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A New Benzoquinone and a New Benzofuran from the Edible

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A New Benzoquinone and a New Benzofuran from the Edible Food Chemistry 141 (2013) 1614–1618 Contents lists available at SciVerse ScienceDirect Food Chemistry journal homepage: www.elsevier.com/locate/foodchem A new benzoquinone and a new benzofuran from the edible mushroom Neolentinus lepideus and their inhibitory activity in NO production inhibition assay ⇑ ⇑ Yongxia Li a,b,1, Li Bao a,1, Bin Song c, Junjie Han b, Heran Li b, , Feng Zhao d, Hongwei Liu a, a State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, No. 9, Beiertiao, Zhongguancun, Haidian District, Beijing 100190, People’s Republic of China b College of Pharmacy, Soochow University, No. 199, Ren Ai Rd., Suzhou Industrial Park, Suzhou, People’s Republic of China c Guangdong Institute of Microbiology, Guangdong Academy of Sciences, No. 100, Xianlie Road, Yuexiu District, Guangdong 510070, People’s Republic of China d School of Pharmacy, Yantai University, No. 32, Qingquan Road, Laishan District, Yantai 264005, People’s Republic of China article info abstract Article history: The fruiting bodies or mycelia of mushrooms have been used as food and food-flavoring material for cen- Received 16 October 2012 turies due to their nutritional and medicinal value and the diversity of their bioactive components. The Received in revised form 21 February 2013 present research is the first to investigate the bioactive secondary metabolites from the solid culture of Accepted 30 April 2013 the edible mushroom Neolentinus lepideus. Two new secondary metabolites, 5-methoxyisobenzofuran- Available online 23 May 2013 4,7(1H,3H)-dione (1) and 1,3-dihydroisobenzofuran-4,6-diol (2), as well as seven known compounds including one benzoquinone derivative (3) and six cinnamic acid derivatives (4–9) were obtained. Their Keywords: structures were established by means of spectroscopic methods, including 1D and 2D NMR. The bioactiv- Neolentinus lepideus ity on the nitric oxide production in lipopolysaccharide-induced macrophages was evaluated for all Structure elucidation NO inhibition metabolites (1–9) isolated. Compound 1 showed strong NO inhibitory activity with the IC50 value of Antioxidation 6.2 lM. Compound 2 displayed moderate NO inhibitory activity with the IC50 value of 88.8 lM. In the DPPH scavenging assay, compound 2 displayed antioxidant activity with IC50 of 68.6 lM. The discovery of new NO production inhibitors from N. lepideus expands its usage as a functional food. Ó 2013 Elsevier Ltd. All rights reserved. 1. Introduction extracts from the fruiting bodies of L. lepideus has been confirmed to contain antihyperlipidemic (Yoon, Lee, et al., 2011), antioxidant Mushrooms have attracted much more attention as functional (Yoon, Alam, et al., 2011), antityrosinase (Yoon, Alam, et al., 2011), foods or physiologically beneficial medicine due to their nutritional and immunomodulating activities (Jung et al., 2008). A number of and medicinal value and the diversity of their bioactive secondary secondary metabolites including a-copaene, a-elemene, metabolites (Barro, Baptista, Estevinho, & Ferreira, 2007; Barros b-farnesene, a-and c-muurolene, d-cadinene, cadina-1,4-diene, et al., 2007). The technique of solid state fermentation (SSF) refers a-calacorene, (À)-torreyol, (À)-T-muurolol, (+)-Tcadinol, a-cadinol, to microbial growth on moist solid medium without free water. cubenol, epicubenol, farneso and drimenol, lentideusether, The traditional Japanese food ‘‘natto’’ (Bacillus-fermented soybean) isolentideusether and 10-hydroxy-lentideusether have been and the Chinese food ‘‘anka’’ (Monascus-fermented rice) were isolated from the fruiting bodies of the basidiomycete L. lepideus produced by this method. Our early studies on edible mushroom (Hanssen, 1982, 1985). In the current research, we reported the iso- showed that mushrooms fermented with this technique could lation of one new benzoquinone (1), one new benzofuran (2), as well enhance their ability in production of the bioactive secondary as seven known secondary metabolites including benzoquinone metabolites (Wang, Bao, Liu, et al., 2012; Wang, Bao, Yang, Dai, derivative (3) and six known cinnamic acid derivatives from the et al., 2012; Wang, Bao, Yang, Li, et al., 2012; Wang, Li, et al., solid culture of N. lepideus fermented on cooked rice. Their chemical 2012; Wang et al., 2013). structures (Fig. 1) were elucidated by their physicochemical proper- Neolentinus lepideus is a basidiomycete mushroom of the genus ties and spectral data, including 1D, 2D NMR and HRESI-MS. Neolentinus, previously well known as Lentinus lepideus. It is one of the popular edible mushroom in China, Japan and Korea. The 2. Materials and methods 2.1. General methods ⇑ Corresponding authors. Tel.: +86 512 65882541 (H. Li), tel.: +86 10 62566577 (H. Liu). E-mail addresses: [email protected] (H. Li), [email protected] (H. Liu). UV data were recorded on a Shimadzu Biospec-1601 spectro- 1 These authors contributed equally to this work. photometer. IR data were recorded using a Nicolet Magna-IR 750 0308-8146/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.foodchem.2013.04.133 Y. Li et al. / Food Chemistry 141 (2013) 1614–1618 1615 (Fr. 2–1–Fr. 2–10). Fr. 2–3 (50 mg) was separated by ODS column using a gradient of methanol–water (20–100%) to afford 9 (22 mg). Fr. 2–5 (80 mg) was separated by ODS column eluted with 200 ml of methanol–water (50%, v/v) followed by HPLC using 29% acetonitrile in water to afford 3 (12 mg, tR 14.92 min). Compounds 4 (2 mg, tR 15.65 min), 7 (2 mg, tR 18.61 min), and 8 (40 mg, tR 15.23 min) were obtained from subfraction 2–8 (70 mg) by HPLC purification using 49% methanol in water. Fr. 3 (100 mg) eluted with dichloromethane–acetone (75:1, v/v) was separated by ODS column using a gradient of methanol–water (20–100%) to give se- ven subfractions (Fr. 3–1–Fr. 3–7). Fr. 3–4 (33 mg) was purified by HPLC using 40% methanol in water to afford 5 (3.8 mg, tR 23.78 min) and 6 (5 mg, tR 28.25 min). Fr. 5 (556 mg) eluted with dichloromethane–acetone (20:1, v/v) was separated by ODS col- umn using a gradient methanol (20–100%) in water to afford thir- teen subfractions (Fr. 5–1–Fr. 5–13). Fr. 5–3 (35 mg) was subjected to a silica gel column eluted with 200 ml of dichloromethane– Fig. 1. Secondary metabolites isolated from Neolentinus lepideus. acetone (90:1, v/v) to give compound 1 (12 mg). Fr. 10 (460 mg) spectrophotometer. ESIMS and HRESIMS data were obtained using eluted with dichloromethane–methanol (20:1, v/v) was first a Bruker APEX III 7.0 T spectrometer. 1H and 13C NMR, along with separated by ODS column using a gradient of methanol–water 2D NMR spectra were acquired with Bruker AV-500 NMR spec- (20–100%) to afford 11 subfractions (Fr. 10–1–Fr. 10–11). Compound 2 (3.2 mg, t 22.1 min) was isolated from subfraction trometer, using (methanol-d4: dH 3.33/dC 49.9; deuterated chloro- R 10–4 (18 mg) by HPLC using 22% methanol in water. The other form: dH 7.26/dC 77.7) as references. The HMQC and HMBC experiments were optimised for 145.0 and 8.0 Hz, respectively. fractions were all separated during the isolation process. The de- tails of the isolation procedure for other fractions are not described TLC was carried out on Silica gel 60F254 and the spots were visual- since we did not get secondary metabolites from these fractions in ised by spraying with 10% H2SO4 and heating. LH-20 (Amersham Biosciences) and ODS (Lobar, 40–63 lm, Merck) were used for col- this research. umn chromatography. Preparative HPLC was performed on an Agi- lent 1200 HPLC system using an ODS column (RP-8, 250 Â 10 mm, 2.3.2. 5-Methoxyisobenzofuran-4,7(1H,3H)-dione (1) YMC Pak, 5 lm; detector: UV) with a flow rate of 2.5 ml/min. Yellow needle crystalline; UV (methanol) kmax nm (log e): 200 (4.02), 255(3.66), 295 (2.82); IR (neat) mmax: 3413, 2931, 1726, 1641, 1589, 1440, 1408, 1236, 1120, 1039, 892 cmÀ1; Positive HRE- 2.2. Fungal material + 1 SIMS: m/z [M+H] 181.0495 (calcd. for C9H8O4H, 181.0529); H 13 The fungal strain used in this study was isolated from fruiting NMR and C NMR data see Table 1. body of mushroom N. lepideus in Guangdong Province, in October 2004, and was identified by Professor Bin Song. The sequence data 2.3.3. 1,3-Dihydroisobenzofuran-4,6-diol (2) derived from the fungal strain has been submitted and deposited at Colourless oil; UV (methanol) kmax nm (log e): 230 (4.22), 280 GenBank with accession number JX401542. BLAST search result (4.16); IR (neat) mmax: 3260, 1606, 1459, 1340, 1140, 1018, À1 + showed that the sequence was similar (99%) to the sequence of 885 cm ; Positive HRESIMS: m/z [M+H] 153.0548 (calcd. for 1 13 N. lepideus (HM536076.1). The strain is preserved with Guangdong C8H8O3H, 153.0546). H NMR and C NMR data see Table 1. Culture Collection Center, Guangdong Institute of Microbiology with accession number GIMCC 5.195. The fungal strain was cul- 2.4. NO inhibition assay (Qiu et al., 2008) tured on slants of potato dextrose agar at 25 °C for 10 d. Agar plugs were inoculated in 500 ml Erlenmeyer flask containing 120 ml of Mouse monocyte-macrophages RAW 264.7 (ATCC TIB-71) were media (0.4% glucose, 1% malt extract, and 0.4% yeast extract), and purchased from the Chinese Academy of Science. RPMI 1640 the final pH of the media was adjusted to 6.5 before sterilisation, medium, penicillin, streptomycin, and foetal bovine serum were and incubated at 25 °C on a rotary shaker at 170 rpm for 7 d.
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