Asian Pacific Journal of Cancer Prevention

Asian Pacific Journal of Cancer Prevention (아시아태평양암예방학회)
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Cytotoxic and Apoptotic-inducing Effects of Purple Rice Extracts and Chemotherapeutic Drugs on Human Cancer Cell Lines

  • Published : 2013.11.30
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Abstract

Pigmented rice is mainly black, red, and dark purple, and contains a variety of flavones, tannin, polyphenols, sterols, tocopherols, ${\gamma}$-oryzanols, amino acids, and essential oils. The present study evaluated the cytotoxic effects of purple rice extracts (PREs) combined with chemotherapeutic drugs on human cancer cells and mechanisms of cell death. Methanolic (MeOH) and dichloromethane (DCM) extracts of three cultivars of purple rice in Thailand: Doisaket (DSK), Nan and Payao (PYO), were tested and compared with white rice (KK6). Cytotoxicity was determined by 3-(4, 5-dimethyl)-2, 5-diphenyltetrazolium bromide (MTT) assay in human hepatocellular carcinoma HepG2, prostate cancer LNCaP and murine normal fibroblast NIH3T3 cells. MeOH-PYO-PRE was the most cytotoxic and inhibited HepG2 cell growth more than that of LNCaP cells but was not toxic to NIH3T3 cells. When PREs were combined with paclitaxel or vinblastine, they showed additive cytotoxic effects on HepG2 and LNCaP cells, except for MeOH-PYO-PRE which showed synergistic effects on HepG2 cells when combined with vinblastine. MeOH-PYO-PRE plus vinblastine induced HepG2 cell apoptosis with loss of mitochondrial transmembrane potential (MTP) but no ROS production. MeOH-PYO-PRE-treated HepG2 cells underwent apoptosis via caspase-9 and-3 activation. The level of ${\gamma}$-oryzanol was highest in DCM-PYO-PRE (44.17 mg/g) whereas anthocyanin content was high in MeOH-PYO-PRE (5.80 mg/g). In conclusion, methanolic Payao purple rice extract was mostly toxic to human HepG2 cells and synergistically enhanced the cytotoxicity of vinblastine. Human HepG2 cell apoptosis induced by MeOH-PYO-PRE and vinblastine was mediated through a mitochondrial pathway.

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References

  1. Abdel-Aal el-SM, Young JC, Rabalski I (2006). Anthocyanin composition in black, blue, pink, purple, and red cereal grains. J Agric Food Chem, 54, 4696-704. https://doi.org/10.1021/jf0606609
  2. Azmi NH, Ismail N, Imam MU, Ismail M (2013). Ethyl acetate extract of germinated brown rice attenuates hydrogen peroxide-induced oxidative stress in human SH-SY5Y neuroblastoma cells: role of anti-apoptotic, pro-survival and antioxidant genes. BMC Complement Altern Med, 13, 177-84. https://doi.org/10.1186/1472-6882-13-177
  3. Bates DJ, Danilov AV, Lowrey CH, Eastman A (2013). Vinblastine rapidly induces Noxa and acutely sensitizes primary chronic lymphocytic leukemia cells to ABT-737. Mol Cancer Ther, (in press).
  4. Briviba K, Abrahamse SL, Pool-Zobel BL, Rechkemmer G (2001). Neurotensin-and EGF-induced metabolic activation of colon carcinoma cells is diminished by dietary flavonoid cyanidin but not by its glycosides. Nutr Cancer, 41, 172-9. https://doi.org/10.1080/01635581.2001.9680629
  5. Chen MH, Choi SH, Kozukue N, Kim HJ, Friedman M (2012). Growth-inhibitory effects of pigmented rice bran extracts and three red bran fractions against human cancer cells: relationships with composition and antioxidative activities. J Agric Food Chem, 60, 9151-61. https://doi.org/10.1021/jf3025453
  6. Chen PN, Chu SC, Chiou HL, et al (2005). Cyanidin 3-glucoside and peonidin 3-glucoside inhibit tumor cell growth and induce apoptosis in vitro and suppress tumor growth in vivo. Nutr Cancer, 53, 232-43. https://doi.org/10.1207/s15327914nc5302_12
  7. Deng GF, Xu XR, Zhang Y, et al (2013). Phenolic compounds and bioactivities of pigmented rice. Crit Rev Food Sci Nutr, 53, 296-306. https://doi.org/10.1080/10408398.2010.529624
  8. Henderson AJ, Ollila CA, Kumar A, et al (2012). Chemopreventive properties of dietary rice bran: current status and future prospects. Adv Nutr, 3, 643-53. https://doi.org/10.3945/an.112.002303
  9. Hiramatsu K, Tani T, Kimura Y, Izumi S, Nakane PK (1990). Effect of gamma-oryzanol on atheroma formation in hypercholesterolemic rabbits. Tokai J Exp Clin Med, 15, 299-305.
  10. Horwitz SB (1994). Taxol (paclitaxel): mechanisms of action. Annal Oncol, 5, 3-6. https://doi.org/10.1093/annonc/5.suppl_5.3
  11. Hu C, Zawistowski J, Ling W, Kitts DD (2003). Black rice (Oryza sativa L. indica) pigmented fraction suppresses both reactive oxygen species and nitric oxide in chemical and biological model systems. J Agric Food Chem, 51, 5271-7. https://doi.org/10.1021/jf034466n
  12. Hui C, Bin Y, Xiaoping Y, et al (2010). Anticancer activities of an anthocyanin-rich extract from black rice against breast cancer cells in vitro and in vivo. Nutr Cancer, 62, 1128-36. https://doi.org/10.1080/01635581.2010.494821
  13. Hyun JW, Chung HS (2004). Cyanidin and Malvidin from Oryza sativa cv. Heugjinjubyeo mediate cytotoxicity against human monocytic leukemia cells by arrest of G(2)/M phase and induction of apoptosis. J Agric Food Chem, 52, 2213-7. https://doi.org/10.1021/jf030370h
  14. Itani T, Tamaki M, Arai E, Horino T (2002). Distribution of amylose, nitrogen, and minerals in rice kernels with various characters. J Agric Food Chem, 50, 5326-32. https://doi.org/10.1021/jf020073x
  15. Itoh M, Nishibori N, Sagara T, et al (2012). Extract of fermented brown rice induces apoptosis of human colorectal tumor cells by activating mitochondrial pathway. Phytother Res, 26, 1661-6. https://doi.org/10.1002/ptr.4631
  16. Ji ZJ, Wang XG, Zeng YX, et al (2012). Comparison of physiological and yield traits between purple- and white-pericarp rice using SLs. Breed Sci, 62, 71-7. https://doi.org/10.1270/jsbbs.62.71
  17. Jiang W, Yu X, Ren G (2013). Inhibition effects of black rice pericarp extracts on cell proliferation of PC-3 cells. Wei Sheng Yan Jiu, 42, 474-7.
  18. Kang SY, Seeram NP, Nair MG, Bourquin LD (2003). Tart cherry anthocyanins inhibit tumor development in Apc(Min) mice and reduce proliferation of human colon cancer cells. Cancer Lett, 194, 13-9. https://doi.org/10.1016/S0304-3940(02)00583-9
  19. Meiers S, Kemeny M, Weyand U, et al (2001). The anthocyanidins cyanidin and delphinidin are potent inhibitors of the epidermal growth-factor receptor. J Agric Food Chem, 49, 958-62. https://doi.org/10.1021/jf0009100
  20. Min B, McClung AM, Chen MH (2011). Phytochemicals and antioxidant capacities in rice brans of different color. J Food Sci, 76, 117-26. https://doi.org/10.1111/j.1750-3841.2010.01929.x
  21. Nanda K, Miyoshi N, Nakamura Y, et al (2004). Extract of vinegar “Kurosu” from unpolished rice inhibits the proliferation of human cancer cells. J Exp Clin Cancer Res, 23, 69-75.
  22. Prommaban A, Kodchakorn K, Kongtawelert P, Banjerdpongchai R (2012). Houttuynia cordata Thunb fraction induces human leukemic Molt-4 cell apoptosis through the endoplasmic reticulum stress pathway. Asian Pac J Cancer Prev, 13, 1977-81. https://doi.org/10.7314/APJCP.2012.13.5.1977
  23. Revilla E, Santa-Maria C, Miramontes E, et al (2013). Antiproliferative and immunoactivatory ability of an enzymatic extract from rice bran. Food Chem, 136, 526-31. https://doi.org/10.1016/j.foodchem.2012.08.044
  24. Ryu SN, Park SZ, Ho CT (1998). High performance liquid chromatographic determination of anthocyanin pigments in some varieties of black rice. J Food Drug Analysis, 6, 729-36.
  25. Wang J, Mazza G (2002). Effects of anthocyanins and other phenolic compounds on the production of tumor necrosis factor alpha in LPS/IFN-gamma-activated RAW 264.7 macrophages. J Agric Food Chem, 50, 4183-9. https://doi.org/10.1021/jf011613d
  26. Wilson TA, Nicolosi RJ, Woolfrey B, Kritchevsky D (2007). Rice bran oil and oryzanol reduce plasma lipid and lipoprotein cholesterol concentrations and aortic cholesterol ester accumulation to a greater extent than ferulic acid in hypercholesterolemic hamsters. J Nutr Biochem, 18, 105-12. https://doi.org/10.1016/j.jnutbio.2006.03.006
  27. Wudtiwai B, Sripanidkulchai B, Kongtawelert P, Banjerdpongchai R (2011). Methoxyflavone derivatives modulate the effect of TRAIL-induced apoptosis in human leukemic cell lines. J Hematol Oncol, 4, 52-65. https://doi.org/10.1186/1756-8722-4-52

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