Abstract
Uncoupling proteins, a subgroup of the mitochondrial anion transporter superfamily, have beenidentified in prokaryotes, plants, and mammalian cells. Evolutionary conservation of thesemolecules reflects their importance as regulators of two critical mitochondrial functions, i.e.,ATP synthesis and the production of reactive oxygen species (ROS). Although the amino acidsequences of the three mammalian uncoupling proteins, UCP1, UCP2 and UCP3, are verysimilar, each homolog is the product of a unique gene and important differences have beendemonstrated in their tissue-specific expression and regulation. UCP1 and UCP3 appear to bekey regulators of energy expenditure, and hence, nonshivering thermogenesis, either in brownadipose tissue (UCP1) or skeletal muscle (UCP3). UCP2 is expressed more ubiquitously,although generally at low levels, in many tissues. There is conflicting evidence about itsimportance as a regulator of resting metabolic rate. However, evidence suggests that thishomolog might modulate the mitochondrial generation of ROS in some cell types, includingmacrophages and hepatocytes. While the induction of various uncoupling protein homologsprovides adaptive advantages, both to the organism (e.g., thermogenesis) and to individual cells(e.g., reduced ROS), increased uncoupling protein activity also increases cellular vulnerability tonecrosis by compromising the mitochondrial membrane potential. This narrow “risk—benefit”margin necessitates tight control of uncoupling protein activity in order to preserve cellularviability and much remains to be learned about the regulatory mechanisms involved.
REFERENCES
Akerman, P., Cote, P., Yang, S. Q., McClain, C., Nelson, S., Bagby, G. J., and Diehl, A. M. (1992). Amer. J. Physiol. 263, G579-G585.
Alvarez, R., DeAndres, J., Yubero, P., Vinas, O., Mampel, T., Iglesias, R., Giralt, J., and Villarroya, F. (1995). J. Biol. Chem. 270, 5666-5673.
Aquila, H., Link, T. A., and Klingenberg, M. (1987). FEBS Lett. 212, 1-9.
Bao, S., Kennedy, A., Wojciechowski, B., Wallace, P., Ganaway, E., and Garvey, W. T. (1998). Diabetes. 47, 1935-1940.
Bernadi, P., Basso, E., Colonna, R., Costantini, P., Di Lisa, F., Eriksson, O., Fontaine, E., Forte, M., Ichas, F., Massari, S., Nicolli, A., Petronilli, V., and Scorrano, L. (1998). Biochim Biophys Acta 1365, 200-206.
Bianco, A. C., and Silva, J. E. (1987). J. Clin. Invest. 79, 295-230.
Bianco, A. C., and Silva, J. E. (1988). Amer. J. Physiol. 328, 207-215.
Biengraeber, M., Echtay, K. S., and Klingenberg, M. (1998). Biochemistry 37, 3-8.
Boss, O., Samec, S., Dulloo, A., Seydoux, J., Muzzin, P., and Giacobino, J.-P. (1997a). FEBS Lett. 412, 111-114.
Boss, O., Samec, S., Paoloni-Giacobino, A., Rossier, C., Dulloo, A., J., S., Muzzin, P., and Giacobino, J.-P. (1997b). FEBS Lett. 408, 39-42.
Boss, O., Bobbioni-Harsch, E., Assimacopoulos-Jeannet, F., Muzzin, P., Munger, R., Giacobino, J.-P., and Golay, A. (1998a). Lancet. 351, 1933.
Boss, O., Muzzin, P., and Giacobino, J. P. (1998b). Eur. J. Endocrinol. 139, 1-9.
Boss, O., Samec, S., Desplanches, D., Mayet, M. H., Seydoux, J., Muzzin, P., and Giacobino, J. P. (1998c). FASEB J. 12, 335-339.
Boss, O., Samec, S., Kuhne, F., Bijlenga, P., Assimacopoulos-Jeannet, F., Seydoux, J., Giacobino, J. P., and Muzzin, P. (1998d). J. Biol. Chem. 273, 5-8.
Bouillaud, F., Arechaga, I., Petit, P. X., Raimbault, S., Levi-Meyrueis, C., Casteilla, L., Laurent, M., Rial, E., and Ricquier, D. (1994). EMBO J. 13, 1990-1997.
Bussquets, S., Sanchis, D., Alvarez, B., Ricquier, D., Lopez-Soriano, F.J., and Argiles, J. M. (1998). FEBS Lett. 440, 348-350.
Campfield, L. A., Smith, F. J., and Burn, P. (1996). Hormone Metab. Res. 28, 619-632.
Carmona, M. C., Valmaseda, A., Brun, S., Vinas, O., T., M., Iglesias, R., Giralt, M., and Villarroya, F. (1998). Biochem. Biophys. Res. Commun. 243, 224-228.
Carretero, M. V., Torres, L., Latasa, U., Garci-Treviajano, E. R., Prieto, J., Mato, J. M., and Avila, M. A. (1998). FEBS Lett. 439, 55-58.
Cassard-Doulcier, A. M., Gelly, C., Fox, N., Schrementi, J., Raimbault, S., Klaus, S., Forest, C., Bouillaud, F., and Ricquier, D. (1993). Mol. Endocrinol. 7, 497-506.
Cassard-Doulcier, A. M., Larose, M., Matamala, J. C., Champigny, O., Bouillaud, F., and Ricquier, D. (1994). J. Biol. Chem. 269, 24335-24342.
Casteilla, L., Blondel, O., Klaus, S., Raimbault, S., Diolez, P., Moreau, F., Bouillaud, F., and Ricquier, D. (1990). Proc. Natl. Acad. Sci. USA 87, 5124-5128.
Champigny, O., and Ricquier, D. (1990). J. Nutr. 120, 1730-1736.
Chavin, K., Yang, S. Q., Lin, H. Z., Chatham, J., Chacko, V. P., Hoek, J. B., Walajtyzs, Rode, E., Rashid, A., Chen, C.-H., Huang, C.-C., Lane, M. D., and Diehl, A. M. (1999). J. Biol. Chem., 274, 5692-5700.
Chen, J., Gokhale, M., Li, Y., Trush, M. A., and Yager, J. D. (1998). Carcinogenesis 19, 2187-2193.
Cortez-Pinto, H., Yang, S. Q., Lin, H. Z., Rashid, A., and Diehl, A. M. (1999). Gastroenterology 116, 1184-93.
Cortez-Pinto, H., Yang, S. Q., Lin, H. Z., Costa, S., Hwang, C.-S., Lane, M. D., Bagby, G., and Diehl, A. M. (1998). Biochem. Biophys. Res. Commun. 251, 313-319.
Emilsson, V., Summers, R. J., Hamilton, S., Liu, Y. L., and Cawthorne, M. A. (1998). Biochem. Biophys. Res. Commun. 252, 450-454.
Factor, V. M., Kiss, A., Woitach, J. T., Wirth, P. J., and Thorgeirsson, S. S. (1998). J. Biol. Chem. 273, 15846-15853.
Faggioni, R., Shigenaga, J., Moser, A., Feingold, K. R., and Grunfeld, C. (1998). Biochem. Biophys. Res. Commun. 244, 75-78.
Fleury, C., Neverova, M., Collins, S., Raimbault, S., Champigny, O., Levi-Meyrueis, C., Bouillaud, R., Seldin, M. F., Surwit, R. S., Ricquier, D., and Warden, C. H. (1997). Nature Genet. 15, 269-272.
Foellmi-Adams, L. A., Wyse, B. M., Herron, D., Nedergaard, J., and Kletzien, R. F. (1996). Biochem. Pharmacol. 52, 693-701.
Gainsford, T., Willson, T. A., Metcalf, D., Handman, E., McFarlane, C., Ng, A., Nicola, N. A., Alexander, W. S., and Hilton, D. J. (1996). Proc. Natl. Acad. Sci. USA 93, 14564-14568.
Giaraudo, S. Q., Kotz, C. M., Grace, M. K., Levine, A. S., and Billington, C. J. (1994). Amer. J. Physiol. 266, R1578-R1583.
Gimeno, R. E., Dembski, M., Weng, X., Deng, N., Shyjan, A. W., Gimeno, C. J., Iris, F., Ellis, S. J., Woolf, E. A., and Tartagli, L. A. (1997). Diabetes 46, 900-906.
Gong, D.-W., He, Y., Karas, M., and Reitman, M. (1997). J. Biol. Chem. 272, 24129-24132.
Grasl-Kraupp, B., Bursch, W., Ruttkay-Nedecky, B., Wagner, A., Lauer, B., and Schulte-Hermann, R. (1994). Proc. Natl. Acad. Sci. USA 91, 9995-9999.
Halestrap, A. P., and Davidson, A. M. (1990). Biochem. J. 268, 153-160.
Hardie, D. G., and Carling, D. (1997).Eur. J. Biochem. 246, 259-273.
Hodny, S., Kolarova, P., M., R., Horakova, M., Nibbelink, M., Penicaud, L., Casteilla, L., and Kopecky, J. (1998). FEBS Lett. 425, 185-190.
Jezek, P., Orosz, D. E., Modriansky, M., and Garlid, K. D. (1994). J. Biol. Chem. 269, 26184-26190.
Jezek, P., Modriansky, M., and Garlid, K. D. (1997). FEBS Lett. 408, 161-165.
Jezek, P., Engstova, H., Zackova, M., Vercesi, A. E., Costa, A. D., Arruda, P., and Garlid, K. D. (1998). Biochim. Biophys. Acta 1365, 319-327.
Kageyama, H., Suga, A., Kashiba, M., Oka, J., Osaka, T., Kashiwa, T., Hiraon, T., Nemoto, K., Namba, Y., Ricquier, D., Giacobino, J. P., and Inoue, S. (1998). FEBS Lett. 4, 450-453.
Kelley, L. J., Vacario, P. P., Thompson, G. C., Candelore, M. R., Doebber, T. W., Ventre, J., Wu, M. S., Meurer, R., Forrest, M. J., Conner, M. W., Cascieri, M. A., and Moller, D. E. (1998). Endocrinology 139, 4920-4927.
Kielar, D., Clark, J. S., Ciechanowicz, A., Kurzawski, G., Sulikowski, T., and Naruszewicz, M. (1998). Metabolism. 47, 844-847.
Klannemark, M., Orho, M., and Groop, L. (1998). Eur. J. Endocrinol. 139, 217-223.
Klaus, S., Ely, M., Encke, D., and Heldmaier, G. (1995). J. Cell. Sci. 108, 3171-3180.
Klaus, S., Munzberg, H., Truloff, C., and Heldmaier, G. (1998). Amer. J. Physiol. 274, R287-R293.
Klingenberg, M., Winkler, E., and Huang, S. (1995). Methods Enzymol. 260, 369-389.
Knott, R. M., Trayburn, P., and Hesketh, J. E. (1992). Brit. J. Nutr. 68, 583-592.
Komiya, T., et al.(1997). EMBO. J. 16, 4267-4275.
Kopecky, J., Clarke, G., Enerback, S., Spiegelman, B., and Kozak, L. P. (1995). J. Clin. Invest. 96, 2914-2923.
Korshunov, S. S., Korkina, O. V., Ruuge, E. K., Skulachev, V. P., and Starkov, A. A. (1998). FEBS Lett. 435, 215-218.
Kowaltowski, A. J., Costa, A. D., and Vercesi, A. E. (1998). FEBS Lett. 425, 213-216.
Kozak, L. P., Britton, J. H., Kozak, U. C., and Wells, J. M. (1988). J. Biol. Chem. 263, 12274-12277.
Kren, B. T., Trembley, J. H., Krarewski, S., Behrens, T. W., Reed, J. C., and Steer, C. J. (1996). Cell Growth Diff. 7, 1633-1642.
Kroemer, G., Dallaporta, B., and Resche-Rignon, M. (1998). Annu. Rev. Physiol. 60, 619-642.
Kubota, T., Mori, H., Tamori, U., Okazawa, H., Kukuda, T., Midi, M., Ito, C., Fleury, C., Bouillaud, F., and Kasuga, M. (1998). J. Clin. Endocrinol Metab. 83, 2800-2804.
Kushi, A., Sasai, H., Koizumi, H., Takeda, N., Yodoyama, M., and Nakamura, M. (1998). Proc. Natl. Acad. Sci. USA 95, 15659-15664.
Kutoh, E., Boss, O., Levasseur, F., and Giacobino, J. P. (1998). Life Sci. 62, 445-451.
Lanni, A., DeFelice, M., Lombardi, A., Moreno, M., Fleury, C., Ricquier, D., and Goglia, P. (1997). FEBS Lett. 418, 171-174.
Larkin, S., Mull, E., Miao, W., Pittner, R., Albrandt, K., Moore, C., Young, A., Denaro, M., and Beaumont, K. (1997). Biochem. Biophys. Res. Commun. 240, 222-227.
Larrouy, D., Laharrague, P., Carrera, G., Viguerie-Bascands, N., Levi-Meyrueis, C., Pecqeur, C., Nibbelink, M., Andre, M., Casteilla, L., and Ricquier, D. (1997). Biochem. Biophys. Res. Commun. 235, 760-764.
Lee, F.-Y., Li, Y., Yang, E. K., Yang, S. Q., Lin, H. Z., Trush, M. A., Dannenberg, A. J., and Diehl, A. M. (1999). Amer. J. Physiol: Cell Physiol. 276, C386-C394.
Lee, F. Y. J., Li, Y., Yang, S. Q., Trush, M., and Diehl, A. M. (1999). Hepatology, 29, 677-687.
Lemasters, J. J. (1998). Gastroenterology 115, 783-786.
Levine, J. A., Eberhardt, N. L., and Jensen, M. D. (1999). Science 283, 212-214.
Liu, Q., Solanes, G., Vidal-Puig, A., Grujic, D., Flier, J. S., and Lowell, B. B. (1997). J. Biol. Chem. 2720, 25433-25436.
Liu, Q., Bai, C., Chen, F., Wang, R., MacDonald, T., Gu, M., Zhang, Q., Morsy, M. A., and Caskey, C. T. (1998). Gene 207, 1-7.
Loffreda, S., Yang, S. Q., Lin, H. Z., Bulkley, G., Bregman, M., Nobel, P., and Diehl, A. M. (1998). FASEB J. 12, 57-65.
Marzo, I., Brenner, C., Zamzami, N., Susin, S. A., Beutner, G., Brdiczka, D., Remy, R., Xie, Z. H., Reed, J. C., and Kroemer, G. (1998a). J. Exp. Med. 187, 1261-1271.
Marzo, I., Brenner, C., Zamzami, N., Jurgensmeier, J. M., Susin, S. A., Vierira, H. L. A., Prevost, M.-C., Xie, Z., Matsuyama, S., Reed, J. C., and Kroemer, G. (1998b). Science 281, 2027-2031.
Masaki, T., Yoshimatsa, H., Kakuma, T., Hidaka, S., Kurokawa, M., and Sakata, T. (1997). FEBS Lett. 418, 323-326.
Matamala, J. C., Gianotti, M., Pericas, J., Quevedo, S., Roca, P., Palou, A., and Garcia-Palmer, F. J. (1996). Biochem. J. 319, 529-534.
Matsuda, J., Hosoda, K., Itoh, H., Son, C., Doi, K., Tanaka, T., Fukunaga, Y., Inoe, G., Nishimura, H., Yoshimasa, Y., Yamori, Y., and Nakao, K. (1997). FEBS Lett. 418, 200-204.
Matsuda, J., Hosoda, K., Itoh, H., Son, C., Doi, K., Hanaoka, I., Inoe, G., Nishimura, H., Yoshimasa, Y., Yamori, Y., Odaka, H., and Nakao, K. (1998). Diabetes 47, 1809-1914.
Merrick, B. A., He, C., Witcher, L. L., Patterson, R. M., Reid, J. J., Pence-Pawlowski, P. M., and Selkirk, J. K. (1996). Biochim. Biophys. Acta 1297, 57-68.
Mignotte, B., and Vayssiere, J. L. (1998). Eur. J. Biochem. 252, 1-15.
Millet, L., Vidal, H., Andreelli, F., Larrouy, D., Riou, J. P., Ricquier, D., Laville, M., and Langin, D. (1997). J. Clin. Invest. 100, 2665-2670.
Millet, L., Vidal, H., Larrouy, D., Andreelli, F., Lavill, M., and Langin, D. (1998). Diabetologia 41, 829-832.
Modriansky, M., Murdza-Inglis, D. L., Patel, H. V., Freeman, K., and Garlid, K. D. (1997). J. Biol. Chem. 272, 24759-24762.
Moriscot, A., Rabcio, R., and Bianco, A. C. (1993). Amer. J. Physiol. 265, E81-E87.
Mory, G., Bouillaud, F., Combes-George, M., and Ricquier, D. (1984). FEBS Lett. 166, 393-396.
Muzzin, P., Revelli, J. P., Ricquier, D., Meier, M. K., Assimacoupoulos-Jeannet, F., and Giacobino, J. P. (1989). Biochem. J. 261, 721-721.
Narita, M., Shimizu, S., Ito, T., Chittenden, T., Lutz, R. J., Matusuda, H., and Tsujimoto, Y. (1998). Proc. Natl. Acad. Sci. USA 95, 14681-14686.
Negre-Salvayre, A., Hirtz, C., Carrera, G., Cazenave, R., Troly, M., Salvayre, R., Penicaud, L., and Casteilla, L. (1997). FASEB J. 11, 809-815.
Nicholls, D. G., and Ferguson, S. J. (1992). Bioenergetics: An Introduction to the Chemiosmotic Theory(2nd ed.), Academic Press, New York.
Nordfors, L., Hoffstedt, J., Nyberg, C., Thorne, A., Arner, P., Schalling, M., and Lonnqvist, F. (1998). Diabetologia 41, 935-939.
Oberkofler, H., Liu, Y. M., Esterbauer, H., Hell, E., Drempler, F., and Patsch, W. (1998). Diabetologia 41, 940-946.
Obregon, M. J., Pitamber, R., Jacobsson, A., Nedergaard, J., and Cannon, B. (1987). Biochem. Biophys. Res. Commun. 148, 9-14.
Pastorino, J. G., Chen, S.-T., Tafani, M., Snyder, J. W., and Farber, J. L. (1998). J. Biol. Chem. 273, 7770-7775.
Paulik, M. A., Buckholz, R. G., Lancaster, M. E., Dallas, W. S., Hull-Ryde, E. A., Weiel, J. E., and Lenhand, J. M. (1998). Pharmacol. Res. 15, 944-999.
Polla, B. S., Kantengwa, S., Francois, D., Salvioli, S., Franceschi, C., Marsac, C., and Cossarizza, A. (1996). Proc. Natl. Acad. Sci. USA 93, 6458-6463.
Puigserver, P., Vazquez, P., Bonet, M. I., Pico, C., and Palou, A. (1996). Biochem. J. 317, 827-833.
Rashid, A., Wu, T.-C., Huang, C.-H., Chen, H.Z., Lin, H.Z., Yang, S.Q., Lee, F.Y.J., and Diehl, A. M. (1999). Hepatology 29, 1131-1138.
Rehnmark, S., Nechad, M., Herron, D., B., C., and Nedergaard, J. (1990). J. Biol. Chem. 265, 16464-16471.
Ricart, J., Egea, G., Izquierdo, J. M., San Martin, C., and Cuezva, J. M. (1997). Biochem. J. 324, 635-643.
Ricquier, D. (1998). Biochem. Soc. Trans. 26, 120-123.
Ricquier, D., Bouillaud, F., Toumelin, P., Mory, G., Bazin, R., J., A., and Penicaud, L.(1986). J. Biol. Chem. 261, 13905-13910.
Samec, S., Seydoux, J., and Dulloo, A. G. (1998). FASEB J. 12, 715-724.
Sanchis, D., Busquets, S., Ivarez, B., Ricquier, D., Lopez-Soriano, F. J.,and Argiles, J. M. (1998). FEBS Lett. 436, 415-418.
Scarpace, P. J., and Matheny, M. (1998). Amer. J. Physiol. 275,E259-E264.
Schleiff, E., and Turnbull, J. L. (1998). Biochemistry 37,13043-13051.
Shimabukaro, M., Zhou, Y. t., Lee, Y., and Unger, R. H. (1997). Biochem. Biophys. Res. Commun. 237, 359-361.
Shimizu, S., Eguchi, Y., Kamiike, W., Funahashi, Y., Mignon, A., Lacronique, V., Matsuda, H., and Tsujimoto, Y. (1998). Proc. Natl. Acad. Sci. USA 95,1455-1459.
Shimokawa, T., Kato, M., Watanabe, Y., Hirayama, R., Kurosaki, E., Shikama, H., and Hashimoto, S. (1998). Bhichem. Biophys. Res. Commun. 25, 374-378.
Siegrist-Kaiser, C. A., Pauli, V., Juge-Aubry, C. E., Boss, O., Pernin, A., Chin, W. W., Cusin, I., Rohner-Jeanrenaud, F., Burger, A. G., Zapf, J., and Meier, C. A. (1997). J. Clin. Invest. 100, 2858-2864.
Silva, J. E., and Rabelo, R. (1997). Eur. J. Endocrinol. 136, 251-164.
Simoneau, J. A., Kelley, D. E., Neverova, M., and Warden, C. H. (1998).FASEB J. 12, 1739-1745.
Simonyan, R. A., and Skulachev, V. P. (1998). FEBS Lett. 436, 81-84.
Skulachev, V. P. (1994). Biochemistry 59, 1433-1434.
Skulachev, V. P. (1995). Mol. Biol. 29, 709-715.
Skulachev, V. P. (1996a). FEBS Lett. 397, 7-10.
Skulachev, V. P. (1996b). Quart. Rev. Biophys. 29, 169-202.
Skulachev, V. P. (1997). Biosci. Rept. 17, 347-366.
Stadler, J., Bentz, B. C., Harbrecht, B. G., Di silvio, M., Curran, R. D., Billiar, T. R., Hoffman, R. A., and Simmons, R. L. (1992). Ann. Surg. 216, 539-546.
Strack, A. M., Bradbury, M. J., and Dallman, M. F. (1995a). Amer. J. Physiol. 268, R183-R191.
Strack, A. M., Horsley, C. J., Sebastian, R. J., Akana, S. F., and Dallman, M. F. (1995b). Amer. J. Physiol. 268, R1209-R1216.
Strobel, A., Combettes-Souverain, M., Doare, L., Strosberg, A. D., and Issad, R. (1998).Interm. J. Obesity Related Metab Disorders 22, 1121-1126.
Stucki, J. W. (1980). Eur. J. Biochem. 109, 269-283.
Takayama, S., Krajewski, S., Krajewska, M., Kiada, S., Zapata, J. M., Kochel, K., Knee, D., Scudiero, D., Tudor, G., Miller, G. J., Miyashita, T., Yamada, M., and Reed, J. C. (1998). Cancer Res. 58, 116-131.
Tartaglia, L. A., Dembski, M., Weng, X., Deng, N., Culpepper, J., Devos, R., Rchards, G. J., Campfield, L. A., Clark, F. T., Deeds, J., et al.(1995).Cell 83(7), 1263-1271.
Teruel, T., Valverde, A. M., Navarro, P., Benito, M., and Lorenzo, M. (1998). J. Cell Physiol. 176, 99-109.
Tsuboyama-Kasaoka, N., Tsunoda, N., Maruyama, K., Takahashi, M., Kim, H., Ikemoto, S., and Ezaki, O. (1998). Biochem. Biophys. Res. Commun. 274, 498-503.
Urhammer, S. A., Dalgaard, L. T., Sorensen, T. I., Tybjaerg-Hanse, A., Echwald, S. M., Andersen, T., Clausen, J. O., and Pedersen, O. (1998). Diabetologia 41, 241-244.
Walder, K., Norman, R. A., Hanson, R. L., Schrauwen, P., Neverova, M., Jenkinson, C. P., Easlick, J., Warden, C. H., Pecqueur, C., Raimbault, S., Ricquier, D., Silver, M. H. K., Shuldiner, A. R., Solanes, G., Lowell, B. B., Chung, W. K., Leibel, R. L., Pratley, R., and Ravussin, E. (1998). Human Mol. Genet. 7, 1431-1435.
Wiegle, D. S., Selfridge, L. I., Schwartz, M. W., Seeley, R. J., Cummings, D. E., Havel, P. J., Kuijper, J. L., and BeltrandelRio, H. (1998). Diabetes 47, 298-302.
Wiesinger, H., Klaus, S., Heldmaier, G., Champigny, O., and Ricquier, D. (1990). Can. J. Physiol. Pharmacol. 68, 195-200.
Winkler, E., Wachler, E., and Klingenberg, M. (1997). Biochemistry 36,148-155.
Wojtczak, L., and Schonfeld, P., (1993). Biochim. Biophys. Acta 1183, 41-57.
Yamada, M., Hashida, T., Shibusawa, N., Iwasaki, T., Murakami, M., Monden, T., Satoh, T., and Mori, M. (1998). FEBS Lett. 432, 65-69.
Yoshitomi, H., Yamazaki, K., Abe, S., and Tanaka, I. (1998). Biochem. Biophys. Res. Commun. 253, 85-91.
Yubero, P., Barbera, M. J., Alvarez, R., Vinal, O., Mampel, T., Iglesias, R., Villarroya, F.,and Giralt, M. (1998). Mol. Endocrinol. 12, 1023-1037.
Zhou, Y. T., Shimabukuro, M., Koyama, K., Lee, Y., Wang, M. Y., Trieu, F., Newgard, C. B., and Unger, R. H. (1997). Proc. Natl. Acad. Sci. USA 94,6386-6390.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Diehl, A.M., Hoek, J.B. Mitochondrial Uncoupling: Role of Uncoupling Protein Anion Carriers and Relationship to Thermogenesis and Weight Control “The Benefits of Losing Control”. J Bioenerg Biomembr 31, 493–506 (1999). https://doi.org/10.1023/A:1005452624640
Issue Date:
DOI: https://doi.org/10.1023/A:1005452624640