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Esculetin, a Coumarin Derivative, Inhibits Aldose Reductase Activity in vitro and Cataractogenesis in Galactose-Fed Rats

  • Kim, Chan-Sik (Korean Medicine Convergence Research Division, Korea Institute of Oriental Medicine) ;
  • Kim, Junghyun (Korean Medicine Convergence Research Division, Korea Institute of Oriental Medicine) ;
  • Lee, Yun Mi (Korean Medicine Convergence Research Division, Korea Institute of Oriental Medicine) ;
  • Sohn, Eunjin (Korean Medicine Convergence Research Division, Korea Institute of Oriental Medicine) ;
  • Kim, Jin Sook (Korean Medicine Convergence Research Division, Korea Institute of Oriental Medicine)
  • Received : 2015.07.13
  • Accepted : 2015.11.20
  • Published : 2016.03.01

Abstract

Naturally occurring coumarin compounds have received substantial attention due to their pharmaceutical effects. Esculetin is a coumarin derivative and a polyphenol compound that is used in a variety of therapeutic and pharmacological strategies. However, its effect on aldose reductase activity remains poorly understood. In this study, the potential beneficial effects of esculetin on lenticular aldose reductase were investigated in galactose-fed (GAL) rats, an animal model of sugar cataracts. Cataracts were induced in Sprague-Dawley (SD) rats via a 50% galactose diet for 2 weeks, and groups of GAL rats were orally treated with esculetin (10 or 50 mg/kg body weight). In vehicle-treated GAL rats, lens opacification was observed, and swelling and membrane rupture of the lens fiber cells were increased. Additionally, aldose reductase was highly expressed in the lens epithelium and superficial cortical fibers during cataract development in the GAL rats. Esculetin reduced rat lens aldose reductase (RLAR) activity in vitro, and esculetin treatment significantly inhibited lens opacity, as well as morphological alterations, such as swelling, vacuolation and liquefaction of lens fibers, via the inhibition of aldose reductase in the GAL rats. These results indicate that esculetin is a useful treatment for galactose-induced cataracts.

Keywords

References

  1. Brubaker, A. N., DeRuiter, J. and Whitmer, W. L. (1986) Synthesis and rat lens aldose reductase inhibitory activity of some benzopyran- 2-ones. J. Med. Chem. 29, 1094-1099. https://doi.org/10.1021/jm00156a031
  2. Crabbe, M. J. and Goode, D. (1998) Aldose reductase: a window to the treatment of diabetic complications? Prog. Retin. Eye. Res. 17, 313-383. https://doi.org/10.1016/S1350-9462(97)00013-X
  3. de la Fuente, J. A. and Manzanaro, S. (2003) Aldose reductase inhibitors from natural sources. Nat. Prod. Rep. 20, 243-251. https://doi.org/10.1039/b204709h
  4. Dvornik, E., Simard-Duquesne, N., Krami, M., Sestanj, K., Gabbay, K. H., Kinoshita, J. H., Varma, S. D. and Merola, L. O. (1973) Polyol accumulation in galactosemic and diabetic rats: control by an aldose reductase inhibitor. Science 182, 1146-1148. https://doi.org/10.1126/science.182.4117.1146
  5. Egan, D., O'Kennedy, R., Moran, E., Cox, D., Prosser, E. and Thornes, R. D. (1990) The pharmacology, metabolism, analysis, and applications of coumarin and coumarin-related compounds. Drug. Metab. Rev. 22, 503-529. https://doi.org/10.3109/03602539008991449
  6. Jung, H. A., Islam, M. D., Kwon, Y. S., Jin, S. E., Son, Y. K., Park, J. J., Sohn, H. S. and Choi, J. S. (2011) Extraction and identification of three major aldose reductase inhibitors from Artemisia montana. Food. Chem. Toxicol. 49, 376-384. https://doi.org/10.1016/j.fct.2010.11.012
  7. Kador, P. F. and Kinoshita, J. H. (1984) Diabetic and galactosaemic cataracts. Ciba. Found. Symp. 106, 110-131.
  8. Kato, A., Minoshima, Y., Yamamoto, J., Adachi, I., Watson, A. A. and Nash, R. J. (2008) Protective effects of dietary chamomile tea on diabetic complications. J. Agric. Food. Chem. 56, 8206-8211. https://doi.org/10.1021/jf8014365
  9. Kawanishi, K., Ueda, H. and Moriyasu, M. (2003) Aldose reductase inhibitors from the nature. Curr. Med. Chem. 10, 1353-1374. https://doi.org/10.2174/0929867033457304
  10. Kim, J., Kim, C. S., Lee, Y. M., Sohn, E., Jo, K., Shin, S. D. and Kim, J. S. (2013) Scopoletin inhibits rat aldose reductase activity and cataractogenesis in galactose-fed rats. Evid. Based Complement. Alternat. Med. 2013, 787138.
  11. Kim, N. H., Kim, Y. S., Lee, Y. M., Jang, D. S. and Kim, J. S. (2010) Inhibition of aldose reductase and xylose-induced lens opacity by puerariafuran from the roots of Pueraria lobata. Biol. Pharm. Bull. 33, 1605-1609. https://doi.org/10.1248/bpb.33.1605
  12. Kim, Y. S., Kim, N. H., Jung, D. H., Jang, D. S., Lee, Y. M., Kim, J. M. and Kim, J. S. (2008) Genistein inhibits aldose reductase activity and high glucose-induced TGF-beta2 expression in human lens epithelial cells. Eur. J. Pharmacol. 594, 18-25. https://doi.org/10.1016/j.ejphar.2008.07.033
  13. Kinoshita, J. H. (1965) Cataracts in galactosemia. The Jonas S. Friedenwald Memorial Lecture. Invest. Ophthalmol. 4, 786-799.
  14. Kinoshita, J. H. (1974) Mechanisms initiating cataract formation. Proctor Lecture. Invest. Ophthalmol. 13, 713-724.
  15. Kinoshita, J. H., Kador, P. and Catiles, M. (1981) Aldose reductase in diabetic cataracts. JAMA 246, 257-261. https://doi.org/10.1001/jama.1981.03320030049032
  16. Kok, S. H., Yeh, C. C., Chen, M. L. and Kuo, M. Y. (2009) Esculetin enhances TRAIL-induced apoptosis through DR5 upregulation in human oral cancer SAS cells. Oral. Oncol. 45, 1067-1072. https://doi.org/10.1016/j.oraloncology.2009.07.018
  17. Lee, J., Kim, N. H., Nam, J. W., Lee, Y. M., Jang, D. S., Kim, Y. S., Nam, S. H., Seo, E. K., Yang, M. S. and Kim, J. S. (2010) Scopoletin from the flower buds of Magnolia fargesii inhibits protein glycation, aldose reductase, and cataractogenesis ex vivo. Arch. Pharm. Res. 33, 1317-1323. https://doi.org/10.1007/s12272-010-0904-z
  18. Lin, W. L., Wang, C. J., Tsai, Y. Y., Liu, C. L., Hwang, J. M. and Tseng, T. H. (2000) Inhibitory effect of esculetin on oxidative damage induced by t-butyl hydroperoxide in rat liver. Arch. Toxicol. 74, 467-472. https://doi.org/10.1007/s002040000148
  19. Lizak, M. J., Secchi, E. F., Lee, J. W., Sato, S., Kubo, E., Akagi, Y. and Kador, P. F. (1998) 3-FG as substrate for investigating flux through the polyol pathway in dog lens by 19F-NMR spectroscopy. Invest. Ophthalmol. Vis. Sci. 39, 2688-2695.
  20. Manzanaro, S., Salva, J. and de la Fuente, J. A. (2006) Phenolic marine natural products as aldose reductase inhibitors. J. Nat. Prod. 69, 1485-1487. https://doi.org/10.1021/np0503698
  21. Murata, M., Ohta, N., Sakurai, S., Alam, S., Tsai, J., Kador, P. F. and Sato, S. (2001) The role of aldose reductase in sugar cataract formation: aldose reductase plays a key role in lens epithelial cell death (apoptosis). Chem. Biol. Interact. 130-132, 617-625. https://doi.org/10.1016/S0009-2797(00)00289-1
  22. Okuda, J., Miwa, I., Inagaki, K., Horie, T. and Nakayama, M. (1982) Inhibition of aldose reductases from rat and bovine lenses by flavonoids. Biochem. Pharmacol. 31, 3807-3822. https://doi.org/10.1016/0006-2952(82)90297-0
  23. Patterson, J. W. and Bunting, K. W. (1966) Sugar cataracts, polyol levels and lens swelling. Doc. Ophthalmol. 20, 64-72.
  24. Peyroux, J. and Sternberg, M. (2006) Advanced glycation endproducts (AGEs): Pharmacological inhibition in diabetes. Pathol. Biol. (Paris) 54, 405-419. https://doi.org/10.1016/j.patbio.2006.07.006
  25. Prabakaran, D. and Ashokkumar, N. (2013) Protective effect of esculetin on hyperglycemia-mediated oxidative damage in the hepatic and renal tissues of experimental diabetic rats. Biochimie. 95, 366-373. https://doi.org/10.1016/j.biochi.2012.10.008
  26. Subramaniam, S. R. and Ellis, E. M. (2011) Esculetin-induced protection of human hepatoma HepG2 cells against hydrogen peroxide is associated with the Nrf2-dependent induction of the NAD(P)H: Quinone oxidoreductase 1 gene. Toxicol. Appl. Pharmacol. 250, 130-136. https://doi.org/10.1016/j.taap.2010.09.025
  27. Tomlinson, D. R., Stevens, E. J. and Diemel, L. T. (1994) Aldose reductase inhibitors and their potential for the treatment of diabetic complications. Trends Pharmacol. Sci. 15, 293-297. https://doi.org/10.1016/0165-6147(94)90010-8
  28. Unakar, N. J. and Tsui, J. Y. (1983) Inhibition of galactose-induced alterations in ocular lens with sorbinil. Exp. Eye. Res. 36, 685-694. https://doi.org/10.1016/0014-4835(83)90106-9
  29. Veeresham, C., Rama Rao, A. and Asres, K. (2014) Aldose reductase inhibitors of plant origin. Phytother. Res. 28, 317-333. https://doi.org/10.1002/ptr.5000
  30. Wang, C. J., Hsieh, Y. J., Chu, C. Y., Lin, Y. L. and Tseng, T. H. (2002) Inhibition of cell cycle progression in human leukemia HL-60 cells by esculetin. Cancer Lett. 183, 163-168. https://doi.org/10.1016/S0304-3835(02)00031-9
  31. Wang, Z., Ling, B., Zhang, R. and Liu, Y. (2008) Docking and molecular dynamics study on the inhibitory activity of coumarins on aldose reductase. J. Phys. Chem. B. 112, 10033-10040. https://doi.org/10.1021/jp8033227

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