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Phenylpropanoids in radioregulation: double edged sword

  • Kim, Wan-Yeon (College of Natural Sciences, Department of Biological Sciences, Pusan National University) ;
  • Seong, Ki-Moon (Division of Radiation Effect Research, Radiation Health Research Institute, Korea Hydro and Nuclear Power Co., Ltd.) ;
  • Youn, Bu-Hyun (College of Natural Sciences, Department of Biological Sciences, Pusan National University)
  • Accepted : 2011.04.07
  • Published : 2011.06.30

Abstract

Radiotherapy, frequently used for treatment of solid tumors, carries two main obstacles including acquired radioresistance in cancer cells during radiotherapy and normal tissue injury. Phenylpropanoids, which are naturally occurring phytochemicals found in plants, have been identified as potential radiotherapeutic agents due to their anti-cancer activity and relatively safe levels of cytotoxicity. Various studies have proposed that these compounds could not only sensitize cancer cells to radiation resulting in inhibition of growth and cell death but also protect normal cells against radiation-induced damage. This review is intended to provide an overview of recent investigations on the usage of phenylpropanoids in combination with radiotherapy in cancer treatment.

Keywords

Acknowledgement

Supported by : Pusan National University

References

  1. Adhikari M, Arora R, Chawla R, Sharma J, Dhaker AS, Gupta D, Dubey N, Kumar R, Ivanov V, Gadjeva V, Gevrenova R, Sharma RK. Evaluation of silymarin as a promising radioprotector. Z Naturforsch C 2010;65:337-46
  2. Aeschbach R, Loliger J, Scott BC, Murcia A, Butler J, Halliwell B, Aruoma OI. Antioxidant actions of thymol, carvacrol, 6-gingerol, zingerone and hydroxytyrosol. Food Chem Toxicol 1994;32:31-6 https://doi.org/10.1016/0278-6915(84)90033-4
  3. Annabi B, Lee YT, Martel C, Pilorget A, Bahary JP, Beliveau R. Radiation induced-tubulogenesis in endothelial cells is antagonized by the antiangiogenic properties of green tea polyphenol (-) epigallocatechin-3-gallate. Cancer Biol Ther 2003;2:642-9
  4. Annabi B, Bouzeghrane M, Moumdjian R, Moghrabi A, Beliveau R. Probing the infiltrating character of brain tumors: inhibition of RhoA/ROK-mediated CD44 cell surface shedding from glioma cells by the green tea catechin EGCg. J Neurochem 2005;94:906-16 https://doi.org/10.1111/j.1471-4159.2005.03256.x
  5. Arai N, Strom A, Rafter JJ, Gustafsson JA. Estrogen receptor beta mRNA in colon cancer cells: growth effects of estrogen and genistein. Biochem Biophys Res Commun 2000;270: 425-31 https://doi.org/10.1006/bbrc.2000.2444
  6. Araujo MC, Dias FL, Takahashi CS. Potentiation by turmeric and curcumin of gamma-radiation-induced chromosome aberrations in Chinese hamster ovary cells. Teratog Carcinog Mutagen 1999;19:9-18 https://doi.org/10.1002/(SICI)1520-6866(1999)19:1<9::AID-TCM2>3.0.CO;2-H
  7. Aravindan N, Veeraraghavan J, Madhusoodhanan R, Herman TS, Natarajan M. Curcumin regulates low-linear energy transfer gamma-radiation-induced NFkappaB- dependent telomerase activity in human neuroblastoma cells. Int J Radiat Oncol Biol Phys 2011;79:1206-15 https://doi.org/10.1016/j.ijrobp.2010.10.058
  8. Archana PR, Nageshwar Rao B, Ballal M, Satish Rao BS. Thymol, a naturally occurring monocyclic dietary phenolic compound protects Chinese hamster lung fibroblasts from radiation-induced cytotoxicity. Mutat Res 2009;680:70-7 https://doi.org/10.1016/j.mrgentox.2009.09.010
  9. Baatout S, Derradji H, Jacquet P, Ooms D, Michaux A, Mergeay M. Enhanced radiation-induced apoptosis of cancer cell lines after treatment with resveratrol. Int J Mol Med 2004a;13:895-902
  10. Baatout S, Jacquet P, Derradji H, Ooms D, Michaux A, Mergeay M. Study of the combined effect of X-irradiation and epigallocatechin-gallate (a tea component) on the growth inhibition and induction of apoptosis in human cancer cell lines. Oncol Rep 2004b;12:159-67
  11. Baatout S, Derradji H, Jacquet P, Mergeay M. Increased radiation sensitivity of an eosinophilic cell line following treatment with epigallocatechin-gallate, resveratrol and curcuma. Int J Mol Med 2005;15:337-52
  12. Baur JA, Sinclair DA. Therapeutic potential of resveratrol: the in vivo evidence. Nat Rev Drug Discov 2006;5:493-506 https://doi.org/10.1038/nrd2060
  13. Bhaumik S, Anjum R, Rangaraj N, Pardhasaradhi BV, Khar A. Curcumin mediated apoptosis in AK-5 tumor cells involves the production of reactive oxygen intermediates. FEBS Lett 1999;456:311-4 https://doi.org/10.1016/S0014-5793(99)00969-2
  14. Calikoglu M, Tamer L, Sucu N, Coskun B, Ercan B, Gul A, Calikoglu I, Kanik A. The effects of caffeic acid phenethyl ester on tissue damage in lung after hindlimb ischemiareperfusion. Pharmacol Res 2003;48:397-403 https://doi.org/10.1016/S1043-6618(03)00156-7
  15. Calveley VL, Jelveh S, Langan A, Mahmood J, Yeung IW, Van Dyk J, Hill RP. Genistein can mitigate the effect of radiation on rat lung tissue. Radiat Res 2010;173:602-11 https://doi.org/10.1667/RR1896.1
  16. Candelaria M, Garcia-Arias A, Cetina L, Duenas-Gonzalez A. Radiosensitizers in cervical cancer. Cisplatin and beyond. Radiat Oncol 2006;1:15 https://doi.org/10.1186/1748-717X-1-15
  17. Carsten RE, Bachand AM, Bailey SM, Ullrich RL. Resveratrol reduces radiation-induced chromosome aberration frequencies in mouse bone marrow cells. Radiat Res 2008;169:633-8 https://doi.org/10.1667/RR1190.1
  18. Chen MF, Wu CT, Chen YJ, Keng PC, Chen WC. Cell killing and radiosensitization by caffeic acid phenethyl ester (CAPE) in lung cancer cells. J Radiat Res (Tokyo) 2004;45:253-60 https://doi.org/10.1269/jrr.45.253
  19. Chen YJ, Liao HF, Tsai TH, Wang SY, Shiao MS. Caffeic acid phenethyl ester preferentially sensitizes CT26 colorectal adenocarcinoma to ionizing radiation without affecting bone marrow radioresponse. Int J Radiat Oncol Biol Phys 2005;63:1252-61 https://doi.org/10.1016/j.ijrobp.2005.08.001
  20. Cho JW, Park K, Kweon GR, Jang BC, Baek WK, Suh MH, Kim CW, Lee KS, Suh SI. Curcumin inhibits the expression of COX-2 in UVB-irradiated human keratinocytes (HaCaT) by inhibiting activation of AP-1: p38 MAP kinase and JNK as potential upstream targets. Exp Mol Med 2005;37:186-92 https://doi.org/10.1038/emm.2005.25
  21. Davis JN, Singh B, Bhuiyan M, Sarkar FH. Genistein-induced upregulation of p21WAF1, downregulation of cyclin B, and induction of apoptosis in prostate cancer cells. Nutr Cancer 1998;32:123-31 https://doi.org/10.1080/01635589809514730
  22. Devipriya N, Sudheer AR, Srinivasan M, Menon VP. Quercetin ameliorates gamma radiation-induced DNA damage and biochemical changes in human peripheral blood lymphocytes. Mutat Res 2008;654:1-7 https://doi.org/10.1016/j.mrgentox.2008.03.003
  23. Fahlman BM, Krol ES. Inhibition of UVA and UVB radiationinduced lipid oxidation by quercetin. J Agric Food Chem 2009a;57:5301-5 https://doi.org/10.1021/jf900344d
  24. Fahlman BM, Krol ES. UVA and UVB radiation-induced oxidation products of quercetin. J Photochem Photobiol B 2009b;97:123-31 https://doi.org/10.1016/j.jphotobiol.2009.08.009
  25. Fassina G, Vene R, Morini M, Minghelli S, Benelli R, Noonan DM, Albini A. Mechanisms of inhibition of tumor angiogenesis and vascular tumor growth by epigallocatechin- 3-gallate. Clin Cancer Res 2004;10:4865-73 https://doi.org/10.1158/1078-0432.CCR-03-0672
  26. Fujiwara K, Iwado E, Mills GB, Sawaya R, Kondo S, Kondo Y. Akt inhibitor shows anticancer and radiosensitizing effects in malignant glioma cells by inducing autophagy. Int J Oncol 2007;31:753-60
  27. Gakova N, Mishurova E, Kropachova K. Effects of flavobion on nucleic acids in tissues of rats irradiated with gamma rays. Biull Eksp Biol Med 1992;113:275-7
  28. Galati G, Sabzevari O, Wilson JX, O'Brien PJ. Prooxidant activity and cellular effects of the phenoxyl radicals of dietary flavonoids and other polyphenolics. Toxicology 2002;177:91-104 https://doi.org/10.1016/S0300-483X(02)00198-1
  29. Gana-Weisz M, Halaschek-Wiener J, Jansen B, Elad G, Haklai R, Kloog Y. The Ras inhibitor S-trans,transfarnesylthiosalicylic acid chemosensitizes human tumor cells without causing resistance. Clin Cancer Res 2002;8:555-65
  30. Grdina DJ, Murley JS, Kataoka Y. Radioprotectants: current status and new directions. Oncology 2002;63 Suppl 2:2-10 https://doi.org/10.1159/000067146
  31. Grunberger D, Banerjee R, Eisinger K, Oltz EM, Efros L, Caldwell M, Estevez V, Nakanishi K. Preferential cytotoxicity on tumor cells by caffeic acid phenethyl ester isolated from propolis. Experientia 1988;44:230-2 https://doi.org/10.1007/BF01941717
  32. Guo S, Hu Y, Liu P, Wang Y, Guo D, Wang D, Liao H. Protective activity of different concentration of tea polyphenols and its major compound EGCG against whole body irradiation-induced injury in mice. Zhongguo Zhong Yao Za Zhi 2010;35:1328-31
  33. Gupta S, Hussain T, Mukhtar H. Molecular pathway for (-)-epigallocatechin-3-gallate-induced cell cycle arrest and apoptosis of human prostate carcinoma cells. Arch Biochem Biophys 2003;410:177-85 https://doi.org/10.1016/S0003-9861(02)00668-9
  34. Gurel A, Armutcu F, Sahin S, Sogut S, Ozyurt H, Gulec M, Kutlu NO, Akyol O. Protective role of alpha-tocopherol and caffeic acid phenethyl ester on ischemia-reperfusion injury via nitric oxide and myeloperoxidase in rat kidneys. Clin Chim Acta 2004;339:33-41 https://doi.org/10.1016/j.cccn.2003.09.013
  35. Hakova H, Misurova E, Kropacova K. The effect of silymarin on concentration and total content of nucleic acids in tissues of continuously irradiated rats. Vet Med (Praha) 1996;41:113-9
  36. Halliwell B. Antioxidants in human health and disease. Annu Rev Nutr 1996;16:33-50 https://doi.org/10.1146/annurev.nu.16.070196.000341
  37. Havsteen B. Flavonoids, a class of natural products of high pharmacological potency. Biochem Pharmacol 1983;32:1141-8 https://doi.org/10.1016/0006-2952(83)90262-9
  38. Hillman GG, Forman JD, Kucuk O, Yudelev M, Maughan RL, Rubio J, Layer A, Tekyi-Mensah S, Abrams J, Sarkar FH. Genistein potentiates the radiation effect on prostate carcinoma cells. Clin Cancer Res 2001;7:382-90
  39. Hillman GG, Wang Y, Kucuk O, Che M, Doerge DR, Yudelev M, Joiner MC, Marples B, Forman JD, Sarkar FH. Genistein potentiates inhibition of tumor growth by radiation in a prostate cancer orthotopic model. Mol Cancer Ther 2004;3:1271-9
  40. Hillman GG, Wang Y, Che M, Raffoul JJ, Yudelev M, Kucuk O, Sarkar FH. Progression of renal cell carcinoma is inhibited by genistein and radiation in an orthotopic model. BMC Cancer 2007;7:4 https://doi.org/10.1186/1471-2407-7-4
  41. Inal ME, Akgun A, Kahraman A. Radioprotective effects of exogenous glutathione against whole-body gamma-ray irradiation: age- and gender-related changes in malondialdehyde levels, superoxide dismutase and catalase activities in rat liver. Methods Find Exp Clin Pharmacol 2002;24:209-12 https://doi.org/10.1358/mf.2002.24.4.678452
  42. Inano H, Onoda M. Radioprotective action of curcumin extracted from Curcuma longa LINN: inhibitory effect on formation of urinary 8-hydroxy-2'-deoxyguanosine, tumorigenesis, but not mortality, induced by gamma-ray irradiation. Int J Radiat Oncol Biol Phys 2002;53:735-43 https://doi.org/10.1016/S0360-3016(02)02794-3
  43. Jagetia GC, Reddy TK. Modulation of radiation-induced alteration in the antioxidant status of mice by naringin. Life Sci 2005;77:780-94 https://doi.org/10.1016/j.lfs.2005.01.015
  44. Javvadi P, Segan AT, Tuttle SW, Koumenis C. The chemopreventive agent curcumin is a potent radiosensitizer of human cervical tumor cells via increased reactive oxygen species production and overactivation of the mitogenactivated protein kinase pathway. Mol Pharmacol 2008;73:1491-501 https://doi.org/10.1124/mol.107.043554
  45. Jeon HY, Kim JK, Kim WG, Lee SJ. Effects of oral epigallocatechin gallate supplementation on the minimal erythema dose and UV-induced skin damage. Skin Pharmacol Physiol 2009;22:137-41 https://doi.org/10.1159/000201562
  46. Kalpana C, Menon VP. Curcumin ameliorates oxidative stress during nicotine-induced lung toxicity in Wistar rats. Ital J Biochem 2004;53:82-6
  47. Kim CH, Moon SK. Epigallocatechin-3-gallate causes the p21/WAF1-mediated G(1)-phase arrest of cell cycle and inhibits matrix metalloproteinase-9 expression in TNF-alpha-induced vascular smooth muscle cells. Arch Biochem Biophys 2005;435:264-72 https://doi.org/10.1016/j.abb.2004.12.022
  48. Kojima-Yuasa A, Hua JJ, Kennedy DO, Matsui-Yuasa I. Green tea extract inhibits angiogenesis of human umbilical vein endothelial cells through reduction of expression of VEGF receptors. Life Sci 2003;73:1299-313 https://doi.org/10.1016/S0024-3205(03)00424-7
  49. Kudugunti SK, Vad NM, Whiteside AJ, Naik BU, Yusuf MA, Srivenugopal KS, Moridani MY. Biochemical mechanism of caffeic acid phenylethyl ester (CAPE) selective toxicity towards melanoma cell lines. Chem Biol Interact 2010;188:1-14 https://doi.org/10.1016/j.cbi.2010.05.018
  50. Kunnumakkara AB, Diagaradjane P, Guha S, Deorukhkar A, Shentu S, Aggarwal BB, Krishnan S. Curcumin sensitizes human colorectal cancer xenografts in nude mice to gamma-radiation by targeting nuclear factor-kappaB-regulated gene products. Clin Cancer Res 2008;14:2128-36 https://doi.org/10.1158/1078-0432.CCR-07-4722
  51. Landauer MR, Srinivasan V, Seed TM. Genistein treatment protects mice from ionizing radiation injury. J Appl Toxicol 2003;23:379-85 https://doi.org/10.1002/jat.904
  52. Laughton MJ, Evans PJ, Moroney MA, Hoult JR, Halliwell B. Inhibition of mammalian 5-lipoxygenase and cyclo-oxygenase by flavonoids and phenolic dietary additives. Relationship to antioxidant activity and to iron ion-reducing ability. Biochem Pharmacol 1991;42:1673-81 https://doi.org/10.1016/0006-2952(91)90501-U
  53. Lee YY, Kao CL, Tsai PH, Tsai TH, Chiou SH, Wu WF, Ku HH, Wong TT. Caffeic acid phenethyl ester preferentially enhanced radiosensitizing and increased oxidative stress in medulloblastoma cell line. Childs Nerv Syst 2008;24:987-94 https://doi.org/10.1007/s00381-008-0636-2
  54. Li Y, Cao Z, Zhu H. Upregulation of endogenous antioxidants and phase 2 enzymes by the red wine polyphenol, resveratrol in cultured aortic smooth muscle cells leads to cytoprotection against oxidative and electrophilic stress. Pharmacol Res 2006;53:6-15 https://doi.org/10.1016/j.phrs.2005.08.002
  55. Linard C, Marquette C, Mathieu J, Pennequin A, Clarencon D, Mathe D. Acute induction of inflammatory cytokine expression after gamma-irradiation in the rat: effect of an NF-kappaB inhibitor. Int J Radiat Oncol Biol Phys 2004;58:427-34 https://doi.org/10.1016/j.ijrobp.2003.09.039
  56. Losa GA. Resveratrol modulates apoptosis and oxidation in human blood mononuclear cells. Eur J Clin Invest 2003;33:818-23 https://doi.org/10.1046/j.1365-2362.2003.01219.x
  57. Marampon F, Gravina GL, Di Rocco A, Bonfili P, Di Staso M, Fardella C, Polidoro L, Ciccarelli C, Festuccia C, Popov VM, Pestell RG, Tombolini V, Zani BM. MEK/ERK inhibitor U0126 increases the radiosensitivity of rhabdomyosarcoma cells in vitro and in vivo by downregulating growth and DNA repair signals. Mol Cancer Ther 2011;10:159-68 https://doi.org/10.1158/1535-7163.MCT-10-0631
  58. McLaughlin N, Annabi B, Bouzeghrane M, Temme A, Bahary JP, Moumdjian R, Beliveau R. The Survivin-mediated radioresistant phenotype of glioblastomas is regulated by RhoA and inhibited by the green tea polyphenol (-)-epigallocatechin-3-gallate. Brain Res 2006;1071:1-9 https://doi.org/10.1016/j.brainres.2005.10.009
  59. Mira L, Silva M, Manso CF. Scavenging of reactive oxygen species by silibinin dihemisuccinate. Biochem Pharmacol 1994;48:753-9 https://doi.org/10.1016/0006-2952(94)90053-1
  60. Motohashi N, Ashihara Y, Yamagami C, Saito Y. Antimutagenic effects of dehydrozingerone and its analogs on UV-induced mutagenesis in Escherichia coli. Mutat Res 1997;377:17-25 https://doi.org/10.1016/S0027-5107(97)00054-7
  61. Muriel P, Garciapina T, Perez-Alvarez V, Mourelle M. Silymarin protects against paracetamol-induced lipid peroxidation and liver damage. J Appl Toxicol 1992;12:439-42 https://doi.org/10.1002/jat.2550120613
  62. Natarajan K, Singh S, Burke TR Jr, Grunberger D, Aggarwal BB. Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-kappa B. Proc Natl Acad Sci USA 1996;93:9090-5 https://doi.org/10.1073/pnas.93.17.9090
  63. Noroozi M, Angerson WJ, Lean ME. Effects of flavonoids and vitamin C on oxidative DNA damage to human lymphocytes. Am J Clin Nutr 1998;67:1210-8 https://doi.org/10.1093/ajcn/67.6.1210
  64. Nyati MK, Maheshwari D, Hanasoge S, Sreekumar A, Rynkiewicz SD, Chinnaiyan AM, Leopold WR, Ethier SP, Lawrence TS. Radiosensitization by pan ErbB inhibitor CI-1033 in vitro and in vivo. Clin Cancer Res 2004;10:691-700 https://doi.org/10.1158/1078-0432.CCR-1041-03
  65. Okunieff P, Xu J, Hu D, Liu W, Zhang L, Morrow G, Pentland A, Ryan JL, Ding I. Curcumin protects against radiation-induced acute and chronic cutaneous toxicity in mice and decreases mRNA expression of inflammatory and fibrogenic cytokines. Int J Radiat Oncol Biol Phys 2006;65:890-8 https://doi.org/10.1016/j.ijrobp.2006.03.025
  66. Patt HM, Tyree EB, Straube RL, Smith DE. Cysteine Protection against X Irradiation. Science 1949;110:213-4 https://doi.org/10.1126/science.110.2852.213
  67. Pietta PG. Flavonoids as antioxidants. J Nat Prod 2000;63:1035-42 https://doi.org/10.1021/np9904509
  68. Pilorget A, Berthet V, Luis J, Moghrabi A, Annabi B, Beliveau R. Medulloblastoma cell invasion is inhibited by green tea (-)epigallocatechin-3-gallate. J Cell Biochem 2003;90:745-55 https://doi.org/10.1002/jcb.10667
  69. Polasa K, Naidu AN, Ravindranath I, Krishnaswamy K. Inhibition of B(a)P induced strand breaks in presence of curcumin. Mutat Res 2004;557:203-13 https://doi.org/10.1016/j.mrgentox.2003.10.016
  70. Prasad NR, Menon VP, Vasudev V, Pugalendi KV. Radio-protective effect of sesamol on gamma-radiation induced DNA damage, lipid peroxidation and antioxidants levels in cultured human lymphocytes. Toxicology 2005;209:225-35 https://doi.org/10.1016/j.tox.2004.12.009
  71. Raffoul JJ, Wang Y, Kucuk O, Forman JD, Sarkar FH, Hillman GG. Genistein inhibits radiation-induced activation of NF-kappaB in prostate cancer cells promoting apoptosis and G2/M cell cycle arrest. BMC Cancer 2006;6:107 https://doi.org/10.1186/1471-2407-6-107
  72. Ramadan LA, Roushdy HM, Abu Senna GM, Amin NE, El-Deshw OA. Radioprotective effect of silymarin against radiation induced hepatotoxicity. Pharmacol Res 2002;45:447-54 https://doi.org/10.1006/phrs.2002.0990
  73. Rao BN, Rao BS, Aithal BK, Kumar MR. Radiomodifying and anticlastogenic effect of Zingerone on Swiss albino mice exposed to whole body gamma radiation. Mutat Res 2009;677:33-41 https://doi.org/10.1016/j.mrgentox.2009.05.004
  74. Rao BN, Rao BS. Antagonistic effects of Zingerone, a phenolic alkanone against radiation-induced cytotoxicity, genotoxicity, apoptosis and oxidative stress in Chinese hamster lung fibroblast cells growing in vitro. Mutagenesis 2010;25:577-87 https://doi.org/10.1093/mutage/geq043
  75. Riley PA. Free radicals in biology: oxidative stress and the effects of ionizing radiation. Int J Radiat Biol 1994;65:27-33 https://doi.org/10.1080/09553009414550041
  76. Rithidech KN, Tungjai M, Whorton EB. Protective effect of apigenin on radiation-induced chromosomal damage in human lymphocytes. Mutat Res 2005;585:96-104 https://doi.org/10.1016/j.mrgentox.2005.04.003
  77. Scarlatti F, Sala G, Ricci C, Maioli C, Milani F, Minella M, Botturi M, Ghidoni R. Resveratrol sensitization of DU145 prostate cancer cells to ionizing radiation is associated to ceramide increase. Cancer Lett 2007;253:124-30 https://doi.org/10.1016/j.canlet.2007.01.014
  78. Seiwert TY, Salama JK, Vokes EE. The concurrent chemoradiation paradigm--general principles. Nat Clin Pract Oncol 2007;4:86-100 https://doi.org/10.1038/ncponc0714
  79. Shao ZM, Wu J, Shen ZZ, Barsky SH. Genistein exerts multiple suppressive effects on human breast carcinoma cells. Cancer Res 1998;58:4851-7
  80. Shapiro S, Guggenheim B. The action of thymol on oral bacteria. Oral Microbiol Immunol 1995;10:241-6 https://doi.org/10.1111/j.1399-302X.1995.tb00149.x
  81. Shimoi K, Masuda S, Furugori M, Esaki S, Kinae N. Radioprotective effect of antioxidative flavonoids in gamma-ray irradiated mice. Carcinogenesis 1994;15:2669-72 https://doi.org/10.1093/carcin/15.11.2669
  82. Shin SG, Kim JY, Chung HY, Jeong JC. Zingerone as an antioxidant against peroxynitrite. J Agric Food Chem 2005;53:7617-22 https://doi.org/10.1021/jf051014x
  83. Silvan S, Manoharan S, Baskaran N, Singh AK. Apigenin: A potent antigenotoxic and anticlastogenic agent. Biomed Pharmacother 2010 [Epub ahead of print]
  84. Srinivasan M, Rajendra Prasad N, Menon VP. Protective effect of curcumin on gamma-radiation induced DNA damage and lipid peroxidation in cultured human lymphocytes. Mutat Res 2006;611:96-103 https://doi.org/10.1016/j.mrgentox.2006.07.002
  85. Surh YJ. Cancer chemoprevention with dietary phytochemicals. Nat Rev Cancer 2003;3:768-80 https://doi.org/10.1038/nrc1189
  86. Torres JL, Varela B, Garcia MT, Carilla J, Matito C, Centelles JJ, Cascante M, Sort X, Bobet R. Valorization of grape (Vitis vinifera) byproducts. Antioxidant and biological properties of polyphenolic fractions differing in procyanidin composition and flavonol content. J Agric Food Chem 2002;50:7548-55 https://doi.org/10.1021/jf025868i
  87. Tsao R, Deng Z. Separation procedures for naturally occurring antioxidant phytochemicals. J Chromatogr B Analyt Technol Biomed Life Sci 2004;812:85-99 https://doi.org/10.1016/S1570-0232(04)00764-0
  88. Valenzuela A, Guerra R, Videla LA. Antioxidant properties of the flavonoids silybin and (+)-cyanidanol-3: comparison with butylated hydroxyanisole and butylated hydroxytoluene. Planta Med 1986:438-40
  89. Valenzuela A, Aspillaga M, Vial S, Guerra R. Selectivity of silymarin on the increase of the glutathione content in different tissues of the rat. Planta Med 1989;55:420-2 https://doi.org/10.1055/s-2006-962056
  90. Vayalil PK, Mittal A, Hara Y, Elmets CA, Katiyar SK. Green tea polyphenols prevent ultraviolet light-induced oxidative damage and matrix metalloproteinases expression in mouse skin. J Invest Dermatol 2004;122:1480-7 https://doi.org/10.1111/j.0022-202X.2004.22622.x
  91. Wang M, Ruan Y, Chen Q, Li S, Wang Q, Cai J. Curcumin induced HepG2 cell apoptosis-associated mitochondrial membrane potential and intracellular free Ca(2+) concentration. Eur J Pharmacol 2011;650:41-7 https://doi.org/10.1016/j.ejphar.2010.09.049
  92. Wei H, Bowen R, Cai Q, Barnes S, Wang Y. Antioxidant and antipromotional effects of the soybean isoflavone genistein. Proc Soc Exp Biol Med 1995;208:124-30 https://doi.org/10.3181/00379727-208-43844
  93. Wei H, Zhang X, Wang Y, Lebwohl M. Inhibition of ultraviolet light-induced oxidative events in the skin and internal organs of hairless mice by isoflavone genistein. Cancer Lett 2002;185:21-9 https://doi.org/10.1016/S0304-3835(02)00240-9
  94. Yashar CM, Spanos WJ, Taylor DD, Gercel-Taylor C. Potentiation of the radiation effect with genistein in cervical cancer cells. Gynecol Oncol 2005;99:199-205 https://doi.org/10.1016/j.ygyno.2005.07.002
  95. Yildiz OG, Soyuer S, Saraymen R, Eroglu C. Protective effects of caffeic acid phenethyl ester on radiation induced lung injury in rats. Clin Invest Med 2008;31:E242-7 https://doi.org/10.25011/cim.v31i5.4870
  96. Yokoyama S, Hirano H, Wakimaru N, Sarker KP, Kuratsu J. Inhibitory effect of epigallocatechin-gallate on brain tumor cell lines in vitro. Neuro Oncol 2001;3:22-8 https://doi.org/10.1093/neuonc/3.1.22
  97. Yuhas JM, Spellman JM, Culo F. The role of WR-2721 in radiotherapy and/or chemotherapy. Cancer Clin Trials 1980; 3:211-6
  98. Zhang B, Liu JY, Pan JS, Han SP, Yin XX, Wang B, Hu G. Combined treatment of ionizing radiation with genistein on cervical cancer HeLa cells. J Pharmacol Sci 2006;102:129-35 https://doi.org/10.1254/jphs.FP0060165

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  7. Effects of traditional oriental medicines as anti-cytotoxic agents in radiotherapy vol.13, pp.6, 2011, https://doi.org/10.3892/ol.2017.6042
  8. Amelioration of Radiation Enteropathy by Dietary Supplementation With Reduced Coenzyme Q10 vol.4, pp.2, 2011, https://doi.org/10.1016/j.adro.2019.01.006
  9. Radioprotective efficacy of dieckol against gamma radiation-induced cellular damage in hepatocyte cells vol.392, pp.8, 2011, https://doi.org/10.1007/s00210-019-01652-z
  10. Ferulic acid enhances the radiation sensitivity of lung and liver carcinoma cells by collapsing redox homeostasis: mechanistic involvement of Akt/p38 MAPK signalling pathway vol.53, pp.9, 2011, https://doi.org/10.1080/10715762.2019.1655559
  11. Radioprotective Effect of Flavonoids on Ionizing Radiation-Induced Brain Damage vol.25, pp.23, 2011, https://doi.org/10.3390/molecules25235719
  12. Genistein From Fructus sophorae Protects Mice From Radiation-Induced Intestinal Injury vol.12, pp.None, 2011, https://doi.org/10.3389/fphar.2021.655652
  13. Novel Anticancer and Treatment Sensitizing Compounds against Pancreatic Cancer vol.13, pp.12, 2011, https://doi.org/10.3390/cancers13122940
  14. Paper Spray Mass Spectrometry on the Analysis of Phenolic Compounds in Rhynchelytrum repens: A Tropical Grass with Hypoglycemic Activity vol.10, pp.8, 2021, https://doi.org/10.3390/plants10081617