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Bradykinin B2 Receptor Modulates Renal Prostaglandin E2 and Nitric Oxide

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Bradykinin B2 Receptor Modulates Renal Prostaglandin E2 and Nitric Oxide (Hypertension. 1997;29:757-762.) © 1997 American Heart Association, Inc. Bradykinin B2 Receptor Modulates Renal Prostaglandin E2 and Nitric Oxide Helmy M. Siragy; Ayad A. Jaffa; Harry S. Margolius the Department of Internal Medicine, University of Virginia Health Sciences Center, Charlottesville, and the Departments of Pharmacology and Medicine, Medical University of South Carolina and Ralph A. Johnson VA Medical Center, Charleston. Correspondence to Helmy M. Siragy, MD, Department of Medicine, Box 482, University of Virginia Health Sciences Center, Charlottesville, VA 22908. ABSTRACT Bradykinin and lys-bradykinin generated intrarenally appear to be important renal paracrine hormones. However, the renal effects of endogenously generated bradykinin are still not clearly defined. In this study, we measured acute changes in renal excretory and hemodynamic functions and renal cortical interstitial fluid levels of bradykinin, prostaglandin E2, and cGMP in response to an acute intrarenal arterial infusion of the bradykinin B2 receptor antagonist Hoe 140 (icatibant), cyclooxygenase inhibitor indomethacin, or nitric oxide synthase inhibitor NG-monomethyl-L-arginine (L-NMMA) given individually or combined in uninephrectomized, conscious dogs (n=10) in low sodium balance. Icatibant caused a significant decrease in urine flow, urinary sodium excretion, and renal plasma flow rate (each P<.001). Glomerular filtration rate did not change during icatibant administration. Icatibant produced an unexpected large increase in renal interstitial fluid bradykinin (P<.0001) while decreasing renal interstitial fluid prostaglandin E2 and cGMP (each P<.001). Both indomethacin and L-NMMA when given individually caused significant antidiuresis and antinatriuresis and decreased renal blood flow (each P<.001). Glomerular filtration rate decreased during L-NMMA administration (P<.001) and did not change during indomethacin administration. Combined administration of icatibant and indomethacin or L-NMMA caused significant decreases in renal excretory and hemodynamic functions, which were not different from changes observed with icatibant alone. The failure of icatibant to change renal function after inhibition of cyclooxygenase and nitric oxide synthase activity suggests that the effects of kinin B2 receptor are mediated by intrarenal prostaglandin E2 and nitric oxide generation. The increase in renal interstitial fluid bradykinin during icatibant requires further study of possible alterations in kinin synthesis, degradation, or clearance as a result of B2 receptor blockade. Key Words: bradykinin • interstitium • sodium • kidney • microdialysis • cyclic GMP • prostaglandin E2 INTRODUCTION Considerable evidence now suggests that the renal kallikrein-kinin system is involved in the regulation of sodium and water excretion and may participate in blood pressure control. Kinins can stimulate production of both NO and eicosanoids.1 2 At least a portion of the renal effects of kinins appears to be mediated by prostaglandins,3 and inhibition of NO synthesis reduces the renal vasodilator response to bradykinin.4 In previous studies, intrarenal infusions of bradykinin in anesthetized dogs resulted in an increase in RPF and 5 6 UNaV. However, the biochemical and physiological effects of exogenously administered kinins may differ from those of endogenously formed kinins.7 Administration of Fab fragments of kinin antibodies, bradykinin antagonist,8 and Fab fragments of monoclonal antibodies to rat urinary kallikrein (Fab-kallikrein)9 decreased UV, UNaV, and PGE2 excretion in rats. The purpose of the present study was to investigate the effects of kinin B2 receptor blockade on intrarenal levels of bradykinin, PGE2, and cGMP, an indirect measure of NO generation. Because previous studies showed that urinary10 and renal interstitial11 kinins increase in response to sodium depletion, we carried out our studies in conscious dogs in sodium metabolic balance at 5 12 13 mEq/d. We used a potent and specific bradykinin B2 receptor antagonist, D-Arg-Arg- Pro-Hyp-Gly-Thi-Ser-L-Tic-Oic-Arg (Hoe 140, icatibant) (Hoechst AG), to begin to evaluate the role of intrarenal bradykinin and this receptor in the regulation of renal levels of PGE2 and NO in conscious, uninephrectomized dogs. METHODS Renal Microdialysis Technique For the determination of RIF kinin, PGE2, and cGMP, we constructed a microdialysis probe as previously described.11 14 15 Each end of a 1-cm-long hollow fiber dialysis tube (0.3 mm ID; molecular mass cutoff, 10 000 D; Hospal) was inserted into a manually dilated end of two 30-cm-long (inflow and outflow) hollow polyethylene tubes (0.12 mm ID, 0.65 mm OD; Bioanalytical Systems). The distance between the ends of the polyethylene tubes was 3 mm (dialysis area), and the dialysis fiber was sealed in place within the polyethylene tubes with cyanoacrylic glue. The dead volume of the dialysis tubing and outflow tube was 3.6 µL. The known kinin-, eicosanoid-, and NO-generating and -degrading enzymes (molecular weights, 34 000 to 150 000) will not cross the dialysis membrane because of their size. The microdialysis probe was sterilized by a gas sterilization method. Animal Preparation and RIF Collection The study protocol was approved by the University of Virginia Animal Research Committee. All studies were carried out in conscious animals to avoid disturbances in renal hormones and function induced by anesthesia.16 Ten female mongrel dogs weighing 15 to 20 kg (mean±SE, 18±0.89 kg) were used in this study. Surgery with dogs under halothane anesthesia was performed as described previously for cannula insertion into the right renal artery, aorta, and inferior vena cava.17 An ultrasonic flow probe (Transonic Systems) was placed around the right renal artery18 for measurement of renal blood flow. A left nephrectomy was performed to eliminate renal compensation and avoid ureteral catheterization in conscious dogs. All cannulas and the wires for the right renal flow probe were tunneled subcutaneously through a bevel-tipped stainless steel tube and exteriorized in separate small stab wounds near the interscapular region. For placement of the microdialysis probe, the right renal capsule was penetrated with an 18-gauge needle that was tunneled under the capsule for 2 cm before exiting again. One end of the dialysis probe then was pulled through the needle until the dialysis fiber was situated in the outer renal cortex about 2 mm from the kidney surface. The needle then was withdrawn. The two ends of the dialysis probe (inflow and outflow tubes) were tunneled under the skin and exited near the interscapular region. The exterior ends of the vascular cannulas and microdialysis probe were protected in the pocket of a close-fitting nylon jacket (Alice King Chatham). In an earlier study,15 a histological examination of the renal tissue 6 weeks after insertion of the dialysis probe did not show any significant fibrosis or scarring. Three weeks was allowed for recovery after surgery. General Animal Care Prevention of clot formation inside the cannulas was ensured by daily flushing with 3 mL of 10% heparin solution (Elkins Sinn). Cannulas also were flushed after each withdrawal of blood or hemodynamic measurement. As a prophylactic measure, antibiotic treatment with 250 mg ampicillin IM (Wyeth-Ayerst Laboratories) twice daily was started immediately after surgery and continued for 7 days. Body temperatures were measured twice daily during the first week after surgery and twice weekly thereafter. Blood urea nitrogen and serum creatinine levels were determined twice weekly (Serometer model 370, Mallinckrodt). Dogs were excluded from the study in the event of elevated temperature or abnormalities (blood urea nitrogen >20 mg/dL, creatinine >1.5 mg/dL) in these tests. Hematocrit levels were 41% to 46% (mean±SE, 43.6±0.87%) and 41% to 45% (42.6±0.82%) before surgery and on the day of the acute study, respectively. Hemodynamic Measurements Systemic arterial pressure was monitored continuously during the acute study from the aortic cannula with a Statham P23 DB pressure transducer and Gould 2400 recorder, as previously described.17 Mean arterial blood pressure was calculated as the mean of three recordings lasting 15 seconds each and taken at 2-minute intervals at the middle of the control and icatibant infusion periods. Analytic Methods Urinary sodium concentrations were measured by an autoanalyzer (NOVA-1, NOVA Biomedical). Venous blood samples (1 mL) for aldosterone measurements were collected at the middle of each experimental period in glass tubes coated with lithium heparin. Peripheral PAC was measured by a Coat-a-Count radioimmunoassay kit (Diagnostic Products). Peripheral venous blood (1 mL) for the determination of PRA was collected at the middle of each experimental period in tubes that contained EDTA (4°C), and plasma was separated after centrifugation and stored at -70°C. Peripheral PRA was measured by radioimmunoassay of angiotensin I generation after 3 hours of incubation19 with reagents obtained from New England Nuclear. RIF kinin, PGE2, and cGMP samples were stored at -20°C until they were measured by radioimmunoassays.20 21 22 Sodium and Fluid Balance Sodium metabolic balance was established in all dogs by placing each dog on a palatable diet containing 5 mmol sodium/d (Hills' H/D) for 15 days. All dogs were in low sodium balance for 10 days before study. The rationale for use of the low sodium diet is provided by our previous study15 which showed that this diet increases renal interstitial
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