate-13-acetate (10-7 mol/L) for 24 hours. In PKC-depleted mesangial cells, 10-5 mol/L lyso-PtdCho and 50 µg/mL oxidized LDL failed to stimulate migration (Table 2).
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Effects of ANP and BNP on Lyso-PtdCho– and Oxidized LDL–Induced
Human Mesangial Cell Migration
To clarify whether the alteration in cell number by oxidized
LDL, lyso-PtdCho, ANP, or BNP modifies the result of migration
response, we examined the effect of these substances on
mesangial cell number for 5- and 10-hour incubations.
However, during the 5- and 10-hour incubations, lyso-PtdCho and
oxidized LDL, as well as ANP(1-28) and BNP-32, did not affect
mesangial cell number under our experimental conditions
(data not shown). Therefore, in our experiments with 5- and
10-hour incubations, proliferation could not have affected the result
of the migration assay.
Figures 6A and 6B show the effects of varying concentrations (10-9, 10-8, and 10-7 mol/L) of human ANP(1-28) and BNP-32 on 10-5 mol/L lyso-PtdCho– or 50 µg/mL oxidized LDL–induced mesangial cell migration. Both human ANP(1-28) and human BNP-32 significantly inhibited lyso-PtdCho– and oxidized LDL–induced migration at concentrations of 10-8 and 10-7 mol/L. On the other hand, 10-7 mol/L ANP and BNP had no significant effect on nonstimulated mesangial cell migration (baseline, 10.3±2.3 cells/4 HPF; ANP 10-7 mol/L, 9.3±1.9 cells/4 HPF; BNP 10-7 mol/L, 8.5±1.3 cells/4 HPF). ANP and BNP increased cellular cGMP in a concentration-dependent manner (control, 3.3±0.5 pmol/5x105 cells; ANP 10-9 mol/L, 7.3±1.3 pmol/5x105 cells; BNP 10-9 mol/L, 7.0±1.4 pmol/5x105 cells; ANP 10-8 mol/L, 15.5±2.1 pmol/5x105 cells; BNP 10-8 mol/L, 14.8±1.7 pmol/5x105 cells; ANP 10-7 mol/L, 34.8±3.6 pmol/5x105 cells; BNP 10-7 mol/L, 30.8±2.2 pmol/5x105 cells), and these effects paralleled the inhibition of migration.
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To clarify the role of biological receptors on the migration-inhibitory effects of natriuretic peptide, we examined the effects of C-ANF, a specific ligand for ANP-clearance receptors, on lyso-PtdCho– and oxidized LDL–induced migration of human mesangial cells. As shown in Table 3, C-ANF could not inhibit lyso-PtdCho– and oxidized LDL–induced migration between 10-9 and 10-7 mol/L.
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Effects of 8-Bromo-cGMP on Lyso-PtdCho– and Oxidized LDL–Induced
Mesangial Cell Migration
To elucidate whether the inhibitory effects of ANP and
BNP on lyso-PtdCho– and oxidized LDL–induced mesangial
cell migration are causally linked to the increase in cellular cGMP, we
examined the effect of 8-bromo-cGMP on lyso-PtdCho
(10-5 mol/L)– and oxidized LDL (50
µg/mL)–induced mesangial cell migration. The inhibition
of lyso-PtdCho– and oxidized LDL–induced mesangial cell
migration by ANP and BNP could be reproduced by this analog at
concentrations of 10-6 and
10-4 mol/L (Table 4).
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Discussion |
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In the present study, we have shown that lyso-PtdCho at concentrations of <10-5 mol/L stimulates the migration of cultured human mesangial cells. In contrast, the migration-stimulatory effect of 10-4 and 5x10-4 mol/L was nonexistent. Furthermore, 10-4 and 5x10-4 mol/L lyso-PtdCho clearly caused morphological cell injury or cell lysis for these cells and a marked increase of LDH release from the cells. These results suggest that 10-4 and 5x10-4 mol/L lyso-PtdCho might be cytotoxic for human mesangial cells and that lyso-PtdCho at concentrations within this approximate range, as expected to be present in the levels of oxidized LDL,10 can stimulate migration. On the other hand, phosphatidylcholine had no significant effect. In addition, we have shown that oxidized LDL stimulates human mesangial cell migration and that this effect of native LDL was modest. Furthermore, both oxidized LDL and lyso-PtdCho have been shown to possess mitogenic properties.10 Therefore, these observations raise the hypothesis that the conversion of phosphatidylcholine to lyso-PtdCho may render it chemotactic for mesangial cells, thus contributing to hypercholesterolemia-aggravated glomerulosclerosis. However, there may be intrinsic differences between the effects of exogenously applied lyso-PtdCho and oxidized LDL in the glomerular lesions. In the former case, lyso-PtdCho at concentrations of <10-5 mol/L was immediately incorporated from the medium into cellular membranes.35 During the oxidation of LDL, however, various possible degradation products other than lyso-PtdCho, such as other lysolipids, lipid peroxides, and oxygenated sterols, are generated36 and might exert effects on mesangial cells. Furthermore, there may be some differences between lyso-PtdCho in solution and lyso-PtdCho in oxidized LDL. During the oxidation of LDL, loss of esterified cholesterol, with a relative and absolute increase in free cholesterol content, is observed.37 Changes in the free cholesterol content can alter membrane physicochemical properties, the function of membrane-bound enzymes, and ion transport.38 Furthermore, free cholesterol is shown to impart resistance to oxidative modification.39 Therefore, caution should be exercised in extrapolation of the present in vitro data to in vivo conditions.
The specific mechanisms of action of oxidized LDL and lyso-PtdCho as chemotactic factors for human mesangial cells at least allow us to conceptualize the possibilities. The PKC inhibitors H 7 and staurosporine inhibited the oxidized LDL– and lyso-PtdCho–stimulated mesangial cell migration. The stimulation of migration by oxidized LDL and lyso-PtdCho is also abolished in the PKC-depleted cells. These results suggest that oxidized LDL and lyso-PtdCho stimulate human mesangial cell migration, at least in part, via a mechanism that probably involves the activation of PKC. On the other hand, lysophosphatidylinositol and lysophosphatidylserine were less effective than lyso-PtdCho. However, the precise structural specificity of lyso-PtdCho that has such an effect on human mesangial cell migration remains to be clarified at this time.
Next, we showed that human ANP(1-28) and BNP-32 strongly
inhibited oxidized LDL– and lyso-PtdCho–induced migration of human
mesangial cells in a concentration-dependent manner. In
fact, 50 µg/mL oxidized LDL– and 10-5 mol/L
lyso-PtdCho–stimulated mesangial cell migration was
significantly inhibited by ANP and BNP at concentrations of
10-8 to 10-7 mol/L.
Although human ANP(1-28) and human BNP-32 are the major circulating
forms of ANP and BNP,19 20 21 22 respectively, the normal
plasma concentrations (
10-11 to
10-10 mol/L) are much lower than those of
synthetic natriuretic peptides that inhibited
mesangial cell migration in the present study. However,
plasma ANP and BNP concentrations were found to be high in patients
with various renal diseases or severe hypertension.21 22
Furthermore, 10% of cardiac output delivered to 1 kidney and a high
density of ANP-A receptors are expressed in glomerular
mesangial cells.23 These observations may
suggest the possibility that elevated plasma ANP and BNP concentrations
in patients with renal diseases or severe hypertension may
represent a compensatory mechanism that tends to offset further
progression of glomerulosclerosis through the
inhibition of mesangial cell migration. However, it remains
to be clarified whether ANP and BNP have
physiological roles as modulators of
mesangial cell migration, because high concentrations of
ANP and BNP are required to inhibit the lyso-PtdCho and oxidized LDL
effects on mesangial cell migration.
In the present study, ANP and BNP did not inhibit the basal migration activity of nonstimulated human mesangial cells. Furthermore, in a trypan blue exclusion test, dead cells stained with trypan blue were not found 5 hours after treatment with 10-7 mol/L ANP or BNP. Therefore, it is likely that the observed migration-inhibitory effect of natriuretic peptides was not a result of cytotoxicity or diminished cell viability.
We have obtained some evidence for a causal link between cGMP production and the inhibition of mesangial cell migration after stimulation with oxidized LDL and lyso-PtdCho. First, ANP and BNP increased cGMP levels, and these effects paralleled the inhibition of migration. Second, a cGMP analog, 8-bromo-cGMP. significantly inhibited oxidized LDL– and lyso-PtdCho–stimulated migration. Third, C-ANF, a specific ligand for ANP clearance receptors,40 could not significantly inhibit oxidized LDL– and lyso-PtdCho–induced migration. These results suggest that cardiac natriuretic peptides inhibit oxidized LDL– and lyso-PtdCho–induced migration, at least in part, through a cGMP-dependent process and that the biological rather than the clearance ANP receptor may be involved in this effect. Recently, nitric oxide is shown to inhibit Ang II–induced migration of rat aortic SMCs in part via a cGMP-dependent mechanism.41 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– or lyso-PtdCho–induced migration of human mesangial cells.
In summary, our present findings suggest that oxidized LDL and its major phospholipid component, lyso-PtdCho, stimulate human mesangial cell migration, at least in part, via a PKC-dependent process and that ANP and BNP can inhibit this stimulated migration, probably through a cGMP-dependent process. Taken together with an antimitogenic effect29 of ANP and BNP on glomerular mesangial cells, migration inhibition by these natriuretic peptides may exert an important beneficial effect that tends to lessen the severity of hypercholesterolemia-induced glomerular damage that involves mainly the mesangium.
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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, Japan. The authors gratefully acknowledge the technical assistance of Atsumi Ohnishi, Yuka Inoshita, and Kazuko Shinagawa (Division of Hypertension and Atherosclerosis, The First Department of Internal Medicine, Osaka City University Medical School).
Received September 10, 1999; first decision October 14, 1999; accepted November 19, 1999.
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References |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
1. Schmitz PG, Kasiske BL, O’Donnell MP, Keane WF. Lipids and progressive renal injury. Semin Nephrol. 1989;9:354–369.[Medline] [Order article via Infotrieve]
2. Moorhead JF, Wheeler DC, Varghese Z. Glomerular structures and lipids in progressive renal disease. Am J Med. 1989;87:5–12N–5–20N.[Medline] [Order article via Infotrieve]
3. Kasiske BL, O’Donnell MP, Cleary MP, Keane WF. Treatment of hyperlipidemia reduces glomerular injury in obese Zucker rats. Kidney Int. 1988;33:667–672.[Medline] [Order article via Infotrieve]
4. Diamond JR. Hyperlipidemia of nephrosis: pathophysiologic role in progressive glomerular disease. Am J Med. 1989;87:25N–29N.[Medline] [Order article via Infotrieve]
5. Wasserman J, Santiago A, Rifici V, Holthofer H, Scharschmidt L, Epstein M, Schlondorff D. Interactions of low density lipoprotein with rat mesangial cells. Kidney Int. 1989;35:1168–1174.[Medline] [Order article via Infotrieve]
6. Wheeler DC, Persaud JW, Fernando R, Sweny P, Varghese Z, Moorhead JF. Effects of low-density lipoproteins on mesangial cell growth and viability in vitro. Nephrol Dial Transplant. 1990;5:185–191.
7. Coritsidis G, Rifici V, Gupta S, Rie J, Shan Z, Neugarten J, Schlondorff D. Preferential binding of oxidized LDL to rat glomeruli in vivo and cultured mesangial cells in vitro. Kidney Int. 1991;39:858–866.[Medline] [Order article via Infotrieve]
8. Neugarten J, Schlondorff D. Lipoprotein interactions with glomerular cells and matrix. Contemp Issues Nephrol. 1991;24:173–206.
9. Gupta S, Rifici V, Growley S, Brownlee M, Shan Z, Schlondorff D. Interactions of LDL and modified LDL with mesangial cells and matrix. Kidney Int. 1992;41:1161–1169.[Medline] [Order article via Infotrieve]
10.
Chai Y-C, Howe PH, DiCorleto PE, Chisolm GM. Oxidized
low density lipoprotein and lysophosphatidylcholine stimulate cell
cycle entry in vascular smooth muscle cells. J Biol
Chem. 1996;271:17791–17797.
11.
Parthasarathy S, Steinberg UP, Barnett J, Witztum
JL, Steinberg D. Essential role of phospholipase
A2 activity in endothelial
cell-induced modification of low density lipoprotein. Proc Natl
Acd Sci U S A. 1985;82:3000–3004.
12. Steinberg D, Parthasarathy S, Carew TE, Khoo JC, Witztum JL. Beyond cholesterol: modifications of low-density lipoproteins that increase its atherogenicity. N Engl J Med. 1989;320:915–924.[Medline] [Order article via Infotrieve]
13.
Kohno M, Yokokawa K, Yasunari K, Minami M, Kano H,
Hanehira T, Yoshikawa J. Induction by lysophosphatidylcholine, a
major phospholipid component of atherogenic lipoproteins, of human
coronary artery smooth muscle cell migration.
Circulation. 1998;98:353–359.
14. Quinn MT, Parthasarathy S, Steinberg D. Lysophosphatidylcholine: a chemotactic factor for human monocytes and its potential role in atherogenesis. Proc Natl Acad Sci U S A.. 1988;85:2805–2809.
15. McMurray HF, Parthasarathy S, Steinberg D. Oxidatively modified low density lipoprotein is a chemoattractant for human T lymphocytes. J Clin Invest. 1993;92:1004–1008.
16. Jaffer F, Saunders C, Shultz P, Throckmorton D, Weinshell E, Abboud HE. Regulation of mesangial cell growth by polypeptide mitogens. Am J Physiol. 1989;135:261–269.
17.
de Bold AJ. Atrial natriuretic factor: a
hormone produced by the heart. Science. 1985;230:767–770.
18. Sudoh T, Kangawa K, Minamino N, Matsuo H. A new natriuretic peptide in porcine brain. Nature. 1988;155:740–746.
19. Minamino N, Aburaya M, Ueda S, Kangawa K, Matsuo H. The presence of brain natriuretic peptide of 12,000 daltons in porcine heart. Biochem Biophys Res Commun. 1988;155:740–746.[Medline] [Order article via Infotrieve]
20.
Sugawara A, Nakao K, Morii N, Sakamoto M, Suda M,
Shimokura M, Kiso Y, Kohara M, Yamori Y, Nishimura K, Soneda J, Ban T,
Imura H. 
-Human atrial natriuretic polypeptide is
released from the heart and circulates in the body. Biochem
Biophys Res Commun. 1985;129:439–446.[Medline]
[Order article via Infotrieve]
21. Mukoyama M, Nakao K, Saito K, Ogawa Y, Hosoda K, Suga S, Shirakami G, Jougasaki M, Imura H. Human brain natriuretic peptide, a novel cardiac hormone. Lancet. 1990;335:801–802.[Medline] [Order article via Infotrieve]
22. Kohno M, Horio T, Yokokawa K, Murakawa K, Yasunari K, Akioka K, Tahara A, Toda I, Takeuchi K, Kurihara N, Takeda T. Brain natriuretic peptide as a cardiac hormone in essential hypertension. Am J Med. 1992;92:29–34.[Medline] [Order article via Infotrieve]
23. Ballermann BJ, Hoover RL, Karnovsky MJ, Brenner BM. Physiologic regulation of atrial natriuretic peptide receptors in rat renal glomeruli. J Clin Invest. 1985;76:2049–2056.
24. Fandrey J, Jelkmann W. Prostaglandin E2 and atriopeptin III oppose the contractile effects of angiotensin II in rat mesangial cell cultures. Prostaglandins. 1988;36:249–257.[Medline] [Order article via Infotrieve]
25.
Singhal PC, Decandido S, Satriano JA, Schlondorff D,
Hays RM. Atrial natriuretic peptide and nitroprusside cause
relaxation of cultured rat mesangial cells. Am J
Physiol. 1989;257:C86–C93.
26. Kohno M, Horio T, Ikeda M, Yokokawa K, Fukui T, Yasunari K, Kurihara N, Takeda T, Johchi M. Angiotensin II stimulates endothelin-1 secretion in cultured rat mesangial cells. Kidney Int. 1992;42:860–866.[Medline] [Order article via Infotrieve]
27. Abell TJ, Richards AM, Ikram H, Espiner EA, Yandle T. Atrial natriuretic factor inhibits proliferation of vascular smooth muscle cells stimulated by platelet-derived growth factor. Biochem Biophys Res Commun. 1989;160:1392–1396.[Medline] [Order article via Infotrieve]
28.
Appel RG. Mechanism of atrial natriuretic
factor-induced inhibition of rat mesangial cell
mitogenesis. Am J Physiol. 1990;259:E312–E318.
29.
Kohno M, Ikeda M, Johchi M, Horio T, Yasunari K,
Kurihara N, Takeda T. Interaction of PDGF and natriuretic
peptides on mesangial cell proliferation and endothelin
secretion. Am J Physiol. 1993;265:E673–E679.
30.
Kohno M, Yokokawa K, Yasunari K, Kano H, Minami M, Ueda
M, Yoshikawa J. Effects of natriuretic peptide family on
the oxidized LDL–induced migration of human coronary artery
smooth muscle cells. Circ Res. 1997;81:585–590.
31. Kohno M, Yasunari K, Yokokawa K, Murakawa K, Horio T, Takeda T. Inhibition by atrial and brain natriuretic peptides of endothelin-1 secretion after stimulation with angiotensin II and thrombin of cultured human endothelial cells. J Clin Invest. 1991;87:1999–2004.
32. Wrobleski I, LaDue JS. Lactic dehydrogenase activity in blood. Proc Soc Exp Biol Med. 1955;90:210–215.
33. Chen Y, Morimoto S, Kitano S, Koh E, Fukuo K, Jiang B, Chen S, Yasuda O, Hirotani A, Ogihara T. Lysophosphatidylcholine cause Ca2+ influx, enhanced DNA synthesis and cytotoxicity in cultured vascular smooth muscle cells. Atherosclerosis. 1995;112:69–76.[Medline] [Order article via Infotrieve]
34.
Wallenstein S, Zucker CL, Fleiss JL. Some statistical
methods useful in circulation research. Circ Res. 1980;47:1–9.
35.
Tamura A, Tanaka T, Yamane T, Nasu R, Fujii T.
Quantitative studies on translocation and metabolic
conversion of lysophosphatidylcholine incorporated into the membrane of
intact human erythrocytes from the medium. J Biochem. 1985;97:353–359.
36. Steinbrecher UP, Parthasarathy S, Leake DS, Witztum JL, Steinberg D. Modification of low density lipoprotein by endothelial cells involves lipid peroxidation and degradation of low density lipoprotein phospholipids. Proc Natl Acad Sci U S A.. 1984;81:3883–3887.
37. Roma P, Catapano AL, Bertulli SM, Varesi L, Fumagalli R, Bernini F. Oxidized LDL increase free cholesterol and fail to stimulate cholesterol esterification in murine macrophages. Biochem Biophys Res Commun. 1990;171:123–131.[Medline] [Order article via Infotrieve]
38. Yeagle PL. Lipid regulation of cell membrane structure and function. FASEB J. 1989;3:1833–1842.[Abstract]
39. Tribble DL, Holl LG, Wood PD, Krauss RM. Variations in oxidative susceptibility among six low density lipoprotein subfractions of differing density and particle size. Atherosclerosis. 1992;93:189–199.[Medline] [Order article via Infotrieve]
40.
Koh GY, Nussenzveig DR, Okolicany J, Price DA, Maack T.
Dynamics of atrial natriuretic factor-guanylate
cyclase receptors and receptor-ligand complexes in cultured
glomerular mesangial and renomedullary
interstitial cells. J Biol Chem. 1992;267:11987–11994.
41. Dubey RK, Jackson EK, Lüscher TF. Nitric oxide inhibits angiotensin II-induced migration of rat aortic smooth muscle cell. J Clin Invest. 1995;96:141–149.
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