Abstract
Triterpenoid compounds are important bioactivity materials. Morchella is an abundant medicinal fungi found worldwide. In this study, we optimised the isolation and purification of triterpenoid compounds from Morchella mycelium fermentation. The results showed that the triterpenoid compounds yield was 35.22 mg/g, and we also identified two triterpenoid compounds using high-performance liquid chromatography. In addition, we evaluated the anti-tumour and antioxidant activity of the products, and the results showed that triterpenoid compounds from Morchella mycelium fermentation showed good bioactivity. The IC50 values of four cancer cell lines treated with the triterpenoid compounds for 48 h were 7.20, 14.96, 4.41, and 13.43 mg/mL, respectively. Morphological changes associated with the apoptosis of PC-3 cells were observed using confocal scanning laser microscopy after treatment with triterpenoid compounds for 48 and 72 h. The triterpenoid compounds also exhibited DPPH radical, hydroxyl, and ABTS-free radical scavenging activities in vitro. These results suggest that triterpenoid compounds from Morchella mycelium fermentation, which are found in functional foods and used in the field of pharmacology, might be excellent products for the treatment of cancer and age-related illnesses.
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References
Aboul-Enein HY, Elmastas M, Turkekul I, Ozturk L, Gulcin I, Isildak O (2006) REMOVED: antioxidant activity of two wild edible mushrooms Morchella vulgaris and Morchella esculenta from north Turkey. Fitoterapia. https://doi.org/10.1016/j.fitote.2006.05.005
Ahmadu AA, Tarimaledei P, Onanuga A (2013) Triterpenoids from Gutenbergia nigritana (Benth) Oliv and Hiern. Afr J Tradition Complement Alternative Med AJTCAM 10:405–409
Basnet BB et al (2019) Four new cytotoxic arborinane-type triterpenes from the endolichenic fungus Myrothecium inundatum. Planta Med 85:701–707. https://doi.org/10.1055/a-0855-4051
Chen HP et al (2018) Anti-proliferative and anti-inflammatory lanostane triterpenoids from the Polish edible mushroom Macrolepiota procera. J Agric Food Chem 66:3146–3154. https://doi.org/10.1021/acs.jafc.8b00287
Chen B, Zhang J, Han J, Zhao R, Bao L, Huang Y, Liu H (2019) Lanostane triterpenoids with glucose-uptake-stimulatory activity from peels of the cultivated edible mushroom Wolfiporia cocos. J Agric Food Chem 67:7348–7364. https://doi.org/10.1021/acs.jafc.9b02606
Chuluunbaatar B et al (2019) Triterpenes from the mushroom Hypholoma lateritium: isolation, structure determination and investigation in Bdelloid Rotifer Assays. Molecules. https://doi.org/10.3390/molecules24020301
Elnaggar MS et al (2017) Two new triterpenoids and a new naphthoquinone derivative isolated from a hard coral-derived fungus Scopulariopsis sp. Fitoterapia 116:126–130. https://doi.org/10.1016/j.fitote.2016.12.003
Fabio GD, Romanucci V, De Marco A, Zarrelli A (2014) Triterpenoids from Gymnema sylvestre and their pharmacological activities. Molecules (Basel, Switzerland) 19:10956–10981. https://doi.org/10.3390/molecules190810956
Gogavekar SS, Rokade SA, Ranveer RC, Ghosh JS, Kalyani DC, Sahoo AK (2014) Important nutritional constituents, flavour components, antioxidant and antibacterial properties of Pleurotus sajor-caju. J Food Sci Technol 51:1483–1491. https://doi.org/10.1007/s13197-012-0656-5
Gupta S, Bhatt P, Chaturvedi P (2018) Determination and quantification of asiaticoside in endophytic fungus from Centella asiatica (L.). Urban World J Microbiol Biotechnol 34:111. https://doi.org/10.1007/s11274-018-2493-9
Gursoy N, Sarikurkcu C, Cengiz M, Solak MH (2009) Antioxidant activities, metal contents, total phenolics and flavonoids of seven Morchella species. Food Chem Toxicol Int J Publ Br Ind Biol Res Assoc 47:2381–2388. https://doi.org/10.1016/j.fct.2009.06.032
He J, Sun Y, Jia Y, Geng X, Chen R, Zhou H, Yang B (2019) Ganoderma triterpenes protect against hyperhomocysteinemia induced endothelial-mesenchymal transition via TGF-beta signaling inhibition. Front Physiol 10:192. https://doi.org/10.3389/fphys.2019.00192
Isaka M, Chinthanom P, Thummarukcharoen T, Boonpratuang T, Choowong W (2019) Highly modified lanostane triterpenes from fruiting bodies of the basidiomycete Tomophagus sp. J Nat Prod 82:1165–1176. https://doi.org/10.1021/acs.jnatprod.8b00869
Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61:69–90. https://doi.org/10.3322/caac.20107
Jin J et al (2019) Insights into triterpene acids in fermented mycelia of edible fungus Poria cocos by a comparative study. Molecules. https://doi.org/10.3390/molecules24071331
Kalyoncu F, Oskay M, Saglam H, Erdogan TF, Tamer AU (2010) Antimicrobial and antioxidant activities of mycelia of ten wild mushroom species. J Med Food 13:415–419. https://doi.org/10.1089/jmf.2009.0090
Lee SR et al (2018) Bioactivity-guided isolation and chemical characterization of antiproliferative constituents from morel mushroom (Morchella esculenta) in human lung adenocarcinoma cells. J Funct Foods 40:249–260. https://doi.org/10.1016/j.jff.2017.11.012
Li S, Gao A, Dong S, Chen Y, Sun S, Lei Z, Zhang Z (2017) Purification, antitumor and immunomodulatory activity of polysaccharides from soybean residue fermented with Morchella esculenta. Int J Biol Macromol 96:26–34. https://doi.org/10.1016/j.ijbiomac.2016.12.007
Liang HQ, Zhang DW, Guo SX, Yu J (2018) Two new tetracyclic triterpenoids from the endophytic fungus Hypoxylon sp. J Asian Nat Prod Res 20:951–956. https://doi.org/10.1080/10286020.2018.1485662
Nitha B, De S, Adhikari SK, Devasagayam TP, Janardhanan KK (2010) Evaluation of free radical scavenging activity of morel mushroom, Morchella esculenta mycelia: a potential source of therapeutically useful antioxidants. Pharm Biol 48:453–460. https://doi.org/10.3109/13880200903170789
Nitha B, Fijesh PV, Janardhanan KK (2013) Hepatoprotective activity of cultured mycelium of Morel mushroom Morchella esculenta. Exp Toxicol Pathol 65:105–112. https://doi.org/10.1016/j.etp.2011.06.007
Park KM, Kwon KM, Lee SH (2015) Evaluation of the antioxidant activities and tyrosinase inhibitory property from mycelium culture extracts. Evid Based Complement Alternat Med 2015:616298. https://doi.org/10.1155/2015/616298
Peng XR et al (2019) C30 and C31 triterpenoids and triterpene sugar esters with cytotoxic activities from edible mushroom Fomitopsis pinicola (Sw. Ex Fr.). Krast J Agric Food Chem 67:10330–10341. https://doi.org/10.1021/acs.jafc.9b04530
Ravanan P, Singh SK, Rao GS, Kondaiah P (2011) Growth inhibitory, apoptotic and anti-inflammatory activities displayed by a novel modified triterpenoid, cyano enone of methyl boswellates. J Biosci 36:297–307
Siegel RL, Miller KD, Jemal A (2017) Cancer statistics, 2017. CA Cancer J Clin 67:7–30. https://doi.org/10.3322/caac.21387
Su CA et al (2013) Isolation and characterization of exopolysaccharide with immunomodulatory activity from fermentation broth of Morchella conica. DARU J Faculty Pharm Tehran Univ Med Sci 21:5. https://doi.org/10.1186/2008-2231-21-5
Tan YS, Baskaran A, Nallathamby N, Chua KH, Kuppusamy UR, Sabaratnam V (2015) Influence of customized cooking methods on the phenolic contents and antioxidant activities of selected species of oyster mushrooms (Pleurotus spp.). J Food Sci Technol 52:3058–3064. https://doi.org/10.1007/s13197-014-1332-8
Tang Y, Zhao ZZ, Yao JN, Feng T, Li ZH, Chen HP, Liu JK (2018) Irpeksins A-E, 1,10-seco-eburicane-type triterpenoids from the medicinal fungus irpex lacteus and their anti-NO activity. J Nat Prod 81:2163–2168. https://doi.org/10.1021/acs.jnatprod.7b00845
Ullah A et al (2019) Antibacterial and antibiofilm properties of traditional medicinal plant from Sheikh Buddin range. Pak J Pharm Sci 32:1313–1319
Vieira V et al (2016) Wild Morchella conica Pers from different origins: a comparative study of nutritional and bioactive properties. J Sci Food Agric 96:90–98. https://doi.org/10.1002/jsfa.7063
Wang M, Zhao Q, Zhao YC, Chen LJ, Zhong GY, Zhou DQ (2015) Biological study on cultivation of Morchella species. In: 2015 4th international conference on energy and environmental protection (ICEEP 2015), pp 1046–1051
Xin H et al (2018) Identification and quantification of triterpenoids in lingzhi or reishi medicinal mushroom, Ganoderma lucidum (Agaricomycetes), with HPLC-MS/MS. Methods Int J Med Mushrooms 20:919–934. https://doi.org/10.1615/IntJMedMushrooms.2018027398
Yang Y et al (2019) Acetylation of polysaccharide from Morchella angusticeps peck enhances its immune activation and anti-inflammatory activities in macrophage RAW2647cells. Food Chem Toxicol 125:38–45. https://doi.org/10.1016/j.fct.2018.12.036
Zhao ZZ et al (2015) Two new triterpenoids from fruiting bodies of fungus Ganoderma lucidum. J Asian Nat Prod Res 17:750–755. https://doi.org/10.1080/10286020.2014.996139
Zolj S, Smith MP, Goines JC, Ali TS, Huff MO, Robinson DL, Lau JM (2018) Antiproliferative effects of a triterpene-enriched extract from lingzhi or reishi medicinal mushroom, Ganoderma lucidum (Agaricomycetes), on human lung cancer cells. Int J Med Mushrooms 20:1173–1183. https://doi.org/10.1615/IntJMedMushrooms.2018028823
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We thank LetPub (https://www.letpub.com) for its linguistic assistance during the preparation of this manuscript.
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This work was supported by the National Key Research and Development Program of China (Grant No. 2018YFC1801200).
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Conceptualization, ZW and YY; hodology, YW; software, YX; formal analysis, ZK; investigation, HW; resources, YY; data curation, YY; writing—original draft preparation, YY; writing—review and editing, ZW; visualization, YY; supervision, YY. All authors have read and agreed to the published version of the manuscript.
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Wang, Z., Wang, H., Kang, Z. et al. Antioxidant and anti-tumour activity of triterpenoid compounds isolated from Morchella mycelium. Arch Microbiol 202, 1677–1685 (2020). https://doi.org/10.1007/s00203-020-01876-1
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DOI: https://doi.org/10.1007/s00203-020-01876-1