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References

  1. Arumugam A, Agullo P, Boopalan T, Nandy S, Lopez R, Gutierrez C, et al. 2014. Neem leaf extract inhibits mammary carcinogenesis by altering cell proliferation, apoptosis, and angiogenesis. Cancer Biol. Ther. 15: 26-34.
    Pubmed PMC CrossRef
  2. Chen Q, Ganapathy S, Singh KP, Shankar S, Srivastava RK. 2010. Resveratrol induces growth arrest and apoptosis through activation of FOXO transcription factors in prostate cancer cells. PLoS One 5: e15288.
    Pubmed PMC CrossRef
  3. Crane C, Panner A, Pieper RO, Arbiser J, Parsa AT. 2009. Honokiol-mediated inhibition of PI3K/mTOR pathway: a potential strategy to overcome immunoresistance in glioma, breast, and prostate carcinoma without impacting T cell function. J. Immunother. 32: 585-592.
    Pubmed PMC CrossRef
  4. Ha J, Wang Y, Jang H, Seog H, Chen X. 2014. Determination of E,E-farnesol in makgeolli (rice wine) using dynamic headspace sampling and stir bar sorptive extraction coupled with gas chromatography-mass spectrometry. Food Chem. 142: 79-86.
    Pubmed CrossRef
  5. Hassan B, Akcakanat A, Holder AM, Meric-Bernstam F. 2013. Targeting the PI3-kinase/Akt/mTOR signaling pathway. Surg. Oncol. Clin. N. Am. 22: 641-664.
    Pubmed PMC CrossRef
  6. Hu Y, Wang S, Wu X, Zhang J, Chen R, Chen M, Wang Y. 2013. Chinese herbal medicine-derived compounds for cancer therapy: a focus on hepatocellular carcinoma. J. Ethnopharmacol. 149: 601-612.
    Pubmed CrossRef
  7. Joo JH, Jetten AM. 2010. Molecular mechanisms involved in farnesol-induced apoptosis. Cancer Lett. 287: 123-135.
    Pubmed PMC CrossRef
  8. Jung H, Lee SJ, Lim JH, Kim BK, Park KJ. 2014. Chemical and sensory profiles of makgeolli, Korean commercial rice wine, from descriptive, chemical, and volatile compound analyses. Food Chem. 152: 624-632.
    Pubmed CrossRef
  9. Kang BS, Lee JE, Park HJ. 2014. Qualitative and quantitative prediction of volatile compounds from initial amino acid profiles in Korean rice wine (makgeolli) model. J. Food Sci. 79: C1106-C1116.
    Pubmed CrossRef
  10. Khuda-Bukhsh AR, Das S, Saha SK. 2014. Molecular approaches toward targeted cancer prevention with some food plants and their products: inflammatory and other signal pathways. Nutr. Cancer 66: 194-205.
    Pubmed CrossRef
  11. Kitagishi Y, Matsuda S, Minami A, Ono Y, Nakanishi A, Ogura Y. 2014. Regulation in cell cycle via p53 and PTEN tumor suppressors Cancer Stud. Mol. Med. Open J. 1: 1-7.
  12. Lehman JA, Waning DL, Batuello CN, Cipriano R, Kadakia MP, Mayo LD. 2011. Induction of apoptotic genes by a p73phosphatase and tensin homolog (p73-PTEN) protein complex in response to genotoxic stress. J. Biol. Chem. 286:36631-36640.
    Pubmed PMC CrossRef
  13. Lee HJ, Lee EO, Rhee YH, Ahn KS, Li GX, Jiang C, et al. 2006. An oriental herbal cocktail, ka-mi-kae-kyuk-tang, exerts anti-cancer activities by targeting angiogenesis, apoptosis and metastasis. Carcinogenesis 27: 2455-2463.
    Pubmed CrossRef
  14. Li Y, Kong D, Bao B, Ahmad A, Sarkar FH. 2011. Induction of cancer cell death by isoflavone: the role of multiple signaling pathways. Nutrients 3: 877-896.
    Pubmed PMC CrossRef
  15. Mukhtar E, Adhami VM, Khan N, Mukhtar H. 2012. Apoptosis and autophagy induction as mechanism of cancer prevention by naturally occurring dietary agents. Curr. Drug Targets 13: 1831-1841.
    Pubmed PMC CrossRef
  16. Pandurangan AK. 2013. Potential targets for prevention of colorectal cancer: a focus on PI3K/Akt/mTOR and Wnt pathways. Asian Pac. J. Cancer Prev. 14: 2201-2205.
    Pubmed CrossRef
  17. Park KY, Lee HJ, Jeong SJ, Lee HJ, Kim HS, Kim SH, et al. 2010. 1,2,3,4,6-Penta-O-galloly-beta-D-glucose suppresses hypoxiainduced accumulation of hypoxia-inducible factor-1α and signaling in LNCaP prostate cancer cells. Biol. Pharm. Bull. 33: 1835-1840.
    Pubmed CrossRef
  18. Pinto MP, Dye WW, Jacobsen BM, Horwitz KB. 2014. Malignant stroma increases luminal breast cancer cell proliferation and angiogenesis through platelet-derived growth factor signaling. BMC. Cancer 14: 735.
    Pubmed PMC CrossRef
  19. Shankar S, Srivastava RK. 2007. Involvement of Bcl-2 family members, phosphatidylinositol 3’-kinase/AKT and mitochondrial p53 in curcumin (diferulolylmethane)-induced apoptosis in prostate cancer. Int. J. Oncol. 30: 905-918.
    CrossRef
  20. Stärkel P, Charette N, Borbath I, Schneider-Merck T, De Saeger C, Abarca J, et al. 2012. Ras inhibition in hepatocarcinoma by S-trans-trans-farnesylthiosalicyclic acid:association of its tumor preventive effect with cell proliferation, cell cycle events, and angiogenesis. Mol. Carcinog. 51: 816-825.
    Pubmed CrossRef
  21. Su CH, Chen LJ, Liao JF, Cheng JT. 2013. Increase of phosphatase and tensin homolog by silymarin to inhibit human pharynx squamous cancer. J. Med. Food 16: 778-784.
    Pubmed PMC CrossRef
  22. Sun CC, Zhang YS, Xue X, Cheng YN, Liu HP, Zhao CR, et al. 2011. Inhibition of angiogenesis involves in anticancer activity of riccardin D, a macrocyclic bisbibenzyl, in human lung carcinoma. Eur. J. Pharmacol. 667: 136-143.
    Pubmed CrossRef
  23. Wu Y, Liu F. 2013. Targeting mTOR: evaluating the therapeutic potential of resveratrol for cancer treatment. Anticancer Agents Med. Chem. 13: 1032-1038.
    Pubmed CrossRef
  24. Yang MH, Kim J, Khan IA, Walker LA, Khan SI. 2014. Nonsteroidal anti-inflammatory drug activated gene-1 (NAG-1) modulators from natural products as anti-cancer agents. Life Sci. 100: 75-84.
    Pubmed CrossRef
  25. Yun TK. 2003. Experimental and epidemiological evidence on non-organ specific cancer preventive effect of Korean ginseng and identification of active compounds. Mutat. Res. 523: 63-74.
    CrossRef
  26. Zhang H, Xu HL, Fu WW, Xin Y, Li MW, Wang SJ, et al. 2014. 20(S)-Protopanaxadiol induces human breast cancer MCF-7 apoptosis through a caspase-mediated pathway. Asian Pac. J. Cancer Prev. 15: 7919-7923.
    Pubmed CrossRef
  27. Zhao Z, Holle L, Song W, Wei Y, Wagner TE, Yu X. 2011. Antitumor and anti-angiogenic activities of Scutellaria barbata extracts in vitro are partially mediated by inhibition of Akt/protein kinase B. Mol. Med. Rep. 5: 788-792.
    Pubmed

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Article

Research article

J. Microbiol. Biotechnol. 2015; 25(9): 1485-1492

Published online September 28, 2015 https://doi.org/10.4014/jmb.1503.03059

Copyright © The Korean Society for Microbiology and Biotechnology.

Dealcoholized Korean Rice Wine (Makgeolli) Exerts Potent Anti-Tumor Effect in AGS Human Gastric Adenocarcinoma Cells and Tumor Xenograft Mice

Eun Ju Shin 1, 2, Sung Hee Kim 1, Jae Ho Kim 1, Jaeho Ha 1, 2 and Jin-Taek Hwang 1, 2*

1Korea Food Research Institute, Seongnam 463-746, Republic of Korea, 2Department of Food Biotechnology, Korea University of Science and Technology, Daejeon 305-333, Republic of Korea

Received: March 17, 2015; Accepted: May 21, 2015

Abstract

Makgeolli is a traditional wine in Korea and has been traditionally believed to exhibit health
benefits. However, the inhibitory effect of dealcoholized makgeolli (MK) on cancer has never
been investigated scientifically. In this study, MK exhibited an anti-angiogenic effect by
inhibiting tube formation in human umbilical vein endothelial cells, without cytotoxicity.
Treatment with MK reduced the proliferation of AGS human gastric adenocarcinoma cells in a
dose-dependent manner and increased the sub-G1 population. Next, we evaluated whether
MK could induce apoptosis in AGS cells by using the terminal deoxynucleotidyl transferase
dUTP nick end labeling (TUNEL) assay or Annexin V method. Treatment with MK at 500 and
1,000 μg/ml increased the number of TUNEL-positive AGS cells. Under the same conditions,
MK-treated (500 and 1,000 μg/ml) cells showed significant induction of early or late apoptosis,
compared with untreated cells (no induction). In addition, MK also induced phosphatase and
tensin homolog (PTEN) expression in AGS cells. However, p53 expression in AGS cells was
not changed by MK treatment. Furthermore, MK at 500 mg/kg·d reduced the tumor size and
volume in AGS tumor xenografts. Taken together, MK may be useful for the prevention of
cancer cell growth.

Keywords: Makgeolli, anti-cancer, anti-angiogenesis, AGS human gastric adenocarcinoma cells, Tumor xenograft

References

  1. Arumugam A, Agullo P, Boopalan T, Nandy S, Lopez R, Gutierrez C, et al. 2014. Neem leaf extract inhibits mammary carcinogenesis by altering cell proliferation, apoptosis, and angiogenesis. Cancer Biol. Ther. 15: 26-34.
    Pubmed KoreaMed CrossRef
  2. Chen Q, Ganapathy S, Singh KP, Shankar S, Srivastava RK. 2010. Resveratrol induces growth arrest and apoptosis through activation of FOXO transcription factors in prostate cancer cells. PLoS One 5: e15288.
    Pubmed KoreaMed CrossRef
  3. Crane C, Panner A, Pieper RO, Arbiser J, Parsa AT. 2009. Honokiol-mediated inhibition of PI3K/mTOR pathway: a potential strategy to overcome immunoresistance in glioma, breast, and prostate carcinoma without impacting T cell function. J. Immunother. 32: 585-592.
    Pubmed KoreaMed CrossRef
  4. Ha J, Wang Y, Jang H, Seog H, Chen X. 2014. Determination of E,E-farnesol in makgeolli (rice wine) using dynamic headspace sampling and stir bar sorptive extraction coupled with gas chromatography-mass spectrometry. Food Chem. 142: 79-86.
    Pubmed CrossRef
  5. Hassan B, Akcakanat A, Holder AM, Meric-Bernstam F. 2013. Targeting the PI3-kinase/Akt/mTOR signaling pathway. Surg. Oncol. Clin. N. Am. 22: 641-664.
    Pubmed KoreaMed CrossRef
  6. Hu Y, Wang S, Wu X, Zhang J, Chen R, Chen M, Wang Y. 2013. Chinese herbal medicine-derived compounds for cancer therapy: a focus on hepatocellular carcinoma. J. Ethnopharmacol. 149: 601-612.
    Pubmed CrossRef
  7. Joo JH, Jetten AM. 2010. Molecular mechanisms involved in farnesol-induced apoptosis. Cancer Lett. 287: 123-135.
    Pubmed KoreaMed CrossRef
  8. Jung H, Lee SJ, Lim JH, Kim BK, Park KJ. 2014. Chemical and sensory profiles of makgeolli, Korean commercial rice wine, from descriptive, chemical, and volatile compound analyses. Food Chem. 152: 624-632.
    Pubmed CrossRef
  9. Kang BS, Lee JE, Park HJ. 2014. Qualitative and quantitative prediction of volatile compounds from initial amino acid profiles in Korean rice wine (makgeolli) model. J. Food Sci. 79: C1106-C1116.
    Pubmed CrossRef
  10. Khuda-Bukhsh AR, Das S, Saha SK. 2014. Molecular approaches toward targeted cancer prevention with some food plants and their products: inflammatory and other signal pathways. Nutr. Cancer 66: 194-205.
    Pubmed CrossRef
  11. Kitagishi Y, Matsuda S, Minami A, Ono Y, Nakanishi A, Ogura Y. 2014. Regulation in cell cycle via p53 and PTEN tumor suppressors Cancer Stud. Mol. Med. Open J. 1: 1-7.
  12. Lehman JA, Waning DL, Batuello CN, Cipriano R, Kadakia MP, Mayo LD. 2011. Induction of apoptotic genes by a p73phosphatase and tensin homolog (p73-PTEN) protein complex in response to genotoxic stress. J. Biol. Chem. 286:36631-36640.
    Pubmed KoreaMed CrossRef
  13. Lee HJ, Lee EO, Rhee YH, Ahn KS, Li GX, Jiang C, et al. 2006. An oriental herbal cocktail, ka-mi-kae-kyuk-tang, exerts anti-cancer activities by targeting angiogenesis, apoptosis and metastasis. Carcinogenesis 27: 2455-2463.
    Pubmed CrossRef
  14. Li Y, Kong D, Bao B, Ahmad A, Sarkar FH. 2011. Induction of cancer cell death by isoflavone: the role of multiple signaling pathways. Nutrients 3: 877-896.
    Pubmed KoreaMed CrossRef
  15. Mukhtar E, Adhami VM, Khan N, Mukhtar H. 2012. Apoptosis and autophagy induction as mechanism of cancer prevention by naturally occurring dietary agents. Curr. Drug Targets 13: 1831-1841.
    Pubmed KoreaMed CrossRef
  16. Pandurangan AK. 2013. Potential targets for prevention of colorectal cancer: a focus on PI3K/Akt/mTOR and Wnt pathways. Asian Pac. J. Cancer Prev. 14: 2201-2205.
    Pubmed CrossRef
  17. Park KY, Lee HJ, Jeong SJ, Lee HJ, Kim HS, Kim SH, et al. 2010. 1,2,3,4,6-Penta-O-galloly-beta-D-glucose suppresses hypoxiainduced accumulation of hypoxia-inducible factor-1α and signaling in LNCaP prostate cancer cells. Biol. Pharm. Bull. 33: 1835-1840.
    Pubmed CrossRef
  18. Pinto MP, Dye WW, Jacobsen BM, Horwitz KB. 2014. Malignant stroma increases luminal breast cancer cell proliferation and angiogenesis through platelet-derived growth factor signaling. BMC. Cancer 14: 735.
    Pubmed KoreaMed CrossRef
  19. Shankar S, Srivastava RK. 2007. Involvement of Bcl-2 family members, phosphatidylinositol 3’-kinase/AKT and mitochondrial p53 in curcumin (diferulolylmethane)-induced apoptosis in prostate cancer. Int. J. Oncol. 30: 905-918.
    CrossRef
  20. Stärkel P, Charette N, Borbath I, Schneider-Merck T, De Saeger C, Abarca J, et al. 2012. Ras inhibition in hepatocarcinoma by S-trans-trans-farnesylthiosalicyclic acid:association of its tumor preventive effect with cell proliferation, cell cycle events, and angiogenesis. Mol. Carcinog. 51: 816-825.
    Pubmed CrossRef
  21. Su CH, Chen LJ, Liao JF, Cheng JT. 2013. Increase of phosphatase and tensin homolog by silymarin to inhibit human pharynx squamous cancer. J. Med. Food 16: 778-784.
    Pubmed KoreaMed CrossRef
  22. Sun CC, Zhang YS, Xue X, Cheng YN, Liu HP, Zhao CR, et al. 2011. Inhibition of angiogenesis involves in anticancer activity of riccardin D, a macrocyclic bisbibenzyl, in human lung carcinoma. Eur. J. Pharmacol. 667: 136-143.
    Pubmed CrossRef
  23. Wu Y, Liu F. 2013. Targeting mTOR: evaluating the therapeutic potential of resveratrol for cancer treatment. Anticancer Agents Med. Chem. 13: 1032-1038.
    Pubmed CrossRef
  24. Yang MH, Kim J, Khan IA, Walker LA, Khan SI. 2014. Nonsteroidal anti-inflammatory drug activated gene-1 (NAG-1) modulators from natural products as anti-cancer agents. Life Sci. 100: 75-84.
    Pubmed CrossRef
  25. Yun TK. 2003. Experimental and epidemiological evidence on non-organ specific cancer preventive effect of Korean ginseng and identification of active compounds. Mutat. Res. 523: 63-74.
    CrossRef
  26. Zhang H, Xu HL, Fu WW, Xin Y, Li MW, Wang SJ, et al. 2014. 20(S)-Protopanaxadiol induces human breast cancer MCF-7 apoptosis through a caspase-mediated pathway. Asian Pac. J. Cancer Prev. 15: 7919-7923.
    Pubmed CrossRef
  27. Zhao Z, Holle L, Song W, Wei Y, Wagner TE, Yu X. 2011. Antitumor and anti-angiogenic activities of Scutellaria barbata extracts in vitro are partially mediated by inhibition of Akt/protein kinase B. Mol. Med. Rep. 5: 788-792.
    Pubmed