MAJOR BIOACTIVE TRITERPENOIDS FROM GANODERMA SPECIES AND THEIR THERAPEUTIC ACTIVITY: A REVIEW

  • ZAHOOR AHMAD BHAT Bhat Department of Botany, Section of Plant Pathology and Mycology, University of Kashmir, Hazaratbal, Srinagar, India.
  • ABDUL HAMID WANI Department of Botany, Section of Plant Pathology and Mycology, University of Kashmir, Hazaratbal, Srinagar, India.
  • MOHD YAQUB BHAT Department of Botany, Section of Plant Pathology and Mycology, University of Kashmir, Hazaratbal, Srinagar, India.
  • ABDUL RASHID MALIK Department of Botany, Section of Plant Pathology and Mycology, University of Kashmir, Hazaratbal, Srinagar, India.

Abstract

Ganoderma a traditional Chinese medicine popularly used for complementary cancer therapy and longevity for centuries. The vast amount of study has been performed on the medicinal properties of Ganoderma lucidum. G. lucidum contains various compounds with a high grade of biological activity, which increase the immunity. Several of these substances belong to the triterpenoids and polysaccharides. Proteins, sterols, phenols, lipids, etc., are also present. Ganoderma triterpenes are important secondary metabolites of G. lucidum. Ganoderma triterpenes are limestone-tetracyclic terpenes which have been reported to possess antioxidant, antitumor, anti-human immunodeficiency virus, anticancer, anti-inflammation, cytotoxic, hepatoprotective, and neuroprotective activities. This review deals with most important triterpenes isolated from Ganoderma and their therapeutic effects.

Keywords: Ganoderma, Bioactive metabolites, triterpenes, anti-cancer

References

1. Jong SC, Birmingham JM. Medicinal benefits of the mushroom Ganoderma. Adv Appl Microbiol 1992;37:101-34.
2. Jonathan SG, Kigigha LT, Ohimain E. Evaluation of the inhibitory potentials of eight higher Nigerian fungi against pathogenic microorganisms. Afr J Biomed Res 2008;11:197-202.
3. Leung SW, Yeung KY, Ricky YL, Man YK. Lingzhi (Ganoderma) Research the Past, Present and Future Perspectives in Ganoderma: Genetics, Chemistry, Pharmacology and Therapeutics Proceedings of International Symposium on Ganoderma Research. Beijing: Beijing Medical University Press; 2002. p. 1-9.
4. Paterson RR. Ganoderma a therapeutic fungal biofactory. Phytochemistry 2006;67:1985-2001.
5. Ziegenbein FC, Hanssen HP, König WA. Secondary metabolites from Ganoderma lucidum and Spongiporus leucomallellus. Phytochemistry 2006;67:202-11.
6. Sanodiya BS, Thakur GS, Baghel RK, Prasad GB, Bisen PS. Ganoderma lucidum: A potent pharmacological macrofungus. Curr Pharm Biotechnol 2009;10:717-42.
7. Ríos JL, Andújar I, Recio MC, Giner RM. Lanostanoids from fungi: A group of potential anticancer compounds. J Nat Prod 2012;75:2016 44.
8. Rios JL, Andujar I. Lanostanoids from fungi as potential medicinal agents. Fungal Metab 2017:931-64.
9. Liu JQ, Wang CF, Li Y, Luo HR, Qiu MH. Isolation and bioactivity evaluation of terpenoids from the medicinal fungus Ganoderma sinense. Planta Med 2012;78:368-76.
10. Gao P, Hirano T, Chen Z, Yasuhara T, Nakata Y, Sugimoto A, et al. Isolation and identification of C-19 fatty acids with anti-tumor activity from the spores of Ganoderma lucidum (reishi mushroom). Fitoterapia 2012;83:490-9.
11. Matute RG, Serra A, Figlas D, Curvetto N. Copper and zinc bioaccumulation and bioavailability of Ganoderma lucidum. J Med Food 2011;14:1273-9.
12. Wachtel-Galor S, Yuen J, Buswell JA, Benzie IFF. Ganoderma lucidum (Lingzhi or Reishi): A medicinal mushroom. In: Herbal Medicine: Bimolecular and Clinical Aspects: Boca Raton, USA: CRC Press Taylor and Francis; 2011.
13. Cör D, Knez Ž, Knez Hrn?i? M. Antitumour, antimicrobial, antioxidant and antiacetylcholinesterase effect of Ganoderma lucidum terpenoids and polysaccharides: A Review. Molecules 2018;23:649.
14. Rex DA. Selenium enriched mushrooms as a food supplement for prevention of neurodegenerative diseases. Int J Pharm Pharm Sci 2014;6:1-2.
15. Wang SY, Hsu ML, Hsu HC, Tzeng CH, Lee SS, Shiao MS, et al. The anti-tumor effect of Ganoderma lucidum is mediated by cytokines released from activated macrophages and T lymphocytes. Int J Cancer 1997;70:699-705.
16. Yuen JW, Gohel MD. Anticancer effects of Ganoderma lucidum: A review of scientific evidence. Nutr Cancer 2005;53:11-7.
17. Yen GC, Wu JY. Antioxidant and radical scavenging properties of extracts from Ganoderma tsugae. Food Chem 1999;65:375-9.
18. Wasser SP. Medicinal mushrooms as a source of antitumor and immunomodulating polysaccharides. Appl Microbiol Biotechnol 2002;60:258-74.
19. Lin ZB, Zhang HN. Anti-tumor and immunoregulatory activities of Ganoderma lucidum and its possible mechanisms. Acta Pharmacol Sin 2004;25:1387-95.
20. Kim HW, Kim BK. Biomedicinal triterpenoids of Ganoderma lucidum (Curt: Fr.) P. Karst. (Aphyllophoromycetidae). Int J Med Mushrooms 1999;1:121-38.
21. Hikino H, Konno C, Mirin Y, Hayashi T. Isolation and hypoglycemic activity of ganoderans A and B, glycans of Ganoderma lucidum fruit bodies. Planta Med 1985;51:339-40.
22. Sato N, Zhang Q, Ma CM, Hattori M. Anti-human immunodeficiency virus-1 protease activity of new lanostane-type triterpenoids from Ganoderma sinense. Chem Pharm Bull (Tokyo) 2009;57:1076-80.
23. Gao Y, Tang W, Gao H, Chan E, Lan J, Li X, et al. Antimicrobial activity of the medicinal mushroom Ganoderma. Food Rev Int 2005;21:211-29.
24. Mizuno T, Wang G, Zhang J, Kawagishi H, Nishitoba T, Reishi LJ. Ganoderma lucidum and Ganoderma tsugae: Bioactive substances and medicinal effects. Food Rev Int 1995;11:151-66.
25. Berger A, Rein D, Kratky E, Monnard I, Hajjaj H, Meirim I, et al. Cholesterol-lowering properties of Ganoderma lucidum in vitro, ex vivo, and in hamsters and minipigs. Lipids Health Dis 2004;3:2.
26. Stanley G, Harvey K, Slivova V, Jiang J, Sliva D. Ganoderma lucidum suppresses angiogenesis through the inhibition of secretion of VEGF and TGF-beta1 from prostate cancer cells. Biochem Biophys Res Commun 2005;330:46-52.
27. Hsu SC, Ou CC, Chuang TC, Li JW, Lee YJ, Wang V, et al. Ganoderma tsugae extract inhibits expression of epidermal growth factor receptor and angiogenesis in human epidermoid carcinoma cells: In vitro and in vivo. Cancer Lett 2009;281:108-16.
28. Park EJ, Ko G, Kim J, Sohn DH. Antifibrotic effects of a polysaccharide extracted from Ganoderma lucidum, glycyrrhizin, and pentoxifylline in rats with cirrhosis induced by biliary obstruction. Biol Pharm Bull 1997;20:417-20.
29. el-Mekkawy S, Meselhy MR, Nakamura N, Tezuka Y, Hattori M, Kakiuchi N, et al. Anti-HIV-1 and anti-HIV-1-protease substances from Ganoderma lucidum. Phytochemistry 1998;49:1651-7.
30. Noguchi M, Kakuma T, Tomiyasu K, Kurita Y, Kukihara H, Konishi F, et al. Effect of an extract of Ganoderma lucidum in men with lower urinary tract symptoms: A double-blind, placebo-controlled randomized and dose-ranging study. Asian J Androl 2008;10:651-8.
31. Shi L, Ren A, Mu D, Zhao M. Current progress in the study on biosynthesis and regulation of ganoderic acids. Appl Microbiol Biotechnol 2010;88:1243-51.
32. Liu J, Kurashiki K, Fukuta A, Kaneko S, Suimi Y, Shimizu K, et al. Quantitative determination of the representative triterpenoids in the extracts of Ganoderma lucidum with different growth stages using high-performance liquid chromatography for evaluation of their 5?-reductase inhibitory properties. Food chem 2012;133:1034-38.
33. Yue QX, Song XY, Ma C, Feng LX, Guan SH, Wu WY, et al. Effects of triterpenes from Ganoderma lucidum on protein expression profile of heLa cells. Phytomedicine 2010;17:606-13.
34. Sonoda Y, Sekigawa Y, Sato Y. In vitro effects of oxygenated lanosterol derivatives on cholesterol biosynthesis from 24,25-dihydrolanosterol. Chem Pharm Bull (Tokyo) 1988;36:966-73.
35. Komoda Y, Shimizu M, Sonoda Y, Sato Y. Ganoderic acid and its derivatives as cholesterol synthesis inhibitors. Chem Pharm Bull (Tokyo) 1989;37:531-3.
36. Min BS, Gao JJ, Nakamura N, Hattori M. Triterpenes from the spores of Ganoderma lucidum and their cytotoxicity against meth-A and LLC tumor cells. Chem Pharm Bull (Tokyo) 2000;48:1026-33.
37. González AG, León F, Rivera A, Padrón JI, González-Plata J, Zuluaga JC, et al. New lanostanoids from the fungus Ganoderma concinna. J Nat Prod 2002;65:417-21.
38. Lin SB, Li CH, Lee SS, Kan LS. Triterpene-enriched extracts from Ganoderma lucidum inhibit growth of hepatoma cells via suppressing protein kinase C, activating mitogen-activated protein kinases and G2-phase cell cycle arrest. Life Sci 2003;72:2381-90.
39. You BJ, Lee MH, Tien N, Lee MS, Hsieh HC, Tseng LH, et al. A novel approach to enhancing ganoderic acid production by Ganoderma lucidum using apoptosis induction. PLoS One 2013;8:e53616.
40. Chudzik M, Korzonek-Szlacheta I, Król W. Triterpenes as potentially cytotoxic compounds. Molecules 2015;20:1610-25.
41. Tang W, Liu JW, Zhao WM, Wei DZ, Zhong JJ. Ganoderic acid T from Ganoderma lucidum mycelia induces mitochondria mediated apoptosis in lung cancer cells. Life Sci 2006;80:205-11.
42. Chen NH, Liu JW, Zhong JJ. Ganoderic acid T inhibits tumor invasion in vitro and in vivo through inhibition of MMP expression. Pharmacol Rep 2010;62:150-63.
43. Yue QX, Cao ZW, Guan SH, Liu XH, Tao L, Wu WY, et al. Proteomics characterization of the cytotoxicity mechanism of ganoderic acid D and computer-automated estimation of the possible drug target network. Mol Cell Proteomics 2008;7:949-61.
44. Chang UM, Li CH, Lin LI, Huang CP, Kan LS, Lin SB, et al. Ganoderiol F, a Ganoderma triterpene, induces senescence in hepatoma hepG2 cells. Life Sci 2006;79:1129-39.
45. Gao JJ, Min BS, Ahn EM, Nakamura N, Lee HK, Hattori M, et al. New triterpene aldehydes, lucialdehydes A-C, from Ganoderma lucidum and their cytotoxicity against murine and human tumor cells. Chem Pharm Bull (Tokyo) 2002;50:837-40.
46. Gao JJ, Hirakawa A, Min BS, Nakamura N, Hattori M. In vivo antitumor effects of bitter principles from the antlered form of fruiting bodies of Ganoderma lucidum. J Nat Med 2006;60:42-8.
47. Niu XM, Li SH, Xiao WL, Sun HD, Che CT. Two new lanostanoids from Ganoderma resinaceum. J Asian Nat Prod Res 2007;9:659-64.
48. Guan SH, Xia JM, Yang M, Wang XM, Liu X, Guo DA, et al. Cytotoxic lanostanoid triterpenes from Ganoderma lucidum. J Asian Nat Prod Res 2008;10:705-10.
49. Hsu PL, Lin YC, Ni H, Mo FE. Ganoderma triterpenoids exert antiatherogenic effects in mice by alleviating disturbed flow-induced oxidative stress and inflammation. Oxid Med Cell Longev 2018;2018:3491703.
50. Tokuyama T, Hayashi Y, Nishizawa M, Tokuda H, Chairul SM, Hayashi Y. Applanoxidic acids A, B, C and D, biologically active tetra cyclic triterpenes from Ganoderma applanatum. Phytochemistry 1991;30:4105-9.
51. Su HJ, Fanny F, Chung MI. New lanostanoids of Ganoderma tsugae. J Nat Prod 2000;63:514-6.
52. Jiang J, Slivova V, Harvey K, Valachovicova T, Sliva D. Ganoderma lucidum suppresses growth of breast cancer cells through the inhibition of Akt/NF-?B signaling. Nutr Cancer 2004;49:209-16.
53. Fukuzawa M, Yamaguchi R, Hide I, Chen Z, Hirai Y, Sugimoto A, et al. Possible involvement of long chain fatty acids in the spores of Ganoderma lucidum (Reishi houshi) to its anti-tumor activity. Biol Pharm Bull 2008;31:1933-7.
54. Jedinak A, Thyagarajan-Sahu A, Jiang J, Sliva D. Ganodermanontriol, a lanostanoid triterpene from Ganoderma lucidum, suppresses growth of colon cancer cells through ß-catenin signaling. Int J Oncol 2011;38:761-7.
55. Wu G, Qian Z, Guo J, Hu D, Bao J, Xie J, et al. Ganoderma lucidum extract induces G1 cell cycle arrest, and apoptosis in human breast cancer cells. Am J Chin Med 2012;40:631-42.
56. Wu GS, Guo JJ, Bao JL, Li XW, Chen XP, Lu JJ, et al. Anti-cancer properties of triterpenoids isolated from Ganoderma lucidum a review. Expert Opin Investig Drugs 2013;22:981-92.
57. Sliva D, Loganathan J, Jiang J, Jedinak A, Lamb JG, Terry C, et al. Mushroom Ganoderma lucidum prevents colitis-associated carcinogenesis in mice. PLoS One 2012;7:e47873.
58. Shtutman M, Zhurinsky J, Simcha I, Albanese C, D’Amico M, Pestell R, et al. The cyclin D1 gene is a target of the ?-catenin/LEF-1 pathway. Proc Natl Acad Sci USA 1999; 96:5522-7.
59. Yan YX, Nakagawa H, Lee MH, Rustgi AK. Transforming growth factor-alpha enhances cyclin D1 transcription through the binding of early growth response protein to a cis-regulatory element in the cyclin D1 promoter. J Biol Chem 1997;272:33181-90.
60. Bartkova J, Lukas J, Strauss M, Bartek J. The PRAD-1/cyclin D1 oncogene product accumulates aberrantly in a subset of colorectal carcinomas. Int J Cancer 1994;58:568-73.
61. Thompson LJ, Fields AP. ?II protein kinase C is required for the G2/M phase transition of cell cycle. J Biol Chem 1996;271:15045-53.
62. Fishman DD, Segal S, Livneh E. The role of protein kinase C in G1 and G2/M phases of the cell cycle (review). Int J Oncol 1998;12:181 6.
63. Hofmann J, O’Connor PM, Jackman J, Schubert C, Ueberall F, Kohn KW, et al. The protein kinase C inhibitor ilmofosine (BM 41 440) arrests cells in G2 phase and suppresses CDC2 kinase activation through a mechanism different from that of DNA damaging agents. Biochem Biophys Res Commun 1994;199:937-43.
64. Arita Y, Buffolino P, Coppock DL. Regulation of the cell cycle at the G2/M boundary in metastatic melanoma cells by 12-O-tetradecanoyl phorbol-13-acetate (TPA) by blocking p34cdc2 kinase activity. Exp Cell Res 1998;242:381-90.
65. Liu Y, Guyton KZ, Gorospe M, Xu Q, Lee JC, Holbrook NJ. Differential activation of ERK, JNK/SAPK and P3/CSBP/RK map kinase family members during the cellular response to arsenite. Free Radic Biol Med 1996;21:771-81.
66. Price MA, Cruzalegui FH, Treisman R. The p38 and ERK MAP kinase pathways cooperate to activate Ternary Complex Factors and c-fos transcription in response to UV light. EMBO J 1996;15:6552-63.
67. Johnson GL, Lapadat R. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 2002;298:1911-2.
68. Li CH, Chen PY, Chang UM, Kan LS, Fang WH, Tsai KS, et al. Ganoderic acid X, a lanostanoid triterpene, inhibits topoisomerases and induces apoptosis of cancer cells. Life Sci 2005;77:252-65.
69. Kumar DS, Senthilkumar P, Surendran L, Sudhagar B. Ganoderma lucidum oriental mushroom mediated synthesis of gold nanoparticles conjugated with doxorubicin and evaluation of its anticancer potential on human breast cancer MCF-7/DOX cells. Int J Pharm Pharm Sci 2017;9:267-74.
70. Liu RM, Li YB, Zhong JJ. Cytotoxic and pro-apoptotic effects of novel ganoderic acid derivatives on human cervical cancer cells in vitro. Eur J Pharmacol 2012;681:23-33.
71. Liu RM, Zhong JJ. Ganoderic acid mf and S induce mitochondria mediated apoptosis in human cervical carcinoma heLa cells. Phytomedicine 2011;18:349-55.
72. Green D, Kroemer G. The central executioners of apoptosis: Caspases or mitochondria? Trends Cell Biol 1998;8:267-71.
73. Green DR, Reed JC. Mitochondria and apoptosis. Science 1998;281:1309-12.
74. Wu TS, Shi LS, Kuo SC. Cytotoxicity of Ganoderma lucidum triterpenes. J Nat Prod 2001;64:1121-2.
75. Zong WX, Li C, Hatzivassiliou G, Lindsten T, Yu QC, Yuan J, et al. Bax and bak can localize to the endoplasmic reticulum to initiate apoptosis. J Cell Biol 2003;162:59-69.
76. Yue GG, Fung KP, Tse GM, Leung PC, Lau CB. Comparative studies of various Ganoderma species and their different parts with regard to their antitumor and immunomodulating activities in vitro. J Altern Complement Med 2006;12:777-89.
77. Lobo V, Patil A, Phatak A, Chandra N. Free radicals, antioxidants and functional foods: Impact on human health. Pharmacogn Rev 2010;4:118-26.
78. Dreher D, Junod AF. Role of oxygen free radicals in cancer development. Eur J Cancer 1996;32A:30-8.
79. Peng XR, Liu JQ, Han ZH, Yuan XX, Luo HR, Qiu MH, et al. Protective effects of triterpenoids from Ganoderma resinaceum on H2O2-induced toxicity in hepG2 cells. Food Chem 2013;141:920-6.
80. Ajith TA, Sudheesh NP, Roshny D, Abishek G, Janardhanan KK. Effect of Ganoderma lucidum on the activities of mitochondrial dehydrogenases and complex I and II of electron transport chain in the brain of aged rats. Exp Gerontol 2009;44:219-23.
81. Cherian E, Sudheesh NP, Janardhanan KK, Patani G. Free-radical scavenging and mitochondrial antioxidant activities of reishi Ganoderma lucidum (Curt: Fr) P. Karst and arogyapacha Trichopus zeylanicus gaertn extracts. J Basic Clin Physiol Pharmacol 2009;20:289-307.
82. Smina TP, De S, Devasagayam TP, Adhikari S, Janardhanan KK. Ganoderma lucidum total triterpenes prevent radiation-induced DNA damage and apoptosis in splenic lymphocytes in vitro. Mutat Res 2011;726:188-94.
83. Smina TP, Mathew J, Janardhanan KK, Devasagayam TP. Antioxidant activity and toxicity profile of total triterpenes isolated from Ganoderma lucidum (Fr.) P. Karst occurring in South India. Environ Toxicol Pharmacol 2011;32:438-46.
84. Smina TP, Joseph J, Janardhanan KK. Ganoderma lucidum total triterpenes prevent ?-radiation induced oxidative stress in Swiss albino mice in vivo. Redox Rep 2016;21:254-61.
85. Paydary K, Khaghani P, Emamzadeh-Fard S, Alinaghi SA, Baesi K. The emergence of drug resistant HIV variants and novel anti-retroviral therapy. Asian Pac J Trop Biomed 2013;3:515-22.
86. Min BS, Nakamura N, Miyashiro H, Bae KW, Hattori M. Triterpenes from the spores of Ganoderma lucidum and their inhibitory activity against HIV-1 protease. Chem Pharm Bull (Tokyo) 1998;46:1607-12.
87. Mizushina Y, Takahashi N, Hanashima L, Koshino H, Esumi Y, Uzawa J, et al. Lucidenic acid O and lactone, new terpene inhibitors of eukaryotic DNA polymerases from a basidiomycete, Ganoderma lucidum. Bioorg Med Chem 1999;7:2047-52.
88. El Dine RS, El Halawany AM, Ma CM, Hattori M. Anti-HIV-1 protease activity of lanostane triterpenes from the Vietnamese mushroom Ganoderma colossum. J Nat Prod 2008;71:1022-6.
89. Cassels BK, Asencio M. Anti-HIV activity of natural triterpenoids and hemisynthetic derivatives 2004-2009. Phytochem Rev 2011;10:545 64.
90. Leber MF, Efferth T. Molecular principles of cancer invasion and metastasis (review). Int J Oncol 2009;34:881-95.
91. Chen NH, Liu JW, Zhong JJ. Ganoderic acid me inhibits tumor invasion through down-regulating matrix metalloproteinases 2/9 gene expression. J Pharmacol Sci 2008;108:212-6.
92. Bielawski K, Bielawska A, S?odownik T, Bo?kun-Skórnicka U, Muszy?ska A. Proline-linked nitrosoureas as prolidase-convertible prodrugs in human breast cancer cells. Pharmacol Rep 2008;60:171 82.
93. Moss LA, Jensen-Taubman S, Stetler-Stevenson WG. Matrix metalloproteinases: Changing roles in tumor progression and metastasis. Am J Pathol 2012;181:1895-9.
94. Chen NH, Zhong JJ. P53 is important for the anti-invasion of ganoderic acid T in human carcinoma cells. Phytomedicine 2011;18:719-25.
95. Cheng CR, Yue QX, Wu ZY, Song XY, Tao SJ, Wu XH, et al. Cytotoxic triterpenoids from Ganoderma lucidum. Phytochemistry 2010;71:1579-85.
96. Brown NS, Jones A, Fujiyama C, Harris AL, Bicknell R. Thymidine phosphorylase induces carcinoma cell oxidative stress and promotes secretion of angiogenic factors. Cancer Res 2000;60:6298-302.
97. Bendre MS, Gaddy-Kurten D, Mon-Foote T, Akel NS, Skinner RA, Nicholas RW, et al. Expression of interleukin 8 and not parathyroid hormone-related protein by human breast cancer cells correlates with bone metastasis in vivo. Cancer Res 2002;62:5571-9.
98. Freund A, Chauveau C, Brouillet JP, Lucas A, Lacroix M, Licznar A, et al. IL-8 expression and its possible relationship with estrogen-receptor-negative status of breast cancer cells. Oncogene 2003;22:256 65.
99. Thyagarajan A, Jiang J, Hopf A, Adamec J, 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 Mol Med 2006;18:657-64.
100. Kohda H, Tokumoto W, Sakamoto K, Fujii M, Hirai Y, Yamasaki K, et al. The biologically active constituents of Ganoderma lucidum (Fr.) karst. Histamine release-inhibitory triterpenes. Chem Pharm Bull (Tokyo) 1985;33:1367-74.
101. Su CH, Lai MN, Chan MH. Hepato-protective triterpenoids from Ganoderma tsugae Murrill. In: Mushroom Biology and Mushroom Products. Hong Kong, China: The Chinese University Press; 1993. p. 275-83.
102. Chen RY, Yu DQ. Studies on the triterpenoid constituents of the spores from Ganoderma lucidum Karst. J Chin Pharm Sci 1993;2:91-6.
103. Liu LY, Chen H, Liu C, Wang HQ, Kang J, Li Y, et al. Triterpenoids of Ganoderma theaecolum and their hepatoprotective activities. Fitoterapia 2014;98:254-9.
104. Wu H, Tang S, Huang Z, Zhou Q, Zhang P, Chen Z, et al. Hepatoprotective effects and mechanisms of action of triterpenoids from lingzhi or reishi medicinal mushroom Ganoderma lucidum (Agaricomycetes) on ?-amanitin-induced liver injury in mice. Int J Med Mushrooms 2016;18:841-50.
105. Wu JG, Kan YJ, Wu YB, Yi J, Chen TQ, Wu JZ, et al. Hepatoprotective effect of Ganoderma triterpenoids against oxidative damage induced by tert-butyl hydroperoxide in human hepatic hepG2 cells. Pharm Biol 2016;54:919-29.
106. Sudheesh NP, Ajith TA, Mathew J, Nima N, Janardhanan KK. Ganoderma lucidum protects liver mitochondrial oxidative stress and improves the activity of electron transport chain in carbon tetrachloride intoxicated rats. Hepatol Res 2012;42:181-91.
107. Fujita A, Arisawa M, Saga M, Hayashi T, Morita N. Two new lanostanoids from Ganoderma lucidum. J Nat Prod 1986;49:1122-5.
108. Lai CS, Yu MS, Yuen WH, So KF, Zee SY, Chang RC. Antagonizing ?-amyloid peptide neurotoxicity of the anti-aging fungus Ganoderma lucidum. Brain Res 2008;1190:215-24.
109. Zhou Y, Qu ZQ, Zeng YS, Lin YK, Li Y, Chung P, et al. Neuroprotective effect of preadministration with Ganoderma lucidum spore on rat hippocampus. Exp Toxicol Pathol 2012;64:673-80.
110. Kubota T, Asaka Y, Miura I, Mori H. Structures of ganoderic acid A and B, two new lanostane type bitter triterpenes from Ganoderma lucidum (FR.) KARST. Helv Chim Acta 1982;65:611-9.
111. Lin LJ, Shiao MS, Yeh SF. Triterpenes from Ganoderma lucidum. Phytochemistry 1988;27:2269-71.
112. Zhang XQ, Ip FC, Zhang DM, Chen LX, Zhang W, Li YL, et al. Triterpenoids with neurotrophic activity from Ganoderma lucidum. Nat Prod Res 2011;25:1607-13.
113. González AG, León F, Rivera A, Muñoz CM, Bermejo J. Lanostanoid triterpenes from Ganoderma lucidum. J Nat Prod 1999;62:1700-1.
114. Lee I, Ahn B, Choi J, Hattori M, Min B, Bae K, et al. Selective cholinesterase inhibition by lanostane triterpenes from fruiting bodies of Ganoderma lucidum. Bioorg Med Chem Lett 2011;21:6603-7.
115. De Marzo AM, Platz EA, Sutcliffe S, Xu J, Grönberg H, Nelson WG, et al. Inflammation in prostate carcinogenesis. Nat Rev Cancer 2007;7:256-69.
116. Birbach A, Eisenbarth D, Kozakowski N, Ladenhauf E, Schmidt- Supprian M, Schmid JA, et al. Persistent inflammation leads to proliferative neoplasia and loss of smooth muscle cells in a prostate tumor model. Neoplasia 2011;13:692-703.
117. Lin CY, Lin CJ, Chen KH, Wu JC, Huang SH, Wang SM, et al. Macrophage activation increases the invasive properties of hepatoma cells by destabilization of the adherens junction. FEBS Lett 2006;580:3042-50.
118. Kimura YN, Watari K, Fotovati A, Hosoi F, Yasumoto K, Izumi H, et al. Inflammatory stimuli from macrophages and cancer cells synergistically promote tumor growth and angiogenesis. Cancer Sci 2007;98:2009-18.
119. Dudhgaonkar S, Thyagarajan A, Sliva D. Suppression of the inflammatory response by triterpenes isolated from the mushroom Ganoderma lucidum. Int Immunopharmacol 2009;9:1272-80.
120. Hirotani M, Ino C, Furuya T, Shiro M. Ganoderic acids T, S and R, new triterpenoids from the cultured mycelia of Ganoderma lucidum. Chem Pharm Bull 1986;234:2282-5.
121. Xu K, Liang X, Gao F, Zhong J, Liu J. Antimetastatic effect of ganoderic acid T in vitro through inhibition of cancer cell invasion. Process Biochem 2010;45:1261-7.
122. Komoda Y, Nakamura H, Ishihara S, Uchida M, Kohda H, Yamasaki K. Structures of new terpenoid constituents of Ganoderma lucidum (Fr.) Karst (Polyporaceae). Chem Pharm Bull 1985;33:4829-35.
123. Jiang J, Grieb B, Thyagarajan A, Sliva D. Ganoderic acids suppress growth and invasive behavior of breast cancer cells by modulating AP-1 and NF-kappaB signaling. Int J Mol Med 2008;21:577-84.
124. Nishitoba T, Sato H, Shirasu S, Sakamura S. Novel triterpenoids from the mycelial mat at the previous stage of fruiting of Ganoderma lucidum. Agric Biol Chem 1987;51:619-22.
125. Chen NH, Zhong JJ. Ganoderic acid Me induces G1 arrest in wild-type p53 human tumor cells while G1/S transition arrest in p53-null cells. Process Biochem 2009;44:928-33.
126. Jiang Z, Jin T, Gao F, Liu J, Zhong J, Zhao H. Effects of ganoderic acid Me on inhibiting multidrug resistance and inducing apoptosis in multidrug resistant colon cancer cells. Process Biochem 2011;46:1307 14.
127. Zhou L, Shi P, Chen NH, Zhong JJ. Ganoderic acid me induces apoptosis through mitochondria dysfunctions in human colon carcinoma cells. Process Biochem 2011;46:219-25.
128. Li F, Wang Y, Wang X, Li J, Cui H, Niu M, et al. Ganoderic acids suppress growth and angiogenesis by modulating the NF-?B signaling pathway in breast cancer cells. Int J Clin Pharmacol Ther 2012;50:712 21.
129. Li P, Deng YP, Wei XX, Xu JH. Triterpenoids from Ganoderma lucidum and their cytotoxic activities. Nat Prod Res 2013;27:17-22.
130. Li YB, Liu RM, Zhong JJ. A new ganoderic acid from Ganoderma lucidum mycelia and its stability. Fitoterapia 2013;84:115-22.
131. Nishitoba T, Sato H, Sakamura S. Novel mycelial components, ganoderic acid Mg, Mh, Mi, Mj and Mk, from the fungus Ganoderma lucidum. Agric Biol Chem 1987;51:1149-53.
132. Chen SY, Chang CL, Chen TH, Chang YW, Lin SB. Colossolactone H, a new Ganoderma triterpenoid exhibits cytotoxicity and potentiates drug efficacy of gefitinib in lung cancer. Fitoterapia 2016;114:81-91.
133. Chen S, Li X, Yong T, Wang Z, Su J, Jiao C, et al. Cytotoxic lanostane-type triterpenoids from the fruiting bodies of Ganoderma lucidum and their structure-activity relationships. Oncotarget 2017;8:10071-84.
134. Jiang J, Jedinak A, Sliva D. Ganodermanontriol (GDNT) exerts its effect on growth and invasiveness of breast cancer cells through the down-regulation of CDC20 and uPA. Biochem Biophys Res Commun 2011;415:325-9.
135. Shiao MS. Triterpenoid natural products in the fungus Ganoderma lucidum. J Chin Chem Soc 1992;39:669-74.
136. Hajjaj H, Macé C, Roberts M, Niederberger P, Fay LB. Effect of 26-oxygenosterols from Ganoderma lucidum and their activity as cholesterol synthesis inhibitors. Appl Environ Microbiol 2005;71:3653-8.
137. Niedermeyer TH, Lindequist U, Mentel R, Gördes D, Schmidt E, Thurow K, et al. Antiviral terpenoid constituents of Ganoderma pfeifferi. J Nat Prod 2005;68:1728-31.
138. Nishitoba T, Oda K, Sato H, Sakamura S. Novel triterpenoids from the fungus Ganoderma lucidum. Agric Biol Chem 1988;52:367-72.
139. Ma BJ, Zhou Y, Ruan Y, Ma JC, Ren W, Wen CN. Lanostane-type triterpenes from the sporoderm-broken spores of Ganoderma lucidum. J Antibiot 2012;65:165-7.
140. Lin CN, Fann YF, Chung MI. Steroids of formosan Ganoderma tsugae. Phytochemistry 1997;46:1143-6.
141. Weng CJ, Chau CF, Hsieh YS, Yang SF, Yen GC. Lucidenic acid inhibits PMA-induced invasion of human hepatoma cells through inactivating MAPK/ERK signal transduction pathway and reducing binding activities of NF-kappaB and AP-1. Carcinogenesis 2008;29:147-56.
142. Hsu CL, Yu YS, Yen GC. Lucidenic acid B induces apoptosis in human leukemia cells via a mitochondria-mediated pathway. J Agric Food Chem 2008;56:3973-80.
143. Nishitoba T, Sato H, Kasai T, Kawagishi H, Sakamura S. New bitter C27 and C30 terpenoids from the fungus Ganoderma lucidum (Reishi). Agric Biol Chem 1985;49:1793-8.
144. Weng CJ, Chau CF, Chen KD, Chen DH, Yen GC. The anti-invasive effect of lucidenic acids isolated from a new Ganoderma lucidum strain. Mol Nutr Food Res 2007;51:1472-7.
145. Kinge TR, Mih AM. Secondary metabolites of oil palm isolate of Ganoderma zonatum Murrill from Cameroon and their cytotoxicity against five human tumor cell lines. Afr J Biotechnol 2011;10:8440-7.
146. Chairul SM, Hayashi Y. Lanostanoid triterpenes from Ganoderma applanatum. Phytochemistry 1994;35:1305-8.
147. Leon F, Valencia M, Rivera A, Nieto I, Quintana J, Estevez F et al. Novel cytostatic lanostanoid triterpenes from Ganoderma australe. Helv Chim Acta 2003;86:3088-95.
148. Kleinwächter P, Anh N, Kiet TT, Schlegel B, Dahse HM, Härtl A, et al. Colossolactone, new triterpenoid metabolites from a Vietnamese mushroom Ganoderma colossum. J Nat Prod 2001;64:236-9.
149. Kikuchi T, Kanomi S, Murai Y, Kadota S, Tsubono K, Ogita ZI. Constituents of the fungus Ganoderma lucidum (FR.) KARST. III. Structures of ganolucidic acids A and B, new lanostane-type triterpenoids. Chem Pharm Bull 1986;34:4030-6.
150. Lee I, Kim H, Youn U, Kim J, Min B, Jung H, et al. Effect of lanostane triterpenes from the fruiting bodies of Ganoderma lucidum on adipocyte differentiation in 3T3-L1 cells. Planta Med 2010;76:1558 63.
151. Mothana RA, Ali NA, Jansen R, Wegner U, Mentel R, Lindequist U, et al. Antiviral lanostanoid triterpenes from the fungus Ganoderma pfeifferi. Fitoterapia 2003;74:177-80.
152. Arisawa M, Fujita A, Saga M, Fukumura H, Hayashi T, Shimizu M, et al. Three new lanostanoids from Ganoderma lucidum. J Nat Prod 1986;49:621-5.
153. Johnson BM, Doonan BP, Radwan FF, Haque A. Ganoderic acid DM: An alternative agent for the treatment of advanced prostate cancer. Open Prost Cancer J 2010;3:78-85.
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Bhat, Z. A. B., ABDUL HAMID WANI, MOHD YAQUB BHAT, and ABDUL RASHID MALIK. “MAJOR BIOACTIVE TRITERPENOIDS FROM GANODERMA SPECIES AND THEIR THERAPEUTIC ACTIVITY: A REVIEW”. Asian Journal of Pharmaceutical and Clinical Research, Vol. 12, no. 4, Mar. 2019, pp. 22-30, https://innovareacademics.in/journals/index.php/ajpcr/article/view/32124.
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