(Hypertension. 1999;33:124-129.)
© 1999 American Heart Association, Inc.
Scientific Contributions |
C-Type Natriuretic Peptide Attenuates Evoked Dopamine Efflux by Influencing Go
From the Department of Pharmacology, University of Minnesota-Duluth, School of Medicine, Duluth, Minn.
Correspondence to Dr George J. Trachte, Department of Pharmacology, University of Minnesota-Duluth, School of Medicine, 10 University Dr, Duluth, MN 55812. E-mail gtracht1{at}d.umn.edu
 |
Abstract |
|---|
 Top Abstract IntroductionMethodsResultsDiscussionReferences |
|---|
Abstract—Natriuretic peptides suppress adrenergic neurotransmission by a mechanism sensitive to pertussis toxin, suggesting that GTP-binding proteins are involved in the response. The major GTP-binding proteins present in the pheochromocytoma (PC12) cells used in this report are Go
and Gi2. We tested the hypothesis that the
more abundant GTP-binding protein, Go, mediates
natriuretic peptide effects in PC12 cells by selectively
ablating Go from the cells with antisense
oligodeoxynucleotides. The results indicate that a
selective ablation of Go with this technique eliminated
C-type natriuretic peptide (CNP) effects and suppressed
dopamine efflux evoked by a depolarizing stimulus. However, the
activation of guanylyl cyclase (GC) by CNP was sustained after the
Go ablation. Further,
N
-nitro-L-arginine methyl
ester suppressed evoked dopamine efflux equally in the presence and
absence of Go. These results suggest that CNP attenuates
evoked catecholamine efflux from PC12 cells by a mechanism
requiring Go but independent of GC activation.
Key Words: neurotransmission • GTP-binding proteins • oligodeoxynucleotides, antisense • pheochromocytoma cells • guanylyl cyclase
|
Introduction |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Atrial natriuretic peptide (ANP) was identified as a hypotensive and natriuretic entity secreted by atria.1 The active peptide was found to contain 28 amino acids, with a cyclic ring consisting of 17 amino acids.2 Subsequently, 2 other natriuretic peptides were discovered and were named brain natriuretic peptide3 and C-type natriuretic peptide (CNP).4 These natriuretic peptides were found to interact with 2 specific classes of membrane receptors, including membrane forms of guanylyl cyclase (GC) and a truncated receptor termed the natriuretic peptide C receptor (NPR-C). The GC natriuretic peptide receptors are designated GC-A and GC-B and contain an extracellular high-affinity binding site for ANP and CNP, respectively, a single transmembrane region, an intracellular protein kinase homology domain, and a cyclase catalytic domain.5 6 Ligand binding to these receptors results in the elevation of intracellular cGMP concentrations that are generally thought to mediate various direct hypotensive actions of the natriuretic peptides. The NPR-C is a lower molecular weight receptor. It binds all natriuretic peptides and contains a single transmembrane-spanning domain and a short cytoplasmic tail of 37 amino acids that is devoid of GC activity.7 The NPR-C has been purported to act solely as a hormonal buffer system mediating the metabolic clearance of natriuretic peptides from the circulation.8 Thus, of the 3 identified receptors for natriuretic peptide, 2 receptors mediate an increase in GC activity in response to natriuretic peptides whereas the third receptor is perceived to facilitate the entry of natriuretic peptides into the cytoplasm of cells but not to participate in mediating biological responses.
This simplified scenario attributing all biological effects to GC
activation has been challenged by studies performed in the last decade.
In vivo, no change in renal metabolic clearance rate occurs
with administration of cANP, a specific ligand of the NPR-C, after a
CNP infusion.9 These results imply that the NPR-C
in canine kidney does not clear all natriuretic peptides.
Further, overwhelming evidence in vitro suggests that the NPR-C
functions as a signal-transducing entity.10 11 12
In particular, pretreatment of cells with pertussis toxin abolishes
NPR-C–activated inhibition of both adenylyl
cyclase13 and catecholamine
efflux14 15 and stimulation of neutrophil
migration,16 suggesting the involvement of a
pertussis toxin–sensitive GTP-binding protein such as
Gi or Go. The current
study defines the GTP-binding protein involvement in the
neuromodulatory effects of CNP with antisense
oligodeoxynucleotides to ablate Go
selectively. The oligodeoxynucleotide used to accomplish
the Go ablation was selected to eliminate both
forms of Go but to leave
Gi unaffected.17
Antisense oligodeoxynucleotide
approaches18 involve delivery of a short
oligodeoxynucleotide with a sequence complementary to
specific mRNA. It selectively binds to target sequences and interferes
with the expression of a specific protein. The significant specificity
derives from the ability of the oligodeoxynucleotide to
hybridize, by very specific Watson-Crick base pairing, to its
corresponding mRNA codon. The properties of the targeted protein can be
deduced from the resulting change of function in the cell. Thus, we
examined natriuretic peptide effects on evoked dopamine
efflux and GC activity to assess the relevance of
Go in these actions.
|
Methods |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Cell Culture
Pheochromocytoma (PC12) cells were grown in DMEM supplemented with 10% FCS and 5% heat-inactivated horse serum. They were plated at a density of 1 million cells per 25-mL flask, coated with rat-tail collagen, and incubated at 37°C in a 95% air-5% CO2 humidified atmosphere. Differentiation of the cells was induced by addition of 1x10-4 g/L 7S nerve growth factor 24 hours after plating in the presence of DMEM supplemented with 10 g/L (1%) FCS. The cells were used for experiments after 8 to 10 days of differentiation.
Materials
Human/rat CNP was purchased from Peninsula Laboratories. Nerve
growth factor, isobutylmethylxanthine,
N-nitro-L-arginine
methyl ester (L-NAME), dihydroxybenzylamine, and dopamine were
purchased from Sigma Chem Co. Reduced serum media (Opti-MEM) were
purchased from Life Technologies. Anti-Go
polyclonal antibody and antitubulin monoclonal antibody were generous
gifts from Dr Timothy Walseth (University of Minnesota, Minneapolis,
MN) and Dr Jon Holy (University of Minnesota-Duluth, Duluth, MN),
respectively. The
anti-Gi1 and
anti-Gi2 antibodies were
purchased from Neomarkers Inc.
Antisense Oligodeoxynucleotides
Antisense (CGCCTTGCYCCGCTCGAG) and missense (CTCCTGGCYACGCCCGTG)
oligodeoxynucleotides were purchased from Oligos Etc Inc.
The detailed properties of these oligodeoxynucleotides were
not disclosed by the manufacturer because of patent pending. The
antisense oligodeoxynucleotide sequence was shown
previously to suppress Go
expression17 after microinjection into
cells.
Oligodeoxynucleotides Transfection/Delivery
GS3815 (Glen Research) was prepared according to the
manufacturer's protocol. Oligodeoxynucleotides were
dissolved in 1/20 vol of Opti-MEM, and GS cytofectin was mixed into
another 1/20 vol of serum-free media. Both solutions were combined to
form the oligocytofectin complex and incubated for 10 minutes. The
remaining 9/10 vol of Opti-MEM containing 10 g/L (1%) FCS was added.
The cells were exposed to the oligocytofectin complex for 12 hours. The
final concentrations of oligodeoxynucleotide and GS
cytofectin were 5x10-8 mol/L and
2.5x10-3 g/L, respectively. The cells were used
in experiments 48 hours later.
SDS-PAGE/Western Blotting
The cells were digested with solubilizing buffer consisting of
the following: 10 g/L (1%) Triton X-100; 5 g/L (0.5%) deoxycholic
acid; 1 g/L (0.1%) sodium dodecyl sulfate;
1.5x10-1 mol/L sodium chloride;
5x10-2 mol/L Tris; and 1 mmol/L EDTA.
Additionally, this buffer contained the following protease
inhibitors: leupeptin, 2x10-3 g/L;
antipain, 4x10-3 g/L; benzamidine,
2x10-2 g/L; and aprotinin, 18 trypsin
inhibitory units per liter. The cell proteins resulting
from this solubilization were separated from cellular debris by
centrifugation (15 000g for 15 minutes at
4°C) and assayed by the Biorad DC protein assay. Aliquots were taken
to equal protein contents among the different treatments, and the
proteins were boiled in 20 g/L (2%) sodium dodecyl sulfate and
resolved by 120 g/L (12%) polyacrylamide gel electrophoresis.
They were transferred from the gel to a nitrocellulose membrane. After
incubation in blocking buffer (30 g/L (3%) nonfat dry milk for 2
hours), the nitrocellulose membrane was bisected at an approximate
molecular weight of 46 kDa, and the lower molecular weight portion was
probed with antibodies for GTP-binding proteins whereas the higher
molecular weight portion was probed with antibodies to ß-tubulin.
Bound antibodies were detected with enhanced chemiluminescence (ECL)
(Amersham). Primary antibodies consisted of the following with the
dilution indicated: anti-Go polyclonal
antibody, 1:10 000;
anti-Gi1 monoclonal
antibody, 1:100;
anti-Gi2 antibody, 1:75;
and anti–ß-tubulin monoclonal antibody, 1:15 000. The secondary
antibodies were either horseradish peroxidase–conjugated anti-rabbit
or anti-mouse immunoglobulin G. Secondary antibodies were purchased
from Jackson Immunoresearch Laboratory.
Catecholamine Release and Measurement
Catecholamine efflux from cells was induced by
depolarization with Krebs buffer as previously
described.14 15 Cells were incubated with either
CNP (10-11, 10-10,
10-9, or 10-8 mol/L) or
L-NAME (2x10-8 or
2x10-7 mol/L) in the depolarizing buffer for 5
minutes. At that point, the medium and cells were assayed for dopamine
contents. Results are expressed as percent of control release.
cGMP Assay
The concentrations of cGMP were measured in experiments
identical to those described for catecholamine release,
except that 2.5 mmol/L of
isobutylmethylxanthine was added to inhibit
phosphodiesterase and the reaction was stopped with 1 mL of ethanol.
Precipitated proteins were separated from soluble extracts by
centrifugation at 10 000 gravitation equivalents for
10 minutes. The ethanol was decanted into polypropylene tubes and
evaporated in a Sybron/Brinkman SC240 sample concentrator. The samples
were reconstituted in assay buffer and assayed by use of Amersham cGMP
assay kits (TRK 500). Results are expressed as percent increase in cGMP
concentrations compared with control levels. Changes in cGMP
concentrations are interpreted as a modification of GC activities
because cGMP degradation was considered to be eliminated by the
isobutylmethylxanthine.
Statistics
The CNP or L-NAME effect on potassium chloride–induced
catecholamine release and cGMP generation was assessed by
2-way ANOVA. Individual values were compared by Student's t
test with Dunnett's correction for multiple comparisons.
|
Results |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Figure 1
shows the effect of
treatment with Go antisense and missense
oligodeoxynucleotides on cell contents of
Go and ß-tubulin. Control cells also were
included to assess nonspecific effects of
oligodeoxynucleotide administration. The
Go migrated at an approximate molecular weight
of 40 kDa, and the ß-tubulin migration was consistent with a
molecular weight of 56 kDa. The ß-tubulin was probed to assess
whether protein contents were equal in the various lanes. As seen in
Figure 1, these levels were fairly consistent, with the control
lane having somewhat more protein than the lanes loaded with proteins
from cells treated with oligodeoxynucleotides. The cells
exposed to the antisense oligodeoxynucleotide
(5x10-8 mol/L) had no detectable
Go, whereas those exposed to the missense
oligodeoxynucleotide exhibited Go
immunoreactivity. The control cells were not treated with
oligodeoxynucleotides and they possessed both more protein,
as indicated by ß-tubulin immunoreactivity, and more
Go protein. These results are
consistent with an effective and specific ablation of the
Go with the antisense protocol used. The
antisense oligodeoxynucleotide for
Go was specific and did not influence
Gi1 or
Gi2 (data not
shown).
|
The antisense oligodeoxynucleotide treatment
(5x10-8 mol/L) tended to reduce the efflux of
dopamine from PC12 cells stimulated with 40 mmol/L potassium
chloride. This effect was statistically significant when the data from
all cells treated in this manner were pooled (N=10; P=0.03).
Efflux of dopamine in response to a depolarizing stimulus averaged
22.6±3.4% in cells treated with the missense
oligodeoxynucleotide and 17.6±2.6% in cells treated with
the antisense oligodeoxynucleotide (data not shown). These
results indicate a tendency for Go ablation to
reduce evoked release of catecholamines.
The inhibitory effect of CNP was intact in cells receiving
the missense oligodeoxynucleotide, as seen in Figure 2. CNP maximally suppressed evoked
dopamine efflux 49±12% at a concentration of
10-8 mol/L. The concentration producing a
half-maximal effect averaged
1x10-10±0.7x10-10
mol/L. In stark contrast, cells treated with the antisense
oligodeoxynucleotide failed to respond to CNP with a
reduction in evoked dopamine efflux. The response to CNP was converted
to a potentiation of evoked dopamine efflux in the cells treated with
the antisense oligodeoxynucleotide, although none of the
potentiative responses differed significantly from the control release
(P=0.24 at 10-9 and
10-8 mol/L). The curves were statistically
different when compared by ANOVA (P=0.006), as were the
slopes of the curves (P=0.03). These data indicate that
Go is essential for the inhibitory
neuromodulatory response to CNP. The dopamine contents of the cells
varied from 9 to 17 ng per culture, with no alteration in dopamine
contents in cells exposed to the Go antisense
oligodeoxynucleotide relative to those exposed to the
missense oligodeoxynucleotide (data not shown).
|
The GC activation occurring in response to natriuretic
peptides is considered both to mediate biological responses to
natriuretic peptides and to be independent of GTP-binding
proteins. Therefore, we used this response to test for nonspecific
effects of GTP-binding protein ablation. As seen in Figure 3, CNP stimulated cGMP accumulation in
cells treated with either the missense or antisense
oligodeoxynucleotide. Significant increases in cGMP
accumulation were not observed at CNP concentrations
<10-7 mol/L in either group. The 2 curves were
not statistically different by ANOVA (P=0.19). A
concentration-dependent effect of CNP was observed
(P=0.0005), with the slopes of the 2 curves being similar
(P=0.14). These results indicate that the GC response to CNP
was intact after Go ablation, as would be
expected. Basal cGMP concentrations in the cultures were
7.7±1.7x10-12 moles per flask in cells treated
with the missense oligodeoxynucleotide and
10.6±2.7x10-12 moles per flask in
antisense-treated cells (data not shown). These values did not differ
significantly.
|
The neuromodulatory effect of L-NAME, an agent acting independently of
GTP-binding proteins, also was examined to ascertain nonspecific
effects of the Go knockdown. As seen in Figure 4, L-NAME was equally effective at
reducing evoked dopamine efflux whether the cells had been treated with
missense or antisense oligodeoxynucleotides. L-NAME
suppressed evoked dopamine efflux to 80±10% and 81±8% of control in
cells treated with the antisense or missense
oligodeoxynucleotide, respectively. These responses
represented concentration-dependent reductions in dopamine
efflux in response to L-NAME (P=0.002), but the responses
between groups did not significantly differ when compared by ANOVA
(P=0.71). Further, both lines had similar slopes
(P=0.84). Collectively, these results indicate that although
the antisense treatment used suppresses neurotransmission, it does not
prevent the activity of all neuromodulators.
|
|
Discussion |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
The present study for the first time determines that the Go
subtype of GTP-binding protein mediates the
signal-transduction pathway initiated by CNP to suppress
neurotransmitter efflux. The neuromodulatory effect of CNP was ablated
specifically by reducing the Go protein by use
of the antisense technique (Figure 2
). In contrast, the neuromodulatory
effect of L-NAME was sustained in the absence of the
Go protein (Figure 4), as was CNP activation
of GC (Figure 3). These data suggest that natriuretic
peptides act via a cGMP-independent mechanism to affect
neurotransmission. This mechanism has been attributed to activation of
the NPR-C19 with coupling to a pertussis
toxin–sensitive GTP-binding protein.20 These
novel data indicate that the GTP-binding protein appears to be
Go. A number of studies have linked the NPR-C with a pertussis toxin–sensitive mechanism presumably involving inhibitory GTP-binding proteins. Specific ligands for the NPR-C suppress adenylyl cyclase activity21 and reduce adrenergic neurotransmitter release20 by pertussis toxin–sensitive mechanisms. More recently, another NPR-C selective natriuretic peptide analog was found to inhibit mitogen-activated protein kinase induced by endothelin-3, platelet-derived growth factor, or phorbol 12-myristate 13-acetate in cultured fetal rat astrocytes.22 Thus, there is support for a signal-transducing role of the NPR-C.
The PC12 cells contain mRNA for GC-A but not for
GC-B.23 The PC12 cells also appear to possess the
NPR-C, as indicated by radiolabeled ANP binding being displaced by
cANP, a selective NPR-C binding agent.24
Collectively, these results indicate that PC12 cells express GC-A and
NPR-C. We have taken advantage of this situation to differentiate
neuromodulatory effects of CNP from GC
stimulation.15 This is possible because of the
dearth of GC-B in the PC12 cells. Indeed, CNP inhibited evoked dopamine
efflux in a concentration range that failed to alter intracellular cGMP
concentrations (Figures 2 and 3) in the present study, as well. The
only identified natriuretic peptide receptor failing to
alter GC activity is the NPR-C, suggesting that CNP inhibition of
dopamine release is dependent on this receptor.
We examined L-NAME effects on the
oligodeoxynucleotide-treated cells to assess the
specificity of the antisense treatment. L-NAME, an NO synthetase
inhibitor, is known to attenuate evoked
catecholamine release in PC12
cells.25 In both antisense- and missense-treated
cells, L-NAME suppressed dopamine efflux in the same manner (Figure 4),
which indicates that the antisense oligodeoxynucleotide
treatment does not affect this inhibitory pathway
nonspecifically. This result, thus, ruled out the possibility of the
antisense treatment nonspecifically impairing the
neurosympathoinhibitory systems in the cells.
This report has implicated Go in the
neuromodulatory signal-transduction pathway of CNP but has not
addressed the effect of Go in promoting a
reduction in evoked neurotransmitter efflux from the cells. This
pathway has been addressed in previous work defining the effect as a
reduction in the sensitivity of the exocytotic apparatus to
calcium.26 Adrenergic tissue is thought to
secrete neurotransmitter in response to an elevation in intracellular
calcium concentration.27 Surprisingly,
natriuretic peptides were observed to augment calcium entry
into PC12 cells.26 These results are
consistent with those obtained in adrenal glomerulosa tissue,
in which natriuretic peptides suppress
aldosterone secretion28 while
augmenting calcium currents.29 This mechanism of
action to suppress calcium sensitivity, rather than suppressing calcium
currents, probably accounts for the inability of
natriuretic peptides to eliminate evoked
catecholamine efflux from the PC12 cells. Further, it could
account for the potentiation of neurotransmitter efflux by CNP observed
in antisense-treated cells (Figure 2).
The inhibitory effect of Go
ablation on evoked dopamine efflux is a novel observation. We have been
unable to locate any other report of GTP-binding protein ablations with
antisense technologies in neural tissue. Previous work with pertussis
toxin revealed a tendency, but no significant effect, to reduce evoked
dopamine efflux in these cells,14 15 20 30
although others have found pertussis toxin pretreatment to augment
evoked catecholamine release.31
Intracellular injection of an antibody to Go
also enhanced evoked neurotransmitter efflux in the latter
study.31 The Go
associates with exocytotic granules and is anticipated to participate
in the exocytotic process.32 The
inhibitory effect of the Go
reduction observed in the present study has not been reported
previously but would be consistent with a potential involvement
of Go in the exocytotic process.
The Go ablation also tended to attenuate GC
responses to CNP (Figure 3), although the reduction in activity was not
statistically significant. Although GTP-binding proteins are not
generally considered to interact with GC, Khurana and
Pandey33 have shown that a GTP-binding protein
activator, mastoparan, augments GC activity. Additionally,
an antibody to Go prevented the effect of the
mastoparan, indicating that Go is capable of
augmenting GC activity. Our data are consistent with their
report except that the results were not statistically significant in
our study.
In conclusion, we demonstrate that the
Go-subunit of heterotrimeric GTP-binding
proteins is involved in the CNP signaling pathway to inhibit evoked
catecholamine release from PC12 cells. This
represents the first report identifying the GTP-binding protein
involved in signal-transducing effects of natriuretic
peptides. Further, this mediatory role of Go
appears to be involved with the NPR-C because the concentration range
for neuromodulatory effects of CNP does not overlap with activation of
GC. Thus, our results are consistent with the NPR-C mediation
of the neuromodulatory action of CNP by an interaction with the
Go protein. Significantly,
Go ablation failed to alter either GC
responses to CNP or neuromodulatory effects of L-NAME. These data
indicate the utility of this antisense technique in providing a
specific assessment of GTP-binding protein involvement in
signal-transduction events.
|
Acknowledgments |
|---|
The authors thank Dr Timothy Walseth and Dr Jon Holy for kindly providing anti-Go
antibody and monoclonal
antitubulin ß antibody, respectively, and Sue Kurki for
excellent clerical expertise in preparing this manuscript. Received May 8, 1998; first decision July 8, 1998; accepted August 31, 1998.
|
References |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
1. de Bold AJ, Borenstein HB, Veress AT, Sonnenberg H. A rapid and potent natriuretic response to intravenous injection of atrial myocardial extract in rats. Life Sci. 1981;28:89–94.[Medline] [Order article via Infotrieve]
2. Flynn TG, de Bold ML, de Bold AJ. The amino acid sequence of an atrial peptide with potent diuretic and natriuretic properties. Biochem Biophys Res Comm. 1983;117:859–865.[Medline] [Order article via Infotrieve]
3. Sudoh T, Kangawa K, Minamino N, Matsuo H. A new natriuretic peptide in porcine brain. Nature. 1988;332:78–81.[Medline] [Order article via Infotrieve]
4. Sudoh T, Minamino N, Kangawa K, Matsuo H. C-type natriuretic peptide (CNP): a new member of natriuretic peptide family identified in porcine brain. Biochem Biophys Res Comm. 1990;168:863–870.[Medline] [Order article via Infotrieve]
5. Chinkers M, Garbers SL, Chang MS, Lowe DG, Chin H, Goeddel DV, Schulz S. A membrane form of guanylate cyclase is an atrial natriuretic peptide receptor. Nature. 1989;338:78–83.[Medline] [Order article via Infotrieve]
6. Schulz S, Green CK, Yuen PST, Garbers DL. Guanylyl cyclase is a heat-stable enterotoxin receptor. Cell. 1990;63:941–948.[Medline] [Order article via Infotrieve]
7. Lewicki JA, Protter AA. Molecular determinants of natriuretic peptide clearance receptor function. In: Samson WK, Levin ER, eds. Contemporary Endocrinology: Natriuretic Peptides in Health and Disease. Totawa, NJ: Humana Press; 1997:51–69.
8.
Maack T, Suzuki M, Almeida FA, Nussenzveig D,
Scarborough RM, McEnroe GA, Lewicki JA.
Physiological role of silent receptors of atrial
natriuretic factor. Science. 1987;238:675–678.
9.
Brandt RR, Heublein DM, Aarhus LL, Lewicki JA, Burnett
JC Jr. Role of natriuretic peptide clearance receptor in in
vivo control of C-type natriuretic peptide. Am J
Physiol. 1995;269:H326–H331.
10.
Levin ER. Natriuretic peptide C-receptor:
more than a clearance receptor. Am J Physiol. 1993;264:E483–E489.
11. Smyth EM, Keenan AK. The vascular ANF-C receptor: role in atrial peptide signaling. Cell Signal. 1994;6:125–133.[Medline] [Order article via Infotrieve]
12. Trachte GJ. Physiology of the clearance receptor. In: Samson WK, Levin ER, eds. Contemporary Endocrinology: Natriuretic Peptides in Health and Disease. Totawa, NJ: Humana Press; 1997:259–274.
13.
Anand-Srivastava MB, Sehl PD, Lowe DG.
Cytoplasmic domain of natriuretic peptide receptor-C
inhibits adenylyl cyclase involvement of a pertussis toxin-sensitive G
protein. J Biol Chem. 1996;271:19324–19329.
14. Drewett JG, Ziegler RJ, Trachte GJ. Neuromodulatory effects of atrial natriuretic peptides correlate with an inhibition of adenylate cyclase but not an activation of guanylate cyclase. J Pharmacol Exp Ther. 1992;257:689–696.
15.
Trachte GJ, Kanwal S, Elmquist BJ, Ziegler RJ. C-type
natriuretic peptide neuromodulates via "clearance"
receptors. Am J Physiol. 1995;268:C978–C984.
16. Elferink JG, De Koster BM. Atrial natriuretic factor stimulates migration by human neutrophils. Eur J Pharmacol. 1995;288:335–340.[Medline] [Order article via Infotrieve]
17. Kleuss C, Hescheler J, Ewel C, Rosenthal W, Schultz G, Wittig B. Assignment of G-protein subtypes to specific receptors inducing inhibition of calcium currents. Nature. 1991;353:43–48.[Medline] [Order article via Infotrieve]
18. Kalkbrenner F, Dippel E, Wittig B, Schultz G. Specificity of interaction between receptor and G protein: use of antisense techniques to relate G protein subunits to function. Biochim Biophys Acta. 1996;1314:125–139.[Medline] [Order article via Infotrieve]
19. Babinski K, Haddad P, Vallerand D, McNicoll N, De Lean A, Ong H. Natriuretic peptides inhibit nicotine-induced whole-cell currents and catecholamine secretion in bovine chromaffin cells: evidence for the involvement of the atrial natriuretic factor R2 receptors. J Neurochem. 1995;64:1080–1087.[Medline] [Order article via Infotrieve]
20.
Drewett JG, Ziegler RJ, Trachte GJ.
Neuromodulatory effects of ANF are independent of guanylate
cyclase in adrenergic, neuronal pheochromocytoma cells.
J Pharmacol Exp Ther. 1990;255:497–503.
21.
Anand-Srivastava MB, Sairam MR, Cantin M. Ring-deleted
analogs of atrial natriuretic factor inhibit
adenylate cyclase/cAMP system. J Biol Chem. 1990;265:8566–8572.
22.
Prins BA, Weber MJ, Hu RM, Pedram A, Daniels M, Levin
ER. Atrial natriuretic peptide inhibits
mitogen-activated protein kinase through the clearance
receptor. Potential role in the inhibition of astrocyte proliferation.
J Biol Chem. 1996;271:14156–14162.
23.
Suga S, Nakao K, Hosoda K, Mukoyama M, Ogawa Y,
Shirakami G, Arai H, Saito Y, Kambayashi Y, Inouye K, Imura H. Receptor
selectivity of natriuretic peptide family, atrial
natriuretic peptide, brain natriuretic peptide,
and C-type natriuretic peptide. Endocrinology. 1992;130:229–239.
24. Rathinavelu A, Isom GE. Differential internalization and processing of atrial natriuretic factor B and C receptors in PC12 cells. Biochem J. 1991;276:493–497.
25. Hirsch DB, Steiner JP, Dawson TM, Mammed A, Hayek E, Snyder SH. Neurotransmitter release regulated by nitric oxide in PC-12 cells and brain synaptosomes. Curr Biol. 1993;3:749–754.[Medline] [Order article via Infotrieve]
26.
Kanwal S, Elmquist BJ, Trachte GJ. Atrial
natriuretic peptide inhibits evoked
catecholamine release by altering sensitivity to calcium.
J Pharmacol Exp Ther. 1997;283:426–433.
27. Douglas WW. Stimulus-secretion coupling: the concept and clues from chromaffin and other cells. Br J Pharmacol. 1968;34:451–474.[Medline] [Order article via Infotrieve]
28.
Lotshaw DP, Franco-Saenz R, Mulrow PJ. Atrial
natriuretic peptide inhibition of calcium ionophore
A23187-stimulated aldosterone secretion in rat adrenal
glomerulosa cells. Endocrinology. 1991;129:2305–2310.
29.
Isales CM, Lewicki JA, Nee JJ, Barrett PQ. ANP-(7–23)
stimulates a DHP-sensitive Ca2+ conductance and
reduces cAMP via a cGMP-independent mechanism. Am J
Physiol. 1992;263:C334–C342.
30.
Bittner MA, Holz RW, Neubig RR. Guanine
nucleotide effects on catecholamine secretion
from digitonin-permeabilized adrenal chromaffin cells.
J Biol Chem. 1986;261:10182–10188.
31. Ohara-Imaizumi M, Kameyama K, Kawae N, Takeda K, Muramatsu S, Kumakura K. Regulatory role of the GTP-binding protein, Go, in the mechanism of exocytosis in adrenal chromaffin cells. J Neurchem. 1992;58:2275–2284.[Medline] [Order article via Infotrieve]
32. Vitale N, Gonon F, Thierse D, Aunis D, Bader MF. Exocytosis in single chromaffin cells: regulation by a secretory granule-associated Go protein. Cell Mol Neurobiol.. 1997;17:71–87.
33. Khurana ML, Pandey KN. Modulation of guanylate cyclase-coupled atrial natriuretic factor receptor activity by mastoparan and ANF in murine Leydig tumor cells: role of G-proteins. Biochim Biophys Acta. 1994;1224:61–67.[Medline] [Order article via Infotrieve]
This article has been cited by other articles:
 |
|
 |
|
  T. L. Pallone, Z. Zhang, and K. Rhinehart Physiology of the renal medullary microcirculation Am J Physiol Renal Physiol, February 1, 2003; 284(2): F253 - F266. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 X.-l. He, D.-c. Chow, M. M. Martick, and K. Christopher Garcia Allosteric Activation of a Spring-Loaded Natriuretic Peptide Receptor Dimer by Hormone Science, August 31, 2001; 293(5535): 1657 - 1662. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Borges, S. Sanchez de Villarroel, N. J. Winand, I. Lippo de Becemberg, M. J. Alfonzo, and R. Gonzalez de Alfonzo Molecular and Biochemical Characterization of a CNP-Sensitive Guanylyl Cyclase in Bovine Tracheal Smooth Muscle Am. J. Respir. Cell Mol. Biol., July 1, 2001; 25(1): 98 - 103. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P.R Kalra, S.D Anker, A.D Struthers, and A.J.S Coats The role of C-type natriuretic peptide in cardiovascular medicine Eur. Heart J., June 2, 2001; 22(12): 997 - 1007. [PDF]
|
|
|
|
 |
|
 K. A. Lucas, G. M. Pitari, S. Kazerounian, I. Ruiz-Stewart, J. Park, S. Schulz, K. P. Chepenik, and S. A. Waldman Guanylyl Cyclases and Signaling by Cyclic GMP Pharmacol. Rev., September 1, 2000; 52(3): 375 - 414. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. J. Trachte Depletion of Natriuretic Peptide C Receptors Eliminates Inhibitory Effects of C-Type Natriuretic Peptide on Evoked Neurotransmitter Efflux J. Pharmacol. Exp. Ther., July 1, 2000; 294(1): 210 - 215. [Abstract] [Full Text]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||