Research and application progress of Ganoderma lucidum triterpenoids

Abstract

Abstract: Abstract: Ganoderma lucidum is rich in many active ingredients with different pharmacological effects. Triterpenoids in Ganoderma lucidum is one of the main active ingredients, which having liver protection, anti-tumor, high immunity, anti-oxidation, hypolipidemic and other effects. The purpose of this review is to summarize literatures of physical and chemical properties, pharmacological activity, fermentation conditions optimization, quality control and functional foods related to Ganoderma lucidum triterpenoids in the past five years. The research trend of Ganoderma lucidum triterpenoids application in the future is also prospected, which will provide a reference for Ganoderma lucidum in food production, processing and clinical application.

Key words: Key words: Ganoderma lucidum triterpenoids, pharmacological activity, fermentation conditions, quality control, functional food

CLC Number:

R284.2

References

[1]陈若芸.灵芝化学成分与质量控制方法的研究综述[J].食药用菌, 2015, 23(05):270-275 [2]Xiao C, Wu Q P, Cai W, et al.Hypoglycemic effects of Ganoderma lucidum polysaccharides in type 2 diabetic mice[J].Archives of Pharmacal Research, 2012, 35(10):1793-1801 [3]Kozarski M, Klaus A, Nik?i? M, et al.Antioxidative activities and chemical characterization of polysaccharide extracts from the widely used mushrooms Ganoderma applanatum,Ganoderma lucidum,Lentinus edodes and Trametes versicolor[J].Journal of Food Composition & Analysis, 2012, 26(1-2):144-153 [4] Ferreira I C, Heleno S A, Reis F S, et al.Chemical features of Ganoderma polysaccharides with antioxidant, antitumor and antimicrobial activities[J].Phytochemistry, 2015, 114:38-55 [5] Baby S, Johnson A J, Govindan B.Baby S, Johnson A J, Govindan B. Secondary metabolites from Ganoderma[J].Phytochemistry, 2015, 114:66-101 [6]Yu G J, Yin Y L, Yu W H, et al.Proteome Exploration to Provide a Resource for the Investigation of Ganoderma lucidum[J].Plos One, 2015, 10(3):e119439- [7] Andrade P B, Valent?o P, Pereira D M.1. Anti-HIV Natural Products[J].Natural Products Targeting Clinically Relevant Enzymes. Wiley‐VCH Verlag GmbH & Co. KGaA, 2017, :- [8]Ferreira I, Vaz J A, Vasconcelos M H, et al.Compounds from Wild Mushrooms with Antitumor Potential[J].Anti-Cancer Agents in Medicinal Chemistry, 2010, 10(5):424-436 [9]Falandysz J, Borovicka J.Macro and trace mineral constituents and radionuclides in mushrooms: health benefits and risks[J].Applied Microbiology and Biotechnology, 2013, 97(2):477-501 [10]Yildiz O, Can Z, Laghari A Q, et al.Wild Edible Mushrooms as a Natural Source of Phenolics and Antioxidants[J].Journal of Food Biochemistry, 2015, 39(2):148-154 [11]Wong F C, Chai T T, Tan S L, et al.Evaluation of Bioactivities and Phenolic Content of Selected Edible Mushrooms in Malaysia[J].Tropical Journal of Pharmaceutical Research, 2014, 12(6):1011-1016 [12]Boh B.Ganoderma lucidum: a potential for biotechnological production of anti-cancer and immunomodulatory drugs[J].Recent patents on anti-cancer drug discovery, 2013, 8(3):255-87 [13]Wang H C, Chu F H, Chien S C, et al.Establishment of the metabolite profile for an Antrodia cinnamomea health food product and investigation of its chemoprevention activity[J].Journal of Agricultural & Food Chemistry, 2013, 61(36):8556-64 [14]Kabir Y, Kimura S, Tamura T.Dietary effect of Ganoderma lucidum mushroom on blood pressure and lipid levels in spontaneously hypertensive rats (SHR)[J].Journal of Nutritional Science & Vitaminology, 1988, 34(4):433-438 [15] Ma H T, Hsieh J F, Chen S T.Anti-diabetic effects of Ganoderma lucidum[J].Phytochemistry, 2015, 114:109-113 [16]Wu G S, Guo J J, Bao J L, et al.Anti-cancer properties of triterpenoids isolated from Ganoderma lucidum - a review[J].Expert Opinion on Investigational Drugs, 2013, 22(8):981-992 [17]Wu Y W, Fang H L, Lin W C.Post-treatment of Ganoderma lucidum reduced liver fibrosis induced by thioacetamide in mice[J].Phytotherapy Research, 2010, 24(4):494-499 [18] Honda K, Komoda Y, Inoué S.[Sleep-promoting effects of Ganoderma extracts in rats: comparison between long-term and acute administrations][J].Iyo Kizai Kenkyujo Hokoku Reports of the Institute for Medical & Dental Engineering Tokyo Medical & Dental University, 1988, 22:77-82 [19]崔月花, 章克昌.灵芝三萜皂苷的体外抗氧化作用[J].食品科学, 2010, 31(19):49-53 [20]Kubota T, Asaka Y, Miura I, et al.Structures of Ganoderic Acid A and B,Two New Lanostane Type Bitter Triter1penes from Ganoderma lucidum (FR) KARST[J].Helvetica Chimica Acta, 1982, 65(65):611-619 [21]Xia Q, Zhang H, Sun X, et al.A comprehensive review of the structure elucidation and biological activity of triterpenoids from Ganoderma spp[J].Molecules, 2014, 19(11):17478-535 [22]Feng J, Feng N, Yang Y, et al.Simple and Reproducible Two-Stage Agitation Speed Control Strategy for Enhanced Triterpene Production by Lingzhi or Reishi Medicinal Mushrooms,Ganoderma lucidum ACCC G0119 (Higher Basidiomycetes) Based on Submerged Liquid Fermentation[J].International Journal of Medicinal Mushrooms, 2015, 17(12):1151-9 [23]李田田, 黄梓芮, 潘雨阳, 等.树舌灵芝化学成分分析及其多糖、三萜组分的抗氧化活性[J].食品工业科技, 2017, 38(19):63-66 [24]梁磊, 黄清铧, 王庆福, 等.响应面优化微波-超声波协同提取灵芝三萜工艺及其清除自由基活性[J].菌物学报, 2017, 36(04):512-521 [25]Tel- ayan G, Ztürk M, Duru M E, et al.Phytochemical investigation,antioxidant and anticholinesterase activities of Ganoderma adspersum[J].Industrial Crops & Products, 2015, 76(2):749-754 [26]Qian‐Yu K, Chen‐Yu Y, Bor‐Chyuan S, et al.The triterpenoids of Ganoderma tsugae prevent stress-induced myocardial injury in mice[J].Molecular Nutrition & Food Research, 2013, 57(10):1892-6 [27]Feng L, Yuan L, Du M, et al.Anti-lung cancer activity through enhancement of immunomodulation and induction of cell apoptosis of total triterpenes extracted from Ganoderma luncidum (Leyssex Fr.) Karst[J].Molecules, 2013, 18(8):9966-81 [28]Liu C, Song Y, Yang N, et al.Ganoderic Acid β Suppressed Th2 Responses and Induced Th1Tregs in Cultures of Peripheral Blood Mononuclear Cells From Asthmatic Patients[J].Journal of Allergy & Clinical Immunology, 2013, 131(2):A-B1 [29] Su L, Chen R, Lu J, et al.O19 Ganoderma triterpenes inhibit kidney cyst development via down-regulating the Ras/MAPK signaling pathway[J].Biochemical Pharmacology, 2017, 139:115-115 [30]Choi S, Nguyen V T, Tae N, et al.Anti-inflammatory and heme oxygenase-1 inducing activities of lanostane triterpenes isolated from mushroom Ganoderma lucidum in RAW2647 cells.[J].Toxicology & Applied Pharmacology, 2014, 280(3):434-442 [31]Jiao Y, Xie T, Zou L H, et al.Lanostane triterpenoids from Ganoderma curtisii and their NO production inhibitory activities of LPS-induced microglia[J].Bioorganic & Medicinal Chemistry Letters, 2016, 26(15):3556-61 [32]Liu C, Dunkin D, Lai J, et al.Anti-inflammatory Effects of Ganoderma Lucidum Triterpenoid in Human Crohn’s Disease Associated with Down-Regulation of NF-κB Signaling[J].Inflammatory Bowel Diseases, 2015, 21(8):1918-1925 [33]Sillapapongwarakorn S, Yanarojana S, Pinthong D, et al.Molecular docking based screening of triterpenoids as potential G-quadruplex stabilizing ligands with anti-cancer activity[J].Bioinformation, 2017, 13(9):284-292 [34]闫征, 王宏旭, 刘莉莹, 等.灵芝三萜类化合物的体外抗肿瘤活性研究[J].国际检验医学杂志, 2017, 38(5):633-634 [35]Kohno T, Hai-Bang T, Zhu Q, et al.Tubulin polymerization-stimulating activity of Ganoderma triterpenoids[J].Journal of Natural Medicines, 2017, 71(2):1-6 [36]Zheng D S, Chen L S.Triterpenoids from Ganoderma lucidum inhibit the activation of EBV antigens as telomerase inhibitors[J].Experimental & Therapeutic Medicine, 2017, 14(4):3273-3278 [37] 王涛.灵芝三萜的提纯及其对前列腺癌细胞生长的影响[D]. 南方医科大学, 2016. [38]Li P, Deng Y P, Wei X X, et al.Triterpenoids from Ganoderma lucidum and their cytotoxic activities[J].Natural Product Research, 2013, 27(1):17-22 [39] Huang S Z, Ma Q Y, Kong F D, et al.Lanostane-type triterpenoids from the fruiting body of Ganoderma calidophilum[J].Phytochemistry, 2017, 143:104-110 [40]Vazirian M, Faramarzi M A, Ebrahimi S E, et al.Antimicrobial effect of the Lingzhi or Reishi medicinal mushroom,Ganoderma lucidum (higher Basidiomycetes) and its main compounds[J].International Journal of Medicinal Mushrooms, 2014, 16(1):77-84 [41]王开金, 胡少婷, 易敏, 等.灵芝提取物对耻垢分枝杆菌基因表达的影响[J].重庆医学, 2013, 42(16):1809-1811 [42]Liu D Z, Zhu Y Q, Li X F, et al.New triterpenoids from the fruiting bodies of Ganoderma lucidum and their bioactivities[J].Chemistry & Biodiversity, 2014, 11(6):982-986 [43]Zhang W, Tao J, Yang X, et al.Antiviral effects of two Ganoderma lucidum triterpenoids against enterovirus 71 infection[J].Biochemical & Biophysical Research Communications, 2014, 449(3):307-12 [44]刘乔, 管晓辉, 黄翠菊, 等.的提取分离工艺优化及其体内抗氧化活性作用[J].食品科学, 2015, 36(24):89-94 [45]Chiu H F, Fu H Y, Lu Y Y, et al.Triterpenoids and polysaccharide peptides-enriched Ganoderma lucidum: a randomized,double-blind placebo-controlled crossover study of its antioxidation and hepatoprotective efficacy in healthy volunteers[J].Pharmaceutical Biology, 2017, 55(1):1041-1046 [46]Peng X R, Liu J Q, Han Z H, et al.Protective effects of triterpenoids from Ganoderma resinaceum on H2O2-induced toxicity in HepG2 cells[J].Food Chemistry, 2013, 141(2):920-926 [47]刘莉莹, 王洪庆, 刘超, 等.树灵芝中三萜类成分及其保肝作用研究[J].天然产物研究与开发, 2017, 29(04):584-589 [48]Sri Fatmawati, Ryuichiro Kondo, Kuniyoshi Shimizu.Structure–activity relationships of lanostane-type triterpenoids from Ganoderma lingzhi,as α-glucosidase inhibitors[J].Bioorganic & Medicinal Chemistry Letters, 2013, 23(21):5900-5903 [49] Smina T P, Maurya D K, Devasagayam T P, et al.Protection of radiation induced DNA and membrane damages by total triterpenes isolated from Ganoderma lucidum (Fr.) P. Karst[J].Chemico-Biological Interactions, 2015, 233:1-7 [50]Smina T P, Joseph J, Janardhanan K K.Ganoderma lucidum total triterpenes prevent γ-radiation induced oxidative stress in Swiss albino mice in vivo[J].Redox Report Communications in Free Radical Research, 2016, 21(6):254-261 [51]Kang D, Mutakin M, Levita J.Computational Study of Triterpenoids of Ganoderma lucidum with Aspartic Protease Enzymes for Discovering HIV-1 and Plasmepsin Inhibitors[J].International Journal of Chemistry, 2015, 7(1):62-68 [52] Hai-Bang T, Shimizu K.Structure–activity relationship and inhibition pattern of reishi-derived ( Ganoderma lingzhi ) triterpenoids against angiotensin-converting enzyme[J].Phytochemistry Letters, 2015, 12:243-247 [53]Nguyen V T, Tung N T, Cuong T D, et al.Cytotoxic and anti-angiogenic effects of lanostane triterpenoids from Ganoderma lucidum[J].Phytochemistry Letters, 2015, 12(12):69-74 [54]Shen C Y, Xu P H, Shen B D, et al.Nanogel for dermal application of the triterpenoids isolated from Ganoderma lucidum (GLT) for frostbite treatment[J].Drug Delivery, 2015, 23(2):610-618 [55]Schwarz S, Lucas S D, Sommerwerk S, et al.Amino derivatives of glycyrrhetinic acid as potential inhibitors of cholinesterases[J].Bioorganic & Medicinal Chemistry, 2014, 22(13):3370-8 [56]Dang Y L, Wu X Q, Xie A Y, et al.Research on the Capsule of Ganoderma lucidum and Zizhiphi spinozae Improving the Sleep in Mice[J].Advance Journal of Food Science & Technology, 2014, 6(3):378-382 [57]董玉玮, 汤步伟, 苗敬芝, 等.海藻酸钠固定灵芝细胞对胞外三萜类产量的影响[J].食品科学, 2012, 33(05):234-237 [58] 赵小瑞.灵归菌质双向发酵过程中抗氧化活性及抑菌活性动态变化的研究[D]. 甘肃农业大学, 2016. [59]张庆明, 徐云燕, 顾宁宁, 等.灵芝菌-玄七通痹胶囊药渣双向发酵工艺的研究[J].东南国防医药, 2016, 18(06):585-590 [60]赵小瑞, 贠建民, 艾对元, 等.种中草药提取物对灵芝液态发酵三萜产物形成的影响[J].食品与发酵工业, 2016, 42(03):97-103 [61]冯杰, 冯娜, 唐庆九, 等.补料方式对灵芝菌丝体液态深层发酵合成灵芝三萜的影响[J].食品科学, 2017, 38(12):57-62 [62]冯杰, 冯娜, 贾薇, 等.氮源对灵芝菌丝体液态深层发酵合成灵芝三萜的影响[J].菌物学报, 2016, 35(06):722-733 [63]冯杰, 冯娜, 唐庆九, 等.氧载体正十二烷对灵芝三萜液态深层发酵的影响[J].食用菌学报, 2016, 23(02):52-58 [64] Zhang J, Gao H X, Li L.Effect of Antibiotics on the Exo-Polysaccharides and Triterpenoids Biosynthesis by the Submerged Culture of Ganoderma lucidum[J].Advanced Materials Research, 2013, 781-784:1298-1301 [65]Oludemi T, Barros L, Prieto M A, et al.Extraction of triterpenoids and phenolic compounds from Ganoderma lucidum: optimization study using the Response Surface Methodology[J].Food & Function, 2017, 9(1):209-226 [66]周晓, 王成忠, 李双, 等.响应面法优化超声辅助提取灵芝三萜的工艺研究[J].食品工业, 2015, 36(06):136-140 [67]卢彦芳, 安静, 蒋晔.微波连续抽提用于灵芝三萜类成分的分析[J].中国中药杂志, 2015, 40(07):1296-1299 [68]Elumba Z S, Teves F G, Malaluan R M.DNA-binding activity and in vivo cytotoxicity of Ganoderma applanatum (Pers) Pat. supercritical-CO 2 extracts[J].African Journal of Microbiology Research, 2013, 7(7（3）):202-210 [69]贾红岩, 王亚涛, 张芝华, 等.高效液相色谱法测定不同产地及品种灵芝三萜类成分的含量[J].微生物学通报, 2017, 44(01):238-244 [70] Liu W, Zhang J, Han W, et al.One single standard substance for the simultaneous determination of 17 triterpenes in Ganoderma lingzhi and its related species using high-performance liquid chromatography[J].J Chromatogr B Analyt Technol Biomed Life Sci, 2017, 1068-1069:49-55 [71]于华峥, 刘艳芳, 周帅, 等.灵芝子实体、菌丝体和孢子粉化学成分的比较[J].食品与生物技术学报, 2016, 35(08):823-827 [72]Chen Y, Xie M, Zhang H, et al.Quantification of total polysaccharides and triterpenoids in Ganoderma lucidum and Ganoderma atrum by near infrared spectroscopy and chemometrics[J].Food Chemistry, 2012, 135(1):268-275 [73] Sakamoto S, Kikkawa N, Kohno T, et al.Immunochromatographic strip assay for detection of bioactive Ganoderma triterpenoid, ganoderic acid A in Ganoderma lingzhi[J].Fitoterapia, 2016, 114:51-55 [74]李广富, 陈伟, 范路平, 等.灵芝功能成分酸奶营养品质与风味物质分析[J].食品科学, 2015, 36(10):168-173 [75] 吴买生, 罗强华, 左晓红, 等.灵芝和猴头菇菌糠对大沙杂种猪肥育性能和胴体品质的影响[J].养猪, 2016, (03):55-56 [76]黄清铧, 王庆福, 梁磊, 等.甘蔗汁灵芝发酵功能性饮料研制[J].食品与发酵工业, 2015, 41(09):83-86 [77]苗敬芝, 徐栋栋, 董玉玮.灵芝、金针菇混合发酵-芦荟复合保健饮料的研制[J].食品工业, 2014, 35(03):101-104 [78]唐晓双, 葛武鹏, 陈瑛, 等.一种新型灵芝枸杞花色羊乳工艺技术研究[J].食品工业, 2014, 35(02):7-10 [79]林伯勋，陈淑德，陈辉煌.富铬灵芝发酵米谷粉之抗氧化和降血糖研究[J].食品与营养科学, 2014, 02(4):56-62 [80]袁学军, 于群, 周佳洁, 等.不同椰肉椰汁配比和过滤时间对椰奶灵芝酒质量的影响[J].中国食用菌, 2017, 36(05):72-74 [81]金凌云, 黄样增, 周岩飞, 等.灵芝咖啡对小鼠免疫功能影响的研究[J].食品科技, 2017, 43(03):83-87