VIzomitin / Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 4. Age-related eye disease. SkQ1 returns vision to blind animals
doi: https://link.springer.com/article/10.1134/S0006297908120043
doi 10.1134/S0006297908120043
Mitochondriatargeted cationic plastoquinone derivative SkQ1 (10(6′plastoquinonyl) decyltriphenylphospho nium) has been investigated as a potential tool for treating a number of ROSrelated ocular diseases. In OXYS rats suffering from a ROSinduced progeria, very small amounts of SkQ1 (50 nmol/kg per day) added to food were found to prevent devel opment of ageinduced cataract and retinopathies of the eye, lipid peroxidation and protein carbonylation in skeletal mus cles, as well as a
decrease in bone mineralization. Instillation of drops of 250 nM SkQ1 reversed cataract and retinopathies in 312monthold (but not in 24monthold) OXYS rats. In rabbits, experimental uveitis and glaucoma were induced by immunization with arrestin and injections of hydroxypropyl methyl cellulose to the eye anterior sector, respectively. Uveitis was found to be prevented or reversed by instillation of 250 nM SkQ1 drops (four drops per day). Development of glauco ma was retarded by drops of 5 µM SkQ1 (one drop daily). SkQ1 was tested in veterinarian practice. A totally of 271 animals (dogs, cats, and horses) suffering from retinopathies, uveitis, conjunctivitis, and cornea diseases were treated with drops of 250 nM SkQ1. In 242 cases, positive therapeutic effect was obvious. Among animals suffering from retinopathies, 89 were blind. In 67 cases, vision returned after SkQ1 treatment. In ex vivo studies of cultivated posterior retina sector, it was found that 20 nM SkQ1 strongly decreased macrophagal transformation of the retinal pigmented epithelial cells, an effect which might explain some of the above SkQ1 activities. It is concluded that low concentrations of SkQ1 are promising in treating retinopathies, cataract, uveitis, glaucoma, and some other ocular diseases.
Abbreviations: MDA, malondialdehyde; ROS, reactive oxygen species; RPE, retinal pigmented epithelium; SkQs, cationic derivatives of plastoquinone or methyl plastoquinone; SkQ1, 10(6′plastoquinonyl) decyltriphenylphosphonium. * To whom correspondence should be addressed. As reported in the preceding papers [13], very small amounts of mitochondriatargeted plastoquinone deriva tives (SkQs) show pronounced antioxidant effects on model membranes, isolated mitochondria, and cell cul tures. In the latter case, strong antiapoptotic and anti necrotic effects were observed in situations when cell death was induced or mediated by reactive oxygen species (ROS) [1]. It was also found that several agerelated pathologies (arrhythmia, heart and kidney infarctions, stroke, p53controlled lymphomas, and certain other types of cancer) can be successfully treated by SkQs in animals [2, 3]. In this paper, we shall continue the latter approach when studying agerelated, ROSmediated ocular dis eases. In fact, retina is a tissue of the the highest risk of the ROSinduced damage since (i) it contains high level of polyunsaturated fatty acids, a very good target for ROS, (ii) it is exposed to light producing such ROS as singlet oxygen, and (iii) oxygen concentration in retina is near arterial, i.e. much higher than in the great majority of other tissues (in spite of the fact that retina is a tissue of highest respiratory activity) [4]. There are numerous indications of a crucial role of ROS in the main agerelated ocular pathologies, i.e. retinopathies (maculodystrophy [5, 6], retinitis pigmen tosa [7, 8], hereditary optic neuropathy [9]), as well as glaucoma [10, 11], cataract [12, 13], and autoimmune uveitis [14, 15]. Polyunsaturated fatty acids in mitochon drial cardiolipin are first of all attacked by mitochondria produced ROS that are quenched by SkQs [1]. This is why the abovelisted pathologies attracted our attention as a possible field of therapeutic application of SkQs. Here we shall describe certain results obtained when animals suf fering from retinopathies, cataract, uveitis, glaucoma, and some other eye diseases were treated with SkQ.
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MATERIALS AND METHODS Studies with OXYS rats. Lipid peroxidation and pro tein carbonylation in skeletal muscles of OXYS and Wistar rats were investigated as described in refs. [16] and [17], respectively. Mineralization of vertebra and bones of extremities were measured with a LUNAR ExpertXL Xray bone densitometer. Measurements of activity of cytochrome P450 isoforms. Microsomes were isolated from OXYS rat livers perfused by solution of 1.15% KCl and 20 mM TrisHCl, pH 7.4. The perfused liver was homogenized in solution of the same composition. Supernatant obtained after lowspeed centrifugation of homogenate was centrifuged at 100,000g for 1 h. Sediment of microsomes was suspended in 0.1 M potassium phosphate, pH 7.4, supplemented with 20% glycerol. Levels of the P450 isoforms CYP1A1, CYP1A2, CYP2B + CYP2C, and CYP2B1 were fluorometrically measured as a rate of formation of resorufin from 7 ethoxyresorufin, 7methoxyresorufin, 7benzoxyre sorufin, and 7penthoxyresorufin, respectively [18]. Ophthalmoscopic studies of OXYS and Wistar rats were carried out with a Betta ophthalmoscope, an Opton fun duscamera, and a ShinNippon SL45 slit lamp. Degree of cataract was estimated as follows: 1 arbitrary unit (a.u.), certain lens area of slightly decreased transparen cy; 2 a.u., certain area of strongly decreased transparen cy; 3 a.u., strong decrease in transparency of the whole lens cortex and/or nucleus. As to retinopathy, also three major stages of retinal damage were distinguished, namely, 1 a.u., appearance of drusen and other pathological changes in the retinal pig mented epithelium (RPE) and a partial atrophy of a choroid capillary layer; 2 a.u., exudative detachment of RPE and of retinal neuroepithelium, further choroid cap illary layer atrophy; 3 a.u., neovascularization and exuda tivehemorrhagic
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detachment of RPE and neuroepitheli um; scarring. Studies of experimental uveitis. Arrestin purification. Bovine retinal outer segments were prepared from retinas following Wilden and Kuhn [19]. Arrestin was purified by specific binding of this protein to phosphorylated and photoactivated rhodopsin [20], followed by chromato graphic separations on a DEAEcellulose column and on a Mono Q column [21]. Immunization of rabbits with arrestin. Arrestin solu tion (1 ml in PBS, 0.8 mg/ml) was emulsified with equal volume of Freund’s complete adjuvant (Sigma, USA) and inoculated into 6monthold New Zealand white rabbits. The second inoculation was performed on day 30. Animals treated with Freund’s adjuvant served as a con trol. After immunization, blood samples were taken from the rabbits and production of antibody was measured using an ELISA test. Measurement of nitrate level in the aqueous humor of anterior sector. Nitric oxide was determined using a spec trophotometric assay based on the Griess reaction. Briefly, 100 µl samples of the aqueous humor of the eye anterior sector were mixed with 1% sulfanilamide and 0.1% naphthyl ethylenediamine. After 10 min incubation at room temperature, we determined the concentration of nitrate in the mixture by measuring absorbance at 550 nm and comparing this value with absorbance of standard solutions of sodium nitrate. SkQ treatment. SkQ1 was dissolved in a solution con taining 10 mM potassium phosphate (pH 6.5) and 0.9% NaCl. Drops of the SkQ1 solution were instillated to one of rabbit’s eyes (four times per day). Studies of experimental glaucoma. Experimental glaucoma was induced by 10 injections (two injections per week) of 0.1 ml viscoelastic Celoftal (2% hydroxypropyl methyl cellulose) to anterior sector of the both eyes of a rabbit [22]. To the right eye, Vetomitin, a pharmaceutical form of SkQ1, was daily instilled whereas the left eye was used as a control to the SkQ1 treatment. Among rabbits treated with SkQ1, four animals obtained drops containing 5 µM SkQ1. Other four rabbits obtained 25 µM SkQ1. Before the first Celoftal injection, the eyes were investigated to measure parameters of the
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healthy animals. The following devices were used: a GlauTest60 eye tonograph, an AngiodinOphthalmo (Russia) ultrasonic ophthalmoscope, and a Cannon (Japan) funduscamera. Cultivation of rat eye posterior sector. Preparations of eye posterior sector were obtained from eyes of narcotized adult (23 months) Wistar rats (the treatment carried out according to bioethics regulations of the Russian Academy of Sciences). Procedures of obtaining, roller cultivation, fixation, as well as methods of investigation of the preparations are described in detail in [23]. Briefly, the eye anterior sector containing the cornea, iris, and lens was removed and two types of the remaining posteri or sector were used for roller cultivation. In one case, the posterior eye sector before cultivation was incubated for 35 times in 5 ml commercial DMEM medium with phe nol red, 3% Lglutamine, 4% gentamicin (medium A), and 10 mM EDTA. Afterward, neural retina was removed and the remaining part of the sector (i.e. RPE, choroid, and sclera) was used. In the other case, neural retina was not removed. In both cases, samples of the eye posterior sector were put into flasks containing medium A and 10% fetal calf serum with 20 nM SkQ1 or without SkQ1. Then the flasks were placed into a roller and cultivated in a dark sterile box at 60 rpm and 35.5°C for 7 or 14 days. The medium was not changed during the whole period of roller cultivation. After cultivation, the samples were fixed with 4% formaldehyde and Bouin’s solution. Serial 7µm crosssections (Reichert OME microtome) were stained with hematoxylin and eosin. To visualize macrophages, an antimacrophage antibody (Sigma) was applied. Images obtained were scrutinized using an Olympus AH3 microscope, a digital camera, and a com puter with Lite, Corel Draw, Adobe Photoshop, Excel, and Plot Calc program package
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RESULTS Prevention and reversal of agedependent cataract and retinopathy in OXYS rats. As a model for in vivo antioxidant effects of SkQs, we used OXYS rats, a strain suffering from constant oxidative stress [24]. In these rats, cataract and retinopathy were shown to appear as early as at threemonth age [2527]. In the first series of experiments, we investigated age dependent consequences of oxidative stress in OXYS rats, trying to abrogate them by means of SkQ1 added to their food. It was found (Fig. 1, a and b) that levels of lipid per oxidation (estimated by measuring malondialdehyde (MDA)) and oxidation (carbonylation) of proteins are higher in skeletal muscles of oneyearold Wistar rats than in threemonthold ones. The effect of age was even larg er in OXYS rats. Feeding with very small amount of SkQ1 (50 nmol/kg per day) resulted in a decrease in the lipid and protein oxidation levels. As to the mineral mass levels in vertebra and extremities, these parameters were lower in OXYS than in Wistar rats due to progeriainduced osteo porosis. Again, SkQ1 feeding proved to be favorable, increasing the mineral mass in OXYS rats (Fig. 2). Thus, the presented data show that SkQ1 is compe tent in preventing some consequences of oxidative stress in OXYS rats. Then an attempt was made to treat by SkQ1 eye diseases in OXYS rats. As experiments showed, addi tion of the same SkQ1 amounts to the food completely prevented development of cataract and retinopathy in OXYS rats up to age of two years (Fig. 3 (see color insert) and Table 1; see also Supplementary information, Figs. S1 and S21 ). Vitamin E added to the food was much less effective than SkQ1 (Fig. 4). It is remarkable that the SkQ1 effects were not accompanied by any induction of cytochromes P450 in liver (Table 2), in contrast to those of vitamin E (not shown). It was also found that instillations of drops of nanomolar SkQ1 significantly reverse pathological changes in middleage OXYS animals (Figs. 5 and 6). The latter effect was also observed in Wistar rats suffering from cataract (Figs. 5 and 6). In very old (more than 18 months) rats, neither cataract nor retinopathy was reversed by SkQ1 (not shown), although it still effectively prevented the diseases (Fig. 3, ac, see color insert). The
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above conclusion concerning preventive effect of SkQ1 on 24monthold OXYS rats was confirmed by histologi cal analysis of sections across the retina (Fig. 7; see color insert). The figure shows that in OXYS rats without SkQ1 the photoreceptor layer is absent, whereas OXYS rats receiving SkQ1 during all their life retained this layer. In old Wistar rats, the photoreceptor layer was present even without SkQ1. These results are in line with our observa tions that the electroretinogram disappeared in the majority of the 24monthold OXYS rats but was retained in OXYS rats with SkQ1 as well as in Wistar rats (Fig. 3c and Table 1). Reversal of an already developed retinopathy by SkQ1 drops was confirmed by electron microscopy data. As shown in Fig. 8 and Table 3, retinopathy in 11month old OXYS rats results in obliteration of choriocapillaries. This parameter is at least partially normalized after 1.5 month instillations of 250 nM SkQ1 (one drop daily). Reappearance of choriocapillaries in the presence of SkQ1 was accompanied with normalization of some other
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morphological features, i.e. distribution of lipofuscin granules in retinal pigment epithelial cells (Fig. S3, a and b) and disappearance of hernias formed due to disruption of Bruch’s membrane (Fig. S3c). Favorable effects of SkQ1 can disappear when it was added in excess. In skeletal muscles of OXYS rats, this occurred at 250 nmol SkQ1/kg per day (Fig. 1). In bones of the same rats, 250 nmol SkQ1 was still as effective as 50 nmol (Fig. 2). In eyes of OXYS rats, drops of 10 nM 1 µM SkQ1 were effective in reversal of cataract and retinopathy, 5 µM being ineffective. As to eyes of Wistar rats, even 25 µM SkQ1 was still of favorable activity (Figs. 5 and 6). The above relationships can be explained assum ing that (i) disappearance of therapeutic action of SkQ1 is due to prooxidant activity of its high concentrations [1] in OXYS rats suffering from constant oxidative stress. SkQ1 prevents and reverses blindness in experimental uveitis. Uveitis has also been shown to be mediated by mitochondrial ROS [25], so we tried to use SkQ1 for treat ment of this eye disease, too. To this end, a rabbit model
of experimental uveitis was investigated. Experimental uveitis was induced by immunization of the animal by a photoreceptorspecific protein, arrestin, which resulted in blindness. This effect was prevented and reversed by SkQ1 instillations (four drops of 250 nM SkQ1 per day; not shown). It was also found (Fig. 9) that the same SkQ1 treatment strongly inhibited formation of NO2 — and NO3 — in eyes of the uveitissuffering animals (under uveitis, these processes are known to be initiated by interaction of NO with О 2 [28, 29]). SkQ1 prevents development of experimental glauco ma in rabbits. In rabbits, experimental glaucoma was induced by a series of Celoftal instillations to the eye anterior sector. This resulted in appearance of such typi cal glaucoma features as an increase in intraocular pres sure (P0), a strong decrease in the aqueous humor outflow as well as in humor production (F), a strong rise of Bekker’s coefficient (BC), and some increase of the lens thickness (Table 4). Analysis of photographs obtained
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using a fundus camera revealed excavation of the optic disk (not shown). All these parameters were normalized if treatment with the glaucoma inducer was accompanied by instillation of drops of 5 µM SkQ1 solution. Higher (25 µM) (Table 4) and lower (0.25 µM; not shown) SkQ1 concentrations proved to be less efficient than 5 µM SkQ1. SkQ1 prevents macrophagal transformation of RPE and destruction of retina ex vivo. A number of retinopathies are known to be accompanied with a ROSmediated transformation of the retinal pigment epithelial (RPE) cells to macrophages that attack other retinal cells [29, 30]. If this process is arrested by SkQ1, this might explain, at least partially, the above described favorable effect of our compound upon certain retinopathies and uveitis. Macrophagal RPE cell transformation was studied in an ex vivo system, i.e. eye posterior sector obtained from twomonthold Wistar rats and cultivation in a sterile box for 7 (Fig. 10, a and c) or 14 (Fig. 10, b and d) days. As one can see in Fig. 10a, one week cultivation results in some loss of RPE cells, which was more pronounced in the center of the sector. Simultaneously, the number of macrophages was strongly increased (Fig. S4). Both these effects were strongly inhibited by 20 nM SkQ1 added to the cultivation medium. This action paralleled prevention of disappearance of the ganglion cells (Fig. 10c) and of inner nuclear layer of the photoreceptor cells (Fig. 10d). Veterinary practice experiment of application of SkQ1 to treat various animal ocular pathologies. Finally, SkQ1 was applied in veterinarian practice in cases when con ventional medical treatments failed. A total of 135 ani mals (dogs, cats, and horses) suffering from various retinopathies were treated daily with drops of 250 nM SkQ1. In 89 cases, the animals were completely blind before the treatment. Vision was returned to 67 of them (Table 5). There was not a single case when SkQ1 had an unfavorable effect or its efficiency declined in the course of the treatment time. Electroretinograms of a dog whose visual function was recovered by means of 250 nM SkQ1 instillations are shown in Fig. 11 (see color insert). The dog was blind because of inherited retinal dysplasia. As the figure shows, before the SkQ1 treatment there was practically no elec tric response to light. After 27 days of SkQ1 instillations, visual function was partially recovered and some electric response appeared. Even larger response was revealed on day 42 of the treatment, which was accompanied with further improvement of vision (for details, see Supplementary Information).
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