Cancer Letters
Volume 286, Issue 2 , Pages 161-171 , 28 December 2009

Gallic acid, a major component of Toona sinensis leaf extracts, contains a ROS-mediated anti-cancer activity in human prostate cancer cells

  • Huei-Mei Chen

      Affiliations

    • Graduate Institute of Natural Products, College of Pharmacy, Kaohsiung Medical University, Kaohsiung 807, Taiwan, ROC
    • Department of Medical Research, E-DA Hospital, Kaohsiung 824, Taiwan, ROC
    • ,
  • Yang-Chang Wu

      Affiliations

    • Graduate Institute of Natural Products, College of Pharmacy, Kaohsiung Medical University, Kaohsiung 807, Taiwan, ROC
    • ,
  • Yi-Chen Chia

      Affiliations

    • Department of Food Science and Technology, Tajen University, Pingtung 907, Taiwan, ROC
    • ,
  • Fang-Rong Chang

      Affiliations

    • Graduate Institute of Natural Products, College of Pharmacy, Kaohsiung Medical University, Kaohsiung 807, Taiwan, ROC
    • ,
  • Hseng-Kuang Hsu

      Affiliations

    • Department of Physiology, Kaohsiung Medical University, Kaohsiung 807, Taiwan, ROC
    • ,
  • Ya-Ching Hsieh

      Affiliations

    • Department of Medical Research, E-DA Hospital, Kaohsiung 824, Taiwan, ROC
    • ,
  • Chih-Chen Chen

      Affiliations

    • Department of Obstetrics and Gynecology, E-DA Hospital, Kaohsiung 824, Taiwan, ROC
    • Corresponding Author InformationCorresponding authors. Address: Department of Medical Research and Department of Obstetrics and Gynecology, E-DA Hospital, I-Shou University, 1, E-DA Road, Jiau-Shu Tsuen, Yan-Chau Shiang, Kaohsiung County, Taiwan 824, ROC. Tel.: +886 7 6151100x5901; fax: +886 7 6155352 (S.-S. Yuan).
    • ,
  • Shyng-Shiou Yuan

      Affiliations

    • Department of Medical Research, E-DA Hospital, Kaohsiung 824, Taiwan, ROC
    • Department of Obstetrics and Gynecology, E-DA Hospital, Kaohsiung 824, Taiwan, ROC
    • Department of Biological Science and Technology, I-Shou University, Kaohsiung 824, Taiwan, ROC
    • Corresponding Author InformationCorresponding authors. Address: Department of Medical Research and Department of Obstetrics and Gynecology, E-DA Hospital, I-Shou University, 1, E-DA Road, Jiau-Shu Tsuen, Yan-Chau Shiang, Kaohsiung County, Taiwan 824, ROC. Tel.: +886 7 6151100x5901; fax: +886 7 6155352 (S.-S. Yuan).

Received 10 January 2009 ,Revised 6 May 2009 ,Accepted 25 May 2009.

References 

  1. Jemal A, Murray T, Ward E, Samuels A, Tiwari RC, Ghafoor A, et al. Cancer statistics 2005 Canada. Cancer J. Clin. 2005;55:10–30
  2. Pu YS, Chiang HS, Lin CC, Huang CY, Huang KH, Chen J. Changing trends of prostate cancer in Asia. Aging Male. 2004;7(2):120–132
  3. Krishnan K, Campbell S, Abdel-Rahman F, Whaley S, Stone WL. Cancer chemoprevention drug targets. Curr. Drug Targets. 2003;4(1):1389–4501
  4. Singh RP, Dhanalakshmi S, Agarwal R. Phytochemicals as cell cycle modulators: a less toxic approach in halting human cancers. Cell Cycle. 2002;1:56–161
  5. Gupta S. Prostate cancer chemoprevention: current status and future prospects. Toxicol. Appl. Pharmacol. 2007;224:369–376
  6. Szatrowski TP, Nathan CF. Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res. 1991;51:794–798
  7. Schumacker PT. Reactive oxygen species in cancer cells: live by the sword, die by the sword. Cancer Cell. 2006;10:175–176
  8. Trachootham D, Zhou Y, Zhang H, Demizu Y, Chen Z, Pelicano H, et al. Selective killing of ncogenically transformed cells through a ROS mediated mechanism by β-phenylethyl isothiocyanate. Cancer Cell. 2006;10:241–252
  9. Pelicano H, Carney D, Huang P. ROS stress in cancer cells and therapeutic implications. Drug Resist. Update. 2004;7:97–110
  10. Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M. Free radical, metals and antioxidants in oxidative stress-induce cancer. Chem. Biol. Interact. 2006;160:1–40
  11. Li GX, Hu H, Jiang C, Schuster T, Lu J. Differential involvement of reactive oxygen species in apoptosis induced by two classes of selenium compounds in human prostate cancer cells. Int. J. Cancer. 2007;120:2034–2043
  12. Zhao R, Xiang N, Domann FE, Zhong W. Expression of p53 enhances selenite-induced superoxide production and apoptosis in human prostate cancer cells. Cancer Res. 2006;66(4):2296–2304
  13. Hseu YC, Chang WH, Chen CS, Liao JW, Huang CJ, Lu FJ, et al. Antioxidant activities of Toona Sinensis leaves extracts using different antioxidant models. Food Chem. Toxicol. 2008;46:105–114
  14. Garcia-Ruiz C, Colell A, Mari M, Morales A, Fernandez-Checa JC. Direct effect of ceramide on the mitochondrial electron transport chain leads to generation of reactive oxygen species. Role of mitochondrial glutathione. J. Biol. Chem. 1997;272:11369–11377
  15. Coyle JT, Puttfarcken P. Oxidative stress, glutamate, and neurodegenerative disorders. Science. 1993;262:689–695
  16. Kim BC, Kim HG, Lee SA, Lim S, Park EH, Kim SJ, et al. Genipin-induced apoptosis in hepatoma cells is mediated by reactive oxygen species/c-Jun NH2-terminal kinase-dependent activation of mitochondrial pathway. Biochem. Pharmacol. 2005;70:1398–1407
  17. Kuo PL, Chen CY, Hsu YL. Isoobtusilactone A induces cell cycle arrest and apoptosis through reactive oxygen species/apoptosis signal-regulating kinase 1 signaling pathway in human breast cancer cells. Cancer Res. 2007;67:7406–7420
  18. Hileman EO, Liu JS, Albitar M, Keating MJ, Huang P. Intrinsic oxidative stress in cancer cells: a biochemical basis for therapeutic selectivity. Cancer Chemother. Pharmacol. 2004;53:209–219
  19. Edmonds JM, Staniforth M. Toona sinensis: Meliaceae. Curtis’s Bot. Mag. 1998;15:186–193
  20. Chang HC, Hung WC, Huang MS, Hsu HK. Extract from the leaves of Toona sinensis roemor exerts potent antiproliferative effect on human lung cancer cells. Am. J. Chinese Med. 2002;30:307–314
  21. Chang HL, Hsu HK, Su JH, Wang PH, Chun YF, Chia YC, et al. The fractionated Toona sinensis leaf extract induces apoptosis of human ovarian cancer cells and inhibits tumor growth in a murine xenograft model. Gynecol. Oncol. 2006;102(2):309–314
  22. Yang HL, Chang WH, Chia YC, Huang CJ, Lu FJ, Hsu HK, et al. Toona sinensis extracts induces apoptosis via reactive oxygen species in human premyelocytic leukemia cells. Food Chem. Toxicol. 2006;44:1978–1988
  23. J.Y.L. Yu, Toona sinensis extract affects gene expression of GLUT4 GLU00 se transporter in adipose tissue of alloxan-induced diabetic rats, in: Proceedings of 5th Congress of the International Diabetic Society, China, May 2002, pp. 4–7.
  24. Hsu HK, Yang YC, Hwang JH, Hong SJ. Effects of Toona sinensis leaf extract on lipolysis in differentiated 3T3-L1 adipocytes. Kaoshiung J. Med. Sci. 2003;19:3855–3890
  25. Cho EJ, Yokozawa T, Rhyu DY, Kim HY, Shibahara N, Park JC. The inhibitory effects of 12 medicinal plants and their component compounds on lipid peroxidation. Am. J. Chinese Med. 2003;31:907–917
  26. Poon SL, Leu SF, Hsu HK, Liu MY, Huang BM. Regulatory mechanism of Toona sinensis on mouse leydig cell steroidogenesis. Life Sci. 2005;76:1473–1487
  27. F.Y. Yang, Study on the physiological function of Toona sinensis Roem in human spermatozoa. Master Thesis in National Cheng Kung University, Tainan, Taiwan, 2003.
  28. Sureda FX, Escubedo E, Gabriel C, Comas J, Camarasa J, Camins A. Mitochondria membrane potential measurement in rat cerebellar neurons by flow cytometry. Cytometry. 1997;28:74–80
  29. LeBel CP, Ischiropoulos H, Bondy SC. Evaluation of the probe 2′,7′-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem. Res. Toxicol. 1992;5:227–231
  30. Lee RF, Steinert S. Use of the single cell gel electrophoresis/comet assay for detecting DNA damage in aquatic (marine and freshwater) animals. Mutat. Res. 2003;544:43–64
  31. Bauer E, Recknagel RD, Fiedler U, Wollweber L, Bock C, Greulich KO. The distribution of the tail moments in single cell gel electrophoresis (comet assay) obeys a chi-square (chi(2)) not a gaussian distribution. Mutat. Res. 1998;398:101–110
  32. Olive PL, Banath JP, Durand RE. Heterogeneity in radiation induced DNA damage and repair in tumor and normal cells measured using the comet assay. Radiat. Res. 1990;122:86–94
  33. Hellman B, Vaghef H, Bostrom B. The concepts of tail moment and tail inertia in the single-cell gel-electrophoresis assay. Mutat. Res. 1995;336:123–131
  34. Yasuhara S, Zhu Y, Matsui T, Tipirneni N, Yasuhara Y, Kaneki M, et al. Comparison of comet assay, electron microscopy, and flow cytometry for detection of apoptosis. J. Histochem. Cytochem. 2003;51:873–885
  35. Pucci B, Kasten M, Giordano A. Cell cycle and apoptosis. Neoplasia. 2000;2:291–299
  36. Smith DM, Gao G, Zhang X, Wang G, Dou QP. Regulation of tumor cell apoptotic sensitivity during the cell cycle (Review). Int. J. Mol. Med. 2000;6:503–507
  37. Collins L, Zhu T, Guo J, Xiao ZJ, Chen CY. Phellinus linteus sensitizes apoptosis induced by doxorubicin in prostate cancer. Brit. J. Cancer. 2006;95:282–288
  38. Bertilaccio MT, Grioni M, Sutherland BW, Degl’Innocenti E, Freschi M, Jachetti E, et al. Vasculature-targeted tumor necrosis factor-alpha increases the therapeutic index of doxorubicin against prostate cancer. Prostate. 2008;68(10):1105–1115
  39. Beer DD, Joubert E, Gelderblom WC, Manley M. Antioxidant activity of South African red and white cultivar wines: free radical scavenging. J. Agric. Food Chem. 2003;51:902–909
  40. Sun J, Chu YF, Wu X, Liu RH. Antioxidant and antiproliferative activities of common fruits. J. Agric. Food Chem. 2002;50:7449–7454
  41. Wolfe K, Wu X, Liu RH. Antioxidant activity of apple peels. J. Agric. Food Chem. 2003;51:609–614
  42. Isuzugawa K, Inoue M, Ogihara Y. Catalase contents in cells determine sensitivity to the apoptosis inducer gallic acid. Biol. Pharm. Bull. 2001;24:1022–1026
  43. Inoue M, Suzuki R, Koide T, Sakaguchi N, Ogihara Y, Yabu Y. Antioxidant, gallic acid, induces apoptosis in HL-60RG cells. Biochem. Biophys. Res. Commun. 1994;204:898–904
  44. Inoue M, Suzuki R, Sakaguchi N, Li Z, Takeda T, Ogihara Y, et al. Selective induction of cell death in cancer cells by gallic acid. Biol. Pharm. Bull. 1995;18:1526–1530
  45. Surh YJ. Cancer chemoprevention with dietary phytochemicals. Nat. Rev. Cancer. 2003;3:768–780
  46. Pan MH, Lai YS, Lai CS, Wang YJ, Li SM, Lo CY, et al. 5-Hydroxy-3,6,7,8,3′,4′-hexamethoxyflavone induces apoptosis through reactive oxygen species production, growth arrest and DNA damage-inducible gene 153 expression, and caspase activation in human leukemia cells. J. Agric. Food Chem. 2007;55:5081–5091
  47. Osman AGM, Mekkawy IA, Verreth J, Wuertz S, Kloas W, Kirschbaum F. Monitoring of DNA breakage in embryonic stages of the African Catifish Clarias gariepinus (Burchell, 1822) after exposure to lead nitrate using alkaline comet assay. Environ. Toxicol. 2008;23(6):679–687
  48. Motwani M, Rizzo C, Sirotnak F, She Y, Schwartz GK. Flavopiridol enhances the effect of docetaxel in vitro and in vivo in human gastric cancer cells. Mol. Cancer Ther. 2003;2:549–555
  49. Caldon CE, Daly RJ, Sutherland RL, Musgrove EA. Cell cycle control in breast cancer cells. J. Cell Biochem. 2006;97:261–274
  50. Smits VA, Medema RH. Checking out the G2/M transition. Biochim. Biophys. Acta. 2001;1519:1–12
  51. Nebreda AR, Ferby I. Regulation of the meiotic cell cycle in oocytes. Curr. Opin. Cell Biol. 2000;12:666–675
  52. Gotoh T, Ohsumi K, Matsui T, Takisawa H, Kishimoto T. Inactivation of the checkpoint kinase Cds1 is dependent on cyclin B-Cdc2 kinase activation at the meiotic G(2)/M-phase transition in Xenopus oocytes. J. Cell Sci. 2001;114:3397–3406
  53. Singh SV, Herman-Antosiewicz A, Singh AV, Lew KL, Srivastava SK, Kamath R. Sulforaphane-induced G2/M phase cell cycle arrest involves checkpoint kinase 2-mediated phosphorylation of cell division cycle 25C. J. Biol. Chem. 2004;279:25813–25822
  54. Bulavin DV, Amundson SA, Fornace AJ. P38 and Chk1 kinases: different conductors for the G(2)/M checkpoint symphony. Currt. Opin. Genet. Dev. 2002;12:92–97
  55. Shibuya EK. G2 cell cycle arrest—a direct link between PKA and Cdc25C. Cell Cycle. 2003;2:39–41
  56. Kuo PL, Hsu YL, Cho CY. Plumbagin induces G2-M arrest and autophagy by inhibiting the AKT/mammalian target of rapamycin pathway in breast cancer cells. Mol. Cancer Ther. 2006;5(12):3209–3221
  57. Green DR, Reed JC. Mitochondria and apoptosis. Science. 1998;281:1309–1312
  58. Henry-Mowatt J, Dive C, Martinou JC, James D. Role of mitochondrial membrane permeabilization in apoptosis and cancer. Oncogene. 2004;23:2850–2860
  59. Hockenbery DM, Giedt CD, O’Neill JW, Manion MK, Banker DE. Mitochondria and apoptosis: new therapeutic targets. Adv. Cancer Res. 2002;85:203–242
  60. Kuwana T, Newmeyer DD. Bcl-2-family proteins and the role of mitochondria in apoptosis. Curr. Opin. Cell Biol. 2003;15:691–699
  61. Ly JD, Grubb DR, Lawen A. The mitochondrial membrane potential (deltapsi(m)) in apoptosis; an update. Apoptosis. 2003;8:115–128
  62. Xiao D, Lew KL, Zeng Y, Xiao H, Marynowski SW, Dhir R, et al. Phenethyl isothiocyanate-induced apoptosis in PC-3 human prostate cancer cells is mediated by reactive oxygen species-dependent disruption of mitochondrial membrance potential. Carcinogenesis. 2006;27(11):2223–2234
  63. Marchetti P, Castedo M, Susin SA, Zamzami N, Hirsch T, Macho A, et al. Mitochondrial permeability transition is a central coordinating event of apoptosis. J. Exp. Med. 1996;184(3):1155–1160
  64. McCollum AK, Teneyck CJ, Sauer BM, Toft DO, Erlichman C. Up-regulation of heat shock protein 27 induces resistance to 17-allylaminodemethoxygeldanamycin through a glutathione-mediated mechanism. Cancer Res. 2006;66:10967–10975
  65. Fulda S, Debatin KM. Sensitization for anticancer drug-induced apoptosis by the chemopreventive agent resveratrol. Oncogene. 2004;23:6702–6711
  66. Adhami VM, Malik A, Zaman N, Sarfaraz S, Siddiqui IA, Syed DN, et al. Combined inhibitory effects of green tea polyphenols and selective cyclooxygenase-2 inhibitors on the growth of human prostate cancer cells both in vitro and in vivo. Clin. Cancer Res. 2007;13(5):1611–1620
  67. Velmurugan B, Mani A, Nagini S. Combination of S-allylcysteine and lycopene induces apoptosis by modulating Bcl-2, Bax, Bim and caspases during experimental gastric carcinogenesis. Eur. J. Cancer Prev. 2005;14:387–393
  68. Khor TO, Keum YS, Lin W. Combined inhibitory effects of curcumin and phenethyl isothiocyanate on the growth of human PC-3 prostate xenografts in immunodeficient mice. Cancer Res. 2006;66:613–621

PII: S0304-3835(09)00377-2

doi: 10.1016/j.canlet.2009.05.040

Cancer Letters
Volume 286, Issue 2 , Pages 161-171 , 28 December 2009

Article Tools

* Image Usage & Resolution