Analysis of the Essential Oils of Five Artemisia Species and Evaluation of their Cytotoxic and Proapoptotic Effects

Author(s): Zahra Tayarani-Najaran, Maryam Akaberi, Bahareh Hassanzadeh, Nazila Shirazi, Javad Asili, Hadi Al-Najjar, Amirhossein Sahebkar, Seyed Ahmad Emami*

Journal Name: Mini-Reviews in Medicinal Chemistry

Volume 19 , Issue 11 , 2019


Become EABM
Become Reviewer
Call for Editor

Graphical Abstract:


Abstract:

Background: In this study, the essential oil composition and cytotoxic activities of five Artemisia species were determined.

Methods: The collected plants were water-distilled separately to obtain oils which were then subjected to gas chromatography (GC) and gas chromatography/mass spectrometry GC/MS analyses to identify their compositions. Cancer cells were exposed to different concentrations of samples and cell viability was measured using AlamarBlue® assay. Apoptotic cells were analyzed by propidium iodide (PI) staining and flow cytometry.

Results & Conclusion: To study the amount of pro-apoptotic proteins and the apoptosis mechanism, Western blot method was used. Although all samples were cytotoxic at the highest concentration, the oil of A. kulbadica showed the strongest activity among other plants. Carvacrol (IC50 21.11 μg/ml) had the most cytotoxic effects among other components. Carvacrol, 1,8-cineole and 4-terpineole caused an increase in the amount of Bax protein and cleaved peroxisome proliferator-activated receptors (PPAR) and caspase proteins in DU 145 cells.

Keywords: Artemisia, Asteraceae, essential oil, chemical composition, cytotoxic, apoptosis.

[1]
Mabberley, D.J. The Plant-Book; Cambridge: Cambridge Press, 2008.
[2]
Podlech, D. Compositae VI Anthemideae In:Flora Iranica; K.H. Rechinger, Ed. Akademische Druck-u, Verlagsansalt: Graz,; , 1986, pp. 159-223.
[3]
Polyakov, P. Artemisia In:Flora of the USSR (English translation); B.K. Shishkin, Ed. Bisnen Singh Scientific Books: Koeringstein, India,; , 1995, pp. 488-489.
[4]
Mucciaralli, M.; Maffel, M. Introduction of the genus Artemisia; Taylor and Francis: London, 2002, pp. 1-50.
[5]
Aghajani, Z.; Kazemi, M.; Dakhili, M.; Rustaiyan, A. Composition and antimicrobial activity of the essential oil of Artemisia kulbadica from Iran. Nat. Prod. Commun., 2009, 4(9), 1261-1266.
[6]
Ghahreman, A.; Attar, F. Biodiversity of plant species in Iran; Tehran University Publication: Tehran, 1999.
[7]
Emami, S.A.; Aghazari, F. Les Phanerogames endemiques de la flore d’Iran.publication de l' Universite' d' Iran des Sciences Medicales: Téhéran; , 2008.
[8]
Mozaffarian, V. Compositae: Anthemideae & Echinapeae. In: Flora of Iran; Research Institute of Forests and Rangelands: Tehran, 2008, pp. 199-261.
[9]
Valles, J.; Garcia, S.; Hidalgo, O.; Martin, J.; Pellicer, J.; Sanz, M.; Garnatje, T. Biology, Genome Evolution, Biotechnological Issues and Research Including Applied Perspectives in Artemisia (Asteraceae). In: Advances in Botanical Research; Kader, J.C.; Delseny, M., Eds.; Elsevier, 2011, pp. 349-419.
[10]
Abad, M.J.; Bedoya, L.M.; Apaza, L.; Bermejo, P. The Artemisia L. genus: A review of bioactive essential oils. Molecules, 2012, 17, 2542-2566.
[11]
Elfawal, M.A.; Towler, M.J.; Reich, N.G.; Golenbock, D.; Weathers, P.J.; Rich, S.M. Dried whole plant Artemisia annua as an antimalarial therapy. PLoS One, 2012, 7(12)
[12]
Bamunuarachchi, G.S.; Ratnasooriya, W.D.; Premakumara, S.; Udagama, P.V. Antimalarial properties of Artemisia vulgaris L. ethanolic leaf extract in a Plasmodium berghei murine malaria model. J. Vector Borne Dis., 2013, 50(4), 278-284.
[13]
Taherkhani, M.; Rustaiyan, A.; Nahrevanian, H.; Naeimi, S.; Taherkhani, T. Comparison of antimalarial activity of Artemisia turanica extract with current drugs in vivo. Proc. Biol. Sci., 2013, 280(1752), 51-56.
[14]
Goswami, P.; Chauhan, A.; Verma, R.S.; Padalia, R.C.; Verma, S.K.; Darokar, M.P.; Chanotiya, C.S. Composition and antibacterial activity of the essential oil of Artemisia nilagirica var. septentrionalis from India. J. Essent. Oil Res., 2016, 28(1), 71-76.
[15]
Marinas, I.C.; Oprea, E.; Chifiriuc, M.C.; Badea, I.A.; Buleandra, M.; Lazar, V. Chemical composition and antipathogenic activity of Artemisia annua essential oil from romania. Chem. Biodivers., 2015, 12(10), 1554-1564.
[16]
Tasdemir, D.; Tierney, M.; Sen, R.; Bergonzi, M.C.; Demirci, B.; Bilia, A.R.; Baser, K.H.C.; Brun, R.; Chatterjee, M. Antiprotozoal effect of Artemisia indica extracts and essential oil. Planta Med., 2015, 81(12-13), 1029-1037.
[17]
Lu, Y.Y.; Chen, T.S.; Qu, J.L.; Pan, W.L.; Sun, L.; Wei, X.B. Dihydroartemisinin (DHA) induces caspase-3-dependent apoptosis in human lung adenocarcinoma ASTC-a-1 cells. J. Biomed. Sci., 2009, 16(16)
[http://dx.doi.org/10.1186/1423-0127-16-16]
[18]
Choi, E.J.; Lee, S.; Chae, J.R.; Lee, H.S.; Jun, C.D.; Kim, S.H. Eupatilin inhibits lipopolysaccharide-induced expression of inflammatory mediators in macrophages. Life Sci., 2011, 88(25-26), 1121-1126.
[19]
Yang, Z.; Ding, J.; Yang, C.; Gao, Y.; Li, X.; Chen, X.; Peng, Y.; Fang, J.; Xiao, S. Immunomodulatory and anti-inflammatory properties of artesunate in experimental colitis. Curr. Med. Chem., 2012, 19(26), 4541-4551.
[20]
Tüÿ, B.A.; Yilmaz, M.; Kivanc, M. Study on the antimicrobial, cytotoxic, and genotoxic activities of the essential oil of Artemisia dracunculus L. Fresen. Environ. Bull, 2009, 18(5 B), 885-889.
[21]
Ebrahimi, M.; Ramezani, M.; Tehrani, S.O.; Malekshah, O.M.; Behravan, J. Cytotoxic effects of methanolic extract and essential oil of Artemisia Kopetdaghensis. J. Essent. Oil Bear. Pl., 2010, 13(6), 732-737.
[22]
Rashid, S.; Rather, M.A.; Shah, W.A.; Bhat, B.A. Chemical composition, antimicrobial, cytotoxic and antioxidant activities of the essential oil of Artemisia indica Willd. Food Chem., 2013, 138(1), 693-700.
[23]
Martínez-Díaz, R.A.; Ibáñez-Escribano, A.; Burillo, J.; de las Heras, L.; del Prado, G.; Agulló-Ortuño, M.T.; Julio, L.F.; González-Coloma, A. Trypanocidal, trichomonacidal and cytotoxic components of cultivated Artemisia absinthium Linnaeus (Asteraceae) essential oil. Mem. Inst. Oswaldo Cruz, 2015, 110(5), 693-699.
[24]
Tilaoui, M.; Mouse, H.A.; Jaafari, A.; Zyad, A. Comparative phytochemical analysis of essential oils from different biological parts of Artemisia herba alba and their cytotoxic effect on cancer cells. PLoS One, 2015, 10(7)
[25]
Rabe, S.T.; Emami, S.A.; Iranshahi, M.; Rastin, M.; Tabasi, N.; Mahmoudi, M. Anti-cancer properties of a sesquiterpene lactone-bearing fraction from Artemisia khorassanica. Asian Pac. J. Cancer Prev., 2015, 16(3), 863-868.
[26]
Emami, S.A.; Taghizadeh Rabe, S.Z.; Iranshahi, M.; Ahi, A.; Mahmoudi, M. Sesquiterpene lactone fraction from Artemisia khorassanica inhibits inducible nitric oxide synthase and cyclooxygenase-2 expression through the inactivation of NF-κB. Immunopharmacol. Immunotoxicol., 2010, 32(4), 688-695.
[27]
Ramezani, M.; Behravan, J.; Yazdinezhad, A. Chemical composition and antimicrobial activity of the volatile oil of Artemisia khorassanica from Iran. Pharm. Biol., 2004, 42(8), 599-602.
[28]
Nahrevanian, H.; Esmaeili, B.; Kazemi, M.; Nazem, H.; Amini, M. In vivo antimalarial effects of iranian flora Artemisia khorassanica against Plasmodium berghei and pharmacochemistry of its natural components. Iran. J. Parasitol., 2010, 5(1), 6-19.
[29]
Ramezani, M.; Behravan, J.; Yazdinezhad, A. Composition and antimicrobial activity of the volatile oil of Artemisia kopetdaghensis Krasch., M.Pop. & Linecz ex Poljak from Iran. Flavour Fragrance J., 2006, 21(6), 869-871.
[30]
Firouzni, A.; Vahedi, H.; Sabbaghi, F.; Bigdeli, M. Composition of the essential oil of Artemisia ciniformis, A. kopetdaghensis, and A. khorasanica in Iran. Chem. Nat. Compd., 2008, 44(6), 804-806.
[31]
Rustaiyan, A.; Tabatabaei-Anaraki, M.; Kazemi, M.; Masoudi, S.; Makipour, P. Chemical composition of essential oil of three Artemisia species growing wild in Iran: Artemisia kermanensis Podl., A. kopetdaghensis Krasch., M.Pop et Lincz. ex Poljak., and A. haussknechtii Boiss. J. Essent. Oil Res., 2009, 21(5), 410-413.
[32]
Oliaee, D.; Boroushaki, M.T.; Oliaee, N.; Ghorbani, A. Evaluation of cytotoxicity and antifertility effect of Artemisia kopetdaghensis. Adv. Pharmacol. Sci., 2014, 2014, 745-760.
[33]
Bahmani, M.; Karamati, S.A.; Hassanzadazar, H.; Forouzan, S.; Rafieian-Kopaei, M.; Kazemi-Ghoshchi, B.; Asadzadeh, J.; Kheiri, A.; Bahmani, E. Ethnobotanic study of medicinal plants in Urmia city: Identification and traditional using of antiparasites plants. Asian Pac. J. Trop. Dis., 2014, 4(S2), S906-S910.
[34]
Azarnivand, H.; Chahouki, M.A.Z. Compositional characteristics of the essential oil from the aerial parts of Artemisia sieberi besser. Vegetos, 2011, 24(2), 13-17.
[35]
Mahboubi, M.; Valian, M.; Kazempour, N. Chemical composition, antioxidant and antimicrobial activity of Artemisia sieberi oils from different parts of Iran and France. J. Essent. Oil Res., 2015, 27(2), 140-147.
[36]
Behmanesh, B.; Heshmati, G.A.; Mazandarani, M.; Rezaei, M.B.; Ahmadi, A.R.; Ghaemi, E.O.; Bakhshandeh Nosrat, S. Chemical composition and antibacterial activity from essential oil of Artemisia sieberi Besser subsp. Sieberi in North of Iran. Asian J. Plant Sci., 2007, 6(3), 562-564.
[37]
Khosravi, A.R.; Shokri, H.; Kermani, S.; Dakhili, M.; Madani, M.; Parsa, S. Antifungal properties of Artemisia sieberi and Origanum vulgare essential oils against Candida glabrata isolates obtained from patients with vulvovaginal candidiasis. J. Mycol. Med., 2011, 21(2), 93-99.
[38]
Mahboubi, M.; Kazempour, N. The antifungal activity of Artemisia sieberi essential oil from different localities of Iran against dermatophyte fungi. J. Mycol. Med., 2015, 25(2), e65-e71.
[39]
Irshaid, F.; Mansi, K.; Aburjai, T. Antidiabetic effect of essential oil from Artemisia sieberi growing in Jordan in normal and alloxan induced diabetic rats. Pak. J. Biol. Sci., 2010, 13(9), 423-430.
[40]
Irshaid, F.I.; Mansi, K.; Bani-Khaled, A.; Aburjia, T. Hepatoprotetive, cardioprotective and nephroprotective actions of essential oil extract of Artemisia sieberi in alloxan induced diabetic rats. Iran. J. Pharm. Res., 2012, 11(4), 1227-1234.
[41]
Asili, J.; Emami, S.A.; Eynolghozat, R.; Noghab, Z.S.; Bazzaz, B.S.F.; Sahebkar, A. Chemical composition and in vitro efficacy of essential oil of seven Artemisia species against ESBL producing multidrug-resistant Escherichia coli. J. Essent. Oil Bear. Pl., 2015, 18(1), 124-145.
[42]
Ezzatzadeh, E.; Farjam, M.H.; Rustaiyan, A. Comparative evaluation of antioxidant and antimicrobial activity of crude extract and secondary metabolites isolated from Artemisia kulbadica. Asian Pac. J. Trop. Dis., 2012, 2(Suppl. 1), S431-S434.
[43]
Emami, S.A.; Rabe, S.Z.T.; Ahi, A.; Mahmoudi, M. Inhibitory activity of eleven Artemisia species from Iran against Leishmania major parasites. Iran. J. Pharm. Res., 2012, 15(2), 807-811.
[44]
Emami, S.A.; Vahdati-Mashhadian, N.; Vosough, R.; Oghazian, M.B. The anticancer activity of five species of Artemisia on Hep2 and HepG2 cell lines. Pharmacol. Online, 2009, 3, 327-339.
[45]
Masoudi, S.; Rustaiyan, A.; Vahedi, M. Volatile oil constituents of different parts of Artemisia chamaemelifolia and the composition and antibacterial activity of the aerial parts of A. turcomanica from Iran. Nat. Prod. Commun., 2012, 7(11), 1519-1522.
[46]
Habibi, Z.; Yousefi, M.; Mohammadi, M.; Eftekhar, F.; Biniyaz, T.; Rustaiyan, A. Chemical composition and antibacterial activity of the volatile oils from Artemisia turcomanica. Chem. Nat. Compd., 2010, 46(5), 819-821.
[47]
Nikbakht, M.R.; Sharifi, S.; Emami, S.A.; Khodaie, L. Chemical composition and antiprolifrative activity of Artemisia persica Boiss. and Artemisia turcomanica Gand. essential oils. Res. Pharm. Sci., 2014, 9(2), 155-163.
[48]
Adams, R.P. Identification of essential oil components by gas chromatography/quadrupole mass spectrometry. Allured Publishing; Carol, Stream, IL, USA,; , 2007.
[49]
Bueno, C.; Villegas, M.L.; Bertolotti, S.G.; Previtali, C.M.; Neumann, M.G.; Encinas, M.V. The excited-state interaction of resazurin and resorufin with aminesin aqueous solutions. photophysics and photochemical reaction. Photochem. Photobiol., 2002, 76(4), 385-390.
[50]
O’Brien, J.; Wilson, I.; Orton, T.; Pognan, F. Investigation of the alamarblue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. Eur. J. Biochem., 2000, 267(17), 5421-5426.
[51]
Nicoletti, I.; Migliorati, G.; Pagliacci, M.C.; Grignani, F.; Riccardi, C. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods, 1991, 139(2), 271-279.
[52]
Barazandeh, M.M. Essential Oil Composition of Artemisia khorassanica Podl. from Iran. J. Essent. Oil Res., 2003, 15(4), 259-260.
[53]
Li, Y.; Ahmad, A.; Kong, D.; Bao, B.; Sarkar, F.H. Recent progress on nutraceutical research in prostate cancer. Cancer Metastasis Rev., 2014, 33, 629-640.
[54]
DeFelice, S.L. The nutraceutical revolution: Its impact on food industry R&D. Trends Food Sci. Technol., 1995, 6, 59-61.
[55]
Scicchitano, P.; Cameli, M. Maiello, M.; Modesti, P.A.; Muiesan, M.L.; Novo, S.; Palmiero, P.; Saba, P.S.; Pedrinelli, R.; Ciccone, M.M. Nutraceuticals and dyslipidaemia: Beyond the common therapeutics. J. Funct. Foods, 2014, 6, 11-32.


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 19
ISSUE: 11
Year: 2019
Published on: 09 July, 2019
Page: [902 - 912]
Pages: 11
DOI: 10.2174/1389557519666190311155021
Price: $65

Article Metrics

PDF: 26
HTML: 1