Phytochemistry 98 (2014) 216–222
Contents lists available at ScienceDirect
Phytochemistry journal homepage: www.elsevier.com/locate/phytochem
Antibacterial chromene and chromane stilbenoids from Hymenocardia acida Courtney M. Starks ⇑, Russell B. Williams, Vanessa L. Norman, Stephanie M. Rice, Mark O’Neil-Johnson, Julie A. Lawrence, Gary R. Eldridge Lead Discovery and Rapid Structure Elucidation Group, Sequoia Sciences, Inc., 1912 Innerbelt Business Center Drive, St. Louis, MO 63114, United States
a r t i c l e
i n f o
Article history: Received 25 July 2013 Received in revised form 30 October 2013 Available online 19 December 2013 Keywords: Hymenocardia acida Phyllanthaceae Chromene Chromane Methicillin-resistant Staphylococcus aureus (MRSA)
a b s t r a c t Six chromene stilbenoids and one chromane stilbenoid were isolated from the African tree Hymenocardia acida. Several were moderately active against methicillin-resistant Staphylococcus aureus clinical isolate MRSA-108, including hymenocardichromanic acid, which was active at 8 lg/ml. None had IC50 values 32 16 16 16 16 16 8 2
7 available, it was not possible to obtain optical rotation values with average magnitudes greater than the standard deviation. However, nine out of ten measurements were in the positive direction. Thus, the absolute configuration of 7 is tentatively assigned to be the same as rhododaurichromanic acid A and anthopogocyclolic acid. This configuration is consistent with the 30 configuration of 3, its likely precursor. The more abundant compounds (1, 2, 3, 4) were tested for proliferation inhibition against several human cancer cell lines, but none had IC50 values 0 (c 0.012, MeOH). The average of ten measured values was less than the standard deviation, however, nine out of ten measured values were positive; UV kmax 227, 264, 309 (broad) nm; for 1H and 13C NMR spectroscopic data, see Table 5; HR-ESIMS m/z 389.1741 [MH] (calcd for C25H25O4: 389.1753). Acknowledgments Sequoia Sciences gratefully acknowledges the Government of Gabon and Madam Nze at IPHA-METRA/CENAREST for permission to collect plants in Gabon. We thank A. Bradley and the staff of the Missouri Botanical Garden for collecting, identifying, and providing H. acida. We acknowledge the scientific collaboration with Advanced Chemistry Development, Inc., (ACD Labs) and the use of the ACD/SpecManager and ACD/Structure Elucidator. Access to the Bruker BioSpin TCI 1.7 mm MicroCryoProbe was made possible through a strategic collaboration between Bruker and Sequoia. References Asakawa, Y., Kondo, K., Tori, M., Hashimoto, T., Ogawa, S., 1991. Chemosystematics of bryophytes. Part 39. Prenyl bibenzyls from the liverwort Radula kojana. Phytochemistry 30, 219–234. Banskota, A.H., Tezuka, Y., Tran, K.Q., Tanaka, K., Saiki, I., Kadota, S., 2000. Thirteen novel cycloartane-type triterpenes from Combretum quadrangulare. J. Nat. Prod. 63, 57–64. Gonzalez, G.J., Martinez, O.E., Delle, M.F., 1995. Citrans and cyclols from Clusia multiflora. Phytochemistry 38, 485–489. Hoet, S., Opperdoes, F., Brun, R., Adjakidje, V., Quetin-Leclercq, J., 2004. In vitro antitrypanosomal activity of ethnopharmacologically selected Beninese plants. J. Ethnopharmacol. 91, 37–42. Hu, J.F., Garo, E., Yoo, H.D., Cremin, P.A., Zeng, L., Goering, M.G., O’Neil-Johnson, M., Eldridge, G.R., 2005. Application of capillary-scale NMR for the structure determination of phytochemicals. Phytochem. Anal. 16, 127–133. Ibrahim, H., Sani, F.S., Danladi, B.H., Ahmadu, A.A., 2007. Phytochemical and antisickling studies of the leaves of Hymenocardia acida Tul. (Euphorbiaceae). Pak. J. Biol. Sci. 10, 788–791. Iwata, N., Kitanaka, S., 2010. Tetracyclic chromane derivatives from Rhododendron anthopogonoides. J. Nat. Prod. 73, 1203–1206. Iwata, N., Kitanaka, S., 2011. New cannabinoid-like chromane and chromene derivatives from Rhododendron anthopogonoides. Chem. Pharm. Bull. 59, 1409– 1412. Kashiwada, Y., Yamazaki, K., Ikeshiro, Y., Yamagishi, T., Fujioka, T., Mihashi, K., Mizuki, K., Cosentino, L.M., Fowke, K., Morris-Natschke, S.L., Lee, K.H., 2001. Isolation of rhododaurichromanic acid B and the anti-HIV principles rhododaurichromanic acid A and rhododaurichromenic acid from Rhododendron dauricum. Tetrahedron 57, 1559–1563. Loughman, J.A., Fritz, S.A., Storch, G.A., Hunstad, D.A., 2009. Virulence gene expression in human community-acquired Staphylococcus aureus infection. J. Infect. Dis. 199, 294–301. Mahmout, Y., Mianpeurem, T., Dolmazon, R., Bouchu, D., Fenet, B., 2005. Amphiphile triterpenoids from Hymenocardia acida Tul. phytoantimalarial and antiinflammatory activities? Curr. Top. Phytochem. 7, 61–66. Manga, F.N., El, K.C., Fontaine, J., Berkenboom, G., Duez, P., Noyon, C., Van, A.P., Nzunzu, J.L., Pochet, S., 2013. Vasorelaxant and antihypertensive effects of methanolic extracts from Hymenocardia acida Tul. J. Ethnopharmacol. 146, 623– 631. Mpiana, P.T., Tshibangu, D.S.T., Shetonde, O.M., Ngbolua, K.N., 2007. In vitro antidrepanocytary actvity (anti-sickle cell anemia) of some Congolese plants. Phytomedicine 14, 192–195. Muanza, D.N., Euler, K.L., Williams, L., Newman, D.J., 1995. Screening for antitumor and anti-HIV activities of nine medicinal plants from Zaire. Int. J. Pharmacogn. 33, 98–106.
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Murakami, H., Tamura, S., Urade, Y., Kubata, B. K., Horii, T., inventors; Sanei Gen FFI Inc., assignee. Flavonoid C glycosides from Hymenocardia acida as antimalarial medicines. Japanese Patent JP2005206501A. 2005 Aug 4. Obidike, I.C., Aboh, M.I., Salawu, O.A., 2011. Microbiological and mucociliary properties of the ethanol extract of Hymenocardia acida on selected respiratory clinical isolates. J. Diet. Suppl. 8, 1–11. Olson, K.M., Starks, C.M., Williams, R.B., O’Neil-Johnson, M., Huang, Z., Ellis, M., Reilly, J.E., Eldridge, G.R., 2011. Novel pentadecenyl tetrazole enhances susceptibility of methicillin-resistant Staphylococcus aureus biofilms to gentamicin. Antimicrob. Agents Chemother. 55, 3691–3695. Pais, M., Marchand, J., Monseur, X., Jarreau, F.X., Goutarel, R., 1967. Peptide alkaloids. Structure of hymenocardine, an alkaloid from Hymenocardia acida. C. R. Hebd. Seances Acad. Sci., Ser. C 264, 1409–1411. Pais, M., Marchand, J., Ratle, G., Jarreau, F.X., 1968. Peptidic alkaloids. VI. Hymenocardine, alkaloid from Hymenocardia acida Tul. Bull. Soc. Chim. Fr. 7, 2979–2984. Shoyama, Y., Oku, R., Yamauchi, T., Nishioka, I., 1972. Cannabis. VI. Cannabicyclolic acid. Chem. Pharm. Bull. 20, 1927–1930. Sofidiya, M.O., Odukoya, O.A., Familoni, O.B., Inya-Agha, S.I., 2006. Free radical scavenging activity of some Nigerian medicinal plant extracts. Pak. J. Biol. Sci. 9, 1438–1441.
Sofidiya, M.O., Odukoya, O.A., Afolayan, A.J., Familoni, O.B., 2009. Phenolic contents, antioxidant and antibacterial activities of Hymenocardia acida. Nat. Prod. Res. 23, 168–177. Sowemimo, A.A., Fakoya, F.A., Awopetu, I., Omobuwajo, O.R., Adesanya, S.A., 2007. Toxicity and mutagenic activity of some selected Nigerian plants. J. Ethnopharmacol. 113, 427–432. Stomberg, R., Li, S., Lundquist, K., Albinsson, B., 1998. Investigation of three stilbene derivatives by X-ray crystallography and NMR spectroscopy. Acta Crystallogr., Sect. C: Cryst. Struct. Commun. C54, 1929–1934. Vonthron-Senecheau, C., Weniger, B., Ouattara, M., Bi, F.T., Kamenan, A., Lobstein, A., Brun, R., Anton, R., 2003. In vitro antiplasmodial activity and cytotoxicity of ethnobotanically selected Ivorian plants. J. Ethnopharmacol. 87, 221–225. Wurdack, K.J., Hoffmann, P., Samuel, R., de, B.A., van, B.M., Chase, M.W., 2004. Molecular phylogenetic analysis of Phyllanthaceae (Phyllanthoideae pro parte, Euphorbiaceae sensu lato) using plastid rbcL DNA sequences. Am. J. Bot. 91, 1882–1900.
Contents lists available at ScienceDirect
Phytochemistry journal homepage: www.elsevier.com/locate/phytochem
Antibacterial chromene and chromane stilbenoids from Hymenocardia acida Courtney M. Starks ⇑, Russell B. Williams, Vanessa L. Norman, Stephanie M. Rice, Mark O’Neil-Johnson, Julie A. Lawrence, Gary R. Eldridge Lead Discovery and Rapid Structure Elucidation Group, Sequoia Sciences, Inc., 1912 Innerbelt Business Center Drive, St. Louis, MO 63114, United States
a r t i c l e
i n f o
Article history: Received 25 July 2013 Received in revised form 30 October 2013 Available online 19 December 2013 Keywords: Hymenocardia acida Phyllanthaceae Chromene Chromane Methicillin-resistant Staphylococcus aureus (MRSA)
a b s t r a c t Six chromene stilbenoids and one chromane stilbenoid were isolated from the African tree Hymenocardia acida. Several were moderately active against methicillin-resistant Staphylococcus aureus clinical isolate MRSA-108, including hymenocardichromanic acid, which was active at 8 lg/ml. None had IC50 values 32 16 16 16 16 16 8 2
7 available, it was not possible to obtain optical rotation values with average magnitudes greater than the standard deviation. However, nine out of ten measurements were in the positive direction. Thus, the absolute configuration of 7 is tentatively assigned to be the same as rhododaurichromanic acid A and anthopogocyclolic acid. This configuration is consistent with the 30 configuration of 3, its likely precursor. The more abundant compounds (1, 2, 3, 4) were tested for proliferation inhibition against several human cancer cell lines, but none had IC50 values 0 (c 0.012, MeOH). The average of ten measured values was less than the standard deviation, however, nine out of ten measured values were positive; UV kmax 227, 264, 309 (broad) nm; for 1H and 13C NMR spectroscopic data, see Table 5; HR-ESIMS m/z 389.1741 [MH] (calcd for C25H25O4: 389.1753). Acknowledgments Sequoia Sciences gratefully acknowledges the Government of Gabon and Madam Nze at IPHA-METRA/CENAREST for permission to collect plants in Gabon. We thank A. Bradley and the staff of the Missouri Botanical Garden for collecting, identifying, and providing H. acida. We acknowledge the scientific collaboration with Advanced Chemistry Development, Inc., (ACD Labs) and the use of the ACD/SpecManager and ACD/Structure Elucidator. Access to the Bruker BioSpin TCI 1.7 mm MicroCryoProbe was made possible through a strategic collaboration between Bruker and Sequoia. References Asakawa, Y., Kondo, K., Tori, M., Hashimoto, T., Ogawa, S., 1991. Chemosystematics of bryophytes. Part 39. Prenyl bibenzyls from the liverwort Radula kojana. Phytochemistry 30, 219–234. Banskota, A.H., Tezuka, Y., Tran, K.Q., Tanaka, K., Saiki, I., Kadota, S., 2000. Thirteen novel cycloartane-type triterpenes from Combretum quadrangulare. J. Nat. Prod. 63, 57–64. Gonzalez, G.J., Martinez, O.E., Delle, M.F., 1995. Citrans and cyclols from Clusia multiflora. Phytochemistry 38, 485–489. Hoet, S., Opperdoes, F., Brun, R., Adjakidje, V., Quetin-Leclercq, J., 2004. In vitro antitrypanosomal activity of ethnopharmacologically selected Beninese plants. J. Ethnopharmacol. 91, 37–42. Hu, J.F., Garo, E., Yoo, H.D., Cremin, P.A., Zeng, L., Goering, M.G., O’Neil-Johnson, M., Eldridge, G.R., 2005. Application of capillary-scale NMR for the structure determination of phytochemicals. Phytochem. Anal. 16, 127–133. Ibrahim, H., Sani, F.S., Danladi, B.H., Ahmadu, A.A., 2007. Phytochemical and antisickling studies of the leaves of Hymenocardia acida Tul. (Euphorbiaceae). Pak. J. Biol. Sci. 10, 788–791. Iwata, N., Kitanaka, S., 2010. Tetracyclic chromane derivatives from Rhododendron anthopogonoides. J. Nat. Prod. 73, 1203–1206. Iwata, N., Kitanaka, S., 2011. New cannabinoid-like chromane and chromene derivatives from Rhododendron anthopogonoides. Chem. Pharm. Bull. 59, 1409– 1412. Kashiwada, Y., Yamazaki, K., Ikeshiro, Y., Yamagishi, T., Fujioka, T., Mihashi, K., Mizuki, K., Cosentino, L.M., Fowke, K., Morris-Natschke, S.L., Lee, K.H., 2001. Isolation of rhododaurichromanic acid B and the anti-HIV principles rhododaurichromanic acid A and rhododaurichromenic acid from Rhododendron dauricum. Tetrahedron 57, 1559–1563. Loughman, J.A., Fritz, S.A., Storch, G.A., Hunstad, D.A., 2009. Virulence gene expression in human community-acquired Staphylococcus aureus infection. J. Infect. Dis. 199, 294–301. Mahmout, Y., Mianpeurem, T., Dolmazon, R., Bouchu, D., Fenet, B., 2005. Amphiphile triterpenoids from Hymenocardia acida Tul. phytoantimalarial and antiinflammatory activities? Curr. Top. Phytochem. 7, 61–66. Manga, F.N., El, K.C., Fontaine, J., Berkenboom, G., Duez, P., Noyon, C., Van, A.P., Nzunzu, J.L., Pochet, S., 2013. Vasorelaxant and antihypertensive effects of methanolic extracts from Hymenocardia acida Tul. J. Ethnopharmacol. 146, 623– 631. Mpiana, P.T., Tshibangu, D.S.T., Shetonde, O.M., Ngbolua, K.N., 2007. In vitro antidrepanocytary actvity (anti-sickle cell anemia) of some Congolese plants. Phytomedicine 14, 192–195. Muanza, D.N., Euler, K.L., Williams, L., Newman, D.J., 1995. Screening for antitumor and anti-HIV activities of nine medicinal plants from Zaire. Int. J. Pharmacogn. 33, 98–106.
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C.M. Starks et al. / Phytochemistry 98 (2014) 216–222
Murakami, H., Tamura, S., Urade, Y., Kubata, B. K., Horii, T., inventors; Sanei Gen FFI Inc., assignee. Flavonoid C glycosides from Hymenocardia acida as antimalarial medicines. Japanese Patent JP2005206501A. 2005 Aug 4. Obidike, I.C., Aboh, M.I., Salawu, O.A., 2011. Microbiological and mucociliary properties of the ethanol extract of Hymenocardia acida on selected respiratory clinical isolates. J. Diet. Suppl. 8, 1–11. Olson, K.M., Starks, C.M., Williams, R.B., O’Neil-Johnson, M., Huang, Z., Ellis, M., Reilly, J.E., Eldridge, G.R., 2011. Novel pentadecenyl tetrazole enhances susceptibility of methicillin-resistant Staphylococcus aureus biofilms to gentamicin. Antimicrob. Agents Chemother. 55, 3691–3695. Pais, M., Marchand, J., Monseur, X., Jarreau, F.X., Goutarel, R., 1967. Peptide alkaloids. Structure of hymenocardine, an alkaloid from Hymenocardia acida. C. R. Hebd. Seances Acad. Sci., Ser. C 264, 1409–1411. Pais, M., Marchand, J., Ratle, G., Jarreau, F.X., 1968. Peptidic alkaloids. VI. Hymenocardine, alkaloid from Hymenocardia acida Tul. Bull. Soc. Chim. Fr. 7, 2979–2984. Shoyama, Y., Oku, R., Yamauchi, T., Nishioka, I., 1972. Cannabis. VI. Cannabicyclolic acid. Chem. Pharm. Bull. 20, 1927–1930. Sofidiya, M.O., Odukoya, O.A., Familoni, O.B., Inya-Agha, S.I., 2006. Free radical scavenging activity of some Nigerian medicinal plant extracts. Pak. J. Biol. Sci. 9, 1438–1441.
Sofidiya, M.O., Odukoya, O.A., Afolayan, A.J., Familoni, O.B., 2009. Phenolic contents, antioxidant and antibacterial activities of Hymenocardia acida. Nat. Prod. Res. 23, 168–177. Sowemimo, A.A., Fakoya, F.A., Awopetu, I., Omobuwajo, O.R., Adesanya, S.A., 2007. Toxicity and mutagenic activity of some selected Nigerian plants. J. Ethnopharmacol. 113, 427–432. Stomberg, R., Li, S., Lundquist, K., Albinsson, B., 1998. Investigation of three stilbene derivatives by X-ray crystallography and NMR spectroscopy. Acta Crystallogr., Sect. C: Cryst. Struct. Commun. C54, 1929–1934. Vonthron-Senecheau, C., Weniger, B., Ouattara, M., Bi, F.T., Kamenan, A., Lobstein, A., Brun, R., Anton, R., 2003. In vitro antiplasmodial activity and cytotoxicity of ethnobotanically selected Ivorian plants. J. Ethnopharmacol. 87, 221–225. Wurdack, K.J., Hoffmann, P., Samuel, R., de, B.A., van, B.M., Chase, M.W., 2004. Molecular phylogenetic analysis of Phyllanthaceae (Phyllanthoideae pro parte, Euphorbiaceae sensu lato) using plastid rbcL DNA sequences. Am. J. Bot. 91, 1882–1900.
