Antioxidant Activities of Bingöl Royal Jelly on SH-SY5Y Cells

Antioxidant Activities of Bingöl Royal Jelly on SH-SY5Y Cells

Royal Jelly is a bee product with high protein content is a unique nutrient for the queen honeybee. It leads to a substantial elongation of the lifetime of the queen in comparison to the worker honeybees via anti-inflammatory, anti-oxidant, anti-cancer and anti-microbial properties. Flavonoids naturally have reported to have anticancer activities thanks to their potent antioxidant activity. The antioxidant activity of RJ is attributed to its rich flavonoid content however anti-oxidant activities of the Bingöl RJ has yet to be explored in detail. The goal of the current study was to investigate the antioxidant activities of Bingöl RJ on SH-SY5Y neuroblastoma cells. The results of our study revealed that Bingöl RJ at a concentration of 0.3 mg/ml significantly augmented ROS level in SH-SY5Y cells while 0.5 mg/ml of RJ had almost no effect on ROS levels. The levels of malondialdehyde in SH-SY5Y cells considerably increased in the presence of 0.3 mg/ml RJ while 0.5 mg/ml RJ had no significant impact on MDA levels in SH-SY5Y cells. The results showed that RJ treatment 0.3 mg/ml) significantly lowered the activities of SOD and CAT activity while 0.5 mg/ml of RJ had negligible effect indicating that RJ could protect the cell membranes from radical mediated cell injuries.

___

  • Abotaleb, M., Samuel, S. M., Varghese, E., Varghese, S., Kubatka, P., Liskova, A., & Büsselberg, D. (2019). Flavonoids in cancer and apoptosis. Cancers, 11(1), 28. https://doi.org/10.3390/cancers11010028
  • Ayala, A., Muñoz, M. F., & Argüelles, S. (2014). Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxidative Medicine and Cellular Longevity, 36043.
  • Ayna, A. (2020). Apoptotic effects of beta-carotene, alpha-tocopherol and ascorbic acid on PC-3 prostate cancer cells. Hacettepe Journal of Biology and Chemistry, 48(3), 211-218.
  • Ayna, A. (2021). Caffeic acid prevents hydrogen peroxide-induced oxidative damage in SH-SY5Y cell line through mitigation of oxidative stress and apoptosis. Bratislavske Lekarske Listy, 122(2), 120-124.
  • Ayna, A., Özbolat, S. N., & Darendelioglu, E. (2020). Quercetin, chrysin, caffeic acid and ferulic acid ameliorate cyclophosphamide-induced toxicities in SH-SY5Y cells. Molecular Biology Reports, 47(11), 8535-8543.
  • Caglayan, C., Kandemir, F. M., Darendelioğlu, E., Küçükler, S., & Ayna, A. (2021). Hesperidin protects liver and kidney against sodium fluoride-induced toxicity through anti-apoptotic and anti-autophagic mechanisms. Life Sciences, 119730.
  • Chan, W. H., Wu, C. C., & Yu, J. S. (2003). Curcumin inhibits UV irradiation‐induced oxidative stress and apoptotic biochemical changes in human epidermoid carcinoma A431 cells. Journal of Cellular Biochemistry, 90(2), 327-338.
  • Du, X., Shi, Z., Peng, Z., Zhao, C., Zhang, Y., Wang, Z., & Li, X. (2017). Acetoacetate induces hepatocytes apoptosis by the ROS‐mediated MAPKs pathway in ketotic cows. Journal of Cellular Physiology, 232(12), 3296-3308.
  • Fratini, F., Cilia, G., Mancini, S., & Felicioli, A. (2016). Royal Jelly: An ancient remedy with remarkable antibacterial properties. Microbiological Research, 192, 130-141.
  • Fujiwara, S., Imai, J., Fujiwara, M., Yaeshima, T., Kawashima, T., & Kobayashi, K. (1990). A potent antibacterial protein in royal jelly. Purification and determination of the primary structure of royalisin. Journal of Biological Chemistry, 265(19), 11333-11337.
  • Gismondi, A., Trionfera, E., Canuti, L., Di Marco, G., & Canini, A. (2017). Royal jelly lipophilic fraction induces antiproliferative effects on SH-SY5Y human neuroblastoma cells. Oncology Reports, 38(3), 1833-1844.
  • Hameed, A., Fatima, G. R., Malik, K., Muqadas, A., & Fazal-ur-Rehman, M. (2019). Scope of Nanotechnology in Cosmetics: Dermatology and Skin Care Products. Journal of Medicinal and Chemical Sciences, 2, 9-16.
  • Hu, F. L., Bíliková, K., Casabianca, H., Daniele, G., Salmen Espindola, F., Feng, M., & Li, L. (2019). Standard methods for Apis mellifera royal jelly research. Journal of Apicultural Research, 58(2), 1-68.
  • Ighodaro, O. M., & Akinloye, O. A. (2018). First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alexandria Journal of Medicine, 54(4), 287-293.
  • Jacquemin, G., Margiotta, D., Kasahara, A., Bassoy, E. Y., Walch, M., Thiery, J., Lieberman J., & Martinvalet, D. (2015). Granzyme B-induced mitochondrial ROS are required for apoptosis. Cell Death and Differentiation, 22(5), 862-874. https://doi.org/10.1038/cdd.2014.180
  • Jelic, M. D., Mandic, A. D., Maricic, S. M., & Srdjenovic, B. U. (2021). Oxidative stress and its role in cancer. Journal of Cancer Research and Therapeutics, 17, 22-28.
  • Kluck, R. M., Bossy-Wetzel, E., Green, D. R., & Newmeyer, D. D. (1997). The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science, 275(5303), 1132-1136.
  • 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, 7074209.
  • Kolayli, S., Sahin, H., Can, Z., Yildiz, O., Malkoc, M., & Asadov, A. (2016). A member of complementary medicinal food: anatolian royal jellies, their chemical compositions, and antioxidant properties. Journal of Evidence-Based Complementary and Alternative Medicine, 21(4), 43-48.
  • Kucukler, S., Benzer, F., Yildirim, S., Gur, C., Kandemir, F. M., Bengu, A. S., & Dortbudak, M. B. (2021). Protective effects of chrysin against oxidative stress and inflammation induced by lead acetate in rat kidneys: a biochemical and histopathological approach. Biological Trace Element Research, 199(4), 1501-1514.
  • Kucukler, S., Darendelioğlu, E., Caglayan, C., Ayna, A., Yıldırım, S., & Kandemir, F. M. (2020). Zingerone attenuates vancomycin-induced hepatotoxicity in rats through regulation of oxidative stress, inflammation and apoptosis. Life Sciences, 259, 118382.
  • Liu, J. R., Yang, Y. C., Shi, L. S., & Peng, C. C. (2008). Antioxidant properties of royal jelly associated with larval age and time of harvest. Journal of Agricultural and Food Chemistry, 56(23), 11447-11452.
  • Louis, C. U., & Shohet, J. M. (2015). Neuroblastoma: molecular pathogenesis and therapy. Annual Review of Medicine, 66, 49-63.
  • Malka, O., Karunker, I., Yeheskel, A., Morin, S., & Hefetz, A. (2009). The gene road to royalty–differential expression of hydroxylating genes in the mandibular glands of the honeybee. The FEBS Journal, 276(19), 5481-5490.
  • Maris, J. M. (2010). Recent advances in neuroblastoma. New England Journal of Medicine, 362(23), 2202-2211.
  • Melliou, E., & Chinou, I. (2005). Chemistry and bioactivity of royal jelly from Greece. Journal of Agricultural and Food Chemistry, 53(23), 8987-8992.
  • Miyata, Y., & Sakai, H. (2018). Anti-cancer and protective effects of royal jelly for therapy-induced toxicities in malignancies. International Journal of Molecular Sciences, 19(10), 3270.
  • Nakajima, Y., Tsuruma, K., Shimazawa, M., Mishima, S., & Hara, H. (2009). Comparison of bee products based on assays of antioxidant capacities. BMC Complementary and Alternative Medicine, 9(1), 4-13.
  • Özbolat, S. N., & Ayna, A. (2021). Chrysin suppresses HT-29 cell death induced by diclofenac through apoptosis and oxidative damage. Nutrition and Cancer, 73(8), 1419-1428.
  • Pan, Y., Rong, Y., You, M., Ma, Q., Chen, M., & Hu, F. (2019). Royal jelly causes hypotension and vasodilation induced by increasing nitric oxide production. Food Science and Nutrition, 7(4), 1361-1370.
  • Park, M. J., Kim, B. Y., Park, H. G., Deng, Y., Yoon, H. J., Choi, Y. S., & Jin, B. R. (2019). Major royal jelly protein 2 acts as an antimicrobial agent and antioxidant in royal jelly. Journal of Asia-Pacific Entomology, 22(3), 684-689.
  • Pasupuleti, V. R., Sammugam, L., Ramesh, N., & Gan, S. H. (2017). Honey, propolis, and royal jelly: a comprehensive review of their biological actions and health benefits. Oxidative Medicine and Cellular Longevity, 1259510.
  • Pfeffer, C. M., & Singh, A. T. (2018). Apoptosis: a target for anticancer therapy. International Journal of Molecular Sciences, 19(2), 448-457.
  • Porta, C., Levy, A., Hawkins, R., Castellano, D., Bellmunt, J., Nathan, P., & Vekeman, F. (2014). Impact of adverse events, treatment modifications, and dose intensity on survival among patients with advanced renal cell carcinoma treated with first‐line sunitinib: a medical chart review across ten centers in five European countries. Cancer Medicine, 3(6), 1517-1526.
  • Premratanachai, P., & Chanchao, C. (2014). Review of the anticancer activities of bee products. Asian Pacific Journal of Tropical Biomedicine, 4(5), 337-344.
  • Ramadan, M. F., & Al-Ghamdi, A. (2012). Bioactive compounds and health-promoting properties of royal jelly: A review. Journal of Functional Foods, 4(1), 39-52.
  • Ramanathan, A. N. K. G., Nair, A. J., & Sugunan, V. S. (2018). A review on Royal Jelly proteins and peptides. Journal of Functional Foods, 44, 255-264.
  • Rossé, T., Olivier, R., Monney, L., Rager, M., Conus, S., Fellay, I.,& Borner, C. (1998). Bcl-2 prolongs cell survival after Bax-induced release of cytochrome c. Nature, 391(6666), 496.
  • Sabatini, A. G., Marcazzan, G. L., Caboni, M. F., Bogdanov, S., & Almeida-Muradian, L. B. D. (2009). Quality and standardisation of royal jelly. Journal of ApiProduct and ApiMedical Science, 1(1), 1-6.
  • Silici, S. (2019). Honeybee Products and Apitherapy. Turkish Journal of Agriculture-Food Science and Technology, 7(9), 1249-1262.
  • Viuda‐Martos, M., Ruiz‐Navajas, Y., Fernández‐López, J., & Pérez‐Álvarez, J. A. (2008). Functional properties of honey, propolis, and royal jelly. Journal of Food Science, 73(9), 117-124.
  • Wang, I. K., Lin-Shiau, S. Y., & Lin, J. K. (1999). Induction of apoptosis by apigenin and related flavonoids through cytochrome c release and activation of caspase-9 and caspase-3 in leukaemia HL-60 cells. European Journal of Cancer, 35(10), 1517-1525.
  • Yanagita, M., Kojima, Y., Mori, K., Yamada, S., & Murakami, S. (2011). Osteoinductive and anti-inflammatory effect of royal jelly on periodontal ligament cells. Biomedical Research, 32(4), 285-291.
  • Yang, J., Liu, X., Bhalla, K., Kim, C. N., Ibrado, A. M., Cai, J., & Wang, X. (1997). Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science, 275(5303), 1129-1132.
  • Yeung, Y. T., & Argüelles, S. (2019). Bee Products: Royal Jelly and Propolis. In: Nonvitamin and Nonmineral Nutritional Supplements. Academic Press: 475-448.
  • Yin, L., Han, H., Zheng, X., Wang, G., Li, Y., & Wang, W. (2019). Flavonoids analysis and antioxidant, antimicrobial, and anti-inflammatory activities of crude and purified extracts from Veronicastrum latifolium. Industrial Crops and Products, 137, 652-661.