DOI QR코드

DOI QR Code

Cytotoxicity Evaluation of Essential Oil and its Component from Zingiber officinale Roscoe

  • Lee, Yongkyu (Department of Energy and Bio Engineering, Dongseo University)
  • Received : 2016.04.11
  • Accepted : 2016.06.07
  • Published : 2016.07.15

Abstract

Zingiber officinale Roscoe has been widely used as a folk medicine to treat various diseases, including cancer. This study aims to re-examine the therapeutic potential of co-administration of natural products and cancer chemotherapeutics. Candidate material for this project, ${\alpha}$-zingiberene, was extracted from Zingiber officinale Roscoe, and ${\alpha}$-zingiberene makes up $35.02{\pm}0.30%$ of its total essential oil. ${\alpha}$-Zingiberene showed low $IC_{50}$ values, $60.6{\pm}3.6$, $46.2{\pm}0.6$, $172.0{\pm}6.6$, $80.3{\pm}6.6$ (${\mu}g/mL$) in HeLa, SiHa, MCF-7 and HL-60 cells each. These values are a little bit higher than $IC_{50}$ values of general essential oil in those cells. The treatment of ${\alpha}$-zingiberene produced nucleosomal DNA fragmentation in SiHa cells, and the percentage of sub-diploid cells increased in a concentration-dependent manner in SiHa cells, hallmark features of apoptosis. Mitochondrial cytochrome c activation and an in vitro caspase-3 activity assay demonstrated that the activation of caspases accompanies the apoptotic effect of ${\alpha}$-zingiberene, which mediates cell death. These results suggest that the apoptotic effect of ${\alpha}$-zingiberene on SiHa cells may converge caspase-3 activation through the release of mitochondrial cytochrome c into cytoplasm. It is considered that anti-proliferative effect of ${\alpha}$-zingiberene is a result of apoptotic effects, and ${\alpha}$-zingiberene is worth furthermore study to develop it as cancer chemotherapeutics.

Keywords

References

  1. Fabian, D., Sabol, M., Domaracka, K. and Bujnakova, D. (2006) Essential oils - their antimicrobial activity against Escherichia coli and effect on intestinal cell viability. Toxicol. In Vitro, 20, 1435-1445. https://doi.org/10.1016/j.tiv.2006.06.012
  2. Barnes, J. (2003) Quality, efficacy and safety of complementary medicines: fashions, facts and the future. Part I. regulation and quality. Br. J. Clin. Pharmacol., 55, 226-233. https://doi.org/10.1046/j.1365-2125.2003.01810.x
  3. Ali, B.H., Blunden, G., Tanira, M.O. and Nemmar, A. (2008) Some phytochemical, pharmacological and toxicological properties of ginger (Zingiber officinale Roscoe): a review of recent research. Food Chem. Toxicol., 46, 409-420. https://doi.org/10.1016/j.fct.2007.09.085
  4. Shukla, Y. and Singh, M. (2007) Cancer preventive properties of ginger: a brief review. Food Chem. Toxicol., 45, 683-690. https://doi.org/10.1016/j.fct.2006.11.002
  5. Vendruscolo, A., Takaki, I., Bersani-Amado, L.E., Dantas, J.A., Bersani-Amado, C.A. and Cuman, R.K. (2006) Antiinflammatory and antinociceptive activities of Zingiber officinale Roscoe essential oil in experimental animal models. Indian J. Pharmacol., 38, 58-59. https://doi.org/10.4103/0253-7613.19856
  6. Carrasco, F.R., Schmidt, G., Romero, A.L., Sartoretto, J.L., Caparroz-Assef, S.M., Bersani-Amado, C.A. and Cuman, R.K. (2009) Immunomodulatory activity of Zingiber officinale Roscoe, Salvia officinalis L. and Syzygium aromaticum L. essential oils; evidence for humor- and cell-mediated responses. J. Pharm. Pharmacol., 61, 961-967. https://doi.org/10.1211/jpp.61.07.0017
  7. Nogueira de Melo, G.A., Grespan, R., Fonseca, J.P., Farinha, T.O., da Silva, E.L., Romero, A.L., Bersani-Amado, C.A. and Cuman, R.K. (2011) Inhibitory effects of ginger (Zingiber officinale Roscoe) essential oil on leukocyte migration in vivo and in vitro. J. Nat. Med., 65, 241-246. https://doi.org/10.1007/s11418-010-0479-5
  8. Lee, E. and Surh, Y.J. (1998) Induction of apoptosis in HL-60 cells by pungent vanilloids, [6]-gingerol and [6]-paradol. Cancer Lett., 134, 163-168. https://doi.org/10.1016/S0304-3835(98)00253-5
  9. Wei, Q.Y., Ma, J.P., Cai, Y.J., Yang, L. and Liu, Z.L. (2005) Cytotoxic and apoptopic activities of diarylheptanoids and gingerol-related compounds from the rhizomes of Chinese ginger. J. Ethnopharmacol., 102, 177-184. https://doi.org/10.1016/j.jep.2005.05.043
  10. Ishiguro, K., Ando, T., Maeda, O., Ohmiya, N., Niwa, Y., Kadomatsu, K. and Goto, H. (2007) Ginger ingredients reduce viability of gastric cancer cells via distinct mechanisms. Biochem. Biophys. Res. Commun., 362, 218-223. https://doi.org/10.1016/j.bbrc.2007.08.012
  11. Norajit, K., Laohakunjit, N. and Kerdchoechuen, O. (2007) Antibacterial effect of Zingiberaceae essential oils. Molecules, 23, 2047-2060.
  12. Moon, H.I., Cho, S.B. and Kim, S.K. (2011) Composition and immunotoxicity activity of essential oils from leaves of Zingiber officinale Roscoe against Aedes aegypti L. Immunopharmacol. Immunotoxicol., 33, 201-204. https://doi.org/10.3109/08923973.2010.495393
  13. Sasidharan, I., Venugopal, V.V. and Menon, A.N. (2012) Essential oil composition of two unique ginger (Zingiber officinale Roscoe) cultivars from Sikkim. Nat. Prod. Res., 26, 1759-1764. https://doi.org/10.1080/14786419.2011.571215
  14. Yamamoto-Ribeiro, M.M., Grespan, R., Kohiyama, C.Y., Ferreira, F.D., Mossini, S.A., Silva, E.L., Filho, B.A., Mikcha, J.M. and Machinski, M. (2013) Effect of Zingiber officinale essential oil on Fusarium verticillioides and fumonisin production. Food Chem., 141, 3147-3152. https://doi.org/10.1016/j.foodchem.2013.05.144
  15. Khrimian, A., Shirali, S. and Guzman, F. (2015) Absolute configurations of zingiberenols isolated from Ginger (Zingiber officinale) rhizomes. J. Nat. Prod., 78, 3071-3074. https://doi.org/10.1021/acs.jnatprod.5b00638
  16. Adams, R.P. (2001) Identification of essential oil components by gas chromatography/quadrupole mass spectroscopy, Allured Publishing Corporation, Carol Stream, pp. 456-460.
  17. Ji, M., Choi, J., Lee, J. and Lee, Y. (2004) Induction of apoptosis by ar-turmerone on various cell lines. Int. J. Mol. Med., 14, 253-256.
  18. Mohammad, A.M., Razieh, Y. and Mohammad, H.S. (2005) The cytotoxic and anti-proliferative effects of 3-hydrogenkwadaphin in K562 and Jurkat cells is reduced by guanosine. J. Biochem. Mol. Biol., 38, 391-398. https://doi.org/10.5483/BMBRep.2005.38.4.391
  19. Finucanne, D.M., Bossy-Wetzel, E., Waterhouse, N.J., Cotter, T.G. and Green, D.R. (1999) Bax-induced caspase activation and apoptosis via cytochrome c release from mitochondria is inhibitable by Bcl-XL. J. Biol. Chem., 274, 2225-2233. https://doi.org/10.1074/jbc.274.4.2225
  20. Kluck, R.M., Bossy-Wetzel, E., Green, D.R. and Newmeyer, D.D. (1997) The release of cytochrome c from mitochondria : a primary site for Bcl-2 regulation of apoptosis. Science, 275, 1132-1136. https://doi.org/10.1126/science.275.5303.1132
  21. Kroemer, G., Dallaporta, B. and Resche-Rigon, M. (1998) The mitochondrial death/life regulator in apoptosis and necrosis. Annu. Rev. Physiol., 60, 619-642. https://doi.org/10.1146/annurev.physiol.60.1.619
  22. Agarwal, M., Walia, S., Dhingra, S. and Khambay, B.P. (2001) Insect growth inhibition, antifeedant and antifungal activity of compounds isolated/derived from Zingiber officinale Roscoe (ginger) rhizomes. Pest Manag. Sci., 57, 289-300. https://doi.org/10.1002/ps.263
  23. Nogueira de Melo, G.A., Grespan, R., Fonseca, J.P., Farinha, T.O., da Silva, E.L., Romero, A.L., Bersani-Amado, C.A. and Cuman, R.K. (2011) Inhibitory effects of ginger (Zingiber officinale Roscoe) essential oil on leukocyte migration in vivo and in vitro. J. Nat. Med., 65, 241-246. https://doi.org/10.1007/s11418-010-0479-5
  24. Bayala, B., Bassole, I.H., Gnoula, C., Nebie, R., Yonli, A., Morel, L., Figueredo, G., Nikiema, J.B., Lobaccaro, J.M. and Simpore, J. (2014) Chemical composition, antioxidant, antiinflammatory and anti-proliferative activities of essential oils of plants from Burkina Faso. PLoS ONE, 9, e92122. https://doi.org/10.1371/journal.pone.0092122
  25. Hoferl, M., Stoilova, I., Wanner, J., Schmidt, E., Jirovetz, L., Trifonova, D., Stanchev, V. and Krastanov, A. (2015) Composition and comprehensive antioxidant activity of ginger (Zingiber officinale) essential oil from Ecuador. Nat. Prod. Commun., 10, 1085-1090.
  26. Blair, J., Aichinger, T., Hackal, G., Hueber, K. and Dachler, M. (2001) Essential oil content and composition in commercially available dill cultivars in comparison to caraway. Ind. Crops Prod., 14, 229-239. https://doi.org/10.1016/S0926-6690(01)00088-7
  27. Galambosi, B. and Peura, P. (1996) Agrobotanical features and oil content of wild and cultivated forms of caraway (Carum carvi L). J. Essent. Oil Res., 8, 389-397. https://doi.org/10.1080/10412905.1996.9700646
  28. Bartley, J.P. and Foley, P. (1994) Supercritical fluid extraction of australian-grown ginger (Zingiber officinale). J. Sci. Food Agric., 66, 365-371. https://doi.org/10.1002/jsfa.2740660314
  29. Chen, W., Lu, Y., Gao, M., Wu, J., Wang, A. and Shi, R. (2011) Anti-angiogenesis effect of essential oil from Curcuma zedoaria in vitro and in vivo. J. Ethnopharmacol., 133, 220-226. https://doi.org/10.1016/j.jep.2010.09.031
  30. Charriaut-Marlangue, C., Margaill, I., Represa, A., Popovici, T., Plotkine, M. and Ben-Ari, Y. (1996) Apoptosis and necrosis after reversible focal ischemia: an in situ DNA fragmentation analysis. J. Cereb. Blood Flow Metab., 16, 186-194. https://doi.org/10.1097/00004647-199603000-00002
  31. Ioannou, Y.A. and Chen, F.W. (1996) Quantitation of DNA fragmentation in apoptosis. Nucleic Acids Res., 24, 992-993. https://doi.org/10.1093/nar/24.5.992
  32. Collins, J.A., Schandi, C.A., Young, K.K., Vesely, J. and Willingham, M.C. (1997) Major DNA fragmentation is a late event in apoptosis. J. Histochem. Cytochem., 45, 923-934. https://doi.org/10.1177/002215549704500702
  33. Chen, S., Dobrovolsky, V.N., Liu, F., Wu, Y., Zhang, Z., Mei, N. and Guo, L. (2014) The role of autophagy in usnic acidinduced toxicity in hepatic cells. Toxicol. Sci., 142, 33-44. https://doi.org/10.1093/toxsci/kfu154
  34. Rubio, V., Calvino, E., Garcia-Perez, A., Herraez, A. and Diez, J.C. (2014) Human acute promyelocytic leukemia NB4 cells are sensitive to esculetin through induction of an apoptotic mechanism. Chem. Biol. Interact., 220, 129-139. https://doi.org/10.1016/j.cbi.2014.06.021
  35. Semisch, A., Ohle, J., Witt, B. and Hartwig, A. (2014) Cytotoxicity and genotoxicity of nano - and microparticulate copper oxide: role of solubility and intracellular bioavailability. Part Fibre Toxicol., 11, 10. https://doi.org/10.1186/1743-8977-11-10
  36. Sun, L.K., Yoshii, Y., Hyodo, A., Tsurushima, H., Saito, A., Harakuni, T., Li, Y.P., Kariva, K., Nozaki, M. and Morine, N. (2003) Apoptotic effect in the glioma cells induced by specific protein extracted from Okinawa Habu (Trimeresurus flavoviridis) venom in relation to oxidative stress. Toxicol. In Vitro, 17, 169-177. https://doi.org/10.1016/S0887-2333(03)00010-9
  37. Komada, Y., Zhang, X.L., Zhou, Y.W., Ido, M. and Azumam E. (1997) Apoptotic cell death of human T lymphoblastoid cells induced by arginine deiminase. Int. J. Hematol., 65, 129-141. https://doi.org/10.1016/S0925-5710(96)00538-5
  38. Zong, B., Ma, Y., Fu, D. and Zhang, C. (2013) Induction of apoptosis in osteosarcoma s180 cells by polysaccharide from Dictyophora indusiata. Cell Biochem. Funct., 31, 719-723. https://doi.org/10.1002/cbf.2961
  39. Ashkenazi, A. (2008) Directing cancer cells to self-destruct with pro-apoptotic receptor agonists. Nat. Rev. Drug Discov., 7, 1001-1012. https://doi.org/10.1038/nrd2637
  40. Elmore, S. (2007) Apoptosis: a review of programmed cell death. Toxicol. Pathol., 35, 495-516. https://doi.org/10.1080/01926230701320337
  41. Rosse, T., Olivier, R., Monney, L., Rager, M., Conus, S., Fellay, I., Jansen, B. and Borner, C. (1998) Bcl-2 prolongs cell survival after Bax-induced release of cytochrome c. Nature 391, 496-499. https://doi.org/10.1038/35160
  42. Decaudin, D., Marzo, I., Brenner, C. and Kroemer, G. (1998) Mitochondria in chemotherapy-induced apoptosis: a prospective novel target of cancer therapy. Int. J. Oncol., 12, 141-152.
  43. Earnshaw, W.C., Martins, L.M. and Kaufmann, S.H. (1999) Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu. Rev. Biochem., 68, 383-424. https://doi.org/10.1146/annurev.biochem.68.1.383

Cited by

  1. Terpenes from Forests and Human Health vol.33, pp.2, 2017, https://doi.org/10.5487/TR.2017.33.2.097
  2. essential oil in the murine hepatoma cells and in the bacteria and fungi 24-h time–kill curve studies vol.55, pp.1, 2017, https://doi.org/10.1080/13880209.2016.1254251
  3. Influence of some spice food based bioproducts on human monocytic cells line type THP-1 vol.655, pp.1, 2017, https://doi.org/10.1080/15421406.2017.1361307