Evaluation of active components and pharmacological activities by UPLC-Q/TOF-MS and network pharmacology in Lentinula edodes and Lyophyllum decastes
Main Article Content
Keywords
edible fungi, active components, pharmacological activities, UPLC-Q/TOF-MS, network pharmacology
Abstract
Lentinula edodes (L. edodes) is a premium edible fungus cultivated extensively throughout China, and Lyophyllum decastes (L. decastes) is a wild edible fungus with a high degree of industrial-level cultivation in China. Regarding the edible value of the two fungi, research on their medicinal properties is relatively scarce. In this study, we utilized ultra-high performance liquid chromatography with quadrupole and time-of-flight mass spectrometry to analyze comprehensively the chemical composition of both fungi. In all, 120 and 144 chemical components were identified in L. edodes and L. decastes, respectively. Subsequently, we elaborated active components, potential biological activities, and therapeutic targets associated with both fungi by using network pharmacology. The results showed that seven active components in L. edodes and nine active components in L. decastes could act on common targets, such as AKT serine/threonine kinase1 and peroxisome proliferator-activated receptor gamma, thereby regulating signaling pathways, such as epidermal growth factor receptor and mitogen-activated protein kinase, to affect the body. In addition, these components affect immune regulation and inhibition of liver cancer. Finally, we used cell experiments to verify their activities. Our findings provided a reliable foundation for future research aimed at harnessing the bioactivities of L. edodes and L. decastes, thereby offering novel strategies for their utilization in the field of functional foods and natural medicine.
References
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Cui, L., Liu, Y., Liu, M., et al., 2022. Identification of phytochemicals from Lentinus edodes and Auricularia auricula with UPLC-Q-Exactive Orbitrap MS. Journal of Future Foods 2(3): 253–260. 10.1016/j.jfutfo.2022.06.006
Dai, J.N., Liu, B.L., Ji, D., et al., 2023a. Extraction, isolation, identification, and bioactivity of polysaccharides from Antrodia cinnamomea. Quality Assurance and Safety of Crops–Foods 15(4): 60–76. 10.15586/qas.v15i4.1341
Dai, Y., Wang, L., Chen, X.Y., et al., 2023b. Lentinula edodessing polysaccharide: extraction, characterization, bioactivities, and emulsifying applications. Foods 12(17): 17. 10.3390/foods12173289
Ding, X., Liu, Y., and Hou, Y. L., 2022. Structure identification and biological activities of a new polysaccharide isolated from Lyophyllum decastes (Fr.) Sing. Pharmacognosy Magazine 18(77): 112–120. 10.4103/pm.pm_185_21
Du, Y.H., Zhao, J.J., Li, X., et al., 2024. Mechanism of pachymic acid in the treatment of gastric cancer based on network pharmacology and experimental verification. World Journal of Gastrointestinal Oncology 16(1): 22. 10.4251/wjgo.v16.i1.30
Fang, X.D., Chen, Y.X., Chen, Y., et al., 2024. Identification and characterization of two immune-related subtypes in human chronic kidney disease. Transplant Immunology 82: 10. 10.1016/j.trim.2023.101983
Fujita, R., Yokono, M., Ube, N., et al., 2021. Suppression of alternaria brassicicola infection by volatile compounds from spent mushroom substrates. Journal of Bioscience and Bioengineering 132(1): 25–32. 10.1016/j.jbiosc.2021.03.003
Gameli-Kwabla, K., 2020. Examining the nutritional composition, value and health benefit of mushrooms. International Journal of Reseach and Scholarly Communication 3(1): 17.
Garcia, J., Rodrigues, F., Saavedra, M.J., et al., 2022. Bioactive polysaccharides from medicinal mushrooms: a review on their isolation, structural characteristics and antitumor activity. Food Bioscience 49: 11. 10.1016/j.fbio.2022.101955
Guerau-Arellano, M., Piedra-Quintero, Z.L.L., and Tsichlis, P.N., 2022. Akt isoforms in the immune system. Frontiers in Immunology 13: 990874. 10.3389/fimmu.2022.990874
Halder, S., Basu, S., Lall, S.P., et al., 2023. Targeting the EGFR signaling pathway in cancer therapy: what’s new in 2023? Expert Opinion on Therapeutic Targets 27(4–5): 305–324. 10.1080/14728222.2023.2218613
Hye-Lim, J., Park, S.-Y., and Nam, J., 2017. Effect of extraction solvent on the antioxidant activity of Lentinula edodes GNA01 extract. Korean Journal of Food and Nutrition 30(1): 51–58. 10.9799/ksfan.2017.30.1.051
Ike, K., Kameyama, N., Ito, A., et al., 2012. Induction of a T-Helper 1 (Th1) immune response in mice by an extract from the pleurotus eryngii (Eringi) mushroom. Journal of Medicinal Food 15(12): 1124–1128. 10.1089/jmf.2012.2239
Katoch, S., Sharma, V., and Patial, V., 2022. Peroxisome proliferator-activated receptor gamma as a therapeutic target for hepatocellular carcinoma: experimental and clinical scenarios. World Journal of Gastroenterology 28(28): 21. 10.3748/wjg.v28.i28.3535
Kim, M., and Ryu, S.E., 2018. Specific binding and catalytic activation of the MAPK-MKP complex. Biodesign 6(4): 79–83.
Lee, J.E., Woo, M.G., Jung, K.H., et al., 2022. Combination therapy of the active KRAS-targeting antibody inRas37 and a PI3K inhibitor in pancreatic cancer. Biomolecules and Therapeutics 30(3): 274–283. 10.4062/biomolther.2021.145
Li, H.Y., Guo, L., Ding, X.Y., et al., 2022. Molecular networking, network pharmacology, and molecular docking approaches employed to investigate the changes in ephedrae herba before and after honey-processing. Molecules 27(13): 18. 10.3390/molecules27134057
Li, Y.H., Liu, X.H., Zhang, X., et al., 2021. Immune cycle-based strategies for cancer immunotherapy. Advanced Functional Materials 31(50): 27. 10.1002/adfm.202107540
Liang, Z., Li, C., Wang, J., et al., 2021. Immunomodulatory effects of polysaccharides from edible fungus: a review. Food Science and Human Wellness 10(4): 393–400. 10.1016/j.fshw.2021.04.001
Lin, M., 2012. Fungi medicine in Chinese materia medica. Chinese Traditional and Herbal Drugs.
Lu, X.S., Hou, H., Fang, D.L., et al., 2022. Identification and characterization of volatile compounds in Lentinula edodes during vacuum freeze-drying. Journal of Food Biochemistry 46(6): 13. 10.1111/jfbc.13814
Sharma, A., Bhardwaj, G., Nayik, G.A. 2023. Phytochemistry and nutritional composition of significant wild medicinal and edible mushrooms. eBook collection. Royal Society of Chemistry, London. 10.1039/9781837672097
Qiu, M.Y., Zhang, J.Q., Wei, W.L., et al., 2024. Integrated UPLC/Q-TOF-MS/MS analysis and network pharmacology to reveal the neuroprotective mechanisms and potential pharmacological ingredients of aurantii fructus immaturus and aurantii fructus. Pharmaceuticals 17(2): 14. 10.3390/ph17020239
Roszczyk, A., Turlo, J., Zagozdzon, R., et al., 2022. Immunomodulatory properties of polysaccharides from Lentinula edodes. International Journal of Molecular Sciences 23(16): 13. 10.3390/ijms23168980
Rudko, O.I., Tretiakov, A.V., Naumova, E.A., et al., 2020. Role of PPARs in progression of anxiety: literature analysis and signaling pathways reconstruction. PPAR Research 2020: 8859017. 10.1155/2020/8859017
Selenz, C., Compes, A., Nill, M., et al., 2022. EGFR inhibition strongly modulates the tumour immune microenvironment in EGFR-Driven non-Small-Cell lung cancer. Cancers 14(16): 15. 10.3390/cancers14163943
Sganzerla, W.G., Todorov, S.D., and da Silva, A.P.G., 2022. Research trends in the study of edible mushroom: nutritional properties and health benefits. International Journal of Medicinal Mushrooms 24(5): 1–18.
Shi, K.Y., Wang, G., Pei, J.P., et al., 2022. Emerging strategies to overcome resistance to third-generation EGFR inhibitors. Journal of Hematology and Oncology 15(1): 44. 10.1186/s13045-022-01311-6
Shin, J.H., and Park, H.-B., 2016. Enhanced anti-tumor reactivity of cytotoxic T lymphocytes expressing PD-1 decoy. Immune Network 16(2): 134–139. 10.4110/in.2016.16.2.134
Stark, J.M., Coquet, J.M., and Tibbitt, C.A., 2021. The role of PPAR-γ in allergic disease. Current Allergy and Asthma Reports 21(11): 8. 10.1007/s11882-021-01022-x
Starzer, A.M., Preusser, M., and Berghoff, A.S., 2022. Immune escape mechanisms and therapeutic approaches in cancer: the cancer-immunity cycle. Therapeutic Advances in Medical Oncology 14: 14. 10.1177/17588359221096219
Sukjamnong, S., Chen, H., Saad, S., et al., 2022. Fimbristylisovata and artemisia vulgaris extracts inhibited AGE-mediated RAGE expression, ROS generation, and inflammation in THP-1 cells. Toxicological Research 38(3): 331–343. 10.1007/s43188-021-00114-0
Vilela, B., Pagès, M., and Lumbreras, V., 2010. Regulation of MAPK signaling and cell death by MAPK phosphatase MKP2. Plant Signaling and Behavior 5(11): 1497–1500. 10.4161/psb.5.11.13645
Wang, Y.H., Yang, Z.Y., Chen, X., et al., 2021. Lenthionine, a key flavor substance in Lentinula edodes, is regulated by cysteine under drought stress. Journal of Agricultural and Food Chemistry, 69(43): 12645–12653. 10.1021/acs.jafc.1c04829
Wei, A.A.J., Iacobucci, C., Schultze, W., et al., 2022. Different oligomeric states of the tumor suppressor p53 show identical binding behavior towards the S100β homodimer. Chembiochem 23(11): 6. 10.1002/cbic.202100665
Wen, S.D., Mo, S., Zhou, J., et al., 2024. Single-cell and spatial-omics in delineating immune-related diseases. Frontiers in Cell and Developmental Biology 12: 3. 10.3389/fcell.2024.1365242
Xie, Y.M., Shi, L.S., He, X.S., et al., 2021. Gastrointestinal cancers in China, the USA, and Europe. Gastroenterology Report 9(2): 91–104. 10.1093/gastro/goab010
Xu, L.L., Yang, W.J., Qiu, T.M., et al., 2023. Complete genome sequences and comparative secretomic analysis for the industrially cultivated edible mushroom Lyophyllum decastes reveals insights on evolution and lignocellulose degradation potential. Frontiers in Microbiology 14: 14. 10.3389/fmicb.2023.1137162
Xu, X.M., Yu, D.H., Wang, Y., et al., 2024. Integrating network pharmacology and renal metabonomics to reveal the protective mechanism of resveratrol on gouty nephropathy. Biomedical Chromatography 38(5): e5839. 10.1002/bmc.5839
Xu, X.Q., Zhang, X.Y., Zhang, Y., et al., 2021. Curcumin suppresses the malignancy of non-small cell lung cancer by modulating the circ-PRKCA/miR-384/ITGB1 pathway. Biomedicine & Pharmacotherapy 138: 111439. 10.1016/j.biopha.2021.111439
Yang, M., Liu, H., Qiu, G.P., et al., 2022. Silencing Akt1 enhances the resistance of prostate cancer cells to starvation and inhibits starvation-induced lung metastasis through epithelial-mesenchymal transition in prostate cancer. Medical Oncology 39(1): 12. 10.1007/s12032-021-01600-z
Yin, Z., Sun-Waterhouse, D., Wang, J., et al., 2022. Polysaccharides from edible fungi Pleurotus spp.: advances and perspectives. Journal of Future Foods 1(2): 128–140. 10.1016/j.jfutfo.2022.01.002
Zhang, P., He, S., Wu, S., et al., 2022. Discovering a multi-component combination against vascular dementia from danshen-honghua herbal pair by spectrum-effect relationship analysis. Pharmaceuticals (Basel) 15(9): 1073. https://www.mdpi.com/1424-8247/15/9/1073
Zhang, G.P., Wang, Y.N., Qin, C.Q., et al., 2023. Structural characterization of an antioxidant polysaccharide isolated from the fruiting bodies of Lyophyllum decastes. Journal of Molecular Structure 1285: 8. 10.1016/j.molstruc.2023.135507
Zhang, T.T., Hu, W., Chen, W., et al., 2021. Plasma membrane integrates biophysical and biochemical regulation to trigger immune receptor functions. Frontiers in Immunology 12: 8. 10.3389/fimmu.2021.613185
Zhou, Y., Chu, M.H., Ahmadi, F., et al., 2023. A comprehensive review on phytochemical profiling in mushrooms: occurrence, biological activities, applications and future prospective. Food Reviews International 40(3): 924–951. 10.1080/87559129.2023.2202738
Zhu, B.J., Nai, G.Y., Pan, T.X., et al., 2023. Combining network pharmacology and bioinformatics to identify bioactive compounds and potential mechanisms of action of Sedum aizoon L in the treatment of atherosclerosis. Quality Assurance and Safety of Crops & Foods 15(3): 104–116. 10.15586/qas.v15i3.1333
Zou, H., Zhou, C., Li, Y., et al., 2020. Speciation analysis of arsenic in edible mushrooms by high-performance liquid chromatography hyphenated to inductively coupled plasma mass spectrometry. Food Chemistry 327: 127033. 10.1016/j.foodchem.2020.127033
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Dec 21, 2024
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