2Z,6E

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All creatures have a number of enzymes to transform materials for carrying out .... The nuclear magnetic resonance(NMR) ... The acidic fraction was reacted with ethereal CH2N2 .... we concluded that the structure of the novel compound 5.
Journal of Oleo Science Copyright ©2013 by Japan Oil Chemists’ Society J. Oleo Sci. 62, (5) 313-318 (2013)

Novel Compound, (2Z,6E)-1-Hydroxy-3,7-dimethyl-2,6octadien-8-oic Acid Produced from Biotransformation of Nerol by Spodoptera litura Larvae Toshirou Ono1, Satoshi Koutari1, Shinsuke Marumoto2 and Mitsuo Miyazawa1* 1 2

Department of Applied Chemistry, Faculty of Science and Engineering, Kinki University (Kowakae, Higashiosaka-shi, Osaka 577-8502, Japan) Research Institute for Sustainable Humanosphere, Kyoto University (Gokasho, Uji-shi, Kyoto 611-0011, Japan)

Abstract: Biotransformation of nerol by larvae of the common cutworm (Spodoptera litura) was investigated. The resulting major metabolites were (2Z,6E)-1-hydroxy-3,7-dimethyl-2,6-octadien-8-oic acid and 8-hydroxynerol, and the minor metabolites were 9-hydroxynerol and (2Z,6E)-1-hydroxy-3,7-dimethyl-2,6octadien-8-al. (2Z,6E)-1-Hydroxy-3,7-dimethyl-2,6-octadien-8-oic acid is a novel compound. The results indicate that biotransformation of nerol by S. litura larvae involved 2 pathways; the main pathway involved oxidation at the methyl group of the geminal dimethyl at C-8 position followed by carboxylation, and the minor pathway involved oxidation at the methyl group of the geminal dimethyl at C-9 position. Key words: biotransformation, nerol, Spodoptera litura, oxidation 1 Introduction Terpenoids are used as raw materials for flavor and fragrance and as biologically active substances. The majority of biologically active terpenoids are produced as secondary metabolites from plants, and these terpenoids have been shown to be biological active against plants, microorganisms, and insects1). However, very few reports have focused on the natural metabolic mechanisms of terpenoids. All creatures have a number of enzymes to transform materials for carrying out important life processes or for adapting to an environment. Biotranformations often involve regioselective and stereoselective reactions under mild conditions that produce optically active compounds, which enables the synthesis of complex products. Various attempts have been made to identify new biologically active terpenoids. Increasingly, research has been focused on biotransformation of monoterpenoids, which is performed by bacteria, fungi, yeasts, and even algae2, 3). However, few reports in the literature have focused on the biotransformation of terpenoids by lepidopteran insects. The reasons for using the larvae of Spodoptera litura, a lepidopteran, as a biological catalyst are as follows:(1)lepidopteran larvae naturally feed on plants containing terpenoids, due to which the larvae have high enzymatic activity against terpenoids; (2) these larvae consume a large amount of plants, which enhances the amount of metabolites obtained; and(3)the

larvae are easy to rear at the laboratory scale. Nerol(1)is one of the oldest known monoterpenoids. Compound 1 is a general terpenoid and is contained in various plants such as Cymbopogon flexuosus, Wisteria brachybotrys, and Rosa damascaena3−5). The biotransformation of 1 in plants, microorganisms, and mammals has been previously published6−23). In addition, we have reported the biotransformation of acyclic monoterpenes by the larvae of the common cutworm(S. litura)24−27). β -Myrcene was oxidized at the 3,10-double bond and 1,2-Dihydromyrdouble bond by the larvae of S. litura24).(−) cenol and(−)-dihydromyrcenyl acetate were oxidized at the 1,2-double bond and C-3 position by the larvae of S. -Citronellene and(−) -citronellene were oxilitura25).(+) dized at the 1,2-double bond and 6,7-double bond by the larvae of S. litura26). These results indicate that the double bonds were preferentially oxidized. In addition, geraniol was oxidized at the C-1 and C-8 positions by the larvae of S. litura27), indicating that the trans positions were preferentially oxidized. In this study, biotransformation of 1 by the larvae of S. litura was investigated to determine the metabolic pathways in insects.



Correspondence to: Mitsuo Miyazawa, Department of Applied Chemistry, Faculty of Science and Engineering, Kinki University, Kowakae, Higashiosaka-shi, Osaka 577-8502, Japan E-mail: [email protected]. Accepted December 28, 2012 (received for review November 30, 2012)

Journal of Oleo Science ISSN 1345-8957 print / ISSN 1347-3352 online

http://www.jstage.jst.go.jp/browse/jos/  http://mc.manusriptcentral.com/jjocs 313

T. Ono, S. Koutari, S. Marumoto et al.

2 Experimental 2.1 Materials Nerol(1)was purchased from Fluka (Tokyo, Japan) . 2.2 General experimental procedures Gas chromatography( GC)was performed using a Hewlett-Packard 5890A gas chromatograph equipped with a flame ionization detector and a fused silica capillary column(DB-5, 30 m length, 0.25 mm i.d.). The chromatographic conditions were as follows: oven temperature was programmed to increase from 80℃ to 270℃ at a rate of 4℃/min; the injector and detector temperatures were 270℃ and 280℃, respectively; split injection of 25:1; and the flow rate of helium gas was 30.0 cm/s. Electron impactmass spectrometry(EI-MS)measurements were obtained using GC-MS. GC-MS was performed using a Hewlett-Packard 5972A mass selective detector and a Hewlett-Packard 5890A gas chromatograph fitted with a capillary column . The chromatograph(HP-5MS, 30 m length, 0.25 mm i.d.) ic conditions were the same as described above. The temperature of the ion source was 230℃, and the electron energy was 70 eV. The infrared(IR)spectra were obtained using a JASCO FT/IR-470-plus Fourier transform infrared spectrometer. The nuclear magnetic resonance( NMR) spectra were obtained using a JEOL FX-500 spectrometer (500 MHz for 1H, 125 MHz for 13C). Tetramethylsilane (TMS)was used as the internal standard in CDCl3. Multiplicities were determined by the distorsionless enhancement by polarization transfer(DEPT)pulse sequence. The specific rotations were measured using a JASCO DIP-1000 digital polarimeter. 2.3 Rearing of larvae The larvae of S. litura were reared in plastic cases (width, 200×300 mm; height, 100 mm; 100 larvae/case) covered with a nylon mesh screen. The rearing conditions were as follows: 25℃, 70% relative humidity, and constant light. The larvae were fed a commercial diet(Insecta LSF; Nihon Nosan Kogyo Co., Ltd. Japan)from the 1st instar. From the 4th instar, the diet was changed to an artificial diet composed of kidney beans(100 g), agar(15 g), and water (600 mL)28). 2.4 Administration of substrate The artificial diet without agar was mixed in a blender. Compound 1(2.2 g)was then directly added into the blender at 3 mg/g of diet. After the agar was dissolved in water, it was boiled and then added into the blender. The diet was then mixed and cooled in a stainless steel tray (width, 220×310 mm; height, 30 mm). The 4th and 5th instar larvae(average weight=0.5 g) were moved into new cases(100 larvae/case), and the larvae were provided a limited amount of food. Groups of 800 larvae were fed the diet containing 1(1.8 g, approximately 2.2 mg/body)for 2

days, and then the artificial diet without 1 for an additional 2 days. The frass collected every 5 h for the 4 days was stored in a solution of diethyl ether (300 mL). To separate the diet and frass, fresh frass was extracted as soon as the fourth and fifth instar larvae excreted. GC analysis using the substrate as an internal standard was performed to quantitatively assess the metabolites. 2.5 Isolation and identification of metabolites from frass The frass was extracted with diethyl ether( 300 mL, twice)and then ethylacetate(300 mL, twice). The extract solution was collected and evaporated under reduced pressure, and 3.1 g of extract was thus obtained. The extract was dissolved in ethyl acetate, and then added to 5% NaHCO3 solution. After shaking, the neutral fraction(1598 mg)was obtained from the ethylacetate layer. The aqueous layer was separated, acidified with 1N HCl (acidic fraction) , and extracted with ethyl acetate. After shaking, the acidic fraction(1120 mg)was obtained from the aqueous layer. Both fractions were analyzed using GC-MS; compounds 2, 3, and 4 were isolated in the neutral fraction, and compound 5 was isolated from the acidic fraction. The neutral fraction was subjected to silica gel open-column chromatography( silica gel 60, 230-400 mesh; Merck)with a hexane/ethyl acetate gradient(9:1-1:1)system; 3 compounds were isolated: 2(563 mg), 3(176 mg), and 4(70 mg). The acidic fraction was reacted with ethereal CH2N2 overnight, and then C5H5N and(CH3CO)2O overnight, and subsequently examined via GC-MS. The results revealed the presence of acetylated and methylated 5 (5AcMe) . The fraction was subjected to silica gel open-column chromatography(silica gel 60, 230-400 mesh; Merck)by using a hexane/diethyl ether gradient(9:1-1:1)system, and the compound 5AcMe(510 mg)was isolated. The metabolic compounds from the frass were identified by comparing established MS, IR, and NMR data6, 21). 2.6 Structure of Metabolic Products 8-hydroxynerol(2): colorless oil. EI-MS, m/z(%) (rel. (1), 121(10), 68(64), 67(61), 55(24), int.): 152[M-H2O]+ 43( 100), 41( 65). IR(KBr)ν max cm −1: 3324, 2924, 1446, 1003. 1H-NMR(500 MHz, CDCl3): δ 1.65(3H, brd, J=1.15 Hz, H-9) , 1.76(3H, q, J=1.45 Hz, H-10), 2.13-2.16 (4H, m, , 4.07(2H, dd, J=0.9 7.5 Hz, H-1), H-4), 3.98(2H, brs, H-8) 5.40 (1H, m, H-6) , 5.43 (1H, qt, J=1.5, 7.5 Hz, H-2) . 13C-NMR shown as Table 1. 9-hydroxynerol(3): Colorless oil. EI-MS, m/z(%) (rel. (1), 119(10), 84(42), 68(51), 67(45), int.): 152[M-H2O]+ 55(29), 43(100), 41(72). IR(KBr)νmax cm−1: 3324, 2925, : δ 1.75(3H, brd, J= 1447, 1001. 1H-NMR(500 MHz, CDCl3) 1.1 Hz, H-10) , 1.80 (3H, brd, J=0.5 Hz, H-8) , 2.12-2.17 (4H, , m, H-4, 5), 4.07(2H, d, J=8.0 Hz, H-1), 4.08(2H, s, H-9) 5.30(1H, brdt, J=0.5, 6.3 Hz, H-6), 5.47(1H, brdt, J=1.1, 8.0 Hz, H-2). 13C-NMR shown as Table 1.

314

J. Oleo Sci. 62, (5) 313-318 (2013)

Novel Compoud, (2Z,6E)-1-Hydoroxy-3,7-dimethyl-2,6-octadien-8-oic Acid Produced from Biotransformation of Nerol by Spodoptera litura Larvae

Table 1 13C-NMR spectral data for metabolites 1-5 (125 MHz, CDCl3)a. compounds

carbon

1

2

3

4

5

5AcMe

1

58.9 (t)

58.9 (t)

58.9 (t)

58.8 (s)

60.5 (s)

60.7 (s)

2

124.3 (d)

124.8 (d)

124.7 (d)

125.4 (d)

119.8 (d)

120.0 (d)

3

139.9 (s)

138.6 (s)

139.6 (s)

138.3 (s)

141.4 (s)

141.3 (s)

4

31.9 (t)

31.3 (t)

32.0 (t)

30.4 (t)

30.8 (t)

30.7 (t)

5

26.5 (t)

25.3 (t)

26.0 (t)

27.4 (t)

27.2 (t)

27.1 (t)

6

123.7 (d)

125.0 (d)

127.5 (d)

153.2 (d)

140.7 (d)

141.0 (d)

7

132.4 (s)

135.6 (s)

135.5 (s)

139.7 (s)

127.8 (s)

128.1 (s)

8

25.6 (q)

68.6 (t)

21.3 (q)

195.1 (t)

168.2 (t)

168.4 (t)

9

17.6 (q)

13.7 (q)

61.3 (t)

9.2 (q)

12.4 (q)

12.3 (q)

10

23.3 (q)

23.3 (q)

23.5 (q)

23.2 (q)

23.2 (q)

21.0 (q)

1-COMe

171.0 (s)

8-COOMe a

23.3 (q)

1-COMe

51.7 (q) 13

NMR spectra were recoded at 125 MHz ( C) in CDCl3 solution using TMS as an internal standard.

(2Z,6E)-1-hydroxy-3,7-dimethyl-2,6-octadien-8-al(4): (1), 150 Colorless oil. EI-MS, m/z(%) (rel. int.): 168[M]+ (8), 97(33), 84(94), 67(22), 55(50), 41(100). IR(KBr) (500 MHz, νmax cm−1: 3396, 2926, 1684, 1644, 1004. 1H-NMR (3H, brd, J=1.2 Hz, H-9) , 1.78 (3H, brd, J= CDCl3): δ 1.75 1.2 Hz, H-10), 2.28(2H, brt, J=7.5 Hz, H-4) , 2.44-2.49 (2H, m, H-5) , 4.14(2H, brd, J=7.2 Hz, H-1) , 5.50 (1H, brt, J= , 9.39 (1H, s, 7.2 Hz, H-2), 6.46(1H, qt, J=1.2, 7.3 Hz, H-6) H-8) . 13C-NMR shown as Table 1. (2Z,6E)-1-hydroxy-3,7-dimethyl-2,6-octadien-8-oic acid + (5) : colorless oil. EI-MS, m/z (%) (rel. int.) : 166 [M-H2O] (1) , 154 (7), 136 (33) , 121 (34) , 107 (11) , 93 (100) , 80(71), 69(81), 55(26), 41(49). IR(KBr)νmax cm−1: 2400-3500, 2926, 1686, 1646. 1H-NMR(500 MHz, CDCl3): δ 1.78(3H, brd, J=0.6 Hz, H-10) , 1.83 (3H, brd, J=1.1 Hz, H-9), 2.212.25 (2H, m, J=6.9 Hz, H-4) , 2.26-2.31 (2H, m, J=6.7, 6.9 Hz, H-5), 4.14 (2H, brd, J=7.5 Hz, H-1) , 5.40 (1H, brt, J= 0.6, 7.5 Hz, H-2), 6.72( 1H, brdt, J=1.1, 6.7 Hz, H-6). 13 C-NMR shown as Table 1. (2Z,6E)-1-acetoxy-3,7-dimethyl-2,6-octadien-8-oic acid methyl ester(5AcMe): colorless oil. EI-MS, m/z(%) (rel. + + (1), 198[M-COCH3] (1), 180(4), 165(8), int.): 240[M] 121(64), 114(78), 83(72), 82(93), 55(60), 53(52), 41 (63). IR (KBr)νmax cm−1: 2951, 1715, 1651, 1269, (100), 39 1235. 1H-NMR(500 MHz, CDCl3): δ 1.78(3H, brd, J=0.6 Hz, H-10), 1.83( 3H, brd, J=1.1 Hz, H-9), 2.05( 3H, s, 1-COMe), 2.21-2.25(2H, m, H-4), 2.26-2.31(2H, m, H-5), 3.73 (3H, s, 8-COOMe) , 4.55 (2H, brd, J=7.5 Hz, H-1) , 5.40 (1H, brt, J=0.6, 7.5 Hz, H-2), 6.72(1H, brdt, J=1.1, 6.7 Hz, H-6) . 13C-NMR shown as Table 1.

3 Results and Discussion We observed biotransformation by the larvae of S. litura by administering the substrate(1) to the larvae in their diet and then detecting and isolating the metabolites from the frass of the larvae. The frass extracts were analyzed via GC, and the larvae that were fed the substrate-free diet were used as the control. The results demonstrated that metabolites were not observed in the frass of the controls. In the biotransformation of 1, the 4 metabolites isolated from the frass were identified as metabolites 2, 3, 4 and methylated and acetylated metabolite 5(5AcMe)by spectral studies (Scheme 1) . Metabolite 5 was obtained by the hydrolysis of 5AcMe. The structure of metabolite 2 was determined by interpretation of the 1H-NMR, 13C-NMR, and mass spectra and comparison to reported data6, 21). Metabolite 3 had a molecular formula of C10H18O2 based on its EI-MS spectra, and the IR spectrum revealed a hydroxyl band at 3324 cm −1. The 1H- and 13C-NMR spectra were similar to that of the substrate, except for C-9 (Table 1) .The NOESY spectrum indicated a correlation cross-peak that was observed between H-6(5.30 ppm)and H-8(1.80 ppm) . In the characteristic HMBC spectrum, a correlation cross-peak was observed on C-6( 127.5 ppm)with one methyl group(1.80 ppm; H-8)and a new methylene group (4.08 ppm; H-9) . From these data, we concluded that the structure of 3 is 9-hydroxynerol. This is the first report revealing the spectral data of 3. Metabolite 4 had a molecular formula of C10H16O2 based on its EI-MS spectra, and the IR spectrum revealed a hydroxyl band at 3396 cm−1 and a carbonyl band at 1684 cm−1. 315

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The 1H- and 13C-NMR spectra were similar to that of the substrate, except for C-8(Table 1). In the characteristic HMBC spectrum, a correlation cross-peak was observed on C-8 (195.1 ppm)with one methyl group (1.75 ppm, H-9) and methine group(6.46 ppm, H-6). The NOESY spectrum indicated a cross-peak that was observed between H-6(6.46 ppm)and H-8(9.39 ppm). From these data, we concluded that the structure of 4 is(2Z,6E)-1-hydroxy-3,7-dimethyl-2,6-octadien-8-al. The structure of metabolite 4 was determined by interpretation of the IR and mass spectra and by comparison to reported data21). The IR spectrum of metabolite 5 showed carbonyl bands at 1738 and 1715 cm−1. The EI-MS spectra showed a significant mass fragment[M-H 2O]+ at m/z 166. The 1H- and 13 C-NMR spectra of 5AcMe were similar to that of the substrate, except for C-8, monoacetate, and methyl ester (Table 1). In the characteristic HMBC spectrum, a crosspeak was observed on C-8(168.4 ppm)with one methyl group (1.83 ppm, H-9) and methine group (6.72 ppm, H-6) . The NOESY spectrum demonstrated a cross-peak between H-5(2.26-2.31 ppm)and H-9(1.83 ppm). From these data, we concluded that the structure of the novel compound 5 is(2Z,6E)-1-hydroxy-3,7-dimethyl-2,6-octadien-8-oic acid. The iridoid and secoiridoid esters of 5 have been previously isolated from Menyanthes thifoliata and Vinca rosea29−31). In the biotransformation of 1, the larvae transformed 1

to 2(14%), 3 (36%), 4 (10%), and 5(36%; Table 2). The results of the biotransformation of 1 revealed the oxidation steps in the main metabolic pathway (1→2→4→5; Scheme 1). Similarly, oxidation at the C-9 position demonstrated the minor metabolic pathway(1→3; Scheme 1). We have previously revealed the biotransformation of geraniol(a nerol isomer)by the larvae of S. litura27). In that study, geraniol was oxidized at C-1 (primary alcohol), but nerol did not undergo similar oxidation in the present study. In this study, C-8(trans allylic position)was preferentially oxidized by S. litura larvae. A previous paper described the participation of S. litura intestinal bacteria in the metabolism of α-terpinene23). The aerobically active intestinal bacteria transformed α-terpinene to p-mentha-1,3-dien-7-ol, and the anaerobically active intestinal bacteria transformed α-terpinene to p-cymene. In the present study, the in vitro metabolism of 1 by intestinal bacteria was also examined in a manner similar to that of the previous paper. However, in our investigation, 1 was not metabolized by these intestinal bacteria (no reaction). These results suggest that the intestinal bacteria did not participate in the metabolism of 1. There have been some reports of biotransformation of 1 by other organisms. Oxidation at the C-8 position(allylic methyl groups)is the main metabolic pathway in the biotransformation of 1 by suspension-cultured cells of Cath-

Table 2 Recovery and yield of metabolites 1-5 obtained from S. litura larvaea. substrate

substrate in the artificial diet (g)

metaboliteb (g)

yieldc (%)

recovery (%) 1

nerol (1)

1.8

2.3

82.2

d

14

2

3

4

5

36

10

4

36

a

Metabolites were obtained from the frass of S. litura larvae. b Caluculated from the peak area on the GC used as aninternal standard (nerol). c Percentage estimated on GC. d Recovered substrate.

Scheme 1 Biotransformation of nerol (1) by the larvae of S. litura. 316

J. Oleo Sci. 62, (5) 313-318 (2013)

Novel Compoud, (2Z,6E)-1-Hydoroxy-3,7-dimethyl-2,6-octadien-8-oic Acid Produced from Biotransformation of Nerol by Spodoptera litura Larvae

aranthus roseus6). However, this biotransformation did not progress to yield a carboxylic acid. In the biotransformation of 1 by microorganisms, oxidations of the primary alcohol group to aldehyde and hydroxylation at C-8 band C-9 positions have been reported21−23). However, these biotransformations did not progress to the carboxylic acid stage. In contrast, carboxylic acid was obtained from 1 during biotransformation by the larvae of S. litura. This reaction rarely occurred in other biocatalysis reactions. Therefore, the metabolic pathway of the S. litura larvae is the only metabolic pathway involved in the metabolism of 1. In conclusion, the larvae of S. litura transformed 1 to 4 compounds 2, 3, 4, and 5. Compound 5 has not been previously reported. These results suggest that regioselective oxidation occurred in the metabolism of 1 by the larvae of S. litura. In this case, compound 1 was oxidized at the methyl group of the geminal dimethyl. These results indicate that the larvae of S. litura recognized the methyl groups and the C-8 position of compound 1 with high efficiency.

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