Abstract
The effect of coenzyme Q10 on glioma-cell proliferation under serum-deprived conditions has been studied. Our results have shown that the addition of coenzyme Q10 into a serum-free culture medium enhances cell viability, stimulates cell growth, restores mitochondrial potential, and increases the quantity of energized mitochondria. It is found that coenzyme Q10-induced glioma-cell proliferation in conditions of serum deficiency is a result of an intracellular reduced glutathione concentration with subsequent activation of protein kinase C, ERK1/2, and phosphoinositol-3-kinase.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- ROS:
-
reactive oxygen species
- EGF:
-
epidermal growth factor
- FBS:
-
fetal bovine serum
- GSH:
-
reduced glutathione
- H2DCF-DA:
-
2,7-dichlorodihydrofluorescein diacetate
- MCB:
-
monochlorobimane
- PI3K:
-
phosphoinositol-3-kinase
- PKC:
-
protein kinase C
- S1P:
-
sphingosine-1-phosphate
- SMPD:
-
sphingomyelin phosphodiesterase
- SphK:
-
sphingosine kinase
References
Bentinger, M., Brismar, K., and Dallner, G., The antioxidant role of coenzyme Q, Mitochondrion, 2007, vol. 7S, pp. 41–50.
Brea-Calvo, G., Rodríguez-Hernández, Á., Fernández-Ayala, D.J.M., Navas, P., and Sánchez-Alcázar, J.A., Chemotherapy induces an increase in coenzyme Q10 levels in cancer cell lines, Free Rad. Biol. Med., 2006, vol. 40, pp. 1293–1302.
Burova, E.B., Vasilenko, K.P., Antonov, V.G., and Nikol’skii, N.N., Transactivation of the epidermal growth factor receptor by oxidized glutathione and its pharmacological analogue glutoxim in A431 cells, Dokl. Biol. Sci., 2005, vol. 404, pp. 392–394.
Chen, C.L., Lin, C.F., Chang, W.T., Huang, W.C., Teng, C.F., and Lin, Y.S., Ceramide induces p38 MAPK and JNK activation through a mechanism involving a thioredoxin-interacting protein-mediated pathway, Blood, 2008, vol. 111, pp. 4365–4374.
Conklin, K.A., Coenzyme Q10 for prevention of anthracycline-induced cardiotoxicity, Integr. Cancer Ther., 2005, vol. 4, pp. 110–130.
Crane, F.L., New functions for coenzyme Q, Protoplasma, 2000, vol. 213, pp. 127–133.
Davis, R.J., Signal transduction by the JNK group of MAP kinases, Cell, 2000, vol. 103, pp. 239–252.
De Cabo, R., Cabello, R., Rios, M., Lopez-Lluch, G., Ingram, D.K., Lane, M.A., and Navas, P., Calorie restriction attenuates age-related alterations in the plasma membrane antioxidant system in rat liver, Exp. Gerontol., 2004, vol. 39, pp. 297–304.
Du, L., Lyle, C.S., Obey, T.B., Gaarde, W.A., Muir, J.A., Bennett, B.L., and Chambers, T.C., Inhibition of cell proliferation and cell cycle progression by specific inhibition of basal JNK activity. Evidence that mitotic Bcl-2 phosphorylation is JNK-independent, J. Biol. Chem., 2004, vol. 279, pp. 11957–11966.
Gómez-Díaz, C., Barroso, M.P., and Navas, P., Plasma membrane coenzyme Q10 and growth control, Protoplasma, 2000, vol. 214, pp. 19–23.
Groneberg, D.A., Kindermann, B., Althammer, M., Klapper, M., Vormann, J., Littarru, G.P., and Doring, F., Coenzyme Q10 affects expression of genes involved in cell signalling, metabolism and transport in human CaCo-2 cells, Int. J. Biochem. Cell Biol., 2005, vol. 37, pp. 1208–1218.
Johnson, K.R., Becker, K.P., Facchinetti, M.M., Hannun, Y.A., and Obeid, L.M., PKC-dependent activation of sphingosine kinase 1 and translocation to the plasma membrane, J. Biol. Chem., 2002, vol. 277, pp. 35257–35262.
Kato, F., Tanaka, M., and Nakamura, K., Rapid fluorometric assay for cell viability and cell growth using nucleic acid staining and cell lysis agents, Toxicol. in Vitro, 1999, vol. 13, pp. 923–929.
Kim, J.H., Kim, J.H., Song, W.K., Kim, J.H., and Chun, J.S., Sphingosine 1-phosphate activates Erk-1/-2 by transactivating epidermal growth factor receptor in Rat-2 cells, Life, 2000, vol. 50, pp. 119–124.
Krylova, N.G., Monitoring of erythrocyte redox-properties with use of 2,7-dichlorofluorescein, in Molodezh’ v nauke–2007: pril. k zhurn. Vestsi NAN Belarusi. 4 (3): 22–26 (Young People in Science–2007: Supplement to Proc. Natl. Acad. Sci. Belarus. 4 (3): 22–26), Minsk: Belarus, Nauka, 2008.
Littarru, P., and Tiano, L., Clinical aspects of coenzyme Q10: an update, Nutrition, 2010, vol. 26, pp. 250–254.
Liu, B. and Hannun, Y.A., Inhibition of the neutral magnesium-dependent sphingomyelinase by glutathione, J. Biol. Chem., 1997, vol. 272, pp. 6281–16287.
López-Lluch, G., Barroso, M.P., Martín, S.F., Fernández-Ayala, D.J.M., Gómez-Díaz, C., Villalba, J.M., and Navas, P., Role of plasma membrane coenzyme Q on the regulation of apoptosis, BioFactors, 1999, vol. 9, pp. 171–177.
Makino, N., Mochizuki, Y., Bannai, S., and Sugita, Y., kinetic studies on the removal of extracellular hydrogen peroxide by cultured fibroblasts, J. Biol. Chem., 1994, vol. 269, pp. 1020–1025.
Mansat, V., Laurent, G., Levade, T., Bettaieb, A., and Jaffrezou, J.-P., The protein kinase c activators phorbol esters and phosphatidylserine inhibit neutral sphingomyelinase activation, ceramide generation, and apoptosis triggered by daunorubicin, Cancer Res., 1997, vol. 57, pp. 5300–5304.
Martin, S.F., Navarro, F., Forthoffer, N., Navas, P., and Villalba, J.M., Neutral magnesium-dependent sphingomyelinase from liver plasma membrane: purification and inhibition by ubiquinol, J. Bioenerg. Biomembr., 2001, vol. 33, pp. 143–153.
Martín, S.F., Gómez-Díaz, C., Bello, R.I., Navas, P., and Villalba, J.M., Inhibition of Neutral Mg2+-dependent sphingomyelinase byubiquinol-mediated plasma membrane electron transport, Protoplasma, 2003, vol. 221, pp. 109–116.
Navarro, F., Villalba, J.M., Crane, F.L., McKellar, W.C., and Navas, P., A phospholipid-dependent NADH-coenzyme Q reductase from liver plasma membrane, Biochem. Biophys. Res. Commun., 1995, vol. 212, pp. 138–143.
Navas, P., Fernández-Ayala, D.J.M., Martín, S.F., López-Lluch, G., de Cabo, R., Rodriguez-Aguilera, J.C., and Villalba, J.M., Ceramide-dependent caspase 3 activation is prevented by coenzyme Q from plasma membrane in serum-deprived cells, Free Rad. Res., 2002, vol. 364, pp. 369–374.
Navas, P., Villalba, J.M., and de Cabo, R., The importance of plasma membrane coenzyme Q in aging and stress responses, Mitochondrion, 2007, vol. 7S, pp. 34–40.
Nordman, T., Xia, L., Björkhem-Bergman, L., Damdimopoulos, A., Nalvarte, I., Arnér, E.S., Spyrou, G., Eriksson, L.C., Björnstedt, M., and Olsson, J.M., Regeneration of the antioxidant ubiquinol by lipoamide dehydrogenase, thioredoxin reductase and glutathione reductase, BioFactors, 2003, vol. 18, pp. 45–50.
Smiley, S.T., Reers, M., Mottola-Hartshorn, C., Lin, M., Chen, A., Smith, T.W., Steele, G.D., and Chen, L.B., Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregateforming lipophilic cation JC-1, Proc. Natl. Acad. Sci. U. S. A., 1991, vol. 88, pp. 3671–3675.
Soni, A., Verma, M., Aggarwal, S., Kaushal, V., and Verma, Y., Role of coenzyme Q10 in current oncology practice: substance or shadow!, OncoExpert, 2015, vol. 1, pp. 14–22.
Thornton, T.M. and Rincon, M., Non-classical p38 MAP kinase functions: cell cycle checkpoints and survival, Int. J. Biol. Sci., 2009, vol. 5, pp. 44–52.
Trachootham, D., Lu, W., Ogasawara, M.A., Rivera-del Valle, N., and Huang, P., Redox regulation of cell survival, Antioxid. Rerox Signal., 2008, vol. 10, pp. 1343–1374.
Ueda, N., Ceramide-induced apoptosis in renal tubular cells: a role of mitochondria and sphingosine-1-phoshate, Int. J. Mol. Sci., 2015, vol. 16, pp. 5076–5124.
Vaupel, P., Tumor microenvironmental physiology and its implications for radiation oncology, Semin. Radiat. Oncol., 2004, vol. 14, pp. 198–206.
Villalba, J.M. and Navas, P., Plasma membrane redox system in the control of stress-induced apoptosis, Antioxid. Redox. Signal., 2000, vol. 2, pp. 213–230.
Wada, T. and Penninger, J.M., Mitogen-activated protein kinases in apoptosis regulation, Oncogene, 2004, vol. 23, pp. 2838–2849.
Wang, Z., Mutual regulation of receptor-mediated cell signalling and endocytosis: EGF receptor system as an example, in Molecular Regulation of Endocytosis, Rijeka: InTech Publ., 2012, pp. 301–330.
Wrona, M. and Wardmann, P., Properties of the radical intermediate obtained on oxidation of 2′,7′-dichlorodihydrofluorescein, a probe for oxidative stress, Free Rad. Biol. Med., 2006, vol. 41, pp. 657–667.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © N.G. Krylova, T.A. Kulahava, S.V. Koran, G.N. Semenkova, 2017, published in Tsitologiya, 2017, Vol. 59, No. 2, pp. 109–116.
Rights and permissions
About this article
Cite this article
Krylova, N.G., Kulahava, T.A., Koran, S.V. et al. Proliferation of cultured glioma cells mediated by coenzyme Q10 under conditions of serum deprivation. Cell Tiss. Biol. 11, 220–226 (2017). https://doi.org/10.1134/S1990519X17030063
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1990519X17030063