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In Vitro Investigation of the Anticancer Activity of Friedelin in Glioblastoma Multiforme

Year 2018, Volume: 18 Issue: 3, 763 - 773, 30.12.2018

Abstract

There are different herbal methods used for support in many cancer diseases. Lichens are important organisms containing unique herbal compounds and it is known that they have different anticancer activities. Starting from these features, the present study was aimed to investigate anticancer activity of friedelin (FRI), a lichen compound against glioblastoma multiforme (GBM) showed dangerous malignant properties within brain cancer species. It was used human U87MG-GBM cancer cell lines and primary rat cerebral cortex (PRCC) non-cancerous cells isolated from Sprague-Dawley rats in order to determine side effect level of FRI. In the experiments, cytotoxic (via 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) and lactate dehydrogenase (LDH) tests), antioxidant (via total antioxidant capacity (TAC) test), pro-oxidant (via total oxidative stress (TOS) test) and genotoxic (via 8-hydroxy-2′-deoxyguanosine (8-OH-dG) test) activities of different concentrations of FRI were tested. As a result of the study, MTT assay revealed that FRI showed higher cytotoxic activity on U87MG cells compared to PRCC cells (median inhibitory concentration (IC50): 46.38 and 1271.77 mg/L, respectively). Based on U87MG cells, it was determined a significant positive correlation between LDH and TOS activities. High positive correlation between TAC and cell viability on healthy PRCC cells exhibited antioxidant capacity of FRI. Consequently, the results obtained from the present study proved the potential of natural product with an antioxidant capacity as a source for anticancer compound against GBM.

References

  • Abuiraq, L., Kanan, G., Wedyan, M. and El-Oqlah, A., 2015. Efficacy of extracts of some lichens for potential antibacterial activity. Research Journal of Pharmaceutical, Biological and Chemical Sciences, 6, 318–331.
  • Alpsoy, L., Aslan, A., Kotan, E., Agar, G. and Anar, M., 2011. Protective role of two lichens in human lymphocytes in vitro. Fresenius Environmental Bulletin, 20, 1661–1666.
  • Ari, F., Celikler, S., Oran, S., Balikci, N., Ozturk, S., Ozel, M.Z., Ozyurt, D. and Ulukaya, E., 2014. Genotoxic, cytotoxic, and apoptotic effects of Hypogymnia physodes (L.) Nyl. on breast cancer cells. Environmental Toxicology, 29, 804–813.
  • Bai, L., Bao, H.Y. and Bau, T., 2014. Isolation and identification of a new benzofuranone derivative from Usnea longissima. Natural Product Research, 28, 534–538.
  • Bézivin, C., Tomasi, S., Lohézic-Le Dévéhat, F. and Boustie, J., 2003. Cytotoxic activity of some lichen extracts on murine and human cancer cell lines. Phytomedicine, 10, 499–503.
  • Bézivin, C., Tomasi, S., Rouaud, I., Delcros, J.G. and Boustie, J., 2004. Cytotoxic activity of compounds from the lichen: Cladonia convoluta. Planta Medica, 70, 874–877.
  • Bosset, J.-F., Collette, L., Calais, G., Mineur, L., Maingon, P., Radosevic-Jelic, L., Daban, A., Bardet, E., Beny, A., Ollier, J.-C. and EORTC Radiotherapy Group Trial 22921, 2006. Chemotherapy with preoperative radiotherapy in rectal cancer. The New England Journal of Medicine, 355, 1114–1123.
  • Boustie, J. and Grube, M., 2005. Lichens-A promising source of bioactive secondary metabolites. Plant Genetic Resources, 3, 273–287.
  • Brisdelli, F., Perilli, M., Sellitri, D., Piovano, M., Garbarino, J.A., Nicoletti, M., Bozzi, A., Amicosante, G. and Celenza, G., 2013. Cytotoxic activity and antioxidant capacity of purified lichen metabolites: an in vitro study. Phytotherapy Research, 27, 431–437.
  • Brodo, I.M., Sharnoff, S.D. and Sharnoff, S., 2001. About the Lichens, in: Lichens of North America. Yale University Press, New Haven & London, 3–113.
  • Clarke, J., Penas, C., Pastori, C., Komotar, R.J., Bregy, A., Shah, A.H., Wahlestedt, C. and Ayad, N.G., 2013. Epigenetic pathways and glioblastoma treatment. Epigenetics, 8, 785–795.
  • Çelikler Kasımoğulları, S., Oran, S., Ari, F., Ulukaya, E., Aztopal, N., Sarimahmut, M. and Öztürk, Ş., 2014. Genotoxic, cytotoxic, and apoptotic effects of crude extract of Usnea filipendula Stirt. in vitro. Turkish Journal of Biology, 38, 940–947.
  • Dogan, M., Emsen, B., Aasim, M. and Yildirim, E., 2017. Ceratophyllum demersum L. extract as a botanical insecticide for controlling the maize weevil, Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae). Egyptian Journal of Biological Pest Control, 27, 11–15.
  • Einarsdóttir, E., Groeneweg, J., Björnsdóttir, G.G., Harethardottir, G., Omarsdóttir, S., Ingólfsdóttir, K. and Ogmundsdóttir, H.M., 2010. Cellular mechanisms of the anticancer effects of the lichen compound usnic acid. Planta Medica, 76, 969–974.
  • Emsen, B., Aslan, A., Togar, B. and Turkez, H., 2016a. In vitro antitumor activities of the lichen compounds olivetoric, physodic and psoromic acid in rat neuron and glioblastoma cells. Pharmaceutical Biology, 54, 1748–1762.
  • Emsen, B., Dogan, M., Aasim, M. and Yildirim, E., 2016b. Insecticidal activity of in vitro propagated aquatic plant Ceratophyllum demersum L. against granary weevil Sitophilus granarius L. (Coleoptera: Curculionidae). Egyptian Journal of Biological Pest Control, 26, 619–624.
  • Emsen, B., Turkez, H., Togar, B. and Aslan, A., 2017. Evaluation of antioxidant and cytotoxic effects of olivetoric and physodic acid in cultured human amnion fibroblasts. Human & Experimental Toxicology, 36, 376–385.
  • Emsen, B., Yildirim, E. and Aslan, A., 2015. Insecticidal activities of extracts of three lichen species on Sitophilus granarius (L.) (Coleoptera: Curculionidae). Plant Protection Science, 51, 156–161.
  • Emsen, B., Yildirim, E., Aslan, A., Anar, M. and Ercisli, S., 2012. Insecticidal effect of the extracts of Cladonia foliacea (Huds.) Willd. and Flavoparmelia caperata (L.) Hale against adults of the grain weevil, Sitophilus granarius (L.) (Coleoptera: Curculionidae). Egyptian Journal of Biological Pest Control, 22, 145–149.
  • Feng, J., Yang, X., Su, S. and He, C., 2009. Studies on chemical constituents from herbs of Usnea longissima. Zhongguo Zhongyao Zazhi, 34, 708–711.
  • Gan, W., Nie, B., Shi, F., Xu, X.M., Qian, J.C., Takagi, Y., Hayakawa, H., Sekiguchi, M. and Cai, J.P., 2012. Age-dependent increases in the oxidative damage of DNA, RNA, and their metabolites in normal and senescence-accelerated mice analyzed by LC-MS/MS: urinary 8-oxoguanosine as a novel biomarker of aging. Free Radical Biology & Medicine, 52, 1700–1707.
  • Gauden, A.J., Hunn, A., Erasmus, A., Waites, P., Dubey, A. and Gauden, S.J., 2009. Combined modality treatment of newly diagnosed glioblastoma multiforme in a regional neurosurgical centre. Journal of Clinical Neuroscience, 16, 1174–1179.
  • Ghate, N.B., Chaudhuri, D., Sarkar, R., Sajem, A.L., Panja, S., Rout, J. and Mandal, N., 2013. An antioxidant extract of tropical lichen, Parmotrema reticulatum, induces cell cycle arrest and apoptosis in breast carcinoma cell line MCF-7. Plos One, 8, e82293.
  • Giglio, P., 2010. Chemotherapy for glioblastoma: Past, present, and future, in: Ray, S.K. (Ed.), Glioblastoma: Molecular Mechanisms of Pathogenesis and Current Therapeutic Strategies. Springer New York, New York, NY, 203–216.
  • Grujičić, D., Stošić, I., Kosanić, M., Stanojković, T., Ranković, B. and Milošević-Djordjević, O., 2014. Evaluation of in vitro antioxidant, antimicrobial, genotoxic and anticancer activities of lichen Cetraria islandica. Cytotechnology, 66, 803–813.
  • Karatas, M., Dogan, M., Emsen, B. and Aasim, M., 2015. Determination of in vitro free radical scavenging activities of various extracts from in vitro propagated Ceratophyllum demersum L. Fresenius Environmental Bulletin, 24, 2946–2952.
  • Koçer, S., Uruş, S., Çakır, A., Güllüce, M., Dığrak, M., Alan, Y., Aslan, A., Tümer, M., Karadayı, M., Kazaz, C. and Dal, H., 2014. The synthesis, characterization, antimicrobial and antimutagenic activities of hydroxyphenylimino ligands and their metal complexes of usnic acid isolated from Usnea longissima. Dalton Transactions, 43, 6148–6164.
  • Kour, A., 2014. Plants exhibiting potential for cancer treatment. International Journal of Pharmaceutical Sciences Review and Research, 27, 23–53.
  • Kumar, J., Dhar, P., Tayade, A.B., Gupta, D., Chaurasia, O.P., Upreti, D.K., Arora, R. and Srivastava, R.B., 2014. Antioxidant capacities, phenolic profile and cytotoxic effects of saxicolous lichens from trans-Himalayan cold desert of Ladakh. Plos One, 9, e98696.
  • Laxinamu, J., Tang, Y.X., Bao, H.Y. and Bau, T., 2013. Chemical constituents from Usnea longgisima, atraditional mongolian medicine. Zhongguo Zhongyao Zazhi, 38, 2125–2128.
  • Manojlović, N., Ranković, B., Kosanić, M., Vasiljević, P. and Stanojković, T., 2012. Chemical composition of three Parmelia lichens and antioxidant, antimicrobial and cytotoxic activities of some their major metabolites. Phytomedicine, 19, 1166–1172.
  • Markiewicz-Żukowska, R., Naliwajko, S.K., Bartosiuk, E., Moskwa, J., Isidorov, V., Soroczyńska, J. and Borawska, M.H., 2013. Chemical composition and antioxidant activity of beebread, and its influence on the glioblastoma cell line (U87MG). Journal of Apicultural Science, 57, 147–157.
  • Mavrogenis, A.F., Papagelopoulos, P.J., Romantini, M., Angelini, A. and Ruggieri, P., 2010. Side effects of chemotherapy in musculoskeletal oncology. Journal of Long-Term Effects of Medical Implants, 20, 1–12.
  • Odimegwu, D.C., Ejikeugwu, C. and Esimone, C.C., 2015. Lichen Secondary Metabolites, in: Ranković, B. (Ed.), Lichen Secondary Metabolites: Bioactive Properties and Pharmaceutical Potential. Springer International Publishing, Cham, 165–177.
  • Ohgaki, H. and Kleihues, P., 2007. Genetic pathways to primary and secondary glioblastoma. The American Journal of Pathology, 170, 1445–1153.
  • Omar, A.I. and Mason, W.P., 2012. Anaplastic astrocytomas. Handbook of Clinical Neurology, 105, 451–466.
  • Paudel, B., Bhattarai, H.D., Pandey, D.P., Hur, J.S., Hong, S.G., Kim, I. and Yim, J.H., 2012. Antioxidant, antibacterial activity and brine shrimp toxicity test of some mountainous lichens from Nepal. Biological Research, 45, 387–391.
  • Perrino, C., Schiattarella, G.G., Magliulo, F., Ilardi, F., Carotenuto, G., Gargiulo, G., Serino, F., Ferrone, M., Scudiero, F., Carbone, A., Trimarco, B. and Esposito, G., 2014. Cardiac side effects of chemotherapy: State of art and strategies for a correct management. Current Vascular Pharmacology, 12, 106–116.
  • Rao, S.A.M., Srinivasan, S., Patric, I.R.P., Hegde, A.S., Chandramouli, B.A., Arimappamagan, A., Santosh, V., Kondaiah, P., Sathyanarayana Rao, M.R. and Somasundaram, K., 2014. A 16-gene signature distinguishes anaplastic astrocytoma from glioblastoma. Plos One, 9, e85200. Reed, M., 2009. Principles of cancer treatment by surgery. Surgery, 27, 178–181.
  • Shrestha, G., El-naggar, A.M., Clair, L.L.S. and Neill, K.L.O., 2015. Anticancer activities of selected species of North American lichen extracts. Phytotherapy Research, 29, 100–107.
  • Smoll, N.R., Schaller, K. and Gautschi, O.P., 2013. Long-term survival of patients with glioblastoma multiforme (GBM). Journal of Clinical Neuroscience, 20, 670–675.
  • Somasundaram, K., Reddy, S.P., Vinnakota, K., Britto, R., Subbarayan, M., Nambiar, S., Hebbar, A., Samuel, C., Shetty, M., Sreepathi, H.K., Santosh, V., Hegde, A.S., Hegde, S., Kondaiah, P. and Rao, M., 2005. Upregulation of ASCL1 and inhibition of Notch signaling pathway characterize progressive astrocytoma. Oncogene, 24, 7073–7083.
  • Sundararaj, J.P., Kuppuraj, S., Ganesan, A., Ponnusamy, P. and Nayaka, S., 2015. In vitro assesssment of antioxidant and antimicrobial activities of different solvent extracts from lichen Ramalina nervulosa. International Journal of Pharmacy and Pharmaceutical Sciences, 7, 200–204.
  • Thadhani, V.M., Choudhary, M.I., Ali, S., Omar, I., Siddique, H. and Karunaratne, V., 2011. Antioxidant activity of some lichen metabolites. Natural Product Research, 25, 1827–1837.
  • Varol, M., Tay, T., Candan, M., Türk, A. and Koparal, A.T., 2015. Evaluation of the sunscreen lichen substances usnic acid and atranorin. Biocell, 39, 25–31.
  • Wang, S., Huang, M., Li, J., Lai, F., Lee, H. and Hsu, Y., 2013. Punicalagin induces apoptotic and autophagic cell death in human U87MG glioma cells. Acta Pharmacologica Sinica, 34, 1411–1419.
  • Zeytinoglu, H., Incesu, Z., Tuylu, B.A., Turk, A.O. and Barutca, B., 2008. Determination of genotoxic, antigenotoxic and cytotoxic potential of the extract from lichen Cetraria aculeata (Schreb.) Fr. in vitro. Phytotherapy Research, 22, 118–123.
  • Zhang, X., Zhang, W., Cao, W.D., Cheng, G. and Zhang, Y.Q., 2012. Glioblastoma multiforme: Molecular characterization and current treatment strategy (Review). Experimental and Therapeutic Medicine, 3, 9–14.
Year 2018, Volume: 18 Issue: 3, 763 - 773, 30.12.2018

Abstract

References

  • Abuiraq, L., Kanan, G., Wedyan, M. and El-Oqlah, A., 2015. Efficacy of extracts of some lichens for potential antibacterial activity. Research Journal of Pharmaceutical, Biological and Chemical Sciences, 6, 318–331.
  • Alpsoy, L., Aslan, A., Kotan, E., Agar, G. and Anar, M., 2011. Protective role of two lichens in human lymphocytes in vitro. Fresenius Environmental Bulletin, 20, 1661–1666.
  • Ari, F., Celikler, S., Oran, S., Balikci, N., Ozturk, S., Ozel, M.Z., Ozyurt, D. and Ulukaya, E., 2014. Genotoxic, cytotoxic, and apoptotic effects of Hypogymnia physodes (L.) Nyl. on breast cancer cells. Environmental Toxicology, 29, 804–813.
  • Bai, L., Bao, H.Y. and Bau, T., 2014. Isolation and identification of a new benzofuranone derivative from Usnea longissima. Natural Product Research, 28, 534–538.
  • Bézivin, C., Tomasi, S., Lohézic-Le Dévéhat, F. and Boustie, J., 2003. Cytotoxic activity of some lichen extracts on murine and human cancer cell lines. Phytomedicine, 10, 499–503.
  • Bézivin, C., Tomasi, S., Rouaud, I., Delcros, J.G. and Boustie, J., 2004. Cytotoxic activity of compounds from the lichen: Cladonia convoluta. Planta Medica, 70, 874–877.
  • Bosset, J.-F., Collette, L., Calais, G., Mineur, L., Maingon, P., Radosevic-Jelic, L., Daban, A., Bardet, E., Beny, A., Ollier, J.-C. and EORTC Radiotherapy Group Trial 22921, 2006. Chemotherapy with preoperative radiotherapy in rectal cancer. The New England Journal of Medicine, 355, 1114–1123.
  • Boustie, J. and Grube, M., 2005. Lichens-A promising source of bioactive secondary metabolites. Plant Genetic Resources, 3, 273–287.
  • Brisdelli, F., Perilli, M., Sellitri, D., Piovano, M., Garbarino, J.A., Nicoletti, M., Bozzi, A., Amicosante, G. and Celenza, G., 2013. Cytotoxic activity and antioxidant capacity of purified lichen metabolites: an in vitro study. Phytotherapy Research, 27, 431–437.
  • Brodo, I.M., Sharnoff, S.D. and Sharnoff, S., 2001. About the Lichens, in: Lichens of North America. Yale University Press, New Haven & London, 3–113.
  • Clarke, J., Penas, C., Pastori, C., Komotar, R.J., Bregy, A., Shah, A.H., Wahlestedt, C. and Ayad, N.G., 2013. Epigenetic pathways and glioblastoma treatment. Epigenetics, 8, 785–795.
  • Çelikler Kasımoğulları, S., Oran, S., Ari, F., Ulukaya, E., Aztopal, N., Sarimahmut, M. and Öztürk, Ş., 2014. Genotoxic, cytotoxic, and apoptotic effects of crude extract of Usnea filipendula Stirt. in vitro. Turkish Journal of Biology, 38, 940–947.
  • Dogan, M., Emsen, B., Aasim, M. and Yildirim, E., 2017. Ceratophyllum demersum L. extract as a botanical insecticide for controlling the maize weevil, Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae). Egyptian Journal of Biological Pest Control, 27, 11–15.
  • Einarsdóttir, E., Groeneweg, J., Björnsdóttir, G.G., Harethardottir, G., Omarsdóttir, S., Ingólfsdóttir, K. and Ogmundsdóttir, H.M., 2010. Cellular mechanisms of the anticancer effects of the lichen compound usnic acid. Planta Medica, 76, 969–974.
  • Emsen, B., Aslan, A., Togar, B. and Turkez, H., 2016a. In vitro antitumor activities of the lichen compounds olivetoric, physodic and psoromic acid in rat neuron and glioblastoma cells. Pharmaceutical Biology, 54, 1748–1762.
  • Emsen, B., Dogan, M., Aasim, M. and Yildirim, E., 2016b. Insecticidal activity of in vitro propagated aquatic plant Ceratophyllum demersum L. against granary weevil Sitophilus granarius L. (Coleoptera: Curculionidae). Egyptian Journal of Biological Pest Control, 26, 619–624.
  • Emsen, B., Turkez, H., Togar, B. and Aslan, A., 2017. Evaluation of antioxidant and cytotoxic effects of olivetoric and physodic acid in cultured human amnion fibroblasts. Human & Experimental Toxicology, 36, 376–385.
  • Emsen, B., Yildirim, E. and Aslan, A., 2015. Insecticidal activities of extracts of three lichen species on Sitophilus granarius (L.) (Coleoptera: Curculionidae). Plant Protection Science, 51, 156–161.
  • Emsen, B., Yildirim, E., Aslan, A., Anar, M. and Ercisli, S., 2012. Insecticidal effect of the extracts of Cladonia foliacea (Huds.) Willd. and Flavoparmelia caperata (L.) Hale against adults of the grain weevil, Sitophilus granarius (L.) (Coleoptera: Curculionidae). Egyptian Journal of Biological Pest Control, 22, 145–149.
  • Feng, J., Yang, X., Su, S. and He, C., 2009. Studies on chemical constituents from herbs of Usnea longissima. Zhongguo Zhongyao Zazhi, 34, 708–711.
  • Gan, W., Nie, B., Shi, F., Xu, X.M., Qian, J.C., Takagi, Y., Hayakawa, H., Sekiguchi, M. and Cai, J.P., 2012. Age-dependent increases in the oxidative damage of DNA, RNA, and their metabolites in normal and senescence-accelerated mice analyzed by LC-MS/MS: urinary 8-oxoguanosine as a novel biomarker of aging. Free Radical Biology & Medicine, 52, 1700–1707.
  • Gauden, A.J., Hunn, A., Erasmus, A., Waites, P., Dubey, A. and Gauden, S.J., 2009. Combined modality treatment of newly diagnosed glioblastoma multiforme in a regional neurosurgical centre. Journal of Clinical Neuroscience, 16, 1174–1179.
  • Ghate, N.B., Chaudhuri, D., Sarkar, R., Sajem, A.L., Panja, S., Rout, J. and Mandal, N., 2013. An antioxidant extract of tropical lichen, Parmotrema reticulatum, induces cell cycle arrest and apoptosis in breast carcinoma cell line MCF-7. Plos One, 8, e82293.
  • Giglio, P., 2010. Chemotherapy for glioblastoma: Past, present, and future, in: Ray, S.K. (Ed.), Glioblastoma: Molecular Mechanisms of Pathogenesis and Current Therapeutic Strategies. Springer New York, New York, NY, 203–216.
  • Grujičić, D., Stošić, I., Kosanić, M., Stanojković, T., Ranković, B. and Milošević-Djordjević, O., 2014. Evaluation of in vitro antioxidant, antimicrobial, genotoxic and anticancer activities of lichen Cetraria islandica. Cytotechnology, 66, 803–813.
  • Karatas, M., Dogan, M., Emsen, B. and Aasim, M., 2015. Determination of in vitro free radical scavenging activities of various extracts from in vitro propagated Ceratophyllum demersum L. Fresenius Environmental Bulletin, 24, 2946–2952.
  • Koçer, S., Uruş, S., Çakır, A., Güllüce, M., Dığrak, M., Alan, Y., Aslan, A., Tümer, M., Karadayı, M., Kazaz, C. and Dal, H., 2014. The synthesis, characterization, antimicrobial and antimutagenic activities of hydroxyphenylimino ligands and their metal complexes of usnic acid isolated from Usnea longissima. Dalton Transactions, 43, 6148–6164.
  • Kour, A., 2014. Plants exhibiting potential for cancer treatment. International Journal of Pharmaceutical Sciences Review and Research, 27, 23–53.
  • Kumar, J., Dhar, P., Tayade, A.B., Gupta, D., Chaurasia, O.P., Upreti, D.K., Arora, R. and Srivastava, R.B., 2014. Antioxidant capacities, phenolic profile and cytotoxic effects of saxicolous lichens from trans-Himalayan cold desert of Ladakh. Plos One, 9, e98696.
  • Laxinamu, J., Tang, Y.X., Bao, H.Y. and Bau, T., 2013. Chemical constituents from Usnea longgisima, atraditional mongolian medicine. Zhongguo Zhongyao Zazhi, 38, 2125–2128.
  • Manojlović, N., Ranković, B., Kosanić, M., Vasiljević, P. and Stanojković, T., 2012. Chemical composition of three Parmelia lichens and antioxidant, antimicrobial and cytotoxic activities of some their major metabolites. Phytomedicine, 19, 1166–1172.
  • Markiewicz-Żukowska, R., Naliwajko, S.K., Bartosiuk, E., Moskwa, J., Isidorov, V., Soroczyńska, J. and Borawska, M.H., 2013. Chemical composition and antioxidant activity of beebread, and its influence on the glioblastoma cell line (U87MG). Journal of Apicultural Science, 57, 147–157.
  • Mavrogenis, A.F., Papagelopoulos, P.J., Romantini, M., Angelini, A. and Ruggieri, P., 2010. Side effects of chemotherapy in musculoskeletal oncology. Journal of Long-Term Effects of Medical Implants, 20, 1–12.
  • Odimegwu, D.C., Ejikeugwu, C. and Esimone, C.C., 2015. Lichen Secondary Metabolites, in: Ranković, B. (Ed.), Lichen Secondary Metabolites: Bioactive Properties and Pharmaceutical Potential. Springer International Publishing, Cham, 165–177.
  • Ohgaki, H. and Kleihues, P., 2007. Genetic pathways to primary and secondary glioblastoma. The American Journal of Pathology, 170, 1445–1153.
  • Omar, A.I. and Mason, W.P., 2012. Anaplastic astrocytomas. Handbook of Clinical Neurology, 105, 451–466.
  • Paudel, B., Bhattarai, H.D., Pandey, D.P., Hur, J.S., Hong, S.G., Kim, I. and Yim, J.H., 2012. Antioxidant, antibacterial activity and brine shrimp toxicity test of some mountainous lichens from Nepal. Biological Research, 45, 387–391.
  • Perrino, C., Schiattarella, G.G., Magliulo, F., Ilardi, F., Carotenuto, G., Gargiulo, G., Serino, F., Ferrone, M., Scudiero, F., Carbone, A., Trimarco, B. and Esposito, G., 2014. Cardiac side effects of chemotherapy: State of art and strategies for a correct management. Current Vascular Pharmacology, 12, 106–116.
  • Rao, S.A.M., Srinivasan, S., Patric, I.R.P., Hegde, A.S., Chandramouli, B.A., Arimappamagan, A., Santosh, V., Kondaiah, P., Sathyanarayana Rao, M.R. and Somasundaram, K., 2014. A 16-gene signature distinguishes anaplastic astrocytoma from glioblastoma. Plos One, 9, e85200. Reed, M., 2009. Principles of cancer treatment by surgery. Surgery, 27, 178–181.
  • Shrestha, G., El-naggar, A.M., Clair, L.L.S. and Neill, K.L.O., 2015. Anticancer activities of selected species of North American lichen extracts. Phytotherapy Research, 29, 100–107.
  • Smoll, N.R., Schaller, K. and Gautschi, O.P., 2013. Long-term survival of patients with glioblastoma multiforme (GBM). Journal of Clinical Neuroscience, 20, 670–675.
  • Somasundaram, K., Reddy, S.P., Vinnakota, K., Britto, R., Subbarayan, M., Nambiar, S., Hebbar, A., Samuel, C., Shetty, M., Sreepathi, H.K., Santosh, V., Hegde, A.S., Hegde, S., Kondaiah, P. and Rao, M., 2005. Upregulation of ASCL1 and inhibition of Notch signaling pathway characterize progressive astrocytoma. Oncogene, 24, 7073–7083.
  • Sundararaj, J.P., Kuppuraj, S., Ganesan, A., Ponnusamy, P. and Nayaka, S., 2015. In vitro assesssment of antioxidant and antimicrobial activities of different solvent extracts from lichen Ramalina nervulosa. International Journal of Pharmacy and Pharmaceutical Sciences, 7, 200–204.
  • Thadhani, V.M., Choudhary, M.I., Ali, S., Omar, I., Siddique, H. and Karunaratne, V., 2011. Antioxidant activity of some lichen metabolites. Natural Product Research, 25, 1827–1837.
  • Varol, M., Tay, T., Candan, M., Türk, A. and Koparal, A.T., 2015. Evaluation of the sunscreen lichen substances usnic acid and atranorin. Biocell, 39, 25–31.
  • Wang, S., Huang, M., Li, J., Lai, F., Lee, H. and Hsu, Y., 2013. Punicalagin induces apoptotic and autophagic cell death in human U87MG glioma cells. Acta Pharmacologica Sinica, 34, 1411–1419.
  • Zeytinoglu, H., Incesu, Z., Tuylu, B.A., Turk, A.O. and Barutca, B., 2008. Determination of genotoxic, antigenotoxic and cytotoxic potential of the extract from lichen Cetraria aculeata (Schreb.) Fr. in vitro. Phytotherapy Research, 22, 118–123.
  • Zhang, X., Zhang, W., Cao, W.D., Cheng, G. and Zhang, Y.Q., 2012. Glioblastoma multiforme: Molecular characterization and current treatment strategy (Review). Experimental and Therapeutic Medicine, 3, 9–14.
There are 48 citations in total.

Details

Primary Language English
Journal Section Articles
Authors

Bugrahan Emsen

Tubanur Engin This is me

Hasan Turkez This is me

Publication Date December 30, 2018
Submission Date January 27, 2018
Published in Issue Year 2018 Volume: 18 Issue: 3

Cite

APA Emsen, B., Engin, T., & Turkez, H. (2018). In Vitro Investigation of the Anticancer Activity of Friedelin in Glioblastoma Multiforme. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi, 18(3), 763-773.
AMA Emsen B, Engin T, Turkez H. In Vitro Investigation of the Anticancer Activity of Friedelin in Glioblastoma Multiforme. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi. December 2018;18(3):763-773.
Chicago Emsen, Bugrahan, Tubanur Engin, and Hasan Turkez. “In Vitro Investigation of the Anticancer Activity of Friedelin in Glioblastoma Multiforme”. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi 18, no. 3 (December 2018): 763-73.
EndNote Emsen B, Engin T, Turkez H (December 1, 2018) In Vitro Investigation of the Anticancer Activity of Friedelin in Glioblastoma Multiforme. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi 18 3 763–773.
IEEE B. Emsen, T. Engin, and H. Turkez, “In Vitro Investigation of the Anticancer Activity of Friedelin in Glioblastoma Multiforme”, Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi, vol. 18, no. 3, pp. 763–773, 2018.
ISNAD Emsen, Bugrahan et al. “In Vitro Investigation of the Anticancer Activity of Friedelin in Glioblastoma Multiforme”. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi 18/3 (December 2018), 763-773.
JAMA Emsen B, Engin T, Turkez H. In Vitro Investigation of the Anticancer Activity of Friedelin in Glioblastoma Multiforme. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi. 2018;18:763–773.
MLA Emsen, Bugrahan et al. “In Vitro Investigation of the Anticancer Activity of Friedelin in Glioblastoma Multiforme”. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi, vol. 18, no. 3, 2018, pp. 763-7.
Vancouver Emsen B, Engin T, Turkez H. In Vitro Investigation of the Anticancer Activity of Friedelin in Glioblastoma Multiforme. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi. 2018;18(3):763-7.