Ergosterol purified from medicinal mushroom Amauroderma rude inhibits cancer growth in vitro and in vivo by up-regulating multiple tumor suppressors

Oncotarget

Volumn 6, Issue 19, 2015, Pages 17832-17846

  Li, Xiangmin ^a,b,c,d   Wu, Qingping ^b   Xie, Yizhen ^b   Ding, Yinrun ^b   Du, William W ^c,d   Sdiri, Mouna ^c,d   Yang, Burton B ^c,d  

^a SOUTH CHINA UNIVERSITY OF TECHNOLOGY   (China)

^b GUANGDONG INSTITUTE OF MICROBIOLOGY   (China)

^c Sunnybrook Health Sciences Centre   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

Bim; Fas; Foxo3a; Herbal medicine; Medicinal mushroom

Indexed keywords

BIML PROTEIN; BIMS PROTEIN; CELL PROTEIN; ERGOSTEROL; FAS ANTIGEN; FAS LIGAND; TRANSCRIPTION FACTOR FKHRL1; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; PLANT EXTRACT;

AMAURODERMA RUDE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BIML GENE; BIMS GENE; BREAST CANCER CELL LINE; CANCER INHIBITION; CANCER SURVIVAL; CELL DEATH; CELL INVASION; CELL MIGRATION; CELL SURVIVAL; CELL VIABILITY; COLONY FORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG IDENTIFICATION; DRUG MECHANISM; DRUG PURIFICATION; DRUG STRUCTURE; FAS GENE; FASL GENE; FOXO3 GENE; FRACTIONATION; GEL CHROMATOGRAPHY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MEDICINAL MUSHROOM; MELANOMA; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; SIGNAL TRANSDUCTION; SURVIVAL TIME; TUMOR SUPPRESSOR GENE; UPREGULATION; AGARICALES; ANIMAL; CELL MOTION; CHEMISTRY; DRUG EFFECTS; FLOW CYTOMETRY; NEOPLASMS, EXPERIMENTAL; PHYTOTHERAPY; PROCEDURES; REAL TIME POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WESTERN BLOTTING;

AGARICALES; ANIMALS; ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; CELL DEATH; CELL LINE, TUMOR; CELL MOVEMENT; CELL SURVIVAL; ERGOSTEROL; FLOW CYTOMETRY; GENES, TUMOR SUPPRESSOR; HUMANS; MICE; NEOPLASMS, EXPERIMENTAL; PHYTOTHERAPY; PLANT EXTRACTS; REAL-TIME POLYMERASE CHAIN REACTION; UP-REGULATION;

EID: 84938254379     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4026     Document Type: Article

References (58)

1. Liu T, Men Q, Wu G, Yu C, Huang Z, Liu X, Li W. Tetrandrine induces autophagy and differentiation by activating ROS and Notch1 signaling in leukemia cells. Oncotarget. 2015; 6:7992-8006.
2. Wu J, Wu Y, Yang BB. Anticancer activity of Hemsleya amabilis extract. Life Sci. 2002; 71:2161-2170.
3. Wong VK, Chiu P, Chung SS, Chow LM, Zhao YZ, Yang BB, Ko BC. Pseudolaric acid B, a novel microtubuledestabilizing agent that circumvents multidrug resistance phenotype and exhibits antitumor activity in vivo. Clin Cancer Res. 2005; 11:6002-6011.
4. Gao G, Chen L, Li J, Zhang D, Fang Y, Huang H, Chen X, Huang C. Isorhapontigenin (ISO) inhibited cell transformation by inducing G0/G1 phase arrest via increasing MKP-1 mRNA Stability. Oncotarget. 2014; 5:2664-2677.
5. Pozarowski P, Halicka DH, Darzynkiewicz Z. Cell cycle effects and caspase-dependent and independent death of HL-60 and Jurkat cells treated with the inhibitor of NF-kappaB parthenolide. Cell Cycle. 2003; 2:377-383.
6. Ryu E, Son M, Lee M, Lee K, Cho JY, Cho S, Lee SK, Lee YM, Cho H, Sung GH, Kang H. Cordycepin is a novel chemical suppressor of Epstein-Barr virus replication. Oncoscience. 2014; 1:866-881.
7. Huang TT, Wu SP, Chong KY, Ojcius DM, Ko YF, Wu YH, Wu CY, Lu CC, Martel J, Young JD, Lai HC. The medicinal fungus Antrodia cinnamomea suppresses inflammation by inhibiting the NLRP3 inflammasome. J Ethnopharmacol. 2014; 155:154-164.
8. Liu DL, Li YJ, Yang DH, Wang CR, Xu J, Yao N, Zhang XQ, Chen ZS, Ye WC, Zhang DM. Ganoderma lucidum derived ganoderenic acid B reverses ABCB1-mediated multidrug resistance in HepG2/ADM cells. Int J Oncol. 2015.
9. Wu QP, Xie YZ, Deng Z, Li XM, Yang W, Jiao CW, Fang L, Li SZ, Pan HH, Yee AJ, Lee DY, Li C, Zhang Z, Guo J, Yang BB. Ergosterol peroxide isolated from Ganoderma lucidum abolishes microRNA miR-38-mediated tumor cells on chemoresistance. PLoS One. 2012; 7:e44579.
10. Sliva D, Loganathan J, Jiang J, Jedinak A, Lamb JG, Terry C, Baldridge LA, Adamec J, Sandusky GE, Dudhgaonkar S. Mushroom Ganoderma lucidum prevents colitis-associated carcinogenesis in mice. PLoS One. 2012; 7:e47873.
11. Zhao S, Ye G, Fu G, Cheng JX, Yang BB, Peng C. Ganoderma lucidum exerts anti-tumor effects on ovarian cancer cells and enhances their sensitivity to cisplatin. Int J Oncol. 2011; 38:1319-1327.
12. Lin ZB. [The integrated studies on Ganoderma lucidum Kayst. Guided by Traditional Chinese medical theories]. Zhongguo Zhong Xi Yi Jie He Za Zhi. 2001; 21:883-884.
13. Xie YZ LS, Yee A, La Pierre DP, Deng Z, Lee DY, Wu QP, Chen Q, Li C, Zhang Z, Guo J, Jiang Z, Yang BB. Ganoderma lucidum inhibits tumor cell proliferation and induces tumor cell death. Enzyme & Microbial Technol. 2006; 40:177-185.
14. Kirk PM CP, Minter DW, Stalpers JA. (2008). Dictionary of the Fungi. (Wallingford: CSIRO PUBLISHING).
15. Zhang SS, Ma QY, Zou XS, Dai HF, Huang SZ, Luo Y, Yu ZF, Luo HR, Zhao YX. Chemical constituents from the fungus Amauroderma amoiensis and their in vitro acetylcholinesterase inhibitory activities. Planta Med. 2013; 79:87-91.
16. Jiao C, Xie YZ, Yang X, Li H, Li XM, Pan HH, Cai MH, Zhong HM, Yang BB. Anticancer activity of Amauroderma rude. PLoS One. 2013; 8:e66504.
17. Chan PM, Kanagasabapathy G, Tan YS, Sabaratnam V, Kuppusamy UR. Amauroderma rugosum (Blume, T. Nees) Torrend: Nutritional Composition and Antioxidant and Potential Anti-Inflammatory Properties. Evid Based Complement Alternat Med. 2013; 2013:304713.
18. Axelrod M, Gordon VL, Conaway M, Tarcsafalvi A, Neitzke DJ, Gioeli D, Weber MJ. Combinatorial drug screening identifies compensatory pathway interactions and adaptive resistance mechanisms. Oncotarget. 2013; 4:622-635.
19. Kim H, Jung KW, Maeng S, Chen YL, Shin J, Shim JE, Hwang S, Janbon G, Kim T, Heitman J, Bahn YS, Lee I. Network-assisted genetic dissection of pathogenicity and drug resistance in the opportunistic human pathogenic fungus Cryptococcus neoformans. Sci Rep. 2015; 5:8767.
20. Lu MY, Fan WL, Wang WF, Chen T, Tang YC, Chu FH, Chang TT, Wang SY, Li MY, Chen YH, Lin ZS, Yang KJ, Chen SM, Teng YC, Lin YL, Shaw JF, et al. Genomic and transcriptomic analyses of the medicinal fungus Antrodia cinnamomea for its metabolite biosynthesis and sexual development. Proc Natl Acad Sci U S A. 2014; 111:E4743-4752.
21. Chan GC, Chan WK, Sze DM. The effects of beta-glucan on human immune and cancer cells. J Hematol Oncol. 2009; 2:25.
22. Newman DJ, Cragg GM. Natural products as sources of new drugs over the last 25 years. J Nat Prod. 2007; 70:461-477.
23. Chen RY, Yu DQ. Progress of studies on the chemical constituents of Ganoderma triterpene [Article in Chinese]. Yao Xue Xue Bao. 1990; 25:940-953.
24. Wu QP XY, Li SZ, La Pierre DP, Deng Z, Chen Q, Li C, Zhang Z, Guo J, Wong CKA, Lee DY, Yee A, Yang BB. Tumor cell adhesion and integrin expression affected by Ganoderma lucidum. Enzyme & Microbial Technol. 2006; 40:32-41.
25. Liao SF, Liang CH, Ho MY, Hsu TL, Tsai TI, Hsieh YS, Tsai CM, Li ST, Cheng YY, Tsao SM, Lin TY, Lin ZY, Yang WB, Ren CT, Lin KI, Khoo KH, et al. Immunization of fucose-containing polysaccharides from Reishi mushroom induces antibodies to tumor-associated Globo H-series epitopes. Proc Natl Acad Sci U S A. 2013; 110:13809-13814.
26. Wu DT, Meng LZ, Wang LY, Lv GP, Cheong KL, Hu DJ, Guan J, Zhao J, Li SP. Chain conformation and immunomodulatory activity of a hyperbranched polysaccharide from Cordyceps sinensis. Carbohydr Polym. 2014; 110:405-414.
27. Cui J, Chisti Y. Polysaccharopeptides of Coriolus versicolor:physiological activity, uses, and production. Biotechnol Adv. 2003; 21:109-122.
28. Hayakawa K, Mitsuhashi N, Saito Y, Takahashi M, Katano S, Shiojima K, Furuta M, Niibe H. Effect of krestin (PSK) as adjuvant treatment on the prognosis after radical radiotherapy in patients with non-small cell lung cancer. Anticancer Res. 1993; 13:1815-1820.
29. Liu C, Wang HQ, Li BM, Chen RY. Studies on chemical constituents from the fruiting bodies of Ganoderma sinense Zhao, Xu et Zhang. [Article in Chinese]. Zhongguo Zhong Yao Za Zhi. 2007; 32:235-237.
30. Li SP, Li P, Lai CM, Gong YX, Kan KK, Dong TT, Tsim KW, Wang YT. Simultaneous determination of ergosterol, nucleosides and their bases from natural and cultured Cordyceps by pressurised liquid extraction and high- performance liquid chromatography. J Chromatogr A. 2004; 1036:239-243.
31. Anderson MJ, Viars CS, Czekay S, Cavenee WK, Arden KC. Cloning and characterization of three human forkhead genes that comprise an FKHR-like gene subfamily. Genomics. 1998; 47:187-199.
32. Salazar M, Lorente M, Garcia-Taboada E, Perez Gomez E, Davila D, Zuniga-Garcia P, Maria Flores J, Rodriguez A, Hegedus Z, Mosen-Ansorena D, Aransay AM, Hernandez-Tiedra S, Lopez-Valero I, Quintanilla M, Sanchez C, Iovanna JL, et al. Loss of Tribbles pseudokinase-3 promotes Akt-driven tumorigenesis via FOXO inactivation. Cell Death Differ. 2015; 22:131-144.
33. Bowman A, Nusse R. Location, location, location: FoxM1 mediates beta-catenin nuclear translocation and promotes glioma tumorigenesis. Cancer Cell. 2011; 20:415-416.
34. Nestal de Moraes G, Bella L, Zona S, Burton MJ, Lam EW. Insights into a Critical Role of the FOXO3a-FOXM1 Axis in DNA Damage Response and Genotoxic Drug Resistance. Curr Drug Targets. 2014; .
35. Myatt SS, Lam EW. The emerging roles of forkhead box (Fox) proteins in cancer. Nat Rev Cancer. 2007; 7:847-859.
36. Hagenbuchner J, Kuznetsov A, Hermann M, Hausott B, Obexer P, Ausserlechner MJ. FOXO3-induced reactive oxygen species are regulated by BCL2L11 (Bim) and SESN3. J Cell Sci. 2012; 125:1191-1203.
37. Wildey GM, Howe PH. Runx1 is a co-activator with FOXO3 to mediate transforming growth factor beta (TGFbeta)-induced Bim transcription in hepatic cells. J Biol Chem. 2009; 284:20227-20239.
38. Lin CH, Lin CC, Ting WJ, Pai PY, Kuo CH, Ho TJ, Kuo WW, Chang CH, Huang CY, Lin WT. Resveratrol enhanced FOXO3 phosphorylation via synergetic activation of SIRT1 and PI3K/Akt signaling to improve the effects of exercise in elderly rat hearts. Age (Dordr). 2014; 36:9705.
39. Akiyama T, Dass CR, Choong PF. Bim-targeted cancer therapy: a link between drug action and underlying molecular changes. Mol Cancer Ther. 2009; 8:3173-3180.
40. Modur V, Nagarajan R, Evers BM, Milbrandt J. FOXO proteins regulate tumor necrosis factor-related apoptosis inducing ligand expression. Implications for PTEN mutation in prostate cancer. J Biol Chem. 2002; 277:47928-47937.
41. Pluchino LA, Liu AK, Wang HC. Reactive oxygen speciesmediated breast cell carcinogenesis enhanced by multiple carcinogens and intervened by dietary ergosterol and mimosine. Free Radic Biol Med. 2015; 80:12-26.
42. Schiffman FJ, Klein I. Rapid induction of amphotericin B sensitivity in L1210 leukaemia cells by liposomes containing ergosterol. Nature. 1977; 269:65-66.
43. Schiffman FJ, Fisher JM, Rabinovitz M. Ergosterolconferred sensitivity to amphotericin B in cultured K1210 mouse leukemia cells. Biochem Pharmacol. 1977; 26:177-180.
44. Kuml D, Dethoup T, Buttachon S, Singburaudom N, Silva AM, Kijjoa A. Spiculisporic acid E, a new spiculisporic acid derivative and ergosterol derivatives from the marine-sponge associated fungus Talaromyces trachyspermus (KUFA 0021). Nat Prod Commun. 2014; 9:1147-1150.
45. Kitchawalit S, Kanokmedhakul K, Kanokmedhakul S, Soytong K. A new benzyl ester and ergosterol derivatives from the fungus Gymnoascus reessii. Nat Prod Res. 2014; 28:1045-1051.
46. Yazawa Y, Yokota M, Sugiyama K. Antitumor promoting effect of an active component of Polyporus, ergosterol and related compounds on rat urinary bladder carcinogenesis in a short-term test with concanavalin A. Biol Pharm Bull. 2000; 23:1298-1302.
47. Takaku T, Kimura Y, Okuda H. Isolation of an antitumor compound from Agaricus blazei Murill and its mechanism of action. J Nutr. 2001; 131:1409-1413.
48. Zhang Y, Mills GL, Nair MG. Cyclooxygenase inhibitory and antioxidant compounds from the fruiting body of an edible mushroom, Agrocybe aegerita. Phytomedicine. 2003; 10:386-390.
49. Lam EW, Brosens JJ, Gomes AR, Koo CY. Forkhead box proteins: tuning forks for transcriptional harmony. Nat Rev Cancer. 2013; 13:482-495.
50. Cho EC, Kuo ML, Liu X, Yang L, Hsieh YC, Wang J, Cheng Y, Yen Y. Tumor suppressor FOXO3 regulates ribonucleotide reductase subunit RRM2B and impacts on survival of cancer patients. Oncotarget. 2014; 5:4834-4844.
51. Ausserlechner MJ, Salvador C, Deutschmann A, Bodner M, Viola G, Bortolozzi R, Basso G, Hagenbuchner J, Obexer P. Therapy-resistant acute lymphoblastic leukemia (ALL) cells inactivate FOXO3 to escape apoptosis induction by TRAIL and Noxa. Oncotarget. 2013; 4:995-1007.
52. Wilk A, Urbanska K, Grabacka M, Mullinax J, Marcinkiewicz C, Impastato D, Estrada JJ, Reiss K. Fenofibrate-induced nuclear translocation of FoxO3A triggers Bim-mediated apoptosis in glioblastoma cells in vitro. Cell Cycle. 2012; 11:2660-2671.
53. Yang X, Rutnam ZJ, Jiao C, Wei D, Xie Y, Du J, Zhong L, Yang BB. An anti-let-7 sponge decoys and decays endogenous let-7 functions. Cell Cycle. 2012; 11:3097-3108.
54. Li H, Yang BB. Stress response of glioblastoma cells mediated by miR-17-5p targeting PTEN and the passenger strand miR-17-p targeting MDM2. Oncotarget. 2012; 3:1653-1668.
55. Siragam V, Rutnam ZJ, Yang W, Fang L, Luo L, Yang X, Li M, Deng Z, Qian J, Peng C, Yang BB. MicroRNA miR-98 inhibits tumor angiogenesis and invasion by targeting activin receptor-like kinase-4 and matrix metalloproteinase-11. Oncotarget. 2012; 3:1370-1385.
56. Fang L, Li H, Wang L, Hu J, Jin T, Wang J, Yang BB. MicroRNA-17-p promotes chemotherapeutic drug resistance and tumor metastasis of colorectal cancer by repressing PTEN expression. Oncotarget. 2014; 5:2974-2987.
57. Li H, Gupta S, Du WW, Yang BB. MicroRNA-7 inhibits tumor growth by stimulating T-cell mediated host immune response. Oncoscience. 2014; 1:531-539.
58. Fang L, Du WW, Yang W, Rutnam ZJ, Peng C, Li H, O'Malley YQ, Askeland RW, Sugg S, Liu M, Mehta T, Deng Z, Yang BB. MiR-93 enhances angiogenesis and metastasis by targeting LATS2. Cell Cycle. 2012; 11:4352-4365.