Hydrogen Peroxide-Mediated Corneol Endothelial Damage
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1 Hydrogen Peroxide-Mediated Corneol Endothelial Damage Induction by Oxygen Free Radical Dovid S. Hull,* Keith Green,*f Lisa Thomas,* and Nancy Alderman* Polymorphonuclear leukocytes and other inflammatory cells release superoxide anion and additional oxidant species following stimulation. Corneal endothelial cells were exposed to a flux of chemically generated superoxide anion (oxygen-free radical) produced by the combination of 1 mm hypoxanthine and 0.06 U/ml xanthine oxidase. Exposure of endothelial cells to the combination of hypoxanthine and xanthine oxidase resulted in anatomic disruption of the cells with interference in the function of endothelial water movement and resultant swelling of the corneal stroma. Catalase reduced the corneal swelling caused by exposure of endothelium to the oxygen-free radical generating system, whereas superoxide dismutase, ascorbic acid, D-mannitol, and ethanol did not prevent damage. The data suggest that hydrogen peroxide produced during the dismutation reaction of the superoxide anion is one of the toxic species, whereas the superoxide anion itself and the hydroxyl-free radical probably do not participate. The data suggest that corneal endothelial cells are susceptible to physiologic and anatomic damage induced by the products of reactive oxygen species, which, from previous studies, are known to be generated by inflammatory cells. The development of therapeutic modalities directed at the prevention of damage produced by hydrogen peroxide and other oxidant species may be of benefit in reducing corneal endothelial cell damage secondary to ocular inflammatory disease processes. Invest Ophthalmol Vis Sci 25: , 1984 Destruction of normal eye tissue is one of the undesirable effects of ocular inflammation. It is known that ocular inflammation may result in alteration of corneal endothelial cell function and a loss in the number of corneal endothelial cells. 1 " 3 It is possible that the functional and structural alterations of coraeal endothelium found following ocular inflammatory disease processes may in part be mediated by superoxide anion, its products, and/or other oxidant species elaborated by inflammatory cells. It was the purpose of this study to determine the endothelial effects of chemically generated superoxide anion used as a model for one of the active oxygen species known to be liberated by phagocytic cells. Studies were made on corneal endothelial cell physiology and ultrastruc- From the Departments of Ophthalmology* and Physiology,! Medical College of Georgia, Augusta, Georgia. Supported in part by research grant EY04479 (DSH), EY04558, (KG) and EY03415 (Core Grant for Vision Research from the National Eye Institute); in part by a research grant from the Georgia Lions Lighthouse Foundation, Inc.; and in part by a Research to Prevent Blindness, Departmental Research Award. Submitted for publication: December 6, Reprint requests: David S. Hull, MD, Department of Ophthalmology, Medical College of Georgia, Augusta, GA ture with the additional purpose of identifying mechanisms by which the toxic effect could be modified. Materials and Methods Adult albino rabbits weighing approximately 2.5 kg of either sex were killed with an overdose of sodium pentobarbital. Eyes were removed from the animals, prepared, and corneas mounted in the specular microscope. 4 ' 5 These techniques conformed to the ARVO Resolution on the Use of Animals in Research. The endothelial surface was perfused with a modified Krebs-Ringer bicarbonate solution 6 consisting of mm NaCl, 4.69 mm KC1, 1.77 mm CaCl 2-2 H 2 O, 1.8 mm KH 2 PO4, 1.18 mm MgSO 4-7 H 2 O, mm dextrose, and mm NaHCO 3. The mean osmolarity of the solution was 290 ± 5 mosm hence it was called "Ringer 290." The osmolarity of "Ringer 290" was adjusted with sucrose to insure that the osmolarity of experimental and control perfusing solutions was similar. A mixture of 97% O 2-3% CO 2 was bubbled through the solution for 30 min and the ph adjusted to 7.3. No adenosine or glutathione was added to the solution. The corneal 1246
2 No. 11 SUPEROXIDE, HYDROGEN PEROXIDE, AND ENDOTHEUUM / Hull er ol endothelium was perfused with the solution at 37 C, 15 mmhg, at a rate of 2 ml/hr. 7 Silicone oil (Dow Corning 360 Medical Fluid) was placed on the epithelial surface to prevent dehydration. The first hour was a stabilization period during which time experimental and control corneas were perfused with "Ringer 290" containing an additional 20 mm sucrose. This solution had an osmolarity of 313 mosm. After the 1-hr stabilization period and the recording of corneal thickness, paired corneas in their brass mounting rings were removed from the specular microscope and the plastic posterior mounting disc was removed. Two-hundred microliters of a mixture containing 1.0 mm hypoxanthine (Sigma; St. Louis, MO) and 0.06 U/ml xanthine oxidase (Sigma) in "Ringer 290" was placed on the upward facing, concave, corneal endothelial surface of the control corneas for 5 min. 8-9 The xanthine oxidase and hypoxanthine were combined immediately prior to their being placed on the endothelial surface. "Ringer 290" containing a variety of combinations and additives (Table 1) and balanced with sucrose to an osmolarity similar to controls was placed on the endothelial surface of paired experimentals for 5 min. After 5 min of exposure experimental and control fluids were removed, the tissue was flushed, replaced in the specular microscope, and perfused with "Ringer 290" containing 20 mm sucrose for an additional 3 hr at a rate of 2 ml/hr. Corneal thickness was recorded every Vi hr. The mean change in corneal thickness was that of a minimum of five corneas per experimental group. The data were plotted on graph paper, and the corneal swelling rate was Table 1. Experimental groups. Controls for each group were exposed to 1.0 mm hypoxanthine and 0.06 U/ml xanthine oxidase (315 mosm, ph = 7.3) Group Experimental perfusion solution mm hypoxanthine + 20 mm sucrose (313 mosm, ph = 7.3) U/ml xanthine oxidase + 10 mm surcrose (312 mosm) mm hypoxanthine U/ml denatured xanthine oxidase and 20 mm sucrose (305 mosm) U/ml superoxide dismutase mm hypoxanthine U/ml xanthine oxidase U/ml catalase mm hypoxanthine U/ml xanthine oxidase (315 mosm) mm ascorbic acid mm hypoxanthine U/ml xanthine oxidase (319 mosm) mm D-mannitol mm hypoxanthine U/ml xanthine oxidase (315 mosm) mm D-mannitol mm hypoxanthine U/ml xanthine oxidase (328 mosm)* ' mm ethanol mm hypoxanthine U/ml xanthine oxidase (316 mosm) * The control perfusing solution for group 8 contained 15.0 mm sucrose mm hypoxanthine U/ml xanthine oxidase (330 mosm). 60 n H o «H ^" ^ 1.0 mm hypoxanthine» 0.06 U/ml xanthine oxidase 1.0 mm hypoxanthine Time (hours) *3 jitrwhr..< 10±2pm/hr Fig. 1. Rabbit corneal swelling following a 5-min exposure of corneal endothelial cells to either a mixture of 1.0 mm hypoxanthine and 0.06 U/ml xanthine oxidase or following a 5-min exposure to 1.0 mm hypoxanthine. Data is plotted as the change in corneal thickness ± 95% confidence limits versus time. determined by linear regression analysis. A comparison of experimental and control regression lines was made by analysis of covariance. 10 Variance in the data was expressed as the mean ±95% confidence limits. Denatured xanthine oxidase was prepared by incubating xanthine oxidase in 10 mm cyanide in neutral phosphate buffer for 2 hr at room temperature. It then was dialyzed against de-ionized water overnight. For preparation of corneas for transmission electron microscopy, tissues were fixed in 2.67% phosphate buffered gluteraldehyde and postfixed in 2% osmium tetroxide. Tissues were dehydrated through graded alcohols and propylene oxide and placed in Spunresin. Following overnight infiltration with Spunresin, tissues were embedded in freshly prepared Spurr resin, and the tissue blocks were polymerized at 70 C. Tissues then were sectioned, stained, and examined. Results Group 1 (Hypoxanthine Control) Corneas exposed to the mixture of 1.0 mm hypoxanthine and 0.06 U/ml xanthine oxidase swelled at a rate of 19 ± 3 ^m/hr (Figs. 1, 2). This was significantly greater (P < 0.05) than the swelling rate of 10 ± 2 fxm/hr found in paired corneas exposed to 1.0 mm hypoxanthine. Swelling began immediately after exposure to the mixture and was nearly linear in configuration (Fig. 1).
3 1248 INVESTIGATIVE OPHTHALMOLOGY b VISUAL SCIENCE / November 1984 Vol n 30- II - tt TO il 15 o +i o 20- ID mm hypoisnlhine - D.06 U/ml lanthine oiidasa 1.0 mm tlypojanlhine 0.06 U/ml janthine oiidase I 1.0 mm hypoxanlhine 0.06 UJml denatured nanthine oiidase nanthine < p<0.05 Fig, 2. Bar graph comparing the corneal swelling rate ± 95% confidence limits over 3 hr as determined by linear regression analysis. The corneal endothelium had been exposed for 5 min to one of the following: (1) 1.0 mm hypoxanthine U/ml xanthine oxidase; (2) 1.0 mm hypoxanthine; (3) 0.06 U/ml xanthine oxidase; and (4) 1,0 mm hypoxanthine U/ml denatured xanthine oxidase. I Scanning electron microscopy of a cornea exposed to 1 mm hypoxanthine and 0.06 U/ml xanthine oxidase showed swelling of scattered endothelial cells (Fig. 3). Transmission electron microscopy of coraeal endothelial cells that appeared to be minimally affected by exposure to the 1.0 mm hypoxanthine and 0.06 U/ml xanthine oxidase mixture showed an intact cell membrane and intercellular space with the formation of large cytoplasmic vacuoles (Fig. 4). Transmission electron microscopy of a coraeal endothelial cell that appeared to be affected severely by exposure to the 1.0 mm hypoxanthine and 0.06 U/ml xanthine oxidase mixture showed an increase in electron density with marked disruption of the nucleus and cytoplasmic organelles (Fig. 5). Scanning electron microscopy of a cornea exposed to 1.0 mm hypoxanthine and 20 mm sucrose showed preservation of the endothelial mosaic. Transmission electron microscopy of comeal endothelial cells exposed to 1.0 mm hypoxanthine and 20 mm sucrose showed a normal cell membrane, intercellular space, nucleus and cytoplasmic organelles (Fig, 6). Fig. 3. Scanning electron micrograph of corneal endothelium following a 5-min exposure to 1.0 mm hypoxanthine U/ml xanthine oxidase, and a subsequent 3-hr perfusion with "Ringer 290" + 20 mm sucrose. Scattered endothelial cells appear to be swollen (original magnification, X500).
4 No. 11 SUPEROXIDE, HYDROGEN PEROXIDE, AND ENDOTHEUUM / Hull er ol Fig. 4. Transmission electron micrograph of corneal endothelium following a 5-min exposure to 1.0 mm hypoxanthine U/ml xanthine oxidase and a subsequent 3-hr perfusion with "Ringer 290" + 20 mm sucrose. The cell membrane, intercellular space, nucleus, and endoplasmic reticulum are intact. There are numerous large vacuoles in the cytoplasm (original magnification, XI 7,425). Croup 2 (Xanthine Oxidase Control) Corneas exposed to the mixture of 1.0 mm hypoxanthine and 0.06 U/ml xanthine oxidase swelled at a rate of 23 ± 3 /mi/hr. This was significantly greater {P < 0.05) than the swelling rate of 14 ± 3 ^ni/hr found in paired corneas exposed to 0.06 U/ml xanthine oxidase (Fig. 2). Scanning electron microscopy of a cornea exposed to 0.06 U/ml xanthine oxidase showed preservation of the endothelial mosaic. Transmission electron microscopy of corneal endothelial cells exposed to 0.06 U/ml xanthine oxidase showed a normal cell membrane, intercellular space, nucleus and endoplasmic reticulum. Several small cytoplasmic vacuoles were present (Fig. 7). Group 3 (Denatured Xanthine Oxidase Control) Corneas exposed to the mixture of 1.0 mm hypoxanthine and 0.06 U/ml xanthine oxidase swelled at 31 ±6 fim/hr. This was significantly greater (P < 0.05) than the swelling rate of 11 ±3 jim/hr found in paired corneas exposed to 1.0 mm hypoxanthine and 0.06 U/ml denatured xanthine oxidase (Fig. 2). Scanning electron microscopy of corneas exposed to 1.0 mm hypoxanthine and 0.06 U/ml denatured xanthine oxidase showed preservation of the endothelial mosaic. Transmission electron microscopy of endothelial cells was unremarkable except for the presence of several small cytoplasmic vacuoles. Groups 4-9 (Superoxide Dismutase, Catalase, Ascorbic Acid, D-Mannitol, Ethanol) The addition of 200 U/ml superoxide dismutase, 5.0 mm ascorbic acid, 3.0 mm D-mannitol, 15.0 mm D-mannitol, or 0.07 mm ethanol did not prevent the corneal swelling induced by exposure of corneal endothelial cells to 1.0 mm hypoxanthine and 0.06 U/ml xanthine oxidase (Fig. 8). Concentrations of ethanol greater than 0.07 mm were toxic to endothelial cells. The addition of 88 U/ml catalase to the perfusing solution resulted in a significant reduction (P < 0.05) in the corneal swelling rate (Fig. 8).
5 1250 INVESTIGATIVE OPHTHALMOLOGY b VISUAL SCIENCE / November 1984 Vol. 25
6 No. 11 SUPEROXIDE, HYDROGEN PEROXIDE, AND ENDOTHELIUM / Hull er ol Fig, 5. Transmission electron micrograph of a comeal endothelial cell that appears to be affected more severely by the hypoxanthinexanthine oxidase mixture then the cell shown in Figure 4. There is an increase in electron density, with marked disruption of the nucleus and cytoplasmic organelles. A cell in the far right of the photo appears to be less severely affected (original magnification, X12,546). Fig. 6. Transmission electron micrograph of corneal endothelium following a 5-min exposure to 1.0 mm hypoxanthine and a subsequent 3-hr perfusion with "Ringer 290" + 20 mm sucrose. The cell membrane, intercellular space, nucleus, and cytoplasmic organelles are intact (original magnification, XI2,546). Discussion Superoxide anion, hydrogen peroxide, hydroxyl radical, singlet oxygen, hypohalite ions and possibly other oxidant species produced during the activation of phagocytic cells with the resultant "respiratory burst" all have been implicated as being capable of oxidizing tissue components and causing irreversible damage. 811 " 12 The present experiment has shown that corneal endothelial cells undergo a physiologic and anatomic alteration following exposure to hydrogen peroxide that is produced by the dismutation of superoxide anion chemically generated by the combination of hypoxanthine with xanthine oxidase. 8 ' 9 The alteration, results in a disruption of cellular architecture and a corneal swelling rate of about 20 r. Perfusion with hypoxanthine or xanthine oxidase alone or perfusion with hypoxanthine with denatured xanthine oxidase did not result in significant cell alteration. The adverse effect of the superoxide anion was not blocked by superoxide dismutase, an agent that catalyzes the conversion of the superoxide anion to hydrogen peroxide 13 : 2 O 2 ~ + 2 H + + H 2 O 2 + O 2. Catalase, however, prevented the adverse effect. Since catalase catalyzes the divalent reduction of H 2 O 2 to H 2 O, it is apparent that the toxic effect on endothelial cells was at least in part secondary to hydrogen peroxide produced during the dismutation reaction of oxygen-free radical. 13 The toxic effect of hydrogen peroxide also was confirmed indirectly by the fact that ascorbic acid, which in an aerobic medium scavenges O 2 ~ but not H 2 O 2, did not have Fig. 7. Transmission electron micrograph of corneal endothelium following a 5-min exposure to 0.06 U/ml xanthine oxidase and a subsequent 3-hr perfusion with "Ringer 290" + 20 mm sucrose. The cell membrane, intercellular space, nucleus and endoplasmic reticulum are intact. Several small cytoplasmic vacuoles are present (original magnification, X8.976).
7 1252 INVESTIGATIVE OPHTHALMOLOGY & VISUAL SCIENCE / November 1984 Vol mm hypoxanthine U/ml xanthine oxidase U/ml superoxide dismutase 1.0 mm hypoxanthine-i U/ml xanthine oxidase 1.0 mm hypoxanthine j U/ml xanthine oxidase + 88 U/ml catalase 1.0 mm hypoxanthine U/ml xanthine oxidase-f mm ascorbic acid 1.0 mm hypoxanthine-f 0.06 U/ml xanthine oxidase mm ethanol 1.0 mm hypoxanthine-f 0.06 U/ml xanthine oxidase mm D-mannitol 1.0 mm hypoxanthine U/ml xanthine oxidase 15 mm D-mannitol < mm hypoxanthine U/ml xanthine oxidase+15 mm sucrose I 25 r 30 Corneal Swelling Rate (^m/hr) ±95% Confidence Limits Fig. 8. Bar graph comparing the corneal swelling rate ± 95% confidence limits over 3 hr as determined by linear regression analysis. The corneal endothelium had been exposed for 5 min to 1.0 mm hypoxanthine and 0.06 U/ml xanthine oxidase alone or in combination with superoxide dismutase, catalase, ascorbic acid, ethanol or D-mannitol. N = 6 in all cases except ethanol where N = 5. P < 0.05 only in the case of catalase. a protective effect. Previous work has shown that a 3 hr perfusion of corneal endothelial cells with 0.5 mm hydrogen peroxide results in endothelial cell damage and corneal stromal swelling. 14 While this experimental model has shown that hydrogen peroxide produced by the dismutation of superoxide anion one of the species causing the endothelial cell damage, it is possible that interactions between hydrogen peroxide and superoxide anion may result additionally in the production of the hydroxyl-free radical and/or singlet oxygen 15 " 19 : H 2 O 2 + O 2 ~ -» OH" + OH* + O 2 *. 19 The hydroxyl radical scavengers D-mannitol (3 mm and 15 mm) and ethanol (0.07 mm) did not modify the corneal swelling. Ethanol at higher concentrations was toxic to endothelial cells. Therefore, within the confines of this experimental model, which did not contain a metal-chelate complex, participation of the hydroxyl-free radical in the mediation of endothelial cell damage appears to be unlikely. The fact that superoxide dismutase did not provide protection to endothelial cells provides some additional, indirect evidence against hydroxyl-free radical and singlet oxygen as causing the tissue damage. Since hydroxyl-free radical and singlet oxygen are produced by interactions of H 2 O 2 and O 2 ~, either superoxide dismutase or catalase would be expected to have a protective effect. However, the participation of singlet oxygen cannot be definitively ruled out. Previous work has shown that corneal endothelial cells are susceptible to damage either from hydrogen peroxide perfused in vitro or produced by the dismutation of photochemically produced superoxide anion. This results in a direct, adverse effect on endothelial cell transport mechanisms and membrane permeability. 14 ' 20 " 22 This study has shown that corneal endothelial cells may be damaged by hydrogen peroxide produced by the dismutation reaction of chemically generated oxygen-free radical. Hydrogen peroxide production always accompanies superoxide production since it is a product of the dismutation reaction. Since hydrogen peroxide, as well as other oxidant species, are produced by phagocytic cells, it would appear that the development of therapeutic agents that have a specific modifying effect on hydrogen peroxide and possibly other oxidant species may be of benefit in reducing the corneal endothelial cell damage caused by ocular inflammatory disease processes. Key words: superoxide anion, free radical, cornea, endothelium, hydrogen peroxide
8 No. 11 SUPEROXIDE, HYDROGEN PEROXIDE, AND ENDOTHEUUM / Hull er ol References 1. Setala K: Corneal endothelial cell density in iridocyclitis. Acta Ophthalmol 57:277, Inomata H, Smelser GK, and Polack FM: The fine structural changes in the corneal endothelium during graft rejection. Invest Ophthalmol 9:263, Inomata H and Smelser GK: Fine structural alterations of corneal endothelium during experimental uveitis. Invest Ophthalmol 9:272, Dikstein S and Maurice DM: The metabolic basis to the fluid pump in the cornea. J Physiol 221:29, McCarey BE, Edelhauser HF, and Van Horn DL: Functional and structural changes in the corneal endothelium during in vitro perfusion. Invest Ophthalmol 12:410, Green K and Green MA: Permeability to water of rabbit corneal membranes. Am J Physiol 217:635, Bowman K and Green K: Hydrostatic pressure effects on deswelling of de-epithelialized and de-endothelialized corneas. Invest Ophthalmol 15:546, Del Maestro RF, Thaw HH, Bjork J, Planker M, and Arfors KE: Free radials as mediators of tissue injury. Acta Physiol Scand 492(Suppl):43, Fridovich I: Quantitative aspects of the production of superoxide anion radical by milk xanthine oxidase. J Biol Chem 245:4053, Shedecor GW and Cochran WG: Statistical Methods, 6th edition. Ames, Iowa State University Press, 1967, pp Babior BM: Oxygen-dependent microbial killing by phagocytes. N Engl J Med 298:659, Babior BM: Oxygen-dependent microbial killing by phagocytes. N Engl J Med 298:721, Fridovich I: Oxygen radicals, hydrogen peroxide, and oxygen toxicity. In Free Radicals in Biology, Vol 1, Pryor WA, editor. New York, Academic Press, 1976, pp Hull DS, Csukas S, Green K, and Livingston V: Hydrogen peroxide and corneal endothelium. Acta Ophthalmol 59:409, Haber F and Weiss J: The catalytic decomposition of hydrogen peroxide by iron salts. Proc R Soc Lond Ser A 147:332, McCord JM and Day ED Jr: Superoxide-dependent production of hydroxyl radical catalyzed by iron-edta complex. FEBS Letters 86:139, McCord JM: Free radicals and inflammation: protection of synovial fluid by superoxide dismutase. Science 185:529, Salin ML and McCord JM: Free radicals and inflammation: Protection of phagocytosing leukocytes by superoxide dismutase. JClin Invest 56:1319, Kellogg EW III and Fridovich I: Superoxide, hydrogen peroxide, and singlet oxygen in lipid peroxidation by a xanthine oxidase system. J Biol Chem 250:8812, Hull DS, Strickland EC, and Green K: Photodynamically induced alteration of cornea endothelial cell function. Invest Ophthalmol Vis Sci 18:1226, Hull DS, Green K, Csukas S, and Livingston V: Photodynamic alteration of cornea endothelium: Relation to bicarbonate fluxes and oxygen concentration. Biochim Biophys Acta 640:231, Hull DS, Green K, and Laughter L: Cornea endothelial rose bengal photosensitization: Effect on permeability, sodium flux and ultrastructure. Invest Ophthalmol Vis Sci 25:455, 1984.
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