Phytochemical Analysis and Biological Activities of Propolis from Geniotrigona thoracica: Evaluating its Therapeutic Applications
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Abstract
Propolis is a substance that safeguards the bee hive against physical and microbiological threats. This research assessed the phytochemical properties and biological effects of propolis produced by stingless bees Geniotrigona thoracica collected from Phatthalung, Southern Thailand. The findings revealed that the ethanolic extract propolis (EEP) from G. thoracica exhibited antibacterial properties against certain foodborne pathogens (Bacillus cereus, Staphylococcus aureus, Escherichia coli, and Salmonella Typhimurium) with moderate to strong zone of inhibition (ZOI) in the range of 10 mm ≤ ZOI ≤ 15 mm. Additionally, the extract propolis demonstrated antioxidant activity, achieving up to 80% DPPH radical scavenging when 50 mg/mL EEP was tested. Furthermore, the crude propolis extract showed anti-inflammatory effects on macrophage cells, resulting in a 72.9% reduction in nitric oxide (NO) levels in LPS-activated RAW 264.7 cells exposed to 100 mg/mL of EEP. The GC-MS chromatogram identified the phytochemical compositions of the EEP, with Lup-20(29)-en-3-ol or lupeol (25.42%) and β-amyrone (22.66%) as the major compounds, both triterpenoid derivatives. Other notable constituents included alkane hydrocarbon pentacosane (6.63%), fatty alcohol cis-9-eicosenol (4.23%), and phenolic compound 3-pentadecylphenol (3.86%). Therefore, the EEP derived from G. thoracica, possessing such diverse biological activities, holds promise for medicinal and functional food applications.
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References
Rasmussen, C.; Cameron, S. A. A molecular phylogeny of the Old World stingless bees (Hymenoptera: Apidae: Meliponini) and the non-monophyly of the large genus Trigona. Systematic Entomology, 2007, 32(1), 26-39. https://doi.org/10.1111/j.1365-3113.2006.00362.x
Engel, M. S.; Rasmussen, C.; Ayala, R.; de Oliveira, F. F. Stingless bee classification and biology (Hymenoptera, Apidae): A review, with an updated key to genera and subgenera. ZooKeys, 2023, 1172, 239. https://doi.org/10.3897/zookeys.1172.104944
Rozman, A. S.; Hashim, N.; Maringgal, B.; Abdan, K. A comprehensive review of stingless bee products: Phytochemical composition and beneficial properties of honey, propolis, and pollen. Applied Sciences, 2022, 12(13), 6370. https://doi.org/10.3390/app12136370
Rocha, V. M.; Portela, R. D.; Dos Anjos, J. P.; De Souza, C. O.; Umsza-Guez, M. A. Stingless bee propolis: Composition, biological activities and its applications in the food industry. Food Production, Processing and Nutrition, 2023, 5(1), 29. https://doi.org/10.1186/s43014-023-00146-z
Chuttong, B.; Lim, K.; Praphawilai, P.; Danmek, K.; Maitip, J.; Vit, P.; Wu, M.-C.; Ghosh, S.; Jung, C.; Burgett, M. Exploring the functional properties of propolis, geopropolis, and cerumen, with a special emphasis on their antimicrobial effects. Foods, 2023, 12(21), 3909. https://doi.org/10.3390/foods12213909
Nazir, H.; Shahidan, W. N. S.; Ibrahim, H. A.; Tuan Ismail, T. N. N. Chemical constituents of Malaysian Geniotrigona thoracica propolis. Pertanika Journal of Tropical Agricultural Science, 2018, 41(3).
Zullkiflee, N.; Taha, H.; Abdullah, N. A.; Hashim, F.; Usman, A. Antibacterial and antioxidant activities of ethanolic and water extracts of stingless bees Tetrigona binghami, Heterotrigona itama, and Geniotrigona thoracica propolis found in Brunei. Philippine Journal of Science, 2022, 151, 1455-1462. https://doi.org/10.56899/151.04.13
Abdullah, N. A.; Zullkiflee, N.; Zaini, S. N. Z.; Taha, H.; Hashim, F.; Usman, A. Phytochemicals, mineral contents, antioxidants, and antimicrobial activities of propolis produced by Brunei stingless bees Geniotrigona thoracica, Heterotrigona itama, and Tetrigona binghami. Saudi Journal of Biological Sciences, 2020, 27(11), 2902-2911. https://doi.org/10.1016/j.sjbs.2020.09.014
Idris, L.; Adli, M. A.; Yaacop, N. N.; Zohdi, R. M. Phytochemical screening and antioxidant activities of Geniotrigona thoracica propolis extracts derived from different locations in Malaysia. Malaysian Journal of Fundamental and Applied Sciences, 2023, 19(6), 1023-1032. https://doi.org/10.11113/mjfas.v19n6.3128
Šuran, J.; Cepanec, I.; Mašek, T.; Radić, B.; Radić, S.; Tlak Gajger, I.; Vlainić, J. Propolis extract and its bioactive compounds-From traditional to modern extraction technologies. Molecules, 2021, 26(10), 2930. https://doi.org/10.3390/molecules26102930
Bankova, V.; Popova, M. Propolis of stingless bees: A promising source of biologically active compounds. Pharmacognosy Reviews, 2007, 1(1).
Campos, J. F.; Santos, U. P. d.; Rocha, P. d. S. d.; Damião, M. J.; Balestieri, J. B. P.; Cardoso, C. A. L.; Paredes-Gamero, E. J.; Estevinho, L. M.; de Picoli Souza, K.; Santos, E. L. d. Antimicrobial, antioxidant, anti‐inflammatory, and cytotoxic activities of propolis from the stingless bee Tetragonisca fiebrigi (Jatai). Evidence-Based Complementary and Alternative Medicine, 2015, 2015(1), 296186. https://doi.org/10.1155/2015/296186
Bees, M. S. (n.d.). Antibacterial and phenolic content of propolis produced by two Malaysian stingless bees, Heterotrigona itama and Geniotrigona thoracica.
Meechai, I.; Chelong, I. Total phenolic content and anti-radical activity of stingless bee honey at different harvesting times. Progress in Applied Science and Technology, 2018, 8(2), 65-72.
Bhaigybati, T.; Sanasam, S.; Gurumayum, J.; Bag, G.; Singh, L. R.; Devi, P. G. Phytochemical profiling, antioxidant activity, antimicrobial activity, and GC-MS analysis of Ipomoea aquatica Forsk collected from EMA market, Manipur. Journal of Pharmacognosy and Phytochemistry, 2020, 9(1), 2335-2342.
Mendez-Encinas, M. A.; Valencia, D.; Ortega-García, J.; Carvajal-Millan, E.; Díaz-Ríos, J. C.; Mendez-Pfeiffer, P.; Soto-Bracamontes, C. M.; Garibay-Escobar, A.; Alday, E.; Velazquez, C. Anti-inflammatory potential of seasonal Sonoran propolis extracts and some of their main constituents. Molecules, 2023, 28(11), 4496. https://doi.org/10.3390/molecules28114496
Mohiuddin, I.; Kumar, T. R.; Zargar, M. I.; Wani, S. U. D.; Mahdi, W. A.; Alshehri, S.; Alam, P.; Shakeel, F. GC-MS analysis, phytochemical screening, and antibacterial activity of Cerana indica propolis from Kashmir region. Separations, 2022, 9(11), 363. https://doi.org/10.3390/separations9110363
Gupta, A.; Naraniwal, M.; Kothari, V. Modern extraction methods for the preparation of bioactive plant extracts. International Journal of Applied and Natural Sciences, 2012, 1(1), 8-26.
Silva, J. C.; Rodrigues, S.; Feás, X.; Estevinho, L. M. Antimicrobial activity, phenolic profile, and role in the inflammation of propolis. Food and Chemical Toxicology, 2012, 50(5), 1790-1795. https://doi.org/10.1016/j.fct.2012.02.097
Cushnie, T. T.; Hamilton, V. E.; Lamb, A. J. Assessment of the antibacterial activity of selected flavonoids and consideration of discrepancies between previous reports. Microbiological Research, 2003, 158(4), 281-289. https://doi.org/10.1078/0944-5013-00206
Epand, R. M.; Walker, C.; Epand, R. F.; Magarvey, N. A. Molecular mechanisms of membrane targeting antibiotics. Biochimica et Biophysica Acta (BBA)-Biomembranes, 2016, 1858(5), 980-987. https://doi.org/10.1016/j.bbamem.2015.10.018
Breijyeh, Z.; Jubeh, B.; Karaman, R. Resistance of gram-negative bacteria to current antibacterial agents and approaches to resolve it. Molecules, 2020, 25(6), 1340. https://doi.org/10.3390/molecules25061340
Hau-Yama, N. E.; Magaña-Ortiz, D.; Oliva, A.; Ortiz-Vázquez, E. Antifungal activity of honey from stingless bee Melipona beecheii against Candida albicans. Journal of Apicultural Research, 2020, 59(1), 12-18. https://doi.org/10.1080/00218839.2019.1665247
Shehu, A.; Ismail, S.; Rohin, M. A. K.; Harun, A.; Abd Aziz, A.; Haque, M. Antifungal properties of Malaysian Tualang honey and stingless bee propolis against Candida albicans and Cryptococcus neoformans. Journal of Applied Pharmaceutical Science, 2016, 6(2), 044-050. https://doi.org/10.7324/JAPS.2016.60206
Tuksitha, L.; Chen, Y.-L. S.; Chen, Y.-L.; Wong, K.-Y.; Peng, C.-C. Antioxidant and antibacterial capacity of stingless bee honey from Borneo (Sarawak). Journal of Asia-Pacific Entomology, 2018, 21(2), 563-570. https://doi.org/10.1016/j.aspen.2018.03.007
Akhir, R. A. M.; Bakar, M. F. A.; Sanusi, S. B. Antioxidant and antimicrobial potential of stingless bee (Heterotrigona itama) by-products. Journal of Advanced Research in Fluid Mechanics and Thermal Sciences, 2018, 42(1), 72-79.
Abbas, A.; Naqvi, S. A. R.; Rasool, M. H.; Noureen, A.; Mubarik, M. S.; Tareen, R. B. Phytochemical analysis, antioxidant and antimicrobial screening of Seriphidium oliverianum plant extracts. Dose-Response, 2021, 19(1), 15593258211004739. https://doi.org/10.1177/15593258211004739
Akhir, R. A. M.; Bakar, M. F. A.; Sanusi, S. B. Antioxidant and antimicrobial activity of stingless bee bread and propolis extracts. In AIP Conference Proceedings. AIP Publishing. 2017 https://doi.org/10.1063/1.5005423
Parichatikanond, W.; Mangmool, S.; Chewchinda, S.; Hirunpanich, V.; Vongsak, B. Anti-inflammatory activity of propolis extract from the stingless bee, Tetragonula pagdeni, in mangosteen orchard. The Thai Journal of Pharmaceutical Sciences, 2024, 47(3), 6. https://doi.org/10.56808/3027-7922.2832
Zulhendri, F.; Lesmana, R.; Tandean, S.; Christoper, A.; Chandrasekaran, K.; Irsyam, I.; Suwantika, A. A.; Abdulah, R.; Wathoni, N. Recent update on the anti-inflammatory activities of propolis. Molecules, 2022, 27(23), 8473. https://doi.org/10.3390/molecules27238473
Bueno-Silva, B.; Kawamoto, D.; Ando-Suguimoto, E. S.; Alencar, S. M.; Rosalen, P. L.; Mayer, M. P. Brazilian red propolis attenuates inflammatory signaling cascade in LPS-activated macrophages. PLOS ONE, 2015, 10(12), e0144954. https://doi.org/10.1371/journal.pone.0144954
Alanazi, S.; Alenzi, N.; Fearnley, J.; Harnett, W.; Watson, D. G. Temperate propolis has anti-inflammatory effects and is a potent inhibitor of nitric oxide formation in macrophages. Metabolites, 2020, 10(10), 413. https://doi.org/10.3390/metabo10100413
Liang, Y.-C.; Tsai, S.-H.; Tsai, D.-C.; Lin-Shiau, S.-Y.; Lin, J.-K. Suppression of inducible cyclooxygenase and nitric oxide synthase through activation of peroxisome proliferator-activated receptor-γ by flavonoids in mouse macrophages. FEBS Letters, 2001, 496(1), 12-18. https://doi.org/10.1016/S0014-5793(01)02393-6
Walker, G.; Pfeilschifter, J.; Kunz, D. Mechanisms of suppression of inducible nitric-oxide synthase (iNOS) expression in interferon (IFN)-γ-stimulated RAW 264.7 cells by dexamethasone: Evidence for glucocorticoid-induced degradation of iNOS protein by calpain as a key step in post-transcriptional regulation. Journal of Biological Chemistry, 1997, 272(26), 16679-16687. https://doi.org/10.1074/jbc.272.26.16679
Sharma, N.; Palia, P.; Chaudhary, A.; Verma, K.; Kumar, I. A review on pharmacological activities of lupeol and its triterpene derivatives. Journal of Drug Delivery and Therapeutics, 2020, 10(5), 325-332. https://doi.org/10.22270/jddt.v10i5.4280
Gallo, M. B.; Sarachine, M. J. Biological activities of lupeol. International Journal of Biomedical and Pharmaceutical Sciences, 2009, 3(1), 46-66.
Ferreira, R. G.; Silva Junior, W. F.; Veiga Junior, V. F.; Lima, Á. A.; Lima, E. S. Physicochemical characterization and biological activities of the triterpenic mixture α, β-amyrenone. Molecules, 2017, 22(2), 298. https://doi.org/10.3390/molecules22020298
Karen Cardoso, B.; Line Marko de Oliveira, H.; Zonta Melo, U.; Mariano Fernandez, C. M.; Franco de Araújo Almeida Campo, C.; Gonçalves, J. E.; Laverde Jr, A.; Barion Romagnolo, M.; Andrea Linde, G.; Cristiani Gazim, Z. Antioxidant activity of α and β-amyrin isolated from Myrcianthes pungens leaves. Natural Product Research, 2020, 34(12), 1777-1781. https://doi.org/10.1080/14786419.2018.1525715