Inhibition of migration and induction of apoptosis in LoVo human colon cancer cells by polysaccharides from Ganoderma lucidum

Molecular Medicine Reports

Volumn 12, Issue 5, 2015, Pages 7629-7636

  Liang, Zeng Enni ^a,b   Yi, You Jin ^b   Guo, Yu Tong ^c   Wang, Ren Cai ^b   Hu, Qiu Long ^b   Xiong, Xing Yao ^b  

^a Hunan Agricultural Bioengineering Research Institute   (China)

^b HUNAN AGRICULTURAL UNIVERSITY   (China)

^c State Administration of Traditional Chinese Medicine   (China)

Author keywords

Apoptosis; Death receptor pathway; Ganoderma lucidum polysaccharides; Human colon cancer

Indexed keywords

ANTINEOPLASTIC AGENT; ARABINOSE; CASPASE 3; CASPASE 8; CASPASE 9; FAS ANTIGEN; FUNGAL POLYSACCHARIDE; GALACTOSE; GLUCOSE; LACTATE DEHYDROGENASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; HERBACEOUS AGENT; POLYSACCHARIDE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER GROWTH; CANCER MORPHOLOGY; CELL DEATH; CELL DENSITY; CELL DIFFERENTIATION; CELL MIGRATION; CELL SURFACE; CHROMATIN; COLON CANCER; CONTROLLED STUDY; CYTOTOXICITY; DNA FRAGMENTATION; ENZYME ACTIVATION; ENZYME RELEASE; GANODERMA LUCIDUM; HUMAN; HUMAN CELL; IC50; IN VITRO STUDY; MICROVILLUS; MIGRATION INHIBITION; MOLECULAR WEIGHT; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN INDUCTION; ULTRAFILTRATION; WESTERN BLOTTING; CELL MOTION; CHEMISTRY; COLON; COLONIC NEOPLASMS; DRUG EFFECTS; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; CASPASE 3; CASPASE 8; CASPASE 9; CELL LINE, TUMOR; CELL MOVEMENT; COLON; COLONIC NEOPLASMS; DRUGS, CHINESE HERBAL; ENZYME ACTIVATION; HUMANS; POLY(ADP-RIBOSE) POLYMERASES; POLYSACCHARIDES; REISHI;

EID: 84943633186     PISSN: 17912997     EISSN: 17913004     Source Type: Journal    
DOI: 10.3892/mmr.2015.4345     Document Type: Article

References (50)

1. Tokunaga T, Oshika Y, Abe Y, Ozeki Y, Sadahiro S, Kijima H, Tsuchida T, Yamazaki H, Ueyama Y, Tamaoki N, et al: Vascular endothelial growth factor (VEGF) mRNA isoform expression pattern is correlated with liver metastasis and poor prognosis in colon cancer. Br J Cancer 77: 998-1002, 1998.
2. Resnick MB, Routhier J, Konkin T, Sabo E and Pricolo VE: Epidermal growth factor receptor, c-MET, beta-catenin, and p53 expression as prognostic indicators in stage II colon cancer: A tissue microarray study. Clin Cancer Res 10: 3069-3075, 2004.
3. Siegel R, Naishadham D and Jermal A: Cancer Statistics, 2013. Ca Cancer J Clin 63: 11-30, 2013.
4. Van Cutsem E, Nordlinger B and Cervantes A; ESMO Guidelines Working Group: Advanced colorectal cancer: ESMO Clinical Practice Guidelines for treatment. Ann Oncol 21 (Suppl 5): v93-v97, 2010.
5. Verweij J, Casali PG, Zalcberg J, LeCesne A, Reichardt P, Blay JY, Issels R, van Oosterom A, Hogendoorn PC, Van Glabbeke M, et al: Progression-free survival in gastrointestinal stromal tumours with high-dose imatinib: Randomised trial. Lancet 36: 1127-1134, 2004.
6. Gordon KB, Tajuddin A, Guitart J, Kuzel TM, Eramo LR and Vonroenn J: Hand-foot syndrome associated with liposome-encapsulated doxorubicin therapy. Cancer 75: 2169-2173, 1995.
7. Berkun Y, Levartovsky D, Rubinow A, Orbach H, Aamar S, Grenader T, Abou Atta I, Mevorach D, Friedman G and Ben-Yehuda A: Methotrexate related adverse effects in patients with rheumatoid arthritis are associated with the A1298C polymorphism of the MTHFR gene. Ann Rheum Dis 63: 1227-1231, 2004.
8. Venditto VJ and Simanek EE: Cancer therapies utilizing the camptothecins: A review of the in vivo literature. Mol Pharm 7: 307-349, 2010.
9. Bao B, Ali S, Banerjee S, Wang Z, Logna F, Azmi AS, Kong D, Ahmad A, Li Y, Padhye S, et al: Curcumin analogue CDF inhibits pancreatic tumor growth by switching on suppressor microRNAs and attenuating EZH2 expression. Cancer Res 72: 335-345, 2012.
10. Tan W, Lu J, Huang M, Li Y, Chen M, Wu G, Gong J, Zhong Z, Xu Z, Dang Y, et al: Anti-cancer natural products isolated from chinese medicinal herbs. Chin Med 6: 27, 2011.
11. Harvey AL: Natural products in drug discovery. Drug Discov Today 13: 894-901, 2008.
12. Liu GT: Recent advances in research of pharmacology and clinical applications of Ganoderma P-Karst. species (Aphyllophoromycetideae) in China. Int J Med Mushrooms 17: 63-67, 2015.
13. Liu YJ, Shen J, Xia YM, Zhang J and Park HS: The polysaccharides from Ganoderma lucidum: Are they always inhibitors on human hepatocarcinoma cells? Carbohydr Polym 90: 1210-1215, 2012.
14. Xu Z, Chen X, Zhong Z, Chen L and Wang Y: Ganoderma lucidum polysaccharides: Immunomodulation and potential anti-tumor activities. Am J Chin Med 39: 15-27, 2011.
15. Shen J, Park HS, Xia YM, Kim GS and Cui SW: The polysaccharides from fermented Ganoderma lucidum mycelia induced miRNAs regulation in suppressed HepG2 cells. Carbohydr Polym 103: 319-324, 2014.
16. Li A, Shuai X, Jia Z, Li H, Liang X, Su D and Guo W: Ganoderma lucidum polysaccharide extract inhibits hepatocellular carcinoma growth by downregulating regulatory T cells accumulation and function by inducing microRNA-125b. J Transl Med 13: 100, 2015.
17. Guo L, Xie J, Ruan Y, Zhou L, Zhu H, Yun X, Jiang Y, Lü L, Chen K, Min Z, et al: Characterization and immunostimulatory activity of a polysaccharide from the spores of Ganoderma lucidum. Int Immunopharmacol 9: 1175-1182, 2009.
18. Zhu XL, Chen AF and Lin ZB: Ganoderma lucidum polysaccharides enhance the function of immunological effector cells in immunosuppressed mice. J Ethnopharmacol 111: 219-226, 2007.
19. Qu HG, Gao L, He D, et al: Effect of reversion of Ganoderma lucidum polysaccharides on cisplatin resistant in ovarian cancer cells and its mechanism. J Jilin Univ (Medicine Edition) 37: 251-255, 2011.
20. Liang Z, Yi YJ, Guo YT, Wang RC and Xiong XY: Effect of combined Ganoderma lucidum polysaccharides and flurouracil proliferation and apoptosis in human colon carcinoma HCT-116 cells. Food Sci 33: 310-314, 2012 (In Chinese).
21. Staub AM: Removal of proteins Sevage method. Methods Carbohydr Chem 5: 5-6, 1965
22. Kochert G: Carbohydrate determination by the phenol-sulfuric acid method. In: Handbook of Phycological Methods, Vol II, Physiological and Biochemical Methods. Hellebust JA and Craigie JS (eds). Cambridge University Press, Cambridge, pp95-97, 1978.
23. Scott RW: Colorimetric determination of hexuronic acids in plant materials. Anal Chem 51: 936-941, 1979.
24. Li YQ, Fang L and Zhang KC: Structure and bioactivities of a galactose rich extracellular polysaccharide from submergedly cultured Ganoderma lucidum. Carbohydr Polym 77: 323-328, 2008.
25. Hu Z, Chen X, Yang X, Gao Y and Zhou S: Water-soluble polysaccharides of Ganoderma lucidum (W-Curt.:Fr.) P. Karst. (Aphyllophoromycetideae) alleviate the dose-limiting toxicities of irinotecan (CPT-11). Int J Med Mushrooms 8: 321-328, 2006.
26. Zhou GQ, Zhao HY and Lu C: Effect of Ganoderma lucidum polysaccharides on intestinal mucosal immune system in H22 liver cancer bearing mice. Zhongguo Zhong Xi Yi Jie He Za Zhi 29: 335-339, 2009 (In Chinese).
27. Shang D, Li Y, Wang C, Wang X, Yu Z and Fu X: A novel polysaccharide from Se-enriched Ganoderma lucidum induces apoptosis of human breast cancer cells. Oncol Rep 25: 267-272, 2011.
28. Ooi VE and Liu F: Immunomodulation and anti-cancer activity of polysaccharide-protein complexes. Curr Med Chem 7: 715-729, 2000.
29. Xu W, Zhang F, Luo Y, Ma L, Kou X and Huang K: Antioxidant activity of a water-soluble polysaccharide purified from Pteridium aquilinum. Carbohydr Res 344: 217-222, 2009.
30. Miyazaki T and Nishijima M: Studies on fungal polysaccharides. XXVII. Structural examination of a water-soluble, antitumor polysaccharide of Ganoderma lucidum. Chem Pharm Bull (Tokyo) 29: 3611-3616, 1981.
31. Mizuno T, Wang G, Zhang J, Kawagishi H, Nishitoba T and Li J: Reishi, Ganoderma lucidum and Ganoderma tsugae: Bioactive substances and medicinal effects. Food Rev Int 11: 151-166, 1995.
32. Zhang L, Zhang M, Zhou Q, Chen J and Zeng F: Solution properties of antitumor sulfated derivative of .(1⋯.>3).D-glucan from Ganoderma lucidum. Biosci Biotechnol Biochem 64: 2172-2178, 2000.
33. Kimura Y, Taniguchi M and Baba K: Antitumor and antimetastatic effects on liver of triterpenoid fractions of Ganoderma lucidum: Mechanism of action and isolation of an active substance. Anticancer Res 22: 3309-3318, 2002.
34. Tang W, Liu JW, Zhao WM, Wei DZ and Zhong JJ: Ganoderic acid T from Ganoderma lucidum mycelia induces mitochondria mediated apoptosis in lung cancer cells. Life Sci 80: 205-211, 2006.
35. Weng CJ and Yen GC: The in vitro and in vivo experimental evidences disclose the chemopreventive effects of Ganoderma lucidum on cancer invasion and metastasis. Clin Exp Metastas 27: 361-369, 2010.
36. Bao XF, Wang XS, Dong Q, Fang JN and Li XY: Structural features of immunologically active polysaccharides from Ganoderma lucidum. Phytochemistry 59: 175-181, 2002.
37. Pan D, Wang L, Chen C, Teng B, Wang C, Xu Z, Hu B and Zhou P: Structure characterization of a novel neutral polysaccharide isolated from Ganoderma lucidum fruiting bodies. Food Chem 135: 1097-1103, 2012.
38. Chan WK, Cheung CC, Law HK, Lau YL and Chan GC: Ganoderma lucidum polysaccharides can induce human monocytic leukemia cells into dendritic cells with immuno-stimulatory function. J Hematol Oncol 1: 9, 2008.
39. Doyle AD, Petrie RJ, Kutys ML and Yamada KM: Dimensions in cell migration. Curr Opin Cell Biol 25: 642-649, 2013.
40. Condeelis J and Pollard JW: Macrophages: Obligate partners for tumor cell migration, invasion, and metastasis. Cell 124: 263-266, 2006.
41. Surh YJ: Cancer chemoprevention with dietary phytochemicals. Nat Rev Cancer 3: 768-780, 2003.
42. Doonan F and Cotter TG: Morphological assessment of apoptosis. Methods 44: 200-204, 2008.
43. Sun B, Cai Y, Li Y, Li J, Liu K, Li Y and Yang Y: The nonstructural protein NP1 of human bocavirus 1 induces cell cycle arrest and apoptosis in Hela cells. Virology 440: 75-83, 2013.
44. Nguyen TTT, Tran E, Nguyen TH, Do PT, Huynh TH and Huynh H: The role of activated MEK-ERK pathway in quercetin-induced growth inhibition and apoptosis in A549 lung cancer cells. Carcinogenesis 25: 647-659, 2004.
45. Chu K, Niu X and Williams LT: A Fas-associated protein factor, FAF1, potentiates Fas-mediated apoptosis. Proc Natl Acad Sci USA 92: 11894-11898, 1995.
46. Huang DC, Hahne M, Schroeter M, Frei K, Fontana A, Villunger A, Newton K, Tschopp J and Strasser A: Activation of Fas by FasL induces apoptosis by a mechanism that cannot be blocked by Bcl-2 or Bcl-x(L). Proc Natl Acad Sci USA 96: 14871-14876, 1999.
47. Li H, Zhu H, Xu CJ and Yuan J: Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94: 491-501, 1998.
48. Xiong J, Cheng G, Tang H, Zhen HN and Zhang X: Ardipusilloside I induces apoptosis in human glioblastoma cells through a caspase-8-independent FasL/Fas-signaling pathway. Environ Toxicol Pharmacol 27: 264-270, 2009.
49. Larrosa M, Tomas-Barberan FA and Espin JC: The dietary hydrolysable tannin punicalagin releases ellagic acid that induces apoptosis in human colon adenocarcinoma Caco-2 cells by using the mitochondrial pathway. J Nutr Biochem 17: 611-625, 2006.
50. Fulda S and Debatin KM: Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene 25: 4798-4811, 2006.