Journal of Microbiology and Biotechnology

  • 제33권6호
  • /
  • Pages.806-822
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  • 2023
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  • 1017-7825(pISSN)
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  • 1738-8872(eISSN)
한국미생물·생명공학회 (The Korean Society for Microbiology and Biotechnology)
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Multi-Function of a New Bioactive Secondary Metabolite Derived from Endophytic Fungus Colletotrichum acutatum of Angelica sinensis

  • Ramy S. Yehia (Department of Biological Sciences, College of Science, King Faisal University)
  • 투고 : 2022.06.09
  • 심사 : 2022.12.15
  • 발행 : 2023.06.28
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초록

In the current study we assessed a new crystallized compound, 5-(1-hydroxybutyl)-4-methoxy-3-methyl-2H-pyran-2-one (C-HMMP), from the endophytic fungus Colletotrichum acutatum residing in the medicinal plant Angelica sinensis for its in vitro antimicrobial, antibiofilm, antioxidant, antimalarial, and anti-proliferative properties. The promising compound was identified as C-HMMP through antimicrobial-guided fraction. The structure of C-HMMP was unambiguously confirmed by 2D NMR and HIRS spectroscopic analysis. Antimicrobial property testing of C-HMMP showed it to be effective against a variety of pathogenic bacteria and fungi with MICs ranging from 3.9 to 31.25 ㎍/ml. The compound displayed excellent antibiofilm activity against C. albicans, S. aureus, and K. pneumonia. Furthermore, the antimalarial and radical scavenging activities of C-HMMP were clearly dosedependent, with IC50 values of 0.15 and 131.2 ㎍/ml. The anti-proliferative activity of C-HMMP against the HepG-2, HeLa, and MCF-7 cell lines in vitro was investigated by MTT assay, revealing notable anti-proliferative activity with IC50 values of 114.1, 90, and 133.6 ㎍/ml, respectively. Moreover, CHMMP successfully targets topoisomerase I and demonstrated beneficial anti-mutagenicity in the Ames test against the reactive carcinogenic mutagen, 2-aminofluorene (2-AF). Finally, the compound inhibited the activity of α-glucosidase and α-amylase with IC50 values of 144.7 and 118.6 ㎍/ml, respectively. To the best of our knowledge, the identified compound C-HMMP was obtained for the first time from C. acutatum of A. sinensis, and this study demonstrated that C-HMMP has relevant biological significance and could provide better therapeutic targets against disease.

키워드

과제정보

This work was supported by the Deanship of Scientific Research, Vice Presidency for Graduate Studies and Scientific Research, King Faisal University, Saudi Arabia [Project No. GRANT2217].

참고문헌

  1. 1. Koehn FE, Carter GT. 2005. The evolving role of natural products in drug discovery. Nat. Rev. Drug Discov. 4: 206-220. https://doi.org/10.1038/nrd1657
  2. Clardy J, Walsh C. 2004. Lessons from natural molecules. Nature 432: 829-837. https://doi.org/10.1038/nature03194
  3. Schulz B, Boyle C, Draeger S, Rommert AK, Krohn K. 2002. Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol. Res. 106: 996-1004. https://doi.org/10.1017/S0953756202006342
  4. Saikkonen K, Faeth SH, Helander M, Sullivan T. 1998. Fungal endophytes: a continuum of interactions with host plants. Annu. Rev. Ecol. Syst. 29: 319-343. https://doi.org/10.1146/annurev.ecolsys.29.1.319
  5. Aly AH, Debbab A, Kjer J, Proksch P. 2010. Fungal endophytes from higher plants: a prolific source of phytochemicals and other bioactive natural products. Fungal Divers 41: 1-16. https://doi.org/10.1007/s13225-010-0034-4
  6. Kaul S, Gupta S, Ahmed M, Dhar MK. 2012. Endophytic fungi from medicinal plants: a treasure hunt for bioactive metabolites. Phytochem. Rev. 11: 487-505. https://doi.org/10.1007/s11101-012-9260-6
  7. Strobel GA. 2003. Endophytes as sources of bioactive products. Microbes Infect. 5: 535-544. https://doi.org/10.1016/S1286-4579(03)00073-X
  8. Kogel KH, Franken P, Huckelhoven R. 2006. Endophyte or parasite - what decides? Curr. Opin. Plant Biol. 9: 358-363. https://doi.org/10.1016/j.pbi.2006.05.001
  9. Porras-Alfaro A, Bayman P. 2011. Hidden fungi, emergent properties: endophytes and microbiomes. Annu. Rev. Phytopathol. 49: 291-315. https://doi.org/10.1146/annurev-phyto-080508-081831
  10. Chutulo EC, Chalannavar RK. 2018. Endophytic mycoflora and their bioactive compounds from Azadirachta indica: a comprehensive review. J. Fungi 4: 42.
  11. Kharwar RN, Mishra A, Gond SK, Stierle A, Stierle D. 2011. Anticancer compounds derived from fungal endophytes: their importance and future challenges. Nat. Prod. Rep. 28: 1208-1228. https://doi.org/10.1039/c1np00008j
  12. Barnett HL, Hunter BB. 1998. Illustrated Genera of Imperfect Fungi, (No. Ed. 4) American Phytopathological Society (APS Press).
  13. Cooke WB. 1958. The ecology of the fungi. Bot. Rev. 24: 341-429. https://doi.org/10.1007/BF02872436
  14. El-Shafie AK. 1996. Soil fungi in Qatar and other Arab countries. Econ. Bot. 50: 242-242. https://doi.org/10.1007/BF02861455
  15. Suryanarayanan TS, Murali TS, Venkatesan G. 2003. Endophytic fungal communities in leaves of tropical forest trees: diversity and distribution patterns. Curr. Sci. 85: 489-493.
  16. White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In PCR Protocols eds. Innis MA, Gelfand DH, Sninsky JJ, White TJ pp. 315-322. Orlando, Florida: Academic Press.
  17. Vilgalys R, Hester M. 1990. Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J. Bacteriol. 172: 4238-4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990
  18. Carbone I, Kohn LM. 1999. A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91: 553-556. https://doi.org/10.1080/00275514.1999.12061051
  19. Guerber JC, Liu B, Correll JC, Johnston PR. 2003. Characterization of diversity in Colletotrichum acutatum by sequence analysis of two gene introns, mtDNA and intron RFLPs, and mating compatibility. Mycologia 95: 872-895. https://doi.org/10.1080/15572536.2004.11833047
  20. CLSI. 2015. Performance standards for antimicrobial disk susceptibility test; approved standard-Twelfth Edition. Clinical and Laboratory Standards Institute M02- A12. Wayne, PA, USA.
  21. CLSI. 2010. Method for antifungal disk diffusion susceptibility testing of non dermatophyte filamentous fungi; approved guideline. Clinical and Laboratory Standards Institute M51-A 30: 1-29.
  22. CLSI. 2008. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Filamentous Fungi; Approved Standard: CLSI Document M38-A2, 2nd Edn. Wayne, PA: Clinical and Laboratory Standards Institute.
  23. Zhao Y, Du SK, Wang H, Cai M. 2014. In vitro antioxidant activity of extracts from common legumes. Food Chem. 152: 462-466. https://doi.org/10.1016/j.foodchem.2013.12.006
  24. Maron D, Ames BN. 1983. Revised methods for the Salmonella mutagenicity test. Mutat. Res. 113: 173-215. https://doi.org/10.1016/0165-1161(83)90010-9
  25. Budimulya AS, Syafruddin Tapchaisri P, Wilariat P, Marzuki S. 1997. The sensitivity of Plasmodium protein synthesis to prokaryotic ribosomal inhibitors. Mol. Biochem. Parasitol. 84: 137-141 https://doi.org/10.1016/S0166-6851(96)02781-8
  26. Worthington TM. 1982. Enzymes and Related Biochemicals. Biochemical Products Division. Worthington Diagnostic System Inc. Freehold, New Jersey.
  27. Zhang J, Zhao S, Yin P, Yan L, Han J, Shi L, et al. 2014. α- Glucosidase inhibitory activity of polyphenols from the burs of Castanea mollissima blume. Molecules 19: 8373-8386. https://doi.org/10.3390/molecules19068373
  28. Christensen GD, Simpson WA, Bisno AL, Beachey EH. 1982. Adherence of slime-producing strains of Staphylococcus epidermidis to smooth surfaces. Infec. Immun. 37: 318-326. https://doi.org/10.1128/iai.37.1.318-326.1982
  29. Onsare JG, Arora DS. 2015. Antibiofilm potential of flavonoids extracted from Moringa oleifera seed coat against Staphylococcus aureus, Pseudomonas aeruginosa and Candida albicans. J. Appl. Microbiol. 118: 313-325. https://doi.org/10.1111/jam.12701
  30. Arora DS, Mahajan H. 2019. Major phytoconstituents of Prunus cerasoides responsible for antimicrobial and antibiofilm potential against some reference strains of pathogenic bacteria and clinical isolates of MRSA. Appl. Biochem. Biotechnol. 188: 1185-1204. https://doi.org/10.1007/s12010-019-02985-4
  31. 31. Yehia RS, Osman GH, Assaggaf H, Salem R, Mohamed MS. 2020. Isolation of potential antimicrobial metabolites from endophytic fungus Cladosporium cladosporioides from endemic plant Zygophyllum mandavillei. S. Afr. J. Bot. 134: 296-302. https://doi.org/10.1016/j.sajb.2020.02.033
  32. Kaur T. 2020. Fungal endophyte-host plant interactions: role in sustainable agriculture, in Sustainable Crop Production, eds Hassanuzaman M, Filho MCM, Fujita M, Nogueira TAR (London: Intech Open), 1-18.
  33. Shan TJ, Feng H, Xie Y, Shao C, Wang J, Mao ZL. 2019. Endophytic fungi isolated from Eucalyptus citriodora Hook. f. and antibacterial activity of crude extracts. Plant Prot. 45: 149-155.
  34. Miguel PSB, Delvaux JC, Oliveira MNV, Moreira BC, Borges AC, Totola MR, et al. 2017. Diversity and distribution of the endophytic fungal community in eucalyptus leaves. Afr. J. Microbiol. Res. 11: 92-105. https://doi.org/10.5897/AJMR2016.8353
  35. Gouda S, Das G, Sen SK, Shin HS, Patra JK. 2016. Endophytes: a treasure house of bioactive compounds of medicinal importance. Front. Microbiol. 7: 1538.
  36. Shah S, Shrestha R, Maharjan S, Selosse MA, Pant B. 2019. Isolation and characterization of plant growth-promoting endophytic fungi from the roots of Dendrobium moniliforme. Plants 8: 5.
  37. Fisher PJ, Petrini O. 1987. Location of fungal endophytes in tissues of Suaeda fruticosa: a preliminary study. Transact. Brit. Mycol. Soc. 89: 246-249. https://doi.org/10.1016/S0007-1536(87)80161-4
  38. Petrini O, Fisher PJ. 1986. Fungal endophytes in Salicornia perennis. Transact. Brit. Mycol. Soc. 87: 647-561.
  39. Khan R, Shahzad S, Choudhary M, Khan SA, Ahmad A. 2007. Biodiversity of endophytic fungi isolated from Calotropis procera (Ait.) R. Br. Pak. J. Bot. 39: 2233-2239.
  40. Shen XY, Cheng YL, Cai CJ, Fan L, Gao J, Hou CL. 2014. Diversity and antimicrobial activity of culturable endophytic fungi isolated from moso bamboo seeds. PLoS One 9: e95838
  41. Koukol O, Kolarik M, Kolarova Z, Baldrian P. 2012. Diversity of foliar endophytes in wind-fallen Picea abies trees. Fungal Divers 54: 69-77. https://doi.org/10.1007/s13225-011-0112-2
  42. Hamzah TNT, Lee SY, Hidayat A, Terhem R, Faridah-Hanum I, Mohamed R. 2018. Diversity and characterization of endophytic fungi isolated from the tropical mangrove species, Rhizophora mucronata, and identification of potential antagonists against the soil-borne fungus, Fusarium solani. Front. Microbiol. 9: 1707.
  43. Arivudainambi USE, Anand TD, Shanmugaiah V, Karunakaran C, Rajenrdan A. 2011. Novel bioactive metabolites producing endophytic fungus Colletotrichum gloeosporioides against multidrug resistant Staphylococcus aureus. FEMS Immunol. Med. Microbiol. 61: 340-345. https://doi.org/10.1111/j.1574-695X.2011.00780.x
  44. Zou WX, Meng JC, Lu H, Chen GX, Shi GX, Zhang TY, et al. 2000. Metabolites of Colletotrichum gloeosporioides, an endophytic fungus in Artemisia mongolica. J. Nat. Prod. 63: 1529-1530. https://doi.org/10.1021/np000204t
  45. Xiong ZQ, Yang YY, Zhao N, Wang Y. 2013. Diversity of endophytic fungi and screening of fungal paclitaxel producer from Anglojap yew, Taxus x media. BMC Microbiol. 13: 71.
  46. Zhang Q, Wei X, Wang J. 2012. Phillyrin produced by Colletotrichum gloeosporioides, an endophytic fungus isolated from Forsythia suspensa. Fitoterapia 83: 1500-1505. https://doi.org/10.1016/j.fitote.2012.08.017
  47. dos Santos IP, da Silva LCN, da Silva MV, de Araujo JM, Cavalcanti MD, Lima VLD. 2015. Antibacterial activity of endophytic fungi from leaves of Indigofera suffruticosa Miller (Fabaceae). Front. Microbiol. 6: 350.
  48. Shan TJ, Tian J, Wang XH, Mou Y, Mao ZL, Lai DW, et al. 2014. Bioactive spirobisnaphthalenes from the endophytic fungus Berkleasmium sp. J. Nat. prod. 77: 2151-2160. https://doi.org/10.1021/np400988a
  49. Kusari S, Pandey SP, Spiteller M. 2013. Untapped mutualistic paradigms linking host plant and endophytic fungal production of similar bioactive secondary metabolites. Phytochemistry 91: 81-87. https://doi.org/10.1016/j.phytochem.2012.07.021
  50. Masi, M, Cimmino A, Boari A, Tuzi A, Zonno MC, Baroncelli R, et al. 2017. Colletochlorins E and F, new phytotoxic tetrasubstituted pyran-2-one and dihydrobenzofuran, isolated from Colletotrichum higginsianum with potential herbicidal activity. J. Agric. Food Chem. 65: 1124-1130. https://doi.org/10.1021/acs.jafc.6b05193
  51. Garcia-Pajon CM, Collado IG. 2003. Secondary metabolites isolated from Colletotrichum species. Nat. Prod. Rep. 20: 426-431. https://doi.org/10.1039/B302183C
  52. Gohbara M, Kosuge Y, Yamasaki S, Kimura Y, Suzuki A, Tamura S. 1978. Isolation, structures and biological activities of colletotrichins, phytotoxic substances from Colletotrichum nicotianae. Agric. Biol. Chem. 42: 1037-1043.
  53. Liu HX, Tan HB, Chen YC, Li SN, Li HH, Zhang WM. 2018. Secondary metabolites from the Colletotrichum gloeosporioides A12, an endophytic fungus derived from Aquilaria sinensis. Nat. Prod. Res. 32: 2360-2365. https://doi.org/10.1080/14786419.2017.1410810
  54. Lu H, Zou WX, Meng JC, Hu J, Tan RX. 2000. New bioactive metabolites produced by Colletotrichum sp., an endophytic fungus in Artemisia annua. Plant Sci. 151: 67-73. https://doi.org/10.1016/S0168-9452(99)00199-5
  55. Wang WX, Kusari S, Laatsch H, Golz C, Kusari P, Strohmann C, et al. 2016. Antibacterial Azaphilones from an endophytic fungus, Colletotrichum sp. BS4. J. Nat. Prod. 79: 704-710. https://doi.org/10.1021/acs.jnatprod.5b00436
  56. Huang L, Luo H, Li Q, Wang D, Zhang J, Hao X, et al. 2015. Pentacyclic triterpene derivatives possessing polyhydroxyl ring A inhibit Gram-positive bacteria growth by regulating metabolism and virulence genes expression. Eur. J. Med. Chem. 95: 64-75. https://doi.org/10.1016/j.ejmech.2015.01.015
  57. Rios JL, Recio MC, Villar A. 1991. Isolation and identification of the antibacterial compounds from Helichrysum stoechas. J. Ethnopharmacol. 33: 51-55. https://doi.org/10.1016/0378-8741(91)90160-F
  58. Zhu H, Li D, Yan Q, An Y, Huo X, Zhang T, et al. 2019. α-Pyrones, secondary metabolites from fungus Cephalotrichum microsporum and their bioactivities. Bioorg. Chem. 83: 129-134. https://doi.org/10.1016/j.bioorg.2018.10.022
  59. Tomas-Lorente F, Iniesta-Sanmartin E, Tomas-Barberan FA, Trowitzsch-Kienast W, Wray V. 1989. Antifungal phloroglucinol derivatives and lipophilic flavonoids from Helichrysum decumbens. Phytochemistry 28: 1613-1615. https://doi.org/10.1016/S0031-9422(00)97809-9
  60. Da Porto C, Calligaris S, Celotti E, Nicoli MC. 2000. Antiradical properties of commercial cognacs assessed by the DPPH(.) test. J. Agric. Food Chem. 48: 4241-4245. https://doi.org/10.1021/jf000167b
  61. Soare JR, Dinis TC, Cunha AP, Almeida LM. 1997. Antioxidant activities of some extracts of Thymus zygis. Free Radic. Res. 26: 469-478. https://doi.org/10.3109/10715769709084484
  62. Pan F, Su TJ, Cai SM, Wu W. 2017. Fungal endophyte-derived Fritillaria unibracteata var. wabuensis: diversity, antioxidant capacities in vitro and relations to phenolic, flavonoid or saponin compounds. Sci. Rep. 7: 42008.
  63. Baxter A, Mittler R, Suzuki N. 2013. ROS as key players in plant stress signaling. J. Exp. Bot. 65: 1229-1240. https://doi.org/10.1093/jxb/ert375
  64. Uzma F, Chowdappa S. 2017. Antimicrobial and antioxidant potential of endophytic fungi isolated from ethnomedicinal plants of Western Ghats Karnataka. J. Pure Appl. Microbiol. 11: 1009-1025. https://doi.org/10.22207/JPAM.11.2.43
  65. Brunetti C, Martina D, Ferdinando MD, Fini A, Pollastri S, Tattini M. 2013. Flavonoids as antioxidants and developmental regulators: relative significance in plants and humans. Int. J. Mol. Sci. 14: 3540-3555. https://doi.org/10.3390/ijms14023540
  66. Gherraf N, Segni L, Brahim L, Samir H. 2011. Evaluation of antioxidant potential of various extract of Traganum nudatum Del. Plant Sci. Feed 1: 155-159.
  67. Kondraganti SR, Fernandez-Salguero P, Gonzalez FJ, Ramos KS, Jiang W, Moorthy B. 2003. Polycyclic aromatic hydrocarbon inducible DNA adducts: evidence by 32P-postlabeling and use of knockout mice for Ah receptor-independent mechanisms of metabolic activation in vivo. Int. J. Cancer 103: 5-11. https://doi.org/10.1002/ijc.10784
  68. DeBaun JR, Smith JY, Miller EC, Miller JA. 1970. Reactivity in vivo of the carcinogen N-hydroxy-2-acetylaminofuorene: increase by sulfate ion. Science 167: 184-186. https://doi.org/10.1126/science.167.3915.184
  69. Miller JA. 1970. Carcinogenesis by chemicals: an overview-GHA clowes memorial lecture. Cancer Res. 30: 559-576.
  70. Phadungkit M, Somdee T, Kangsadalampai K. 2012. Phytochemical screening, antioxidant and antimutagenic activities of selected Thai edible plant extracts. J. Med. Plants Res. 6: 662-666.
  71. Cowman AF, Duraisingh MT. 2001. An old enemy, a new battle plan: perspectives on combating drug-resistance malaria. EMBO Rep. 2: 77-79. https://doi.org/10.1093/embo-reports/kve032
  72. Pink R, Hudson A, Mouries MA, Bendig M. 2005. Opportunities and challenges in antiparasitic drug discovery. Nat. Rev. Drug Discov. 4: 727-740. https://doi.org/10.1038/nrd1824
  73. Jansen O, Tits M, Angenot L. et al. 2012. Anti-plasmodial activity of Dicoma tomentosa (Asteraceae) and identification of urospermal A-15-O-acetate as the main active compound. Malar. J. 11: 289.
  74. Wiyakrutta S, Sriubolmas N, Panphut W, Thongon N, Danwisetkanjana K, Ruangrungsi N, et al. 2004. Endophytic fungi with antimicrobial, anti-cancer and antimalarial activities isolated from Thai medicinal plants. World J. Microbiol. Biotechnol. 20: 265-272. https://doi.org/10.1023/B:WIBI.0000023832.27679.a8
  75. Jimenez-Romero C, Ortega-Barria E, Arnold AE, Cubilla-Rios L. 2008. Activity against Plasmodium falciparum of lactones isolated from the endophytic fungus Xylaria sp. Pharm. Biol. 46: 700-703. https://doi.org/10.1080/13880200802215859
  76. Surya S, Salam AD, Tomy DV, Carla B, Kumar RA, Sunil C. 2014. Diabetes mellitus and medicinal plasnts-a review. Asian Pac. J. Trop. Dis. 4: 337-347. https://doi.org/10.1016/S2222-1808(14)60585-5
  77. Wu PP, Zhang K, Lu YJ, He P, Zhao SQ. 2014. In vitro and in vivo evaluation of the antidiabetic activity of ursolic acid derivatives. Eur. J. Med. Chem. 80: 502-508. https://doi.org/10.1016/j.ejmech.2014.04.073
  78. Schmidit D, Frommer W, Junge B, Muller L, Wingender W, Truscheit E, et al. 1977. α-Glucosidase inhibitors. Naturwissenschaften 64: 535-536. https://doi.org/10.1007/BF00483561
  79. Sohretoglu D, Sari S, Barut B, Ozel A. 2018. Discovery of potent α-glucosidase inhibitor favonols: insights into mechanism of action through inhibition kinetics and docking simulations. Bioorg. Chem. 79: 257-264. https://doi.org/10.1016/j.bioorg.2018.05.010
  80. Indrianingsih AW, Tachibana S. 2017.α-Glucosidase inhibitor produced by an endophytic fungus, Xylariaceae sp. QGS 01 from Quercus gilva Blume. Food Sci. Human Wellness 6: 88-95. https://doi.org/10.1016/j.fshw.2017.05.001
  81. Wu XJ, Hansen C. 2008. Antioxidant capacity, phenolic content, and polysaccharide content of Lentinus edodes grown in whey permeate-based submerged culture. J. Food Sci. 73: M1-M8.
  82. Burton GW, Ingold KU. 1999. Mechanism of antioxidant action: preventive and chain breaking antioxidants. In J. Miquel (Ed.), CRC handbook of free radicals and antioxidants in biomedicine (Chap. 10, pp. 29-43). Boca Raton: CRC Press.
  83. Baral B, Mozafari MR. 2020. Strategic moves of "superbugs" against available chemical scaffolds: signaling, regulation, and challenges. ACS Pharmacol. Transl. Sci. 3: 373-400. https://doi.org/10.1021/acsptsci.0c00005
  84. Stewart PS, Costerton JW. 2001. Antibiotic resistance of bacteria in biofilms. Lancet 358: 135-138. https://doi.org/10.1016/S0140-6736(01)05321-1
  85. Nemoto K, Hirota K, Ono T, Murakami K, Murakami K, Nagao D, et al. 2000. Effect of Varidase (streptokinase) on biofilm formed by Staphylococcus aureus. Chemotherapy 46: 111-115. https://doi.org/10.1159/000007264
  86. O'Toole G, Kaplan HB, Kolter R. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54: 49-79. https://doi.org/10.1146/annurev.micro.54.1.49
  87. Hurdle JG, O'Neill AJ, Chopra I, Lee RE. 2011. Targeting bacterial membrane function: an underexploited mechanism for treating persistent infections. Nat. Rev. Microbiol. 9: 62-75. https://doi.org/10.1038/nrmicro2474
  88. Wojnicz D, Tichaczek-Goska D, Kicia M. 2015. Pentacyclic triterpenes combined with ciprofloxacin help to eradicate the biofilm formed in vitro by Escherichia coli. Indian J. Med. Res. 141: 343-353. https://doi.org/10.4103/0971-5916.156631
  89. Rajivgandhi G, Vijayan R, Maruthupandy M, Vaseeharan B, Manoharan N. 2018. Antibiofilm effect of Nocardiopsis sp. GRG 1 (KT235640) compound against biofilm forming Gram negative bacteria on UTIs. Microb. Pathog. 118: 190-198. https://doi.org/10.1016/j.micpath.2018.03.011
  90. Tunney M, Ramage G, Field T. et al. 2004. Rapid colorimetric assay for antimicrobial susceptibility testing of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 48: 1879-1881. https://doi.org/10.1128/AAC.48.5.1879-1881.2004
  91. Nascimento AM, Conti R, Turatti IC, Cavalcanti BC, Costa-Lotufo LV, Pessoa C, et al. 2012. Bioactive extracts and chemical constituents of two endophytic strains of Fusarium oxysporum. Rev. Bras. Farmacogn. 22: 1276-1281. https://doi.org/10.1590/S0102-695X2012005000106
  92. Zhan J, Burns AM, Liu MX, Faeth SH, Gunatilaka AA. 2007. Search for cell motility and angiogenesis inhibitors with potential anticancer activity: Beauvericin and other constituents of two endophytic strains of Fusarium oxysporum. J. Nat. Prod. 70: 227-232. https://doi.org/10.1021/np060394t
  93. Fairlamb IJS, Marrison LR, Dickinson JM, Lu FJ, Schmidt JP. 2004. 2-Pyrones possessing antimicrobial and cytotoxic activities. Bioorg. Med. Chem. 12: 4285-4299. https://doi.org/10.1016/j.bmc.2004.01.051
  94. Barcelos RC, Pastre JC, Caixeta V, Vendramini-Costa DB, de Carvalho JE, Pilli RA. 2012. Synthesis of methoxylated goniothalamin, aza-goniothalamin and γ-pyrones and their in vitro evaluation against human cancer cells. Bioorg. Med. Chem. 20: 3635-3651. https://doi.org/10.1016/j.bmc.2012.03.059
  95. Suzuki K, Kuwahara A, Yoshida H, Fujita SI, Nishikiori T, Nakagawa T. 1997. NF00659A(1), A(2), A(3), B-1 and B-2, novel antitumor antibiotics produced by Aspergillus sp. NF00659 .1. Taxonomy, fermentation, isolation and biological activities. J. Antibiot. 50: 314-317. https://doi.org/10.7164/antibiotics.50.314
  96. Kondoh M, Usui T, Kobayashi S, Tsuchiya K, Nishikawa K, Nishikiori T, et al. 1998. Cell cycle arrest and antitumor activity of pironetin and its derivatives. Cancer Lett. 126: 29-32. https://doi.org/10.1016/S0304-3835(97)00528-4
  97. Marrison LR, Dickinson JM, Fairlamb IJS. 2002. Bioactive 4-substituted-6-methyl-2-pyrones with promising cytotoxicity against A2780 and K562 cell lines. Bioorg. Med. Chem. Lett. 12: 3509-3513. https://doi.org/10.1016/S0960-894X(02)00824-7
  98. Kohn KW. 1996. DNA filter elution: a window on DNA damage in mammalian cells. Bioessays 18: 505-513. https://doi.org/10.1002/bies.950180613
  99. Hurley LH. 2002. DNA and associated processes as targets for cancer therapy. Nat. Rev. Cancer 2: 188-200. https://doi.org/10.1038/nrc749
  100. Nitiss JL. 1998. Investigating the biological functions of DNA topoisomerases in eukaryotic cells. Biochim. Biophys. Acta. 1400: 63-81. https://doi.org/10.1016/S0167-4781(98)00128-6
  101. Wang JC. 1996. DNA topoisomerases. Annu. Rev. Biochem. 65: 635-692. https://doi.org/10.1146/annurev.bi.65.070196.003223
  102. Liu LF. 1989. DNA topoisomerase poisons as antitumor drugs. Annu. Rev. Biochem. 58: 351-375. https://doi.org/10.1146/annurev.bi.58.070189.002031
  103. Pommier Y. 1998. Diversity of DNA topoisomerases I and inhibitors. Biochimie 80: 255-270. https://doi.org/10.1016/S0300-9084(98)80008-4
  104. Barrett JF, Sutcliffe JA, Gootz TD. 1990. In vitro assays used to measure the activity of topoisomerases. Antimicrob. Agents Chemother. 34: 1-7. https://doi.org/10.1128/AAC.34.1.1