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Green tea polyphenol (-)-epigallocatechin-3-gallate prevents ultraviolet-induced apoptosis in PC12 cells

  • Woo, Su-Mi (Department of Oral Physiology, Dental Science Research Institute, School of Dentistry, Chonnam National University) ;
  • Kim, Yoon-Jung (Department of Oral Physiology, Dental Science Research Institute, School of Dentistry, Chonnam National University) ;
  • Cai, Bangrong (School of Pharmacy, Henan University of Traditional Chinese Medicine) ;
  • Park, Sam-Young (Department of Oral Physiology, Dental Science Research Institute, School of Dentistry, Chonnam National University) ;
  • Kim, Young (Department of Oral Pathology, Dental Science Research Institute, School of Dentistry, Chonnam National University) ;
  • Kim, Ok Joon (Department of Oral Pathology, Dental Science Research Institute, School of Dentistry, Chonnam National University) ;
  • Kang, In-Chol (Department of Oral Microbiology, Dental Science Research Institute, School of Dentistry, Chonnam National University) ;
  • Kim, Won-Jae (Department of Oral Physiology, Dental Science Research Institute, School of Dentistry, Chonnam National University) ;
  • Jung, Ji-Yeon (Department of Oral Physiology, Dental Science Research Institute, School of Dentistry, Chonnam National University)
  • Received : 2020.11.03
  • Accepted : 2020.11.11
  • Published : 2020.12.31

Abstract

Green tea polyphenol (-)-epigallocatechin-3-gallate (EGCG) is a potent antioxidant with protective effects against neurotoxicity. However, it is currently unclear whether EGCG protects neuronal cells against radiation-induced damage. Therefore, the objective of this study was to investigate the effects of EGCG on ultraviolet (UV)-induced oxidative stress and apoptosis in PC12 cells. The effects of UV irradiation included apoptotic cell death, which was associated with DNA fragmentation, reactive oxygen species (ROS) production, enhanced caspase-3 and caspase-9 activity, and poly (ADP-ribose) polymerase cleavage. UV irradiation also increased the Bax/Bcl-2 ratio and mitochondrial pathway-associated cytochrome c expression. However, pretreatment with EGCG before UV exposure markedly decreased UV-induced DNA fragmentation and ROS production. Furthermore, the UV irradiation-induced increase in Bax/Bcl-2 ratio, cytochrome c upregulation, and caspase-3 and caspase-9 activation were each ameliorated by EGCG pretreatment. Additionally, EGCG suppressed UV-induced phosphorylation of p38 and rescued UV-downregulated phosphorylation of ERK. Taken together, these results suggest that EGCG prevents UV irradiation-induced apoptosis in PC12 cells by scavenging ROS and inhibiting the mitochondrial pathways known to play a crucial role in apoptosis. In addition, EGCG inhibits UV-induced apoptosis via JNK inactivation and ERK activation in PC12 cells. Thus, EGCG represents a potential neuroprotective agent that could be applied to prevent neuronal cell death induced by UV irradiation.

Keywords

References

  1. Matsumura Y, Ananthaswamy HN. Toxic effects of ultraviolet radiation on the skin. Toxicol Appl Pharmacol 2004;195:298-308. doi: 10.1016/j.taap.2003.08.019.
  2. Melnikova VO, Ananthaswamy HN. Cellular and molecular events leading to the development of skin cancer. Mutat Res 2005;571:91-106. doi: 10.1016/j.mrfmmm.2004.11.015.
  3. Masuma R, Kashima S, Kurasaki M, Okuno T. Effects of UV wavelength on cell damages caused by UV irradiation in PC12 cells. J Photochem Photobiol B 2013;125:202-8. doi: 10.1016/j.jphotobiol.2013.06.003.
  4. Jiang W, Ananthaswamy HN, Muller HK, Kripke ML. p53 protects against skin cancer induction by UV-B radiation. Oncogene 1999;18:4247-53. doi: 10.1038/sj.onc.1202789.
  5. Subrahmanyam K, Rao KS. Ultraviolet light-induced unscheduled DNA-synthesis in isolated neurons of rat brain of different ages. Mech Ageing Dev 1991;57:283-91. doi: 10.1016/0047-6374(91)90053-3.
  6. Griffiths HR, Mistry P, Herbert KE, Lunec J. Molecular and cellular effects of ultraviolet light-induced genotoxicity. Crit Rev Clin Lab Sci 1998;35:189-237. doi: 10.1080/10408369891234192.
  7. Kulms D, Schwarz T. Molecular mechanisms of UV-induced apoptosis. Photodermatol Photoimmunol Photomed 2000;16:195-201. doi: 10.1034/j.1600-0781.2000.160501.x.
  8. Kulms D, Schwarz T. Molecular mechanisms involved in UV-induced apoptotic cell death. Skin Pharmacol Appl Skin Physiol 2002;15:342-7. doi: 10.1159/000064539.
  9. McCollum AT, Nasr P, Estus S. Calpain activates caspase-3 during UV-induced neuronal death but only calpain is necessary for death. J Neurochem 2002;82:1208-20. doi: 10.1046/j.1471-4159.2002.01057.x.
  10. McCollum AT, Estus S. NGF acts via p75 low-affinity neurotrophin receptor and calpain inhibition to reduce UV neurotoxicity. J Neurosci Res 2004;77:552-64. doi: 10.1002/jnr.20184.
  11. Green DR, Reed JC. Mitochondria and apoptosis. Science 1998;281:1309-12. doi: 10.1126/science.281.5381.1309.
  12. Hengartner MO. The biochemistry of apoptosis. Nature 2000;407:770-6. doi: 10.1038/35037710.
  13. Cohen GM. Caspases: the executioners of apoptosis. Biochem J 1997;326(Pt 1):1-16. doi: 10.1042/bj3260001.
  14. Wolf BB, Green DR. Suicidal tendencies: apoptotic cell death by caspase family proteinases. J Biol Chem 1999;274:20049-52. doi: 10.1074/jbc.274.29.20049.
  15. Kroemer G. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat Med 1997;3:614-20. doi: 10.1038/nm0697-614.
  16. Reed JC. Double identity for proteins of the Bcl-2 family. Nature 1997;387:773-6. doi: 10.1038/42867.
  17. Landis-Piwowar KR, Huo C, Chen D, Milacic V, Shi G, Chan TH, Dou QP. A novel prodrug of the green tea polyphenol (-)-epigallocatechin-3-gallate as a potential anticancer agent. Cancer Res 2007;67:4303-10. doi: 10.1158/0008-5472.CAN-06-4699.
  18. Rashidi B, Malekzadeh M, Goodarzi M, Masoudifar A, Mirzaei H. Green tea and its anti-angiogenesis effects. Biomed Pharmacother 2017;89:949-56. doi: 10.1016/j.biopha.2017.01.161.
  19. Gao X, Lin X, Li X, Zhang Y, Chen Z, Li B. Cellular antioxidant, methylglyoxal trapping, and anti-inflammatory activities of cocoa tea (Camellia ptilophylla Chang). Food Funct 2017;8:2836-46. doi: 10.1039/c7fo00368d.
  20. Singh BN, Shankar S, Srivastava RK. Green tea catechin, epigallocatechin-3-gallate (EGCG): mechanisms, perspectives and clinical applications. Biochem Pharmacol 2011;82:1807-21. doi: 10.1016/j.bcp.2011.07.093.
  21. Eng QY, Thanikachalam PV, Ramamurthy S. Molecular understanding of Epigallocatechin gallate (EGCG) in cardiovascular and metabolic diseases. J Ethnopharmacol 2018;210:296-310. doi: 10.1016/j.jep.2017.08.035.
  22. Steinmann J, Buer J, Pietschmann T, Steinmann E. Anti-infective properties of epigallocatechin-3-gallate (EGCG), a component of green tea. Br J Pharmacol 2013;168:1059-73. doi: 10.1111/bph.12009.
  23. Itoh T, Imano M, Nishida S, Tsubaki M, Hashimoto S, Ito A, Satou T. (-)-Epigallocatechin-3-gallate protects against neuronal cell death and improves cerebral function after traumatic brain injury in rats. Neuromolecular Med 2011;13:300-9. doi: 10.1007/s12017-011-8162-x.
  24. Singh NA, Mandal AK, Khan ZA. Potential neuroprotective properties of epigallocatechin-3-gallate (EGCG). Nutr J 2016; 15:60. doi: 10.1186/s12937-016-0179-4.
  25. Mandel S, Weinreb O, Amit T, Youdim MB. Cell signaling pathways in the neuroprotective actions of the green tea polyphenol (-)-epigallocatechin-3-gallate: implications for neurodegenerative diseases. J Neurochem 2004;88:1555-69. doi: 10.1046/j.1471-4159.2003.02291.x.
  26. Abu-Raya S, Blaugrund E, Trembovler V, Lazarovici P. Rasagiline, a novel monoamine oxidase-B inhibitor with neuroprotective effects under ischemic conditions in PC12 cells. Drug Dev Res 2000;50:285-90. doi: 10.1002/1098-2299(200007/08)50:3/4<285::AID-DDR11>3.0.CO;2-8.
  27. 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. doi: 10.1073/pnas.73.7.2424.
  28. Salakou S, Kardamakis D, Tsamandas AC, Zolota V, Apostolakis E, Tzelepi V, Papathanasopoulos P, Bonikos DS, Papapetropoulos T, Petsas T, Dougenis D. Increased Bax/Bcl-2 ratio up-regulates caspase-3 and increases apoptosis in the thymus of patients with myasthenia gravis. In Vivo 2007;21:123-32.
  29. Friedlander RM. Apoptosis and caspases in neurodegenerative diseases. N Engl J Med 2003;348:1365-75. doi: 10.1056/NEJMra022366.
  30. McIlwain DR, Berger T, Mak TW. Caspase functions in cell death and disease. Cold Spring Harb Perspect Biol 2015;7:a026716. doi: 10.1101/cshperspect.a026716.
  31. Boulares AH, Yakovlev AG, Ivanova V, Stoica BA, Wang G, Iyer S, Smulson M. Role of poly(ADP-ribose) polymerase (PARP) cleavage in apoptosis. Caspase 3-resistant PARP mutant increases rates of apoptosis in transfected cells. J Biol Chem 1999;274:22932-40. doi: 10.1074/jbc.274.33.22932.
  32. Zhang W, Liu HT. MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell Res 2002;12:9-18. doi: 10.1038/sj.cr.7290105.
  33. Valencia A, Moran J. Reactive oxygen species induce different cell death mechanisms in cultured neurons. Free Radic Biol Med 2004;36:1112-25. doi: 10.1016/j.freeradbiomed.2004.02.013.
  34. Levites Y, Amit T, Youdim MB, Mandel S. Involvement of protein kinase C activation and cell survival/ cell cycle genes in green tea polyphenol (-)-epigallocatechin 3-gallate neuroprotective action. J Biol Chem 2002;277:30574-80. doi: 10.1074/jbc.M202832200.
  35. Weinreb O, Mandel S, Amit T, Youdim MB. Neurological mechanisms of green tea polyphenols in Alzheimer's and Parkinson's diseases. J Nutr Biochem 2004;15:506-16. doi: 10.1016/j.jnutbio.2004.05.002.
  36. Seong KJ, Lee HG, Kook MS, Ko HM, Jung JY, Kim WJ. Epigallocatechin-3-gallate rescues LPS-impaired adult hippocampal neurogenesis through suppressing the TLR4-NF-κB signaling pathway in mice. Korean J Physiol Pharmacol 2016;20:41-51. doi: 10.4196/kjpp.2016.20.1.41.
  37. de Jager TL, Cockrell AE, Du Plessis SS. Ultraviolet light induced generation of reactive oxygen species. Adv Exp Med Biol 2017;996:15-23. doi: 10.1007/978-3-319-56017-5_2.
  38. Basu A, Sanchez K, Leyva MJ, Wu M, Betts NM, Aston CE, Lyons TJ. Green tea supplementation affects body weight, lipids, and lipid peroxidation in obese subjects with metabolic syndrome. J Am Coll Nutr 2010;29:31-40. doi: 10.1080/07315724.2010.10719814.
  39. Katiyar SK, Afaq F, Perez A, Mukhtar H. Green tea polyphenol (-)-epigallocatechin-3-gallate treatment of human skin inhibits ultraviolet radiation-induced oxidative stress. Carcinogenesis 2001;22:287-94. doi: 10.1093/carcin/22.2.287.
  40. Yan J, Zhao Y, Suo S, Liu Y, Zhao B. Green tea catechins ameliorate adipose insulin resistance by improving oxidative stress. Free Radic Biol Med 2012;52:1648-57. doi: 10.1016/j.freeradbiomed.2012.01.033.
  41. He Y, Tan D, Mi Y, Bai B, Jiang D, Zhou X, Ji S. Effect of epigallocatechin-3-gallate on acrylamide-induced oxidative stress and apoptosis in PC12 cells. Hum Exp Toxicol 2017;36:1087-99. doi: 10.1177/0960327116681648.
  42. Ye Q, Ye L, Xu X, Huang B, Zhang X, Zhu Y, Chen X. Epigallocatechin-3-gallate suppresses 1-methyl-4-phenyl-pyridine-induced oxidative stress in PC12 cells via the SIRT1/PGC-1α signaling pathway. BMC Complement Altern Med 2012;12:82. doi: 10.1186/1472-6882-12-82.
  43. Rolland SG, Conradt B. New role of the BCL2 family of proteins in the regulation of mitochondrial dynamics. Curr Opin Cell Biol 2010;22:852-8. doi: 10.1016/j.ceb.2010.07.014.
  44. Bossy-Wetzel E, Newmeyer DD, Green DR. Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVDspecific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J 1998;17:37-49. doi: 10.1093/emboj/17.1.37.
  45. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997;91:479-89. doi: 10.1016/s0092-8674(00)80434-1.
  46. Fan TJ, Han LH, Cong RS, Liang J. Caspase family proteases and apoptosis. Acta Biochim Biophys Sin (Shanghai) 2005;37:719-27. doi: 10.1111/j.1745-7270.2005.00108.x.