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Effectors of the mammalian plasma membrane NADH-oxidoreductase system. Short-chain ubiquinone analogues as potent stimulators

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Abstract

In the presence of effectors variations in the two recognized activities of the plasma membrane NADH-oxidoreductase system were studied in separate, specificin vitro assays. We report here that ubiquinone analogues that contain a short, less hydrophobic side chain than coenzyme Q-10 dramatically stimulate the NADH-oxidase activity of isolated rat liver plasma membranes whereas they show no effect on the reductase activity of isolated membranes. If measured in assays of the NADH∶ferricyanide reductase of living cultured cells these compounds have only a limited effect; the oxidase activity of whole cells is not measurable in our hands. We have furthermore identified selective inhibitors of both enzyme activities. In particular, the NADH-oxidase activity can be significantly inhibited by structural analogues of ubiquinone, such as capsaicin and resiniferatoxin. The NADH∶ferricyanide reductase, on the other hand, is particularly sensitive to pCMBS, indicating the presence of a sulfhydryl group or groups at its active site. The identification of these specific effectors of the different enzyme activities of the PMOR yields further insights into the function of this system.

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Abbreviations

DCIP:

2,6-dichlorophenol-indophenol

DTNB:

5,5′-dithio-bis(2-nitrobenzoic acid)

FAC:

ferric ammonium citrate

pCMBS:

p-chloromercuriphenylsulfonic acid

PMOR:

plasma membrane NADH-oxidoreductase

coenzyme Q-0:

2,3-dimethoxy-5-methyl-1,4-benzoquinone

SH:

sulfhydryl group

References

  • Afanas'ev, I. B., Korkina, L. G., Suslova, T. B., and Soodaeva, S. K. (1990).Arch. Biochem. Biophys. 281, 245–250.

    PubMed  Google Scholar 

  • Aledort, L. M., Troup, S. B., and Weed, R. I. (1968).Blood 31, 471–479.

    PubMed  Google Scholar 

  • Beaufay, H., Amar-Costesec, A., Feytmans, E., Thinès-Sempoux, D., Wibo, M., Robbi, M., and Berthet, J. (1974).J. Cell Biol. 61, 188–200.

    Google Scholar 

  • Bérczi, A., Sizensky, J. A., Crane, F. L., and Faulk, W. P. (1991).Biochim. Biophys. Acta 1073, 562–570.

    PubMed  Google Scholar 

  • Bradford, M. M. (1976).Anal. Biochem. 72, 248–254.

    PubMed  Google Scholar 

  • Brandt, U., and Trumpower, B. (1994).Crit. Rev. Biochem. Mol. Biol. 29, 165–197.

    PubMed  Google Scholar 

  • Braun, B. S., Benbow, U., Lloyd-Williams, P., Bruce, J. M., and Dutton, P. L. (1986).Methods Enzymol. 125, 119–129.

    PubMed  Google Scholar 

  • Brightman, A. O., Wang, J., Miu, R. K.-m., Sun, I. L., Barr, R., Crane, F. L., and Morré, D. J. (1992).Biochim. Biophys. Acta 1105, 109–117.

    PubMed  Google Scholar 

  • Clark, M. G., Partick, E. J., Patten, G. S., Crane, F. L., Löw, H., and Grebing, C. (1981).Biochem. J. 200, 565–572.

    PubMed  Google Scholar 

  • Crane, F. L., Roberts, H., Linnane, A. W., and Löw, H. (1982).J. Bioenerg. Biomembr. 14, 191–205.

    PubMed  Google Scholar 

  • Crane, F. L., Sun, I. L., Clark, M. G., Grebing, C., and Löw, H. (1985).Biochim. Biophys. Acta 811, 233–264.

    PubMed  Google Scholar 

  • Crane, F. L., Sun, I. L., Barr, R., and Löw, H. (1991).J. Bioenerg. Biomembr. 23, 773–803.

    PubMed  Google Scholar 

  • Crane, F. L., Sun, I. L., and Sun, E. E. (1993).Clin. Invest. 71, S55-S59.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Ellem, K. A. O., and Kay, G. F. (1983).Biochem. Biophys. Res. Commun. 112, 183–190.

    PubMed  Google Scholar 

  • Goldenberg, H., Crane, F. L., and Morré, D. J. (1979).J. Biol. Chem. 254, 2491–2498.

    PubMed  Google Scholar 

  • Hochstein, P. (1983).Fundam. Appl. Toxicol. 3, 215–217.

    PubMed  Google Scholar 

  • Inman, R. S., and Wessling-Resnick, M. (1993).J. Biol. Chem. 268, 8521–8528.

    PubMed  Google Scholar 

  • King, M. P., and Attardi, G. (1989).Science 246, 500–503.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Larm, J. A., Wolvetang, E. J., Vaillant, F., Martinus, R. D., Lawen, A., and Linnane, A. W. (1995).Protoplasma 184, 173–180.

    Google Scholar 

  • Lawen, A., Martinus, R. D., McMullen, G. L., Nagley, P., Vaillant, F., Wolvetang, E. J., and Linnane, A. W. (1994).Mol. Aspects Med. 15, s13-s27.

    PubMed  Google Scholar 

  • Lenaz, G., Pasquali, P., Bertoli, E., and Parenti-Castelli, G. (1975).Arch. Biochem. Biophys. 169, 217–226.

    PubMed  Google Scholar 

  • Löw, H., Grebing, C., Lindgren, A., Tally, M., Sun, I. L., and Crane, F. L. (1987).J. Bioenerg. Biomembr. 19, 535–549.

    PubMed  Google Scholar 

  • Luft, R. (1994).Proc. Natl. Acad. Sci. USA 91, 8731–8738.

    PubMed  Google Scholar 

  • Mahler, H. R. (1955).Methods Enzymol. 2, 688–693.

    Google Scholar 

  • Martinus, R. D., Linnane, A. W., and Nagley, P. (1993).Biochem. Mol. Biol. Int. 31, 997–1005.

    PubMed  Google Scholar 

  • Morré, D. J., and Brightman, A. O. (1991).J. Bioenerg. Biomembr. 23, 469–489.

    PubMed  Google Scholar 

  • Morré, D. J., and Morré, D. M. (1989).BioTechniques 7, 946–958.

    PubMed  Google Scholar 

  • Nagley, P., Zhang, C., Martinus, R. D., Vaillant, F., and Linnane, A. W. (1993). InMitochondrial DNA in Human Pathology (DiMauro, S., and Wallace, D. C., eds.), Raven Press, New York, pp. 137–157.

    Google Scholar 

  • Naruta, Y. (1980).J. Am. Chem. Soc. 102, 3774–3783.

    Google Scholar 

  • Navas, P., Estévez, A., Burón, M. I., Villalba, J. M., and Crane, F. L. (1988).Biochem. Biophys. Res. Commun. 154, 1029–1033.

    PubMed  Google Scholar 

  • Navas, P., Nowack, D. D., and Morré, D. J. (1989).Cancer Res. 49, 2147–2156.

    PubMed  Google Scholar 

  • Nishinaka, Y., Aramaki, Y., Yoshida, H., Masuya, H., Sugawara, T., and Ichimori, Y. (1993).Biochem. Biophys. Res. Commun. 193, 554–559.

    PubMed  Google Scholar 

  • Nyormoi, O., Klein, G., Adams, A., and Dombos, L. (1973).Int. J. Cancer 12, 396–408.

    PubMed  Google Scholar 

  • Sottocasa, G. L., Kuylenstierna, B., Ernster, L., and Bergstrand, A. (1967).J. Cell Biol. 32, 415–438.

    PubMed  Google Scholar 

  • Sun, I. L., Toole-Simms, W., Crane, F. L., Golub, E. S., Díaz de Pagán, T., Morré, D. J., and Löw, H. (1987).Biochem. Biophys. Res. Commun. 146, 976–982.

    PubMed  Google Scholar 

  • Sun, I. L., Crane, F. L., Grebing, C., and Löw, H. (1984a).J. Bioenerg. Biomembr. 16, 583–595.

    PubMed  Google Scholar 

  • Sun, I. L., Crane, F. L., Löw, H., and Grebing, C. (1984b).J. Bioenerg. Biomembr. 16, 209–221.

    PubMed  Google Scholar 

  • Sun, I. L., Sun, E. E., and Crane, F. L. (1992a).Biochem. Biophys. Res. Commun. 189, 8–13.

    PubMed  Google Scholar 

  • Sun, I. L., Sun, E. E., Crane, F. L., Morré, D. J., Lindgren, A., and Löw, H. (1992b).Proc. Natl. Acad. Sci. USA 89, 11126–11130.

    PubMed  Google Scholar 

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

    Google Scholar 

  • Vaillant, F., and Nagley, P. (1995).Hum. Mol. Genet. 4, 903–914.

    PubMed  Google Scholar 

  • Vaillant, F., Loveland, B. E., Nagley, P., and Linnane, A. W. (1991).Biochem. Int. 23, 571–580.

    PubMed  Google Scholar 

  • van Iwaarden, P. R., Driessen, A. J. M., and Konings, W. N. (1992).Biochim. Biophys. Acta 1113, 161–170.

    PubMed  Google Scholar 

  • VanSteveninck, J., Weed, R. I., and Rothstein, A. (1965).J. Gen. Physiol. 48, 617–632.

    PubMed  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.

    PubMed  Google Scholar 

  • Wan, Y.-R, Williams, R. H., Folkers, K., Leung, K. H., and Racker, E. (1975).Biochem. Biophys. Res. Commun. 63, 11–15.

    PubMed  Google Scholar 

  • Wanders, R. J. A., Kos, M., Roest, B., Meijer, A. J., Schrakamp, G., Heymans, H. S. A., Tegelaers, W. H. H., van den Bosch, H., Schutgens, R. B. H., and Tager, J. M. (1984).Biochem. Biophys. Res. Commun. 123, 1054–1061.

    PubMed  Google Scholar 

  • Wolvetang, E. J., Johnson, K. L., Krauer, K., Ralph, S. J., and Linnane, A. W. (1994).FEBS Lett. 339, 40–44.

    PubMed  Google Scholar 

  • Wolvetang, E. J., Larm, J. A., Mousoulas, P. and Lawen, A. (1996).Cell Growth Differ. 7, in press.

  • Wróblewski, F., and LaDue, J. S. (1955).Proc. Soc. Exp. Biol. Med. 90, 210–213.

    PubMed  Google Scholar 

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Vaillant, F., Larm, J.A., McMullen, G.L. et al. Effectors of the mammalian plasma membrane NADH-oxidoreductase system. Short-chain ubiquinone analogues as potent stimulators. J Bioenerg Biomembr 28, 531–540 (1996). https://doi.org/10.1007/BF02110443

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