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Plasma Membrane Ubiquinone Controls Ceramide Production and Prevents Cell Death Induced by Serum Withdrawal

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Abstract

Serum provides cultured cells with survival factors required to maintain growth. Its withdrawal induces the development of programmed cell death. HL-60 cells were sensitive to serum removal, and an increase of lipid peroxidation and apoptosis was observed. Long-term treatment with ethidium bromide induced the mitochondria-deficient ρ°HL-60 cell line. These cells were surprisingly more resistant to serum removal, displaying fewer apoptotic cells and lower lipid peroxidation. HL-60 cells contained less ubiquinone at the plasma membrane than ρ°HL-60 cells. Both cell types increased plasma membrane ubiquinone in response to serum removal, although this increase was much higher in ρ° cells. Addition of ubiquinone to both cell cultures in the absence of serum improved cell survival with decreasing lipid peroxidation and apoptosis. Ceramide was accumulated after serum removal in HL-60 but not in ρ°HL-60 cells, and exogenous ubiquinone reduced this accumulation. These results demonstrate a relationship between ubiquinone levels in the plasma membrane and the induction of serum withdrawal induced apoptosis, and ceramide accumulation. Thus, ubiquinone, which is a central component of the plasma membrane electron transport system, can represent a first level of protection against oxidative damage caused by serum withdrawal.

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REFERENCES

  • Alcaín, F. J., Burón, M. I., Villalba, J. M., and Navas, P. (1991). Biochim. Biophys. Acta 1073, 380–385.

    Google Scholar 

  • Beyer, R. E. (1994). J. Bioenerg. Biomembr. 26, 349–358.

    PubMed  Google Scholar 

  • de Jong, D., Prins, F. A., Maason, D. Y., Reed, J. C., van Ommen, G. B., and Kluin, P. M. (1994). Cancer Res. 54, 256–260.

    PubMed  Google Scholar 

  • Desjardins, P., Frost, E., and Morais, R. (1985). Mol. Cell. Biol. 5, 1163–1169.

    PubMed  Google Scholar 

  • Do, T. Q., Schultz, J. R., and Clarke, C. F. (1996). Proc. Natl. Acad. Sci. USA 93, 7534–7539.

    PubMed  Google Scholar 

  • Gómez-Díaz, C., Rodríguez-Aguilera, J. C., Barroso, M. P., Villalba, J. M., Navarro, F., Crane, F. L., and Navas, P. (1997). J. Bioenerg. Biomembr. 29, 251–257.

    PubMed  Google Scholar 

  • Greenlund, L. J. S., Beckwerth, T. L., and Johnson, E. M. J. (1995). Neuron 14, 303–314.

    PubMed  Google Scholar 

  • Hannun, Y. A. (1996). Science 274, 1855–1859.

    PubMed  Google Scholar 

  • Hockenbery, D. M., Oltvai, Z. N., Yin, X.-M., Milliman, C. L., and Korsmeyer, S. J. (1993). Cell 75, 241–251.

    PubMed  Google Scholar 

  • Ishizaki, Y., Cheng, L., Mudge, A. W., and Raff, M. C. (1995). Mol. Biol. Cell. 6, 1443–1458.

    PubMed  Google Scholar 

  • Jacobson, M. D., and Raff, M. C. (1995). Nature 374, 814–816.

    Article  PubMed  Google Scholar 

  • Jacobson, M. D., Burne, J. F., King, M. P., Miyashita, T., Reed, J. C., and Raff, M. C. (1993). Nature 361, 365–369.

    PubMed  Google Scholar 

  • Jarvis, W. D., Kolesnick, R. N., Fornari, F. A., Traylor, R. S., Gewirtz, D. A., and Grant, S. (1994). Proc. Natl. Acad. Sci. USA 91, 73–77.

    PubMed  Google Scholar 

  • Jayadev, S., Lin, B., Bielawska, A. E., Lee, J. Y., Nazaire, F., Pushkareva, M. Y., Obeid, L. M., and Hannun, Y. A. (1995). J. Biol. Chem. 270, 2047–2052.

    PubMed  Google Scholar 

  • Kane, D. J., Sarafian, T. A., Anton, R., Hahn, H., Gralla, E. B., Valentine, J. S., Örd, T., and Bredesen, D. E. (1993). Science 262, 1274–1277.

    PubMed  Google Scholar 

  • Krajewski, S., Tanaka, S., Takayama, S., Schibler, M. J., Fenton, W., Reed, J. C. (1993). Cancer Res. 53, 4701–4714.

    PubMed  Google Scholar 

  • Larm, J. A., Vaillant, F., Linnane, A. W., and Lawen, A. (1994). J. Biol. Chem. 269, 30097–30100.

    PubMed  Google Scholar 

  • Leibowitz, R. D. (1971). J. Cell Biol. 51, 116–122.

    PubMed  Google Scholar 

  • Lithgow, T., van Driel, R., Bertram, J. F., and Strasser, A. (1994). Cell Growth Diff. 5, 411–417.

    PubMed  Google Scholar 

  • Martin, S. J., Obrein, G. A., Nishioka, W. K. Mcgahon, A. J., Mahboubi, A., Saido, T. C., and Green, D. R. (1995). J. Biol. Chem. 270, 6425–6428.

    PubMed  Google Scholar 

  • Marzuki, S., Noer, A. S., Lertrit, P., Uttanaphol, P., Thyagarajan, D., Kapsa, R., Sudoyo, H., and Byrne, E. (1991). In Progress in Neuropathology (Sato, T., and DiMauro, S., eds.), Raven Press, New York, Vol. 7, pp. 181–193.

    Google Scholar 

  • Matsura, T., Yamada, K., and Kawasaki, T. (1995). Redox Rep. 1, 343–347.

    Google Scholar 

  • Mizushima, N., Koike, R., Kohsaka, H., Kushi, Y., Handa, S., Yagita, H., and Miyasaka, N. (1996). FEBS Lett. 395, 267–271.

    PubMed  Google Scholar 

  • Monaghan, P., Robertson, D., Amos, A. S., Dyer, M. J. S., Mason, D. Y., and Greaves, M. F. (1992). J. Histochem. Cytochem. 40, 1819–1825.

    PubMed  Google Scholar 

  • Muschel, R. J., Bernhard, E. J., Garza, L., Mackenna, W. C., and Koch, C. J. (1995). Cancer Res. 55, 995–998.

    PubMed  Google Scholar 

  • Navarro, F., Villalba, J. M., Crane, F. L., Mackellar, W. C., and Navas, P. (1995). Biochem. Biophys. Res. Commun. 212, 138–143.

    PubMed  Google Scholar 

  • Obeid, L. M., Linardic, C.-M., Karolak, L. A., and Hannun, Y. A. (1993). Science 259, 1769–1771.

    PubMed  Google Scholar 

  • Preiss, J., Loomis, C. R., Bishop, W. R., Stein, R., Niedel, J. E., and Bell, R. M. (1986). J. Biol. Chem. 261, 8597–8600.

    PubMed  Google Scholar 

  • Raff, M. C. (1992). Nature. 356, 397–400.

    Article  PubMed  Google Scholar 

  • Reed, J. C. (1994). J. Cell Biol. 124, 1–6.

    Article  Google Scholar 

  • Sandstrom, P. A., Tebbey, P. W., Van Cleave, S., and Buttke, T. M. (1994). J. Biol. Chem. 269, 798–801.

    PubMed  Google Scholar 

  • Schulze-Osthoff, K., Kramer, P. H., and Döge, W. (1994). EMBO J. 13, 4587–4596.

    PubMed  Google Scholar 

  • Shimizu, S., Eguchi, Y., Kosaka, H., Kamiike, W., Matsuda, H., and Tsujimoto, Y. (1995). Nature 374, 811–813.

    PubMed  Google Scholar 

  • Slater, A. F. G., Stefan, C., Nobel, I., van den Dobbelsteen, D. J., and Orrenius, S. (1996). Cell. Death Diff. 3, 57–62.

    Google Scholar 

  • Smyth, M. J., Perry, D. K., Zhang, J. D., Poirier, G. G., Hannun, Y. A., and Obeid, L. M. (1996). Biochem. J. 316, 25–28.

    PubMed  Google Scholar 

  • Storrie, B., and Madden, E. A. (1990). Methods Ernymol. 182, 203–225.

    Google Scholar 

  • Sun, I. L., Sun, E. E., Crane, F. L., Morré, D. J., Lindgren, A., and Löw, H. (1992). Proc. Natl. Acad. Sci. USA 89, 11126–111130.

    PubMed  Google Scholar 

  • Sun, J. L., Sun, E. E., and Crane, F. L. (1995). Protoplasma. 184, 214–219.

    Google Scholar 

  • Tilly, J. L. and Tilly, K. I. (1995). Endocrinology 136, 242–252.

    PubMed  Google Scholar 

  • Vaux, D. L., and Strasser, A. (1996). Proc. Natl. Acad. Sci. USA 92, 8443–8447.

    Google Scholar 

  • Villalba, J. M, Navarro, F., Córdoba, F., Serrano, A., Arroyo, A., Crane, F. L., and Navas, P. (1995). Proc. Natl. Acad, Sci. USA. 92, 4887–4891.

    Google Scholar 

  • Villalba, J. M., Córdoba, F., and Navas, P. (1996). In Subcellular Biochemistry (Harris, J. R., ed.), Plenum Press, New York, Vol. 25, pp. 57–81.

    Google Scholar 

  • Weil, M., Jacobson, M. D., Coles, H. S. R., Davies, T. J., Gardner, R. L., Raff, K. D., and Raff, M. C. (1996). J. Cell. Biol. 133, 1053–1059.

    PubMed  Google Scholar 

  • Wolvetang, E. J., Larm, J. A., Montsoulas, P., and Lawen, A. (1996). Cell Growth Diff. 7, 1315–1325.

    PubMed  Google Scholar 

  • Zhang, J., Alter, N., Reed, J. C., Borner, C., Obeid, L. M., and Hanum, Y. A. (1996). Proc. Natl. Acad. Sci. USA 93, 5325–5328.

    PubMed  Google Scholar 

  • Zhong, L.-T., Sarafian, T., Kane, D. J., Charles, A. C., Mah, S. P., Edwards, R. H., and Bredesen, D. E. (1993). Proc. Natl. Acad. Sci. USA 90, 4533–4537.

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Departamento de Biología Celular, Facultad de Ciencias, Universidad de Córdoba, 14004, Córdoba, Spain

    María P. Barroso, Consuelo Gómez-Díaz, José M. Villalba, María I. Burón, Guillermo López-Lluch & Plácido Navas

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  1. María P. Barroso
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  2. Consuelo Gómez-Díaz
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  3. José M. Villalba
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  4. María I. Burón
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  5. Guillermo López-Lluch
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  6. Plácido Navas
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Barroso, M.P., Gómez-Díaz, C., Villalba, J.M. et al. Plasma Membrane Ubiquinone Controls Ceramide Production and Prevents Cell Death Induced by Serum Withdrawal. J Bioenerg Biomembr 29, 259–267 (1997). https://doi.org/10.1023/A:1022462111175

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