Agarol, an ergosterol derivative from Agaricus blazei, induces caspase-independent apoptosis in human cancer cells

International Journal of Oncology

Volumn 48, Issue 4, 2016, Pages 1670-1678

  Shimizu, Takamitsu ^a,b   Kawai, Junya ^a   Ouchi, Kenji ^a   Kikuchi, Haruhisa ^b   Osima, Yoshiteru ^b   Hidemi, Rikiishi ^b  

^a J   (Japan)

^b TOHOKU UNIVERSITY   (Japan)

Author keywords

Agaricus blazei; Agarol; apoptosis inducing factor; caspase independent apoptosis; p53; reactive oxygen species

Indexed keywords

AGAROL; APOPTOSIS INDUCING FACTOR; BENZYLOXYCARBONYLASPARTYLGLUTAMYLVALYLASPARTYL FLUOROMETHYL KETONE; BETULIC ACID; CASPASE 3; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53; REACTIVE OXYGEN METABOLITE; ANTINEOPLASTIC AGENT; CASPASE; ERGOSTEROL;

AGARICUS BLAZEI; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CARCINOMA CELL LINE; CELL MUTANT; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; DRUG MECHANISM; ENZYME ACTIVITY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; MTT ASSAY; MURINE MODEL; NONHUMAN; OXIDATIVE STRESS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR XENOGRAFT; WESTERN BLOTTING; WILD TYPE; AGARICUS; ANIMAL; CELL PROLIFERATION; CELL SURVIVAL; CHEMISTRY; DRUG EFFECTS; DRUG SCREENING; GENE EXPRESSION REGULATION; METABOLISM; NEOPLASMS; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

AGARICUS; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CASPASES; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; ERGOSTEROL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; NEOPLASMS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84959019372     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2016.3391     Document Type: Article

References (32)

1. Xu T, Beelman RB, and Lambert JD. The cancer preventive effects of edible mushrooms. Anticancer Agents Med Chem. 12: 1255-1263, 2012.
2. Kidd PM. The use of mushroom glucans, and proteoglycans in cancer treatment. Altern Med Rev. 5: 4-27, 2000.
3. Ohno N, Furukawa M, Miura NN, Adachi Y, Motoi M, and Yadomae T. Antitumor beta glucan from the cultured fruit body of Agaricus blazei. Biol Pharm Bull. 24: 820-828, 2001.
4. Takaku T, Kimura Y, and Okuda H. Isolation of an antitumor compound from Agaricus blazei Murill, and its mechanism of action. J Nutr. 131: 1409-1413, 2001.
5. Su Z-Y, Tung Y-C, Hwang LS, and Sheen L-Y: Blazeispirol A from Agaricus blazei fermentation product induces cell death in human hepatoma Hep 3B cells through caspase-dependent, and caspase-independent pathways. J Agric Food Chem. 59: 5109-5116, 2011.
6. Ziliotto L, Pinheiro F, Barbisan LF, and Rodrigues MAM. Screening for in vitro, and in vivo antitumor activities of the mushroom Agaricus blazei. Nutr Cancer. 61: 245-250, 2009.
7. Suzuki M, Endo M, Shinohara F, Echigo S, and Rikiishi H. Differential apoptotic response of human cancer cells to organoselenium compounds. Cancer Chemother Pharmacol. 66: 475-484, 2010.
8. Kroemer G, and Martin SJ. Caspase-independent cell death. Nat Med. 11: 725-730, 2005.
9. Hirose T, and Horvitz HR. An Sp1 transcription factor coordinates caspase-dependent, and -independent apoptotic pathways. Nature. 500: 354-358, 2013.
10. Kim E-A, Jang J-H, Lee Y-H, Sung EG, Song IH, Kim JY, Kim S, Sohn HY, and Lee TJ. Dioscin induces caspase-independent apoptosis through activation of apoptosis-inducing factor in breast cancer cells. Apoptosis. 19: 1165-1175, 2014.
11. Yogeeswari P, and Sriram D. Betulinic acid, and its derivatives: A review on their biological properties. Curr Med Chem. 12: 657-666, 2005.
12. Liu Y, and Luo W. Betulinic acid induces Bax/Bak-independent cytochrome c release in human nasopharyngeal carcinoma cells. Mol Cells. 33: 517-524, 2012.
13. Hetland G, Johnson E, Lyberg T, and Kvalheim G. The mushroom Agaricus blazei murill elicits medicinal effects on tumor, infection, allergy and inflammation through its modulation of innate immunity, and amelioration of Th1/Th2 imbalance, and inflammation. Adv Pharmacol Sci 2011: 157015, 2011.
14. Ooi VE, and Liu F. Immunomodulation, and anti-cancer activity of polysaccharide-protein complexes. Curr Med Chem. 7: 715-729, 2000.
15. Yu C-H, Kan S-F, Shu C-H, Lu T-J, Sun-Hwang L, and Wang PS. Inhibitory mechanisms of Agaricus blazei Murill on the growth of prostate cancer in vitro, and in vivo. J Nutr Biochem. 20: 753-764, 2009.
16. Kobayashi H, Yoshida R, Kanada Y, Fukuda Y, Yagyu T, Inagaki K, Kondo T, Kurita N, Suzuki M, Kanayama N, et al. Suppressing effects of daily oral supplementation of beta-glucan extracted from Agaricus blazei Murill on spontaneous, and peritoneal disseminated metastasis in mouse model. J Cancer Res Clin Oncol. 131: 527-538, 2005.
17. Jin C-Y, Choi YH, Moon D-O, Park C, Park YM, Jeong SC, Heo MS, Lee TH, Lee JD, and Kim GY. Induction of G2/M arrest, and apoptosis in human gastric epithelial AGS cells by aqueous extract of Agaricus blazei. Oncol Rep. 16: 1349-1355, 2006.
18. Rieber M, and Rieber MS. Signalling responses linked to betulinic acid-induced apoptosis are antagonized by MEK inhibitor U0126 in adherent or 3D spheroid melanoma irrespective of p53 status. Int J Cancer. 118: 1135-1143, 2006.
19. Green DR, and Kroemer G. Cytoplasmic functions of the tumour suppressor p53. Nature. 458: 1127-1130, 2009.
20. Tung Y-C, Su Z-Y, Kuo M-L, and Sheen L-Y: Ethanolic extract of Agaricus blazei fermentation product inhibits the growth, and invasion of human hepatoma HA22T/VGH, and SK-Hep-1 cells. J Tradit Complement Med. 2: 145-153, 2012.
21. Hajnóczky G, Davies E, and Madesh M. Calcium signaling, and apoptosis. Biochem Biophys Res Commun. 304: 445-454, 2003.
22. Holley AK, Dhar SK, and St Clair DK. Manganese superoxide dismutase versus p53: The mitochondrial center. Ann NY Acad Sci 1201: 72-78, 2010.
23. Maillet A, and Pervaiz S. Redox regulation of p53, redox effectors regulated by p53: A subtle balance. Antioxid Redox Signal. 16: 1285-1294, 2012.
24. Kim M-O, Moon D-O, Jung JM, Lee WS, Choi YH, and Kim G-Y: Agaricus blazei extract induces apoptosis through ROS-dependent JNK activation involving the mitochondrial pathway, and suppression of constitutive NF-?B in THP-1 cells. Evid Based Complement Alternat Med 2011: 838172, 2011.
25. Chintharlapalli S, Papineni S, Lei P, Pathi S, and Safe S. Betulinic acid inhibits colon cancer cell, and tumor growth, and induces proteasome-dependent, and -independent downregulation of specificity proteins (Sp) transcription factors. BMC Cancer. 11: 371, 2011.
26. Li X, Zhao X, Wang H, Han J, and Liu L. A polysaccharide from the fruiting bodies of Agaricus blazei Murill induces caspasedependent apoptosis in human leukemia HL-60 cells. Tumour Biol. 35: 8963-8968, 2014.
27. Xie J, Xu Y, Huang X, Chen Y, Fu J, Xi M, and Wang L. Berberineinduced apoptosis in human breast cancer cells is mediated by reactive oxygen species generation, and mitochondrial-related apoptotic pathway. Tumour Biol. 36: 1279-1288, 2015.
28. Su J, Cheng H, Zhang D, Wang M, Xie C, Hu Y, Chang HC, and Li Q. Synergistic effects of 5-fluorouracil, and gambogenic acid on A549 cells: Activation of cell death caused by apoptotic, and necroptotic mechanisms via the ROS-mitochondria pathway. Biol Pharm Bull. 37: 1259-1268, 2014.
29. Wu M-F, Chen Y-L, Lee M-H, Shih YL, Hsu YM, Tang MC, Lu HF, Tang NY, Yang ST, Chueh FS, et al. Effect of Agaricus blazei Murrill extract on HT-29 human colon cancer cells in SCID mice in vivo. In Vivo. 25: 673-677, 2011.
30. Wasser SP. Medicinal mushrooms as a source of antitumor, and immunomodulating polysaccharides. Appl Microbiol Biotechnol. 60: 258-274, 2002.
31. Nozaki H, Itonori S, Sugita M, Nakamura K, Ohba K, Suzuki A, and Kushi Y. Mushroom acidic glycosphingolipid induction of cytokine secretion from murine T cells, and proliferation of NK1.1 a/β TCR-double positive cells in vitro. Biochem Biophys Res Commun. 373: 435-439, 2008.
32. Lee JS, and Hong EK. Agaricus blazei Murill enhances doxorubicin-induced apoptosis in human hepatocellular carcinoma cells by NF?B-mediated increase of intracellular doxorubicin accumulation. Int J Oncol. 38: 401-408, 2011.