Journal of the Korean Society of Food Culture (한국식생활문화학회지)

Korean Society of Food Culture (한국식생활문화학회)
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Anti-proliferative and Apoptotic Activity of Extracts of Lindera glauca Blume root in Human HCT116 Colorectal Cancer Cells

감태나무 뿌리 추출물에 의한 대장암세포의 성장억제 및 세포사멸유도

  • Kim, Yeah-Un (Department of Food and Nutrition, Kwangju Women's University) ;
  • Moon, Ha-Rin (Department of Food and Nutrition, Chonnam National University) ;
  • Han, Inhwa (Department of Food and Nutrition, Kwangju Women's University) ;
  • Yun, Jung-Mi (Department of Food and Nutrition, Chonnam National University)
  • Received : 2021.03.15
  • Accepted : 2021.04.07
  • Published : 2021.04.30
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Abstract

Lindera glauca Blume has been used in Korean traditional medicine to treat the symptoms of paralysis, abdominal pain, speech disorders, extravasations, contusions, and pain caused by rheumatoid arthritis. We investigated the effect of L. glauca Blume extracts on the proliferation of colorectal cancer cells in vitro using HCT116 human colorectal cancer cell lines. We also investigated its mechanism of action. For this purpose, we used the MTT assay, western blotting, DNA fragmentation analysis, and flow cytometry. HCT116 cells were cultured in several concentrations of ethanol extracts of L. glauca Blume root (0, 50, 100 ㎍/mL). In this study, colon cancer cell growth was inhibited by L. glauca Blume root extract in a dose-dependent manner. It was associated with induction of apoptosis as assessed by nuclear fragmentation and cell cycle analysis. Apoptosis was assessed using western blotting for TNF-α, IL-6, NF-κB, Caspase-3, PARP, Bax, Bcl-2, and SIRT1. The extract also dose-dependently upregulated the expression Bax, the pro-apoptotic gene and downregulated the expression of the anti-apoptotic gene Bcl-2. Furthermore, the extract enhanced Caspase-3 activity in a dose-dependent manner. Our findings provide evidence that L. glauca Blume extract may mediate its anti-proliferative effect via the modulation of apoptosis.

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References

  1. Alves NL, Lier RA, Eldering E. 2007. Withdrawal symptoms on display: Bcl-2 members under investigation. Trends Immunol., 28(1):26-32 https://doi.org/10.1016/j.it.2006.11.003
  2. Amaral, JD, Xavier JM, Steer CJ, Rodrigues CM. 2010. The role of p53 in apoptosis. Discov Med., 9(45):145-152
  3. Ashkenazi A, Dixit VM. 1999. Apoptosis control by death and decoy receptors. Curr. Opin. Cell Biol., 11(2):255-260 https://doi.org/10.1016/S0955-0674(99)80034-9
  4. Baliga B, Kumar S. 2003. Apaf-1/cytochrome c apoptosome: an essential initiator of caspase activation or just a sideshow?. Cell Death Differ., 10(1):16-18 https://doi.org/10.1038/sj.cdd.4401166
  5. Bratton SB, Walker G, Srinivasula SM, Sun XM, Butterworth M, Alnemri ES, Cohen GM. 2001. Recruitment, activation and retention of caspases-9 and-3 by Apaf-1 apoptosome and associated XIAP complexes. EMBO J., 20(5):998-1009
  6. Chang YC, Chang FR, Wu YC. 2000. The constituents of Lindera glauca. J. Chin. Chem. Soc., 47(2):373-380 https://doi.org/10.1002/jccs.200000050
  7. Chang YC, Chen CY, Chang FR, Wu YC. 2001. Alkaloids from Lindera glauca. J. Chin. Chem. Soc., 48(4):811-815 https://doi.org/10.1002/jccs.200100116
  8. De Alencar M, Islam MT, De Lima RMT, Paz M, Dos Reis AC, Da Mata A, Filho J, Cerqueira GS, Ferreira PMP, JMC ES, Mubarak MS, Melo-Cavalcante AAC. 2019. Phytol as an anticarcinogenic and antitumoral agent: An in vivo study in swiss mice with DMBA-Induced breast cancer. IUBMB Life., 71(2): 200-212 https://doi.org/10.1002/iub.1952
  9. Debatin KM. 2004. Apoptosis pathways in cancer and cancer therapy. Cancer Immunol. Immunother., 53(3):153-159 https://doi.org/10.1007/s00262-003-0474-8
  10. Delgado AV, McManus AT, Chambers JP. 2003. Production of tumor necrosis factor-alpha, interleukin 1-beta, interleukin 2, and interleukin 6 by rat leukocyte subpopulations after exposure to substance P. Neuropeptides, 37(6):355-361 https://doi.org/10.1016/j.npep.2003.09.005
  11. Delhalle S, Devoix A, Schnekenburger M, Morceau F, Dicato M, Diederich M. 2003. An introduction to the molecular mechanisms of apoptosis. Ann. N. Y. Acad. Sci., 1010(1): 1-8 https://doi.org/10.1196/annals.1299.001
  12. Doan HV, Sritangos P, Iyara R, Chudapongse N. 2020. Chrysophyllum cainito stem bark extract induces apoptosis in Human hepatocarcinoma HepG2 cells through ROS-mediated mitochondrial pathway. PeerJ., 10(8):e10168
  13. Donovan M, Cotter TG. 2004. Control of mitochondrial integrity by Bcl-2 family members and caspase-independent cell death. Biochim. Biophys. Acta. Mol. Cell Res., 1644(2-3):133-147
  14. Green DR, Reed JC. 1998. Mitochondria and apoptosis. Science., 281(5381):1309-1312
  15. Guon TE, Jeong JS, Sook CH. 2017. Effect of Woojeon Extract on Antioxidant and Apoptosis in HCT116 Human Colon Cancer Cells. J. Kor. Tea Soc., 23(3):59-65
  16. Gustin DM, Brenner DE. 2002. Chemoprevention of colon cancer: current status and future prospects. Cancer Metastasis Rev., 21(3-4):323-348 https://doi.org/10.1023/A:1021271229476
  17. Haigis MC, Guarente LP. 2006. Mammalian sirtuins-emerging roles in physiology, aging, and calorie restriction. Genes Dev., 20(21):2913-2921 https://doi.org/10.1101/gad.1467506
  18. Hayden MS, Ghosh S. 2004. Signaling to NF-κB. Genes Dev., 18(18):2195-2224 https://doi.org/10.1101/gad.1228704
  19. Hidalgo A. 2003. The control of cell number during central nervous syroot development in flies and mice. Mech Dev., 120(11):1311-1325 https://doi.org/10.1016/j.mod.2003.06.004
  20. Hu X, Wang J, Xia Y, Simayi M, Ikramullah S, He Y, Cui S, Li S, Wushouer Q. 2016. Resveratrol induces cell cycle arrest and apoptosis in human eosinophils from asthmatic individuals. Mol. Med. Rep., 14(6):5231-5236 https://doi.org/10.3892/mmr.2016.5884
  21. Huang CC, Hwang JM, Tsai JH, Chen JH, Lin H, Lin GJ, Yang HL, Liu JY, Yang CY, Ye JC. 2020. Aqueous Ocimum gratissimum extract induces cell apoptosis in human hepatocellular carcinoma cells. Int. J. Medical Sci., 17(3):338 https://doi.org/10.7150/ijms.39436
  22. Huh GW, Park JH, Kang JH, Jeong TS, Kang HC, Baek NI. 2014. Flavonoids from Lindera glauca Blume as low-density lipoprotein oxidation inhibitors. Nat. Prod. Res., 28(11):831-834 https://doi.org/10.1080/14786419.2013.879583
  23. Huh GW, Park JH, Shrestha S, Lee YH, Ahn EM, Kang HC, Baek NI. 2011. Sterols from Lindera glauca Blume stem wood. J. Appl. Biol. Chem., 54(4):309-312 https://doi.org/10.3839/jabc.2011.050
  24. Huh GW, Park JH, Shrestha S, Lee YH, Ahn EM, Kang HC, Kim YB, Baek NI. 2012. New diarylpropanoids from Lindera glauca Bl. heartwood. Holzforschung., 66(5):585-590 https://doi.org/10.1515/hf.2011.185
  25. Jemal A, Siegel R, Ward E, Murray T, Xu J, Thun MJ. 2007. Cancer statistics, 2007. CA Cancer J. Clin., 57(1):43-66
  26. Jo EH, Kim SH, Ra JC, Kim SR, Cho SD, Jung JW, Yang SR, Park JS, Hwang JW, Aruoma OI, Kim TY, Lee YS, Kang KS, Kang KS. 2005. Chemopreventive properties of the ethanol extract of chinese licorice (Glycyrrhiza uralensis) root: induction of apoptosis and G1 cell cycle arrest in MCF-7 human breast cancer cells. Cancer Lett., 230(2):239-247 https://doi.org/10.1016/j.canlet.2004.12.038
  27. Jo KJ, Yoon MY, Lee MR, Cha MR, Park HR. 2007. The anticancer effect of extracts from Vitex rotundifolia on human colon carcinoma cell lines. J. Appl. Biol. Chem., 50(3):228-232
  28. Kaplanski G, Marin V, Montero-Julian F, Mantovani A, Farnarier C. 2003. IL-6: a regulator of the transition from neutrophil to monocyte recruitment during inflammation. Trends Immunol., 24(1):25-29 https://doi.org/10.1016/S1471-4906(02)00013-3
  29. Kawamura M, Toiyama Y, Tanaka K, Saigusa S, Okugawa Y, Hiro J, Uchida K, Mohri Y, Inoue Y, Kusunoki M. 2012. CXCL5, a promoter of cell proliferation, migration and invasion, is a novel serum prognostic marker in patients with colorectal cancer. Eur. J. Cancer., 48(14):2244-2251 https://doi.org/10.1016/j.ejca.2011.11.032
  30. Khan F, Pandey P, Ahmad V, Upadhyay TK. 2020. Moringa oleifera methanolic leaves extract induces apoptosis and G0/G1 cell cycle arrest via downregulation of Hedgehog Signaling Pathway in human prostate PC-3 cancer cells. J. Food Biochem., 44(8): e13338
  31. Kim BM, Kim GT, Kim EJ, Lim EG, Kim SY, Kim YM. 2016. The Extract from Artemisia annua Linne. Induces p53-independent Apoptosis through Mitochondrial Signaling Pathway in A549 Lung Cancer Cells. J. Life Sci., 26(8):887-894 https://doi.org/10.5352/JLS.2016.26.8.887
  32. Kim HN, Park GH, Kim JD, Park SB, Eo HJ, Jeong JB. 2019a. Effect of the extracts from the leaves and branches of Sageretia thea on β-catenin proteasomal degradation in human colorectal and lung cancer cells. J. Plant Biotechnol., 32(2):153-159
  33. Kim SY, Jeong SI, Kim SZ, Shim JS, Jang SI. 2009. Effects of Continentalic from Aralia Continentalis on Growth Inhibition and Apoptosis Induction in Human Leukemia HL-60 Cells. J Physiol & Pathol Korean Med., 23(6): 1314-1319
  34. Kim TY, Han HS, Lee YJ. 2013. Apoptosis induction of HCT-15 cells by extracts of Undaria pinnatifida with fermented micro-organism. Kor. J. Herbology., 28(4):33-40
  35. Kim YS, Kim EK, Dong X, Park JS, Shin WB, Kim SJ, Go EA, Park PJ, Lim BO. 2019b. Lindera glauca (Siebold et Zucc.) Blume Root Extracts Protect Against tert-Butyl Hydroperoxide-Induced Oxidative Stress. J. Med. Food., 22(5):508-520 https://doi.org/10.1089/jmf.2018.4289
  36. Kim YU, Yun JM. 2015. Antioxidative and Antiproliferative Effects of Lindera glauca Blume on Human Colorectal Cancer Cells. Korean J. Food Cook Sci., 44(4):635-640
  37. Korsmeyer SJ, Shutter JR, Veis DJ, Merry DE, Oltvai ZN. 1993. Bcl-2/Bax: a rheostat that regulates an anti-oxidant pathway and cell death. Semin. Cancer Biol., 4(6):327-332
  38. Lazebnik YA, Kaufmann S, Desnoyers S, Poirier G, Earnshaw W. 1994. Cleavage of poly (ADP-ribose) polymerase by a proteinase with properties like ICE. Nature., 371(6495): 346-347
  39. Lee CC, Hsiao CY, Lee SC, Huang XF, Chang KF, Lee MS, Hsieh MC, Tsai NM. 2020. Suppression of oral cancer by induction of cell cycle arrest and apoptosis using Juniperus communis extract. Biosci. Rep., 40(9): BSR20202083 https://doi.org/10.1042/bsr20202083
  40. Lee JH, Jung SJ, Park YK. 2007. Effects of Euphorbiae lathyridis Semen on cell apoptosis in HCT116 human colon cancer cells. Kor. J. Herbology., 22(2):65-72
  41. Lee S, Seo E. 2019. Effects of Rutin on Anti-inflammatory in Adipocyte 3T3-L1 and Colon Cancer Cell SE-480. J. Korean Soc., 35(1):84-92
  42. Lee SG, Yu MH, Lee SP, Lee IS. 2008. Antioxidant activities and induction of apoptosis by methanol extracts from avocado. J. Korea Soc. Food Sci. Nutr., 37(3):269-275 https://doi.org/10.3746/JKFN.2008.37.3.269
  43. Lee WK, Kim SJ. 2011. Sulforaphane-induced apoptosis was regulated by p53 and Caspase-3 dependent pathway in human chondrosarcoma, HTB-94. J. Life Sci., 21(6):851-857 https://doi.org/10.5352/JLS.2011.21.6.851
  44. Lee YS, Kim HS, Kim SK, Kim SD. 2000. IL-6 mRNA expression in mouse peritoneal macrophages and NIH3T3 fibroblasts in response to Candida albicans. J. Microbiol. Biotechnol., 10(1):8-15
  45. Letai A. 2005. Pharmacological manipulation of Bcl-2 family members to control cell death. J. Clin. Investig., 115(10): 2648-2655 https://doi.org/10.1172/JCI26250
  46. Lim SO, Jun S. 2019. Factors Influencing the Improvement in Lifestyle Among Patients with Colorectal Cancer. Korean J. Adult Nurs., 31(3):325-336 https://doi.org/10.7475/kjan.2019.31.3.325
  47. Lin HI, Chu SJ, Wang D, Feng NH. 2004. Pharmacological modulation of TNF production in macrophages. J. Microbiol. Immunol. Infect., 37(1):8-15
  48. Liu CM, Kao CL, Wu HM, Li WJ, Huang CT, Li HT, Chen CY. 2014. Antioxidant and anticancer aporphine alkaloids from the leaves of Nelumbo nucifera Gaertn. cv. Rosaplena. Molecules., 19(11):17829-17838
  49. Lowe SW, Lin AW. 2000. Apoptosis in cancer. J. Carcinog., 21(3): 485-495
  50. Lundberg IE. 2000. The role of cytokines, chemokines, and adhesion molecules in the pathogenesis of idiopathic inflammatory myopathies. Curr. Rheumatol. Rep., 2(3): 216-224 https://doi.org/10.1007/s11926-000-0082-y
  51. Luo J, Su F, Chen D, Shiloh A, Gu W. 2000. Deacetylation of p53 modulates its effect on cell growth and apoptosis. Nature., 408(6810):377-381
  52. Malumbres M, Barbacid M. 2009. Cell cycle, CDKs and cancer: a changing paradigm. Nat. Rev. Cancer., 9(3):153-166 https://doi.org/10.1038/nrc2602
  53. McGeer PL, McGeer EG. 2008. Glial reactions in Parkinson's disease. J. Mov. Disord., 23(4):474-483
  54. Mosmann T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods., 65(1-2):55-63
  55. Niu J, Hou X, Fang C, An J, Ha D, Qiu L, Ju Y, Zhao H, Du W, Qi J. 2015. Transcriptome analysis of distinct Lindera glauca tissues revealed the differences in the unigenes related to terpenoid biosynthesis. Gene, 559(1):22-30 https://doi.org/10.1016/j.gene.2015.01.002
  56. Novotny L, Szekeres T. 2003. Cancer therapy: new targets for chemotherapy. Hematology, 8(3):129-137 https://doi.org/10.1080/1024533031000112257
  57. Park C, Hyun SK, Hwang HJ, Choi SH, Choi YH. 2010. Induction of apoptosis and inhibition of prostaglandin E2 production by proteoglycan of Phellinus linteus in U937 human leukemia cells. Cancer Prev. Res., 15(1):83-91
  58. Park K-U, Kim JY, Seo KI. 2009. Antioxidative and cytotoxicity activities against human colon cancer cells exhibited by edible crude saponins from soybean cake. J. Korean Soc. Food. Sci. Nutr., 16(5):754-758
  59. Pierce BT, Napolitano PG, Pierce LM, Apodaca CC, Hume Jr RF, Calhoun BC. 2001. The effects of hypoxia and hyperoxia on fetal-placental vascular tone and inflammatory cytokine production. AM. J. Obstet. Gynecol., 185(5): 1068-1072 https://doi.org/10.1067/mob.2001.117636
  60. Reed JC. 2001. Apoptosis-regulating proteins as targets for drug discovery. Trends Mol. Med0., 7(7):314-319 https://doi.org/10.1016/S1471-4914(01)02026-3
  61. Rocca B, FitzGerald GA. 2002. Cyclooxygenases and prostaglandins: shaping up the immune response. Int. Immunopharmacol., 2(5):603-630 https://doi.org/10.1016/S1567-5769(01)00204-1
  62. Ruan QF, Jiang SQ, Zheng XY, Tang YQ, Yang B, Yi T, Jin J, Cui H, Zhao Z. 2020. Pseudoguaianelactones A-C: three unusual sesquiterpenoids from Lindera glauca with anti-inflammatory activities by inhibiting the LPS-induced expression of iNOS and COX-2. Chem Commun (Camb)., 56(10):1517-1520 https://doi.org/10.1039/c9cc09159a
  63. Seki K, Sasaki T, Haga K, Kaneko R. 1994. Two methoxybutanolides from Lindera glauca. Phytochemistry., 36(4): 949-951
  64. Seki K, Sasaki T, Wano S, Haga K, Kaneko R. 1995. Linderanolides and isolinderanolides, ten butanolides from Lindera glauca. Phytochemistry., 40(4):1175-1181
  65. Sheu MJ, Chou PY, Huang CS, Tsai IC, Chien YC, Lin SY, Tsai HY, Cheng HC, Wu CH. 2010. Pipoxolan inhibits proliferation of HL-60 human leukaemia cancer cells by arresting the cell cycle at the G0/G1 phase. Clin. Exp. Pharmacol. Physiol., 37(5-6):605-612 https://doi.org/10.1111/j.1440-1681.2010.05358.x
  66. Shin DY, Yoom MK, Choi YW, Gweon OC, Kim JI, Choi YH. 2009. Apoptosis induction by aged black garlic extracts in AGS human gastric carcinoma cells. Cancer Prev. Res., 14(4):350-358
  67. Shin EJ, Chung S, Hwang JT. 2017. Effect of γ-oryzanol on proliferation and apoptosis of AGS human gastric carcinoma cell. KSBB Journal, 32(2):83-89 https://doi.org/10.7841/ksbbj.2017.32.2.83
  68. Silverman N, Maniatis T. 2001. NF-κB signaling pathways in mammalian and insect innate immunity. Genes Dev., 15(18): 2321-2342 https://doi.org/10.1101/gad.909001
  69. Skaper SD. 2007. The brain as a target for inflammatory processes and neuroprotective strategies. Ann. N. Y. Acad. Sci., 1122(1): 23-34 https://doi.org/10.1196/annals.1403.002
  70. Song G, Mao YB, Cai QF, Yao LM, Ouyang GL, Bao SD. 2005. Curcumin induces human HCT116 colon adenocarcinoma cell apoptosis by activating p53 and regulating apoptosis-related protein expression. Braz. J. Med. Biol. Res., 38(12):1791-1798 https://doi.org/10.1590/S0100-879X2005001200007
  71. Suh WS, Kim KH, Kim HK, Choi SU, Lee KR. 2015. Three new lignan derivatives from Lindera glauca (Siebold et Zucc.) Blume. Helv. Chim. Acta., 98(8):1087-1094 https://doi.org/10.1002/hlca.201500002
  72. Sun SY, Hail Jr N, Lotan R. 2004. Apoptosis as a novel target for cancer chemoprevention. J. Natl. Cancer Inst., 96(9): 662-672 https://doi.org/10.1093/jnci/djh123
  73. Sung B, Chung JW, Bae HR, Choi JS, Kim CM, Kim ND. 2015. Humulus japonicus extract exhibits antioxidative and anti-aging effects via modulation of the AMPK-SIRT1 pathway. Exp. Ther. Med., 9(5):1819-1826 https://doi.org/10.3892/etm.2015.2302
  74. Vaux DL, Korsmeyer SJ. 1999. Cell death in development. Cell., 96(2):245-254 https://doi.org/10.1016/S0092-8674(00)80564-4
  75. Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C. 1995. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J. Immunol. Methods., 184(1): 39-51
  76. Wang R, Tang S, Zhai H, Duan H. 2011. Studies on anti-tumor metastatic constituents from Lindera glauca. Zhongguo Zhong Yao Za Zhi., 36(8):1032-1036
  77. Wang S, Liu Z, Wang L, Zhang X. 2009. NF-κB signaling pathway, inflammation and colorectal cancer. Cell Mol. Immunol., 6(5):327
  78. Wenzel U, Kuntz S, Brendel MD, Daniel H. 2000. Dietary flavone is a potent apoptosis inducer in human colon carcinoma cells. Cancer Res., 60(14):3823-3831
  79. Yang D, Wang F, Ren S, Zhang H, Peng J. 1999. Chemical constituents of the essential oil from the fruits of Lindera glauca and its antifungal activities. Zhong yao cai., 22(6):295-298
  80. Yeung F, Hoberg JE, Ramsey CS, Keller MD, Jones DR, Frye RA, Mayo MW. 2004. Modulation of NF-κB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J., 23(12):2369-2380 https://doi.org/10.1038/sj.emboj.7600244
  81. Ye M, Liu JK, Lu ZX, Zhao Y, Liu SF, Li LL, Tan M, Weng XX, Li W, Cao Y. 2005. Grifolin, a potential antitumor natural product from the mushroom Albatrellus confluens, inhibits tumor cell growth by inducing apoptosis in vitro. FEBS Lett., 579(16):3437-3443 https://doi.org/10.1016/j.febslet.2005.05.013
  82. Yoon WK, Kim DC. 2008. Toosendan Fructus Induces Apoptotic Cell Death in MCF-7 Cell, Via the Inhibition of Bcl-2 Expression. Obstet. Gynecol. Sci., 21(3):18-33
  83. Yu JS, Moon E, Kim KH. 2017. A new cerebroside from the twigs of Lindera glauca (Sieb. et Zucc.) Blume. Bioorg. Chem., 74: 122-125 https://doi.org/10.1016/j.bioorg.2017.07.016
  84. Zhao Q, Kim YU, Han IH, Yun JM. 2016. Inhibition of cell proliferation and induction of apoptosis by ethanolic extract of Lespedeza cuneata G. Don in human colorectal cancer HCT116 cells. J. Korean Soc. Food Sci. Nutr., 45(6):911-917 https://doi.org/10.3746/JKFN.2016.45.6.911
  85. Zou H, Li Y, Liu X, Wang X. 1999. An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J. Biol. Chem., 274(17):11549-11556 https://doi.org/10.1074/jbc.274.17.11549