Apoptotic Induction Mechanism of Artonin E in 3D Ovarian Cancer Cell Lines
Keywords:
Apoptosis, Ovarian Cancer, Artonin E, Artocarpus elasticus, 3D-culture
Abstract
Artonin E is a naturally isolated compound from Artocarpus elasticus and was evaluated for their anticancer property in the present study. This study aimed to develop a 3D ovarian cell culture model and to examine the cytotoxicity of artonin E in 2D and 3D cell culture models. The 3D cell culture was performed using BD™ Puramatrix™ Peptide Hydrogel. Alamar blue assay, selectivity index analysis, morphological apoptotic double staining and immunofluorescence study were conducted to study the antiproliferative and apoptotic induction mechanism of artonin E in 3D SKOV-3 spheroid culture. SKOV-3 cells encapsulated in BD™ Puramatrix™ Peptide Hydrogel clearly demonstrated 3D-spheroid formation. The Alamar blue assay result showed that artonin E inhibited the growth of SKOV-3 cells in 2D and 3D culture with the IC50 values at 72 h treatment of 6.0 ± 0.8 µg/mL and 25.0 ± 0.8 µg/mL, respectively. This compound was found to be less toxic to the normal human ovarian cell lines, T1074, with IC50 values at 72 h of 28.0 ± 0.8 µg/mL in 2D culture and 85.0 ± 0.5 µg/mL in 3D culture, respectively. The selectivity index analysis more than 2 indicated that artonin E was selective against cancer cells compared to normal cells. Artonin E treatment caused apoptotic morphological changes in 3D SKOV-3 spheroids. In a 3D immunofluorescence study, elevated levels of cleaved caspase-3, cleaved caspase-9, apoptotic proteins bax, and decreased levels of antiapoptotic proteins bcl-2, Hsp70, and survivin were observed. In conclusion, artonin E increases chemoresistance and induces cell death in a 3D SKOV-3 spheroids culture via a pro- and anti-apoptotic protein pathway. These findings demonstrate that 3D spheroid culture is an effective platform for testing artonin E therapeutic candidates in an in vivo mimic microenvironment.
References
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Badea, M. A., Balas, M., Hermenean, A., Ciceu, A., Herman, H., Ionita, D., & Dinischiotu, A. (2019). Influence of Matrigel on Single- and Multiple-Spheroid Cultures in Breast Cancer Research. SLAS Discovery. https://doi.org/10.1177/2472555219834698
Boice, A., & Bouchier-Hayes, L. (2020). Targeting apoptotic caspases in cancer. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research, 118688.
Bonnier, F., Keating, M. E., Wrobel, T. P., Majzner, K., Baranska, M., Garcia-Munoz, A., … Byrne, H. J. (2015). Cell viability assessment using the Alamar blue assay: a comparison of 2D and 3D cell culture models. Toxicology in Vitro, 29(1), 124–131.
Borghese, C., Casagrande, N., Corona, G., & Aldinucci, D. (2020). Adipose-Derived Stem Cells Primed with Paclitaxel Inhibit Ovarian Cancer Spheroid Growth and Overcome Paclitaxel Resistance. Pharmaceutics, 12(5), 401.
Bray, F., Ferlay, J., Soerjomataram, I., Siegel, R. L., Torre, L. A., & Jemal, A. (2018). Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: A Cancer Journal for Clinicians, 68(6), 394–424.
Brüningk, S. C., Rivens, I., Box, C., Oelfke, U., & ter Haar, G. (2020). 3D tumour spheroids for the prediction of the effects of radiation and hyperthermia treatments. Scientific Reports. https://doi.org/10.1038/s41598-020-58569-4
Calderón-Montaño, J. M., Martínez-Sánchez, S. M., Burgos-Morón, E., Guillén-Mancina, E., Jiménez-Alonso, J. J., García, F., … López-Lázaro, M. (2019). Screening for selective anticancer activity of plants from Grazalema Natural Park, Spain. Natural Product Research, 33(23), 3454–3458.
D’Arcy, M. S. (2019). Cell death: a review of the major forms of apoptosis, necrosis and autophagy. Cell Biology International.
Dochez, V., Caillon, H., Vaucel, E., Dimet, J., Winer, N., & Ducarme, G. (2019). Biomarkers and algorithms for diagnosis of ovarian cancer: CA125, HE4, RMI and ROMA, a review. Journal of Ovarian Research, 12(1), 1–9.
Elmallah, M. I. Y., Cordonnier, M., Vautrot, V., Chanteloup, G., Garrido, C., & Gobbo, J. (2020). Membrane-anchored heat-shock protein 70 (Hsp70) in cancer. Cancer Letters, 469, 134–141.
Godugu, C., Patel, A. R., Desai, U., Andey, T., Sams, A., & Singh, M. (2013). AlgiMatrixTM Based 3D Cell Culture System as an In-Vitro Tumor Model for Anticancer Studies. PLoS ONE. https://doi.org/10.1371/journal.pone.0053708
Goldar, S., Khaniani, M. S., Derakhshan, S. M., & Baradaran, B. (2015). Molecular mechanisms of apoptosis and roles in cancer development and treatment. Asian Pacific Journal of Cancer Prevention, 16(6), 2129–2144.
Hadi, L. M., Yaghini, E., Stamati, K., Loizidou, M., & MacRobert, A. J. (2018). Therapeutic enhancement of a cytotoxic agent using photochemical internalisation in 3D compressed collagen constructs of ovarian cancer. Acta Biomaterialia. https://doi.org/10.1016/j.actbio.2018.09.041
Hassan, M., Watari, H., AbuAlmaaty, A., Ohba, Y., & Sakuragi, N. (2014). Apoptosis and molecular targeting therapy in cancer. BioMed Research International, 2014.
Hennigs, J. K., Minner, S., Tennstedt, P., Löser, R., Huland, H., Klose, H., … Bokemeyer, C. (2020). Subcellular compartmentalization of Survivin is Associated with Biological Aggressiveness and prognosis in prostate cancer. Scientific Reports, 10(1), 1–9.
Ibrahim, M. Y., Hashim, N. M., Mohan, S., Abdulla, M. A., Abdelwahab, S. I., Kamalidehghan, B., … Karimian, H. (2017). Involvement of NF-κB and HSP70 signaling pathways in the apoptosis of MDA-MB-231 cells induced by a prenylated xanthone compound, α-mangostin, from Cratoxylum arborescens [Retraction]. Drug Design, Development and Therapy, 11, 1399–1400.
Indrayanto, G., Putra, G. S., & Suhud, F. (2020). Validation of in-vitro bioassay methods: Application in herbal drug research. Profiles of Drug Substances, Excipients, and Related Methodology, 46, 273–307.
Jamali, T., Kavoosi, G., & Ardestani, S. K. (2020). In-vitro and in-vivo anti-breast cancer activity of OEO (Oliveria decumbens vent essential oil) through promoting the apoptosis and immunomodulatory effects. Journal of Ethnopharmacology. https://doi.org/10.1016/j.jep.2019.112313
Jamali, T., Kavoosi, G., Safavi, M., & Ardestani, S. K. (2018). In-vitro evaluation of apoptotic effect of OEO and thymol in 2D and 3D cell cultures and the study of their interaction mode with DNA. Scientific Reports. https://doi.org/10.1038/s41598-018-34055-w
Jensen, C., & Teng, Y. (2020). Is It Time to Start Transitioning From 2D to 3D Cell Culture? Frontiers in Molecular Biosciences. https://doi.org/10.3389/fmolb.2020.00033
Jones, M. R., Kamara, D., Karlan, B. Y., Pharoah, P. D. P., & Gayther, S. A. (2017). Genetic epidemiology of ovarian cancer and prospects for polygenic risk prediction. Gynecologic Oncology, 147(3), 705–713.
Kuete, V., Ango, P. Y., Fotso, G. W., Dwf Kapche, G., Dzoyem, J. P., Wouking, A. G., … Abegaz, B. M. (2011). Antimicrobial activities of the methanol extract and compounds from Artocarpus communis (Moraceae). https://doi.org/10.1186/1472-6882-11-42
Langhans, S. A. (2021). Using 3D in vitro cell culture models in anti-cancer drug discovery. Expert Opinion on Drug Discovery, (just-accepted).
Lee, E. F., Harris, T. J., Tran, S., Evangelista, M., Arulananda, S., John, T., … Gunasingh, G. (2019). BCL-XL and MCL-1 are the key BCL-2 family proteins in melanoma cell survival. Cell Death & Disease, 10(5), 1–14.
Lehar, J., Krueger, A. S., Zimmermann, G. R., & Borisy, A. A. (2009). Therapeutic selectivity and the multi-node drug target. Discovery Medicine, 8(43), 185–190.
Li-Weber, M. (2013). Targeting apoptosis pathways in cancer by Chinese medicine. Cancer Letters, 332(2), 304–312.
Loessner, D., Stok, K. S., Lutolf, M. P., Hutmacher, D. W., Clements, J. A., & Rizzi, S. C. (2010). Bioengineered 3D platform to explore cell-ECM interactions and drug resistance of epithelial ovarian cancer cells. Biomaterials. https://doi.org/10.1016/j.biomaterials.2010.07.064
López-Lázaro, M. (2015). How many times should we screen a chemical library to discover an anticancer drug? Drug Discovery Today, 2(20), 167–169.
Nayak, M., Nagarajan, A., Majeed, M., & Choudhury, A. K. (2018). In vitro anti-acne activity of phytoactives from the stem bark of Artocarpus hirsutus Lam . and characterisation of pyranocycloartobiloxanthone A as a mixture of two anomers. Natural Product Research, 6419, 1–5. https://doi.org/10.1080/14786419.2017.1365068
Nunes, A. S., Barros, A. S., Costa, E. C., Moreira, A. F., & Correia, I. J. (2019). 3D tumor spheroids as in vitro models to mimic in vivo human solid tumors resistance to therapeutic drugs. Biotechnology and Bioengineering, 116(1), 206–226.
Orr, B., & Edwards, R. P. (2018). Diagnosis and treatment of ovarian cancer. Hematology/Oncology Clinics, 32(6), 943–964.
Pfeffer, C., & Singh, A. (2018). Apoptosis: a target for anticancer therapy. International Journal of Molecular Sciences, 19(2), 448.
Rahman, M.A., Ramli, F., Karimian, H., Dehghan, F., Nordin, N., Ali, H. M., … Hashim, N. M. (2016). Artonin E induces apoptosis via mitochondrial dysregulation in SKOV-3 ovarian cancer cells. PLoS ONE, 11(3). https://doi.org/10.1371/journal.pone.0151466
Rahman, Mashitoh Abd, Ramli, F., Karimian, H., Dehghan, F., Nordin, N., Mohd Ali, H., … Mohd Hashim, N. (2016). Artonin E Induces Apoptosis via Mitochondrial Dysregulation in SKOV-3 Ovarian Cancer Cells. PLOS ONE, 11(3), e0151466. https://doi.org/10.1371/journal.pone.0151466
Rahman, S. F. A., Muniandy, K., Soo, Y. K., Tiew, E. Y. H., Tan, K. X., Bates, T. E., & Mohana-Kumaran, N. (2020). Co-inhibition of BCL-XL and MCL-1 with selective BCL-2 family inhibitors enhances cytotoxicity of cervical cancer cell lines. Biochemistry and Biophysics Reports, 22, 100756.
Ramli, F., Rahmani, M., Ismail, I. S., Sukari, M. A., Rahman, M. A., Zajmi, A., … Go, R. (2016). A new bioactive secondary metabolite from artocarpus elasticus. Natural Product Communications, 11(8).
Rolver, M. G., Elingaard-Larsen, L. O., & Pedersen, S. F. (2019). Assessing cell viability and death in 3d spheroid cultures of cancer cells. Journal of Visualized Experiments. https://doi.org/10.3791/59714
Roth, A. D., Lama, P., Dunn, S., Hong, S., & Lee, M. Y. (2018). Polymer coating on a micropillar chip for robust attachment of PuraMatrix peptide hydrogel for 3D hepatic cell culture. Materials Science and Engineering C. https://doi.org/10.1016/j.msec.2018.04.092
Salehi, F., Behboudi, H., Kavoosi, G., & Ardestani, S. K. (2017). Monitoring ZEO apoptotic potential in 2D and 3D cell cultures and associated spectroscopic evidence on mode of interaction with DNA. Scientific Reports. https://doi.org/10.1038/s41598-017-02633-z
Segun, P. A., Ogbole, O. O., Ismail, F. M. D., Nahar, L., Evans, A. R., Ajaiyeoba, E. O., & Sarker, S. D. (2019). Resveratrol derivatives from Commiphora africana (A. Rich.) Endl. display cytotoxicity and selectivity against several human cancer cell lines. Phytotherapy Research, 33(1), 159–166.
Stewart, C., Ralyea, C., & Lockwood, S. (2019). Ovarian cancer: an integrated review. In Seminars in oncology nursing (Vol. 35, pp. 151–156). Elsevier.
Suhartati, T., Yandri, Y., Suwandi, J. F., & Hadi, S. (2010). In vitro and in vivo antiplasmodial activity of oxyresveratrol and artonine isolated from two Artocarpus plants in Indonesia. Oriental Journal of Chemistry, 26(3), 825–830.
Torre, L. A., Trabert, B., DeSantis, C. E., Miller, K. D., Samimi, G., Runowicz, C. D., … Siegel, R. L. (2018). Ovarian cancer statistics, 2018. CA: A Cancer Journal for Clinicians, 68(4), 284–296.
Tsunoda, T., Ishikura, S., Doi, K., Matsuzaki, H., Iwaihara, Y., & Shirasawa, S. (2014). Resveratrol induces luminal apoptosis of human colorectal cancer HCT116 cells in three-dimensional culture. In Anticancer Research.
Weiswald, L. B., Bellet, D., & Dangles-Marie, V. (2015). Spherical Cancer Models in Tumor Biology. Neoplasia (United States). https://doi.org/10.1016/j.neo.2014.12.004
Xin, X., Wu, Y., Zang, R., & Yang, S. T. (2019). A fluorescent 3D cell culture assay for high throughput screening of cancer drugs down-regulating survivin. Journal of Biotechnology. https://doi.org/10.1016/j.jbiotec.2018.11.018
Zajmi, A., Hashim, N. M., Noordin, M. I., Khalifa, S. A. M., Ramli, F., Ali, H. M., & El-Seedi, H. R. (2015). Ultrastructural study on the antibacterial activity of artonin e versus streptomycin against Staphylococcus aureus strains. PLoS One, 10(6), e0128157.
Zhao, Y., Onda, K., Yuan, B., Tanaka, S., Kiyomi, A., Sugiyama, K., … Hirano, T. (2018). Arsenic disulfide-induced apoptosis and its potential mechanism in two-And three-dimensionally cultured human breast cancer MCF-7 cells. International Journal of Oncology. https://doi.org/10.3892/ijo.2018.4357
Agrawal, S. N. (2019). The Vital Phenomena of Apoptosis: A Review. South Asian Res. J. Med. Sci, 1(1), 15–193.
Badea, M. A., Balas, M., Hermenean, A., Ciceu, A., Herman, H., Ionita, D., & Dinischiotu, A. (2019). Influence of Matrigel on Single- and Multiple-Spheroid Cultures in Breast Cancer Research. SLAS Discovery. https://doi.org/10.1177/2472555219834698
Boice, A., & Bouchier-Hayes, L. (2020). Targeting apoptotic caspases in cancer. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research, 118688.
Bonnier, F., Keating, M. E., Wrobel, T. P., Majzner, K., Baranska, M., Garcia-Munoz, A., … Byrne, H. J. (2015). Cell viability assessment using the Alamar blue assay: a comparison of 2D and 3D cell culture models. Toxicology in Vitro, 29(1), 124–131.
Borghese, C., Casagrande, N., Corona, G., & Aldinucci, D. (2020). Adipose-Derived Stem Cells Primed with Paclitaxel Inhibit Ovarian Cancer Spheroid Growth and Overcome Paclitaxel Resistance. Pharmaceutics, 12(5), 401.
Bray, F., Ferlay, J., Soerjomataram, I., Siegel, R. L., Torre, L. A., & Jemal, A. (2018). Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: A Cancer Journal for Clinicians, 68(6), 394–424.
Brüningk, S. C., Rivens, I., Box, C., Oelfke, U., & ter Haar, G. (2020). 3D tumour spheroids for the prediction of the effects of radiation and hyperthermia treatments. Scientific Reports. https://doi.org/10.1038/s41598-020-58569-4
Calderón-Montaño, J. M., Martínez-Sánchez, S. M., Burgos-Morón, E., Guillén-Mancina, E., Jiménez-Alonso, J. J., García, F., … López-Lázaro, M. (2019). Screening for selective anticancer activity of plants from Grazalema Natural Park, Spain. Natural Product Research, 33(23), 3454–3458.
D’Arcy, M. S. (2019). Cell death: a review of the major forms of apoptosis, necrosis and autophagy. Cell Biology International.
Dochez, V., Caillon, H., Vaucel, E., Dimet, J., Winer, N., & Ducarme, G. (2019). Biomarkers and algorithms for diagnosis of ovarian cancer: CA125, HE4, RMI and ROMA, a review. Journal of Ovarian Research, 12(1), 1–9.
Elmallah, M. I. Y., Cordonnier, M., Vautrot, V., Chanteloup, G., Garrido, C., & Gobbo, J. (2020). Membrane-anchored heat-shock protein 70 (Hsp70) in cancer. Cancer Letters, 469, 134–141.
Godugu, C., Patel, A. R., Desai, U., Andey, T., Sams, A., & Singh, M. (2013). AlgiMatrixTM Based 3D Cell Culture System as an In-Vitro Tumor Model for Anticancer Studies. PLoS ONE. https://doi.org/10.1371/journal.pone.0053708
Goldar, S., Khaniani, M. S., Derakhshan, S. M., & Baradaran, B. (2015). Molecular mechanisms of apoptosis and roles in cancer development and treatment. Asian Pacific Journal of Cancer Prevention, 16(6), 2129–2144.
Hadi, L. M., Yaghini, E., Stamati, K., Loizidou, M., & MacRobert, A. J. (2018). Therapeutic enhancement of a cytotoxic agent using photochemical internalisation in 3D compressed collagen constructs of ovarian cancer. Acta Biomaterialia. https://doi.org/10.1016/j.actbio.2018.09.041
Hassan, M., Watari, H., AbuAlmaaty, A., Ohba, Y., & Sakuragi, N. (2014). Apoptosis and molecular targeting therapy in cancer. BioMed Research International, 2014.
Hennigs, J. K., Minner, S., Tennstedt, P., Löser, R., Huland, H., Klose, H., … Bokemeyer, C. (2020). Subcellular compartmentalization of Survivin is Associated with Biological Aggressiveness and prognosis in prostate cancer. Scientific Reports, 10(1), 1–9.
Ibrahim, M. Y., Hashim, N. M., Mohan, S., Abdulla, M. A., Abdelwahab, S. I., Kamalidehghan, B., … Karimian, H. (2017). Involvement of NF-κB and HSP70 signaling pathways in the apoptosis of MDA-MB-231 cells induced by a prenylated xanthone compound, α-mangostin, from Cratoxylum arborescens [Retraction]. Drug Design, Development and Therapy, 11, 1399–1400.
Indrayanto, G., Putra, G. S., & Suhud, F. (2020). Validation of in-vitro bioassay methods: Application in herbal drug research. Profiles of Drug Substances, Excipients, and Related Methodology, 46, 273–307.
Jamali, T., Kavoosi, G., & Ardestani, S. K. (2020). In-vitro and in-vivo anti-breast cancer activity of OEO (Oliveria decumbens vent essential oil) through promoting the apoptosis and immunomodulatory effects. Journal of Ethnopharmacology. https://doi.org/10.1016/j.jep.2019.112313
Jamali, T., Kavoosi, G., Safavi, M., & Ardestani, S. K. (2018). In-vitro evaluation of apoptotic effect of OEO and thymol in 2D and 3D cell cultures and the study of their interaction mode with DNA. Scientific Reports. https://doi.org/10.1038/s41598-018-34055-w
Jensen, C., & Teng, Y. (2020). Is It Time to Start Transitioning From 2D to 3D Cell Culture? Frontiers in Molecular Biosciences. https://doi.org/10.3389/fmolb.2020.00033
Jones, M. R., Kamara, D., Karlan, B. Y., Pharoah, P. D. P., & Gayther, S. A. (2017). Genetic epidemiology of ovarian cancer and prospects for polygenic risk prediction. Gynecologic Oncology, 147(3), 705–713.
Kuete, V., Ango, P. Y., Fotso, G. W., Dwf Kapche, G., Dzoyem, J. P., Wouking, A. G., … Abegaz, B. M. (2011). Antimicrobial activities of the methanol extract and compounds from Artocarpus communis (Moraceae). https://doi.org/10.1186/1472-6882-11-42
Langhans, S. A. (2021). Using 3D in vitro cell culture models in anti-cancer drug discovery. Expert Opinion on Drug Discovery, (just-accepted).
Lee, E. F., Harris, T. J., Tran, S., Evangelista, M., Arulananda, S., John, T., … Gunasingh, G. (2019). BCL-XL and MCL-1 are the key BCL-2 family proteins in melanoma cell survival. Cell Death & Disease, 10(5), 1–14.
Lehar, J., Krueger, A. S., Zimmermann, G. R., & Borisy, A. A. (2009). Therapeutic selectivity and the multi-node drug target. Discovery Medicine, 8(43), 185–190.
Li-Weber, M. (2013). Targeting apoptosis pathways in cancer by Chinese medicine. Cancer Letters, 332(2), 304–312.
Loessner, D., Stok, K. S., Lutolf, M. P., Hutmacher, D. W., Clements, J. A., & Rizzi, S. C. (2010). Bioengineered 3D platform to explore cell-ECM interactions and drug resistance of epithelial ovarian cancer cells. Biomaterials. https://doi.org/10.1016/j.biomaterials.2010.07.064
López-Lázaro, M. (2015). How many times should we screen a chemical library to discover an anticancer drug? Drug Discovery Today, 2(20), 167–169.
Nayak, M., Nagarajan, A., Majeed, M., & Choudhury, A. K. (2018). In vitro anti-acne activity of phytoactives from the stem bark of Artocarpus hirsutus Lam . and characterisation of pyranocycloartobiloxanthone A as a mixture of two anomers. Natural Product Research, 6419, 1–5. https://doi.org/10.1080/14786419.2017.1365068
Nunes, A. S., Barros, A. S., Costa, E. C., Moreira, A. F., & Correia, I. J. (2019). 3D tumor spheroids as in vitro models to mimic in vivo human solid tumors resistance to therapeutic drugs. Biotechnology and Bioengineering, 116(1), 206–226.
Orr, B., & Edwards, R. P. (2018). Diagnosis and treatment of ovarian cancer. Hematology/Oncology Clinics, 32(6), 943–964.
Pfeffer, C., & Singh, A. (2018). Apoptosis: a target for anticancer therapy. International Journal of Molecular Sciences, 19(2), 448.
Rahman, M.A., Ramli, F., Karimian, H., Dehghan, F., Nordin, N., Ali, H. M., … Hashim, N. M. (2016). Artonin E induces apoptosis via mitochondrial dysregulation in SKOV-3 ovarian cancer cells. PLoS ONE, 11(3). https://doi.org/10.1371/journal.pone.0151466
Rahman, Mashitoh Abd, Ramli, F., Karimian, H., Dehghan, F., Nordin, N., Mohd Ali, H., … Mohd Hashim, N. (2016). Artonin E Induces Apoptosis via Mitochondrial Dysregulation in SKOV-3 Ovarian Cancer Cells. PLOS ONE, 11(3), e0151466. https://doi.org/10.1371/journal.pone.0151466
Rahman, S. F. A., Muniandy, K., Soo, Y. K., Tiew, E. Y. H., Tan, K. X., Bates, T. E., & Mohana-Kumaran, N. (2020). Co-inhibition of BCL-XL and MCL-1 with selective BCL-2 family inhibitors enhances cytotoxicity of cervical cancer cell lines. Biochemistry and Biophysics Reports, 22, 100756.
Ramli, F., Rahmani, M., Ismail, I. S., Sukari, M. A., Rahman, M. A., Zajmi, A., … Go, R. (2016). A new bioactive secondary metabolite from artocarpus elasticus. Natural Product Communications, 11(8).
Rolver, M. G., Elingaard-Larsen, L. O., & Pedersen, S. F. (2019). Assessing cell viability and death in 3d spheroid cultures of cancer cells. Journal of Visualized Experiments. https://doi.org/10.3791/59714
Roth, A. D., Lama, P., Dunn, S., Hong, S., & Lee, M. Y. (2018). Polymer coating on a micropillar chip for robust attachment of PuraMatrix peptide hydrogel for 3D hepatic cell culture. Materials Science and Engineering C. https://doi.org/10.1016/j.msec.2018.04.092
Salehi, F., Behboudi, H., Kavoosi, G., & Ardestani, S. K. (2017). Monitoring ZEO apoptotic potential in 2D and 3D cell cultures and associated spectroscopic evidence on mode of interaction with DNA. Scientific Reports. https://doi.org/10.1038/s41598-017-02633-z
Segun, P. A., Ogbole, O. O., Ismail, F. M. D., Nahar, L., Evans, A. R., Ajaiyeoba, E. O., & Sarker, S. D. (2019). Resveratrol derivatives from Commiphora africana (A. Rich.) Endl. display cytotoxicity and selectivity against several human cancer cell lines. Phytotherapy Research, 33(1), 159–166.
Stewart, C., Ralyea, C., & Lockwood, S. (2019). Ovarian cancer: an integrated review. In Seminars in oncology nursing (Vol. 35, pp. 151–156). Elsevier.
Suhartati, T., Yandri, Y., Suwandi, J. F., & Hadi, S. (2010). In vitro and in vivo antiplasmodial activity of oxyresveratrol and artonine isolated from two Artocarpus plants in Indonesia. Oriental Journal of Chemistry, 26(3), 825–830.
Torre, L. A., Trabert, B., DeSantis, C. E., Miller, K. D., Samimi, G., Runowicz, C. D., … Siegel, R. L. (2018). Ovarian cancer statistics, 2018. CA: A Cancer Journal for Clinicians, 68(4), 284–296.
Tsunoda, T., Ishikura, S., Doi, K., Matsuzaki, H., Iwaihara, Y., & Shirasawa, S. (2014). Resveratrol induces luminal apoptosis of human colorectal cancer HCT116 cells in three-dimensional culture. In Anticancer Research.
Weiswald, L. B., Bellet, D., & Dangles-Marie, V. (2015). Spherical Cancer Models in Tumor Biology. Neoplasia (United States). https://doi.org/10.1016/j.neo.2014.12.004
Xin, X., Wu, Y., Zang, R., & Yang, S. T. (2019). A fluorescent 3D cell culture assay for high throughput screening of cancer drugs down-regulating survivin. Journal of Biotechnology. https://doi.org/10.1016/j.jbiotec.2018.11.018
Zajmi, A., Hashim, N. M., Noordin, M. I., Khalifa, S. A. M., Ramli, F., Ali, H. M., & El-Seedi, H. R. (2015). Ultrastructural study on the antibacterial activity of artonin e versus streptomycin against Staphylococcus aureus strains. PLoS One, 10(6), e0128157.
Zhao, Y., Onda, K., Yuan, B., Tanaka, S., Kiyomi, A., Sugiyama, K., … Hirano, T. (2018). Arsenic disulfide-induced apoptosis and its potential mechanism in two-And three-dimensionally cultured human breast cancer MCF-7 cells. International Journal of Oncology. https://doi.org/10.3892/ijo.2018.4357
Published
2022-03-17
How to Cite
Abd Rahman, M., & Mohd Hashim, N. (2022). Apoptotic Induction Mechanism of Artonin E in 3D Ovarian Cancer Cell Lines. Indonesian Journal of Pharmacy, 33(1), 147-158. https://doi.org/10.22146/ijp.3527
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Section
Research Article
