Toxicological Research

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

DOI QR Code

Propolis Inhibits Neurite Outgrowth in Differentiating SH-SY5Y Human Neuroblastoma Cells

  • Received : 2016.06.07
  • Accepted : 2016.06.16
  • Published : 2016.07.15
Download PDF
⟨ Previous Next ⟩

Abstract

Propolis is a multicomponent, active, complex resinous substance collected by honeybees from a variety of plant sources. We have studied the effect of propolis on neurite outgrowth of SH-SY5Y human neuroblastoma cells induced to differentiate by all-trans-retinoic acid (RA). Propolis, at a concentration of $3{\mu}g/mL$, had no significant effect on the viability of differentiating SH-SY5Y cells. However, the neurite outgrowth of the differentiating SH-SY5Y cells treated with propolis ($0.3{\sim}3{\mu}g/mL$) for 48 hr was significantly inhibited in a dose-dependent manner. Treatment of RA-stimulated differentiating SH-SY5Y cells with 0.3 to $3{\mu}g/mL$ propolis resulted in decreased level of transglutaminase and 43-kDa growth-associated protein (GAP-43) in a dose-dependent manner. The results indicate that propolis is able to inhibit neurite outgrowth of differentiating SH-SY5Y cells.

Keywords

References

  1. Drago, B., Mombelli, B., De Vecchi, E., Fassina, M.C., Tocalli, L. and Gismondo, M.R. (2000) In vitro antimicrobial activity of propolis dry extract. J. Chemother., 12, 390-395. https://doi.org/10.1179/joc.2000.12.5.390
  2. Mizoeva, O.K. and Calder, P.C. (1996) The effect of propolis and its components on eicosanoid production during the inflammatory response. Prostaglandins Leukot. Essent. Fatty Acids, 55, 441-449. https://doi.org/10.1016/S0952-3278(96)90129-5
  3. Krol, W., Czuba, Z., Scheller, S., Gabrys, J., Grabiec, S. and Shani, J. (1990) Anti-oxidant property of ethanolic extract of propolis (EEP) as evaluated by inhibiting the chemiluminescence oxidation of luminal. Biochem. Int., 21, 593-597.
  4. Scheller, S., Wilczok, T., Imielski, S., Krol, W., Gabrys, J. and Shani, J. (1990) Free radical scavenging by ethanol extract of propolis. Int. J. Radiat. Biol., 57, 461-465. https://doi.org/10.1080/09553009014552601
  5. Chen, S.N., Weng, M.S., Wu, C.L. and Lin, J.K. (2004) Comparison of radical scavenging activity, cytotoxic effects and apoptosis induction in human melanoma cells by Taiwanese propolis from different sources. Evid. Based Complement. Alternat. Med., 1, 175-185. https://doi.org/10.1093/ecam/neh034
  6. Matsuno, T. (1993) Isolation and characterization of the tumoricidal substance from Brazilian propolis. Honeybee Sci., 13, 49-54.
  7. Castaldo, S. and Capasso, F. (2002) Propolis, an old remedy used in modern medicine. Fitoterapia, 73, S1-S6. https://doi.org/10.1016/S0367-326X(02)00185-5
  8. Scheller, S., Krol, W., Swiacik, J., Owezarek, S., Gabrys, J. and Shani, J. (1989) Antitumoral property of ethanolic extract of propolis in mice-bearing Ehrlich carcinoma, as compared to bleomycin. Z. Naturforsch., C, J. Biosci., 44, 1063-1065.
  9. 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.
  10. Rao, C.V., Desai, D., Rivenson, A., Simi, B., Amin, S. and Reddy, B.S. (1995) Chemoprevention of colon carcinogenesis by phenylethyl-3-methylcaffeate. Cancer Res., 55, 2310-2315.
  11. Fournier, A.E., Takizawa, B.T. and Strittmatte, S.M. (2003) Rho kinase inhibition enhances axonal regeneration in the injured CNS. J. Neurosci., 23, 1416-1423. https://doi.org/10.1523/JNEUROSCI.23-04-01416.2003
  12. Lehmann, M., Fournier, A., Selles-Navarro, I., Dergham, P., Sebok, A., Leclerc, N., Tigyi, G. and McKerracher, L. (1999) Inactivation of Rho signaling pathway promotes CNS axon regeneration. J. Neurosci., 19, 7537-7547. https://doi.org/10.1523/JNEUROSCI.19-17-07537.1999
  13. Itano, Y. and Nomura, Y. (1995) 1-Methyl-4-phenylpyridinium ion (MPP+) causes DNA fragmentation and increases Bcl-2 expression in human neuroblastoma, SH-SY5Y cells, through different mechanisms. Brain Res., 704, 240-245. https://doi.org/10.1016/0006-8993(95)01120-X
  14. Tosetti, P., Taglietti, V. and Toselli, M. (1998) Functional changes in potassium conductances of the human neuroblastoma cell line SH-SY5Y during in vitro differentiation. J. Neurophysiol., 79, 648-658. https://doi.org/10.1152/jn.1998.79.2.648
  15. Uberti, D., Piccioni, L., Colzi, A., Bravi, D., Canonico, P.L. and Memo, M. (2002) Pergolide protects SH-SY5Y cells against neurodegeneration induced by $H_2O_2$. Eur. J. Pharmacol., 434, 17-20. https://doi.org/10.1016/S0014-2999(01)01537-0
  16. Singh, U.S., Pan, J., Kao, Y.L., Joshi, S., Young, K.L. and Baker, K.M. (2003) Tissue transglutaminase mediates activation of RhoA and MAP kinase pathways during retinoic acidinduced neuronal differentiation of SH-SY5Y cells. J. Biol. Chem., 278, 391-399. https://doi.org/10.1074/jbc.M206361200
  17. Tucholski, J., Lesort, M. and Johnson, G.V. (2001) Tissue transglutaminase is essential for neurite outgrowth in human neuroblastoma SHSY5Y cells. Neuroscience, 102, 481-491. https://doi.org/10.1016/S0306-4522(00)00482-6
  18. Kosik, K.S., Orecchio, L.D., Bruns, G.A., Benowitz, L.I., MacDonald, G.P., Cox, D.R. and Neve, R.L. (1988) Human GAP-43: its deduced amino acid sequence and chromosomal localization in mouse and human. Neuron, 1, 127-132. https://doi.org/10.1016/0896-6273(88)90196-1
  19. Keilbaugh, S.A., Prusoff, W.H. and Simpson, M.V. (1991) The PC12 cell as a model for studies of the mechanism of induction of peripheral neuropathy by anti-HIV-1 dideoxynucleoside analogs. Biochem. Pharmacol., 42, R5-R8. https://doi.org/10.1016/0006-2952(91)90672-R
  20. Bankova, V.S., De Castro, S.L. and Marucci, M.C. (2000) Propolis: recent advances in chemistry and plant origin. Apidologie, 31, 3-15. https://doi.org/10.1051/apido:2000102
  21. Tucholski, J., Lesort, M. and Johnson, G.V. (2001) Tissue transglutaminase is essential for neurite outgrowth in human neuroblastoma SH-SY5Y cells. Neuroscience, 102, 481-491. https://doi.org/10.1016/S0306-4522(00)00482-6
  22. Zhang, J., Lesort, M., Guttmann, R.P. and Johnson, G.V. (1998) Modulation of the in situ activity of tissue transglutaminase by calcium and GTP. J. Biol. Chem., 273, 2288-2295. https://doi.org/10.1074/jbc.273.4.2288
  23. Sidell, N. (1982) Retinoic acid-induced growth inhibition and morphologic differentiation of human neuroblastoma cells in vitro. J. Natl. Cancer Inst., 68, 589-596.
  24. Pahlman, S., Ruusala, A.I., Abrahamsson, L., Mattsson, M.E. and Esscher, T. (1984) Retinoic acid-induced differentiation of cultured human neuroblastoma cells: a comparison with phorbolester-induced differentiation. Cell Differ., 14, 135-144. https://doi.org/10.1016/0045-6039(84)90038-1
  25. Sforcin, J.M., Kaneno, R. and Funari, S.R.C. (2002) Absence of seasonal effect on the immunomodulatory action of Brazilian propolis on natural killer activity. J. Venom. Anim. Toxins, 8, 19-29. https://doi.org/10.1590/S0104-79302002000100003
  26. Chen, Y.J., Huang, A.C., Chang, H.H., Liao, H.F., Jiang, C.M., Lai, L.Y., Chan, J.T., Chen, Y.Y. and Chiang, J. (2009) Caffeic acid phenethyl ester, an antioxidant from propolis, protects peripheral blood mononuclear cells of competitive cyclists against hyperthermal stress. J. Food Sci., 74, H162-H167. https://doi.org/10.1111/j.1750-3841.2009.01199.x
  27. Gekker, G., Hu, S., Spivak, M., Lokensgard, J.R. and Peterson, P.K. (2005) Anti-HIV-1 activity of propolis in CD4(+) lymphocyte and microglial cell cultures. J. Ethnopharmacol., 102, 158-163. https://doi.org/10.1016/j.jep.2005.05.045
  28. Sforcin, J.M., Fernandes, A. Jr., Lopes, C.A.M., Funari, S.R.C. and Bankova, V. (2001) Seasonal effect of Brazilian propolis on Candida albicans and Candida tropicalis. J. Venom. Anim. Toxins, 7, 139-144. https://doi.org/10.1590/S0104-79302001000100009
  29. Freitas, S.F., Shinohara, L., Sforcin, J.M. and Guimaraes, S. (2006) In vitro effects of propolis on Giardia duodenalis trophozoites. Phytomedicine, 13, 170-175. https://doi.org/10.1016/j.phymed.2004.07.008
  30. Heinrich, M., Modarai, M. and Kortenkamp, A. (2008) Herbal extracts used for upper respiratory tract infections: are there clinically relevant interactions with the cytochrome P450 enzyme system? Planta Med., 74, 657-660. https://doi.org/10.1055/s-2008-1034292
  31. Edsjo, A., Holmquist, L. and Pahlman, S. (2007) Neuroblastoma as an experimental model for neuronal differentiation and hypoxia-induced tumor cell dedifferentiation. Semin. Cancer Biol., 17, 248-256. https://doi.org/10.1016/j.semcancer.2006.04.005
  32. Fournier, A.E., Takizawa, B.T. and Strittmatte, S.M. (2003) Rho kinase inhibition enhances axonal regeneration in the injured CNS. J. Neurosci., 23, 1416-1423. https://doi.org/10.1523/JNEUROSCI.23-04-01416.2003

Cited by

  1. Caffeic Acid Phenethyl Ester (CAPE) Protects PC12 Cells from Cisplatin-Induced Neurotoxicity by Activating the NGF-Signaling Pathway pp.1476-3524, 2017, https://doi.org/10.1007/s12640-017-9849-z
  2. Mechanism of Activating the Proprioceptive NT-3/TrkC Signalling Pathway by Reverse Intervention for the Anterior Cruciate Ligament–Hamstring Reflex Arc with Electroacupuncture vol.2018, pp.2314-6141, 2018, https://doi.org/10.1155/2018/6348764