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Antiapoptotic effect of gangliosides on PC12 cells exposed to bacterial lipopolysaccharide

  • Comparative and Ontogenic Biochemistry
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Abstract

Lipopolysaccharide (LPS) from the Escherichia coli serotype 0111:B4 at concentrations of 0.1 and 0.125 mg/ml was shown to exert an apoptotic effect on the neuronal PC12 cell line in DMEM (serum free medium). Gangliosides GD1a and GM1 at a concentration of 100 μM were found to raise the PC12 cell line viability and decrease the percentage of PC12 cells in the late-phase apoptosis after exposure to LPS.

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References

  1. Anisman, H., Merali, Z., and Hayley, S., Neurotransmitter, peptide and cytokine processes in relation to depressive disorder: comorbidity between depression and neurodegenerative disorders, Prog. Neurobiol., 2008, vol. 85(1), pp. 1–74.

    Article  CAS  PubMed  Google Scholar 

  2. Ye, J., Liu, Z., Wei, J., Lu, L., Huang, Y., Luo, L., and Xie, H., Protective effect of SIRT1 on toxicity of microglial-derived factors induced by LPS to PC12 cells via the p53-caspase-3-dependent apoptotic pathway, Neurosci. Lett., 2013, vol. 553, pp. 72–77.

    Article  CAS  PubMed  Google Scholar 

  3. Mayer, A.M., Therapeutic implications of microglia activation by lipopolysaccharide and reactive oxygen species generation in septic shock and central nervous system pathologies: a review, Medicina, 1998, vol. 58, pp. 377–385.

    CAS  PubMed  Google Scholar 

  4. Heneka, M.T., Loschmann, P.A., Gleichmann, M., Weller, M., Schulz, J.B., Wullner, U., and Klockgether, T., Induction of nitric oxide synthase and nitric oxide-mediated apoptosis in neuronal PC12 Cells after stimulation with tumor necrosis factor-alpha/lipopolysaccharide, J. Neurochem., 1998, vol. 71, pp. 88–94.

    Article  CAS  PubMed  Google Scholar 

  5. Huang, Y.H., Chang, A.Y., Huang, C.M., Huang, S.W., and Chan, S.H., Proteomic analysis of lipopolysaccharide-induced apoptosis in PC12 cells, Proteomics, 2002, vol. 2, pp. 1220–1228.

    Article  CAS  PubMed  Google Scholar 

  6. Ansari, N., Khodagholi, F., Amini, M., and Shaerzadeh, F., Attenuation of LPS-induced apoptosis in NGF differentiated PC12 cells via NF-κB pathway and regulation of redox status by an oxazine derivative, Biochimie, 2011, vol. 93, pp. 899–908.

    Article  CAS  PubMed  Google Scholar 

  7. Ansari, N., Khodagholi, F., Ramin, M., Amini, M., Irannejad, H., Dargahi, L., and Amirabad, A.D., Inhibition of LPS-induced apoptosis in differentiated PC12 by new thiazin derivatives through NF-κB-mediated suppression of COX-2, Neurochem. Int., 2010, vol. 57, pp. 958–968.

    Article  CAS  PubMed  Google Scholar 

  8. Dholakiya, S.L. and Benzeroual, K.E., Protective effect of diosmin on LPS-induced apoptosis in PC12 cells and inhibition of TNF-α expression, Toxicol. In Vitro, 2011, vol. 25, pp. 1039–1044.

    Article  CAS  PubMed  Google Scholar 

  9. Avrova, N.F., Sokolova, T.V., Vlasova, Y.A., Zakharova, I.O., Furaev, V.V., and Rychkova, M.P., Protective and antioxidative effects of GM1 ganglioside in PC12 cells exposed to hydrogen peroxide are mediated by Trk tyrosine kinase, Neurochem. Res., 2010, vol. 35, pp. 85–98.

    Article  CAS  PubMed  Google Scholar 

  10. Avrova, N.F., Victorov, I.V., Tyurin, V.A., Zakharova, I.O., Sokolova, T.V., Andreeva, N.A., Stelmaschuk, E.V., Tyurina, Y.Y., and Gonchar, V.S., Inhibition of glutamate-induced intensification of free radical reactions by gangliosides: possible role in their protective effect in rat cerebellar granule cells and brain synaptosomes, Neurochem. Res., 1998, vol. 23, pp. 945–952.

    Article  CAS  PubMed  Google Scholar 

  11. Fighera, M.R., Royes, L.F., Furian, A.F., Oliveira, M.S., Florenza, N.G., Frussa-Filho, R., Petry, J.C., Coelho, R.C., and Mello, C.F., GM1 prevents seizures, Na+,K+-ATP-ase activity inhibition and oxidative stress induced by glutaric acid and pentylenetetrazole, Neurobiol. Dis., 2006, vol. 22, pp. 611–623.

    Article  CAS  PubMed  Google Scholar 

  12. Park, E.J., Thomson, A.B., and Clandinin, M.T., Protection of intestinal occludin tight junction protein by dietary gangliosides in lipopolysaccaride-induced acute inflammation, J. Pediatr. Gastroenterol. Nutr., 2010, vol. 50, pp. 321–328.

    Article  CAS  PubMed  Google Scholar 

  13. Hansen, M.B., Nielsen, S.E., and Berg, K., Reexamination and further development of a precise and rapid dye method for measuring cell growth/cell kill, J. Immunol. Methods, 1989, vol. 119, pp. 203–210.

    Article  CAS  PubMed  Google Scholar 

  14. Folch, J., Lees, M., and Sloan-Stanley, G.H., A simple method for isolation and purification of total lipids from animal tissue, J. Biol. Chem., 1957, vol. 226., pp. 497–509.

    CAS  PubMed  Google Scholar 

  15. Bayunova, L.V., Vlasova, Yu.A., Sokolova, T.V., Zakharova, I.O., Parnova, R.G., and Avrova, N.F., Protective effect of ganglioside GD1a and inhibitor of nitrite oxide synthase under influence of bacterial lipopolysaccharide on PC12 cells, Neirokhimiya, 2012, vol. 29, no. 4, pp. 305–310.

    Google Scholar 

  16. Vlasova, Yu.A., Bayunova, L.V., Mikurova, E.I., Lyakhovnenko, Yu.B., Nikolaeva, S.D., Parnova, R.G., and Avrova, N.F., Protective effect of gangliosides against toxic influence on PC12 cells of bacterial lipopolysaccharide of different serotypes, Ross. Fisiol. Zh. im. I.M.Sechenova, 2013, vol. 99, no. 7, pp. 876–887.

    CAS  Google Scholar 

  17. Hadjiconstantinou, M. and Neff, N.H., GM1 ganglioside: in vivo and in vitro trophic actions on central neurotransmitter systems, J. Neurochem., 1998, vol. 70, pp. 1535–1345.

    Google Scholar 

  18. Bachis, A., Rabin, S.J., Del Fiacco, M., and Moccheti, I., Gangliosides prevent excitotoxicity through activation of TrkB receptor, Neurotox. Res., 2002, vol. 4, pp. 225–234.

    Article  CAS  PubMed  Google Scholar 

  19. Sokolova, T.V., Zakharova, I.O., Furaev, V.V., Rychkova, M.P., and Avrova, N.F., Neuroprotective effect of ganglioside GM1 on the cytotoxic action of hydrogen peroxide and amyloid betapeptide in PC12 cells, J. Neurochem. Res., 2007, vol. 32, pp. 1302–1313.

    Article  CAS  Google Scholar 

  20. Kreutz, F., Frozza, R.L., Breier, A. C., de Oliveira, V.A., Horn, A.P., Pettenuzzo, L.F., Netto, C.A., Salbego, C.G., and Trindade, V.M., Amyloid-β induced toxicity involves ganglioside expression and is sensitive to GM1 neuroprotective action, Neurochem. Int., 2011, vol. 59, pp. 648–655.

    Article  CAS  PubMed  Google Scholar 

  21. Ferrari, G., Anderson, B.L., Stephens, R.M., Kaplan, D.R., and Greene, L.A., Prevention of apoptotic neuronal death by GM1 ganglioside. Involvement of Trk neurotrophin receptors, J. Biol. Chem., 1995, vol. 270, pp. 3074–3080.

    Article  CAS  PubMed  Google Scholar 

  22. Ferrari, G. and Greene, L.A., Prevention of neuronal apoptotic death by neurotrophic agents and ganglioside GM1: insights and speculations regarding a common mechanism, Perspect. Dev. Neurobiol., 1996, vol. 3, pp. 93–100.

    CAS  PubMed  Google Scholar 

  23. Schnabl, K.L., Larsen, B., Van Aerde, J.E., Lees, G., Evans, M., Belosevic, M., Field, C., Thomson, A.B., and Clandinin, M.T., Gangliosides protect bowel in an infant model of necrotizing enterocolitis by suppressing proinflammatory signals, J. Pediatr. Gastroenterol. Nutr., 2009, vol. 49, pp. 382–392.

    Article  CAS  PubMed  Google Scholar 

  24. Shen, W., Stone, K., Jales, A., Leitenberg, D., and Ladisch, S.J., Inhibition of TLR activation and upregulation of IL IR-associated kinase M expression by exogenous gangliodides, J. Immunol., 2008, vol. 180, pp. 4425–4432.

    Article  CAS  PubMed  Google Scholar 

  25. Sharifi, A.M., Hoda, F.E., and Noor, A.M., Studying the effect of LPS on cytotoxicity and apoptosis in PC12 neuronal cells: role of Bax, Bcl-2, and Caspase-3 protein expression, Toxicol. Mech. Methods, 2010, vol. 20, pp. 318–320.

    Article  Google Scholar 

  26. Omata, Y., Saito, Y., Fujita, K., Ogawa, Y., Nishio, K., Yoshida, Y., and Niki, E., Induction of adaptive response and enhancement of PC12 cell tolerance by lipopolysaccharide primarily through the upregulation of glutathione S-transferase A3 via Nrf2 activation, Free Radic Biol Med., 2008, vol. 45, pp. 1437–1445.

    Article  CAS  PubMed  Google Scholar 

  27. Olsson, S. and Sundler, R., The role of lipid rafts in LPS-induced signaling in a macrophage cell line, Mol. Immunol., 2006, vol. 43, pp. 607–612.

    Article  CAS  PubMed  Google Scholar 

  28. Nikolaeva, S., Sokolova, T., Bayunova, L., and Parnova, R., Protective effect of GD1a and GM1 gangliosides against the toxic action of bacterial lipopolysaccharide on neuronal and epithelial cells, FEBS J., 2013, Suppl. 1, p. 433.

    Google Scholar 

  29. Sibiryak, S.V., Kha’dukov, S.V., and Zurochka, A.V., Evaluation of Apoptosis in Immunologi cal Investigations, Voprosy sovremennoi protochnoi tsitometrii. Klinicheskoe primenenie (Problems of Contemporary Flow Cytometry. Clinical Application), Kha’dukov, S.V. and Zurochka, A.V., Eds., Chelyabinsk, 2008, pp. 63–112.

    Google Scholar 

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Correspondence to L. V. Bayunova.

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Original Russian Text © L.V. Bayunova, R.G. Parnova, N.F. Avrova, 2015, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2015, Vol. 51, No. 2, pp. 88–95.

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Bayunova, L.V., Parnova, R.G. & Avrova, N.F. Antiapoptotic effect of gangliosides on PC12 cells exposed to bacterial lipopolysaccharide. J Evol Biochem Phys 51, 98–106 (2015). https://doi.org/10.1134/S0022093015020027

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  • DOI: https://doi.org/10.1134/S0022093015020027

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