One-step Bio-guided Isolation of Secondary Metabolites from the Endophytic Fungus Penicillium crustosum Using High-resolution Semi-preparative HPLC


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Background:An endophytic fungal strain Penicillium crustosum was isolated from the seagrass Posidonia oceanica and investigated to identify its antimicrobial constituents and characterize its metabolome composition. The ethyl acetate extract of this fungus exhibited antimicrobial activity against methicillin-resistant Staphylococcus aureus (MRSA) as well as an anti-quorum sensing effect against Pseudomonas aeruginosa.

Methods:The crude extract was profiled by UHPLC-HRMS/MS, and the dereplication was assisted by feature-based molecular networking. As a result, more than twenty compounds were annotated in this fungus. To rapidly identify the active compounds, the enriched extract was fractionated by semipreparative HPLC-UV applying a chromatographic gradient transfer and dry load sample introduction to maximise resolution. The collected fractions were profiled by 1H-NMR and UHPLC-HRMS.

Results:The use of molecular networking-assisted UHPLC-HRMS/MS dereplication allowed preliminary identification of over 20 compounds present in the ethyl acetate extract of P. crustosum. The chromatographic approach significantly accelerated the isolation of the majority of compounds present in the active extract. The one-step fractionation allowed the isolation and identification of eight compounds (1-8).

Conclusion:This study led to the unambiguous identification of eight known secondary metabolites as well as the determination of their antibacterial properties.

Об авторах

Abdulelah Alfattani

School of Pharmaceutical Sciences, University of Geneva

Email: info@benthamscience.net

Emerson Queiroz

School of Pharmaceutical Sciences, University of Geneva

Email: info@benthamscience.net

Laurence Marcourt

School of Pharmaceutical Sciences, University of Geneva

Email: info@benthamscience.net

Sara Leoni

Department of Botany and Plant Biology, University of Geneva

Email: info@benthamscience.net

Didier Stien

Laboratoire de Biodiversité et Biotechnologie Microbiennes, Sorbonne Université,Observatoire Océanologique

Email: info@benthamscience.net

Valerie Hofstetter

Plant Protection Research Division, Agroscope

Email: info@benthamscience.net

Katia Gindro

Plant Protection Research Division, Agroscope

Email: info@benthamscience.net

Karl Perron

Department of Botany and Plant Biology, University of Geneva

Email: info@benthamscience.net

Jean-Luc Wolfender

School of Pharmaceutical Sciences, University of Geneva

Автор, ответственный за переписку.
Email: info@benthamscience.net

Список литературы

  1. World-Health-Organization, Antimicrobial resistance. 2020. Available from: https://www.who.int/news-room/fact-sheets/detail/antimicrobial-resistance
  2. Pendleton, J.N.; Gorman, S.P.; Gilmore, B.F. Clinical relevance of the ESKAPE pathogens. Expert Rev. Anti Infect. Ther., 2013, 11(3), 297-308. doi: 10.1586/eri.13.12 PMID: 23458769
  3. Haidar, R.; Najjar, M.; Boghossian, A.D.; Tabbarah, Z. Propionibacterium acnes causing delayed postoperative spine infection (Review). Scand. J. Infect. Dis., 2010, 42(6-7), 405-411. doi: 10.3109/00365540903582459 PMID: 20199135
  4. Dréno, B.; Pécastaings, S.; Corvec, S.; Veraldi, S.; Khammari, A.; Roques, C. Cutibacterium acnes (Propionibacterium acnes) and acne vulgaris: a brief look at the latest updates. J. Eur. Acad. Dermatol. Venereol., 2018, 32(S2), 5-14. doi: 10.1111/jdv.15043 PMID: 29894579
  5. Hutchings, M.I.; Truman, A.W.; Wilkinson, B. Antibiotics: past, present and future. Curr. Opin. Microbiol., 2019, 51, 72-80. doi: 10.1016/j.mib.2019.10.008 PMID: 31733401
  6. Saeki, E.K.; Kobayashi, R.K.T.; Nakazato, G. Quorum sensing system: Target to control the spread of bacterial infections. Microb. Pathog., 2020, 142, 104068. doi: 10.1016/j.micpath.2020.104068 PMID: 32061914
  7. Rutherford, S.T.; Bassler, B.L. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb. Perspect. Med., 2012, 2(11), a012427. doi: 10.1101/cshperspect.a012427 PMID: 23125205
  8. Schneider, Y.K. Bacterial natural product drug discovery for new antibiotics: Strategies for tackling the problem of antibiotic resistance by efficient bioprospecting. Antibiotics, 2021, 10(7), 842. doi: 10.3390/antibiotics10070842 PMID: 34356763
  9. Nisa, H.; Kamili, A.N. Fungal endophytes from medicinal plants as a potential source of bioactive secondary metabolites and volatile organic compounds: An overview.Endophytes and Secondary Metabolites; Jha, S., Ed.; Springer International Publishing: Cham, 2019, pp. 1-11. doi: 10.1007/978-3-319-90484-9_29
  10. Sonjak, S.; Frisvad, J.C.; Gunde-Cimerman, N. Comparison of secondary metabolite production by Penicillium crustosum strains, isolated from Arctic and other various ecological niches. FEMS Microbiol. Ecol., 2005, 53(1), 51-60. doi: 10.1016/j.femsec.2004.10.014 PMID: 16329929
  11. Skouboe, P.; Frisvad, J.C.; Taylor, J.W.; Lauritsen, D.; Boysen, M.; Rossen, L. Phylogenetic analysis of nucleotide sequences from the ITS region of terverticillate Penicillium species. Mycol. Res., 1999, 103(7), 873-881. doi: 10.1017/S0953756298007904
  12. El-Morsy, E.M.; Ibrahim, H.A.H.; Amal Zaki, F.; Mohsien, M.T.; Abu El-Regal, M. Pathogenicity of fungi colonizing some hard corals and invertebrates from the northern egyptian red sea coast. Egypt. J. Aquat. Biol. Fish., 2017, 21(2), 47-61. doi: 10.21608/ejabf.2017.3532
  13. Liu, C.C.; Zhang, Z.Z.; Feng, Y.Y.; Gu, Q.Q.; Li, D.H.; Zhu, T.J. Secondary metabolites from Antarctic marine-derived fungus Penicillium crustosum HDN153086. Nat. Prod. Res., 2019, 33(3), 414-419. doi: 10.1080/14786419.2018.1455045 PMID: 29600717
  14. Amer, M.S.; Abd Ellatif, H.H.; Hassan, S.W.M.; Aboelela, G.M.; Gad, A.M. Characterization of some fungal strains isolated from the Eastern coast of Alexandria, Egypt, and some applications of Penicillium crustosum. Egypt. J. Aquat. Res., 2019, 45(3), 211-217. doi: 10.1016/j.ejar.2019.06.006
  15. Zeng, W.L.; Li, W.K.; Han, H.; Tao, Y.Y.; Yang, L.; Wang, Z.T.; Chen, K.X. Microbial biotransformation of gentiopicroside by the endophytic fungus Penicillium crustosum 2T01Y01. Appl. Environ. Microbiol., 2014, 80(1), 184-192. doi: 10.1128/AEM.02309-13 PMID: 24141132
  16. Fan, J.; Liao, G.; Kindinger, F.; Ludwig-Radtke, L.; Yin, W.B.; Li, S.M. Peniphenone and penilactone formation in Penicillium crustosum via 1, 4-Michael additions of ortho-quinone methide from hydroxyclavatol to γ-butyrolactones from crustosic acid. J. Am. Chem. Soc., 2019, 141(10), 4225-4229. doi: 10.1021/jacs.9b00110 PMID: 30811183
  17. Wu, G.; Ma, H.; Zhu, T.; Li, J.; Gu, Q.; Li, D. Penilactones A and B, two novel polyketides from Antarctic deep-sea derived fungus Penicillium crustosum PRB-2. Tetrahedron, 2012, 68(47), 9745-9749. doi: 10.1016/j.tet.2012.09.038
  18. Wolfender, J.L.; Nuzillard, J.M.; van der Hooft, J.J.J.; Renault, J.H.; Bertrand, S. Accelerating metabolite identification in natural product research: toward an ideal combination of liquid chromatography-high-resolution tandem mass spectrometry and NMR profiling, in silico databases, and chemometrics. Anal. Chem., 2019, 91(1), 704-742. doi: 10.1021/acs.analchem.8b05112 PMID: 30453740
  19. Yang, J.Y.; Sanchez, L.M.; Rath, C.M.; Liu, X.; Boudreau, P.D.; Bruns, N.; Glukhov, E.; Wodtke, A.; de Felicio, R.; Fenner, A.; Wong, W.R.; Linington, R.G.; Zhang, L.; Debonsi, H.M.; Gerwick, W.H.; Dorrestein, P.C. Molecular networking as a dereplication strategy. J. Nat. Prod., 2013, 76(9), 1686-1699. doi: 10.1021/np400413s PMID: 24025162
  20. Allard, P.M.; Péresse, T.; Bisson, J.; Gindro, K.; Marcourt, L.; Pham, V.C.; Roussi, F.; Litaudon, M.; Wolfender, J.L. Integration of molecular networking and in-silico MS/MS fragmentation for natural products dereplication. Anal. Chem., 2016, 88(6), 3317-3323. doi: 10.1021/acs.analchem.5b04804 PMID: 26882108
  21. Weber, R.W.; Stenger, E.; Meffert, A.; Hahn, M. Brefeldin A production by Phoma medicaginis in dead pre-colonized plant tissue: a strategy for habitat conquest? Mycol. Res., 2004, 108, 662-671. doi: 10.1017/s0953756204000243
  22. Schoch, C.L.; Seifert, K.A.; Huhndorf, S.; Robert, V.; Spouge, J.L.; Levesque, C.A.; Chen, W. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc. Natl. Acad. Sci. USA, 2012, 109(16), 6241-6246. doi: 10.1073/pnas.1117018109
  23. Hofstetter, V.; Buyck, B.; Eyssartier, G.; Schnee, S.; Gindro, K. The unbearable lightness of sequenced-based identification. Fungal Divers., 2019, 96(1), 243-284. doi: 10.1007/s13225-019-00428-3
  24. Rutz, A.; Dounoue-Kubo, M.; Ollivier, S.; Bisson, J.; Bagheri, M.; Saesong, T.; Ebrahimi, S.N.; Ingkaninan, K.; Wolfender, J.L.; Allard, P.M. Taxonomically informed scoring enhances confidence in natural products annotation. Front. Plant Sci., 2019, 10(1329), 1329. doi: 10.3389/fpls.2019.01329 PMID: 31708947
  25. Wang, M.; Carver, J.J.; Phelan, V.V.; Sanchez, L.M.; Garg, N.; Peng, Y.; Nguyen, D.D.; Watrous, J.; Kapono, C.A.; Luzzatto-Knaan, T.; Porto, C.; Bouslimani, A.; Melnik, A.V.; Meehan, M.J.; Liu, W.T.; Crüsemann, M.; Boudreau, P.D.; Esquenazi, E.; Sandoval-Calderón, M.; Kersten, R.D.; Pace, L.A.; Quinn, R.A.; Duncan, K.R.; Hsu, C.C.; Floros, D.J.; Gavilan, R.G.; Kleigrewe, K.; Northen, T.; Dutton, R.J.; Parrot, D.; Carlson, E.E.; Aigle, B.; Michelsen, C.F.; Jelsbak, L.; Sohlenkamp, C.; Pevzner, P.; Edlund, A.; McLean, J.; Piel, J.; Murphy, B.T.; Gerwick, L.; Liaw, C.C.; Yang, Y.L.; Humpf, H.U.; Maansson, M.; Keyzers, R.A.; Sims, A.C.; Johnson, A.R.; Sidebottom, A.M.; Sedio, B.E.; Klitgaard, A.; Larson, C.B.; Boya, P. C.A.; Torres-Mendoza, D.; Gonzalez, D.J.; Silva, D.B.; Marques, L.M.; Demarque, D.P.; Pociute, E.; O’Neill, E.C.; Briand, E.; Helfrich, E.J.N.; Granatosky, E.A.; Glukhov, E.; Ryffel, F.; Houson, H.; Mohimani, H.; Kharbush, J.J.; Zeng, Y.; Vorholt, J.A.; Kurita, K.L.; Charusanti, P.; McPhail, K.L.; Nielsen, K.F.; Vuong, L.; Elfeki, M.; Traxler, M.F.; Engene, N.; Koyama, N.; Vining, O.B.; Baric, R.; Silva, R.R.; Mascuch, S.J.; Tomasi, S.; Jenkins, S.; Macherla, V.; Hoffman, T.; Agarwal, V.; Williams, P.G.; Dai, J.; Neupane, R.; Gurr, J.; Rodríguez, A.M.C.; Lamsa, A.; Zhang, C.; Dorrestein, K.; Duggan, B.M.; Almaliti, J.; Allard, P.M.; Phapale, P.; Nothias, L.F.; Alexandrov, T.; Litaudon, M.; Wolfender, J.L.; Kyle, J.E.; Metz, T.O.; Peryea, T.; Nguyen, D.T.; VanLeer, D.; Shinn, P.; Jadhav, A.; Müller, R.; Waters, K.M.; Shi, W.; Liu, X.; Zhang, L.; Knight, R.; Jensen, P.R.; Palsson, B.Ø.; Pogliano, K.; Linington, R.G.; Gutiérrez, M.; Lopes, N.P.; Gerwick, W.H.; Moore, B.S.; Dorrestein, P.C.; Bandeira, N. Sharing and community curation of mass spectrometry data with global natural products social molecular networking. Nat. Biotechnol., 2016, 34(8), 828-837. doi: 10.1038/nbt.3597 PMID: 27504778
  26. Shannon, P.; Markiel, A.; Ozier, O.; Baliga, N.S.; Wang, J.T.; Ramage, D.; Amin, N.; Schwikowski, B.; Ideker, T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res., 2003, 13(11), 2498-2504. doi: 10.1101/gr.1239303 PMID: 14597658
  27. Houriet, J.; Allard, P-M.; Queiroz, E.F.; Marcourt, L.; Gaudry, A.; Vallin, L. A mass spectrometry based metabolite profiling workflow for selecting abundant specific markers and their structurally related multi-component signatures in traditional chinese medicine multi‐herb formulae. Front. Pharmacol., 1774, 2020, 11. PMID: 33362543
  28. Queiroz, E.F.; Alfattani, A.; Afzan, A.; Marcourt, L.; Guillarme, D.; Wolfender, J.L. Utility of dry load injection for an efficient natural products isolation at the semi-preparative chromatographic scale. J. Chromatogr. A, 2019, 1598, 85-91. doi: 10.1016/j.chroma.2019.03.042 PMID: 30926257
  29. Wiegand, I.; Hilpert, K.; Hancock, R.E.W. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat. Protoc., 2008, 3(2), 163-175. doi: 10.1038/nprot.2007.521 PMID: 18274517
  30. Eloff, J. A sensitive and quick microplate method to determine the minimal inhibitory concentration of plant extracts for bacteria. Planta Med., 1998, 64(8), 711-713. doi: 10.1055/s-2006-957563 PMID: 9933989
  31. Hentzer, M.; Riedel, K.; Rasmussen, T.B.; Heydorn, A.; Andersen, J.B.; Parsek, M.R.; Rice, S.A.; Eberl, L.; Molin, S.; Høiby, N.; Kjelleberg, S.; Givskov, M. Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology (Reading), 2002, 148(1), 87-102. doi: 10.1099/00221287-148-1-87 PMID: 11782502
  32. Schaefler, S.; Perry, W.; Jones, D. Methicillin-resistant strains of Staphylococcus aureus phage type 92. Antimicrob. Agents Chemother., 1979, 15(1), 74-80. doi: 10.1128/AAC.15.1.74 PMID: 154874
  33. Horváth, B.; Hunyadkürti, J.; Vörös, A.; Fekete, C.; Urbán, E.; Kemény, L.; Nagy, I. Genome sequence of Propionibacterium acnes type II strain ATCC 11828. J. Bacteriol., 2012, 194(1), 202-203. doi: 10.1128/JB.06388-11 PMID: 22156398
  34. Medeiros, A.A.; O’Brien, T.F.; Wacker, W.E.C.; Yulug, N.F. Effect of salt concentration on the apparent in-vitro susceptibility of Pseudomonas and other gram-negative bacilli to gentamicin. J. Infect. Dis., 1971, 124(Suppl. 1), S59-S64. doi: 10.1093/infdis/124.Supplement_1.S59 PMID: 5001630
  35. Buckingham, J.E. Dictionary of natural products; Chapman and Hall/CRC: Boca Raton, Florida, 2007.
  36. Nothias, L.F.; Petras, D.; Schmid, R.; Dührkop, K.; Rainer, J.; Sarvepalli, A.; Protsyuk, I.; Ernst, M.; Tsugawa, H.; Fleischauer, M.; Aicheler, F.; Aksenov, A.A.; Alka, O.; Allard, P.M.; Barsch, A.; Cachet, X.; Caraballo-Rodriguez, A.M.; Da Silva, R.R.; Dang, T.; Garg, N.; Gauglitz, J.M.; Gurevich, A.; Isaac, G.; Jarmusch, A.K.; Kameník, Z.; Kang, K.B.; Kessler, N.; Koester, I.; Korf, A.; Le Gouellec, A.; Ludwig, M.; Martin, H. C.; McCall, L.I.; McSayles, J.; Meyer, S.W.; Mohimani, H.; Morsy, M.; Moyne, O.; Neumann, S.; Neuweger, H.; Nguyen, N.H.; Nothias-Esposito, M.; Paolini, J.; Phelan, V.V.; Pluskal, T.; Quinn, R.A.; Rogers, S.; Shrestha, B.; Tripathi, A.; van der Hooft, J.J.J.; Vargas, F.; Weldon, K.C.; Witting, M.; Yang, H.; Zhang, Z.; Zubeil, F.; Kohlbacher, O.; Böcker, S.; Alexandrov, T.; Bandeira, N.; Wang, M.; Dorrestein, P.C. Feature-based molecular networking in the GNPS analysis environment. Nat. Methods, 2020, 17(9), 905-908. doi: 10.1038/s41592-020-0933-6 PMID: 32839597
  37. Lin, H.C.; Chiou, G.; Chooi, Y.H.; McMahon, T.C.; Xu, W.; Garg, N.K.; Tang, Y. Elucidation of the concise biosynthetic pathway of the communesin indole alkaloids. Angew. Chem. Int. Ed., 2015, 54(10), 3004-3007. doi: 10.1002/anie.201411297 PMID: 25571861
  38. Jadulco, R.; Edrada, R.A.; Ebel, R.; Berg, A.; Schaumann, K.; Wray, V.; Steube, K.; Proksch, P. New communesin derivatives from the fungus Penicillium sp. derived from the Mediterranean sponge Axinella verrucosa. J. Nat. Prod., 2004, 67(1), 78-81. doi: 10.1021/np030271y PMID: 14738391
  39. Huang, S.; Chen, H.; Li, W.; Zhu, X.; Ding, W.; Li, C. Bioactive chaetoglobosins from the mangrove endophytic fungus Penicillium chrysogenum. Mar. Drugs, 2016, 14(10), 172. doi: 10.3390/md14100172 PMID: 27690061
  40. Iwamoto, C.; Yamada, T.; Ito, Y.; Minoura, K.; Numata, A. Cytotoxic cytochalasans from a Penicillium species separated from a marine alga. Tetrahedron, 2001, 57(15), 2997-3004. doi: 10.1016/S0040-4020(01)00153-3
  41. Numata, A.; Takahashi, C.; Ito, Y.; Minoura, K.; Yamada, T.; Matsuda, C.; Nomoto, K. Penochalasins, a novel class of cytotoxic cytochalasans from a Penicillium species separated from a marine alga: structure determination and solution conformation. J. Chem. Soc., Perkin Trans. 1, 1996, (3), 239-245. doi: 10.1039/p19960000239
  42. Zhu, X.; Zhou, D.; Liang, F.; Wu, Z.; She, Z.; Li, C. Penochalasin K, a new unusual chaetoglobosin from the mangrove endophytic fungus Penicillium chrysogenum V11 and its effective semi-synthesis. Fitoterapia, 2017, 123, 23-28. doi: 10.1016/j.fitote.2017.09.016 PMID: 28958956
  43. Flewelling, A.J.; Bishop, A.L.; Johnson, J.A.; Gray, C.A. Polyketides from an endophytic Aspergillus fumigatus isolate inhibit the growth of Mycobacterium tuberculosis and MRSA. Nat. Prod. Commun., 2015, 10(10), 1934578X1501001. doi: 10.1177/1934578X1501001009 PMID: 26669098
  44. Jiang, C.; Song, J.; Zhang, J.; Yang, Q. Identification and characterization of the major antifungal substance against Fusarium Sporotrichioides from Chaetomium globosum. World J. Microbiol. Biotechnol., 2017, 33(6), 108. doi: 10.1007/s11274-017-2274-x PMID: 28466302
  45. Chen, C.; Zhu, H.; Wang, J.; Yang, J.; Li, X.N.; Wang, J.; Chen, K.; Wang, Y.; Luo, Z.; Yao, G.; Xue, Y.; Zhang, Y. Armochaetoglobins K–R, anti-HIV pyrrole-based cytochalasans from Chaetomium globosum TW1-1. Eur. J. Org. Chem., 2015, 2015(14), 3086-3094. doi: 10.1002/ejoc.201403678
  46. Thohinung, S.; Kanokmedhakul, S.; Kanokmedhakul, K.; Kukongviriyapan, V.; Tusskorn, O.; Soytong, K. Cytotoxic 10-(indol-3-yl)-13cytochalasans from the fungus Chaetomium elatum ChE01. Arch. Pharm. Res., 2010, 33(8), 1135-1141. doi: 10.1007/s12272-010-0801-5 PMID: 20803114
  47. Fujita, M.; Yamada, M.; Nakajima, S.; Kawai, K.; Nagai, M. O-Methylation effect on the carbon-13 nuclear magnetic resonance signals of ortho-disubstituted phenols and its application to structure determination of new phthalides from Aspergillus silvaticus. Chem. Pharm. Bull. (Tokyo), 1984, 32(7), 2622-2627. doi: 10.1248/cpb.32.2622 PMID: 6499082
  48. Kimura, Y.; Yoshinari, T.; Koshino, H.; Fujioka, S.; Okada, K.; Shimada, A. Rubralactone, rubralides A, B and C, and rubramin produced by Penicillium rubrum. Biosci. Biotechnol. Biochem., 2007, 71(8), 1896-1901. doi: 10.1271/bbb.70112 PMID: 17690484
  49. Fink-Grernmels, J. Mycotoxins: Their implications for human and animal health. Vet. Q., 1999, 21(4), 115-120. doi: 10.1080/01652176.1999.9695005 PMID: 10568000
  50. Guillarme, D.; Nguyen, D.T.T.; Rudaz, S.; Veuthey, J.L. Method transfer for fast liquid chromatography in pharmaceutical analysis: Application to short columns packed with small particle. Part I: Isocratic separation. Eur. J. Pharm. Biopharm., 2007, 66(3), 475-482. doi: 10.1016/j.ejpb.2006.11.027 PMID: 17267188
  51. Guillarme, D.; Nguyen, D.T.T.; Rudaz, S.; Veuthey, J.L. Method transfer for fast liquid chromatography in pharmaceutical analysis: Application to short columns packed with small particle. Part II: Gradient experiments. Eur. J. Pharm. Biopharm., 2008, 68(2), 430-440. doi: 10.1016/j.ejpb.2007.06.018 PMID: 17703929
  52. Bennett, M.; Gill, G.B.; Pattenden, G.; Shuker, A.J.; Stapleton, A. Ylidenebutenolide mycotoxins. Concise syntheses of patulin and neopatulin from carbohydrate precursors. J. Chem. Soc., Perkin Trans. 1, 1991, (4), 929-937. doi: 10.1039/p19910000929
  53. Wu, H.H.; Tian, L.; Feng, B.M.; Li, Z.F.; Zhang, Q.H.; Pei, Y.H. Three new compounds from the marine fungus Penicillium sp. J. Asian Nat. Prod. Res., 2010, 12(1), 15-19. doi: 10.1080/10286020903442020 PMID: 20390738
  54. Ishimaru, K.; Nonaka, G.; Nishioka, I. Tannins and related-compounds. 54. phenolic glucoside gallates from Quercus mongolica and Quercus acutissima. Phytochemistry, 1987, 26(4), 1147-1152. doi: 10.1016/S0031-9422(00)82367-5
  55. Numata, A.; Takahashi, C.; Ito, Y.; Takada, T.; Kawai, K.; Usami, Y.; Matsumura, E.; Imachi, M.; Ito, T.; Hasegawa, T. Communesins, cytotoxic metabolites of a fungus isolated from a marine alga. Tetrahedron Lett., 1993, 34(14), 2355-2358. doi: 10.1016/S0040-4039(00)77612-X
  56. Sekita, S.; Yoshihira, K.; Natori, S. Chaetoglobosins, cytotoxic 10-(indol-3-yl)-(13)cytochalasans from Chaetomium spp. IV. 13C-Nuclear magnetic resonance spectra and their application to a biosynthetic study. Chem. Pharm. Bull. (Tokyo), 1983, 31(2), 490-498. doi: 10.1248/cpb.31.490
  57. Musuku, A.; Selala, M.I.; de Bruyne, T.; Claeys, M.; Schepens, P.J.C.; Tsatsakis, A.; Shtilman, M.I. Isolation and structure determination of a new roquefortine-related mycotoxin from Penicillium verrucosum var. cyclopium isolated from cassava. J. Nat. Prod., 1994, 57(7), 983-987. doi: 10.1021/np50109a017
  58. Shangguan, N.; Hehre, W.J.; Ohlinger, W.S.; Beavers, M.P.; Joullié, M.M. The total synthesis of roquefortine C and a rationale for the thermodynamic stability of isoroquefortine C over roquefortine C. J. Am. Chem. Soc., 2008, 130(19), 6281-6287. doi: 10.1021/ja800067q PMID: 18412344
  59. Ando, S.; Grote, A.L.; Koide, K. Diastereoselective synthesis of diketopiperazine bis-αβ-epoxides. J. Org. Chem., 2011, 76(4), 1155-1158. doi: 10.1021/jo102096d PMID: 21250704
  60. Brown, R.; Kelley, C.; Wiberley, S.E. The Production of 3-Benzylidene-6-isobutylidene-2,5-dioxopiperazine, 3,6-Dibenzylidene-2,5-dioxopiperazine, 3-Benzyl-6-benzylidene-2,5-dioxopiperazine, and 3,6-Dibenzyl-2,5-dioxopiperazine by a Variant of Streptomyces noursei. J. Org. Chem., 1965, 30(1), 277-280. doi: 10.1021/jo01012a066
  61. Gerber, N.N. Phenazines, phenoxazinones, and dioxopiperazines from Streptomyces thioluteus. J. Org. Chem., 1967, 32(12), 4055-4057. doi: 10.1021/jo01287a075 PMID: 5622472
  62. Kamei, H.; Oka, M.; Hamagishi, Y.; Tomita, K.; Konishi, M.; Oki, T. Piperafizines A and B potentiators of cytotoxicity of vincristine. J. Antibiot. (Tokyo), 1990, 43(8), 1018-1020. doi: 10.7164/antibiotics.43.1018 PMID: 2211350
  63. Goetz, M.A.; Zhang, C.; Zink, D.L.; Arocho, M.; Vicente, F.; Bills, G.F.; Polishook, J.; Dorso, K.; Onishi, R.; Gill, C.; Hickey, E.; Lee, S.; Ball, R.; Skwish, S.; Donald, R.G.K.; Phillips, J.W.; Singh, S.B. Coelomycin, a highly substituted 2,6-dioxo-pyrazine fungal metabolite antibacterial agent discovered by Staphylococcus aureus fitness test profiling. J. Antibiot. , 2010, 63(8), 512-518. doi: 10.1038/ja.2010.86 PMID: 20664605
  64. Pompeo, M.M.; Cheah, J.H.; Movassaghi, M. Total synthesis and anti-cancer activity of all known communesin alkaloids and related derivatives. J. Am. Chem. Soc., 2019, 141(36), 14411-14420. doi: 10.1021/jacs.9b07397 PMID: 31422662
  65. Pinedo, C.; Wright, S.A.I.; Collado, I.G.; Goss, R.J.M.; Castoria, R.; Hrelia, P.; Maffei, F.; Durán-Patrón, R. Isotopic labeling studies reveal the patulin detoxification pathway by the biocontrol yeast Rhodotorula kratochvilovae LS11. J. Nat. Prod., 2018, 81(12), 2692-2699. doi: 10.1021/acs.jnatprod.8b00539 PMID: 30460844

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