Mycobiology

  • 제51권4호
  • /
  • Pages.246-255
  • /
  • 2023
  • /
  • 1229-8093(pISSN)
  • /
  • 2092-9323(eISSN)
한국균학회 (The Korean Society of Mycology)
권호 표지
DOI QR코드

DOI QR Code

Steroid Components of Marine-Derived Fungal Strain Penicillium levitum N33.2 and Their Biological Activities

  • Chi K. Hoang (Institute of Natural Products Chemistry, Vietnam Academy of Science and Technology) ;
  • Cuong H. Le (Institute of Natural Products Chemistry, Vietnam Academy of Science and Technology) ;
  • Dat T. Nguyen (Center for Research and Technology Transfer, Vietnam Academy of Science and Technology) ;
  • Hang T. N. Tran (Institute of Natural Products Chemistry, Vietnam Academy of Science and Technology) ;
  • Chinh V. Luu (Institute of Natural Products Chemistry, Vietnam Academy of Science and Technology) ;
  • Huong M. Le (Institute of Natural Products Chemistry, Vietnam Academy of Science and Technology) ;
  • Ha T. H. Tran (Institute of Natural Products Chemistry, Vietnam Academy of Science and Technology)
  • 투고 : 2023.03.22
  • 심사 : 2023.08.11
  • 발행 : 2023.08.31
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Genus Penicillium comprising the most important and extensively studied fungi has been well-known as a rich source of secondary metabolites. Our study aimed to analyze and investigate biological activities, including in vitro anti-cancer, anti-inflammatory and anti-diabetic properties, of metabolites from a marine-derived fungus belonging to P. levitum. The chemical compounds in the culture broth of P. levitum strain N33.2 were extracted with ethyl acetate. Followingly, chemical analysis of the extract leaded to the isolation of three ergostane-type steroid components, namely cerevisterol (1), ergosterol peroxide (2), and (3β,5α,22E)-ergosta-6,8(14),22-triene-3,5-diol (3). Among these, (3) was the most potent cytotoxic against human cancer cell lines Hep-G2, A549 and MCF-7 with IC50 values of 2.89, 18.51, and 16.47 ㎍/mL, respectively, while the compound (1) showed no significant effect against tested cancer cells. Anti-inflammatory properties of purified compounds were evaluated based on NO-production in LPS-induced murine RAW264.7 macrophages. As a result, tested compounds performed diverse inhibitory effects on NO production by the macrophages, with the most significant inhibition rate of 81.37±1.35% at 25 ㎍/mL by the compound (2). Interestingly, compounds (2) and (3) exhibited inhibitory activities against pancreatic lipase and α-glucosidase enzymes in vitro assays. Our study brought out new data concerning the chemical properties and biological activities of isolated steroids from a P. levitum fungus.

키워드

과제정보

This work was supported by the Vietnam Academy of Science and Technology under grants VAST 02.04/21-22 and DLTE 00.10/22-23.

참고문헌

  1. Strobel G, Daisy B, Castillo U, et al. Natural products from endophytic microorganisms. J Nat Prod. 2004;67(2):257-268. doi: 10.1021/np030397v.
  2. Trivedi P, Leach JE, Tringe SG, et al. Plant-microbiome interactions: from community assembly to plant health. Nat Rev Microbiol. 2020;18(11):607-621. doi: 10.1038/s41579-020-0412-1.
  3. Stierle A, Strobel G, Stierle D. Taxol and taxane production by Taxomyces andreanae, an endophytic fungus of Pacific yew. Science. 1993;260(5105):214-216. doi: 10.1126/science.8097061.
  4. Pu X, Qu X, Chen F, et al. Camptothecin-producing endophytic fungus Trichoderma atroviride LY357: isolation, identification, and fermentation conditions optimization for camptothecin production. Appl Microbiol Biotechnol. 2013;97(21):9365-9375. doi: 10.1007/s00253-013-5163-8.
  5. Zhang ZB, Zeng QG, Yan RM, et al. Endophytic fungus Cladosporium cladosporioides LF70 from Huperzia serrata produces Huperzine A. World J Microbiol Biotechnol. 2011;27(3):479-486. doi: 10.1007/s11274-010-0476-6.
  6. Dissanayake RK, Ratnaweera PB, Williams DE, et al. Antimicrobial activities of endophytic fungi of the Sri Lankan aquatic plant Nymphaea nouchali and chaetoglobosin a and C, produced by the endophytic fungus Chaetomium globosum. Mycology. 2016;7(1):1-8. doi: 10.1080/21501203.2015.1136708.
  7. Supaphon P, Phongpaichit S, Rukachaisirikul V, et al. Antimicrobial potential of endophytic fungi derived from three seagrass species: Cymodocea serrulata, Halophila ovalis and Thalassia hemprichii. PLOS One. 2013;8(8):e72520. doi: 10.1371/journal.pone.0072520.
  8. Zheng H, Yu Z, Jiang X, et al. Endophytic Colletotrichum species from aquatic plants in southwest China. JoF. 2022;8(1):87. doi: 10.3390/jof8010087.
  9. Larkum AW, Orth RJ, Duarte CM. Seagrasses: biology, ecology and conservation. Phycologia. 2006;45(5):5.
  10. Arunpanichlert J, Rukachaisirikul V, Tadpetch K, et al. A dimeric chromanone and a phthalide: metabolites from the seagrass-derived fungus Bipolaris sp. PSU-ES64. Phytochem Lett. 2012;5(3):604-608. doi: 10.1016/j.phytol.2012.06.004.
  11. Arunpanichlert J, Rukachaisirikul V, Phongpaichit S, et al. Meroterpenoid, isocoumarin, and phenol derivatives from the seagrass-derived fungus Pestalotiopsis sp. PSU-ES194. Tetrahedron. 2015;71(5):882-888. doi: 10.1016/j.tet.2014.12.009.
  12. Houbraken J, Kocsub e S, Visagie CM, et al. Classification of Aspergillus, Penicillium, Talaromyces and related genera (Eurotiales): an overview of families, genera, subgenera, sections, series and species. Stud Mycol. 2020;95:5-169. doi: 10.1016/j.simyco.2020.05.002.
  13. Fleming A. On the antibacterial action of cultures of a Penicillium, with special reference to their use in the isolation of B. influenzae. Br J Exp Pathol. 1929;10(3):226.
  14. Toghueo RMK, Boyom FF. Endophytic Penicillium species and their agricultural, biotechnological, and pharmaceutical applications. 3 Biotech. 2020;10(3):107. doi: 10.1007/s13205-020-2081-1.
  15. Liu S, Su M, Song SJ, et al. Marine-derived Penicillium species as producers of cytotoxic metabolites. Mar Drugs. 2017;15(10):329. doi: 10.3390/md15100329.
  16. Zhabinskii VN, Drasar P, Khripach VA. Structure and biological activity of ergostane-type steroids from fungi. Molecules. 2022;27(7):2103. doi: 10.3390/molecules27072103.
  17. White TJ, Bruns T, Lee S, et al. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR protocols: a guide to methods and applications. New York (NY): Academic Press; 1990. p. 315-322.
  18. Gardes M, Bruns TD. ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol. 1993;2(2):113-118. doi: 10.1111/j.1365-294x.1993.tb00005.x.
  19. Visagie CM, Houbraken J, Frisvad JC, et al. Identification and nomenclature of the genus Penicillium. Stud Mycol. 2014;78(1):343-371. doi: 10.1016/j.simyco.2014.09.001.
  20. Berridge MV, Herst PM, Tan AS. Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction. Biotechnol Annu Rev. 2005;11:127-152. https://doi.org/10.1016/S1387-2656(05)11004-7
  21. Green LC, Wagner DA, Glogowski J, et al. Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Anal Biochem. 1982;126(1):131-138. doi: 10.1016/0003-2697(82)90118-x.
  22. Lewis DR, Liu DJ. Direct measurement of lipase inhibition by orlistat using a dissolution linked in vitro assay. Clin Pharmacol Biopharm. 2012;1:1000103.
  23. Matsui T, Yoshimoto C, Osajima K, et al. In vitro survey of α-glucosidase inhibitory food components. Biosci Biotechnol Biochem. 1996;60(12):2019-2022. doi: 10.1271/bbb.60.2019.
  24. Pitt JI. An appraisal of identification methods for Penicillium species: novel taxonomic criteria based on temperature and water relations. Mycologia. 1973;65(5):1135-1157. doi: 10.1080/00275514.1973.12019533.
  25. Palama TL, Khatib A, Choi YH, et al. Metabolic changes in different developmental stages of Vanilla planifolia pods. J Agric Food Chem. 2009;57(17):7651-7658. doi: 10.1021/jf901508f.
  26. Yoneyama T, Takahashi H, Grudniewska A, et al. Ergostane-type sterols from several Cordyceps strains. Nat Prod Commun. 2022;17(6):1934578X 2211053. doi: 10.1177/1934578X221105363.
  27. Wang H, Liu T, Xin Z. A new glucitol from an endophytic fungus Fusarium equiseti salicorn 8. Eur Food Res Technol. 2014;239(3):365-376. doi: 10.1007/s00217-014-2230-z.
  28. Merdivan S, Lindequist U. Ergosterol peroxide: a mushroom-derived compound with promising biological activities - a review. Int J Med Mushrooms. 2017;19(2):93-105. doi: 10.1615/IntJMedMushrooms.v19.i2.10.
  29. Sharma JN, Al-Omran A, Parvathy SS. Role of nitric oxide in inflammatory diseases. Inflammopharmacology. 2007;15(6):252-259. doi: 10.1007/s10787-007-0013-x.
  30. Alam MB, Chowdhury NS, Sohrab MH, et al. Cerevisterol alleviates inflammation via suppression of MAPK/NF-㮡B/AP-1 and activation of the Nrf2/HO-1 signaling cascade. Biomolecules. 2020;10(2):199. doi: 10.3390/biom10020199.
  31. Li W, Zhou W, Cha JY, et al. Sterols from Hericium erinaceum and their inhibition of TNF-α and NO production in lipopolysaccharide-induced RAW 264.7 cells. Phytochem. 2015;115:231-238. doi: 10.1016/j.phytochem.2015.02.021.
  32. Mukherjee M. Human digestive and metabolic lipases-a brief review. J Mol Catal B Enzym. 2003;22(5-6):369-376. doi: 10.1016/S1381-1177(03)00052-3.
  33. Nowak R, Nowacka-Jechalke N, Pietrzak W, et al. A new look at edible and medicinal mushrooms as a source of ergosterol and ergosterol peroxideUHPLC-MS/MS analysis. Food Chem. 2022;369:130927. doi: 10.1016/j.foodchem.2021.130927.
  34. Shan WG, Wu ZY, Pang WW, et al. a-Glucosidase inhibitors from the fungus Aspergillus terreus 3.05358. Chem Biodivers. 2015;12(11):1718-1724. doi: 10.1002/cbdv.201500027.
  35. Su CH, Lu TM, Lai MN, et al. Inhibitory potential of Grifola frondosa bioactive fractions on α-amylase and α-glucosidase for management of hyperglycemia. Biotechnol Appl Biochem. 2013;60(4):446-452. doi: 10.1002/bab.1105.
  36. Gonc,alves MF, Santos L, Silva BM, et al. Biodiversity of Penicillium species from marine environments in Portugal and description of Penicillium lusitanum sp. nov., a novel species isolated from sea water. Int J Syst Evol Microbiol. 2019;69(10):3014-3021. doi: 10.1099/ijsem.0.003535.
  37. Ugarelli K, Chakrabarti S, Laas P, et al. The seagrass holobiont and its microbiome. Microorganisms. 2017;5(4):81. doi: 10.3390/microorganisms5040081.
  38. Cantrell SA, Casillas-Mart inez L, Molina M. Characterization of fungi from hypersaline environments of solar salterns using morphological and molecular techniques. Mycol Res. 2006;110(8):962-970. doi: 10.1016/j.mycres.2006.06.005.
  39. Trigos A, Ortega-Regules A. Selective destruction of microscopic fungi through photo- oxidation of ergosterol. Mycologia. 2002;94(4):563-568. doi: 10.1080/15572536.2003.11833184.
  40. Krzyczkowski W, Malinowska E, Suchocki P, et al. Isolation and quantitative determination of ergosterol peroxide in various edible mushroom species. Food Chem. 2009;113(1):351-355. doi: 10.1016/j.foodchem.2008.06.075.
  41. Gao JM, Wang M, Liu LP, et al. Ergosterol peroxides as phospholipase A2 inhibitors from the fungus Lactarius hatsudake. Phytomedicine. 2007;14(12):821-824. doi: 10.1016/j.phymed.2006.12.006.
  42. Koolen HHF, Soares ER, Silva FMA, et al. Chemical constituents of Penicillium chrysogenum, an endophytic fungus from Strychnos toxifera. Chem Nat Compd. 2014;49(6):1164-1165. doi: 10.1007/s10600-014-0851-x.
  43. Nes WD, Heupel RC, Le PH. Biosynthesis of ergosta-6(7),8(14),22(23)-trien-3β-ol by Gibberella fujikuroi: its importance to ergosterol's metabolic pathway. J Chem Soc Chem Commun. 1985;20(20):1431-1433. doi: 10.1039/C39850001431.