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Phenylbutanoid derivatives from Croton schiedeanus
Biochemical Systematics and Ecology 33 (2005) 849e854 www.elsevier.com/locate/biochemsyseco
Phenylbutanoid derivatives from Croton schiedeanus P. Puebla a,*, S.X. Correa b, M.F. Guerrero b, A. San Feliciano a a
Departamento de Quı´mica Farmace´utica, Facultad de Farmacia, E-37007 Salamanca, Spain b Departamento de Farmacia, Facultad de Ciencias, Universidad Nacional de Colombia, Bogota´ AA 11430, Colombia Received 30 June 2004; accepted 24 December 2004
Keywords: Croton schiedeanus; Euphorbiaceae; Phenylbutanoids
1. Subject and source Croton schiedeanus Schlecht (Euphorbiaceae) is a tree which grows widely in south and central America. In Colombia it is particularly widespread in the Amazonian and Cundinamarca regions, where it is popularly known as ‘‘almizclillo’’ and used in Folk Medicine for treating hypertension (Correa and Bernal, 1992). The aerial part of C. schiedeanus was collected from the region of Tocaima, Cundinamarca, Colombia, in April 2002. Its identity was confirmed by Dr. Jose´ Luis Ferna´ndez and a voucher specimen deposited under No. 432164 in the Herbarium, Natural Sciences Institute of National University, Colombia.
* Corresponding author. Tel.: C34 23 294528; fax: C34 23 294515. E-mail address: [email protected] (P. Puebla). 0305-1978/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.bse.2004.12.018
850
P. Puebla et al. / Biochemical Systematics and Ecology 33 (2005) 849e854
2. Previous work In a previous work we tested the hypotensive and vasorelaxant effects of aqueous and ethanolic extracts from this plant (Guerrero et al., 2001, 2002a). Other studies showed that the flavonoids isolated from C. schiedeanus also elicit vasorelaxant effects (Guerrero et al., 2002b), and these effects were partially NO/cGMP pathwaydependent (Guerrero et al., 2002c). In a phytochemical report we described the isolation and identification of four diterpenoids with clerodane skeleton and two flavonoids (ayanin and quercetin 3,7dimethyl ether) (Puebla et al., 2003).
3. Present study As part of our study on the chemical constituents of this plant, we report here the isolation and structural characterization of two new phenylbutanoids related to rhododendrol. The dried sample (10 kg) was soaked in 96% EtOH (50 l) at room temperature for three days. The EtOH was removed in vacuo to yield a dark residue (160 g), which was partitioned between CHCl3 and H2O to give CHCl3 soluble fraction (90 g). The CHCl3 extract was further fractionated with aqueous 4% NaOH yielding an acid part (18 g) and a neutral part (65 g). The acid part was separated by flash column chromatography, over silica gel, gradient elution with 0e100% EtOAc/hexane, yielding 7,9-dimethoxyrhododendrol (1) (350 mg) as a brown oil. The neutral part was also separated by flash column chromatography, in similar conditions to afford 2-acetoxy-7,9-dimethoxyrhododendrol (2) (65 mg). The identification of these compounds was carried out by interpretation of its spectral data (IR, HRMS, 1H NMR, 13C NMR, DEPT, COSY, HMQC, HMBC), as well as by comparison of the experimental data with those found in the literature values for rhododendrol and derivatives (Shikishima et al., 2001). The acetylation of (1), using acetic anhydride and pyridine, yielded 2,8-diacetoxy-7,9-dimethoxyrhododendrol (3), which served to confirm the structure proposed (Fig. 1). The absolute configuration at position C-2 for 7,9-dimethoxyrhododendrol (1), was determined by 1H NMR using a chiral auxiliary reagent, following the methodology described by Seco, Quin˜oa´ and Riguera (Seco et al., 2001, 2004), these authors describe a guide for the assignment of the absolute configuration of secondary alcohols, based on the regularity of chemical shift differences (DdRS) between equivalent signals of each diastereoisomer. In this work we used R-MPA and S-MPA (methoxyphenyl acetic acid) as chiral auxiliary reagents to prepare the corresponding diastereomeric esters. The experimental Dd values of those derivatives are represented in Fig. 2, these data are in accordance with an S configuration at C-2 for the natural compound 1. Compound 3 is the acetylated derivative of compound 1, therefore, the configuration at C-2 is the same. Compound 2 presents the same optical rotation sign as 3, which implies an S configuration at C-2.
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P. Puebla et al. / Biochemical Systematics and Ecology 33 (2005) 849e854
OH 6
MeO 7
5
8
4
3
2
1
10
HO
OAc
OAc MeO
MeO
AcO
HO
9
OMe
OMe
OMe
1
2
3
OH
HO
rhododendrol Fig. 1. Phenylbutanoids from Croton schiedeanus.
3.1. Preparation of esters The esters were prepared by treatment of alcohol 1 (0.5 mmol) with the corresponding acid R- or S-MPA (0.5 mmol) in presence of 1,3-dicyclohexylcarbodiimide (DCC) (0.6 mmol) and 4-(dimethylamino)pyridine (DMAP) (catalytic) in CH2Cl2. The reaction mixture was filtered to remove the dicyclohexylurea and the esters were purified by flash chromatography on silica gel using mixtures of hexane/ EtOAc. (2S)-7,9-Dimethoxyrhododendrol (1): IR (film): 3430, 1712, 1612, 1518, 1116 cmÿ1. HR-FABMS: 249.1112 [M C 23] (Calcd for C12H18O4 C Na 249.1102). [a]D Z C11.1 (c Z 0.75 CHCl3). 1H and 13C NMR (CDCl3, 400 MHz): (Tables 1 and 2).
L1= Me-1 ∆δRS=
- 0.11
L2= H-3
H-4
+ 0.21
and
+ 0.32
H-6,10 + 0.22
∆δRSL2>0
∆δRSL1<0 H
H ∆δRS>0 MPA-O ∆δRS<0
MPA-O
H L2 L1
HO
S-configuration Fig. 2. Assignment of the configuration of compound 1 (according Seco et al., 2001).
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P. Puebla et al. / Biochemical Systematics and Ecology 33 (2005) 849e854
Table 1 1 H NMR of compounds 1, 2 and 3 (d in ppm, multiplicity and J in Hz) H
1
2
3
1 2 3
1.23 d 6.2 3.85 m 1.76 m
1.25 d 6.2 4.95 m 1.77 m
1.25 d 6.2 4.98 m 1.84 m
4
2.58 m
2.61 m
6
2.58 ddd 6.7, 9.1, 13.8 2.68 ddd 7.2, 9.0, 13.8 6.24 s
6.39 s
6.41 s
10 OMe-C7,C9 Ac-C2 Ac-C8
6.24 s 3.87 s e e
6.39 s 3.88 s 2.05 s e
6.41 3.80 2.04 2.32
s s s s
(2S)-Acetoxy-7,9-dimethoxyrhododendrol (2): IR (film): 3463, 1730, 1612, 1518, 1461, 1116 cmÿ1. HR-FABMS: 291.1201 [M C 23] (Calcd for C14H20O5 C Na 291.1208). [a]D Z ÿ13.3 (c Z 0.45 CHCl3). 1H and 13C NMR (CDCl3, 400 MHz): (Tables 1 and 2). (2S)-2,8-Diacetoxy-7,9-dimethoxyrhododendrol (3): IR (film): 1764, 1731, 1603, 1509 cmÿ1. [a]D Z ÿ20.1 (c Z 0.12 CHCl3). 1H and 13C NMR (CDCl3, 200 MHz): (Tables 1 and 2).
4. Chemotaxonomic significance The genus Croton comprises about 800 species of trees, shrubs and herbs, distributed in tropical and subtropical regions, and is one of the richest sources of diterpenes with clerodane skeleton (Merritt and Ley, 1992), in addition flavonoids and alkaloids are also commonly found in this genus but, as far as we know, Table 2 13 C NMR of compounds 1, 2 and 3 (d in ppm) C
1
2
3
1 2 3 4 5 6 7 8 9 10 OMe-C7, C9 Ac-C2 Ac-C8
23.6 67.5 41.0 32.3 132.8 105.0 147.0 133.1 147.0 105.0 56.2 e e
20.0 70.4 37.8 32.0 132.5 105.0 146.9 132.9 146.9 105.0 56.2 170.7; 21.3
20.2 70.5 37.6 32.5 126.9 105.0 152.0 140.1 152.0 105.0 56.2 170.8; 21.4 169.0; 20.5
P. Puebla et al. / Biochemical Systematics and Ecology 33 (2005) 849e854
853
phenylbutanoids have not been reported before in Croton, and the compounds 1 and 2 are new natural products. Phenylbutanoids occur in several species of different genus, particularly in genera Betula (Pan and Lundgren, 1994; Santamour and Lundgren, 1997; Fuchino et al., 1995, 1996, 1998), Rheum (Abe et al., 2001; Shikishima et al., 2001), Taxus (Chu et al., 1994; Rao and Johnson, 1998), Chrysanthemum (Matsuda et al., 2002), Rhododendron (Das et al., 1993), Acer (Morikawa et al., 2003), Alpinia (Kikuzaki et al., 2001), Zingiber (Nugroho et al., 1996) and Hypochoeris (Ohmura et al., 1989). A mechanism for the formation of this type of compounds was proposed for Abe et al. (2001), according to these authors the benzalacetone synthase (BAS) catalyzes a one step decarboxylative condensation of 4-coumaroyl-CoA with malonyl-CoA to produce the C6eC4 skeleton of phenylbutanoids in higher plants. Acknowledgements This work was supported by the EC project ALFA-RELAPLAMED.2 (Network1233), the Iberoamerican Program of Science and Technology for Development, (CYTED), Subprogram X, Departamento de Farmacia, Universidad Nacional de Colombia and MCYT-SPAIN (SAF-2001-0037-004-04).
References Abe, I., Takahashi, Y., Morita, H., Noguchi, H., 2001. Eur. J. Biochem. 268, 3354. Chu, A., Furlan, M., Davin, L.B., Zajicek, J., Towers, G.H.N., Soucy-Breau, C.M., Rettig, S.J., Croteau, R., Lewis, N.G., 1994. Phytochemistry 36, 975. Correa, J., Bernal, H., 1992. Especies Vegetales Promisorias de los Paı´ ses del Convenio Andre´s Bello. T. VII, Santafe´ de Bogota´, DC, Colombia, pp. 314e322. Das, B., Rao, S.P., Srinivas, K.V.N.S., Yadav, J.S., 1993. Phytochemistry 33, 1529. Fuchino, H., Satoh, T., Tanaka, N., 1995. Chem. Pharm. Bull. 43, 1937. Fuchino, H., Konishi, S., Satoh, T., Yagi, A., Saitsu, K., Tatsumi, T., Tanaka, N., 1996. Chem. Pharm. Bull. 44, 1033. Fuchino, H., Satoh, T., Hida, J., Terada, M., Tanaka, N., 1998. Chem. Pharm. Bull. 46, 1051. Guerrero, M.F., Carro´n, R., Martı´ n, M.L., San Roma´n, L., Reguero, M.T., 2001. J. Ethnopharmacol. 75, 33. Guerrero, M.F., Puebla, P., Carro´n, R., Martı´ n, M.L., Arteaga, L., San Roma´n, L., 2002a. J. Ethnopharmacol. 80, 37. Guerrero, M.F., Puebla, P., Carro´n, R., Martı´ n, M.L., San Roma´n, L., 2002b. J. Pharm. Pharmacol. 54, 1373. Guerrero, M.F., Puebla, P., Martı´ n, M.L., Carro´n, R., San Roma´n, L., Reguero, M.T., Arteaga, L., 2002c. Planta Med. 68, 322. Kikuzaki, H., Tesaki, S., Yonemori, S., Nakatani, N., 2001. Phytochemistry 56, 109. Matsuda, H., Morikawa, T., Toguchida, I., Harima, S., Yoshikawa, M., 2002. Chem. Pharm. Bull. 50, 972. Merritt, A.T., Ley, S.V., 1992. Nat. Prod. Rep. 9, 243. Morikawa, T., Tao, J., Toguchida, I., Matsuda, H., Yoshikawa, M., 2003. J. Nat. Prod. 66, 86. Nugroho, B.W., Schwarz, B., Wray, V., Proksch, P., 1996. Phytochemistry 41, 129. Ohmura, K., Miyase, T., Ueno, A., 1989. Phytochemistry 28, 1919. Pan, H., Lundgren, L.N., 1994. Phytochemistry 36, 79.
854
P. Puebla et al. / Biochemical Systematics and Ecology 33 (2005) 849e854
Puebla, P., Lo´pez, J.L., Guerrero, M., Carro´n, R., Martı´ n, M.L., San Roma´n, L., San Feliciano, A., 2003. Phytochemistry 62, 551. Rao, K.V., Johnson, J.H., 1998. Phytochemistry 49, 1361. Santamour Jr., F.S., Lundgren, L.N., 1997. Biochem. Syst. Ecol. 25, 335. Seco, J.M., Quin˜oa´, E., Riguera, R., 2001. Tetrahedron: Asymmetry 12, 2915. Seco, J.M., Quin˜oa´, E., Riguera, R., 2004. Chem. Rev. 104, 17. Shikishima, Y., Takaishi, Y., Honda, G., Ito, M., Takeda, Y., Kodzhimatov, O.K., Ashurmetov, O., 2001. Phytochemistry 56, 377.
Phenylbutanoid derivatives from Croton schiedeanus P. Puebla a,*, S.X. Correa b, M.F. Guerrero b, A. San Feliciano a a
Departamento de Quı´mica Farmace´utica, Facultad de Farmacia, E-37007 Salamanca, Spain b Departamento de Farmacia, Facultad de Ciencias, Universidad Nacional de Colombia, Bogota´ AA 11430, Colombia Received 30 June 2004; accepted 24 December 2004
Keywords: Croton schiedeanus; Euphorbiaceae; Phenylbutanoids
1. Subject and source Croton schiedeanus Schlecht (Euphorbiaceae) is a tree which grows widely in south and central America. In Colombia it is particularly widespread in the Amazonian and Cundinamarca regions, where it is popularly known as ‘‘almizclillo’’ and used in Folk Medicine for treating hypertension (Correa and Bernal, 1992). The aerial part of C. schiedeanus was collected from the region of Tocaima, Cundinamarca, Colombia, in April 2002. Its identity was confirmed by Dr. Jose´ Luis Ferna´ndez and a voucher specimen deposited under No. 432164 in the Herbarium, Natural Sciences Institute of National University, Colombia.
* Corresponding author. Tel.: C34 23 294528; fax: C34 23 294515. E-mail address: [email protected] (P. Puebla). 0305-1978/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.bse.2004.12.018
850
P. Puebla et al. / Biochemical Systematics and Ecology 33 (2005) 849e854
2. Previous work In a previous work we tested the hypotensive and vasorelaxant effects of aqueous and ethanolic extracts from this plant (Guerrero et al., 2001, 2002a). Other studies showed that the flavonoids isolated from C. schiedeanus also elicit vasorelaxant effects (Guerrero et al., 2002b), and these effects were partially NO/cGMP pathwaydependent (Guerrero et al., 2002c). In a phytochemical report we described the isolation and identification of four diterpenoids with clerodane skeleton and two flavonoids (ayanin and quercetin 3,7dimethyl ether) (Puebla et al., 2003).
3. Present study As part of our study on the chemical constituents of this plant, we report here the isolation and structural characterization of two new phenylbutanoids related to rhododendrol. The dried sample (10 kg) was soaked in 96% EtOH (50 l) at room temperature for three days. The EtOH was removed in vacuo to yield a dark residue (160 g), which was partitioned between CHCl3 and H2O to give CHCl3 soluble fraction (90 g). The CHCl3 extract was further fractionated with aqueous 4% NaOH yielding an acid part (18 g) and a neutral part (65 g). The acid part was separated by flash column chromatography, over silica gel, gradient elution with 0e100% EtOAc/hexane, yielding 7,9-dimethoxyrhododendrol (1) (350 mg) as a brown oil. The neutral part was also separated by flash column chromatography, in similar conditions to afford 2-acetoxy-7,9-dimethoxyrhododendrol (2) (65 mg). The identification of these compounds was carried out by interpretation of its spectral data (IR, HRMS, 1H NMR, 13C NMR, DEPT, COSY, HMQC, HMBC), as well as by comparison of the experimental data with those found in the literature values for rhododendrol and derivatives (Shikishima et al., 2001). The acetylation of (1), using acetic anhydride and pyridine, yielded 2,8-diacetoxy-7,9-dimethoxyrhododendrol (3), which served to confirm the structure proposed (Fig. 1). The absolute configuration at position C-2 for 7,9-dimethoxyrhododendrol (1), was determined by 1H NMR using a chiral auxiliary reagent, following the methodology described by Seco, Quin˜oa´ and Riguera (Seco et al., 2001, 2004), these authors describe a guide for the assignment of the absolute configuration of secondary alcohols, based on the regularity of chemical shift differences (DdRS) between equivalent signals of each diastereoisomer. In this work we used R-MPA and S-MPA (methoxyphenyl acetic acid) as chiral auxiliary reagents to prepare the corresponding diastereomeric esters. The experimental Dd values of those derivatives are represented in Fig. 2, these data are in accordance with an S configuration at C-2 for the natural compound 1. Compound 3 is the acetylated derivative of compound 1, therefore, the configuration at C-2 is the same. Compound 2 presents the same optical rotation sign as 3, which implies an S configuration at C-2.
851
P. Puebla et al. / Biochemical Systematics and Ecology 33 (2005) 849e854
OH 6
MeO 7
5
8
4
3
2
1
10
HO
OAc
OAc MeO
MeO
AcO
HO
9
OMe
OMe
OMe
1
2
3
OH
HO
rhododendrol Fig. 1. Phenylbutanoids from Croton schiedeanus.
3.1. Preparation of esters The esters were prepared by treatment of alcohol 1 (0.5 mmol) with the corresponding acid R- or S-MPA (0.5 mmol) in presence of 1,3-dicyclohexylcarbodiimide (DCC) (0.6 mmol) and 4-(dimethylamino)pyridine (DMAP) (catalytic) in CH2Cl2. The reaction mixture was filtered to remove the dicyclohexylurea and the esters were purified by flash chromatography on silica gel using mixtures of hexane/ EtOAc. (2S)-7,9-Dimethoxyrhododendrol (1): IR (film): 3430, 1712, 1612, 1518, 1116 cmÿ1. HR-FABMS: 249.1112 [M C 23] (Calcd for C12H18O4 C Na 249.1102). [a]D Z C11.1 (c Z 0.75 CHCl3). 1H and 13C NMR (CDCl3, 400 MHz): (Tables 1 and 2).
L1= Me-1 ∆δRS=
- 0.11
L2= H-3
H-4
+ 0.21
and
+ 0.32
H-6,10 + 0.22
∆δRSL2>0
∆δRSL1<0 H
H ∆δRS>0 MPA-O ∆δRS<0
MPA-O
H L2 L1
HO
S-configuration Fig. 2. Assignment of the configuration of compound 1 (according Seco et al., 2001).
852
P. Puebla et al. / Biochemical Systematics and Ecology 33 (2005) 849e854
Table 1 1 H NMR of compounds 1, 2 and 3 (d in ppm, multiplicity and J in Hz) H
1
2
3
1 2 3
1.23 d 6.2 3.85 m 1.76 m
1.25 d 6.2 4.95 m 1.77 m
1.25 d 6.2 4.98 m 1.84 m
4
2.58 m
2.61 m
6
2.58 ddd 6.7, 9.1, 13.8 2.68 ddd 7.2, 9.0, 13.8 6.24 s
6.39 s
6.41 s
10 OMe-C7,C9 Ac-C2 Ac-C8
6.24 s 3.87 s e e
6.39 s 3.88 s 2.05 s e
6.41 3.80 2.04 2.32
s s s s
(2S)-Acetoxy-7,9-dimethoxyrhododendrol (2): IR (film): 3463, 1730, 1612, 1518, 1461, 1116 cmÿ1. HR-FABMS: 291.1201 [M C 23] (Calcd for C14H20O5 C Na 291.1208). [a]D Z ÿ13.3 (c Z 0.45 CHCl3). 1H and 13C NMR (CDCl3, 400 MHz): (Tables 1 and 2). (2S)-2,8-Diacetoxy-7,9-dimethoxyrhododendrol (3): IR (film): 1764, 1731, 1603, 1509 cmÿ1. [a]D Z ÿ20.1 (c Z 0.12 CHCl3). 1H and 13C NMR (CDCl3, 200 MHz): (Tables 1 and 2).
4. Chemotaxonomic significance The genus Croton comprises about 800 species of trees, shrubs and herbs, distributed in tropical and subtropical regions, and is one of the richest sources of diterpenes with clerodane skeleton (Merritt and Ley, 1992), in addition flavonoids and alkaloids are also commonly found in this genus but, as far as we know, Table 2 13 C NMR of compounds 1, 2 and 3 (d in ppm) C
1
2
3
1 2 3 4 5 6 7 8 9 10 OMe-C7, C9 Ac-C2 Ac-C8
23.6 67.5 41.0 32.3 132.8 105.0 147.0 133.1 147.0 105.0 56.2 e e
20.0 70.4 37.8 32.0 132.5 105.0 146.9 132.9 146.9 105.0 56.2 170.7; 21.3
20.2 70.5 37.6 32.5 126.9 105.0 152.0 140.1 152.0 105.0 56.2 170.8; 21.4 169.0; 20.5
P. Puebla et al. / Biochemical Systematics and Ecology 33 (2005) 849e854
853
phenylbutanoids have not been reported before in Croton, and the compounds 1 and 2 are new natural products. Phenylbutanoids occur in several species of different genus, particularly in genera Betula (Pan and Lundgren, 1994; Santamour and Lundgren, 1997; Fuchino et al., 1995, 1996, 1998), Rheum (Abe et al., 2001; Shikishima et al., 2001), Taxus (Chu et al., 1994; Rao and Johnson, 1998), Chrysanthemum (Matsuda et al., 2002), Rhododendron (Das et al., 1993), Acer (Morikawa et al., 2003), Alpinia (Kikuzaki et al., 2001), Zingiber (Nugroho et al., 1996) and Hypochoeris (Ohmura et al., 1989). A mechanism for the formation of this type of compounds was proposed for Abe et al. (2001), according to these authors the benzalacetone synthase (BAS) catalyzes a one step decarboxylative condensation of 4-coumaroyl-CoA with malonyl-CoA to produce the C6eC4 skeleton of phenylbutanoids in higher plants. Acknowledgements This work was supported by the EC project ALFA-RELAPLAMED.2 (Network1233), the Iberoamerican Program of Science and Technology for Development, (CYTED), Subprogram X, Departamento de Farmacia, Universidad Nacional de Colombia and MCYT-SPAIN (SAF-2001-0037-004-04).
References Abe, I., Takahashi, Y., Morita, H., Noguchi, H., 2001. Eur. J. Biochem. 268, 3354. Chu, A., Furlan, M., Davin, L.B., Zajicek, J., Towers, G.H.N., Soucy-Breau, C.M., Rettig, S.J., Croteau, R., Lewis, N.G., 1994. Phytochemistry 36, 975. Correa, J., Bernal, H., 1992. Especies Vegetales Promisorias de los Paı´ ses del Convenio Andre´s Bello. T. VII, Santafe´ de Bogota´, DC, Colombia, pp. 314e322. Das, B., Rao, S.P., Srinivas, K.V.N.S., Yadav, J.S., 1993. Phytochemistry 33, 1529. Fuchino, H., Satoh, T., Tanaka, N., 1995. Chem. Pharm. Bull. 43, 1937. Fuchino, H., Konishi, S., Satoh, T., Yagi, A., Saitsu, K., Tatsumi, T., Tanaka, N., 1996. Chem. Pharm. Bull. 44, 1033. Fuchino, H., Satoh, T., Hida, J., Terada, M., Tanaka, N., 1998. Chem. Pharm. Bull. 46, 1051. Guerrero, M.F., Carro´n, R., Martı´ n, M.L., San Roma´n, L., Reguero, M.T., 2001. J. Ethnopharmacol. 75, 33. Guerrero, M.F., Puebla, P., Carro´n, R., Martı´ n, M.L., Arteaga, L., San Roma´n, L., 2002a. J. Ethnopharmacol. 80, 37. Guerrero, M.F., Puebla, P., Carro´n, R., Martı´ n, M.L., San Roma´n, L., 2002b. J. Pharm. Pharmacol. 54, 1373. Guerrero, M.F., Puebla, P., Martı´ n, M.L., Carro´n, R., San Roma´n, L., Reguero, M.T., Arteaga, L., 2002c. Planta Med. 68, 322. Kikuzaki, H., Tesaki, S., Yonemori, S., Nakatani, N., 2001. Phytochemistry 56, 109. Matsuda, H., Morikawa, T., Toguchida, I., Harima, S., Yoshikawa, M., 2002. Chem. Pharm. Bull. 50, 972. Merritt, A.T., Ley, S.V., 1992. Nat. Prod. Rep. 9, 243. Morikawa, T., Tao, J., Toguchida, I., Matsuda, H., Yoshikawa, M., 2003. J. Nat. Prod. 66, 86. Nugroho, B.W., Schwarz, B., Wray, V., Proksch, P., 1996. Phytochemistry 41, 129. Ohmura, K., Miyase, T., Ueno, A., 1989. Phytochemistry 28, 1919. Pan, H., Lundgren, L.N., 1994. Phytochemistry 36, 79.
854
P. Puebla et al. / Biochemical Systematics and Ecology 33 (2005) 849e854
Puebla, P., Lo´pez, J.L., Guerrero, M., Carro´n, R., Martı´ n, M.L., San Roma´n, L., San Feliciano, A., 2003. Phytochemistry 62, 551. Rao, K.V., Johnson, J.H., 1998. Phytochemistry 49, 1361. Santamour Jr., F.S., Lundgren, L.N., 1997. Biochem. Syst. Ecol. 25, 335. Seco, J.M., Quin˜oa´, E., Riguera, R., 2001. Tetrahedron: Asymmetry 12, 2915. Seco, J.M., Quin˜oa´, E., Riguera, R., 2004. Chem. Rev. 104, 17. Shikishima, Y., Takaishi, Y., Honda, G., Ito, M., Takeda, Y., Kodzhimatov, O.K., Ashurmetov, O., 2001. Phytochemistry 56, 377.