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Use of P450 Cytochrome Inhibitors in Studies of Enokipodin Biosynthesis

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Use of P450 Cytochrome Inhibitors in Studies of Enokipodin Biosynthesis Brazilian Journal of Microbiology 44, 4, 1285-1290 (2013) Copyright © 2013, Sociedade Brasileira de Microbiologia ISSN 1678-4405 www.sbmicrobiologia.org.br Research Paper Use of P450 cytochrome inhibitors in studies of enokipodin biosynthesis Noemia Kazue Ishikawa1, Satoshi Tahara2, Tomohiro Namatame2, Afgan Farooq2, Yukiharu Fukushi2 1Division of Environmental Resources, Graduate School of Agriculture, Hokkaido University, Sapporo, Japan. 2Division of Applied Bioscience, Graduate School of Agriculture, Hokkaido University, Sapporo, Japan. Submitted: November 27, 2011; Approved: April 4, 2013. Abstract Enokipodins A, B, C, and D are antimicrobial sesquiterpenes isolated from the mycelial culture me- dium of Flammulina velutipes, an edible mushroom. The presence of a quaternary carbon stereo- center on the cyclopentane ring makes enokipodins A-D attractive synthetic targets. In this study, nine different cytochrome P450 inhibitors were used to trap the biosynthetic intermediates of highly oxygenated cuparene-type sesquiterpenes of F. velutipes. Of these, 1-aminobenzotriazole produced three less-highly oxygenated biosynthetic intermediates of enokipodins A-D; these were identified as (S)-(-)-cuparene-1,4-quinone and epimers at C-3 of 6-hydroxy-6-methyl-3-(1,2,2-trimethyl- cyclopentyl)-2-cyclohexen-1-one. One of the epimers was found to be a new compound. Key words: Antimicrobial compound, cuparene-1,4-quinone, edible mushroom, enokitake, Flammulina velutipes. Introduction Srikrishna et al., 2006, Secci et al., 2007, Yoshida et al., 2009, Luján-Montelongo and Ávila-Zarraga, 2010, Flammulina velutipes (Curt. Fr.) Sing. (Enokitake in Srikrishna and Rao, 2010, Leboeuf et al., 2013). The influ- Japanese), in the family Physalacriaceae (Agaricales, ence of mycelial culture conditions on biosynthetic produc- Agaricomycetes), is one of the most popular edible mush- tion by F. velutipes was also studied (Ishikawa et al., 2005, rooms in Japan. Many bioactive metabolites have been iso- Melo et al., 2009). We speculated that the antimicrobial ac- lated from this fungus, including proteins (Komatsu et al., tivity of enokipodins A-D correlates to a highly oxygenated 1963, Lin et al., 1974, Tsuda, 1979, Ko et al., 1995, Tomita et al., 1998), glycoproteins (Ikekawa et al., 1985), polysac- cuparene nucleus. The involvement of cytochrome P450s charides (Yoshioka et al., 1973, Leung et al., 1997, Yaoita in many complex bioconversion processes, including de- et al., 1998, Wasser and Wess, 1999, Smiderle et al., 2006), toxification reactions and the production of secondary me- sterols (Yaoita et al., 1998), and monoterpenetriol (Hirai et tabolites, has been established in fungi (van den Brink et al., 1998). In a previous screen for antimicrobial secondary al., 1998). Although these enzymes carry out a wide range metabolites from edible mushrooms, we identified four of biocatalytic conversions, the general equation for all of highly oxygenated cuparene-type sesquiterpenes, these reactions may be summarized as RH + NAD(P)H + + ® + enokipodins A-D (compounds 1-4), from F. velutipes H +O2 ROH + NAD(P) +H2O (van den Brink et al., (Ishikawa et al., 2000, 2001). Enokipodins A-D demon- 1998). The presence of a quaternary carbon stereocenter on strated antimicrobial activity against the fungus the cyclopentane ring has made enokipodins A-D attractive Cladosporium herbarum (Ishikawa et al., 2000, 2001) and synthetic targets. However, considering the absence of bio- the Gram-positive bacteria Bacillus subtilis and Staphylo- synthetic studies involving these sesquiterpenes, the aim of coccus aureus (Ishikawa et al., 2005). Following our re- the present study was to trap the biosynthetic intermediates port, several research groups synthesized these compounds of highly oxygenated cuparene-type sesquiterpenes of F. (Srikrishna and Rao, 2004, Saito and Kuwahara, 2005, velutipes using cytochrome P450 inhibitors. Send correspondence to N.K. Ishikawa. Coordenação de Biodiversidade, Instituto Nacional de Pesquisas da Amazônia, Av. André Araújo 2936, 69067-375 Manaus, AM, Brazil. E-mail: [email protected]. 1286 Ishikawa et al. Materials and Methods -2, respectively. The fractions containing B-1 were purified by TLC using hexane-EtOAc (20:1) as a mobile phase to General notes obtain compound 5 (6.1 mg). Those fractions containing Merck Kieselgel 60 F254, 0.25-mm thick TLC plates B-2 were purified by preparative TLC using toluene-ace- were used to purify the metabolites, while the spots were tone (15:1) and hexane-EtOAc (3:1) to give compounds 6 1 viewed under UV light (254 and 365 nm). IR spectra were and 7 (14.0 mg) as a 3.7:1 mixture of epimers ( H-NMR recorded on a PerkinElmer 2000 FTIR, while mass spectra analysis). were recorded on a JEOL JMS-SX 102 mass spectrometer. Compound 5 1H- and 13C-NMR as well as 2D-NMR spectra were re- corded on a Bruker AMX-500 spectrometer. Conformation M.p.: 68-75 °C (lit. 72-73 °C) (Matsuo et al., 1977). 24 analysis was assisted by MM2 calculations using the [a]D : -7º (c 0.01, CHCl3), +10º for (R)-enantiomer ChemBio3D molecular modeling program in ChemOffice (Matsuo et al., 1977). IR max (film) 2959, 1642, 1370 cm-1. (CambridgeSoft). EIMS m/z (rel. int.): 233 (M+1+, 6), 232 (M+, 36), 217 (M+-15, 32), 202 (8), 189 (43), 164 (100), 150 (34), 149 Cultivation of the fungus (19), 137 (18), 95 (22), and 69 (28). HREIMS m/z 232.1486 1 13 Flammulina velutipes (Fv-4) was cultivated in a (C15H20O2 requires 232.1464). For H and C spectral anal- 300 mL volume in 22 Erlenmeyer flasks containing 100 mL ysis, see Table 1. of malt peptone broth (3% Difco malt extract and 0.3% A 3.7:1 mixture of compounds 6 and 7 Merck peptone in distilled water, pH 4.5; the medium was 24 sterilized by autoclaving at 121 °C for 15 min). Each flask [a]D : -61º (c 0.01, CHCl3), IR max (film) 3445, was inoculated with five disks (7 mm i.d.) of freshly grown 1645 cm-1. EIMS m/z (rel. int.): 237 (M++1, 9), 237 (M+, mycelia on malt agar plates, and cultured for 30 days at 50), 218 (M+-H2O, 16), 203 (15), 180 (34), 135 (38), 121 25 °C under stationary conditions. (52), 109 (100), 91 (77), 79 (40), and 43 (81). HREIMS m/z 1 13 236.1770, (C15H24O2 requires 236.1772). For H and C Incubation with cytochrome P450 inhibitors spectral analyses of the major diastereomer compound 6, On day 20 of fermentation,a1mMethanolic solution see Table 2. (1 mL) of each inhibitor was passed through a Millipore membrane filter (0.22 nm pore size) and added to two flasks Compound 7 1 under aseptic conditions. To investigate the mechanism of H NMR (CDCl3, 500 MHz): (Apparent signals were enokipodin oxygenation, the fungus was inoculated with selected.) 1.97 (1H,ddd, Hb-2), 2.10 (1H, ddd, Ha-2), 2.42 nine cytochrome P450 inhibitors: 1-aminobenzotriazole, (1H, dddd, Ha-1), 2.59 (1H, ddd, Hb-1), 3.63 (1H, s, OH), a-naphthoflavone, ancymidol, 1-benzylimidazole, chloro- 13 6.00 (1H, d, H-5). C NMR d (CDCl3, 125 MHz) 19.3, choline chloride, ketoconazole, miconazole, SKF-525A, 22.3, 24.0, 24.9, 26.3, 27.8, 35.7, 36.7, 40.6, 44.6, 52.7, and xanthotoxin. Of these, 1-aminobenzotriazole produced 72.3, 122.2, 172.6, and 202.7. three less highly oxygenated metabolites (compounds 5-7). The carbon atoms in compounds 5-7 were numbered on the Results and Discussion basis of biosynthetic considerations. Two flasks inoculated with ethanol (1 mL each) and two uninoculated flasks were 1-Aminobenzotriazole inhibited the biosynthesis of used as a negative control. Fermentation was carried out at enokipodins A-D (1-4) to produce two less-highly oxygen- 25 °C for an additional 10 days. The mycelia were filtered, ated metabolites (compounds 5-7) by inhibiting the activity washed with water and ethyl acetate (EtOAc), and the broth of the fungal cytochrome P450 enzymes. thus obtained was extracted with EtOAc (600 mL each). The EIMS of compound 5 showed a molecular ion The extracts were concentrated in a vacuum and the crude peak at m/z 232, which was confirmed by recording the extracts thus obtained were spotted on TLC plates in paral- FDMS. HREIMS of the metabolite showed the precise mo- lel with an aliquot of enokipodins A-D as references. The lecular mass to be 232.1486, corresponding to the molecu- analysis suggested that 1-aminobenzotriazole produced lar formula C15H20O2, and hence proved that the compound two less-polar new spots (B-1 and -2). In this test, the Rf contained one less oxygen and two more protons than 1 13 values using toluene-acetone (4:1), in order of polarity, enokipodin B. The H-NMR, C-NMR, and HMQC spec- were: enokipodin C (Rf 0.09), enokipodin D (Rf 0.23), tra of compound 5 exhibited the presence of four methyl, compound B-2 (Rf 0.30), enokipodin A (Rf 0.43), enoki- three methylene, two methane, and six quaternary carbons. podin B (Rf 0.75), and compound B-1 (Rf 0.87). The exper- Two quaternary carbons resonated at d 188.2 and 188.5 due iment was therefore scaled up to 5 L and repeated using to the carbonyls of the quinone moiety. A quaternary ole- 1-aminobenzotriazole. Part (567 mg) of the gum (810 mg) finic and an olefinic methine carbon were featured at d thus obtained was chromatographed on a silica gel (tolu- 143.6 and 135.5, respectively. Assignments of all proton ene: acetone = 6:1) to give two fractions containing B-1 and and carbon signals were made based on HMQC, HMBC, Studies of enokipodin biosynthesis 1287 1 13 Table 1 - H and C NMR spectral data of compound 5 in CDCl3.
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