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Effects of αTocopherol and Its Short-Chain Analog on Metabolic Processes in Tissues of the Rabbit


Neurophysiology, Vol. 44, No. 2, June, 2012

Effects of α-Tocopherol and Its Short-Chain Analog on Metabolic Processes in Tissues of the Rabbit Visual Analyzer under Conditions of Light Stress
S. G. Kolomiychuk1 and N. F. Leus1
Received May 10, 2011.
We studied changes in the contents of nicotinamide co-enzymes (NAD, NADH, NADP, and NADPH) and of ratios of their levels in the crystalline lens, retina, and tissue of the visual neocortex, as well as in the liver and blood, of rabbits subjected to long-lasting light stress (9-h-long sessions of exposure to light of mercury-tungsten lamps, daily, for 23 weeks, spectral range 350-1150 nm, and power flux density 30 mW/cm2). Parallel injections of α-tocopherol acetate and its short-chain analog 2-4-methyl3-pentenyl-6-acetohydroxy-2,5,7,8-tetramethyl chromane significantly compensated the light-stressinduced negative modifications of levels of reduced forms of nicotinamide co-enzymes in tissues of the rabbit visual analyzer, liver, and blood (especially ratios of NADPH/NADP levels under the action of an analog of vitamin E).

Keywords: light stress, polychromatic light, visual analyzer, nicotinamide co-enzymes, vitamin E, rabbits.

INTRODUCTION
Regulation of metabolic activity is a fundamental process maintaining homeostasis in cells, tissues, and organs. Such regulation plays a most important role in the adaptation of the visual analyzer to the action of different factors of the environment [1-4]. Under conditions of a few modern techniques using high-intensity light sources, the mechanisms of natural adaptation cannot always provide normal functioning of the visual analyzer [5-7]. Considering this, examination of the mechanisms of physiological and metabolic disturbances in tissues of the eye and also in the organism in general after exposures to intense light, as well as a search for the corresponding means of prophylaxis and increase in the resistivity of the organ of vision, is obviously necessary [3-8]. It is known that vitamin E (tocopherol), a most important antioxidant, significantly participates in regulation of the functioning of cell organelles and metabolism [9-13]. Nicotinamide co-enzymes, which play a crucial role in oxidation-reduction reactions, exert significant regulatory effects on
Filatov Institute of Ophthalmology and Tissue Therapy of the Academy of Medical Sciences of Ukraine, Odessa, Ukraine. Correspondence should be addressed to S. G. Kolomiychuk and N. F. Leus (e-mail: filatova_biochem@mail.ru).
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the rate and direction of metabolic processes in the cells. This is why disturbances of the redox state of pyridine nucleotides and intensification of the processes of peroxidation and free-radical oxidation can promote significant changes in the functional state of the visual analyzer. Such changes can be realized both in the peripheral (neurosensory cells, retinal pigment epithelium) and also in the central (visual neocortex) parts of this analyzer, as well as in the transparent media of the eye (crystalline lens, aqueous humor, and vitreous humor) [1, 3, 6, 11, 14]. In our study, we examined the possibility of controlling the metabolic process in tissues of the rabbit visual analyzer using injections of α-tocopherol and its short-chain analog under conditions of chronic action of high-intensity light (light stress). It is obvious that different physiological dysfunctions of the ocular organ can not only stem from changes in the intensity of metabolism directly in tissues of the visual analyzer but also from metabolic disturbance of the status of the organism as a whole. This is why we also studied metabolic indices in the blood and liver (contents of nicotinamide co-enzymes) under the above conditions [15-19].

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0090-2977/12/4402-0157 ? 2012 Springer Science+Business Media, Inc.

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METHODS
In our experiments, we used chinchilla rabbits. The animals ( n = 28) were subjected to total exposure to high-intensity light (daily, within the daytime, 9-h-long sessions) for 23 weeks. Two mercury-tungsten arc lamps (spectral range 3501150?nm, power flux density 30 mW/cm 2, and electrical power 750 W) served as the light sources [20]. The first group (9 animals) was exposed to isolated light action. The second and third groups (10 and 9 rabbits, respectively) additionally obtained, against the background of light stress, courses of injections of α-tocopherol acetate (TPhA) and its short-chain analog, 2-4-methyl-3-pentenyl6-acetohydroxy-2,5,7,8-tetramethyl chromane (TPhCh). These agents were kindly donated by the Palladin Institute of Biochemistry of the NAS of Ukraine. Three-course injections of TPhA (daily dose 25 mg/kg) and TPhCh in doses equimolar to those of α-tocopherol were performed. The courses included five intramuscular daily injections and were performed with a 1-month-long interval. The control group consistedx of animals kept under standard vivarium conditions at a standard level of illumination (15?rabbits). Throughout the experiment, the state of rabbit transparent media of the eye was controlled with the help of a slit lamp (Carl Zeiss, Germany), while that of the retina was controlled using an indirect binocular ophthalmoscope. The contents of nicotinamide co-enzymes (NAD, NADH, NADP, and NADPH) in the rabbit crystalline lens, retina, occipital cortex, liver, and blood were estimated using a standard spectrophotometric technique [21]. The obtained data were statistically processed using the t -test for independent samplings [22].

S. G. Kolomiychuk and N. F. Leus
lens, retina, and tissue of the cortical occipital parts were significantly ( P < 0.05) lower than those in the control (76.9, 70.0, and 80.6%, respectively; Fig. 1). In the crystalline lens, we observed only a trend toward decrease in the level of deoxidized NAD (this index was 83.8%, P > 0.05), while the levels of NADH in the retina and visual cortex (occipital lobes) were significantly ( Р < 0.05) lower than the corresponding control values. The level of NAD in the liver and the concentration of NADH in the blood and liver of the studied rabbits exposed to intense polychromic light were also significantly lower (Fig. 2). Ratios of the NAD/NADH levels in tissues of the visual analyzer of animals subjected to light stress demonstrated no significant changes, while in the blood and liver these indices shifted toward predominance of the oxidized forms. Data on the content of deoxidized NADP (taking into account that the involvement in regeneration of reduced glutathione at the expense of oxidation of NADPH is an important function of nicotinamide co-enzymes ) are of special interest [6]. Estimates of the levels of NADPH in tissues of experimental animals after light stress were indicative of a significant decrease in the content of this form of the co-enzyme in the crystalline lens (65.6%), retina (70.4%), and cortical occipital lobes (75.3% with respect to the control). It should be noted that the level of NADP in tissues of the visual analyzer under conditions of light stress did not differ significantly from the control values (Fig. 1). In the blood and liver of rabbits exposed to light stress, the levels of NADPH were 89.5 and 78% of the norm, respectively. The level of NADP in the blood decreased significantly (75.5%), but in the liver this index nearly corresponded to that in the control (Fig. 2). It should also be noted that, under conditions of exposure to high-intensity light, the reduction potential of the NADPH/NADP pair in the crystalline lens, retina, occipital cortical lobes, and liver was 29, 18, 14, 19% lower, while in the blood it was 18% higher than the respective figures in the control. After injections of TPhA and TPhCh, the level of oxidized NAD in tissues of the visual analyzer in animals subjected to light stress was lower than that in the control (as compared with the level of reduced NAD). A significantly higher level of NADH in tissues ( P < 0.05) was observed when we used the short-chain vitamin?Е analog (in the retina,

RESULTS
Our experiments showed that total chronic exposure of animals to polychromic highintensity light close in spectral range to sunlight induced decreases in the contents of nicotinamide co-enzymes not only in tissues of the visual analyzer but also in the blood and liver, as compared with the corresponding indices in the control group (Figs. 1 and 2). After exposure to the above-mentioned light stress, levels of oxidized NAD in the crystalline

Effects of α-Tocopherol on Metabolism under Light Stress Conditions A
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Fig. 1. Effects of vitamin E (tocopherol acetate, TPhA) and its short-chain analog (TPhCh) on the content of nicotinamide co-enzymes (nmol/g tissue) in tissues of the rabbit visual analyzer (panels А-C correspond to the crystalline lens, retina, and visual cortex, respectively). 1-4) Contents of NAD (1) NADH (2), NADP (3), and NADPH (4) in control animals (Contr.), rabbits subjected to light stress (LS), and stressed rabbits injected with TPhA and TPhCh (LS + TPhA and LS + TPhCh, respectively). Asterisks indicate cases of significant differences (Р < 0.05) from the values in the control group; crosses show those from the values in the LS group.

118.3%; in the occipital cortex, 120.6%). In the crystalline lens, we observed only a trend toward an increase, although clearly expressed (112.6%, Р > > 0.05), as compared with the corresponding indices in the group of stressed animals without injections of the above-mentioned agents (Fig. 1). In the blood and liver of the stressed animals injected with both TPhA and TPhCh, we found significantly higher levels of NADH compared to those in the former group . In these animal groups, the levels of oxidized NAD were lower than in the first group (Fig. 2). The oxidation potential of the NAD/NADH pair in the studied tissues of rabbits injected with TPhA and TPhCh decreased (mainly at the expense of changes

in the level of deoxidized NAD). The use of TPhA and TPhCh prevented drops in the level of NADPH in tissues of the visual analyzer of rabbits subjected to light stress; the most expressed changes were observed in the case where we used the derivative of vitamin?E (TPhCh; Fig. 1). In the blood and liver, we also observed normalization of the level of NADPH after injections of TPhA, while after injections of TPhCh the level of deoxidized NADP reached 120.5 and 117.3%, respectively (in both cases, Р < 0.05) with respect to analogous values in the control group (Fig. 2). In the examined tissues, the levels of oxidized NADP did not differ significantly from the control.

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S. G. Kolomiychuk and N. F. Leus A
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200 150 100 50 0

3

+

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450 400 350 300 250 200 150 100 50 0

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*+

Fig. 2. Effects of vitamin?E (tocopherol acetate, TPhA) and its short-chain analog (TPhCh) on the contents of nicotinamide coenzymes (nmol/g tissue) in the rabbit blood (A) and liver (B) under conditions of the norm and light stress (LS). Other designations are the same as in Fig. 1.

Therefore, the use of TPhA and TPhCh under conditions of light stress led to an appreciable rise in the NADPH/NADP ratios in tissues of the visual analyzer, blood, and liver at the expense of an increase in the level of the deoxidized form of this co-enzyme. The most expressed enhancement of the reduction potential of the NADPH/NADP pair was observed (precisely after TPhCh injections) in the crystalline lens (by 59%) and also in the liver (by 44% with respect to the corresponding indices in rabbits subjected to the isolated light influence).

DISCUSSION
Shifts of the levels and ratios of nicotinamide co-enzymes in tissues of the visual analyzer under conditions of the action of high-intensity light can, to a certain extent, result from photoinitiation of the processes of lipid peroxidation and free-radical oxidation [3, 14], which led to modifications of the activity of enzymes participating in synthesis and destruction of NAD and NADP. Under analogous conditions, we found a clearly pronounced

Effects of α-Tocopherol on Metabolism under Light Stress Conditions
reduction of the rate of synthesis of NAD in tissues of the eye, which is probably related to injury of the respective enzyme, nicotinamide mononucleotideadenylyl transferase [6]. It is known that the level of NAD in tissues is determined by not only the intensity of its biosynthesis but also by the activity of enzyme systems responsible for its splitting. In this relation, NAD-glycohydrolase can play the role of a significant regulator of the NAD level in the cell [23]. The effect of intense polychromatic light on the processes of synthesis of nicotinamide co-enzymes can also be of an indirect nature; it can be realized with the involvement of neurohumoral mechanisms of the stress reactivity controlling synthesis of the functioning proteins in the liver and other organs [24]. In our experiments, chronic intense light action led to a clearly pronounced drop in the reduction potential of nicotinamide co-enzymes in tissues of the experimental animals. A decrease in the NADPH/ NADP ratio in the examined tissues can be due to a drop in the intensity of generation of reduced NADP that is produced due to the activity of the pentose phosphate pathway [6, 25]. It is known that longlasting exposure to high-intensity polychromic light exerts a damaging effect on the membranes of lysosomes in cells of the eye tissues, including cells of the pigment epithelium of the retina. The activity of glucose-6-phosphate dehydrogenase decreases, the functioning of the antiradical system is suppressed, while the oxidation-reduction potential of glutathione drops [7, 25, 26]. Taking into account that reduced glutathione, which occupies a central position in the enzyme/ co-enzyme system of “extinction” of free radicals and peroxides, is, under such conditions, intensely consumed, while the processes of detoxication in the eye tissues and also in the organism in general are subjected to considerable stress, it is obvious that the maintenance of effective concentrations of the reduced NADP form in the crystalline lens and retina under the action of any disturbing factor, including intense photoillumination, is extraordinarily important [16, 25, 26]. The normal (or close to normal) redox status of nicotinamide co-enzymes and the glutathione system is the basis for the adequate state of the general redox system responsible for coordinated functioning of dehydrogenases, reductases, and peroxidases in different metabolic pathways. This determines, to a significant extent, the general

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state of regulation of metabolic processes. The ratios of NAD/NADH and NADPH/NADP are the most important regulatory factors with respect to dehydrogenases of the pentose-phosphate pathway, glycolysis, and lipogenesis; these factors determine the general direction of metabolic processes. The glutathione system is responsible for the maintenance of a rather high level of reduction of proteins in the tissues [1, 2, 16, 25-27]. Therefore, the chronic action of intense polychromic light results in noticeable disorders of the metabolic status of nicotinamide co-enzymes, which plays a leading role in the control of metabolic processes in tissues of the visual analyzer and also in the organism in whole. The use of α-tocopherol acetate (TPhA) and its short-chain analog, 2-4-methyl-3-pentenyl6-acetohydroxy-2,5,7,8-tetramethyl chromane (TPhCh), promotes under such conditions a significant increase in the level of reduced forms of nicotinamide co-enzymes in tissues of the visual analyzer, as well as in the blood and liver. A rise in the reduction potential of the ratio of pyridine nucleotides (especially NADPH/NADP ratios in the case where a short-chain analog of vitamin E is used) can promote the effective correction of the metabolic imbalance and provide relative stability of the protein and membrane components in the tissues under the action of disturbing factors of the environment, in particular under conditions of light stress.

REFERENCES
1. N. N. Velikii and P. K. Parkhomets, “Role of redox state of nicotinamide co-enzymes in the control of cellular metabolism,” Vitaminy , 9 , 3-15 (1976). 2. D. Holten, D. Procsal, and Y. Shang, “Regulation of pentose phosphate pathway dehydrogenases by NADP/ NADPH ratios,” Biochem. Biophys. Res. Commum. , 68 , No. 2, 436-441 (1976). 3. A. M. Azimova, A. L. Berman, E. G. Skvortsevich, et al., “Light-induced change in the activity of Na, K-ATPase of retinal photoreceptors in vertebrates: probable mechanism,” Biokhimiya , 45 , No. 4, 704-709 (1980). 4. N. S. Lutsenko and V. S. Yakushev, “Enzymatic activity of Krebs cycle in the rat visual analyzer in norm and stress,” Zh. Vyssh. Nerv. Deyat., 42 , No. 2, 357-362 (1992). 5. ?. V. Mal’tsev, V. V. Vit, S. N. Chernyayeva, and N. A. Bagirov, “Nonspecific effects of light on the organ of vision (Review),” Oftal’mol. Zh. , No. 2, 88-92 (1999). 6. N. F. Leus, I. P. Metelitsyna, T. V. Oleinik, et al., “Role of vitamins and co-enzymes in degenerative diseases of

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the organ of vision (review of the published and own studies),” Zh. Akad. Med. Nauk Ukr. , 11 , No. 4, 737-752 (2005). 7. S. V. Logvinov, E. Yu. Varakuta, and A. V. Potapov, “Lesion of neurosecretory retinal cells and retinal pigment epithelium of the rat eyes under the action of highly-intense visible light against the background of alloxan diabetes,” Radiats. Biol. Radioékol. , 45 , No. 6, 732-735 (2005). 8. N. Khettab, M. C. Amory, and G. Briand, “Photoprotective effect of vitamins A and E on polyamine and oxygenated free radical metabolism in hairless mouse epidermis,” Biochemie , 70 , No. 12, 1709-1713 (1988). 9. G. V. Petrova, Examination of the Role of Vitamin E and α-Tocopherol-Binding Proteins in the Functioning of Cellular Nucleus [in Russian], Abstract of Candidate’s Thesis in Biol. Sci., Kyiv (1992). 10. M. Koteghava, M. Sugiyama, K. Shoji, et al., “Effect of α-tocopherol on high energy phosphate metabolite levels in rat heart by P-NMR using a 20-Langendo V perfusion technique,” J. Mol. Cell Cardiol ., 25 , 10671074 (1993). 11. C. Behl, “Vitamin E and other antioxidant in neuro? protection,” Int. J. Vitam. Nutr. Res. , 69 , 213-219 (1999). 12. R. Brigelius-Flohe and M. G. Traber, “Vitamin E: function and metabolism,” FASEB J ., 13 , 1145-1155 (1999). 13. G. V. Petrova, “α-Tocopherol prevents antimycin? Aand oligomycin-induced death of rat thymocytes,” Ukr. Biokhim. Zh. , 81 , No. 2, 85-92 (2009). 14. E. B. Menshikov, V. Z. Lankin, N. K. Zenkov, et al., Oxidative Stress. Prooxidants and Antioxidants [in Russian], Slovo, Moscow (2006). 15. P. F. Jacques, L. T. Chylack, R. B. Mc Gandy, and S. C. Hartz, “Antioxidant status in persons with and without senile cataract,” Arch. Ophthalmol ., 106 , No. 3, 337-340 (1988). 16. N. F. Leus, “Lens coenzymes and cataract formation,” Lens Eye Toxicity Res ., 8 , Nos. 2/3, 353-371 (1991). 17. Sh. K. West, “Who develops cataracts?” Arch. Ophthalmol ., 109 , No. 2, 196-197 (1991). 18. I. P. Metelitsyna, S. G. Kolomiychuk, N. F. Leus, and L. I. Kravchenko, “Provision with some vitamins and

S. G. Kolomiychuk and N. F. Leus
redox-state of free nicotinamide coenzymes in patients with senile cataract,” Minerva Oftalmol. , 40 , No. 4, 245248 (1998). 19. A. M. Petrunya, Immune, Metabolic, and Micro? circulatory Disorders in Pathogenesis of Damage to the Visual Organ in Diseases of the Liver and Their Correction [in Ukrainian], Abstract of Doctoral Thesis in Med. Sci., Odessa (1996). 20. Patent of Ukraine No. 20178, MPK G 09 В 23/28, Technique for Modeling of Radiation Cataract [in Ukrainian], M. F. Leus, I. P. Metelitsyna, G. I. Drozh? zhina, E. F. Titarchyuok, and S. G. Kolomiychuk, Publ. December 25, 1997, Byull. No.?6. 21. F. Giblin and V. Reddy, “Pyridine nucleotide in ocular tissues as determined by the cycling assay,” Exp. Eye Res. , 31 , 601-609 (1980). 22. O. Yu. Rebrova, Statistical Analysis of Medical Data. The use of Applied STATISTICA Softwares [in Russian], Media Safera, Moscow (2003). 23. R. V. Chagovets, A. G. Khalmuradov, and C. I. Shushe? vich, “Change in the activity of NAD-ase in the liver under conditions of excess injection of nicotinic acid, 3-methylpyridine, and nicotinamide into rats,” Dokl. Akad. Nauk SSSR , 181 , No. 1, 245-247 (1968). 24. A. L. Greenbaum, L. B. Clark, and P. McLean, “The activities of nicotinamide mononucleotide adenylyl transferase and of nicotinamide-adenine dinucleotide kinase in the livers of rats subjected to different hormonal treatments,” Biochem. J. , 96 , 507-516 (1965). 25. ?. V. Mal’tsev, A. M. Alsharif Yasir, S. G. Kolomiychuk, et al., “System of generation of the reduction potential of nicotinamide co-enzymes of the crystalline lens, aqueous humor, and blood under conditions of cataractgenic influence of light radiation. Report I. Crystalline lens,” Oftal’mol. Zh. , No. 5, 70-75 (2003). 26. N. F. Leus, V. V. Savko, and O. Yu. Yurevich, “Light damage of the retina related to a decrease in the level of glutathione in the organism,” Oftal’mol. Zh ., No.?5, 67-70 (2004). 27. S. G. Kolomiychuk and N. F. Leus, “Effect of flavinate of the redox system of free nicotinamide co-enzymes in the crystalline lens of rabbit with experimental cataract,” Visn. Probl. Biol. Med. , 20 , 23-27 (1998).


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