(Hypertension. 1997;30:1342-1347.)
© 1997 American Heart Association, Inc.
Articles |
Tissue-Specific Regulation of Renal and Cardiac Atrial Natriuretic Factor Gene Expression in Deoxycorticosterone Acetate–Salt Rats
From the University of Ottawa Heart Institute at the Ottawa Civic Hospital (T.O., N.Y.) and the Departments of Physiology (B.G.B., A.J. de B.) and Pathology (M.L.K. de B., A.J. de B.), University of Ottawa (Ontario, Canada).
Correspondence to Adolfo J. de Bold, PhD, University of Ottawa Heart Institute Research Centre at the Ottawa Civic Hospital, 1053 Carling Ave, Ottawa, Ontario K1Y 4E9, Canada.
 |
Abstract |
|---|
 Top Abstract IntroductionMethodsResultsDiscussionReferences |
|---|
Abstract Atrial natriuretic factor (ANF) is expressed in several noncardiac tissues where it may have an autocrine or paracrine function. Such function may be expected of locally synthesized ANF in the renal parenchyma. Previous investigations of the existence of ANF mRNA in the renal parenchyma have yielded conflicting results. The investigations reported here were designed to detect and measure ANF mRNA in normal rats and in rats subjected to a deoxycorticosterone acetate (DOCA)–salt treatment schedule known to strongly activate cardiac ANF gene expression. The expression of the renal ANF gene was measured using a newly developed quantitative competitive reverse transcription–polymerase chain reaction (QC-RT-PCR). This method uses an internal competitor thatserves as an internal standard and makes the procedure independent of measurement relative to housekeeping genes. It was found that renal ANF mRNA levels were 107 times lower than those found in left or right atria, but immunoreactive (ir) renal ANF concentration by specific radioimmunoassay was 104 times lower than that of atrial irANF levels. Reverse-phase high-performance liquid chromatography analysis revealed that more than 99% of renal irANF is processed ANF99-126. This finding suggests that most of the irANF measured in kidney extracts likely originates from atrial sources. Left atrial ANF mRNA levels after 1 week of DOCA-salt treatment was significantly higher than that of control rats ([21.06±2.99]x10-15 mol/µg total RNA versus [8.59±1.26]x10-15 mol/µg total RNA, P<.05). However, renal ANF mRNA levels in DOCA-salt rats were significantly decreased compared with those of control rats ([1.64±0.34]x10-22 mol/µg total RNA versus [3.96±0.61]x10-22 mol/µg total RNA, P<.05). These results indicate that (1) renal ANF mRNA can be consistently and specifically demonstrated after reverse transcription and PCR amplification; (2) renal and cardiac ANF synthesis are regulated in a tissue-specific, opposite manner during DOCA-salt treatment; and (3) the finding that renal ANF mRNA is downregulated by DOCA-salt treatment together with previous findings suggest the need for further investigation into the role of renal ANF mRNA downregulation in the pathogenetic mechanism that leads to volume expansion and hypertension after chronic DOCA-salt treatment.
Key Words: atrial natriuretic factor • polymerase chain reaction • deoxycorticosterone acetate • kidney
|
Introduction |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
In mammals, the major site of production, storage, and release of the natriuretic peptides ANF and BNP is the heart. Nevertheless, both these hormones are expressed in several noncardiac tissues where they are assumed to play an autocrine or paracrine function.1 2 Such a function may be expected of locally synthesized ANF in the renal parenchyma.
The ANF concentration in the kidney is many-fold lower than that present in the heart. Immunoreactive N-terminal ANF (ANF1-98) as well as the circulating form ANF99-126 have been measured in rat kidney, suggesting that ANF is synthesized by the kidney.3 In addition, ANF1-126 has been demonstrated in neonatal and adult rat renal cell cultures.4
Immunohistochemical detection of ANF has been reported. Saba et al,5 working with human kidney, demonstrated irANF in multiple sites in the kidney parenchyma, which would suggest the presence of considerable amounts of ANF transcript in the kidney. In our own experience, however, irANF localizes in the rat kidney in the intercalated cells of the distal tubule (according to our own unpublished findings and those in Reference 66 ). Similar results have been reported in human kidney.7 These findings are in line with the fact that the abundance of ANF transcripts in the rat kidney is very low. Unlike other extra atrial tissues such as the cardiac ventricle, where natriuretic peptide transcripts may be demonstrated by Northern blot analysis, or aortic tissues, where reverse transcription followed by PCR unfailingly demonstrates specific transcripts, the abundance of natriuretic peptide gene transcripts in the kidney is exceedingly low and has been undetectable at times after a high number of PCR amplification cycles of reverse-transcribed renal mRNA.2 8 9 10
In the present report, we describe investigations carried out to define renal ANF gene expression and to determine whether renal ANF transcripts are altered in parallel with changes in atrial ANF gene expression in normal and DOCA-salt–treated rats. We have previously reported that a 1-week DOCA-salt treatment in the rat is a strong stimulator of ANF release leading to increased circulating levels, partial depletion of left atrial ANF stores, and degranulation.11 12 To quantify renal ANF expression, we developed a QC-RT-PCR procedure based on the use of a recombinant ANF RNA competitor,13 thus allowing for quality control from extraction to the absolute quantification of ANF mRNA and independence from measurements relative to housekeeping genes.
The data obtained show that ANF gene expression is regulated in a tissue-specific manner that consisted of upregulation of left atrial ANF gene expression, downregulation of renal expression, and unchanged expression in the right atrium and the ventricles.
|
Methods |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Experimental Animals
Male Sprague-Dawley rats weighing 100 to 125 g were used following institutional guidelines. The DOCA-salt rats were injected subcutaneously with a suspension of DOCA (30 mg/kg; Sigma Chemical) dissolved in sesame oil and were given free access to 1% NaCl drinking solution during the experiment. One week later, all animals were killed by decapitation, and trunk blood was collected into ice-cooled tubes containing 1.5 mg/mL 15 mg K3EDTA. The heart, kidney, brain, and liver samples were rapidly removed and immediately frozen in liquid nitrogen and kept at -80°C until used. The heart chambers were dissected individually. The interatrial and interventricular septa were included in their respective left chambers.
Total RNA Extraction
Tissue samples were extracted using Trizol (GIBCO-BRL). To
remove contaminating genomic DNA, RNA samples were incubated with 1
unit of RNAse-free DNAse (Promega) for 10 minutes at 37°C in 50 µL
of a buffer containing 40 mmol/L Tris-HCl (pH 7.9), 10
mmol/L NaCl, 6 mmol/L MgCl2, and 10
mmol/L CaCl2. After DNAse treatment, the samples
were reextracted with 10 vol of Trizol, and the RNA was quantified by
spectrophotometry.
RT-PCR and Southern Blot Analysis
RNA samples were reverse-transcribed using Super Script II
RNASE H- Reverse Transcriptase and
oligo(dT)12-18 primer of an RT kit (GIBCO-BRL). After RT,
the template RNA was eliminated by incubation with 1 unit of DNAse-free
RNAse for 20 minutes at 37°C. One fifth of the cDNA product was
used for PCR amplification using the ANF primers shown in Table 1
. For primers, design, and calculation
of optimal annealing temperatures, Oligo software (National
Biosciences)14 15 was used, with the rat ANF cDNA
sequence16 used as template. PCRs were conducted in a
final volume of 50 µL containing PCR buffer (10 mmol/L
Tris-HCl, pH 8.3, and 50 mmol/L KCl), 0.2
mmol/L of each deoxynucleotide triphosphate,
0.4 µmol/L primers, 1.25 units of Ampli Taq DNA
Polymerase (Perkin-Elmer) followed by HotWax Mg2+ Beads
(Invitrogen). The reactions were heated at 95°C for 2 minutes and
cycled 40 times through a 60-second denaturing step at 95°C, a
45-second annealing step at 58°C, and a 90-second extension step at
72°C. After the final cycle, a 10-minute extension step at 72°C was
included. These conditions except for the annealing temperature were
used for all amplifications. Aliquots (5 µL) of the PCR product
were electrophoresed on a 2% agarose gel and were visualized by
ethidium bromide staining. For Southern blot analysis, the PCR
products electrophoresed on an agarose gel were transferred to
nylon membranes (Hybond N+, Amersham). Membranes were
prehybridized in 2.5x Denhardt's solution, 5x SSC, 50% formamide,
25 mmol/L KH2PO4, 0.2% SDS, and
0.2 mg/mL herring sss DNA for 2 hours at 42°C. Hybridization
was then carried out for 16 hours at 42°C with the same solution as
the prehybridization except for the presence of the radiolabeled
probe,16 which was a 900-bp
EcoRI/HindIII fragment containing the full-length
rat ANF cDNA. The cDNA was labeled with 5'-[
32P]dCTP
(3000 Ci/mmol; Amersham) using the Megaprime DNA labeling system
(Amersham). At the end of the hybridization, the membranes were washed
twice at 42°C with 2x SSC and 1% SDS and twice at 55°C with 1x
SSC and 0.1% SDS and then autoradiographed.
|
Preparation of Competitor RNA
Viral-ANF DNA was obtained by PCR amplification of a viral
DNA (v-erb) (PCR MIMIC construction kit, CLONTECH) using composite
primers and an annealing temperature of 58°C (Fig 1). These primers contain sequences that
hybridize to the viral DNA fragment and are flanked by ANF-specific
sequences (Table 1
). Two microliters of the PCR product were used
for reamplification with the ANF primers (Table 1). Two microliters of
a 1:100 dilution of the second PCR product was reamplified using
another two composite primers, with an annealing temperature of 62°C.
The forward primer contained the T7 promoter and ANF forward sequence.
The reverse primer contained the ANF reverse sequence and poly
(dT)18 (Table 1). The final PCR product was purified
with a spin cartridge (MICROCON-3d AMICON) and quantified by
spectrophotometry. One microgram of the purified PCR product was
transcribed into RNA using the Riboprobe Gemini II in vitro
transcription system (Promega). The recombinant RNA was subsequently
treated with RNAse-free DNAse to remove the DNA template and extracted
once with water-saturated phenol/chloroform and once with
chloroform/isoamyl alcohol (24:1), followed by ethanol precipitation.
The RNA was resuspended in diethyl pyrocarbonate–treated water and
quantified by spectrophotometry.
|
QC-RT-PCR
For each sample, aliquots of total RNA (15 ng for atrium,
600 ng for ventricle, and 5 µg for kidney, brain, and liver,
respectively) were prepared and a 2x dilution series of competitor RNA
was spiked into these aliquots (Fig 1). After RT-PCR with an annealing
temperature of 58°C, aliquots (5 µL) of the PCR product were
electrophoresed on a 2% agarose gel and visualized by ethidium bromide
staining. Negative photographs were taken using Polaroid 55 film. The
negatives were scanned using an Ultrascan XL laser densitometer and
Gelscan XL 2000 software package. The ratio of the density of the
competitor RNA to the target RNA was plotted against the amount of the
competitor RNA added to each reaction. The competitor RNA amount at
which this ratio is equal to 1 represents the amount of ANF
mRNA present in the initial RNA sample.
Extraction of Plasma and Tissue Samples and RIA for ANF
Plasma samples were acidified by adding 100 µL/mL of 1
mol/L HCl and passed through Sep-Pak C18 cartridges (Millipore)
that were prewetted with 5 mL of 60% ACN in 0.1% TFA, and 10 mL of
0.1% TFA. The cartridges with the absorbed peptides were washed with
20 mL of 0.1% TFA and then eluted with 3 mL of 60% ACN in 0.1%
TFA.17 Tissue samples were homogenized in 10
volumes of an extracting mixture consisting of 0.1 N HCl, 1.0
mol/L acetic acid, and 1% NaCl and centrifuged at 10
000g for 30 minutes at 4°C.18 The
supernatants were then extracted using Sep-Pak C18 cartridges as
described above for plasma except that elution was with 80% ACN in
0.1% TFA. The eluates were freeze-dried and used in a RIA with
anti-rat ANF99-126 serum from Peninsula Laboratories as
previously described.17
RP-HPLC
RP-HPLC analysis was performed as previously
described18 on a C18 Vydac column (0.78x30 cm) using a
linear gradient of ACN from 15% to 55% in 0.1% TFA at a flow rate of
1.5 mL/min. Three milliliter fractions were freeze-dried and processed
for ANF RIA.
Statistical Analysis
All data are expressed as mean±SEM. To determine statistical
differences between groups, a Student's t test was
performed. A level of P<.05 was considered significant.
|
Results |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
After RT-PCR and gel electrophoresis, a single 697-bp amplification product was detected in heart, kidney, and brain but not in liver samples (Fig 2
). Southern
blot analysis with a rat ANF cDNA probe identified a single DNA
species in heart, kidney, and brain tissues, confirming that the single
band that appeared after RT-PCR was a result of specific amplification
of ANF mRNA (Fig 2).
|
To measure ANF mRNA concentration by QC-RT-PCR in the various tissues,
various amounts of competitor RNA were spiked into aliquots of total
RNA from each tissue sample. After RT-PCR, a single 697-bp band for ANF
and a single 437-bp band for the competitor RNA were identifiable in
each lane (Figs 3 and 4). The ANF/ANF competitor ratio from
each lane was calculated and plotted. The ANF competitor RNA amount at
which this ratio equals 1 represents the amount of ANF mRNA
present in the initial RNA sample. ANF mRNA levels found in heart,
kidney, and brain tissues are shown in Table 2. The concentration of ANF mRNA was
highest in the atria. The left ventricle, right ventricle, and kidney
ANF mRNA levels were about 102, 103, and
107 times lower than that of the atrium, respectively.
Renal irANF levels were about 104 times lower than those
previously found in atria.11
|
|
|
RP-HPLC of kidney tissue extracts revealed a single peak eluting
in the position of ANF99-126. No peak was detected in the
position corresponding to ANF1-126 (Fig 5).
|
In DOCA-salt rats, the ANF mRNA level of the left atrium was
significantly increased compared with that in control rats, whereas the
left atrial ANF level and the renal ANF mRNA level in DOCA-salt rats
were significantly decreased compared with those in control rats (Table 2). The plasma ANF level in DOCA-salt
rats was significantly higher than that in control rats (Table 2).
|
Discussion |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
In mammals, the bulk of ANF is normally produced in a regulated manner by atrial cardiocytes as ANF1-126. Co-secretional processing yields the circulating form ANF99-126. From the fact that ANF is present in a large number of tissues, it can be inferred that this peptide may also act through paracrine and autocrine interactions by locally synthesized peptide. This may be the case for renal ANF. ANF1-126 has been detected in cultured kidney cells of neonatal and adult rats. In addition, these cells secrete radiolabeled ANF1-126 after being pulsed with [35S]methionine, and cycloheximide decreases its synthesis.3 4 The detection of ANF transcripts in the adult kidney has been more difficult. Northern blot analysis fails to detect ANF mRNA in kidneys,9 whereas RT-PCR analysis of ANF transcript has yielded conflicting results. Some investigators have detected very low levels of renal ANF mRNA with RT-PCR, whereas others were either unable to do so or were not always successful in doing so.2 8 9 10 19 The lack of consistent detection of renal ANF message may be due to technical difficulties inherent in detecting very low copy numbers of a specific mRNA species by RT-PCR. In addition, it has been suggested that all genes are transcribed at very low levels in all cell types, and therefore sufficient rounds of amplification will identify specific mRNAs in just about any source (the so-called "illegitimate transcription").20 Moreover, blood cell types containing the transcript of interest may be present in the tissue samples being analyzed. In the present studies, the lack of amplification of ANF mRNA in liver extracts indicates that our detection of ANF mRNA in kidney is specific and is not due to artificial detection of illegitimate transcriptions or tissue contamination. However, we have found that a combination of DNAse treatment of the RNA samples previous to RT and a hot-start for PCR are crucial for effective and specific amplification of low copy mRNA species.
In the present work it was found that renal ANF mRNA level is 107 times lower than left atrial ANF mRNA level, whereas renal irANF level is only 104 times less than atrial irANF level. This finding may have its basis in the possibility that the RIA for renal irANF measures both ANF synthesized in situ as well as receptor-bound ANF. This interpretation is supported by the HPLC results which showed that more than 99% of irANF extracted from renal tissue is processed ANF99-126. Therefore, the ANF concentration measured in renal tissue extracts does not reflect the level of synthesis of ANF peptide in kidney. It is also possible, however, that the difference between the half-lives of ANF mRNA and ANF peptide may partly explain the disparate concentration of ANF mRNA and ANF peptide in kidney if the measurements did not reflect a steady state condition.
Although the experiments presented here were designed primarily to allow us to detect and subsequently see the effect of DOCA-salt treatment, a strong activator of cardiac ANF, on renal ANF mRNA, the results obtained, which show opposite regulation of cardiac and renal ANF mRNA, may be relevant to the understanding of the role of renal ANF in mineralocorticoid escape or mineralocorticoid-induced hypertension. We have shown previously that ANF mediates the natriuresis that occurs after induction of a transient sodium-positive balance by mineralocorticoid administration, a phenomenon referred to as mineralocorticoid escape.21 Continued administration of mineralocorticoid plus salt, however, results in a state of volume expansion and positive sodium balance, leading to hypertension and cardiac hypertrophy despite a significant elevation of plasma ANF and activation of the cardiac ANF gene. It is not clear why this activation is not sufficient to maintain normal hydrosaline balance, but the findings presented here together with previous findings regarding changes in ANF binding and metabolism in the kidney induced by mineralocorticoid and salt excess may be relevant as follows.
The effects of ANF are mediated by the A-type guanylyl cyclase–linked receptor (GC-A receptor), and the GC-A mRNA has been identified and characterized in glomeruli and IMCD.22 23 In the latter, microperfusion and electrophysiological and immunocytochemical approaches have localized these receptors in apical, basal, and basolateral sites24 25 26 27 28 so that both filtered and circulating ANF can potentially affect sodium reabsorption in the IMCD. However, filtered ANF can be degraded by the neutral endopeptidase activity that is particularly abundant in the brush border of the proximal tubule. Furthermore, neutral endopeptidase activity has been shown to be significantly increased by chronic salt loading29 and by DOCA-salt treatment.30 The administration of neutral endopeptidase inhibitors dramatically augments the renal actions of ANF31 in volume-expanded states including the DOCA-salt model,30 32 33 34 35 suggesting that filtered ANF is needed to effect natriuresis in these models.
Renal ANF has been localized in intercalated cells of the distal tubule (according to our unpublished findings and those in Reference 66 ), and, therefore, it is downstream from the major site of ANF inactivation by neutral endopeptidase but upstream from the IMCD receptor sites. Hence, renal ANF, secreted from specific tubular cells in the distal nephron, can reach the IMCD apical receptor sites unimpeded by neutral endopeptidase degradation. In addition, the natriuretic peptide clearance receptor, while present in glomeruli, is not detectable in IMCD.22 These considerations are noteworthy given that ANF is one of the most important contributors to salt excretion in the IMCD.36 Viewed in this light, the finding in our current study that DOCA salt decreases renal ANF mRNA levels has special importance because it suggests that diminished levels of renal ANF should be investigated as a contributing factor in the pathogenetic mechanism leading to volume expansion and hypertension induced by chronic DOCA-salt treatment. This finding would also explain why in the DOCA-salt model, natriuresis appears to become dependent on filtered ANF and possibly on other peptides that are known to be sensitive to neutral endopeptidase degradation.
It is intriguing that DOCA-salt treatment decreases renal ANF gene expression, whereas it strongly activates expression in the heart. Because DOCA does not directly affect ANF gene expression in cultured atrial cardiocytes,37 it does not seem likely that DOCA itself can modulate renal ANF gene expression, nor is there evidence that ANF synthesis is subjected to negative feedback by ANF itself. One interesting possibility in the DOCA-salt model exists in the fact that DOCA-salt treatment suppresses the renal RAS. Both the heart and kidney38 possess a local RAS, and it has been shown to be involved in regulating hypertrophy and contractility in the heart and in regulating sodium reabsorption and glomerular hemodynamics in the kidney.39 It has been reported40 that in cultured ventricular cardiocytes mechanical stretch stimulates ANF gene expression and increases angiotensin II secretion into the medium and that an angiotensin type 1 receptor–selective antagonist inhibits the stretch-induced increase of ANF mRNA level. In suprarenal aortic banded hypertensive rats treated with both 1 mg/kg and 10 µg/kg of the angiotensin-converting enzyme inhibitor ramipril, we have demonstrated that cardiac tissue RAS and plasma RAS were independently related to the elevation of ventricular ANF gene expression.41 These reports suggest that angiotensin II stimulates ANF gene expression in cardiocytes and that, by extension, it may do so in the renal cell as well. On the other hand, DOCA may downregulate ANF gene expression by inhibiting tissue RAS both in atrium and kidney. It may be possible that in the atrium the mechanical stimulus brought about by volume expansion causes ANF mRNA elevation by mechanisms independent of local RAS, whereas the RAS-mediated inhibiting effect of DOCA prevails in kidney, leading to a decrease in ANF mRNA levels. Indeed, a RAS-independent increase in ANF gene expression by stretch has been suggested by studies in cultured cardiocytes. In these investigations, angiotensin II blockade could not completely suppress increased ANF gene expression, and a large contribution by endothelin-1, independent from angiotensin II, has been shown.42 43 However, there seems to be no reports dealing with these possibilities in renal tissue.
In summary, absolute quantification of ANF mRNA by QC-RT-PCR demonstrates the presence of this transcript in renal parenchyma and demonstrates that renal and cardiac ANF gene expression in DOCA-salt rats is regulated in an opposite fashion. The finding that renal ANF mRNA is downregulated together with previous findings showing extensive degradation of filtered ANF suggests future studies on the role of renal ANF mRNA downregulation in the pathogenetic mechanism leading to volume expansion and hypertension after chronic DOCA-salt treatment.
|
Selected Abbreviations and Acronyms |
|---|
|
|
Acknowledgments |
|---|
This work was supported by grants from the Ontario Heart and Stroke Foundation and the Medical Research Council of Canada. We thank Michelle Stevenson, Amalia Ponce, and Carole Frost for their excellent assistance.
Received April 22, 1997; first decision May 26, 1997; accepted June 9, 1997.
|
References |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
1. Gardner DG, Deschepper CF, Ganong WF, Hane S, Fiddes J, Baxter JD, Lewicki J. Extra-atrial expression of the gene for atrial natriuretic factor. Proc Natl Acad Sci U S A. 1986;83:6697-6701.
2.
Dagnino L, Drouin J, Nemer M. Differential
expression of natriuretic peptide genes in cardiac and
extracardiac tissues. Mol Endocrinol. 1991;5:1292-1300.
3. Vesely DL, Palmer PA, Giordano AT. Atrial natriuretic factor prohormone peptides are present in a variety of tissues. Peptides. 1992;13:165-170.[Medline] [Order article via Infotrieve]
4. Ritter D, Needleman P, Greenwald JE. Synthesis and secretion of an atriopeptin-like protein in rat kidney cell culture. J Clin Invest. 1991;87:208-212.
5. Saba SR, Ramirez G, Vesely DL. Immunocytochemical localization of ProANF 1-30, ProANF 31-67, atrial natriuretic factor and urodilation in the human kidney. Am J Nephrol. 1993;13:85-93.[Medline] [Order article via Infotrieve]
6. McKenzie JC, Tanaka I, Misono KS, Inagami T. Immunocytochemical localization of atrial natriuretic factor in the kidney, adrenal medulla, pituitary, and atrium of rat. J Histochem Cytochem. 1985;33:828-832.[Abstract]
7. Figueroa CD, Lewis HM, MacIver AG, Mackenzie JC, Bhoola KD. Cellular localisation of atrial natriuretic factor in the human kidney. Nephrol Dial Transplant. 1990;5:25-31.
8.
Greenwald JE, Ritter D, Tetens E, Rotwein PS.
Renal expression of the gene for atrial natriuretic
factor. Am J Physiol. 1992;263:F974–F978.
9. Golomb E, Friedman E, Abassi ZA, Trachewsky D, Keiser HR. Rare renal transcription of the atrial natriuretic factor gene in rats: demonstration by polymerase chain reaction. Am J Hypertens. 1993;6:867-872.[Medline] [Order article via Infotrieve]
10. Suzuki E, Hirata Y, Hayakawa H, Omata M, Kojima M, Kangawa K, Minamino N, Matsuo H. Evidence for C-type natriuretic peptide production in the rat kidney. Biochem Biophys Res Commun. 1993;192:532-538.[Medline] [Order article via Infotrieve]
11. Yokota N, Bruneau BG, Fernandez BE, Kuroski-de Bold ML, Piazza LA, Eid H, de Bold AJ. Dissociation of cardiac hypertrophy, myosin heavy chain isoform expression, and natriuretic peptide production in DOCA-salt rats. Am J Hypertens. 1995;8:301-310.[Medline] [Order article via Infotrieve]
12. de Bold AJ. Heart atria granularity effects of changes in water-electrolyte balance. Proc Soc Exp Biol Med. 1979;161:508-511.[Medline] [Order article via Infotrieve]
13. Heuvel JPV, Tyson FL, Bell DA. Construction of recombinant RNA templates for use as internal standards in quantitative RT-PCR. Biotechniques. 1993;14:395-398.[Medline] [Order article via Infotrieve]
14.
Rychlik W, Rhoads RE. A computer program for
choosing optimal oligonucleotides for filter
hybridization,sequencing and in vitro amplification of DNA.
Nucleic Acids Res. 1989;17:8543-8551.
15.
Rychlik W, Spencer WJ, Rhoads RE. Optimization
of the annealing temperature for DNA amplification in vitro.
Nucleic Acids Res. 1990;18:6409-6412.
16.
Flynn TG, Davies PL, Kennedy BP, de Bold ML, de
Bold AJ. Alignment of rat cardionatrin sequences with the
preprocardionatrin sequence from complementary DNA.
Science. 1985;228:323-325.
17. Sarda IR, de Bold ML, de Bold AJ. Optimization of atrial natriuretic factor radioimmunoassay. Clin Biochem. 1989;22:11-15.[Medline] [Order article via Infotrieve]
18. de Bold AJ, Flynn TG. Cardionatrin I: a novel heart peptide with potent diuretic and natriuretic properties. Life Sci. 1983;33:297-302.[Medline] [Order article via Infotrieve]
19.
Chen C, Lokhandwala MF. Identification of
1-adrenoceptor subtypes involved in the
antinatriuretic response to intrarenal infusion of
phenylephrine. Eur J Pharmacol. 1995;287:1-6.[Medline]
[Order article via Infotrieve]
20.
Chelly J, Concordet J, Kaplan J, Kahn A.
Illegitimate transcription: Transcription of any gene in any cell
type. Proc Natl Acad Sci U S A. 1989;86:2617-2621.
21. Yokota N, Bruneau BG, Kuroski-de Bold ML, de Bold AJ. Atrial natriuretic factor significantly contributes to the mineralocorticoid escape phenomenon: evidence for a guanylate cyclase-mediated pathway. J Clin Invest. 1994;94:1938-1946.
22. Yamamoto T, Feng L, Mizuno T, Hirose S, Kawasaki K, Yaoita E, Kihara I, Wilson CB. Expression of mRNA for natriuretic peptide receptor subtypes in bovine kidney. Am J Physiol. 1994;267(pt 2):F318–F324.
23.
Gunning ME, Ballermann BJ, Silva P, Brenner BM, Zeidel
ML. Characterization of ANP receptors in rabbit inner medullary
collecting duct cells. Am J Physiol. 1988;255:F324–F330.
24.
Sonnenberg H, Honrath U, Wilson DR. In vivo
microperfusion of inner medullary collecting duct in rats: effect of
amiloride and ANF. Am J Physiol. 1990;259:F222–F226.
25.
Light DB, Schwiebert EM, Karlson KH, Stanton BA.
Atrial natriuretic peptide inhibits a cation channel in
renal inner medullary collecting duct cells.
Science. 1989;243:383-385.
26. Hashimoto Y, Ozaki J, Yasuhara M, Hori R, Suga S, Itoh H, Nakao K, Inui K. Functional evidence for an apical ANP receptor in LLCPK1 kidney epithelial cells. Eur J Pharmacol-Molec Pharm. 1994;268:443-445.[Medline] [Order article via Infotrieve]
27. Ritter D, Dean AD, Guan ZH, Greenwald JE. Polarized distribution of renal natriuretic peptide receptors in normal physiology and ischemia. Am J Physiol. 1995;269(pt 2):F918–F925.
28.
Rocha AS, Kudo LH. Atrial peptide and cGMP
effects on NaCl transport in inner medullary collecting duct.
Am J Physiol. 1990;259:F258–F268.
29. Aviv R, Gurbanov K, Hoffman A, Blumberg S, Winaver J. Urinary neutral endopeptidase 24.11 activity: modulation by chronic salt loading. Kidney Int. 1995;47:855-860.[Medline] [Order article via Infotrieve]
30. Hirata Y, Suzuki Y, Suzuki E, Hayakawa H, Kimura K, Goto A, Omata M, Minamino N, Kangawa K, Matsuo H. Mechanisms underlying the augmented responses of deoxycorticosterone acetate-salt hypertensive rats to neutral endopeptidase inhibitors. J Hypertens. 1994;12:367-374.[Medline] [Order article via Infotrieve]
31. Margulies KB, Cavero PG, Seymour AA, Delaney NG, Burnett JC Jr. Neutral endopeptidase inhibition potentiates the renal actions of atrial natriuretic factor. Kidney Int. 1990;38:67-72.[Medline] [Order article via Infotrieve]
32. Scott JM, Barclay PL, Shepperson NB. Renal effects of neutral endopeptidase inhibition in euvolemic and hypervolemic rats. Eur J Pharmacol. 1993;242:91-97.[Medline] [Order article via Infotrieve]
33.
Seymour AA, Asaad MM, Lanoce VM, Fennell SA, Cheung HS,
Rogers WL. Inhibition of neutral endopeptidase
3.4.24.11 in conscious dogs with pacing induced heart failure.
Cardiovasc Res. 1993;27:1015-1023.
34. Pham I, el Amrani AI, Fournie-Zaluski MC, Corvol P, Roques B, Michel J. Effects of the selective neutral endopeptidase inhibitor, retrothiorphan, on renal function and blood pressure in conscious normotensive Wistar and hypertensive DOCA-salt rats. J Cardiovasc Pharmacol. 1992;20:847-857.[Medline] [Order article via Infotrieve]
35. Seymour AA, Asaad MM, Abboa-Offei BE, Smith PL, Rogers WL. Sodium loads enhance the natriuretic responses to atrial natriuretic peptide and neutral endopeptidase inhibitors in conscious cynomolgus monkeys. Clin Exp Pharmacol Physiol. 1994;21:845-856.[Medline] [Order article via Infotrieve]
36. Sonnenberg H. Renal regulation of salt balance: a primer for non-purists. Pediatr Nephrol. 1990;4:354-357.[Medline] [Order article via Infotrieve]
37. Gardner DG, Gertz BJ, Deschepper CF, Kim DY. Gene for the rat atrial natriuretic peptide is regulated by glucocorticoids in vitro. J Clin Invest. 1988;82:1275-1281.
38. Schunkert H, Ingelfinger JR, Hirsch AT, Tang SS, Litwin SE, Talsness CE, Dzau VJ. Evidence for tissue-specific activation of renal angiotensinogen mRNA expression in chronic stable experimental heart failure. J Clin Invest. 1992;90:1523-1529.
39.
Dzau VJ. Tissue renin-angiotensin
system in myocardial hypertrophy and failure.
Arch Int Med. 1993;153:937-942.
40. Sadoshima J, Xu Y, Slayter HS, Izumo S. Autocrine release of angiotensin II mediates stretch-induced hypertrophy of cardiac myocytes in vitro. Cell. 1993;75:977-984.[Medline] [Order article via Infotrieve]
41.
Ogawa T, Linz W, Stevenson M, Bruneau BG, Kuroski-de
Bold ML, Chen JH, Eid H, Schölkens BA, de Bold AJ.
Evidence for load-dependent and load-independent determinants of
cardiac natriuretic peptide production.
Circulation. 1996;93:2059-2067.
42.
Yamazaki T, Komuro I, Kudoh S, Zou Y, Shiojima I,
Mizuno T, Takano H, Hiroi Y, Ueki K, Tobe K, Kadowaki T, Nagai R,
Yazaki Y. Angiotensin II partly mediates mechanical
stress–induced cardiac hypertrophy. Circ
Res. 1995;77:258-265.
43.
Yamazaki T, Komuro I, Kudoh S, Zou Y, Shiojima I, Hiroi
Y, Mizuno T, Maemura K, Kurihara H, Aikawa R, Takano H, Yazaki
Y. Endothelin-1 is involved in mechanical stress-induced
cardiomyocyte hypertrophy. J
Biol Chem. 1996;271:3221-3228.
This article has been cited by other articles:
 |
|
 |
|
  T. Ogawa, W. Linz, B. A. Scholkens, and A. J. de Bold Variable Renal Atrial Natriuretic Factor Gene Expression in Hypertension Hypertension, June 1, 1999; 33(6): 1342 - 1347. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||