- Email: [email protected]
Phenylpropanoid amides and phenylethanols from Nanophyton erinaceum
Biochemical Systematics and Ecology 61 (2015) 399e401
Contents lists available at ScienceDirect
Biochemical Systematics and Ecology journal homepage: www.elsevier.com/locate/biochemsyseco
Phenylpropanoid amides and phenylethanols from Nanophyton erinaceum Jianxin Han a, Liya Li b, Li Han b, Xueshi Huang b, Tao Yuan a, * a
The Key Laboratory of Plant Resources and Chemistry of Arid Zone, State Key Laboratory of Xinjiang Indigenous Medicinal Plants Resource Utilization, Xinjiang Technical Institute of Physics and Chemistry, Chinese Academy of Sciences, Urumqi 830011, China b Institute of Microbial Pharmaceuticals, College of Life and Health Sciences, Northeastern University, Shenyang 110819, China
a r t i c l e i n f o
a b s t r a c t
Article history: Received 2 June 2015 Received in revised form 5 July 2015 Accepted 11 July 2015 Available online xxx
Phytochemical investigation of the aerial parts of Nanophyton erinaceum (Pall.) Bunge led to the isolation and identification of one new (1) and eight known phenylpropanoid amides (2e9), four phenylethanols (10e13), two flavonoids (14e15) and one coumarin (16). This is the first report of these isolates from the genus Nanophyton and their chemotaxonomic significance is summarized herein. © 2015 Published by Elsevier Ltd.
Keywords: Nanophyton erinaceum Nanophyton Phenylpropanoid amides Phenylethanol glycosides Chemotaxonomic
1. Subject and source The genus Nanophyton (Chenopodiaceae) contains only one species, Nanophyton erinaceum (Pall.) Bunge which is widely distributed in Central and West Asia (Flora Compilation Committee of Chinese Academy of Science, 1979). N. erinaceum, which is good forage grass for camel, horses, and sheep, also grows in Xinjiang, China, close to the Central Asian countries, Kazakhstan, Tajikistan, Kyrgyzstan and Uzbekistan. The aerial parts of N. erinaceum were collected from Urumqi, Xinjiang Province, China, in October 2014, and identified by Prof. Yan Wei (College of Grassland and Environment Sciences, Xinjiang Agricultural University). A voucher specimen (NE201410) has been deposited in the Key Laboratory of Plant Resources and Chemistry of Arid Zone, Xinjiang Technical Institute of Physics and Chemistry, Chinese Academy of Sciences (Xinjiang, China).
2. Previous work Previous phytochemical investigations of N. erinaceum yielded two piperidine alkaloids, 2,6-dimethylpiperidine and 1,2,6trimethylpiperidine from the aerial parts (Kuzovkov and Men'shikov, 1950).
* Corresponding author. E-mail address: [email protected] (T. Yuan). http://dx.doi.org/10.1016/j.bse.2015.07.012 0305-1978/© 2015 Published by Elsevier Ltd.
400
J. Han et al. / Biochemical Systematics and Ecology 61 (2015) 399e401
3. Present study The dried aerial parts of N. erinaceum (1.5 kg) were ground and extracted exhaustively with methanol (3 5 L) at room temperature. The dried methanol extract (44.6 g) was re-suspended in water and partitioned successively with petroleum ether (3 1000 mL), ethyl acetate (3 1000 mL) and n-butanol (3 1000 mL). The ethyl acetate extract (1.6 g) was subjected to C18 silica gel column chromatography eluted with MeOH/H2O (MeOH/H2O, 50/50 to 100/0, v/v) to yield six fractions AeG. Fraction A (182.0 mg) was separated by semi-preparative HPLC eluted with MeOH/H2O (0e30 min: 40:60 to 50:50; 30e31 min: 50:50 to 100:0; 31e32 min: 100:0; 32e33 min: 100:0 to 40:60; 33e40 min: 40:60; v/v, 3 mL/ min) to yield compounds 1 (5.6 mg), 2 (5.4 mg), 5 (28.0 mg), and 6 (19.5 mg). Fraction B (270.0 mg) was purified on a Sephadex LH-20 column (3 120 cm) eluted with an isocratic solvent system consisting of MeOH to yield three subfractions B1eB3. Purification of sub-fraction B2 (153.6 mg) by semi-preparative HPLC (0e30 min: 40:60 to 50:50; 30e31 min: 50:50 to 100:0; 31e32 min: 100:0; 32e33 min: 100:0 to 40:60; 33e40 min: 40:60; v/v, 3 mL/min) afforded compounds 3 (33.7 mg), 4 (30.8 mg), 7 (2.3 mg), 8 (6.1 mg), and 9 (2.9 mg). Purification of sub-fraction B3 (47.3 mg) by semi-preparative HPLC (0e15 min: 40:60 to 80:20; 15e16 min: 80:20 to 100:0; 16e17 min: 100:0; 17e18 min: 100:0 to 40:60; 18e25 min: 40:60; v/v, 3 mL/min) afforded compounds 14 (9.5 mg), and 15 (10.9 mg). The n-butanol extract (2.6 g) was subjected to C18 silica gel column chromatography by eluting with MeOH/H2O (MeOH/H2O, 30/70 to 100/0, v/v) to yield seven fraction: HeN. Purification of fraction I (123.5 mg) with semi-preparative HPLC (0e25 min: 10:90 to 34:66; 25e26 min: 34:66 to 100:0; 26e27 min: 100:0; 27e28 min: 100:0 to 10:90; 28e35 min: 10:90; v/v, 3 mL/min) yielded compound 10 (34.8 mg) and two impure fractions: I1eI2. Sub-fraction I1 (11.6 mg) was purified by Sephadex LH-20 column (3 120 cm), eluted with an isocratic solvent system consisting of MeOH, to yield compound 13 (5.4 mg). Purification of sub-fraction I2 (12.6 mg) by silica gel column eluted with CHCl3/MeOH (15:1 to 5:1, v/v) yielded compounds 11 (2.3 mg) and 16 (3.3 mg). Fraction J (52.7 mg) was purified by semi-preparative HPLC (0e25 min: 20:80 to 28:72; 25e26 min: 28:72 to 100:0; 26e27 min: 100:0; 27e28 min: 100:0 to 20:80; 28e35 min: 20:80; v/v, 3 mL/min) to yield compound 12 (4.6 mg). The structures of the isolates were elucidated by a combination of spectroscopic methods (ESI-MS, 1H and 13C NMR) and comparison of these data to literature when available. The 1H NMR data of compound 1 was similar to N-p-coumaroyl-N0 trans-feruloyl-putrescine (3) (Choi et al., 2007) the only difference being the presence of a cis double bond at C-70, 80 of 1, which was confirmed by their small coupling constant (J70 ,80 ¼ 12.6 Hz). The structure of compound 1 was thus determined as N-p-coumaroyl-N0 -cis-feruloyl-putrescine. Compounds 2e16 were elucidated as N-trans-feruloyl-N0 -cis-feruloyl-putrescine (2) (Lo et al., 2009), N-p-coumaroyl-N0 -trans-feruloyl-putrescine (3) (Choi et al., 2007), N,N0 -diferuloyl-putrescine (4) (Choi et al., 2007), N-trans-feruloyltyramine (5) (Xie et al., 2014), N-trans-caffeoyltyramine (6) (Xie et al., 2014), N-trans-feruloyloctopamine (7) (Yin et al., 2013), N-cis-caffeoyltyramine (8) (Chen et al., 1998), N-cis-feruloyltyramine (9) (Li et al., 2012), salidroside (10) (Xia et al., 2013), 2-(4-hydroxy-3-methoxyphenyl)ethyl b-D-glucopyranoside (11) (Zheng et al., 2013), 2-(3hydroxy-4-methoxyphenyl)ethyl b-D-glucopyranoside (12) (Zhang et al., 2007), hydroxytyrosol 4-b-D-glucoside (13) (Romero et al., 2002), isorhamnetin 3-O-b-D-glucopyranoside (14) (Surget et al., 2015), tricin (15) (Liu et al., 2012), and scopolin (16) (Kim et al., 2015).
4. Chemotaxonomic significance In the current study, sixteen compounds (1e16) were isolated and identified from the aerial parts of N. erinaceum (Fig. 1), which were classified as phenylpropanoid amides (1e9), phenylethanols (10e13), flavonoids (14e15) and a coumarin (16). The structural classes of these isolates support the taxonomic placement of N. erinaceum in the family Chenopodiaceae, which is characterized by alkaloids, flavonoids, steroids and terpenes (Du et al., 2007). All of the isolates are being reported from the genus Nanophyton for the first time. Furthermore, this is the first report of twelve of these compounds (1e8, 10e13) from the Chenopodiaceae family. Notably, the new compound 1 contains the cis configuration of feruloyl moiety, compared to the trans configuration present in compound 3. Phenylpropanoid amides and phenylethanols have been reported from other species of family Chenopodiaceae. For example, compound 9, Ntrans-feruloyl-4-O-methyldopamine and N-trans-feruloyl-3-O-methyldopamine were isolated from Beta vulgaris (Chenopodiaceae) (Kim et al., 2003), Chenopodium album (Chenopodiaceae) (Horio et al., 1993) and Salsola collina (Chenopodiaceae) (Zhao and Ding, 2004), respectively. A phenylethanol derivative, tetranins A, has been isolated from the roots of Salsola tetrandra (Beyaoui et al., 2012). Moreover, compounds 14 and 15 have been isolated from several members of Chenopodiaceae family (Liu et al., 2012). Phenylpropanoid amides have been reported from the related Chenopodium, Salsola, and Beta genera but they were not the major chemical constituents present therein as in the genus Nanophyton. Also, phenylethanols are present as glycosides in N. erinaceum unlike tetranin A, an aryl substituted phenylethanol present in S. tetrandra. Therefore, the phenylpropanoid amides, phenylethanols and flavonoids identified in the current study can be regarded as chemotaxonomic markers of the N. erinaceum species. Also, while only one coumarin was identified herein, whether it may be regarded as a chemotaxonomic marker of N. erinaceum species remains to be established.
J. Han et al. / Biochemical Systematics and Ecology 61 (2015) 399e401
401
Fig. 1. The structures of compounds isolated from Nanophyton erinaceum.
Acknowledgements This project was supported by Recruitment Program of Global Experts (Tao Yuan), China. The authors would like to thank Prof. Yan Wei (Xinjiang Agricultural University, China) and Prof. Navindra Seeram (University of Rhode Island, USA) for assistance with plant authentication and linguistic revision of the manuscript, respectively. Appendix A. Supplementary data Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.bse.2015.07.012. References Beyaoui, A., Chaari, A., Ghouila, H., Hamza, M.A., Jannet, H.B., 2012. Nat. Prod. Res. 26, 235. Chen, C., Chang, F., Yen, H., Wu, Y., 1998. Phytochemistry 49, 1443. Choi, S.W., Lee, S.K., Kim, E.O., Oh, J.H., Yoon, K.S., Parris, N., Hicks, K.B., Moreau, R.A., 2007. J. Agric. Food Chem. 55, 3920. Du, H., Zhou, L., Li, C., Sui, P., 2007. Nat. Prod. Res. Dev. 19, 884. Flora Compilation Committee of Chinese Academy of Science, 1979 (2). Flora of China, vol. 25. Science Press, Beijing, p. 187. Horio, T., Yoshida, K., Kikuchi, H., Kawabata, J., Mizutani, J., 1993. Phytochemistry 33, 807. Kim, Y., Han, M.S., Lee, J.S., Kim, J., Kim, Y.C., 2003. Phytother. Res. 17, 983. Kim, A.R., Ko, H.J., Chowdhury, M.A., Chang, Y., Woo, E., 2015. Arch. Pharm. Res. 38, 1059. Kuzovkov, A.D., Men0 shikov, G.P., 1950. Zh. Obshch. Khim 20, 1524. Li, Z., Wang, Q., Feng, Y., Rao, Y., Yang, S., Pei, Y., 2012. Chin. Tradit. Herb. Drugs 43, 1273. Liu, S., Sun, W., Yang, H., Sun, W., 2012. Nat. Prod. Res. Dev. 24, 1738. Lo, Y., Lin, R., Lin, Y., Liu, Y., Lee, M., 2009. J. Ethnopharmacol. 124, 625. Romero, C., Brenes, M., García, P., Garrido, A., 2002. J. Agric. Food Chem. 50, 3835. rard, F., Poupart, N., 2015. J. Photochem. Surget, G., Stiger-Pouvreau, V., Lann, K.L., Kervarec, N., Couteau, C., Coiffard, L.J.M., Gaillard, F., Cahier, K., Gue Photobiol. B 143, 52. Xia, F., Sun, J., Jiang, Y., Tu, P., 2013. China J. Chin. Mater. Med. 38, 3299. Xie, L., Atanasov, A.G., Guo, D., Malainer, C., Zhang, J., Zehl, M., Guan, S., Heiss, E.H., Urban, E., Dirsch, V.M., Kopp, B., 2014. J. Ethnopharmacol. 152, 470. Yin, H., Li, J., Dong, J., 2013. Junshi Yixue 37, 279. Zhang, X., Wang, H., Yin, Z., Ye, W., Zhao, S., 2007. J. China Pharm. Univ. 38, 21. Zhao, Y.X., Ding, X.B., 2004. Acta Pharm. Sin. 39, 598. Zheng, C., Guo, Y., Meng, Y., Dou, S., Shao, J., Yang, Y., 2013. Indian J. Chem. B 52B, 654.
Contents lists available at ScienceDirect
Biochemical Systematics and Ecology journal homepage: www.elsevier.com/locate/biochemsyseco
Phenylpropanoid amides and phenylethanols from Nanophyton erinaceum Jianxin Han a, Liya Li b, Li Han b, Xueshi Huang b, Tao Yuan a, * a
The Key Laboratory of Plant Resources and Chemistry of Arid Zone, State Key Laboratory of Xinjiang Indigenous Medicinal Plants Resource Utilization, Xinjiang Technical Institute of Physics and Chemistry, Chinese Academy of Sciences, Urumqi 830011, China b Institute of Microbial Pharmaceuticals, College of Life and Health Sciences, Northeastern University, Shenyang 110819, China
a r t i c l e i n f o
a b s t r a c t
Article history: Received 2 June 2015 Received in revised form 5 July 2015 Accepted 11 July 2015 Available online xxx
Phytochemical investigation of the aerial parts of Nanophyton erinaceum (Pall.) Bunge led to the isolation and identification of one new (1) and eight known phenylpropanoid amides (2e9), four phenylethanols (10e13), two flavonoids (14e15) and one coumarin (16). This is the first report of these isolates from the genus Nanophyton and their chemotaxonomic significance is summarized herein. © 2015 Published by Elsevier Ltd.
Keywords: Nanophyton erinaceum Nanophyton Phenylpropanoid amides Phenylethanol glycosides Chemotaxonomic
1. Subject and source The genus Nanophyton (Chenopodiaceae) contains only one species, Nanophyton erinaceum (Pall.) Bunge which is widely distributed in Central and West Asia (Flora Compilation Committee of Chinese Academy of Science, 1979). N. erinaceum, which is good forage grass for camel, horses, and sheep, also grows in Xinjiang, China, close to the Central Asian countries, Kazakhstan, Tajikistan, Kyrgyzstan and Uzbekistan. The aerial parts of N. erinaceum were collected from Urumqi, Xinjiang Province, China, in October 2014, and identified by Prof. Yan Wei (College of Grassland and Environment Sciences, Xinjiang Agricultural University). A voucher specimen (NE201410) has been deposited in the Key Laboratory of Plant Resources and Chemistry of Arid Zone, Xinjiang Technical Institute of Physics and Chemistry, Chinese Academy of Sciences (Xinjiang, China).
2. Previous work Previous phytochemical investigations of N. erinaceum yielded two piperidine alkaloids, 2,6-dimethylpiperidine and 1,2,6trimethylpiperidine from the aerial parts (Kuzovkov and Men'shikov, 1950).
* Corresponding author. E-mail address: [email protected] (T. Yuan). http://dx.doi.org/10.1016/j.bse.2015.07.012 0305-1978/© 2015 Published by Elsevier Ltd.
400
J. Han et al. / Biochemical Systematics and Ecology 61 (2015) 399e401
3. Present study The dried aerial parts of N. erinaceum (1.5 kg) were ground and extracted exhaustively with methanol (3 5 L) at room temperature. The dried methanol extract (44.6 g) was re-suspended in water and partitioned successively with petroleum ether (3 1000 mL), ethyl acetate (3 1000 mL) and n-butanol (3 1000 mL). The ethyl acetate extract (1.6 g) was subjected to C18 silica gel column chromatography eluted with MeOH/H2O (MeOH/H2O, 50/50 to 100/0, v/v) to yield six fractions AeG. Fraction A (182.0 mg) was separated by semi-preparative HPLC eluted with MeOH/H2O (0e30 min: 40:60 to 50:50; 30e31 min: 50:50 to 100:0; 31e32 min: 100:0; 32e33 min: 100:0 to 40:60; 33e40 min: 40:60; v/v, 3 mL/ min) to yield compounds 1 (5.6 mg), 2 (5.4 mg), 5 (28.0 mg), and 6 (19.5 mg). Fraction B (270.0 mg) was purified on a Sephadex LH-20 column (3 120 cm) eluted with an isocratic solvent system consisting of MeOH to yield three subfractions B1eB3. Purification of sub-fraction B2 (153.6 mg) by semi-preparative HPLC (0e30 min: 40:60 to 50:50; 30e31 min: 50:50 to 100:0; 31e32 min: 100:0; 32e33 min: 100:0 to 40:60; 33e40 min: 40:60; v/v, 3 mL/min) afforded compounds 3 (33.7 mg), 4 (30.8 mg), 7 (2.3 mg), 8 (6.1 mg), and 9 (2.9 mg). Purification of sub-fraction B3 (47.3 mg) by semi-preparative HPLC (0e15 min: 40:60 to 80:20; 15e16 min: 80:20 to 100:0; 16e17 min: 100:0; 17e18 min: 100:0 to 40:60; 18e25 min: 40:60; v/v, 3 mL/min) afforded compounds 14 (9.5 mg), and 15 (10.9 mg). The n-butanol extract (2.6 g) was subjected to C18 silica gel column chromatography by eluting with MeOH/H2O (MeOH/H2O, 30/70 to 100/0, v/v) to yield seven fraction: HeN. Purification of fraction I (123.5 mg) with semi-preparative HPLC (0e25 min: 10:90 to 34:66; 25e26 min: 34:66 to 100:0; 26e27 min: 100:0; 27e28 min: 100:0 to 10:90; 28e35 min: 10:90; v/v, 3 mL/min) yielded compound 10 (34.8 mg) and two impure fractions: I1eI2. Sub-fraction I1 (11.6 mg) was purified by Sephadex LH-20 column (3 120 cm), eluted with an isocratic solvent system consisting of MeOH, to yield compound 13 (5.4 mg). Purification of sub-fraction I2 (12.6 mg) by silica gel column eluted with CHCl3/MeOH (15:1 to 5:1, v/v) yielded compounds 11 (2.3 mg) and 16 (3.3 mg). Fraction J (52.7 mg) was purified by semi-preparative HPLC (0e25 min: 20:80 to 28:72; 25e26 min: 28:72 to 100:0; 26e27 min: 100:0; 27e28 min: 100:0 to 20:80; 28e35 min: 20:80; v/v, 3 mL/min) to yield compound 12 (4.6 mg). The structures of the isolates were elucidated by a combination of spectroscopic methods (ESI-MS, 1H and 13C NMR) and comparison of these data to literature when available. The 1H NMR data of compound 1 was similar to N-p-coumaroyl-N0 trans-feruloyl-putrescine (3) (Choi et al., 2007) the only difference being the presence of a cis double bond at C-70, 80 of 1, which was confirmed by their small coupling constant (J70 ,80 ¼ 12.6 Hz). The structure of compound 1 was thus determined as N-p-coumaroyl-N0 -cis-feruloyl-putrescine. Compounds 2e16 were elucidated as N-trans-feruloyl-N0 -cis-feruloyl-putrescine (2) (Lo et al., 2009), N-p-coumaroyl-N0 -trans-feruloyl-putrescine (3) (Choi et al., 2007), N,N0 -diferuloyl-putrescine (4) (Choi et al., 2007), N-trans-feruloyltyramine (5) (Xie et al., 2014), N-trans-caffeoyltyramine (6) (Xie et al., 2014), N-trans-feruloyloctopamine (7) (Yin et al., 2013), N-cis-caffeoyltyramine (8) (Chen et al., 1998), N-cis-feruloyltyramine (9) (Li et al., 2012), salidroside (10) (Xia et al., 2013), 2-(4-hydroxy-3-methoxyphenyl)ethyl b-D-glucopyranoside (11) (Zheng et al., 2013), 2-(3hydroxy-4-methoxyphenyl)ethyl b-D-glucopyranoside (12) (Zhang et al., 2007), hydroxytyrosol 4-b-D-glucoside (13) (Romero et al., 2002), isorhamnetin 3-O-b-D-glucopyranoside (14) (Surget et al., 2015), tricin (15) (Liu et al., 2012), and scopolin (16) (Kim et al., 2015).
4. Chemotaxonomic significance In the current study, sixteen compounds (1e16) were isolated and identified from the aerial parts of N. erinaceum (Fig. 1), which were classified as phenylpropanoid amides (1e9), phenylethanols (10e13), flavonoids (14e15) and a coumarin (16). The structural classes of these isolates support the taxonomic placement of N. erinaceum in the family Chenopodiaceae, which is characterized by alkaloids, flavonoids, steroids and terpenes (Du et al., 2007). All of the isolates are being reported from the genus Nanophyton for the first time. Furthermore, this is the first report of twelve of these compounds (1e8, 10e13) from the Chenopodiaceae family. Notably, the new compound 1 contains the cis configuration of feruloyl moiety, compared to the trans configuration present in compound 3. Phenylpropanoid amides and phenylethanols have been reported from other species of family Chenopodiaceae. For example, compound 9, Ntrans-feruloyl-4-O-methyldopamine and N-trans-feruloyl-3-O-methyldopamine were isolated from Beta vulgaris (Chenopodiaceae) (Kim et al., 2003), Chenopodium album (Chenopodiaceae) (Horio et al., 1993) and Salsola collina (Chenopodiaceae) (Zhao and Ding, 2004), respectively. A phenylethanol derivative, tetranins A, has been isolated from the roots of Salsola tetrandra (Beyaoui et al., 2012). Moreover, compounds 14 and 15 have been isolated from several members of Chenopodiaceae family (Liu et al., 2012). Phenylpropanoid amides have been reported from the related Chenopodium, Salsola, and Beta genera but they were not the major chemical constituents present therein as in the genus Nanophyton. Also, phenylethanols are present as glycosides in N. erinaceum unlike tetranin A, an aryl substituted phenylethanol present in S. tetrandra. Therefore, the phenylpropanoid amides, phenylethanols and flavonoids identified in the current study can be regarded as chemotaxonomic markers of the N. erinaceum species. Also, while only one coumarin was identified herein, whether it may be regarded as a chemotaxonomic marker of N. erinaceum species remains to be established.
J. Han et al. / Biochemical Systematics and Ecology 61 (2015) 399e401
401
Fig. 1. The structures of compounds isolated from Nanophyton erinaceum.
Acknowledgements This project was supported by Recruitment Program of Global Experts (Tao Yuan), China. The authors would like to thank Prof. Yan Wei (Xinjiang Agricultural University, China) and Prof. Navindra Seeram (University of Rhode Island, USA) for assistance with plant authentication and linguistic revision of the manuscript, respectively. Appendix A. Supplementary data Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.bse.2015.07.012. References Beyaoui, A., Chaari, A., Ghouila, H., Hamza, M.A., Jannet, H.B., 2012. Nat. Prod. Res. 26, 235. Chen, C., Chang, F., Yen, H., Wu, Y., 1998. Phytochemistry 49, 1443. Choi, S.W., Lee, S.K., Kim, E.O., Oh, J.H., Yoon, K.S., Parris, N., Hicks, K.B., Moreau, R.A., 2007. J. Agric. Food Chem. 55, 3920. Du, H., Zhou, L., Li, C., Sui, P., 2007. Nat. Prod. Res. Dev. 19, 884. Flora Compilation Committee of Chinese Academy of Science, 1979 (2). Flora of China, vol. 25. Science Press, Beijing, p. 187. Horio, T., Yoshida, K., Kikuchi, H., Kawabata, J., Mizutani, J., 1993. Phytochemistry 33, 807. Kim, Y., Han, M.S., Lee, J.S., Kim, J., Kim, Y.C., 2003. Phytother. Res. 17, 983. Kim, A.R., Ko, H.J., Chowdhury, M.A., Chang, Y., Woo, E., 2015. Arch. Pharm. Res. 38, 1059. Kuzovkov, A.D., Men0 shikov, G.P., 1950. Zh. Obshch. Khim 20, 1524. Li, Z., Wang, Q., Feng, Y., Rao, Y., Yang, S., Pei, Y., 2012. Chin. Tradit. Herb. Drugs 43, 1273. Liu, S., Sun, W., Yang, H., Sun, W., 2012. Nat. Prod. Res. Dev. 24, 1738. Lo, Y., Lin, R., Lin, Y., Liu, Y., Lee, M., 2009. J. Ethnopharmacol. 124, 625. Romero, C., Brenes, M., García, P., Garrido, A., 2002. J. Agric. Food Chem. 50, 3835. rard, F., Poupart, N., 2015. J. Photochem. Surget, G., Stiger-Pouvreau, V., Lann, K.L., Kervarec, N., Couteau, C., Coiffard, L.J.M., Gaillard, F., Cahier, K., Gue Photobiol. B 143, 52. Xia, F., Sun, J., Jiang, Y., Tu, P., 2013. China J. Chin. Mater. Med. 38, 3299. Xie, L., Atanasov, A.G., Guo, D., Malainer, C., Zhang, J., Zehl, M., Guan, S., Heiss, E.H., Urban, E., Dirsch, V.M., Kopp, B., 2014. J. Ethnopharmacol. 152, 470. Yin, H., Li, J., Dong, J., 2013. Junshi Yixue 37, 279. Zhang, X., Wang, H., Yin, Z., Ye, W., Zhao, S., 2007. J. China Pharm. Univ. 38, 21. Zhao, Y.X., Ding, X.B., 2004. Acta Pharm. Sin. 39, 598. Zheng, C., Guo, Y., Meng, Y., Dou, S., Shao, J., Yang, Y., 2013. Indian J. Chem. B 52B, 654.