Departments of Physiology and Medicine, Medical College of Virginia, Virginia Commonwealth University, Richmond, Virginia 23298-0711
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ABSTRACT |
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Single-transmembrane natriuretic peptide clearance
receptor (NPR-C), which is devoid of a cytoplasmic guanylyl cyclase
domain, interacts with pertussis toxin (PTx)-sensitive G proteins to
activate endothelial nitric oxide synthase (eNOS) expressed in
gastrointestinal smooth muscle cells. We examined the ability of NPR-C
to activate other effector enzymes in eNOS-deficient tenia coli smooth
muscle cells; these cells expressed NPR-C and NPR-B but not NPR-A.
Atrial natriuretic peptide (ANP), the selective NPR-C ligand
cANP-(4-23), and vasoactive intestinal peptide (VIP) inhibited
125I-ANP and 125I-VIP binding to muscle
membranes in a pattern indicating high-affinity binding to NPR-C.
Interaction of VIP with NPR-C was confirmed by its ability to inhibit
125I-ANP binding to membranes of NPR-C-transfected COS-1
cells. In tenia muscle cells, all ligands selectively activated
Gi-1 and Gi-2; VIP also activated
Gs via VIP2 receptors. All ligands stimulated phosphoinositide hydrolysis, which was inhibited by ANP-(1-11), PTx, and antibodies to phospholipase C-3 (PLC-
3) and G
.
cANP-(4-23) contracted tenia muscle cells; contraction was blocked
by U-73122 and PTx and by antibodies to PLC-
3 and G
in intact and
permeabilized muscle cells, respectively. VIP and ANP contracted muscle
cells only after inhibition of cAMP- and cGMP-dependent protein
kinases. ANP and cANP-(4-23) inhibited forskolin-stimulated cAMP
in a PTx-sensitive fashion. We conclude that NPR-C is coupled to
activation of PLC-
3 via
-subunits of Gi-1 and
Gi-2 and to inhibition of adenylyl cyclase via
-subunits.
G protein; smooth muscle; vasoactive intestinal peptide; signal transduction; phosphoinositide metabolism; phospholipase C
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INTRODUCTION |
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THREE MAMMALIAN single-transmembrane natriuretic peptide receptors (NPR-A, NPR-B, and NPR-C) have been identified (5, 8, 14). NPR-A and NPR-B are receptor guanylyl cyclases, with intracellular kinase and guanylyl cyclase domains corresponding to guanylyl cyclase-A (NPR-A) and guanylyl cyclase-B (NPR-B) (8, 11). The intracellular domain of NPR-C is devoid of kinase and guanylyl cyclase activities and consists of a 37-amino acid sequence, recently shown to bind and activate pertussis toxin (PTx)-sensitive, guanine nucleotide-binding proteins (G proteins) (4, 23). NPR-D, a recently cloned natriuretic peptide receptor, is a species homologue of NPR-C expressed in the tissues of the eel (13).
The high affinity of all natriuretic peptides for NPR-C and the ability
of NPR-C to recycle rapidly in the presence or absence of natriuretic
peptides suggests that it might act as a clearance receptor to
internalize and degrade circulating natriuretic peptides (15, 24, 29).
Its ability to couple to PTx-sensitive G proteins implies that it can
also act to transduce external signals. Consistent with this notion,
atrial natriuretic peptide (ANP) and the selective NPR-C agonist
[des(Gln18,Ser19,Gln20,Leu21,Gly22)ANP-(4-23)-NH2;
cANP-(4-23)] inhibited adenylyl cyclase activity in
platelets that express only NPR-C and in membranes from vascular and
cardiac muscle, the anterior pituitary, the adrenal cortex, and the
brain (2, 3). A synthetic peptide consisting of the 37-amino acid
intracellular sequence of NPR-C inhibited adenylyl cyclase activity in
cardiac muscle membranes (4). cANP-(4-23) and/or ANP also
stimulated phosphoinositide (PI) hydrolysis in aortic smooth muscle
membranes (10) and isolated parotid acinar cells (6), suggesting G
protein-dependent activation of other effector enzymes [e.g.,
phospholipase C- (PLC-
)]. Our recent studies (23, 30)
showed that both ANP and cANP-(4-23) activate nitric oxide
synthase (NOS) and stimulate nitric oxide (NO) formation in gastric
smooth muscle cells that express endothelial NOS (eNOS). The signaling
cascade involves G protein-dependent stimulation of Ca2+
influx and activation of eNOS bound to calmodulin in the plasma membrane; in turn, NO activates soluble guanylyl cyclase, resulting in
formation of cGMP and activation of cGMP-dependent protein kinase. The
homologous neuropeptides vasoactive intestinal peptide (VIP) and
pituitary adenylate cyclase-activating peptide (PACAP) bind with high
affinity to NPR-C and initiate an identical signaling cascade. The two
neuropeptides interact also with their cognate VIP2/PACAP3 receptors (current nomenclature,
VPAC2 receptors) coupled via Gs to adenylyl
cyclase (23, 31).
The signaling cascade initiated by interaction of ANP,
cANP-(4-23), VIP, and PACAP with NPR-C is mediated by
Gi-1 and Gi-2 (23). We postulate that the same
G proteins mediate activation of other effector enzymes. In this study,
we have used freshly dispersed and cultured tenia coli smooth muscle
cells that do not express eNOS (30) to examine the ability of NPR-C to
activate other effector enzymes via Gi-1 and
Gi-2. Our results show that ANP and cANP-(4-23)
activated PLC-3 via the
-subunits of Gi-1 and
Gi-2, inducing PI hydrolysis and muscle contraction, and
inhibited adenylyl cyclase activity. VIP also activated PLC-
3 via
the
-subunits of Gi-1 and Gi-2.
Inhibition of adenylyl cyclase was masked by a predominant activation
via Gs mediated by VIP2 receptors.
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MATERIALS AND METHODS |
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Preparation of dispersed and cultured muscle cells. Muscle cells were isolated from guinea pig tenia coli by sequential enzymatic digestion, filtration, and centrifugation as described previously (23, 30). In experiments with blocking antibodies, the cells were permeabilized with saponin (35 µg/ml) in a medium containing 0.34 mM CaCl2 and 1 mM EGTA and resuspended in 1.5 mM ATP and ATP-regenerating system (5 mM creatine phosphate and 10 U/ml creatine phosphokinase). The cells were cultured as described previously (7, 30) in DMEM containing 10% FCS. All experiments were done on cells in first passage.
Expression of natriuretic peptide receptors in smooth muscle cells. Expression of natriuretic peptide receptors (NPR-A, NPR-B, and NPR-C) was determined by RT-PCR and Northern blot analysis as described previously (23, 30, 31). Six micrograms of total RNA were reverse transcribed. The specific primers and conditions for RT-PCR were those used in studies (23) with cultured rabbit gastric smooth muscle cells. Cloned full-length cDNAs for rat NPR-A, NPR-B, and NPR-C were used as positive controls.
For Northern blot analysis, 20 µg of total RNA were fractionated by electrophoresis in 1.1% formaldehyde agarose gel. cDNA inserts for NPR-A and NPR-B using full-length rat cDNA and for NPR-C using the cloned 541-bp RT-PCR product were labeled with 32P using random hexamers as a probe. Hybridization was carried out under standard conditions, and autoradiography was performed atTransfection of NPR-C into COS-1 cells.
The rat NPR-C cDNA was cloned into the mammalian expression vector
pCDL-SR. The plasmid DNA was purified using a Qiagen Midi kit. COS-1
cells were cultured in 90% DMEM supplemented with 10% fetal bovine
serum at 37°C as previously described (23). Transfection of
recombinant plasmid DNA was performed using Lipofectamine Plus reagent.
COS-1 cells were cotransfected with 6 µg of pCDL-SR
-rat NPR-C DNA
and 6 µg of pGreen Lantern-1 DNA for 72 h. Control cells were
transfected with 6 µg of pCDL-SR
DNA and 6 µg of pGreen Lantern-1 DNA. Transfection efficiency was monitored microscopically by
the expression of the green fluorescent protein using FITC filters.
Radioligand binding. Homogenates of cultured tenia coli muscle cells or NPR-C transfected COS-1 cells were centrifuged at 500 g for 5 min at 4°C. The supernatant was centrifuged at 30,000 g for 1 h at 4°C, and the pellet was suspended at a concentration of 3 mg protein/ml in 50 mM Tris · HCl medium containing 5 mM MgCl2, 0.5% BSA, 0.5% bacitracin, and 10 mg/ml aprotinin. Membranes (30 µg protein/sample) were incubated with 50 pM 125I-labeled ANP or 125I-VIP at 25°C for 15 min in the presence or absence of unlabeled ANP, cANP-(4-23), or VIP. The samples were centrifuged at 12,000 g for 4 min, and the pellet was washed with PBS. Nonspecific binding to membranes of muscle cells was ~30% of total binding.
Identification of receptor-activated G proteins.
G proteins selectively activated by ANP, cANP-(4-23), and VIP were
identified by an adaptation of the method of Okamoto et al. (25), as
described previously (23). Muscle cells were homogenized in 20 mM HEPES
medium, centrifuged at 25,000 g for 15 min, and solubilized in
1%
3-[(3-cholamidopropyl)dimethylammonio]-1-propanesulfonate at 4°C. The solubilized membranes were incubated for 20 min at 37°C with 60 nM 35S-labeled guanosine
5'-O-(-thio)triphosphate
([35S]GTP
S) in 10 mM HEPES medium containing
100 µM EDTA and 10 mM MgCl2 in the presence or absence of
various agonists. After the reaction was stopped, the membranes were
incubated for 2 h on ice in wells precoated with specific antibodies to
G
i-1, G
i-2, G
i-3,
Gs
, and G
q/11. The wells were washed with
phosphate buffer containing 0.05% Tween 20, and the radioactivity from
each well was counted.
Assay of PLC- activity.
PLC-
activity was determined by a modification of the method of
Uhing et al. (32) in plasma membranes of muscle cells prelabeled with
myo-[3H]inositol, as described
previously (17, 20). The assay was initiated by addition of 0.1 mg of
membrane protein to 25 mM Tris · HCl medium
containing 0.5 mM EGTA, 10 mM MgCl2, 300 nM free Ca2+, 1 µM GTP
S, 5 mM phosphocreatine, and 50 U/ml
creatine phosphokinase in a total volume of 0.4 ml. After incubation at
31°C for 60 s, the supernatant was extracted with diethyl ether and
the amount of labeled inositol phosphates in the aqueous phase was
counted. PLC-
activity was expressed as counts per minute per
milligram of protein per minute.
Assay for cAMP and cGMP in dispersed muscle cells. cAMP and cGMP were measured in freshly dispersed muscle cells as described previously (23). Aliquots (0.5 ml) containing 106 cells/ml were incubated for 60 s with forskolin (10 µM) in the presence of 200 µM IBMX followed by addition of 1 µM ANP or 1 µM cANP-(4-23) for 60 s. cAMP and cGMP were measured in duplicate by RIA using 100-µl aliquots of reconstituted samples, and the results were expressed as picomoles per 106 cells.
Measurement of contraction in dispersed muscle cells.
Contraction was measured in intact and permeabilized muscle cells by
scanning micrometry as described previously (16, 20). The effects of
specific antibodies for PLC- and G protein subunits were determined
in saponin-permeabilized muscle cells after preincubation for 1 h with
10 µg/ml of each antibody (16, 20). Under each condition, the lengths
of muscle cells treated with agonists were measured and compared with
the lengths of untreated cells. Contraction was expressed in
micrometers as the mean decrease in cell length from control.
Materials.
ANP, cANP-(4-23), and VIP were obtained from Bachem (Torrance,
CA).
(8R,9S,11S)-()-9-methoxy-carbamyl-8-methyl-2,3,9,10-tetrahydro-8,11-epoxy-1H,8H,11H-2,7b,11a-trizadibenzo (a,g)cycloocta(c,d,e)-trinden-1-one
(KT-5823) was from Kamiya Biomedical (Thousand Oaks, CA).
N-2[(p-bromocinnamylamino)ethyl]-5-isoquinolinesulfonamide hydrochloride (H-89) and PTx were obtained from Calbiochem (San Diego,
CA). 125I-ANP, 125I-VIP, 125I-cAMP,
125I-cGMP, [35S]GTP
S, and
myo-[3H]inositol were from New England
Nuclear (Boston, MA), and polyclonal antibodies to G
subunits, a
common G
subunit, and various PLC-
isoforms were from Santa Cruz
Biotechnology (Santa Cruz, CA). pGreen Lantern-1 and Lipofectamine Plus
reagent were obtained from Life Technologies GIBCO BRL (Rockville, MD).
NPR-A and NPR-B cDNA were gifts from Dr. David L. Garbers, University
of Texas Southwestern Medical Center. NPR-C cDNA was a gift from Dr.
David G. Lowe, Genentech.
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RESULTS |
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Selective expression of NPR-C and NPR-B in tenia coli smooth muscle
cells.
RT-PCR on RNA extracted from cultured tenia coli muscle cells yielded
PCR products of the expected size with specific primers for NPR-B and
NPR-C but not NPR-A (Fig. 1). Northern blot
analysis detected a single mRNA transcript for NPR-B (3.5 kb) and a
main transcript for NPR-C (7.5 kb) with some of smaller size (<3.5 kb) but none for NPR-A (Fig. 1). The absence of NPR-A expression was
confirmed using primers based on the human NPR-A sequence (data not
shown). A similar pattern of selective expression of NPR-B and NPR-C
was previously obtained in rabbit gastric muscle cells (23). The size
of the NPR-C transcripts was similar to that reported in other tissues
(9, 27, 28).
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Binding of 125I-ANP and 125I-VIP to muscle
membranes.
125I-ANP binding to tenia coli muscle membranes was
completely inhibited by ANP (dissociation constant 0.26 ± 0.03 nM;
density of binding sites 9.3 ± 0.2 fmol/mg protein) but only partly
inhibited by VIP (58 ± 4% at 10 µM) and the selective NPR-C ligand
cANP-(4-23) (66 ± 2% at 10 µM) (Fig.
2). The results implied that
VIP and cANP-(4-23) recognized a set of binding sites labeled by
125I-ANP. Competition binding with 125I-VIP as
radioligand was examined at 1 nM and 10 µM. 125I-VIP
binding was completely inhibited by 10 µM VIP but only partly inhibited by 10 µM ANP (58 ± 6%) and cANP-(4-23) (65 ± 3%)
(Fig. 3). The results implied that ANP and
cANP-(4-23) recognized a set of binding sites labeled by
125I-VIP. These binding sites were analyzed further by
eliminating the component of VIP binding to VIP2 receptors.
VIP2 receptors were desensitized by treating cultured
muscle cells for 30 min with 1 µM VIP: 125I-VIP binding
to membranes derived from these cells decreased by 57 ± 2%, and
residual binding was abolished by 10 µM ANP, cANP-(4-23), and
VIP. The pattern of binding was similar to that observed in rabbit
gastric muscle cells (23) and implied that ANP and VIP bound to a
receptor, i.e., NPR-C, that is selectively recognized by
cANP-(4-23).
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Identification of G proteins and PLC- isoform
activated by natriuretic peptides and VIP.
Both ANP and cANP-(4-23) selectively activated Gi-1
and Gi-2, causing a significant increase in the binding of
[35S]GTP
S to G
i-1 and
G
i-2 but not to Gs
, G
i-3,
and G
q/11 (Table 1). VIP
also caused a significant increase in the binding of [35S]GTP
S to G
i-1 and
G
i-2, as well as to G
s (Table
1).
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Inhibition of adenylyl cyclase by natriuretic peptides.
ANP and cANP-(4-23) inhibited forskolin-stimulated cAMP formation
(33.3 ± 4.9 pmol/106 cells) by 62 ± 4% and 64 ± 7%,
respectively, in freshly dispersed tenia coli muscle cells (Fig.
6). The inhibition was reversed by
pretreatment of the cells for 1 h with 400 ng/ml of PTx. The inhibition
was consistent with activation of Gi-1 and Gi-2
by ANP and cANP-(4-23).
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Stimulation of muscle cell contraction by NPR-C agonists.
Activation of PLC-3 by cANP-(4-23) in tenia coli muscle cells
suggested that this ligand could act as a contractile agonist by
stimulating inositol 1,4,5-trisphosphate-dependent Ca2+
release from sarcoplasmic stores. Consistent with this notion, cANP-(4-23) caused a concentration-dependent contraction of
freshly dispersed tenia coli muscle cells (EC50 7.5 ± 3.4 nM) that was inhibited by U-73122 (86 ± 4%) and by 1-h treatment
with 400 ng/ml of PTx (93 ± 5%) (Table
2). Contraction was not affected by 10-min treatment with nifedipine (1 µM).
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DISCUSSION |
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This study shows that ANP, cANP-(4-23), and VIP bind with high
affinity to NPR-C expressed in tenia coli smooth muscle cells and
stimulate PI hydrolysis by activating PLC-3 via the
-subunits of Gi-1 and Gi-2. ANP and cANP-(4-23) also
inhibit adenylyl cyclase, presumably via the
-subunit of both G
proteins. The results identify Gi-1 and Gi-2 as
the G proteins mediating PTx-sensitive inhibition of adenylyl cyclase
and stimulation of PI hydrolysis reported in previous studies
(2-4, 10). Inhibition of adenylyl cyclase by VIP is probably
masked by concurrent activation of adenylyl cyclase via the
VIP2 receptor recently shown to be expressed in these
muscle cells (12, 31). We base these conclusions on the following findings.
RT-PCR and Northern blot analysis demonstrated expression of NPR-C and NPR-B but not NPR-A, a pattern identical to that in gastric muscle cells (23). The absence of NPR-A was confirmed by primers derived from rat and human NPR-C.
125I-ANP binding was partially inhibited by the selective NPR-C ligand cANP-(4-23) and VIP, and this reflected the component of 125I-ANP binding to NPR-C. 125I-VIP binding was partially inhibited by ANP and cANP-(4-23), and this reflected the component of 125I-VIP binding to NPR-C. The pattern of binding to tenia coli muscle cells was similar to that observed in gastric muscle cells (23). In both muscle cell types, VIP bound to cognate VIP2 receptors and to NPR-C, whereas ANP bound to NPR-C and NPR-B, the only other natriuretic peptide receptor expressed in these cells. cANP-(4-23) bound exclusively to NPR-C. A previous study by Akiho et al. (1) in guinea pig cecal muscle cells showed that VIP partially inhibited ANP binding and ANP partially inhibited VIP binding, but that group did not identify NPR-C as the receptor recognized by VIP.
The ability of VIP to interact with NPR-C was demonstrated conclusively in COS-1 cells transfected with NPR-C. In these cells, both cANP-(4-23) and VIP inhibited 125I-ANP binding in a concentration-dependent fashion, providing direct evidence for interaction of VIP with NPR-C. This was further corroborated by recent functional studies (23) showing that COS-1 cells transfected with NPR-C could be activated by ANP and cANP-(4-23), as well as by VIP.
All three ligands selectively activated both Gi-1 and Gi-2 in tenia coli muscle cells. In addition, VIP activated Gs.
PI hydrolysis was stimulated by all three ligands and inhibited by the
NPR antagonist ANP-(1-11) (1, 4), implying interaction of all
three ligands with NPR-C. PI hydrolysis was also inhibited by PTx and
by antibodies to PLC-3 and G
, consistent with activation of
PLC-
3 by the
-subunits of Gi-1 and
Gi-2. The results conformed to a pattern previously
established for selective activation of PLC-
3 by the
-subunits
of inhibitory G proteins in gastric and intestinal muscle cells. The
specific G protein involved depended on the receptor (16, 19-21,
23).
Both ANP and cANP-(4-23) inhibited forskolin-stimulated cAMP. The inhibition was completely reversed by PTx.
cANP-(4-23) contracted dispersed tenia coli muscle cells, and the
contraction was abolished by the PLC- inhibitor U-73122 and PTx.
Contraction was also inhibited by antibodies to PLC-
3 and G
. The
effectiveness of G
and PLC-
3 antibodies in inhibiting contraction
paralleled their ability to block PI hydrolysis.
VIP and ANP stimulated PI hydrolysis but only caused contraction in the
presence of cAMP-dependent kinase and cGMP-dependent kinase inhibitors.
The contraction was inhibited by U-73122, PTx, and antibodies to
PLC-3 and G
.
The results obtained in tenia coli muscle cells suggested that the
inhibition of adenylyl cyclase or activation of PLC- by ANP or
cANP-(4-23) observed in other cell types (2-4, 10) may have
been mediated by the
-subunits (inhibition of adenylyl cyclase) and
-subunits (activation of PLC-
) of Gi-1 and
Gi-2. Natriuretic peptides possess high affinity for their
specific receptors, (i.e., the receptor guanylyl cyclases NPR-A and
NPR-B), as well as for NPR-C. There is no evidence that either NPR-A or
NPR-B is coupled to G proteins, whereas NPR-C, which is devoid of an
intracellular guanylyl cyclase domain, is coupled to inhibitory G
proteins, identified in this and a previous study (23) on gastric
muscle as Gi-1 and Gi-2. G protein
coupling is mediated by the 37-amino acid cytoplasmic domain of NPR-C.
A synthetic peptide corresponding to this domain inhibited adenylyl
cyclase activity in cardiac muscle membranes; the inhibition was
reversed by PTx and by antibodies to the peptide (4). In recent studies
(22), we have identified a fragment in the middle region of the
cytoplasmic domain of NPR-C that selectively activated Gi-1
and Gi-2 and stimulated PI hydrolysis. A sequence with
similar motif capable of binding to various G proteins has been
identified in the cytoplasmic domain of the single-transmembrane
receptor (insulin-like growth factor-II/mannose 6-phosphate receptor)
(26).
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ACKNOWLEDGEMENTS |
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This work was supported by National Institute of Diabetes and Digestive and Kidney Diseases Grants DK-15564 and DK-28300.
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FOOTNOTES |
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The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Address for reprint requests and other correspondence: G. M. Makhlouf, PO Box 980711, Medical College of Virginia, Virginia Commonwealth Univ., Richmond, VA 23298-0711.
Received 17 September 1999; accepted in final form 4 January 2000.
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