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European Journal of Heart Failure 2000 2(1):33-40; doi:10.1016/S1388-9842(99)00074-4
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© 2000 European Society of Cardiology

The modulating actions of sulfonylurea on atrial natriuretic peptide release in experimental acute heart failure

Horng H. Chen*, Karen Y. Oh1, Andre Terzic and John C. Burnett, Jr.

Cardiorenal and Cardiovascular Research Laboratories, Division of Cardiovascular Diseases, Departments of Medicine, Physiology and Pharmacology, Mayo Clinic, Mayo Foundation Rochester, MN, USA

* Corresponding author. 915 Guggenheim, Mayo Clinic, Rochester, MN 55905, USA. Tel.: +1-507-284-4343; fax: +1-507-266-4710. E-mail address: chen.horng{at}mayo.edu


   Abstract
Top
 Notes
 Abstract
1. Introduction
 2. Methods
 3. Results
 4. Discussion
 References
 
Objectives: This study defined the modulating actions of sulfonylurea on acute release of atrial natriuretic peptide (ANP) in experimental acute heart failure.

Background: Sulfonylurea drugs, blockers of cardioprotective ATP-sensitive K+ (KATP) channels, may increase the risk of early cardiovascular mortality. In cardiovascular diseases such as acute heart failure, early release of ANP is essential for cardiorenal homeostasis. Although KATP channels regulate secretion of hormones, such as insulin, it is unknown whether sulfonylureas interfere with ANP release in acute heart failure.

Methods: The effects of acute administration of glyburide (0.3 mg/kg), a prototype sulfonylurea, on ANP release and sodium excretion were measured in vivo in a canine model of pacing-induced acute heart failure characterized by acute atrial stretch. Immunoreactivity, in atrial tissue, for ANP and the KATP channel subunit, Kir6.2, was determined using specific antibodies.

Results: With increased left atrial pressure in heart failure, plasma levels of ANP increased rapidly and peaked within 25±3 min. Glyburide delayed the time required for peak plasma ANP secretion to 48±5 min. This resulted in reduced natriuresis from 84±17 µEq/min in the absence of glyburide, to 34±9 µEq/min in the presence of glyburide. However, glyburide did not alter the renal natriuretic responsiveness to exogenously administered ANP in normal dogs. In atrial tissue, both ANP and the KATP channel subunit, Kir6.2, displayed strong immunoreactivity and co-localization.

Conclusions: Glyburide delays release of ANP in acute heart failure resulting in impaired natriuresis. This cannot be ascribed to an antinatriuretic effect on the kidney, but rather may be due to interference with KATP channel-dependent ANP secretion from the atrium. Such adverse outcome of sulfonylurea drug use could reduce the compensatory capacity to preserve cardiorenal homeostasis in acute heart failure.

Key Words: ATP-sensitive K+ channel • Kir6.2 • Cardioprotection • Kidney • Natriuresis • Sulfonylurea

Received August 4, 1999; Accepted December 1, 1999


   1. Introduction
Top
 Notes
 Abstract
 1. Introduction
2. Methods
 3. Results
 4. Discussion
 References
 
In clinical practice, sulfonylurea drugs are the most commonly used oral hypoglycemic agents [1]. Although their therapeutic efficacy is well recognized, there has been renewed concern regarding the safety of these agents [2,3]. This follows previous reports suggesting increased cardiovascular morbidity and mortality associated with sulfonylurea drug use [4], and a recent observation indicating a greater risk for early in-hospital mortality amongst diabetic patients on sulfonylurea drugs undergoing coronary angioplasty for acute myocardial infarction [5].

Sulfonylurea drugs, while promoting release of insulin through blockade of metabolism regulated adenosine triphosphate-sensitive potassium (KATP) channels present in pancreatic β-cells [6], also block KATP channels present in the heart [7,8]. Pancreatic and cardiac KATP channels share a common pore-forming subunit, the inwardly rectifying K+ channel Kir6.2 [9,10], which assembles with tissue-specific regulatory subunits to form functional channels [11–13]. In the heart, KATP channels are believed essential for ischemic preconditioning which can protect the heart from lethal injury [14–20]. More recently, in studies performed in isolated heart, cardiac KATP channels have also been implicated as regulators of release of the atrial natriuretic peptide (ANP) [21,22]. This peptide hormone, of atrial origin, possesses powerful natriuretic properties, which together with vasodilating actions regulate cardiac preload and afterload [23,24]. It is the early release of ANP, induced by atrial stretch [25,26], that contributes to the preservation of myocardial function through maintenance of sodium homeostasis [27,28]. While sulfonylurea drugs have already been shown to abolish cardioprotection afforded by ischemic preconditioning [14,19], it remains unknown whether these hypoglycemic agents can also impede the endocrine function of the heart.

Therefore, in the present study, we investigated the modulating properties of the sulfonylurea, glyburide, on release of ANP and associated natriuresis in an in vivo model of acute heart failure characterized by acute atrial stretch. We report that the prototype sulfonylurea, glyburide, delays stretch-induced release of ANP in acute heart failure, resulting in an impaired renal natriuretic response. Such a side-effect of a sulfonylurea could reduce the endogenous protective potential of the failing myocardium in maintaining optimal cardiorenal homeostasis.


   2. Methods
Top
 Notes
 Abstract
 1. Introduction
 2. Methods
3. Results
 4. Discussion
 References
 
These studies were conducted in accordance with the guidelines of animal care set forth by the American Physiological Society, and with the approval of the Mayo Clinic Animal Care and Use Committee.

2.1. Animals
Experiments were performed with dogs weighing between 17 and 25.5 kg. The day preceding the study, each dog was given 300 mg lithium carbonate orally for assessment of renal tubular function, and was fasted with water allowance until the next morning. On the day of the study, dogs were anesthetized using 30 mg/kg pentobarbital sodium (i.v.) with supplemental doses given as needed. Dogs were intubated with a 9.5-mm endotracheal tube, and mechanically ventilated (Harvard Apparatus, Dover, MA) with supplemental oxygen (10 l/min) at 16 cycles/min.

2.2. Surgical preparation
Surgical preparation began by isolating the right external jugular vein and advancing a 7.5 French balloon-tipped, flow-directed thermodilution catheter (Ohmeda, Madison, WI) into the pulmonary artery to measure pulmonary arterial pressure, left atrial pressure and cardiac output. The right femoral vein and artery were also isolated, and polyethylene catheters were placed for infusion of drugs, arterial blood pressure monitoring, and blood sampling (from the arterial line). A left thoracotomy was performed at the fifth intercostal space, a small incision made into the pericardium, and an epicardial pacing wire placed in the apex of the left ventricle (pulse generator model 5320; Medtronic Corporation, Minneapolis, MN) for ventricular pacing. The left kidney was exposed by flank incision, and the left ureter was cannulated with a polyethylene catheter for urine collection. Renal blood flow was measured by fitting of an electromagnetic flow probe (Carolina Instruments, King, NC) onto the left renal artery. Anesthetized animals were kept in a prone position, over a heating pad at 37°C, for the duration of the experiment.

2.3. Acute heart failure
Following surgical preparation, animals were allowed to equilibrate for 60 min, during which time an inulin infusion was started at 1 ml/min to determine glomerular filtration rate. A 30-min baseline clearance period (BL-1) was then performed, with assessment of cardiovascular and endocrine parameters. These parameters included heart rate, mean arterial blood pressure, pulmonary artery pressure, left atrial pressure, and cardiac output, all measured in triplicate. Blood samples were drawn to measure the endocrine parameters, including ANP and electrolyte levels. Blood glucose was also measured at this time using a glucose meter (Advantage, CA, USA), and a bolus of 15 ml 40% dextrose was administered if blood glucose declined more than 15 units below baseline. Urine was collected to determine urinary electrolytes.

After the 30-min baseline clearance, the vehicle group (n=6) received an intravenous bolus of vehicle (V, 1 ml polyethylene glycol, 1 ml ethanol, 1 ml NaOH and 10 ml normal saline), while the glyburide (GL) group (n=6) received glyburide plus the vehicle. The glyburide dose was chosen at 0.3 mg/kg in order to block cardiac KATP channels without exerting hypertensive effects on the peripheral vasculature reported with higher doses [29]. Following a 15-min lead-in period, a second 30-min baseline clearance (BL-V or BL-GL) was performed, with the same parameters measured as with the first clearance. Rapid ventricular pacing was initiated with a rate set to double left atrial pressure. During the next 60 min, two 30-min clearances were performed, with blood sampling every 15 min. This model of acute heart failure has been utilized in previous reports, and mimics human acute heart failure, with regard to acute left ventricular failure with increase in left atrial pressure, decrease in cardiac output and mean arterial pressure and rapid release of ANP [27,28,30].

2.4. Renal response to exogenous ANP in normal dogs
In order to assess the effect of glyburide on the natriuretic response of exogenous ANP in normal dogs, in a separate set of experiments, we measured sodium excretion at baseline and after administration of exogenous ANP without inducing experimental acute atrial stretch and heart failure. One group of normal dogs (n=5) received vehicle with exogenous ANP infusion (100 ng/kg/min), while another group (n=5) received glyburide (0.3 mg/kg) with vehicle followed by an exogenous ANP infusion (100 ng/kg/min) after 90 min of equilibration. After ANP infusion was started, a 15-min lead-in followed, and cardiovascular and endocrine parameters, as well as urine collection, were assessed for two 30-min clearances (ANP-1 and ANP-2).

2.5. Immunohistochemistry
Sections for immunohistochemical staining were taken from atrial free walls from six normal dogs. Immunohistochemical studies were performed by the previously established indirect immunoperoxidase method. Tissues were fixed with 10% buffered formalin, embedded in paraffin and 6-µm-thick sections were cut and mounted on silanized glass slides. Sections were deparaffinized with graded concentrations of xylene and hydrated with ethanol. To block the activity of endogenous peroxidase, slides were incubated with 0.6% hydrogen peroxide in methanol for 20 min at room temperature. After being washed, sections were incubated in 5% goat serum (Dako, Carpinteria, CA) for 10 min at room temperature to reduce non-specific, background staining, and then incubated with either rabbit anti-ANP (Phoenix, Mountainview, CA) or rabbit anti-rKir 6.2 (courtesy of Dr M. Puceat, Inserm, France) antibodies at a dilution of 1:500 in humidified chambers for 18 h at room temperature. All slides were incubated for 30 min with a second antibody–horseradish peroxidase conjugate (BioSource, Camarillo, CA, USA). The reaction was visualized by incubating the sections with a solution of 3'-amino-9'-ethylcarbazole (Sigma) in dimethylformamide and sodium acetate. The sections were counterstained with hematoxylin, coverslipped and imaged with an Olympus microscope (40x). Control sections were stained with 1% non-immune goat serum.

2.6. Analytical methods
Plasma ANP was measured by a specific radioimmunoassay (RIA) [23]. Blood for hormone analysis was collected in pre-chilled ethylenediaminetetraacetic acid (EDTA) tubes and immediately placed in ice. Following centrifugation at 2500 rev./min at 4°C, plasma was separated and stored at –20°C until assayed. ANP was extracted using a C18 Sep-Pak column. ANP was measured by RIA using antibodies raised against human ANP. Interassay variation was 6%, and cross-reactivity was 100% with canine ANP.

The glomerular filtration rate (GFR) was determined by clearance of inulin, and plasma and urine inulin were measured by the anthrone method. Plasma and urine electrolytes, including lithium, were measured by flame-emission spectrophotometry (IL943 Flame Photometer, Instrumentation Laboratory, Lexington, MA, USA). Using lithium clearance (CLLi), distal fractional reabsorption of sodium (DFRNa) were calculated as follows: DFRNa=(CLLi–CLNa)/CLLix100, where CLLi=(Urine LixUrine Flow)/Plasma Li, and CLNa=(Urine NaxUrine flow)/Plasma Na. Systemic vascular resistance (SVR) was calculated using the equation SVR(RU)=[MAP(mmHg)–RAP(mmHg)/CO(l/min)]. Renal vascular resistance (RVR) was calculated using the equation RVR(RU)=[MAP(mmHg)–RAP(mmHg)/RBF(ml/min)].

2.7. Drugs
Glyburide was obtained from Sigma Chemical Corporation (St. Louis, MO, USA), and 0.3 mg/kg was dissolved in 1 ml of polyethylene glycol, 1 ml ethanol and 1 ml NaOH, and finally diluted with 10 ml saline (vehicle).

2.8. Statistical analysis
Data from each group is expressed as mean±S.E. With each group, comparisons were made using analysis of variance for repeated measures and Fisher’s least significant difference. Comparisons between groups were made using unpaired t-test. Statistical significance was defined at a P-value<0.05.


   3. Results
Top
 Notes
 Abstract
 1. Introduction
 2. Methods
 3. Results
4. Discussion
 References
 
3.1. Basal conditions
In the absence of heart failure, the plasma level of ANP and the urinary sodium excretion are illustrated in Fig. 1. Administration of glyburide (0.3 mg/kg) did not significantly change plasma ANP nor urinary sodium excretion (P>0.05; Fig. 1). In addition, the sulfonylurea did not modify cardiovascular and renal hemodynamics (Table 1).


Figure 1
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  		Fig. 1 Illustrates plasma atrial natriuretic peptide(ANP) and urinary sodium excretion (UNaV) at basal condition in vehicle- and glyburide-treated groups.

 


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  		Table 1 Cardiovascular and renal hemodynamicsa

 
3.2. Acute heart failure
Rapid ventricular pacing induced acute heart failure with a significant decrease in cardiac output from 3.8±0.4 to 2.5±0.1 l/min, and elevation in left atrial pressure from 5.8±0.8 to 11.8±1.5 mmHg (n=6; Table 1). In addition, mean arterial pressure decreased, while systemic vascular resistance increased (Table 1). With development of acute heart failure, there was a marked increase in plasma ANP with levels reaching 195±76 pg/ml in the vehicle group which was similar to the glyburide group which reached 170±70 pg/ml. The sulfonylurea, however, prolonged the time required to achieve the peak ANP plasma levels. Compared to 25±3 min in the vehicle group, in the glyburide-treated group peak plasma ANP levels were only reached after 48±5 min (Fig. 2). This delayed ANP release resulted in a significantly lower urinary sodium excretion in the glyburide-treated group, as urinary sodium excretion was 84±17 µEq/min in the vehicle group as compared to 34±9 mEq/min in the glyburide group (P<0.01; Fig. 3). Moreover, treatment with glyburide was associated with an increased the fraction of sodium reabsorbed in the distal tubule (Fig. 3), the primary site of action of ANP. Treatment with 0.3 mg/kg glyburide did not alter cardiovascular and renal hemodynamic values (Table 1).


Figure 2
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  		Fig. 2 Illustrates peak plasma atrial natriuretic peptide (ANP) levels and time taken to achieve peak plasma ANP levels in both vehicle- and glyburide-treated groups during acute heart failure. *P<0.05 vs. vehicle group.

 


Figure 3
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  		Fig. 3 Illustrates urinary sodium excretion (UNaV) and distal fractional sodium reabsorption in both vehicle- and glyburide-treated groups during acute heart failure. *P<0.05 vs. vehicle group.

 
3.3. Renal response to exogenous ANP
To exclude an anti-natriuretic effect of glyburide upon the kidney, we administered exogenous ANP to two groups of normal dogs which were treated with either vehicle or glyburide (0.3 mg/kg). In response to exogenous ANP (100 ng/kg/min), urinary sodium excretion increased in both groups (Fig. 4). In fact, there was a trend for a greater natriuretic response in the presence of glyburide than in the vehicle group. Thus, glyburide does not exhibit a direct anti-natriuretic effect.


Figure 4
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  		Fig. 4 Illustrates urinary sodium excretion (UNaV) in both vehicle- and glyburide-treated groups at baseline (BL) and during atrial natriuretic peptides infusion (ANP-1 and ANP-2). *P<0.05 vs. baseline (BL).

 
3.4. Co-immunoreactivity of ANP and KATP channels in the atrium
Using epitope-specific antibodies raised against the C-terminus of ANP or the N-terminus of the pore-forming Kir6.2 KATP channel protein, we immunostained slices of atrial myocardium. Immunohistochemistry revealed a widely positive immunostaining pattern for both ANP and the KATP channel subunit throughout the atrial myocardium (Fig. 5).


Figure 5
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  		Fig. 5 Illustrates the immunochemistry with atrial natriuretic peptide (ANP) antibody, Kir6.2 antibody and non-immune goat serum in canine atrial tissue.

 

   4. Discussion
Top
 Notes
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
References
 
This report provides first evidence for a sulfonylurea-induced impairment of ANP release resulting in a deficient natriuretic response in the setting of acute experimental heart failure. Such an effect was demonstrated in vivo using the sulfonylurea prototype, glyburide, which delayed stretch-activated ANP release and blunted sodium excretion when administered acutely in a pacing model of acute atrial stretch and heart failure. Since early atrial release of ANP is a protective humoral response by the heart to limit the increase in preload and prevent ventricular overload [27], the present finding indicates a possible adverse outcome of sulfonylurea drug use by reducing this compensatory endocrine capacity of the heart to preserve cardiorenal homeostasis under this acute experimental condition.

Prior indication that sulfonylurea drugs may have adverse consequences came from epidemiological studies which found increased cardiovascular morbidity and mortality in certain patient populations taking these agents [4,5]. Experimentally, sulfonylurea drug use has been associated with the increase in infarct size, accelerated death of hypoxic cardiomyocytes, prevention of coronary vasodilatation in response to ischemia, and inhibition of the endogenous fibrinolytic system [14,31,32]. In this regard, the present study identifies a previously unrecognized adverse action of sulfonylurea drugs on the endocrine function of the heart resulting in impaired ANP-dependent cardiorenal compensatory mechanisms.

Previously, conditions associated with impaired responsiveness to ANP through blockade of natriuretic peptide receptors or genetic disruption of such receptors, have all produced an inability for the kidney to respond to an acute increase in plasma ANP in response to volume expansion or acute heart failure [27,33]. Here we found that during acute experimental heart failure, administration of glyburide significantly delayed the rapid increase in peak plasma ANP levels and reduced renal sodium excretion. Such attenuated renal natriuretic response was linked to a lack of decrease in distal tubule reabsorption, a nephron site rich in ANP receptors [34]. Thus, the impaired ANP response to acute atrial stretch was associated with a parallel delay in renal sodium handling at a nephron site known to be the renal target for ANP. At least in principle, the mechanism of such altered renal response could have been due to a direct action of glyburide on the kidney itself. This is, however, unlikely since the sulfonylurea drug did not interfere with basal plasma ANP levels and sodium excretion in the absence of acute heart failure or with the renal natriuretic response to exogenous ANP. Indeed, there was a trend toward enhancing the renal response to exogenous ANP in line with previous reports of possible natriuretic properties of glyburide-related compounds [35]. Therefore, we conclude that the sulfonylurea did not directly attenuate ANP-induced natriuresis, but rather interfered with the early release of ANP.

In acute heart failure, the primary site of ANP release is the left atrium [24,25]. In accord with previous reports, we also here find a high accumulation of ANP immunoreactivity within left atrial tissue. Importantly, atrial tissue also displayed high immunoreactivity for the pore-forming subunit of the KATP channel, Kir6.2, suggesting a high density of this channel population in the atrium. Although atrial KATP channels have not been fully characterized, it is known that these ion conductances are highly sensitive to sulfonylurea drugs, such as glyburide, and can be further gated by mechanosensitive stimuli, including stretch [36]. Thus, it is conceivable that glyburide may have interfered with ANP release by interacting with atrial KATP channels. This is supported by the general function of KATP channels which regulate hormone secretion in a number of tissues including pancreatic β-cells and the brain, and the more recent finding that KATP channels may also control release of ANP from isolated atrial preparations [21,22]. Our study provides further support for the endocrine role of this channel in the regulation of release of the biologically active peptide ANP, in vivo, under conditions of acute experimental heart failure.

In conclusion, the current studies report the effect of the sulfonylurea, glyburide, a KATP channel antagonist, on circulating ANP and urinary sodium excretion in an experimental model of acute heart failure. The finding, that glyburide delayed the peak increase in plasma ANP levels, resulting in an attenuated renal natriuretic response, provides new insight into the pharmacology of this commonly used hypoglycemic agent under conditions of simulated acute heart failure. These findings clearly warrant further clinical evaluation of sulfonylurea drugs with regard to ANP release and renal response, particularly in the setting of chronic congestive heart failure and diabetes.


   Acknowledgements
 
The authors gratefully acknowledge the technical assistance provided by Sharon M. Sandberg, Denise M. Heublein, and Gail Harty. This work was supported by grants from the American Heart Association, the National Institute of Health (HL 36634), National Kidney Foundation of the Upper Midwest, the Miami Heart Research Institute, the Bruce and Ruth Rappaport Program in Vascular Biology and Gene Delivery, and the General Mills Clinician-Investigator Program at the Mayo Foundation.


   Notes
Top
 Notes
Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 References
 
1 Karen Y. Oh is currently at LDS Hospital, Salt Lake City, UT, USA. Back


   References
Top
 Notes
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 References
 

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