Redox state of endogenous coenzyme q modulates the inhibition of linoleic acid-induced uncoupling by guanosine triphosphate in isolated skeletal muscle mitochondria.
[en] The skeletal muscle mitochondria contain two isoforms of uncoupling protein, UCP2 and mainly UCP3, which had been shown to be activated by free fatty acids and inhibited by purine nucleotides in reconstituted systems. On the contrary in isolated mitochondria, the protonophoretic action of muscle UCPs had failed to be demonstrated in the absence of superoxide production. We showed here for the first time that muscle UCPs were activated in state 3 respiration by linoleic acid and dissipated energy from oxidative phosphorylation by decreasing the ADP/O ratio. The efficiency of UCPs in mitochondrial uncoupling increased when the state 3 respiratory rate decreased. The inhibition of the linoleic acid-induced uncoupling by a purine nucleotide (GTP), was not observed in state 4 respiration, in uninhibited state 3 respiration, as well as in state 3 respiration inhibited by complex III inhibitors. On the contrary, the progressive inhibition of state 3 respiration by n -butyl malonate, which inhibits the uptake of succinate, led to a full inhibitory effect of GTP. Therefore, as the inhibitory effect of GTP was observed only when the reduced state of coenzyme Q was decreased, we propose that the coenzyme Q redox state could be a metabolic sensor that modulates the purine nucleotide inhibition of FFA-activated UCPs in muscle mitochondria.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Jarmuszkiewicz, Wieslawa
Navet, Rachel
Alberici, L.
Douette, P.
Sluse-Goffart, Claudine
Sluse, Francis ; Université de Liège - ULiège > Département des sciences de la vie > Bioénergétique et physiologie cellulaire
Vercesi, A.
Language :
English
Title :
Redox state of endogenous coenzyme q modulates the inhibition of linoleic acid-induced uncoupling by guanosine triphosphate in isolated skeletal muscle mitochondria.
Publication date :
2004
Journal title :
Journal of Bioenergetics and Biomembranes
ISSN :
0145-479X
eISSN :
1573-6881
Publisher :
Kluwer Academic/Plenum Publishers, New York, United States - New York
Almeida, A. M., Jarmuszkiewicz, W., Khomsi, H., Arruda, P., Vercesi, A. E., and Sluse, F. E. (1999). Plant Physiol. 119, 1323-1330.
Andreyev, A. Y., Bondareva, T. O., Dedukhova, V. I., Mokhova, E. N., Skulachev, V. P., Tsofina, L. M., Volkov, N. I., and Vygodina, T. V. (1989). Eur. J. Biochem. 182, 585-592.
Argyropoulos, G., and Harper, M. E. (2002). J. Appl. Physiol. 92, 2187-2198.
Boss, O., Samec, S., Paoloni-Giacobino, A., Rossier, C., Dulloo, A., Seydoux, J., Muzzin, P., and Giacobino, J.-P. (1997). FEBS Lett. 408, 39-42.
Echtay, K. S., and Brand, M. D. (2001). Biochem. Soc. Trans. 29, 763-768.
Echtay, K. S., Roussel, D., St.-Pierre, J., Jekabsons, M. B., Cadenas, S., Stuart, J. A., Harper, J. A., Roubuck, S. J., Morrison, A., Pickering, S., Clapham, J. C., and Brand, M. D. (2002). Nature 415, 96-99.
Echtay, K. S., Winkler, E., Frischmuth, K., and Klingenberg, M. (2001). Proc. Natl. Acad. Sci. 98, 1416-1421.
Echtay, K. S., Winkler, E., and Klingenberg, M. (2000). Nature 408, 609-613.
Esteves, T. C., Echtay, K. S., Jonassen, T., Clarke, C. F., and Brand, M. D. (2004). Biochem. J. 379, 309-315.
Fleury, C., Neverova, M., Collins, S., Raimbault, S., Champigny, O., Levi-Meyrueis, C., Boillaud, F., Seldin, M. F., Surwit, R. S., Ricquier, D., and Warden, C. H. (1997). Nat. Genet. 15, 269-272.
Gornall, A. G., Bradawill, C. J., and David, M. M. (1949). J. Biol. Chem. 177, 751-766.
Huang, S.-G., Lin, Q.-S., and Klingenberg, M. (1998). J. Biol. Chem. 273, 859-864.
Jaburek, M., and Garlid, K. D. (2003). J. Biol. Chem. 278, 25825-25831.
Jaburek, M., Varecha, M., Gimeno, R. E., Dembski, M., Jeẑek, P., Zhang, M., Burn, P., Tartaglia, L. A., and Garlid, K. D. (1999). J. Biol. Chem. 274, 26003-26007.
Jarmuszkiewicz, W., Almeida, A. M., Sluse-Goffart, C. M., Sluse, F. E., and Vercesi, A. E. (1998a). J. Biol. Chem. 273, 34882-34886.
Jarmuszkiewicz, W., Almeida, A. M., Vercesi, A. E., Sluse, F. E., and Sluse-Goffart, C. M. (2000a). J. Biol. Chem. 275, 13315-13320.
Jarmuszkiewicz, W., Antos, N., Swida, A., Czarna, M., and Sluse, F. E. (2004). FEBS Lett. 569, 178-184.
Jarmuszkiewicz, W., Behrendt, M., Navet, R., and Sluse, F. E. (2002a). FEBS Lett. 532, 459-464.
Jarmuszkiewicz, W., Hryniewiecka, L., and Sluse, F. E. (2002b). J. Bioenerg. Biomembr. 34, 221-226.
Jarmuszkiewicz, W., Milani, G., Fortes, F., Schreiber, A. Z., Sluse, F. E., and Vercesi, A. E. (2000b). FEBS Lett. 467, 145-149.
Jarmuszkiewicz, W., Sluse-Goffart, C. M., Hryniewiecka, L., Michejda, J., and Sluse, F. E. (1998b). J. Biol Chem. 273, 10174-10180.
Jarmuszkiewicz, W., Sluse-Goffart, C. M., Hryniewiecka, L., and Sluse, F. E. (1999). J. Biol. Chem. 274, 23198-23202.
Jarmuszkiewicz, W., Sluse-Goffart, C. M., Vercesi, A. E., and Sluse, F. E. (2001). Biosci. Rep. 21, 213-221.
Jekabsons, M. B., Echtay, K. S., Brand, M. D. (2002). Biochem. J. 366, 565-571.
Jekabsons, M. B., and Horwitz, B. A. (2001). Biochim. Biophys. Acta 1503, 314-328.
Ježek, P. (2002). Int. J. Biochem. Cell Biol. 34, 1190-1206.
Ježek, P., Costa, A. D., and Vercesi, A. E. (1997). J. Biol. Chem. 272, 24272-24278.
Kamo, N., Muratsugu, M., Hongoh, R., and Kobatake, Y. (1979). J. Membr. Biol. 49, 105-121.
Klingenberg, M., and Echtay, K. S. (2001). Biochim. Biophys. Acta 1504, 128-143.
Laloi, M., Klein, M., Riesmeier, J. W., Müller-Röber, B., Fleury, C., Bouillaud, F., and Ricquier, D. (1997). Nature 389, 135-136.
Mao, W. G., Yu, X. X., Zhong, A., Li, W. L., Brush, J., Sherwood, S. W., Adams, S. H., and Pan, G. (1999). FEBS Lett. 443, 326-330.
McKee, E. E., Bentley, A. T., Smith, R. M., Jr., Kraas, J. R., and Ciaccio, C. E. (2000). Am. J. Physiol. Cell Physiol. 279, 1870-1879.
Nicholls, D. G., and Rial, E. A. (1999). J. Bioenerg. Biomembr. 31, 399-406.
Samartsev, V. N., Mokhova, E. N., and Skulachev, V. P. (2000). FEBS Lett. 412, 179-182.
Sanchis, D., Fleury, C., Chomiki, N., Goubern, M., Huang, Q. L., Neverova, M., Gregoire, F., Easlick, J., Raimbault, S., Levi-Meyrueis, C., Miroux, B., Collins, S., Seldin, M., Richard, D., Warden, C., Bouillaud, F., and Ricquier, D. (1998). J. Biol. Chem. 273, 34611-34615.
Skulachev, V. P. (1998). Biochim. Biophys. Acta 1363, 100-124.
Sluse, F. E., and Jarmuszkiewicz, W. (2002). FEBS Lett. 510, 117-120.
Talbot, D. A., Lambert, A. J., and Brand, M. D. (2004). FEBS Lett. 556, 111-115.
Tonkonogi, M., and Salhin, K. (1997). Acta Physiol. Scand. 161, 345-353.
Van den Bergen, C. W., Wagner, A. M., Krab, K., and Moore, A. L. (1994). Eur. J. Biochem. 226, 1071-1078.
Vercesi, A. E., Martins, I. S., Silva, M. A. P., Leite, H. M. F., Cuccovia, I. M., and Chamovich, H. (1995). Nature 375, 24.
Vidal-Puig, A., Solanes, G., Grujic, D., Flier, J. S., and Lowell, B. B. (1997). Biochem. Biophys. Res. Commun. 235, 79-82.
Wieckowski, M. R., and Wojtczak, L. (1997). Biochem. Biophys. Res. Commun. 232, 414-117.
Žácková, M., Kramer, R., and Ježek, P. (2000). Int. J. Biochem. Cell Biol. 32, 499-508.
Žácková, M., Škobisová, E., Urbánková, E., and Ježek, P. (2003). J. Biol. Chem. 278, 20761-20769.
