(Hypertension. 1997;29:414.)
© 1997 American Heart Association, Inc.
State-of-the-Art-Lecture |
Expression of Guanylyl Cyclase-A/Atrial Natriuretic Peptide Receptor Blocks the Activation of Protein Kinase C in Vascular Smooth Muscle Cells
Role of cGMP and cGMP-Dependent Protein Kinase
From the Department of Biochemistry and Molecular Biology (R.K., W.A.C., K.N.P.), Medical College of Georgia, School of Medicine, Augusta, and the Department of Pathology (T.M.L.), University of Alabama at Birmingham.
Correspondence to Dr Kailash N. Pandey, Department of Biochemistry and Molecular Biology, Medical College of Georgia School of Medicine, Augusta, GA 30912-2100
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Abstract |
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To understand the molecular mechanisms of cellular signaling of atrial natriuretic peptide (ANP), we have studied its effect on the enzymatic activity of endogenous and overexpressed protein kinase C (PKC) in rat thoracic aortic vascular smooth muscle (RTASM) cells. Angiotensin II (ANG II), endothelin-1 (ET-1), and 12-O-tetradecanoylphorbol 13-acetate (TPA) stimulated fourfold to fivefold PKC activity in PKC-
cDNA-transfected RTASM cells. However, pretreatment of these cells with ANP significantly inhibited the agonist-stimulated PKC activity in a dose-dependent manner. The inhibitory effect of ANP was more effective if cells were transfected with both PKC- and guanylyl cyclase-A/atrial natriuretic peptide receptor (Npra) cDNAs. The agonist-stimulated PKC activity was also inhibited if RTASM cells were pretreated with cGMP analog 8-bromo-cGMP; however, the treatment of cells with a cAMP analog, dibutyryl-cAMP, did not show any discernible effect. The pretreatment of cells with Npra antagonist A-71915, significantly blocked the production of cGMP as well as the inhibitory effect of ANP on PKC activity. To further examine whether the antagonistic action of ANP and 8-bromo-cGMP on agonist-stimulated PKC activity were mediated through cGMP-dependent protein kinase (PKG), cells were treated with ANP or 8-bromo-cGMP and activators of PKC in the presence of KT-5823, a specific inhibitor of PKG. The treatment of cells with KT-5823 significantly attenuated the inhibitory effects of both ANP and 8-bromo-cGMP on agonist-stimulated PKC activity. The results from these studies provide strong evidence that ANP antagonizes the activation of PKC in RTASM cells, involving guanylyl cyclase-A receptor Npra and second messenger cGMP. Our data further support the notion that ANP acts as a negative mediator of signaling cross-talks between Npra and PKC in a cGMP-dependent manner, probably involving cGMP-dependent protein kinase in this process.
Key Words: atrial natriuretic peptide • guanylyl cyclase • receptor-A • protein kinase C • cGMP • angiotensin II • phorbol ester • vascular smooth muscle cells
Abbreviations: ANG II = angiotensin II • ANP = atrial natriuretic peptide • BNP = brain natriuretic peptide • CNP = C-type natriuretic peptide • ET-1 = endothelin-1 • IP3 = inositol 1,4,5 triphosphate • Npra = guanylyl cyclase-linked ANP receptor • PKC, PKG = protein kinase C, G • RTASM = rat thoracic aortic smooth muscle • TPA = 12-O-tetradecanolyphorbol 13-acetate
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Introduction |
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A trial natriuretic peptide is an endogenous and potent hypotensive hormone that regulates sodium excretion, water balance, steroidogenesis, and cell proliferation.1–4 One of the principal components involved in the regulatory action of ANP is the guanylyl cyclase-linked atrial natriuretic peptide receptor (GC-A), also designated as Npra.5 Natriuretic peptide receptor/ guanylyl cyclase-A is a unique class of cell surface receptors that contain an extracellular ligand-binding domain, a single transmembrane spanning region and intracellular protein kinase-like and guanylyl cyclase catalytic domains that synthesizes the intracellular second messenger cGMP in response to ANP binding.6,7 In addition to Npra, another natriuretic peptide receptor with guanylyl cyclase activity (GC-B) has been cloned and designated as Nprb.5 The evidence suggests that both ANP and BNP selectively bind to Npra, and CNP has been shown primarily to bind Nprb.8,9 However, all three natriuretic peptides (ANP, BNP, and CNP) indiscriminately bind to natriuretic peptide-clearance receptor (Nprc), which has been suggested to clear natriuretic peptides from the circulation.10 Although vascular smooth muscle cells predominantly contain Nprc,11 all three natriuretic peptides (ANP, BNP, and CNP) produce increased levels of intracellular cGMP in these cells.12–15 Hitherto, the signaling mechanisms of natriuretic peptides in vascular smooth muscle cells are relatively complex and only poorly understood.
Vascular hypertrophy and increased growth is a characteristic response of the terminally differentiated vascular smooth muscle cells to growth stimuli in vitro.16–18 This is characterized by an increase in protein synthesis and also by load-specific changes in the pattern of gene expression in vivo that can be recapitulated in cultured cells subjected to growth-stimulatory agents in vitro.19 A cascade of the intracellular signaling processes, largely identified in vascular smooth muscle cells, has been proposed to mediate the adaptive response of these cells, a central component of which is the activation of calciumdependent isoforms of PKC. Whether this signaling cascade triggers an adaptive vascular smooth muscle cell hypertrophy and/or normal cellular growth in vivo in still unclear. Previously, Npra has been shown to interact with PKC20,21; however, the exact mechanisms of these interactions have not been clearly elucidated. Accordingly, using rat vascular smooth muscle cells as a model system, we have sought to determine whether coexpression and the activation of PKC- and Npra play a role in signaling pathways and cellular responses of these cells in vitro.
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Methods |
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Materials
ANP (rat-28) was from Peninsula Laboratories. TPA, phosphatidylserine, dibutyryl-cAMP, 8-bromo-cGMP, guanidinium isothiocyanate, and formaldehyde were from Sigma Chemical Co. The EGF-R peptide (VRRTLRL) was from LC Laboratory.
[32P]ATP was from Amersham. [32P]dCTP was from ICN. A-71915 was from Abbott Laboratories. Tissue-culture supplies and formamide were from Life Technologies. PKC- cDNA, cloned from human acute T-cell leukemia, jurkat cell line, was from ATCC. Murine Npra cDNA was previously cloned in our laboratory.7 All other chemicals were of Sigma molecular biology grade.
Cell Cultures
RTASM cell culture was established essentially as previously described.22 Cells were cultured in Dulbecco's modified Eagle's medium (DMEM) containing 10% (vol/vol) fetal calf serum. All cultures were maintained at 37°C in an atmosphere of 5% CO2 and 95% O2. Cultures were fed on alternate days and were sub-cultured every 6 days.
Plasmid Construction
A full-length cDNA coding the PKC- was removed from the plasmid Bluescript by EcoRI digestion and subcloned into the previously EcoRI-digested site of the mammalian expression vector pcDNA3 (Invitrogen). A complete Npra cDNA coding sequence was removed from Bluescript by Not I digestion and was subcloned into the previously Not I-digested pcDNA3 vector in which the expression is derived from the cytomegalovirus with SV-40 origin of replication.
Transfection
RTASM cells were electroporated with 15 to 25 µg circular plasmid DNA at 220 volts with a capacitance setting of 960 µF using a Gene Pulser (BioRad), according to the manufacturer's protocol. After electroporation, cells were seeded into 60-mm culture dishes containing DMEM with 10% bovine fetal calf serum. The medium was changed after 24 hours of transfection. The efficiency and reproducibility of transfection were examined with the ß-X-gal method according to MacGregor.23 Cells were washed with Ca2+/Mg2+-free PBS and fixed in 1% vol/vol formamide in PBS for 30 minutes, after which cells were rinsed twice with PBS and stained overnight at room temperature in a solution containing 1 x PBS, 0.004 mol/L ferrocyanide, 0.004 mol/L ferricyanide, 0.002 mol/L MgCl2, and 500 µg/mL X-gal. Transfection efficiency was quantitated with microscopic inspection of stained cells.
Hormonal Treatment
All treatments were done in culture medium containing 0.1% BSA without serum with vehicular control as DMSO. After 48 hours of transfection, cells were treated with several concentrations of TPA (a potent PKC activator) and vasoconstrictors ANG II and ET-1. Cells were pretreated with ANP, 8-bromo-cGMP, Npra inhibitor A-71915, which blocks the production of cGMP in response to ANP, KT-5823, a specific inhibitor of cGMP-dependent protein kinase, and staurosporine, which is a potent calcium-dependent PKC inhibitor. All treatments were done for 15 minutes unless otherwise indicated.
Preparation of Whole Cell Extracts
Cells were washed twice with PBS and then with 0.01 mol/L Tris-HCl, pH 7.5. The cells were scraped in buffer A containing Tris-HCl (0.02 mol/L, pH 7.5), EDTA (0.005 mol/L), EGTA (0.01 mol/L), ß-mercaptoethanol (0.05 mol/L), Triton X-100 (0.5%), leupeptin (5 µg/mL), aprotinin (5 µg/mL), and PMSF (50 µg/mL). Cells were homogenized by 50 strokes with a dounce homogenizer and incubated for 30 minutes on ice. The homogenate was centrifuged at 12 000g for 15 minutes. The supernatant was loaded onto a 0.5 mL DEAE-Sephacel column preequilibrated with buffer A. The column was washed with 10 volumes of buffer A containing 0.03 mol/L NaCl. The PKC fractions were eluted with buffer A containing 0.2 mol/L NaCl.
Assay of PKC Activity
PKC activity was determined using the EGF-R peptide VRKRTLRRL, a specific PKC substrate as described previously.24 The reaction mixture contained 20 to 25 µL partially purified column eluate, 8 mole percent L-phosphatidyl-L-serine, 0.0025 mol/L DTT, 0.001 mol/L calcium acetate, 9x10-8 mol/L EGF-R peptide substrate, 0.015 mol/L magnesium acetate, 5x10-7 mol/L ATP, and 1x10-8 mol Ci/[32P]ATP and incubated at 25°C for 15 minutes. The reaction was stopped by adding 100 µL of 30% (vol/vol) acetic acid. An aliquot (125 µL) was removed from the reaction mixture and applied to p81 phosphocellulose paper. After two washes with 5% acetic acid, the papers were dried and bound radioactivity was determined by scintillation counting. The specific activity of PKC is expressed as picomoles 32P transferred per milligram substrate protein per minute. Total protein was estimated with the BioRad protein assay reagent kit, using BSA as a standard.
Western Blotting
For immunological detection of cGMP-dependent protein kinase-1, samples were prepared according Keilback et al.25 Confluent RTASM cells were washed twice with ice-cold PBS and scraped in a buffer containing; 0.0081 mol/L NaHPO4, 0.0018 mol/L KH2 PO4, pH 7.2, 0.137 mol/L NaCl, and 0.0027 mol/L KCl. After centrifugation, cell pellets were suspended in a solution containing 0.02 mol/L K2HPO4, pH 7.0, 0.002 mol/L EDTA, and 0.002 mol/L benzamidine. After freezing and thawing, the cell suspension was homogenized with a Teflon-glass homogenizer and centrifuged at 15 000g for 30 minutes at 4°C. Proteins from the supernatant were electrophoresed on a 7.5% SDS-polyacrylamide gel, according to Laemmli,26 and blotted onto Immobilon P membrane (Millipore) by the method of Towbin et al.27 Nonspecific sites were blocked by overnight incubation of membrane in 5% nonfat dry milk in PBS, pH 7.5, containing 0.1% Tween 20. Membranes were incubated with specific polyclonal antibodies of PKG-1 (1:400 dilution) for 2 to 3 hours and then washed three times (10 minutes each wash) with PBS/ Tween 20. The binding of primary antibody was detected with a horseradish peroxidase conjugated secondary antibody and an enhanced chemiluminescence Western blotting detection system (Amersham).
Antibodies against bovine cGMP-dependent protein kinase were produced as described previously.28 These antibodies at dilutions between 1:50 and 1:1000 reacted with one protein on Western blots and were identified as the cGMP-dependent protein kinase with molecular mass of 70 kD. At lower dilutions, the antiserum was able to react with a 40 kD protein which was identified as the catalytic subunit of the cAMP-dependent protein kinase.
RNA Isolation and Northern Analysis
Total RNA was isolated form RTASM cells by a modification of the guanidinium isothiocyanate method, according to Chomczynski and Sacchi.29 Total RNA (20 µg) from RTASM cells was resolved by a 1% denaturing formaldehyde agarose gel and transferred onto a nylon membrane (Duralon membrane, Stratagene) by a pressure blotter, according to the manufacturer's protocol. The membranes were fixed by UV crosslinking using Stratalinker (Stratagene). Ribosomal RNA on the membrane was stained with methylene blue to detect potential differences in loading and/or transfer efficiencies. Prehybridization and hybridization were done at 42°C in solution containing 50% deionized formamide, 5x SSC, 5x Denhardt's solution, 1% SDS, and 100 µg/mL denatured salmon sperm DNA added only into prehybridization solution. The membrane was hybridized with a 1.2-kb EcoRI restriction fragment of murine Npra cDNA,7 which was labeled with [-32P]dCTP by a random primer oligolabeling kit (Pharmacia). The membrane was washed twice with 2x SSC/ 0.1% SDS at room temperature for 15 minutes and once with 0.01xSSC/0.1% SDS at 65°C for 15 minutes. RNA bands containing Npra mRNA homology were made visible by exposing Kodak X-Omat AR film to the washed membrane at -80°C with intensifying screen.
Assay of Intracellular cGMP
RTASM cells were treated with ANP at 37°C for 10 minutes in the presence of 0.0002 mol/L 3-isobutyl-1-methylxanthine (IBMX). Cells were washed three times with PBS and scraped in 0.005 mol/L HCl and placed in boiling water bath for 3 minutes. After centrifugation at 15 000g for 15 minutes at 4°C, supernatant was collected and lyophilized. Samples were reconstituted with acetate buffer and recentrifuged. cGMP was determined by RIA kit (Biomedical Technologies, Inc), according to the manufacturer's protocol with modification.30
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Data presented in Fig 1 show that treatment of rat vascular smooth muscle cells with TPA resulted in more than 1.6-fold increase in PKC activity compared with vehicle (DMSO)-treated cells. However, if cells were transfected with PKC-
cDNA and treated with TPA, it caused approximately fourfold to five fold induction in PKC activity compared with untransfected or cells transfected with vector alone. The treatment of cells with both ANP and TPA showed an approximately 12% inhibition in TPA-stimulated PKC activity in vector-transfected cells (Fig 2). On the other hand, if cells were transfected with PKC-cDNA, and then treated with ANP and TPA, an approximately 35% inhibition in PKC activity was observed. The TPA concentration of 0.1 mol/L was required to reach an apparent plateau of PKC activation (data not shown). A more detailed time course of the effect of 0.1 mol/L TPA showed that the activation time of PKC required to reach a maximum stimulatory level was 15 minutes, after which PKC activity was downregulated (Fig 3).
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RTASM cells were cotransfected with PKC- and Npra cDNAs to examine the effect of ANP on TPA-stimulated and overexpressed PKC activity in these cells. In the cotransfected RTASM cells, TPA (0.1 mol/L) stimulated the PKC activity by more than fourfold and pretreatment with ANP (0.1 mol/L) inhibited the agonist-stimulated PKC activity by more than 65% (Fig 4). The overexpression of PKC was confirmed by the Western blot analysis using the polyclonal antibodies against PKC- which indicated an approximately 2.5-fold greater PKC immunoreactivity in PKC- cDNA-transfected cells than in nontransfected cells (data not shown). The overexpression of Npra in RTASM cells was examined by quantitating the levels of Npra mRNA in transfected and control cells. Northern blot analysis revealed that Npra mRNA was expressed, approximately at a 2.5-fold to 3-fold higher level in the cDNA-transfected cells than in cells transfected with vector alone (Fig 5). To further confirm the overexpression of Npra in RTASM cells, the intracellular accumulation of cGMP was determined. In Npra-transfected cells, ANP induced approximately 65-fold to 70-fold higher cGMP production than in nontransfected or vector-transfected RTASM cells (Fig 6).
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Vasoconstrictors ANG II and ET-1 also stimulated PKC activity by more than fourfold in PKC--transfected cells compared with the cells transfected with vector alone (Fig 7a and 7b). The maximum stimulatory effects of ANG II and ET-1 were exhibited at 0.1 mol/L peptide concentrations in these cells. Treatment of PKC-- and Npra-co-transfected cells with either ANG II or ET-1 also stimulated approximately 3.5-fold to 4-fold PKC activity; however, the pretreatment of these cells with ANP exhibited a reduction of more than 65% to 70% in ANG II- or ET-1—stimulated PKC activity (Fig 8). Treatment of vector-transfected RTASM cells with ANG II or ET-1 resulted in an approximately 1.5-fold increase in PKC activity, and pretreatment of these cells with ANP attenuated only 18% to 20% PKC enzymatic activity.
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In separate experiments, we further examined whether the inhibitory effect of ANP on PKC activity was mediated through the involvement of second messenger cGMP and cGMP-dependent protein kinase (PKG) in RTASM cells. To test this hypothesis, we utilized Npra antagonist A-71915, which blocked the ANP-dependent intracellular accumulation of cGMP (Fig 6). Furthermore, using polyclonal antibodies, we detected PKG-1 immunoreactivity by Western blot in RTASM cells (Fig 9). The pretreatment of cells with Npra antagonist A-71915 reversed the ANP-dependent inhibition of agonist-stimulated PKC activity (Table). Data presented in the Table further show that TPA-stimulated PKC activity in RTASM cells was also inhibited by 8-bromo-cGMP, which correlated with ANP effects. Similar concentrations of dibutyryl-cAMP were unable to inhibit the PKC activity in these cells. By exposure of both transfected and untransfected cells to KT-5823, an antagonist of cGMP-dependent protein kinase, the inhibitory effect of ANP on agonist-stimulated PKC activity was significantly neutralized (Table). Staurosporine, a PKC antagonist, blocked the agonist-stimulated PKC activity in RTASM cells.
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Discussion |
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The results presented herein demonstrate that ANP exerts an inhibitory effect on both endogenous and overexpressed PKC activity in RTASM cells. ANP inhibited the agonist-stimulated PKC activity in both untransfected and transfected cells in a time- and dose-dependent manner, indicating that RTASM cells are responsive to ANP signal. The inhibitory effect of ANP on PKC activity was further increased if cells were cotransfected with PKC-
and Npra cDNAs, suggesting that ANP effect was exerted in a receptor-mediated manner involving Npra that synthesizes intracellular second messenger cGMP after ANP binding. To demonstrate whether ANP antagonized PKC activity involving Npra and its second messenger cGMP, we utilized Npra antagonist A-71915 and KT-5823, an inhibitor of cGMP-dependent protein kinase (PKG), respectively. Npra antagonist A-71915 blocked the ANP-dependent synthesis of intracellular cGMP in transfected RTASM cells in a manner similar to that shown in other cell systems.31,32 To further investigate whether the inhibitory effect of ANP on PKC activity involved PKG, we utilized KT-5823, a specific inhibitor of this kinase. Our results demonstrated that KT-5823 significantly attenuated the effect of ANP on agonist-stimulated PKC activity in PKC- and Npra transfected cells, providing strong evidence for the involvement of cGMP and cGMP-dependent protein kinase in the signaling mechanism of ANP in vascular smooth muscle cells. The inhibitory effects of ANP on PKC activity correlated with the effects of cells exposed to 8-bromo-cGMP, which also attenuated the enzymatic activity of PKC.
Although ANP stimulates the intracellular accumulation of cGMP in vascular smooth muscle cells, the involvement of specific receptor subtypes in ANP-mediated responses of these cells has not been fully resolved.15 The results obtained in the present study demonstrate that the inhibitory effect of ANP on PKC activity in RTASM cells is mediated through guanylyl cyclase-A receptor and the second messenger cGMP, which is considered an important regulator of vascular smooth muscle cell contraction.33 It has previously been suggested that cGMP interacts with three types of intracellular receptor proteins, which may include cGMP-dependent protein kinase, cGMP-regulated ion channels, and cGMP-activated phosphodiesterases.34 It is possible that cGMP can alter cell function through various mechanisms, including stimulation of protein phosphorylation and/or by an inhibitory effect on this process. Our previous studies as well as data reported from other laboratories have shown that both ANP and cGMP inhibited the autophosphorylation and enzymatic activity of PKC in plasma membrane preparations of various target cells.35–40 Nevertheless, those previous studies on the inhibitory effects of ANP and cGMP, with regard to either autophosphorylation or the enzymatic activity of PKC, did not provide the specificity of PKC isocnzymes and the involvement of specific ANP receptor subtypes. The present results provide direct evidence that ANP exerts an inhibitory effect on the agonist-stimulated enzymatic activity of PKC in RTASM cells, involving the guanylyl cyclase-A receptor and intracellular second messenger cGMP. Although PKG is considered a major receptor for cGMP in vascular smooth muscle cells, its level is markedly decreased with culture conditions of these cells.41 Furthermore, it has been suggested that a crossover in the signaling mechanisms of cAMP and cGMP occurs in vascular smooth muscle cells.42 RTASM cells used in the present study contained a detectable amount of PKG 1, and both ANP and 8-bromo-cGMP inhibited the PKC activity; however, dibutyryl-cAMP did not show any discernible effect. Recently, it has been suggested that cGMP-dependent signaling mechanism of Npra in vascular smooth muscle cells is probably initiated at the level of receptor gene.43 Previous studies have suggested that cultured vascular smooth muscle cells predominantly contain ANP-clearance receptor (90% to 95%) and a very low level of Npra (1% to 5%).11,12,15 Our present results demonstrate that ANP inhibited only 30% to 35% of agonist-stimulated PKC activity in PKC- overexpressing RTASM cells. However, if cells were cotransfected with both Npra and PKC-, the inhibitory effect of ANP was increased by more than 65% to 70%. These observations suggest that by increasing the number of guanylyl cyclase-linked receptors, the threshold effect of ANP can also be increased in vascular smooth muscle cells.
The activation of PKC has been suggested to trigger the agonist-dependent phosphorylation of many cellular proteins, causing alterations in various pathophysiological conditions; including hypertension,44–46 cardiac hypertrophy,47 ischemia,48 and atherosclerosis.49,50 PKC is a multifunctional serine/threonine kinase that is activated by Ca2+/phospholipids and phorbol esters.51,52 On the basis of molecular cloning, PKC is believed to be a multigene family, consisting of at least 12 isoenzymes that can be divided into classical, novel, and atypical forms.53,54 Some of these isoforms (e, 
, 
, and 
) do not require Ca2+, while other isoforms (
and 
) do not require Ca2+ or diacylglycerol for activity. It is possible that seemingly opposite effects might be induced by PKC activation, which is likely due to the differential expression, activation, and translocation of a particular isoform. Agonists that activate PKC also produce two distinct second messengers, IP3, which elevates cytosolic free calcium, and diacylglycerol, which stimulates PKC enzymatic activity.52,55,56 PKC is well recognized to inhibit receptor-mediated phosphoinositol hydrolysis, IP3 formation, and subsequently intracellular calcium mobilization in a number of different cell types.57–59 Our recent studies have suggested that ANP inhibits the formation of IP3 in a cGMP-dependent manner in intact Leydig tumor (MA-10) cells, suggesting that the inhibitory effects of ANP on PKC activity might be linked with its antagonistic action on IP3 formation.60 However, further studies are warranted to support these observations in other ANP-responsive cell systems. A number of vasoactive substances are known to activate phosphatidylinositol hydrolysis through protein-coupled receptors, which result in the formation of IP3 and production of diacylglycerol. The receptor-coupled second messenger system may be critical to downregulation of PKC and to production of more second messenger cGMP in response to ANP action. The inhibitory effects of PKC may also involve the stimulatory effect on protein phosphorylation of key regulatory proteins in ANP/cGMP-dependent pathways, which may attenuate and/or play modulatory roles in ANP-mediated relaxation of vascular smooth muscle cells.
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Acknowledgments |
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This study was supported by grants from the National Institutes of Health (HD 25527) and the American Heart Association Established Investigatorship Award (900260) and grants-in-aid from the National Center (92-1011) and Georgia Affiliate. We thank Kamala Pandey for the help with cell culture. Authors also thank Dr Thomas von Geldern for a gift of A-71915. The expert secretarial assistance of Sarah A. Taylor is sincerely acknowledged in the preparation of this manuscript.
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