Nutrition Research and Practice

The Korean Nutrition Society (한국영양학회)
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Epigallocatechin gallate attenuates L-DOPA-induced apoptosis in rat PC12 cells

  • Lee, Myung-Yul (Department of Food and Nutrition, College of Natural Science, Chosun University) ;
  • Choi, Eun Joo (College of Pharmacy, Chosun University) ;
  • Lee, Myung-Koo (College of Pharmacy, Chungbuk National University) ;
  • Lee, Jae-Joon (Department of Food and Nutrition, College of Natural Science, Chosun University)
  • Received : 2013.01.11
  • Accepted : 2013.05.16
  • Published : 2013.08.01
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Abstract

In this study, the protective effects of EGCG on L-3,4-dihydroxyphenylalanine (L-DOPA)-induced oxidative cell death in catecholaminergic PC12 cells, the in vitro model of Parkinson's disease, were investigated. Treatment with L-DOPA at concentrations higher than $150{\mu}M$ caused cytotoxicity in PC12 cells, as determined using the 3-(4,5-dimetylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay and flow cytometry detection. The apoptotic ratio was similar in cells treated with $100{\mu}M$ EGCG plus $150{\mu}M$ L-DOPA (5.02%) and the control (0.96%) (P > 0.05), and was lower than that of cells treated with L-DOPA only (32.24%, P < 0.05). The generation level of ROS (% of control) in cells treated with EGCG plus L-DOPA was lower than that in cells treated with L-DOPA only (123.90% vs 272.32%, P < 0.05). The optical density in production of TBARS in cells treated with L-DOPA only was higher than that in the control ($0.27{\pm}0.05$ vs $0.08{\pm}0.04$, P < 0.05), and in cells treated with EGCG only ($0.14{\pm}0.02$, P < 0.05), and EGCG plus L-DOPA ($0.13{\pm}0.02$, P < 0.05). The intracellular level of GSH in cells treated with EGCG plus L-DOPA was higher than that in cells treated with L-DOPA only ($233.25{\pm}16.44$ vs $119.23{\pm}10.25$, P < 0.05). These results suggest that EGCG protects against L-DOPA-induced oxidative apoptosis in PC12 cells, and might be a potent neuroprotective agent.

Keywords

References

  1. Agid Y. Parkinson's disease: pathophysiology. Lancet 1991;337:1321-4. https://doi.org/10.1016/0140-6736(91)92989-F
  2. Lee JJ, Kim YM, Yin SY, Park HD, Kang MH, Hong JT, Lee MK. Aggravation of L-DOPA-induced neurotoxicity by tetrahydropapaveroline in PC12 cells. Biochem Pharmacol 2003;66:1787-95. https://doi.org/10.1016/S0006-2952(03)00421-0
  3. Migheli R, Godani C, Sciola L, Delogu MR, Serra PA, Zangani D, De Natale G, Miele E, Desole MS. Enhancing effect of manganese on L-DOPA-induced apoptosis in PC12 cells: role of oxidative stress. J Neurochem 1999;73:1155-63.
  4. Spencer JP, Jenner P, Halliwell B. Superoxide-dependent depletion of reduced glutathione by L-DOPA and dopamine. Relevance to Parkinson's disease. Neuroreport 1995;6:1480-4. https://doi.org/10.1097/00001756-199507310-00004
  5. Hirsch EC. Biochemistry of Parkinson's disease with special reference to the dopaminergic systems. Mol Neurobiol 1994;9:135-42. https://doi.org/10.1007/BF02816113
  6. Mizuno Y, Ikebe S, Hattori N, Nakagawa-Hattori Y, Mochizuki H, Tanaka M, Ozawa T. Role of mitochondria in the etiology and pathogenesis of Parkinson's disease. Biochim Biophys Acta 1995;1271:265-74. https://doi.org/10.1016/0925-4439(95)00038-6
  7. Dexter DT, Carter CJ, Wells FR, Javoy-Agid F, Agid Y, Lees A, Jenner P, Marsden CD. Basal lipid peroxidation in substantia nigra is increased in Parkinson's disease. J Neurochem 1989;52:381-9. https://doi.org/10.1111/j.1471-4159.1989.tb09133.x
  8. Chung KK, Dawson VL, Dawson TM. New insights into Parkinson's disease. J Neurol 2003;250 Suppl 3:III15-24. https://doi.org/10.1007/s00415-003-1103-1
  9. Heo HJ, Choi SJ, Choi SG, Shin DH, Lee JM, Lee CY. Effects of banana, orange, and apple on oxidative stress-induced neurotoxicity in PC12 cells. J Food Sci 2008;73:H28-32. https://doi.org/10.1111/j.1750-3841.2007.00632.x
  10. Bastianetto S, Zheng WH, Quirion R. The Ginkgo biloba extract (EGb 761) protects and rescues hippocampal cells against nitric oxide-induced toxicity: involvement of its flavonoid constituents and protein kinase C. J Neurochem 2000;74:2268-77.
  11. Bordoni A, Hrelia S, Angeloni C, Giordano E, Guarnieri C, Caldarera CM, Biagi PL. Green tea protection of hypoxia/ reoxygenation injury in cultured cardiac cells. J Nutr Biochem 2002;13:103-11. https://doi.org/10.1016/S0955-2863(01)00203-0
  12. Nie G, Jin C, Cao Y, Shen S, Zhao B. Distinct effects of tea catechins on 6-hydroxydopamine-induced apoptosis in PC12 cells. Arch Biochem Biophys 2002;397:84-90. https://doi.org/10.1006/abbi.2001.2636
  13. Song DU, Jung YD, Chay KO, Chung MA, Lee KH, Yang SY, Shin BA, Ahn BW. Effect of drinking green tea on ageassociated accumulation of Maillard-type fluorescence and carbonyl groups in rat aortic and skin collagen. Arch Biochem Biophys 2002;397:424-9. https://doi.org/10.1006/abbi.2001.2695
  14. Dong Z, Ma W, Huang C, Yang CS. Inhibition of tumor promoterinduced activator protein 1 activation and cell transformation by tea polyphenols, (-)-epigallocatechin gallate, and theaflavins. Cancer Res 1997;57:4414-9.
  15. Guo Q, Zhao B, Li M, Shen S, Xin W. Studies on protective mechanisms of four components of green tea polyphenols against lipid peroxidation in synaptosomes. Biochim Biophys Acta 1996;1304:210-22. https://doi.org/10.1016/S0005-2760(96)00122-1
  16. Guo Q, Zhao B, Shen S, Hou J, Hu J, Xin W. ESR study on the structure-antioxidant activity relationship of tea catechins and their epimers. Biochim Biophys Acta 1999;1427:13-23. https://doi.org/10.1016/S0304-4165(98)00168-8
  17. Jin CF, Shen SR Sr, Zhao BL. Different effects of five catechins on 6-hydroxydopamine-induced apoptosis in PC12 cells. J Agric Food Chem 2001;49:6033-8. https://doi.org/10.1021/jf010903r
  18. Levites Y, Youdim MB, Maor G, Mandel S. Attenuation of 6-hydroxydopamine (6-OHDA)-induced nuclear factor-kappaB (NF-kappaB) activation and cell death by tea extracts in neuronal cultures. Biochem Pharmacol 2002;63:21-9. https://doi.org/10.1016/S0006-2952(01)00813-9
  19. Yoneda T, Hiramatsu M, Sakamoto M, Togasaki K, Komatsu M, Yamaguchi K. Antioxidant effects of "beta catechin". Biochem Mol Biol Int 1995;35:995-1008.
  20. Koh SH, Kim SH, Kwon H, Park Y, Kim KS, Song CW, Kim J, Kim MH, Yu HJ, Henkel JS, Jung HK. Epigallocatechin gallate protects nerve growth factor differentiated PC12 cells from oxidative-radical-stress-induced apoptosis through its effect on phosphoinositide 3-kinase/Akt and glycogen synthase kinase-3. Brain Res Mol Brain Res 2003;118:72-81. https://doi.org/10.1016/j.molbrainres.2003.07.003
  21. Casarejos MJ, Solano RM, Menéndez J, Rodríguez-Navarro JA, Correa C, García de Yébenes J, Mena MA. Differential effects of L-DOPA on monoamine metabolism, cell survival and glutathione production in midbrain neuronal-enriched cultures from parkin knockout and wild-type mice. J Neurochem 2005;94:1005-14. https://doi.org/10.1111/j.1471-4159.2005.03249.x
  22. Walkinshaw G, Waters CM. Induction of apoptosis in catecholaminergic PC12 cells by L-DOPA. Implications for the treatment of Parkinson's disease. J Clin Invest 1995;95:2458-64. https://doi.org/10.1172/JCI117946
  23. Boyce S, Rupniak NM, Steventon MJ, Iversen SD. Nigrostriatal damage is required for induction of dyskinesias by L-DOPA in squirrel monkeys. Clin Neuropharmacol 1990;13:448-58. https://doi.org/10.1097/00002826-199010000-00006
  24. Cheng N, Maeda T, Kume T, Kaneko S, Kochiyama H, Akaike A, Goshima Y, Misu Y. Differential neurotoxicity induced by L-DOPA and dopamine in cultured striatal neurons. Brain Res 1996;743:278-83. https://doi.org/10.1016/S0006-8993(96)01056-6
  25. Basma AN, Morris EJ, Nicklas WJ, Geller HM. L-DOPA cytotoxicity to PC12 cells in culture is via its autoxidation. J Neurochem 1995;64:825-32.
  26. Greene LA, Tischler AS. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A 1976;73:2424-8. https://doi.org/10.1073/pnas.73.7.2424
  27. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983;65:55-63. https://doi.org/10.1016/0022-1759(83)90303-4
  28. Gunasekar PG, Kanthasamy AG, Borowitz JL, Isom GE. NMDA receptor activation produces concurrent generation of nitric oxide and reactive oxygen species: implication for cell death. J Neurochem 1995;65:2016-21.
  29. Draper HH, Hadley M. Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol 1990;186:421-31. https://doi.org/10.1016/0076-6879(90)86135-I
  30. Griffith OW. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 1980;106:207-12. https://doi.org/10.1016/0003-2697(80)90139-6
  31. Raza H, John A. In vitro effects of tea polyphenols on redox metabolism, oxidative stress, and apoptosis in PC12 cells. Ann N Y Acad Sci 2008;1138:358-65. https://doi.org/10.1196/annals.1414.037
  32. Watanabe H, Kobayashi A, Yamamoto T, Suzuki S, Hayashi H, Yamazaki N. Alterations of human erythrocyte membrane fluidity by oxygen-derived free radicals and calcium. Free Radic Biol Med 1990;8:507-14. https://doi.org/10.1016/0891-5849(90)90150-H
  33. Zeevalk GD, Bernard LP, Albers DS, Mirochnitchenko O, Nicklas WJ, Sonsalla PK. Energy stress-induced dopamine loss in glutathione peroxidase-overexpressing transgenic mice and in glutathionedepleted mesencephalic cultures. J Neurochem 1997;68:426-9.
  34. Levites Y, Weinreb O, Maor G, Youdim MB, Mandel S. Green tea polyphenol (-)-epigallocatechin-3-gallate prevents N-methyl- 4-phenyl-1,2,3,6-tetrahydropyridine-induced dopaminergic neurodegeneration. J Neurochem 2001;78:1073-82. https://doi.org/10.1046/j.1471-4159.2001.00490.x
  35. Levites Y, Youdim MB, Maor G, Mandel S. Attenuation of 6-hydroxydopamine (6-OHDA)-induced nuclear factor-kappaB (NF-kappaB) activation and cell death by tea extracts in neuronal cultures. Biochem Pharmacol 2002;63:21-9. https://doi.org/10.1016/S0006-2952(01)00813-9
  36. Levites Y, Amit T, Mandel S, Youdim MB. Neuroprotection and neurorescue against Abeta toxicity and PKC-dependent release of nonamyloidogenic soluble precursor protein by green tea polyphenol (-)-epigallocatechin-3-gallate. FASEB J 2003;17:952-4.
  37. Jeong JH, Kim HJ, Lee TJ, Kim MK, Park ES, Choi BS. Epigallocatechin 3-gallate attenuates neuronal damage induced by 3-hydroxykynurenine. Toxicology 2004;195:53-60. https://doi.org/10.1016/j.tox.2003.08.007
  38. Jung JY, Mo HC, Yang KH, Jeong YJ, Yoo HG, Choi NK, Oh WM, Oh HK, Kim SH, Lee JH, Kim HJ, Kim WJ. Inhibition by epigallocatechin gallate of CoCl2-induced apoptosis in rat PC12 cells. Life Sci 2007;80:1355-63. https://doi.org/10.1016/j.lfs.2006.11.033
  39. Inanami O, Watanabe Y, Syuto B, Nakano M, Tsuji M, Kuwabara M. Oral administration of (-)catechin protects against ischemiareperfusion- induced neuronal death in the gerbil. Free Radic Res 1998;29:359-65. https://doi.org/10.1080/10715769800300401
  40. Seyfried J, Soldner F, Schulz JB, Klockgether T, Kovar KA, Wullner U. Differential effects of L-buthionine sulfoximine and ethacrynic acid on glutathione levels and mitochondrial function in PC12 cells. Neurosci Lett 1999;264:1-4. https://doi.org/10.1016/S0304-3940(99)00107-X
  41. Wüllner U, Löschmann PA, Schulz JB, Schmid A, Dringen R, Eblen F, Turski L, Klockgether T. Glutathione depletion potentiates MPTP and MPP+ toxicity in nigral dopaminergic neurones. Neuroreport 1996;7:921-3. https://doi.org/10.1097/00001756-199603220-00018
  42. Raza H, John A. Green tea polyphenol epigallocatechin-3-gallate differentially modulates oxidative stress in PC12 cell compartments. Toxicol Appl Pharmacol 2005;207:212-20. https://doi.org/10.1016/j.taap.2005.01.004
  43. Skrzydlewska E, Ostrowska J, Farbiszewski R, Michalak K. Protective effect of green tea against lipid peroxidation in the rat liver, blood serum and the brain. Phytomedicine 2002;9:232-8. https://doi.org/10.1078/0944-7113-00119

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