Alpha-1 Adrenergic Receptors on Rabbit Retinal Pigment Epithelium

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1 Investigative Ophthalmology & Visual Science, Vol. 29, No. 5, May 1988 Copyright Association for Research in Vision and Ophthalmology Alpha-1 Adrenergic Receptors on Rabbit Retinal Pigment Epithelium Donald A. Frambach,*t John L. Valentine,* and John J. Weirer*f Retinal pigment epithelium (RPE)-choroid-sclera preparations from black, dutch-belted rabbits were sealed in an Ussing chamber. The RPE-generated trans-rpe voltage (V c ) and electrical resistance (R) were monitored. Epinephrine (an alpha and beta adrenergic agonist) reduced V e by as much as 39% without affecting R. A response to epinephrine was noted at concentrations as low as 1.4 X 10~ 7 M. Phenylephrine (an alpha adrenergic agonist) had essentially the same effect as epinephrine at identical concentrations. Clonidine (an alpha-2 adrenergic agonist) had a very slight effect but only at 10~ 4 M. Isoproterenol (a beta adrenergic agonist) had no apparent effect upon V c or R. The RPE response to epinephrine and phenylephrine was blocked by the alpha adrenergic antagonist phentolamine and by the alpha-1 adrenergic antagonist prazosin but not by the alpha-2 adrenergic antagonist yohimbine or by the beta adrenergic antagonist propranolol. Dibutyryl cyclic AMP (in the presence and absence of IBMX) and cyclic GMP (as cgmp and in the dibutyryl form) had no apparent effect upon V e or R. These results indicate that rabbit RPE possesses an alpha-1 adrenoreceptor which, when stimulated, substantially reduces the RPE generated trans-rpe electrical current. Invest Ophthalmol Vis Sci 29: ,1988 The retinal pigment epithelium (RPE) is an epithelial layer that lies between the photoreceptors and the rich blood supply of the choriocapillaris. An important role of the RPE is to maintain the appropriate extracellular environment in the outer retina necessary for normal photoreceptor function. 1 The transepithelial transport properties of the RPE have been studied in vitro in several laboratories. 2 " 4 In addition to determining the components of RPE active transport, it has been important to understand how this transport is regulated. Cyclic AMP (camp) has been reported to slow bullfrog RPE-mediated fluid movement 5 and ion transport 6 in vitro. In vivo rabbit experiments have suggested that camp slows RPE-mediated fluid movement while cyclic GMP (cgmp) accelerates this fluid movement. 7 We have recently developed an in vitro rabbit RPE-choroid-sclera preparation that is well suited for studying the effects of pharmacologic agents (applied to the RPE apical membrane) on RPE-generated trans-rpe electrical current. 8 This electrical current, more commonly called the "short circuit current" (I sc ), has been related to RPE transport in several spe- From the *Eye Research Institute of Retina Foundation and the fmassachusetts Eye and Ear Infirmary, Boston, Massachusetts. Presented in part at the May 1987 meeting of the Association for Research in Vision and Ophthalmology, Sarasota, Florida. Supported by NIH Grant EY-05422, Bethesda, Maryland. Submitted for publication: April 9, 1987; accepted December 14, Reprint requests: Donald Frambach, MD, Estelle Doheny Eye Institute, 1355 San Pablo Street, Los Angeles, CA cies. 2 6 Since RPE-mediated fluid movement in rabbits is dependent upon active transport, 9 it seemed important to determine the effects of camp and cgmp on rabbit RPE I sc. Three of the four known adrenergic receptor types use camp as their "second messenger." 10 Therefore, we also sought to determine whether rabbit RPE possesses adrenergic receptors that might modify intracellular cyclic nucleotide levels and serve in vivo as regulators of RPE transport. The experiments described herein show that dibutyryl camp (in the presence and absence of IBMX) and cgmp (as cgmp and in the dibutyryl form) do not affect I sc. However, the experiments do show that rabbit RPE possesses an alpha-1 adrenoreceptor that, when stimulated, substantially reduces the RPE-generated trans-rpe electrical current. Materials and Methods Rabbit retinal pigment epithelium (RPE)-choroidsclera explants were sealed within an Ussing chamber using techniques that we have previously described. 8 We have adhered to the principles of the ARVO Resolution on the Use of Animals in Research. Briefly, black dutch-belted rabbits were anesthetized with xylazine (27 mg/kg IM, Rompun, Miles Laboratories, Elkhart, IN) and ketamine (130 mg/kg IM, Vetalar, Parke-Davis, Morris Plains, NJ)." For one set of experiments, pentobarbital (36 mg/kg subcutaneously) was used instead of xylazine. 9 The retina was separated from the RPE by making total retinal detachments in vivo using a technique previously described. 12 Pupillary dilation (required to make the 737

2 738 INVESTIGATIVE OPHTHALMOLOGY b VISUAL SCIENCE / May 1988 Vol mv , EPINEPHRINE Fig. 1. Epinephrine at 1.4 X 10 4 reduced the short circuit current (Isc) of preparations by 39%. Epinephrine has both alpha and beta adrenergic activity. retinal detachments) was obtained with one drop of 1% cyclopentolate (AK-Pentolate, Akorn Inc., Abita Springs, LA). The rabbits' eyes were then enucleated and RPE-choroid-sclera explants were obtained and sealed in an acrylic chamber such that the explants separated two otherwise electrically isolated saline solutions. Electronics within the chamber allowed us to measure the spontaneous transepithelial voltage (V e ) and electrical resistance (R) of the preparations. The RPE-generated trans-rpe electrical current or "short circuit current" (I sc ) was calculated from V e and R using Ohm's Law. Previous work with these preparations has shown that all of the V e and essentially all of the R can be attributed to the RPE. 8 The bathing media consisted of (in millimoles per liter): 143 Na, 3.6 K, 1.2 Ca, 2.5 Mg, 125 Cl, jja/cm mv 600 n EPINEPHRINE-DOSE RESPONSE epinephrine (1.4 x 10" 7 M) t epinephrine epinephrine epinephrine (1.4 X 10" 6 M) (1.4 X lct 5 M) (1.4 X lo- 1 M) Fig. 2. Epinephrine at 1.4 X 10~ 7 M reduced the RPE I^ which then recovered spontaneously without washout. This was also noted when epinephrine was applied at 1.4 X 10~ 6 M and then at 1.4 X 10~ 5 M. When epinephrine was applied at 1.4 X 10~" 4 M, the Isc fell and did not recover. HCO 3, 2.5 SO 4,0.5 PO 4, 10 glucose. Water-saturated 5% CO 2-95% O 2 was bubbled into each side of the chamber to provide mixing and to maintain a ph of 7.4 (±0.1). The chamber was surrounded by a water jacket and kept at C. The pharmacologic agents employed in these experiments were epinephrine, phenylephrine, clonidine, isoproterenol, propranolol, phentolamine, yohimbine, prazosin, N 6,2'-O-dibutyryladenosine 3': 5'-cyclic monophosphate (dibutyryl camp), N 2,2'-Odibutyrylguanosine 3':5'-cyclic monophosphate (dibutyryl cgmp), guanosine 3':5'-cyclic monophosphate (cgmp), and 3-isobutyl-l-methyl-xanthine (IBMX). Except for isoproterenol (Elkins-Sinn, Cherry Hill, NJ), phentolamine (Regitine IV, CIBA, Inc., Summit, NJ), propranolol (Inderal IV, Ayerst, New York, NY), and prazosin (Minipress,Pfizer, New York, NY), these agents were obtained from Sigma Chemical Co. (St. Louis, MO). Experiments consisted of sealing the RPE-choroidsclera explants within the Ussing chamber and taking baseline measurements. The desired drug, typically in 100 jul volumes, was then injected into one (or both) sides of the chamber and its effect upon V e, R, and I sc determined. Except where specifically noted, agents were added to both sides of the preparation. Results Typical RPE-choroid-sclera preparations produced a spontaneous transepithelial voltage (V e ) of 12.5 mv (apical side positive) and an electrical resistance (R) of 350 that gradually fell during the course of the experiments. RPE-choroid-sclera preparations typically lose V e and R with time, 48 presumably because the conditions in the Ussing chamber do not perfectly replicate the in vivo state as a consequence of which the preparations deteriorate. When epinephrine, an adrenergic agonist with both alpha and beta activity, 13 was added to both sides of the preparation, there was a marked fall in V e and calculated short circuit current (I sc ) with no effect upon R. At epinephrine concentrations of 1.4 X 10" 4 M, I sc fell by 39% (±6% SD, n = 5). A typical experiment is illustrated in Figure 1. When lower concentrations of epinephrine were used, there were smaller reductions in V e and I sc with no apparent effect upon R. At epinephrine concentrations less than 10~ 4 M, the V e and I sc spontaneously recovered even though the epinephrine was not washed out of the chamber. This occasionally occurred when the epinephrine concentration exceeded 10~ 4 M. Figure 2 shows a typical response of the RPE to increasing epinephrine concentrations ranging from 1.4 X 10" 7 M to 1.4 X 1O~ 4 M. Epinephrine was also effective when applied to only the apical side of the RPE (n = 3) but there was no apparent effect when epinephrine was

3 No. 5 ALPHA-1 ADRENORECEPTORS ON RABBIT RPE / Fromboch er ol mv _ PROPRANOLOL mv _. PHENYLEPHRINE phenylephrine (1.4 x 10"* M) epinephrine (i.4 x 10" 1 M) t Isc 300 _ 355 -, ^^* tm *"^tmsnim II IIJJiLLl^ Ve R Fig. 3. Propranolol (a beta adrenergic antagonist) did not block the effect of epinephrine Fig. 4. Phenylephrine (an alpha adrenergic agonist) produced a RPE response that was similar to that seen with epinephrine. 20 applied to only the scleral side of the preparation (n = 3). When isoproterenol, an agent with predominantly beta adrenergic agonist activity, was added to both sides of the preparation, there was no apparent response at concentrations of 2.5 X 10~ 5 M (n = 3). To confirm this lack of beta adrenergic activity, the RPE preparations were incubated in 10~ 4 M propranolol, a potent beta adrenergic antagonist, and then exposed to epinephrine. The fall in I sc in response to epinephrine in these preparations incubated in propranolol (40% ± 8% SD, n = 3) was essentially identical to that noted when tissues were exposed to epinephrine without propranolol. Figure 3 shows an experiment where propranolol did not block the epinephrine response. When the preparations were exposed to phenylephrine, an adrenergic agent with predominantly alpha agonist activity, 14 the responses were similar to those seen with epinephrine. After exposure to phenylephrine, further stimulation with epinephrine produced only a small change in V e and I sc (Fig. 4). At 1.4 X 10" 4 M, the average fall in I sc was 32% (±10% SD, n = 4). Clonidine, an adrenergic agent with predominantly alpha-2 agonist activity, 14 had very little effect upon the preparations. Clonidine concentrations of 10~ 4 M were necessary before an effect could be seen. Since xylazine, the agent used to anesthetize the rabbits, has alpha-2 adrenergic agonist activity, 14 it was possible that this anesthesia could have prestimulated RPE alpha-2 adrenoreceptors. Consequently, three clonidine experiments were performed under the pentobarbital and ketamine anesthesia used in earlier experiments. 9 With pentobarbital substituted for xylazine, there could be no prestimulation of alpha-2 adrenoreceptors. Figure 5 shows a typical clonidine experiment where pentobarbital and ketamine rather than xylazine and ketamine were used for anesthesia. There was no apparent difference in responses to clonidine when xylazine was used for anesthesia (n = 3) and when xylazine was not used (n = 3). The effect of epinephrine was completely blocked by 10~ 3 M phentolamine, a potent alpha adrenergic antagonist 14 (n = 3). Figure 6 shows a typical experiment where phentolamine completely blocked the effect of 10~ 4 M epinephrine. Yohimbine, an adrenergic agent with predominantly alpha-2 antagonist activity, 1415 at 10" 4 M did not affect the RPE response to 10~ 4 M epinephrine (n = 3). This is illustrated in Figure 7. Prazosin, an alpha-1 adrenergic antagonist, 14 at 10~ 5 M markedly attenuated the RPE response to epinephrine (n = 10) and to phenylephrine (n = 7). Figure 8 shows the RPE response to epinephrine blocked by prazosin. Dibutyryl camp at 10~ 3 M had no apparent effect 29.5 jia/cm mv 490 CLONIDINE-DOSE RESPONSE clonidine clonidine clonidine epinephrine (10-6 M) (10" 5 M) (10-* M) (1.1 x lo" 4 M) 1L t t Fig. 5. Clonidine (an alpha-2 adrenergic agonist) produced a RPE response only in high concentrations.

4 740 INVESTIGATIVE OPHTHALMOLOGY b VISUAL SCIENCE / May 1988 Vol. 29 PHENTOLAMINE PRAZOSIN 32.0 )ja/cm 2 phentolamine epinephrine (1(H M) (1.4 x 10-'' M) 30.0 jja/cm 2 prazosin epinephrine epinephrine do' 5 M) (1.4 x lo' 5 M) (1.4 x 10" 4 M) 10.0 mv 13.0 mv _ , 4 6 Fig. 6. Phentolamine (an alpha adrenergic antagonist) blocked the RPE response to epinephrine. upon the preparations (n = 3). A typical run is illustrated in Figure 9. IBMX (5 X 10~ 4 M) had no apparent effect (n = 3). Dibutyryl camp (10" 3 M) had no apparent effect upon preparations pretreated with IBMX (n = 3). Cyclic GMP [both in dibutyryl form, 1CT 3 M (n = 3), and as cgmp 10" 4 M (n = 3)] also had no effect upon the preparations. Discussion The results of these experiments clearly indicate that the retinal pigment epithelium (RPE) of rabbits has a receptor for epinephrine that can influence RPE-generated trans-rpe electrical currents. Epinephrine has both alpha and beta adrenergic activity 13 and 1.4 X 10~ 4 M epinephrine reduced the calculated short circuit current (I sc ) by 39%. Epinephrine was effective only when applied to the apical side of the RPE. This, however, is only weak Fig. 8. Prazosin (an alpha-1 adrenergic antagonist) blocked the RPE response to epinephrine and to phenylephrine. evidence that the epinephrine receptors are localized to the RPE apical membrane because the intact choroid and sclera may have prevented epinephrine applied to the scleral side of the preparation from reaching the RPE basolateral membrane. It was interesting to note that the RPE recovered from the effects of lower concentrations of epinephrine even though the epinephrine was not removed from the chamber (Fig. 2). There are at least two possible explanations for this. First, epinephrine is quickly innactivated by oxygenation 16 and may simply have become oxidized by the 95% O 2 that we bubbled through the chamber. Second, the RPE may have internalized the epinephrine receptors 17 or in some other way the receptors may have become less responsive to epinephrine. 18 The epinephrine receptor clearly is not a beta adrenergic receptor because it is neither stimulated by the beta adrenergic agonist, isoproteronol, nor YOHIMBINE DIBUTYRYL camp 20.0 ia/cm 2 yohimbine epinephrine do" 4 M) (1.4 x 10" 4 M) 30.0 dibutyryl camp (10- J M) 12.0 mv mv , 450 _, Fig. 7. Yohimbine (an alpha-2 adrenergic antagonist) failed to block the RPE response to epinephrine Fig. 9. Cyclic AMP at 10~ 3 M did not affect RPE electrical activity.

5 No. 5 ALPHA-1 ADRENORECEPTORS ON RABBIT RPE / Fromboch er ol. 741 blocked by the beta adrenergic antagonist, propranolol. It is possible that the isoproterenol concentration (2.5 X 10" 5 M) was not sufficiently high to rule out the presence of a beta adrenoreceptor. However, were a beta adrenoreceptor present, at least a portion of the epinephrine response should have been blocked by propranolol. Furthermore, the RPE responded to phenylephrine, an alpha adrenergic agonist, in essentially the same way it responded to epinephrine. Since phenylephrine has predominantly alpha-1 adrenergic activity, 14 this suggests that the epinephrine receptor is an alpha-1 adrenoreceptor. The experiments where clonidine, an alpha-2 adrenergic agonist, 14 failed to affect RPE electrical activity except in high concentrations support this hypothesis. (At these high concentrations, clonidine presumably acted as both an alpha-2 and an alpha-1 adrenergic agonist.) Phentolamine blocks both alpha-1 and alpha-2 adrenoreceptors 14 and completely blocked the RPE response to epinephrine. Yohimbine, an alpha-2 adrenergic antagonist, 1415 appeared to have no effect upon the RPE response to epinephrine. Prazosin (an alpha-1 adrenergic antagonist) 14 blocked the RPE response to epinephrine and to phenylephrine. These experiments with alpha adrenergic antagonists confirm that the RPE epinephrine receptor is the alpha-1 subtype. The "second messenger" for alpha-1 adrenoreceptor responses appears to be intracellular calcium and, in many cases, increased phosphoinositol hydrolysj s io.i9.2o j n con t ras t the "second messenger" for alpha-2 adrenoreceptors and for both beta-1 and beta-2 adrenoreceptors is cyclic AMP. 10 It has been reported that exogenously applied cyclic AMP and promoters of intracellular cyclic AMP formation decrease bullfrog RPE-mediated fluid movement 5 and ion transport. 6 Bullfrog RPE-mediated fluid movement is thought to occur via an active transport process. 21 Cyclic AMP has also been reported to slow (and cyclic GMP accelerate) resorption of fluid from the subretinal space in rabbits 7 which is dependent upon RPE active transport process. 9 We could detect no effect of exogenously applied dibutyryl camp (in the presence or absence of IBMX) or cyclic GMP (as cgmp or in the dibutyryl form) on I sc. It appears that the alpha-1 receptor that we have identified acts independently of cyclic AMP, as has been reported for alpha-1 adrenoreceptors from other tissues Further work is required to understand the biologic effect and significance of this alpha-1 adrenoreceptor on rabbit RPE. If a similar receptor is present on human RPE, it may have important therapeutic implications. Key words: alpha-1 adrenoreceptor, epinephrine, prazosin, rabbit, retinal pigment epithelium Acknowledgments Prazosin was generously supplied by Pfizer, Inc. (New York, NY). References 1. Cunha-Vaz JG (editor): The Blood-Retinal Barriers. New York. Plenum Press, Miller SS and Steinberg RH: Active transport of ions across frog retinal pigment epithelium. Exp Eye Res 25:235, DiMattio J, Degan K.J, and Zadunaisky JA: A model for transepithelial ion transport across isolated retinal pigment epithelium of the frog. Exp Eye Res 37:409, Frambach DA and Misfeldt DS: Furosemide-sensitive Cl transport in embryonic chicken retinal pigment epithelium. Am J Physiol 244:F679, Miller SS, Hughes BA, and Machen TA: Fluid transport across retinal pigment epithelium is inhibited by cyclic AMP. Proc Natl Acad Sci USA 79:2111, Hughes BA, Miller SS, and Machen TA: Effects of cyclic AMP on fluid absorption and ion transport across frog retinal pigment epithelium. J Gen Physiol 83:875, Marmor MF and Negi A: Pharmacologic modification of subretinal fluid resorption in the rabbit eye. Arch Ophthalmol 104:1674, Frambach DA, Valentine JL, and Wciter JJ: Initial observations of rabbit retinal pigment epithelium-choroid-sclera preparations. Invest Ophthalmol Vis Sci 29:XXX, Frambach DA and Marmor MF: The rate and route of fluid resorption from the subretinal space of the rabbit. Invest Ophthalmol Vis Sci 22:292, Motulsky HJ and Insel PA: Adrenergic receptors in man: Direct identification, physiologic regulation, and clinical alterations. N Engl J Mcd 307: Boles SF, Frambach DA, Gargano DA, and Wciter JJ: Xylazine/ketamine anesthesia in rabbits. ARVO Abstracts. Invest Ophthalmol Vis Sci 27(Suppl):356, Marmor MF, Abdul-Rahim AS, and Cohen DS: The effect of metabolic inhibitors on retinal adhesion and subretinal fluid resorption. Invest Ophthalmol Vis Sci 19:893, Ahlquist RP: A study of the adrenotropic receptors. Am J Physiol 153:586, Wikbert JE: The pharmacologic classification of adrenergic alpha-1 and alpha-2 receptors and their mechanisms of action. Acta Physiol Scand 468(Suppl):4, Goldberg MR and Robertson D: Yohimbine: A pharmacologic probe for the study of the alpha-2-adrenoreccptor. Pharmacol Rev 35:143, Windholz M (editor): The Merck Index. Rahway, New Jersey, Merck and Co., 1983, pp Brandt JD, Bartels SP, and Neufeld AH: Adrcncrgic stimulation of ciliary process epithelium causes surface membrane internalization. Invest Ophthalmol Vis Sci 28:431, Harden TK: Agonist-induced desensitization of the betaadrenergic receptor-linked adenylate cyclase. Pharmacol Rev 35:5, Mitchell RH: Inositol lipid breakdown as a step in alphaadrenergic stimulus-response coupling. Clin Sci 68(Suppl 10):43s, Reinhart PH, Taylor WM, and Bygrave FL: The role of calcium ions in the mechanism of action of alpha-adrenergic agonists in rat liver. Biochem J 223:1, Frambach DA, Weiter JJ, Adler AJ: A photogrammetric method to measure fluid movement across isolated frog retinal pigment epithelium. Biophys J 47:547, 1985.

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