Triterpenes from ganoderma lucidum induce autophagy in colon cancer through the inhibition of p38 mitogen-activated kinase (p38 MAPK)

Nutrition and Cancer

Volumn 62, Issue 5, 2010, Pages 630-640

  Thyagarajan, Anita ^a   Jedinak, Andrej ^a   Nguyen, Hai ^a   Terry, Colin ^a   Baldridge, Lee Ann ^b   Jiang, Jiahua ^a   Sliva, Daniel ^a,b  

^a METHODIST RESEARCH INSTITUTE   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; BECLIN 1; GANODERMA LUCIDUM EXTRACT; MITOGEN ACTIVATED PROTEIN KINASE P38; NATURAL PRODUCT; PROGRAMMED DEATH 1 LIGAND 2; TRITERPENE DERIVATIVE; 4-(4-FLUOROPHENYL)-2-(4-HYDROXYPHENYL)-5-(4-PYRIDYL)IMIDAZOLE; IMIDAZOLE DERIVATIVE; PYRIDINE DERIVATIVE; TRITERPENE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CANCER CELL; CANCER INHIBITION; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL PROLIFERATION; CELL STRAIN HT29; COLON CANCER; CONTROLLED STUDY; CYTOTOXICITY; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TUMOR XENOGRAFT; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; COLONIC NEOPLASMS; DRUG EFFECTS; DRUG SCREENING; GANODERMA LUCIDUM; HT 29 CELL LINE; PATHOLOGY;

ANIMALS; AUTOPHAGY; CELL PROLIFERATION; COLONIC NEOPLASMS; HT29 CELLS; HUMANS; IMIDAZOLES; MALE; MICE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PYRIDINES; REISHI; TRITERPENES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

BASIDIOMYCOTA; GANODERMA LUCIDUM;

EID: 77953988178     PISSN: 01635581     EISSN: None     Source Type: Journal    
DOI: 10.1080/01635580903532390     Document Type: Article

References (54)

1. Jemal A, Siegel R, Ward E, Hao Y, T, Xu J, et al.: Cancer statistics, 2009. CA: A Cancer J Clin 59, 71-96, 2009.
2. World Cancer Research Fund/American Institute for Cancer Research: Food, Nutrition, Physical Activity, and the Prevention of Cancer: A Global Perspective. Washington, DC: American Institute for Cancer Research, 2007.
3. Kim HJ, Chang WK, Kim MK, Lee SS, and Choi BY: Dietary factors and gastric cancer in Korea: a case-control study. Int J Cancer 97, 531-535, 2002.
4. Wasser SP. Reishi (Ganoderma lucidum). In: Encyclopedia of Dietary Supplements. Marcel Dekker, Taylor & Francis Group, CRC Press, 2005.
5. Gao Y and Zhou S: Cancer prevention and treatment by ganoderma, a mushroom with medical properties. Food Rev Int 19, 275-325, 2003.
6. Lin ZB: Cellular and molecular mechanisms of immuno-modulation by Ganoderma lucidum. J Pharm Sci 99, 144-153, 2005.
7. 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.
8. LinKI, Kao YY,Kuo HK,Yang WB, Chou A, et al.: Reishi polysaccharides induce immunoglobulin production through the TLR4/TLR2-mediated induction of transcription factor Blimp-1. J Biol Chem 281, 24111-24123, 2006.
9. Hua KF, Hsu HY, Chao LK, Chen ST,Yang WB, et al.:Ganoderma lucidum polysaccharides enhance CD14 endocytosis of LPS and promote TLR4 signal transduction of cytokine expression. J Cell Physiol 212, 537-550, 2007.
10. Toth JO, Luu B, Ourisson G: Les acides ganoderiques T & Z: triterpenes cytotoxiques de Ganoderma lucidum (Polyporacee). Tetrahedron Lett 24, 1081-1084, 1983.
11. Lin CN, Tome WP, and Won SJ: Novel cytotoxic principles of Formosan Ganoderma lucidum. J Nat Prod 54, 998-1002, 1991.
12. Min BS, Gao JJ, Nakamura N, andHattori M: Triterpenes from the spores of Ganoderma lucidum and their cytotoxicity against meth-A and LLC tumor cells. Chem Pharm Bull 48, 1026-1033, 2000.
13. Gao JJ, Min BS, Ahn EM, Nakamura N, Lee HK, et al.: New triterpene aldehydes, lucialdehydes A-C, from Ganoderma lucidum and their cytotoxicity against murine and human tumor cells. Chem Pharm Bull 50, 837-840, 2002.
14. Wu TS, Shi LS, and Kuo SC: Cytotoxicity of Ganoderma lucidum triterpenes. J Nat Prod 64, 1121-1122, 2001.
15. Lee S, Park S, Oh JW, and Yang C: Natural inhibitors for protein prenyltransferase. Planta Medica 64, 303-308, 1998.
16. ZhuM, Chang Q,Wong LK, Chong FS, and Li RC: Triterpene antioxidants from ganoderma lucidum. Phytotherapy Res 13, 529-531, 1999.
17. Liu J, Kurashiki K, Shimizu K, and Kondo R: 5α-Reductase inhibitory effect of triterpenoids isolated from Ganoderma lucidum. Biol Pharm Bull 29, 392-395, 2006.
18. Li C, Li Y, and Sun HH: New ganoderic acids, bioactive triterpenoid metabolites from the mushroom Ganoderma lucidum. Nat Prod Res 20, 985-991, 2006.
19. Jiang J, Slivova V, Harvey K, Valachovicova T, and Sliva D: Ganoderma lucidum suppresses growth of breast cancer cells through the inhibition of Akt/NF-kappaB signaling. Nutr Cancer 49, 209-216, 2004.
20. Sliva D, Sedlak M, Slivova V, Valachovicova T, Lloyd FP Jr., et al.: Biologic activity of spores and dried powder from Ganoderma lucidum for the inhibition of highly invasive human breast and prostate cancer cells. J Alt Comp Med 9, 491-497, 2003.
21. Jiang J, Slivova V, and Sliva D: Ganoderma lucidum inhibits proliferation of human breast cancer cells by down-regulation of estrogen receptor and NF-kappaB signaling. Int J Oncol 29, 695-703, 2006.
22. Thyagarajan A, Jiang J, Hopf A, Adamec J, and Sliva D: Inhibition of oxidative stress-induced invasiveness of cancer cells by Ganoderma lucidum is mediated through the suppression of interleukin-8 secretion. Int J of Mol Med 18, 657-664, 2006.
23. Jiang J, Slivova V, Valachovicova T, Harvey K, and Sliva D: Ganoderma lucidum inhibits proliferation and induces apoptosis in human prostate cancer cells PC-3. Int J Oncol 24, 1093-1099, 2004.
24. Stanley G, Harvey K, Slivova V, Jiang J, and Sliva D: Ganoderma lucidum suppresses angiogenesis through the inhibition of secretion of VEGF and TGF-beta1 from prostate cancer cells. Biochem Biophys Res Commun 330, 46-52, 2005.
25. Li C, Yin J, Guo F, Zhang D, and Sun HH: Ganoderic acid Sz, a new lanostanoid from the mushroom Ganoderma lucidum. Nat Prod Res 19, 461-465, 2005.
26. Ma J, Ye Q, Hua Y, Zhang D, Cooper R, et al.: New lanostanoids from the mushroom Ganoderma lucidum. J Nat Prod 65, 72-75, 2002.
27. Sliva D, Harvey K, Mason R, Lloyd F Jr., and English D: Effect of phosphatidic acid on human breast cancer cells exposed to doxorubicin. Cancer Inv 19, 783-790, 2001.
28. Singletary K and Milner J: Diet, autophagy, and cancer: a review. Cancer Epidemiol Biomarkers Prev 17, 1596-1610, 2008.
29. Comes F, Matrone A, Lastella P, Nico B, Susca FC, et al.: A novel cell type-specific role of p38alpha in the control of autophagy and cell death in colorectal cancer cells. Cell Death Diff 14, 693-702, 2007.
30. Seglen PO and Gordon PB: 3-Methyladenine: specific inhibitor of autophagic/ lysosomal protein degradation in isolated rat hepatocytes. Proc Nat Acad Sci U S A 79, 1889-1892, 1982.
31. Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, et al.: Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Inv 112, 1809-1820, 2003.
32. Kirkegaard K, Taylor MP, and Jackson WT: Cellular autophagy: surrender, avoidance and subversion by microorganisms. Nat Rev Microbiol 2, 301-314, 2004.
33. Lu H, Kyo E, Uesaka T, Katoh O, andWatanabe H: Prevention of development of N,N'-dimethylhydrazine-induced colon tumors by a water-soluble extract from cultured medium of Ganoderma lucidum (Rei-shi) mycelia in male ICR mice. Int J Mol Med 9, 113-117, 2002.
34. Lu H, Kyo E, Uesaka T, Katoh O, andWatanabe H: A water-soluble extract from culturedmedium of Ganoderma lucidum (Rei-shi) mycelia suppresses azoxymethane-induction of colon cancers in male F344 rats. Oncol Rep 10, 375-379, 2003.
35. Hong KJ, Dunn DM, Shen CL, and Pence BC: Effects of Ganoderma lucidum on apoptotic and anti-inflammatory function inHT-29 human colonic carcinoma cells. Phytotherapy Res 18, 768-770, 2004.
36. Cheung KL, Khor TO, Yu S, and Kong ANT: PEITC induces G1 cell cycle arrest on HT-29 cells through the activation of p38 MAPK signaling pathway. AAPS J 10, 277-281, 2008.
37. Hu H, AhnN-S,YangX, Lee YS, andKang KS: Ganoderma lucidum extract induces cell cycle arrest and apoptosis in MCF-7 human breast cancer cell. Int J Cancer 102, 250-253, 2002.
38. Li CH, Chen PY, Chang UM, Kan LS, Fang WH, et al.: Ganoderic acid X, a lanostanoid triterpene, inhibits topoisomerases and induces apoptosis of cancer cells. Life Sci 77, 252-265, 2005.
39. 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.
40. Lieu CW, Lee SS, and Wang SY: The effect of Ganoderma lucidum on induction of differentiation in leukemic U937 cells. Anticancer Res 12, 1211-1215, 1992.
41. Wang SY, Hsu ML, Hsu HC, Tzeng CH, Lee SS, et al.: The antitumor effect of Ganoderma lucidum is mediated by cytokines released from activated macrophages and T lymphocytes. Intl J Cancer 70, 699-705, 1997.
42. Muller CI, Kumagai T, O'Kelly J, Seeram NP, Heber D, et al.: Ganoderma lucidum causes apoptosis in leukemia, lymphoma and multiple myeloma cells [see comment]. Leukemia Res 30, 841-848, 2006.
43. Hsu CL, Yu YS, and Yen GC: Lucidenic acid B induces apoptosis in human leukemia cells via a mitochondria-mediated pathway. J Agri Food Chem 56, 3973-3980, 2008.
44. Yuen JWM, Gohel MDI, and Au DWT: Telomerase-associated apoptotic events by mushroom ganoderma lucidum on premalignant human urothelial cells. Nutr Cancer 60, 109-119, 2008.
45. Ellington AA, Berhow M, and Singletary KW: Induction of macroautophagy in human colon cancer cells by soybean B-group triterpenoid saponins. Carcinogenesis 26, 159-167, 2005.
46. Ellington AA, Berhow MA, and Singletary KW: Inhibition of Akt signaling and enhanced ERK1/2 activity are involved in induction ofmacroautophagy by triterpenoid B-group soyasaponins in colon cancer cells. Carcinogenesis 27, 298-306, 2006.
47. Xu ZX, Liang J, Haridas V, Gaikwad A, Connolly FP, et al.: A plant triterpenoid, avicin D, induces autophagy by activation of AMP-activated protein kinase. Cell Death Diff 14, 1948-1957, 2007.
48. Tang G, Yue Z, Talloczy Z, Hagemann T, Cho W, et al.: Autophagy induced by Alexander disease-mutant GFAP accumulation is regulated by p38/MAPK and mTOR signaling pathways. Human Mol Genetics 17, 1540-1555, 2008.
49. Lui B, Cheng Y, Zhang B, Bian HG, and Bao JK: Polygonatum cyrtonema lectin induces apoptosis and autophagy in human melanoma A375 cells through a mitochondria-mediated ROS-p38-p53 pathway. Cancer Lett [Epub ahead of print], 2008.
50. Kondo Y, Kanzawa T, Sawaya R, and Kondo S: The role of autophagy in cancer development and response to therapy. Nature Rev Cancer 5, 726-734, 2005.
51. Chang AW, Miles PG: Ganoderma lucidum (Curt:Fr.) P. Karst. (Aphyllophoromycetideae)-a mushrooming medicinal mushroom. Int J Med Mushrooms 1, 139-146, 1999.
52. Wachtel-Galor S, Tomlinson B, and Benzie IFF: Ganoderma lucidum ("Lingzhi"), a Chinese medicinal mushroom: biomarker responses in a controlled human supplementation study. Br J Nutr 91, 263-269, 2004.
53. Li EK, Tam L-S, Wong CK, Li WC, Lam CW, et al.: Safety and efficacy of Ganoderma lucidum (lingzhi) and San Miao San supplementation in patients with rheumatoid arthritis: a double-blind, randomized, placebo-controlled pilot trial. Arthritis Rheum 57, 1143-1150, 2007.
54. Gao Y, Tang W, Dai X, Gao H, Chen G, et al.: Effects of water-soluble Ganoderma lucidum polysaccharides on the immune functions of patients with advanced lung cancer. J Med Food 8, 159-168, 2005.