Home / Regular Issue / JSSH Vol. 46 (1) Feb. 2023 / JTAS-2472-2022


Therapeutic Evaluation of Ethanolic Bee Pollen Extract from Malaysian Stingless Bee in MCF-7 and MCF-10A Cell Lines

Nurdianah Harif Fadzilah and Wan Adnan Wan Omar

Pertanika Journal of Social Science and Humanities, Volume 46, Issue 1, February 2023

DOI: https://doi.org/10.47836/pjtas.46.1.03

Keywords: MCF-7, MCF-10A, stingless bee pollen, therapeutic index

Published on: 22 Febuary 2023

Bee pollen is a complete food containing comprehensive nutrients and therapeutic properties that could eliminate free radicals. Three stingless bee species native to Malaysia were used to prepare bee pollen ethanolic extracts (BPE): Geniotrigona thoracica, Heterotrigona itama, and Tetrigona apicalis. The methodology used in this study was a trypan blue exclusion assay for cell proliferation activity in cultured breast adenocarcinoma human cell lines (MCF-7) and mammary epithelial human cell lines (MCF-10A). In addition, the therapeutic index (TI) was analyzed to assess the relative antiproliferative activity of BPE on cancer versus normal cells. Geniotrigona thoracica, BPE exhibited the highest therapeutic index (TI = 3.12) compared to H. itama (TI = 1.16) and T. apicalis (TI = 0.90) BPE. Each species represents different bioactive compounds due to different pollen foraging activities. Therefore, the highest TI species (G. thoracica) could be a potential candidate to be developed as a potential chemotherapeutic agent.

  • Abughazaleh, R. D., & Tracy, T. S. (2014). Therapeutic index. Wiley StatsRef: Statistics Reference Online. https://doi.org/10.1002/9781118445112.stat07121

  • Ahmad, F., Seerangan, P., Mustafa, M. Z., Osman, Z. F., Abdullah, J. M., & Idris, Z. (2019). Anti-cancer properties of Heterotrigona itama sp. honey via induction of apoptosis in malignant glioma cells. Malaysian Journal of Medical Sciences, 26(2), 30–39. https://doi.org/10.21315/mjms2019.26.2.4

  • American Type Culture Collection. (n.d.). MCF 10A (CRL-10317™). ATCC. https://www.atcc.org/products/all/CRL-10317.aspx#history

  • Aslantürk, Ö. S. (2018). In vitro cytotoxicity and cell viability assays: Principles, advantages, and disadvantages. In M. L. Larramendy & S. Soloneski (Eds.), Genotoxicity - A predictable risk to our actual world. IntechOpen. https://doi.org/10.5772/intechopen.71923

  • Azamjah, N., Soltan-Zadeh, Y., & Zayeri, F. (2019). Global trend of breast cancer mortality rate: A 25-year study. Asian Pacific Journal of Cancer Prevention, 20(7), 2015–2020. https://doi.org/10.31557/APJCP.2019.20.7.2015

  • Campos, M. G. R., Frigerio, C., Lopes, J., & Bogdanov, S. (2010). What is the future of Bee-Pollen?. Journal of ApiProduct and ApiMedical Science, 2(4), 131–144. https://doi.org/10.3896/ibra.

  • Cha, M. C., Lin, A., & Meckling, K. A. (2005). Low dose docosahexaenoic acid protects normal colonic epithelial cells from araC toxicity. BMC Pharmacology, 5, 7. https://doi.org/10.1186/1471-2210-5-7

  • Choudhari, M. K., Haghniaz, R., Rajwade, J. M., & Paknikar, K. M. (2013). Anticancer activity of Indian stingless bee propolis: An in vitro study. Evidence-Based Complementary and Alternative Medicine, 2013, 928280. https://doi.org/10.1155/2013/928280

  • Deepa, P. R., Vandhana, S., Jayanthi, U., & Krishnakumar, S. (2012). Therapeutic and toxicologic evaluation of anti-lipogenic agents in cancer cells compared with non-neoplastic cells. Basic and Clinical Pharmacology and Toxicology, 110(6), 494–503. https://doi.org/10.1111/j.1742-7843.2011.00844.x

  • Franchi, G. C., Moraes, C. S., Toreti, V. C., Daugsch, A., Nowill, A. E., & Park, Y. K. (2012). Comparison of effects of the ethanolic extracts of brazilian propolis on human leukemic cells as assessed with the MTT assay. Evidence-Based Complementary and Alternative Medicine, 2012, 918956. https://doi.org/10.1155/2012/918956

  • Harif Fadzilah, N., Jaapar, M. F., Jajuli, R., & Wan Omar, W. A. (2017). Total phenolic content, total flavonoid and antioxidant activity of ethanolic bee pollen extracts from three species of Malaysian stingless bee. Journal of Apicultural Research, 56(2), 130–135. https://doi.org/10.1080/00218839.2017.1287996

  • Kandaswami, C. C. (2014). Re: What is the difference between an antiproliferative assay and a cytotoxicity assay?. ResearchGate. https://www.researchgate.net/post/What-is-the-difference-between-an-antiproliferative-assay-and-a-cytotoxicity-assay/53a079e2d4c1188e0a8b4626/citation/download

  • Kocot, J., Kiełczykowska, M., Luchowska-Kocot, D., Kurzepa, J., & Musik, I. (2018). Antioxidant potential of propolis, bee pollen, and royal jelly: Possible medical application. Oxidative Medicine and Cellular Longevity, 2018, 7074209. https://doi.org/10.1155/2018/7074209

  • Kuppusamy, P., Yusoff, M. M., Maniam, G. P., Ichwan, S. J. A., Soundharrajan, I., & Govindan, N. (2014). Nutraceuticals as potential therapeutic agents for colon cancer: A review. Acta Pharmaceutica Sinica B, 4(3), 173–181. https://doi.org/10.1016/j.apsb.2014.04.002

  • Kustiawan, P. M., Puthong, S., Arung, E. T., & Chanchao, C. (2014). In vitro cytotoxicity of Indonesian stingless bee products against human cancer cell lines. Asian Pacific Journal of Tropical Biomedicine, 4(7), 549–556. https://doi.org/10.12980/APJTB.4.2014APJTB-2013-0039

  • Lee, A. V., Oesterreich, S., & Davidson, N. E. (2015). MCF-7 cells - Changing the course of breast cancer research and care for 45 years. Journal of the National Cancer Institute, 107(7), djv073. https://doi.org/10.1093/jnci/djv073

  • MarÉchal, E. (2011). Measuring bioactivity: KI, IC50 and EC50. In E. Marechal, S. Roy, L. Lafanechère (Eds.), Chemogenomics and chemical genetics (pp. 55–65). Springer. https://doi.org/10.1007/978-3-642-19615-7_5

  • Muller, P. Y., & Milton, M. N. (2012). The determination and interpretation of the therapeutic index in drug development. Nature Reviews Drug Discovery, 11(10), 751–761. https://doi.org/10.1038/nrd3801

  • Norowi, M. H., Mohd, F., Sajap, A. S., Rosliza, J., & Suri, R. (2010). Conservation and sustainable utilization of stingless bees for pollination services in agricultural ecosystems in Malaysia. ResearchGate. https://www.researchgate.net/publication/318338675

  • Premratanachai, P., & Chanchao, C. (2014). Review of the anticancer activities of bee products. Asian Pacific Journal of Tropical Biomedicine, 4(5), 337–344. https://doi.org/10.12980/APJTB.4.2014C1262

  • Qu, Y., Han, B., Yu, Y., Yao, W., Bose, S., Karlan, B. Y., Giuliano, A. E. & Cui, X. (2015). Evaluation of MCF10A as a reliable model for normal human mammary epithelial cells. PLOS One, 10(7), e0131285. https://doi.org/10.1371/journal.pone.0131285

  • Riss, T., Niles, A., Moravec, R., Karassina, N., Vidugiriene, J., Markossian, S., Grossman, A., Brimacombe, K., Arkin, M., Auld, D., Austin, C., Baell, J., Chung, T. D. Y., Coussens, N. P., Dahlin, J. L., Devamarayan, V., Foley, T. L., Glicksman, M., Hass, J. V., … Xu, X. (Eds.). Cytotoxicity assays: In vitro methods to measure dead cells. In Assay guidance manual. Eli Lilly & Company and the National Center for Advancing Translational Sciences. https://pubmed.ncbi.nlm.nih.gov/31070879/

  • Rzepecka-Stojko, A., Stojko, J., Kurek-Górecka, A., Górecki, M., Kabała-Dzik, A., Kubina, R., Moździerz, A., & Buszman, E. (2015). Polyphenols from bee pollen: Structure, absorption, metabolism and biological activity. Molecules, 20(12), 21732–21749. https://doi.org/10.3390/molecules201219800

  • Samsudin, S. F., Mamat, M. R., & Hazmi, I. R. (2018). Taxonomic study on selected species of stingless bee (Hymenoptera: Apidae: Meliponini) in Peninsular Malaysia. Serangga, 23(2), 203–258.

  • Sebaugh, J. L. (2011). Guidelines for accurate EC50/IC50 estimation. Pharmaceutical Statistics, 10(2), 128–134. https://doi.org/10.1002/pst.426

  • Seely, J. M., & Alhassan, T. (2018). Screening for breast cancer in 2018 — What should we be doing today?. Current Oncology, 25(s1), 115–124. https://doi.org/10.3747/co.25.3770

  • Stordal, B. K., Davey, M. W., & Davey, R. A. (2006). Oxaliplatin induces drug resistance more rapidly than cisplatin in H69 small cell lung cancer cells. Cancer Chemotherapy and Pharmacology, 58(2), 256–265. https://doi.org/10.1007/s00280-005-0148-7

  • Strober, W. (2015). Trypan blue exclusion test of cell viability. Current Protocols in Immunology, 111, A3.B1-A3.B3. https://doi.org/10.1002%2F0471142735.ima03bs111

  • Tamargo, J., Le Heuzey, J. Y., & Mabo, P. (2015). Narrow therapeutic index drugs: A clinical pharmacological consideration to flecainide. European Journal of Clinical Pharmacology, 71(5), 549–567. https://doi.org/10.1007/s00228-015-1832-0

  • T-Johari, S. A. T., Hashim, F., Ismail, W. I. W., & Ali, A. M. (2019). Combinatorial cytotoxic effects of gelam honey and 5-fluorouracil against human adenocarcinoma colon cancer HT-29 cells in vitro. International Journal of Cell Biology, 2019, 9050626. https://doi.org/10.1155/2019/9050626

  • Wang, H., Khor, T. O., Shu, L., Su, Z., Fuentes, F., Lee, J.-H., & Kong, A.-N. T. (2012). Plants against cancer: A review on natural phytochemicals in preventing and treating cancers and their druggability. Anti-cancer Agents in Medical Chemistry, 12(10), 1281–1305. https://doi.org/10.2174%2F187152012803833026

  • Yang, K., Wu, D., Ye, X., Liu, D., Chen, J., & Sun, P. (2013). Characterization of chemical composition of bee pollen in China. Journal of Agricultural and Food Chemistry, 61(3), 708–718. https://doi.org/10.1021/jf304056b