Abstract
This study evaluated the cytotoxicity activity of the essential oils of Tagetes erecta L., Asteraceae (TEOE), Tetradenia riparia (Hochst.) Codd, Lamiaceae (TR-OE), Bidens sulphurea (Cav.) Sch. Bip., Asteraceae (BS-OE), and Foeniculum vulgare Mill., Apiaceae (FV-OE), traditionally used in folk medicine, against the tumor cell lines murine melanoma (B16F10), human colon carcinoma (HT29), human breast adenocarcinoma (MCF-7), human cervical adenocarcinoma (HeLa), human hepatocellular liver carcinoma (HepG2), and human glioblastoma (MO59J, U343, and U251). Normal hamster lung fibroblasts (V79 cells) were included as control. The cells were treated with essential oil concentrations ranging from 3.12 to 400 μg/ml for 24 h. The cytotoxic activity was evaluated using the XTT assay; results were expressed as IC50, and the selectivity index was calculated. The results were compared with those achieved for classic chemotherapeutic agents. TE-OE was the most promising among the evaluated oils: it afforded the lowest IC50 values for B16F10 cells (7.47 ± 1.08 μg/ml) and HT29 cells (6.93 ± 0.77 μg/ml), as well as selectivity indices of 2.61 and 2.81, respectively. The major BS-EO, FV-EO and TE-EO chemical constituents were identified by gas chromatography mass spectrometry as being (E)-caryophyllene (10.5%), germacrene D (35.0%) and 2,6-di-tert-butyl-4-methylphenol (43.0%) (BS-EO); limonene (21.3%) and (E)-anethole (70.2%) (FV-EO); limonene (10.4%), dihydrotagetone (11.8%), α-terpinolene (18.1%) and (E)-ocimenone (13.0%) (TE-EO); and fenchone (6.1%), dronabinol (11.0%), aromadendrene oxide (14.7%) and (E,E)–farnesol (15.0%) (TR-EO). 2,6-di-tert-butyl-4-methylphenol (43.0%), (E)-anethole (70.2%) and α-terpinolene (18.1%), respectively. These results suggest that TE-OE may be used to treat cancer without affecting normal cells.
Article PDF
References
Adams, R., 2005. Identification of Essential Oils Components by Gas Chromatography/ Mass Spectrometry, 4th ed. Allured Publishing, Carol Stream, IL.
Agarwal, R., Gupta, S.K., Agarwal, S.S., Srivastava, S., Saxena, R., 2008. Oculohypotensive effects of Foeniculum vulgare in experimental models of glaucoma. Indian J. Physiol. Pharmacol. 52, 77–83.
Aguiar, G.P., Melo, N.I., Wakabayashi, K.A.L., Lopes, M.H.S., Mantovani, A.L.L., Dias, H.J., Fukui, M.J., Keles, L.C., Rodrigues, V., Groppo, M., Silva-Filho, A.A., Cunha, W.R., Magalhães, L.G., Crotti, A.E.M., 2013. Chemical composition and in vitro schistosomicidal activity of the essential oil from the flowers of Bidens sulphurea (Asteraceae). Nat. Prod. Res. 27, 920–924.
Akgul, A., Bayrak, A., 1988. Comparative volatile oil composition of various parts from Turkish bitter fennel (Foeniculum vulgare var. vulgare). Food Chem. 30, 319–323.
Anwar, F., Ali, M., Hussain, A.I., Shahid, M., 2009. Antioxidant and antimicrobial activities of essential oil and extracts of fennel (Foeniculum vulgare Mill.) seeds from Pakistan. Flavour Frag. J. 24, 170–176.
Baslas, R.K., Singh, A.K., 1981. Chemical examination of essential oil from the leaves of Tagetes erecta Linn. J. Indian Chem. Soc. 58, 104.
Bézivin, C., Tomasi, F., Lohézie-Le, D., Boustie, J., 2003. Cytotoxic activity of some lichen extracts on murine and human cancer cell lines. Phytomedicine 10, 499–503.
Bisset, N.G., 1994. Herbal Drugs and Phytopharmaceuticals–A Handbook for Practice on a Scientific Bases. London/Stuttgart, Medpharm/CRC Press.
Botsaris, A.S., 2007. Plants used tradicionally to treat malaria in Brazil: the archives of flora medicinal. J. Ethnobiol. Ethnomed. 3, 2–8.
Campbell, W.E., Gammon, D.W., Smith, P., Abrahams, M., Purves, T., 1997. Composition and antimalarial activity in vitro of the essential oil of Tetradenia riparia. Planta Med. 63, 270–272.
Chung, I.-M., Ro, H.-M., Moon, H.-I., 2011. Major essential oils composition and immunotoxicity activity from leaves of Foeniculum vulgare against Aedes aegypti L. Immunopharmacol. Immunotoxicol. 33, 450–453.
Cosge, B., Gurbuz, B., Kendir, H., Ipek, A., 2008. Composition of essential oil in sweet fennel (Foeniculum vulgare mill. var. dulce) lines originated from Turkey. Asian J. Chem. 20, 1137–1142.
De Mesquita, M.L., de Paula, J.E., Pessoa, C., De Moraes, M.O., Costa-Lotufo, L.V., Grougnet, R., Michel, S., Tillequin, F., Espindola, L.S., 2007. Cytotoxic activity of Brazilian Cerrado plants used in traditional medicine against cancer cell lines. J. Ethnopharmacol. 123, 439–445.
Dunkel, F., Weaver, D., Van Puyvelde, L., Cusker, J.L., Serugend, A., 1990. Population suppression effects of Rwandan medicinal plant, Tetradenia riparia (Hochst.) Codd (Lamiaceae) on stored grain and bean insects. In: Proc. 5th Int. Wkg. Conf. Stored Prod. Prot, pp. 1609–1617.
Fabio, A., Carmelli, C., Fabio, G., Nicoletti, P.I., Quaglio, P., 2007. Screening of the antibacterial effects of a variety of essential oils on microorganisms responsible for respiratory infections. Phytother. Res. 21, 374–377.
Fernandez, C.M.M., Barba, E.L., Fernandez, A.C.M., Cardoso, B.K., Borges, I.B., Takemura, O.S., Martins, L.D., Cortez, L.E.R., Cortez, D.A.G., Gazim, Z.C., 2014. Larvicidal activity of essential oil from Tetradenia riparia to control of Aedes aegypti larvae in function of season variation. J. Essent. Oil Bear. Pl. 17, 813–823.
García-Jiménez, N., Perez-Alonso, M.J., Velasco-Negueruela, A., 2000. Chemical composition of fennel oil, Foeniculum vulgare Miller, from Spain. J. Essent. Oil Res. 12, 159–162.
Gazim, Z.C., Amorim, A.C.L., Hovell, A.M.C., Rezende, C.M., Nascimento, I.A., Ferreira, G.A., Cortez, D.A.G., 2010. Seasonal variation, chemical composition, and analgesic and antimicrobial activities of the essential oil from leaves of Tetradenia riparia (Hochst.) Codd in Southern Brazil. Molecules 15, 5509–5524.
Gazim, Z.C., Rodrigues, F.F.G., Amorin, A.C.L., de Rezende, C.M., Sokovic, M., Tesevic, V., Vuckovic, I., Krstic, G., Cortez, L.E.R., Colauto, N.B., Linde, G.A., Cortez, D.A.G., 2014. New natural diterpene-type abietane from Tetradenia riparia essential oil with cytotoxic and antioxidant activities. Molecules 19, 514–524.
Gross, M., Friedman, J., Dudai, N., Larkov, O., Cohen, Y., Bar, E., Ravid, U., Putievsky, E., Lewinsohn, E., 2002. Biosynthesis of estragole and trans-anethole in bitter fennel (Foeniculum vulgare Mill. var. vulgare) chemotypes. Changes in SAM:phenylpropene O-methyltransferase activities during development. Plant Sci. 162, 1047–1053.
He, W.P., Huang, B.K., 2011. A review of chemistry and bioactivities of a medicinal spice: Foeniculum vulgare. J. Med. Plants Res. 5, 3595–3600.
Krishna, A., Kumar, S., Mallavarapu, G.R., Ramesh, S., 2004. Composition of the essential oils of the leaves and flowers of Tagetes erecta L. J. Essent. Oil Res. 16, 520–522.
Nakagawa, Y., Suzuki, T., 2003. Cytotoxic and xenoestrogenic effects via biotransformation of trans-anethole on isolated rat hepatocytes and cultured MCF-7 human breast cancer cells. Biochem. Pharmacol. 66, 63–73.
Neher, R.T., 1968. The ethnobotany of Tagetes. Econ. Bot. 22, 317–325.
Ogunwande, I.A., Olawore, N.O., 2006. The essential oil from the leaves and flowers of African Marigold, Tagetes erecta L. J. Essent. Oil Res. 18, 366–368.
Omolo, M.O., Okinyo, D., Ndiege, I.O., Lwande, W., Hassanali, A., 2004. Repellency of essential oils of some Kenyan plants against Anopheles gambiae. Phytochemistry 65, 2797–2802.
Ozcan, M.M., Chalchat, J.C., 2006. Effect of collection time on chemical composition of the essential oil of Foeniculum vulgare subsp piperitum growing wild in Turkey. Eur. Food Res. Technol. 224, 279–281.
Peter, W., Deogracious, O., 2006. The in vitro ascaricidal activity of selected indigenous medicinal plants used in ethnoveterinary practices in Uganda. Afr. J. Tradit. Complem. 3, 94–103.
Rabi, T., Bishayee, A., 2009. d-Limonene sensitizes docetaxel-induced cytotoxicity in human prostate cancer cells: Generation of reactive oxygen species and induction of apoptosis. J. Carcinog. 8, 9.
Ram, B., Mandlik, M., Kumar, K., 2013. Antimicrobial activity of Cosmos sulphureus flowers around Pune. Int. J. Pharm. Res. Dev. 5, 27–31.
Sefidkon, F., Salehyar, S., Mirza, M., Dabiri, M., 2004. The essential oil of Tagetes erecta L. occurring in Iran. Flavour Frag. J. 19, 579–581.
Sharma, M.L., Nigam, M.C., Handa, K.L., Chopra, I.C., 1961. Essential oil of Tagetes erecta. Perfum. Essential Oil Rec. 4, 561–562.
Singh, G., Singh, O.P., De Lampasona, M.P., Catalan, C., 2003. Studies on essential oils. Part 35: Chemical and biocidal investigations on Tagetes erecta leaf volatile oil. Flavour Fragr. J. 18, 62–65.
Stasi, L.C., Hiruma-Lima, C.A., 2002. Plantas medicinais na Amazônia e na Mata Atlântica, 2nd ed. UNESP, São Paulo.
Suffness, M., Pezzuto, J.M., 1990. Assays related to cancer drug discovery. In: Hostettmann, K. (Ed.), Methods in Plant Biochemistry: Assays for Bioactivity. Academic Press, London, pp. 71–133.
Tinoco, M.T., Martins, M.R., Cruz-Morais, J., 2007. Antimicrobial activity of Foeniculum vulgare Miller essential oil. Rev. Ciências Agrárias 30, 448–454.
Tonuci, L.R.S., Melo, N.I., Dias, H.J., Wakabayashi, K.A.L., Aguiar, G.P., Aguiar, D.P., Mantovani, A.L.L., Ramos, R.C., Groppo, M., Rodrigues, V., Veneziani, R.C.S., Cunha, W.R., Silva-Filho, A.A., Magalhães, L.G., Crotti, A.E.M., 2012. In vitro schistosomicidal effects of the essential oil of Tagetes erecta. Rev. Bras. Farmacogn 22, 88–93.
Vallisuta, O., Nukoolkarn, V., Mitrevi, A., Sarisuta, N., Leelapornpisid, P., Phrutivorapongkul, A., Sinchaipanid, N., 2014. In vitro studies on the cytotoxicity and elastase and tyrosinase inhibitory activities of marigold (Tagetes erecta L.) flower extracts. Exp. Ther. Med. 7, 246–250.
Villarini, M., Pagiotti, R., Dominici, L., Fatigoni, C., Vanini, S., Levorato, S., Moretti, M., 2014. Investigation of the cytotoxic, genotoxic, and apoptosis-inducing effects of estragole isolated from the fennel (Foeniculum vulgare). J. Nat. Prod. 77, 773–778.
Wakabayashi, K.A.L., Melo, N.I., Aguiar, D.P., Oliveira, P.F., Groppo, M., Silva-Filho, A.A., Rodrigues, V., Cunha, W.R., Tavares, D.C., Magalhães, L.G., Crotti, A.E.M., 2015. Anthelmintic effects of the essential oil of fennel (Foeniculum vulgare Mill., Apiaceae) against Schistosoma mansoni. Chem. Biodiv. 12 (Epub ahead of print).
Acknowledgments
The authors thank the FAPESP Brazil, for a PhD scholarship (P.F.O; grant # 2009/21310-2) and the financial support (grant # 2007/54241-8). The authors are also grateful to CNPq for fellowships.
Author information
Authors and Affiliations
Contributions
HJD contributed in the essential oil extractions and GC-FID andGC-MS analyses. PFO, JMA, JLD and RAMO contributed to biologicalassays and helped in the draft of the manuscript. AEMC collectedthe plant, confected the herbarium samples to taxonomic identifi-cation, supervised the GC-FID and GC-MS analyses and helped in the draft of the manuscript. DCT supervised the biological tests. Allthe authors have read the final manuscript and approved the latesubmission.
Corresponding author
Ethics declarations
The authors declare no conflicts of interest.
Rights and permissions
This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
de Oliveira, P.F., Alves, J.M., Damasceno, J.L. et al. Cytotoxicity screening of essential oils in cancer cell lines. Rev. Bras. Farmacogn. 25, 183–188 (2015). https://doi.org/10.1016/j.bjp.2015.02.009
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1016/j.bjp.2015.02.009