Toxicological Research

Korean Society of Toxicology & Korea Environmental Mutagen Society (한국독성학회)
권호 표지
DOI QR코드

DOI QR Code

Propolis Inhibits UVA-Induced Apoptosis of Human Keratinocyte HaCaT Cells by Scavenging ROS

  • Received : 2016.07.03
  • Accepted : 2016.07.26
  • Published : 2016.10.15
Download PDF
⟨ Previous Next ⟩

Abstract

Propolis is a resinous material collected by honeybees from several plant sources. This research aimed at showing its protective effect against UVA-induced apoptosis of human keratinocyte HaCaT cells. Using Hoechst staining, it was demonstrated that propolis (5 and $10{\mu}g/mL$) significantly inhibited the apoptosis of HaCaT cells induced by UVA-irradiation. Propolis also showed the protective effect against loss of mitochondrial membrane potential induced by UVA-irradiaiton in HaCaT cells. Propolis also inhibited the expression of activated caspase-3 induced by UVA-irradiation. To investigate the role of ROS in UVA-induced apoptosis and protection by propolis, the generation of ROS was determined in cells. The results showed that the generation of ROS was markedly reduced in cells pretreated with propolis. Consequently, propolis protected human keratinocyte HaCaT cells against UVA-induced apoptosis, which might be related to the reduction of ROS generation by UVA-irradiation.

Keywords

References

  1. Aragane, Y., Kulms, D., Metze, D., Wilkes, G., Poppelmann, B., Luger, T.A. and Schwarz, T. (1998) UV light induces apoptosis via direct activation of CD95 (Fas/APO- 1) independently of it's ligand CD95L. J. Cell Biol., 140, 171-182. https://doi.org/10.1083/jcb.140.1.171
  2. Danno, K. and Horio, T. (1987) Sunburn cell: factors involved in its formation. Photochem. Photobiol., 45, 683-690. https://doi.org/10.1111/j.1751-1097.1987.tb07401.x
  3. Ziegler, A., Jonason, A.S., Leffell, D.J., Simon, J.A., Sharma, H.W., Kimmelman, J., Remington, L., Jacks, T. and Brash, D.E. (1994) Sunburn and p53 in the onset of skin cancer. Nature, 372, 773-776. https://doi.org/10.1038/372773a0
  4. Fuchs, J. and Packer, L. (1991) Photooxidative Stress in the Skin in Oxidative Stress: Oxidants and Antioxidants (Sies, H. Ed.). Academic Press, London, pp. 559-583.
  5. Heck, D.E., Gerecke, D.R., Vetrano, A.M. and Laskin, J.D. (2004) Solar ultraviolet radiation as a trigger of cell signal transduction. Toxicol. Appl. Pharmacol., 195, 288-297. https://doi.org/10.1016/j.taap.2003.09.028
  6. Banskota, A.H., Tezuka, Y. and Kadota, S. (2001) Recent progress in pharmacological research of propolis. Phytother. Res., 15, 561-571. https://doi.org/10.1002/ptr.1029
  7. Burdock, G.A. (1998) Review of the biological properties and toxicity of bee propolis (propolis). Food Chem. Toxicol., 36, 347-363. https://doi.org/10.1016/S0278-6915(97)00145-2
  8. Bankova, V. (2005) Chemical diversity of propolis and the problem of standardization. J. Ethnopharmacol., 100, 114-117. https://doi.org/10.1016/j.jep.2005.05.004
  9. Sforcin, J.M., Fernandes, A. Jr., Lopes, C.A., Bankova, V. and Funari, S.R. (2000) Seasonal effect on Brazilian propolis antibacterial activity. J. Ethnopharmacol., 73, 243-249. https://doi.org/10.1016/S0378-8741(00)00320-2
  10. Kujumgiev, A., Tsvetkova, I., Serkedjieva, Y., Bankova, V., Christov, R. and Popov, S. (1999) Antibacterial, antifungal and antiviral activity of propolis of different geographic origin. J. Ethnopharmacol., 64, 235-240. https://doi.org/10.1016/S0378-8741(98)00131-7
  11. Ledon, N., Casaco, A., Gonzalez, R., Merino, N., Gonzalez, A. and Tolon, Z. (1997) Antipsoriatic, anti-inflammatory, and analgesic effects of an extract of red propolis. Zhongguo Yao Li Xue Bao, 18, 274-276.
  12. Chen, C.N., Wu, C.L., Shy, H.S. and Lin, J.K. (2003) Cytotoxic prenylflavanones from Taiwanese propolis. J. Nat. Prod., 66, 503-506. https://doi.org/10.1021/np0203180
  13. Heim, K.E., Tagliaferro, A.R. and Bobilya, A.R. (2002) Flavonoid antioxidants: chemistry, metabolism and structure activity relationships. J. Nutr. Biochem., 13, 572-584. https://doi.org/10.1016/S0955-2863(02)00208-5
  14. Orsolic, N. and Basic, I. (2003) Immunomodulation by water-soluble derivative of propolis: a factor of antitumor reactivity. J. Ethnopharmacol., 84, 265-273. https://doi.org/10.1016/S0378-8741(02)00329-X
  15. Aso, K., Kanno, S., Tadano, T., Satoh, S. and Ishikawa, M. (2004) Inhibitory effect of propolis on the growth of human leukemia U937. Biol. Pharm. Bull., 27, 727-730. https://doi.org/10.1248/bpb.27.727
  16. Liu, G.A. and Zheng, R.L. (2002) Protection against damaged DNA in the single cell by polyphenols. Pharmazie., 57, 852-854.
  17. Orsolic, N., Benkovic, V., Horvat-Knezevic, A., Kopjar, N., Kosalec, I., Bakmaz, M., Mihaljevic, Z., Bendelja, K. and Basic, I. (2007) Assessment by survival analysis of the radioprotective properties of propolis and its polyphenolic compounds. Biol. Pharm. Bull., 30, 946-951. https://doi.org/10.1248/bpb.30.946
  18. Castaldo, S. and Capasso, F. (2002) Propolis, an old remedy used in modern medicine. Fitoterapia, 73 Suppl 1, S1-S6. https://doi.org/10.1016/S0367-326X(02)00185-5
  19. Simoes, L.M., Gregorio, L.E., Da Silva Filho, A.A., De Souza, M.L., Azzolini, A.E., Bastos, J.K. and Lucisano-Vlim, Y.M. (2004) Effect of Brazilian green propolis on the production of reactive oxygen species by stimulated neutrophils. J. Ethnopharmacol., 94, 59-65. https://doi.org/10.1016/j.jep.2004.04.026
  20. Uma Devi, P., Ganasoundari, A., Rao, B.S. and Srinivasan, K.K. (1999) In vivo radioprotection by ocimum flavonoids: survival of mice. Radiat. Res., 151, 74-78. https://doi.org/10.2307/3579750
  21. Arora, R., Chawla, R., Puri, S.C., Sagar, R., Singh, S., Kumar, R., Sharma, A.K., Prasad, J., Singh, S., Kaur, G., Chaudhary, P., Qazi, G.N. and Sharma, R.K. (2005) Radioprotective and antioxidant properties of low-altitude Podophyllum hexandrum (LAPH). J. Environ. Pathol. Toxicol. Oncol., 24, 299-314. https://doi.org/10.1615/JEnvironPatholToxicolOncol.v24.i4.70
  22. Benkovic, V., Horvat Knezevic, A., Brozovic, G., Knezevic, F., Dikic, D., Bevanda, M., Basic, I. and Orsolic, N. (2007) Enhanced antitumor activity of irinotecan combined with propolis and its polyphenolic compounds on Ehrlich ascites tumor in mice. Biomed. Pharmacother., 61, 292-297. https://doi.org/10.1016/j.biopha.2007.02.012
  23. Benkovic, V., Knezevic, A.H., Dikic, D., Lisicic, D., Orsolic, N., Basic, I., Kosalec, I. and Kopjar, N. (2008) Radioprotective effects of propolis and quercetin in c-irradiated mice evaluated by the alkaline comet assay. Phytomedicine, 15, 851-858. https://doi.org/10.1016/j.phymed.2008.02.010
  24. Lu, Y.Y., Chen, T.S., Wang, X.P., Qu, J.L. and Chen, M. (2010) The JNK inhibitor SP600125 enhances dihydroartemisinin-induced apoptosis by accelerating Bax translocation into mitochondria in human lung adenocarcinoma cells. FEBS Lett., 584, 4019-4026. https://doi.org/10.1016/j.febslet.2010.08.014
  25. Shin, D.Y., Kim, G.Y., Li, W., Choi, B.T., Kim, N.D., Kang, H.S. and Choi, Y.H. (2009) Implication of intracellular ROS formation, caspase-3 activation and Egr-1 induction in platycodon D-induced apoptosis of U937 human leukemia cells. Biomed. Pharmacother., 63, 86-94. https://doi.org/10.1016/j.biopha.2008.08.001
  26. Zoratti, M. and Szabo, I. (1995) The mitochondrial permeability transition. Biochim. Biophys. Acta, 1241, 139-176. https://doi.org/10.1016/0304-4157(95)00003-A
  27. Vander Heiden, M.G., Chandel, N.S., Williamson, E.K., Schumacker, P.T. and Thompson, C.B. (1997) Bcl-xL regulates the membrane potential and volume homeostasis of mitochondria. Cell, 91, 627-637. https://doi.org/10.1016/S0092-8674(00)80450-X
  28. Fiers, W., Beyaert, R., Declercq, W. and Vandenabeele, P. (1999) More than one way to die: apoptosis, necrosis and reactive oxygen damage. Oncogene, 18, 7719-7730. https://doi.org/10.1038/sj.onc.1203249
  29. Fleury, C., Mignotte, B. and Vayssiere, J.L. (2002) Mitochondrial reactive oxygen species in cell death signaling. Biochimie, 84, 131-141. https://doi.org/10.1016/S0300-9084(02)01369-X
  30. Chakraborti, T., Das, S., Mondal, M., Roychoudhury, S. and Chakraborti, S. (1999) Oxidant, mitochondria and calcium: an overview. Cell. Signal., 1, 77-85.
  31. Garssen, J., van Steeg, H., de Gruijl, F., de Boer, J., van der Horst, G.T., van Kranen, H., van Loveren, H., van Dijk, M., Fluitman, A., Weeda, G. and Hoeijmakers, J.H. (2000) Transcription coupled and global genome repair differentially influence UV-B-induced acute skin effects and systemic immunosuppression. J. Immunol., 164, 6199-6205. https://doi.org/10.4049/jimmunol.164.12.6199
  32. Wenk, J., Brenneisen, P., Meewes, C., Wlaschek, M., Peters, T., Blaudschun, R., Ma, W., Kuhr, L., Schneider, L. and Scharffetter-Kochanek, K. (2001) UV-induced oxidative stress and photoaging. Curr. Probl. Dermatol., 29, 83-94.
  33. Kulms, D., Zeise, E., Poppelmann, B. and Schwarz, T. (2002) DNA damage, death receptor activation and reactive oxygen species contribute to ultraviolet radiation induced apoptosis in an essential and independent way. Oncogene, 21, 5844-5851. https://doi.org/10.1038/sj.onc.1205743
  34. Chen, Y.C., Lin-Shiau, S.Y. and Lin, J.K. (1998) Involvement of reactive oxygen species and caspase 3 activation in arsenite-induced apoptosis. J. Cell. Physiol., 177, 324-333. https://doi.org/10.1002/(SICI)1097-4652(199811)177:2<324::AID-JCP14>3.0.CO;2-9
  35. Irani, K. (2000) Oxidant signaling in vascular cell growth, death, and survival: a review of the roles of reactive oxygen species in smooth muscle and endothelial cell mitogenic and apoptotic signaling. Circ. Res., 87, 179-183. https://doi.org/10.1161/01.RES.87.3.179
  36. Moreno, M.I.N., Isla, M.I., Sampietro, A.R. and Vattuone, M.A. (2000) Comparison of the free radical-scavenging activity of propolis from several regions of Argentina. J. Ethnopharmacol., 71,109-114. https://doi.org/10.1016/S0378-8741(99)00189-0
  37. Kumazawa, S., Hamasaka, T. and Nakayama, T. (2004) Antioxidant activity of propolis of various geographic origins. Food Chem., 84, 329-339. https://doi.org/10.1016/S0308-8146(03)00216-4
  38. Banskota, A.H., Tezuka, Y., Adnyana, I.K., Ishii, E., Midorikawa, K., Matsushige, K. and Kadota, S. (2001) Hepatoprotective and anti-Helicobacter pylori activities of constituents from Brazilian propolis. Phytomedicine, 8, 16-23. https://doi.org/10.1078/0944-7113-00004
  39. Mohammadzadeh, S., Sharriatpanahi, M., Hamedi, M., Amanzadeh, Y., Ebrahimi, S.E.S. and Ostad, S.N. (2007) Antioxidant power of Iranian propolis extract. Food Chem., 103, 729-733. https://doi.org/10.1016/j.foodchem.2006.09.014
  40. Chiao, C., Carothers, A.M., Grunberger, D., Solomon, G., Preston, A.G. and Barrett, C.J. (1995) Apoptosis and altered redox state induced by caffeic acid phenethyl ester (CAPE) in transformed rat fibroblast cells. Cancer Res., 55, 3576-3583.
  41. Rao, C.V., Desai, D., Rivenson, A., Simi, B., Amin, S. and Reddy, S.B. (1995) Chemoprevention of colon carcinogenesis by phenylethyl-3-methylcaffeate. Cancer Res., 55, 2310-2315.
  42. Xuan, H., Zhao, J., Miao, J., Li, Y., Chu, Y. and Hu, F. (2011) Effect of Brazilian propolis on human umbilical vein endothelial cell apoptosis. Food Chem. Toxicol., 49, 78-85. https://doi.org/10.1016/j.fct.2010.09.034
  43. Eom, H.S., Lee, E.J., Yoon, B.S. and Yoo, B.S. (2010) Propolis inhibits the proliferation of human leukaemia HL-60 cells by inducing apoptosis through the mitochondrial pathway. Nat. Prod. Res., 24, 375-386. https://doi.org/10.1080/14786410903370908
  44. Chen, C.N., Wu, C.L. and Lin, J.K. (2007) Apoptosis of human melanoma cells induced by the novel compounds propolin A and propolin B from Taiwenese propolis. Cancer Lett., 245, 218-231. https://doi.org/10.1016/j.canlet.2006.01.016
  45. Ishihara, M., Naoi, K., Hashita, M., Itoh, Y. and Suzui, M. (2009) Growth inhibitory activity of ethanol extract of Chinese and Brazilian propolis in four human colon carcinoma cell lines. Oncol. Rep., 22, 349-354.
  46. Huang, W.J., Huang, C.H., Wu, C.L., Lin, J.K., Chen, Y.W., Lin, C.L., Chuang, S.E., Huang, C.Y. and Chen, C.N. (2007) Propolin G, a prenylflavanone, isolated from Taiwanese propolis, induces caspase-dependent apoptosis in brain cancer cells. J. Agric. Food Chem., 55, 7366-7376. https://doi.org/10.1021/jf0710579
  47. Weng, M.S., Liao, C.H., Chen, C.N., Wu, C.L. and Lin, J.K. (2007) Propolin H. from Taiwanese propolis induces G1 arrest in human lung carcinoma cells. J. Agric. Food Chem., 55, 5289-5298. https://doi.org/10.1021/jf070201n
  48. Sforcin, J.M. (2007) Propolis and the immune system: a review. J. Ethnopharmacol., 113, 1-14. https://doi.org/10.1016/j.jep.2007.05.012
  49. Moon, J.Y., Lee, E.J. and Yoo, B.S. (2012) Propolis Protects Human Keratinocyte HaCaT Cells against UV-induced Apoptosis. Journal of Apiculture, 27, 243-249.
  50. Tavares, D.C., Mazzaron Barcelos, G.R., Silva, L.F., Chacon Tonin, C.C. and Bastos, J.K. (2006) Propolis-induced genotoxicity and antigenotoxicity in Chinese hamster ovary cells. Toxicol. In Vitro, 20, 1154-1158. https://doi.org/10.1016/j.tiv.2006.02.009

Cited by

  1. 3-Bromo-4,5-dihydroxybenzaldehyde Enhances the Level of Reduced Glutathione via the Nrf2-Mediated Pathway in Human Keratinocytes vol.15, pp.9, 2017, https://doi.org/10.3390/md15090291
  2. RIP1-dependent reactive oxygen species production executes artesunate-induced cell death in renal carcinoma Caki cells vol.435, pp.1-2, 2017, https://doi.org/10.1007/s11010-017-3052-7
  3. Luteolin induces apoptotic cell death via antioxidant activity in human colon cancer cells vol.51, pp.4, 2017, https://doi.org/10.3892/ijo.2017.4091
  4. Risk management of free radicals involved in air travel syndromes by antioxidants vol.21, pp.2, 2018, https://doi.org/10.1080/10937404.2018.1427914
  5. Proteomic Changes in Chick Brain Proteome Post Treatment with Lathyrus Sativus Neurotoxin, β-N-Oxalyl-L-α,β-Diaminopropionic Acid (L-ODAP): A Better Insight to Transient Neurolathyrism vol.34, pp.3, 2018, https://doi.org/10.5487/TR.2018.34.3.267
  6. Particulate matter 2.5 damages skin cells by inducing oxidative stress, subcellular organelle dysfunction, and apoptosis vol.92, pp.6, 2018, https://doi.org/10.1007/s00204-018-2197-9
  7. Induction of Apoptosis by Citrus unshiu Peel in Human Breast Cancer MCF-7 Cells: Involvement of ROS-Dependent Activation of AMPK vol.41, pp.5, 2018, https://doi.org/10.1248/bpb.b17-00898
  8. peel in MDA-MB-231 human breast carcinoma cells vol.12, pp.2, 2018, https://doi.org/10.4162/nrp.2018.12.2.129
  9. Natural Antioxidants: Multiple Mechanisms to Protect Skin From Solar Radiation vol.9, pp.1663-9812, 2018, https://doi.org/10.3389/fphar.2018.00392
  10. Dihydrocaffeic Acid Prevents UVB-Induced Oxidative Stress Leading to the Inhibition of Apoptosis and MMP-1 Expression via p38 Signaling Pathway vol.2019, pp.1942-0994, 2019, https://doi.org/10.1155/2019/2419096