Artículos de revistas
Plant Uncoupling Mitochondrial Protein And Alternative Oxidase: Energy Metabolism And Stress
Registration in:
Bioscience Reports. , v. 25, n. 3-4, p. 271 - 286, 2005.
1448463
10.1007/s10540-005-2889-2
2-s2.0-27744542600
Author
Borecky J.
Vercesi A.E.
Institutions
Abstract
Energy-dissipation in plant mitochondria can be mediated by inner membrane proteins via two processes: redox potential-dissipation or proton electrochemical potential-dissipation. Alternative oxidases (AOx) and the plant uncoupling mitochondrial proteins (PUMP) perform a type of intrinsic and extrinsic regulation of the coupling between respiration and phosphorylation, respectively. Expression analyses and functional studies on AOx and PUMP under normal and stress conditions suggest that the physiological role of both systems lies most likely in tuning up the mitochondrial energy metabolism in response of cells to stress situations. Indeed, the expression and function of these proteins in non-thermogenic tissues suggest that their primary functions are not related to heat production. © 2005 Springer Science+Business Media, Inc. 25 3-4 271 286 Almeida, A.M., Jarmuszkiewicz, W., Khomsi, H., Arruda, P., Vercesi, A.E., Sluse, F.E., Cyanide-resistant, ATP-synthesis-sustained, and uncoupling-protein- sustained respiration during postharvest ripening of tomato fruit (1999) Plant Physiol., 119, pp. 1323-1329 Affourtit, C., Krab, K., Moore, A.L., Control of plant mitochondrial respiration (2001) Biochim. Biophys. Acta, 1504, pp. 58-69 Arsenijevic, D., Onuma, H., Pecqueur, C., Raimbault, S., Manning, B.S., Couplan, E., Alves-Guerra, M.C., Ricquier, D., Disruption of the uncoupling protein 2 gene in mice reveals a role in immunity and reactive oxygen species production (2000) Nat. Genet., 26, pp. 435-439 Barata, H., De Meis, L., Uncoupled ATP hydrolysis and thermogenic activity of the sarcoplasmic reticulum Ca2+-ATPase: Coupling effects of dimethyl sulfoxide and low temperature (2002) J. Biol. Chem., 277, pp. 16868-16872 Barzu, O., Satre, M., Determination of oxygen affinity of respiratory systems using oxyhemoglobin as oxygen donor (1970) Analytic. Biochem., 36, pp. 428-433 Bendall, D.S., Bonner, W.D., Cyanide-insensitive respiration in plant mitochondria (1971) Plant Physiol., 47, pp. 236-245 Berthold, D.A., Siedow, J.N., Partial purification of the cyanide-resistant alternative oxidase of skunk cabbage (Symplocarpus foetidus) mitochondria (1993) Plant Physiol., 101, pp. 113-119 Borecký, J., Maia, I.G., Costa, A.D., Jezek, P., Chaimovich, H., De Andrade, P.B., Vercesi, A.E., Arruda, P., Functional reconstitution of Arabidopsis thaliana plant uncoupling mitochondrial protein (AtPUMP1) expressed in Escherichia coli (2001) FEBS Lett., 505, pp. 240-244 Borecký, J., Maia, I.G., Arruda, P., Mitochondrial uncoupling proteins in mammals and plants (2001) Biosci. Rep., 21, pp. 201-211 Boss, O., Samec, S., Paolonigiacobino, A., Rossier, C., Dulloo, A., Seydoux, J., Muzzin, P., Giacobino, J.-P., Uncoupling protein-3: A new member of the mitochondrial carrier family with tissue-specific expression (1997) FEBS Lett., 408, pp. 39-42 Bouillaud, F., Ricquier, D., Thibault, J., Weissenbach, J., Molecular approach to thermogenesis in brown adipose tissue: CDNA cloning of the mitochondrial uncoupling protein (1985) Proc. Natl. Acad. Sci. USA, 82, pp. 445-448 Brandalise, M., Maia, I.G., Borecký, J., Vercesi, A.E., Arruda, P., ZmPUMP encodes a maize mitochondrial uncoupling protein that is induced by oxidative stress (2003) Plant Sci., 165, pp. 329-335 Brandalise, M., Maia, I.G., Borecký, J., Vercesi, A.E., Arruda, P., Overexpression of plant uncoupling mitochondrial protein in transgenic tobacco increases tolerance to oxidative stress (2003) J. Bioenerg. Biomembr., 35, pp. 203-209 Calegario, F.F., Cosso, R.G., Fagian, M.M., Almeida, F.V., Jardim, W.F., Ježek, P., Arruda, P., Vercesi, A.E., Stimulation of potato tuber respiration by cold stress is associated with an increased capacity of both plant uncoupling mitochondrial protein (PUMP) and alternative oxidase (2003) J. Bioenerg. Biomembr., 35, pp. 211-220 Cavalheiro, R.A., Fortes, F., Borecký, J., Faustinoni, V.C., Schreiber, A.Z., Respiration, oxidative phosphorylation, and uncoupling protein in Candida albicans (2004) Braz. J. Med. Biol. Res., 37, pp. 1455-461 Clarkson, A.B., Bienen, E.J., Pollakis, G., Grady, R.J., Respiration of bloodstream forms of the parasite Trypanosoma brucei brucei is dependent on a plant-like alternative oxidase (1989) J. Biol. Chem., 264, pp. 17770-17776 Considine, M.J., Holtzapffel, R.C., Day, D.A., Whelan, J., Millar, A.H., Molecular Distinction between Alternative Oxidase from Monocots and Dicots (2002) Plant Physiology, 129, pp. 949-953 Considine, M.J., Daley, D.O., Whelan, J., The expression of alternative oxidase and uncoupling protein during fruit ripening in mango (2001) Plant Physiol., 126, pp. 1619-1629 Considine, M.J., Goodman, M., Echtay, K.S., Laloi, M., Whelan, J., Brand, M.D., Sweetlove, L.J., Superoxide stimulates a proton leak in potato mitochondria that is related to the activity of uncoupling protein (2003) J. Biol. Chem., 278, pp. 22298-22302 Costa, A.D.T., Nantes, I.L., Ježek, P., Leite, A., Arruda, P., Vercesi, A.E., Plant Uncoupling Mitochondrial Protein Activity in Mitochondria Isolated from Tomatoes at Different Stages of Ripening (1999) J. Bioenerg. Biomembr., 31, pp. 527-533 Day, D.A., Wiskich, J., Regulation of alternative oxidase activity in higher plants (1995) J. Bioenerg. Biomembr., 27, pp. 379-385 De Meis, L., Brown adipose tissue Ca2+-ATPase: Uncoupled ATP hydrolysis and thermogenic activity (2003) J. Biol. Chem., 278, pp. 41856-41861 Dry, J.B., Moore, A.L., Day, D.A., Wiskich, J.T., Regulation of alternative pathway activity in plant mitochondria: Nonlinear relationship between electron flux and the redox poise of the quinone pool (1989) Arch. Biochem. Biophys., 273, pp. 148-157 Echtay, K.S., Brand, M.D., Coenzyme Q induces GDP sensitive proton conductance in kidney mitochondria (2001) Biochem. Soc. Trans., 29, pp. 763-768 Echtay, K.S., Winkler, E., Frischmuth, K., Klingenberg, M., Uncoupling proteins 2 and 3 are highly active H (+) transporters and highly nucleotide sensitive when activated by coenzyme Q (ubiquinone) (2001) Proc. Natl. Acad. Sci. USA, 98, pp. 1416-1421 Echtay, K.S., Esteves, T.C., Pakay, J.L., Jekabsons, M.B., Lambert, A.J., Portero-Otin, M., Pamplona, R., Brand, M.D., A signalling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling (2003) EMBO J., 22, pp. 4103-4110 Echtay, K.S., Roussel, D., St-Pierre, J., Jekabsons, M.B., Cadenas, S., Stuart, J.A., Harper, J.A., Brand, M.D., Superoxide activates mitochondrial uncoupling proteins (2002) Nature, 415, pp. 96-99 Echtay, K.S., Murphy, M.P., Smith, R.A., Talbot, D.A., Brand, M.D., Superoxide activates mitochondrial uncoupling protein 2 from the matrix side. Studies using targeted antioxidants (2002) J. Biol. Chem., 277, pp. 47129-47135 Echtay, K.S., Winkler, E., Klingenberg, M., Coenzyme Q is an obligatory cofactor for uncoupling protein function (2000) Nature, 408, pp. 609-613 Elmoualij, B., Duyckaerts, C., Lamotte-Brasseur, J., Sluse, F.E., Phylogenetic classification of the mitochondrial carrier family of Saccharomyces cerevisiae (1997) Yeast, 13, pp. 573-581 Elthon, T.E., Nickels, R.L., McIntosh, L., Monoclonal antibodies to the alternative oxidase of higher plant mitochondria (1989) Plant Physiol., 89, pp. 1311-1317 Fleury, C., Neverova, M., Collins, S., Raimbault, S., Champigny, O., Levi-Meyrueis, C., Bouillaud, F., Warden, C.H., Uncoupling protein-2: A novel gene linked to obesity and hyperinsulinemia (1997) Nat. Genet., 15, pp. 269-272 Fridell, Y.W., Sanchez-Blanco, A., Silvia, B.A., Helfand, S.L., Functional characterization of a Drosophila mitochondrial uncoupling protein (2004) J. Bioenerg. Biomembr., 36, pp. 219-228 Garlid, K.D., Orosz, D.E., Modrianský, M., Vassanelli, S., Ježek, P., On the mechanism of fatty acid-induced proton transport by mitochondrial uncoupling protein (1996) J. Biol. Chem., 271, pp. 2615-2620 Gilliland, A., Singh, D.P., Hayward, J.M., Moore, C.A., Murphy, A.M., York, C.J., Slator, J., Carr, J.P., Genetic modification of alternative respiration has differential effects on antimycin A-induced versus salicylic acid-induced resistance to tobacco mosaic virus (2003) Plant Physiol, 132, pp. 1518-1528 Higo, K., Ugawa, Y., Iwamoto, M., Korenaga, T., Plant cis-acting regulatory DNA elements (PLACE) database: 1999 (1999) Nucleic Acid Res., 27, pp. 297-300 Hirabayashi, M., Ijiri, D., Kamei, Y., Tajima, A., Kanai, Y., Transformation of skeletal muscle from fast to slow-twitch during acquisition of cold tolerance in the chick (2005) Endocrinology, 146, pp. 399-405 Hourton-Cabassa, C., Rita Matos, A., Zachowski, A., Moreau, F., The plant uncoupling protein homologues: A new family of energy-dissipating proteins in plant mitochondria (2004) Plant Physiol. Biochem., 42, pp. 283-290 Iba, K., Acclimative response to temperature stress in higher plants: Approaches of gene engineering for temperature tolerance (2002) Annu. Rev. Plant Biol., 53, pp. 225-245 Ikuma, H., Schindler, F.J., Bonner, W.D., Kinetic analysis of oxidases in tightly coupled plant mitochondria (1964) Plant Physiol., 39, pp. 1x Ito, K., Isolation of two distinct cold-inducible cDNAs encoding plant uncoupling proteins from the spadix of skunk cabbage (Symplocarpus foetidus) (1999) Plant Sci., 149, pp. 167-173 Jabůrek, M., Garlid, K.D., Reconstitution of recombinant uncoupling proteins: UCP1, -2, and -3 have similar affinities for ATP and are unaffected by coenzyme Q10 (2003) J. Biol. Chem., 278, pp. 25825-25831 Jarmuszkiewicz, W., Sluse-Goffart, C.M., Vercesi, A.E., Sluse, F.E., Alternative oxidase and uncoupling protein: Thermogenesis versus cell energy balance (2001) Biosci Rep., 21, pp. 213-222 Jarmuszkiewicz, W., Navet, R., Alberici, L.C., Douette, P., Sluse-Goffart, C.M., Sluse, F.E., Vercesi, A.E., Redox State of Endogenous Coenzyme Q Modulates the Inhibition of Linoleic Acid-Induced Uncoupling by Guanosine Triphosphate in Isolated Skeletal Muscle Mitochondria (2004) J. Bioenerg. Biomembr., 36, pp. 493-502 Jarmuszkiewicz, W., Behrendt, M., Navet, R., Sluse, F.E., Uncoupling protein and alternative oxidase of Dictyostelium discoideum: Occurrence, properties and protein expression during vegetative life and starvation-induced early development (2002) FEBS Lett., 532, pp. 459-464 Jarmuszkiewicz, W., Milani, G., Fortes, F., Schreiber, A.Z., Sluse, F.E., Vercesi, A.E., First evidence and characterization of an uncoupling protein in fungi kingdom: CpUCP of Candida parapsilosis (2000) FEBS Lett., 467, pp. 145-149 Jarmuszkiewicz, W., Sluse-Goffart, C.M., Hryniewiecka, L., Sluse, F.E., Identification and characterization of a protozoan uncoupling protein in Acanthamoeba castellanii (1999) J. Biol. Chem., 274, pp. 23198-23202 Jarmuszkiewicz, W., Wagner, A.M., Wagner, M.J., Hryniewiecka, L., Immunological identification of the alternative oxidase of Acanthamoeba castellanii mitochondria (1997) FEBS Lett., 411, pp. 110-114 Ježek, P., Possible physiological roles of mitochondrial uncoupling proteins-UCPn (2002) Int. J. Biochem. Cell Biol., 34, pp. 1190-1206 Ježek, P., Borecký, J., Žáčková, M., Costa, A.D., Arruda, P., Possible basic and specific functions of plant uncoupling proteins (pUCP) (2001) Biosci Rep., 21, pp. 237-245 Ježek, P., Costa, A.D., Vercesi, A.E., Evidence for anion-translocating plant uncoupling mitochondrial protein in potato mitochondria (1996) J. Biol. Chem., 271, pp. 32743-32748 Ježek, P., Costa, A.D., Vercesi, A.E., Reconstituted plant uncoupling mitochondrial protein allows for proton translocation via fatty acid cycling mechanism (1997) J. Biol. Chem., 272, pp. 24272-24278 Ježek, P., Garlid, K.D., New substrates and competitive inhibitors of the Cl- translocating pathway of the uncoupling protein of brown adipose tissue mitochondria (1990) J. Biol. Chem., 265, pp. 19303-19311 Ježek, P., Garlid, K.D., Mammalian mitochondrial uncoupling proteins (1998) Int. J. Biochem. Cell Biol., 30, pp. 1163-1168 Ježek, P., Žáčková, M., Košařová, J., Rodrigues, E.T., Madeira, V.M., Vicente, J.A., Occurrence of Plant-Uncoupling Mitochondrial Protein (PUMP) in Diverse Organs and Tissues of Several Plants (2000) J. Bioenerg. Biomembr., 32, pp. 549-561 Kadenbach, B., Intrinsic and extrinsic uncoupling of oxidative phosphorylation (2003) Biochim. Biophys. Acta., 1604, pp. 77-94 Kannerworff, W.A., Van Der Plas, L.H.W., Respiration of bulb scale fragments of tulip after storage at 5°C (1994) Plant Sci., 104, pp. 31-38 Klein, S.L., Strausberg, R.L., Wagner, L., Pontius, J., Clifton, S.W., Richardson, P., Genetic and genomic tools for Xenopus research: The NIH Xenopus initiative (2002) Dev. Dyn., 225, pp. 384-391 Klingenberg, M., Mechanism and evolution of the uncoupling protein of brown adipose tissue (1990) Trends Biochem. Sci., 15, pp. 108-112 Kowaltowski, A.J., Costa, A.D.T., Vercesi, A.E., Activation of the potato plant uncoupling mitochondrial protein inhibits reactive oxygen species generation by the respiratory chain (1998) FEBS Lett., 425, pp. 213-216 Laloi, M., Klein, M., Riesmeier, J.W., Muller-Rober, B., Fleury, C., Bouillaud, F., Ricquier, D., A plant cold-induced uncoupling protein (1997) Nature, 389, pp. 135-136 Lambowitz, A.M., Sabourin, J.R., Bertrand, H., Nickels, R., McIntosh, L., Immunological identification of the alternative oxidase of Neurospora crassa mitochondria (1989) Mol. Cell. Biol., 9, pp. 1362-1364 Ledesma, A., De Lacoba, M.G., Rial, E., The mitochondrial uncoupling proteins (2002) Genome Biol., 3, pp. 3015-1-30159 Lescot, M., Dehais, P., Thijs, G., Marchal, K., Moreau, Y., Van De Peer, Y., Rouze, P., Rombauts, S., PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences (2002) Nucleic Acid Res., 30, pp. 325-327 Li, L.-X., Skorpen, F., Egenberg, K., Jorgensen, I.H., Grill, V., Uncoupling protein 2 participates in cellular defence against oxidative stress in clonal ß-cells (2001) Biochem. Biophys. Res. Commun., 282, pp. 273-277 Maia, I.G., Benedetti, C.E., Leite, A., Turcinelli, S.R., Vercesi, A.E., Arruda, P., AtPUMP: An Arabidopsis gene encoding a plant uncoupling mitochondrial protein (1998) FEBS Lett., 429, pp. 403-406 Mao, W., Yu, X.X., Zhong, A., Li, W., Brush, J., Sherwood, S.W., Adams, S.H., Pan, G., UCP4, a novel brain-specific mitochondrial protein that reduces membrane potential in mammalian cells (1999) FEBS Lett., 443, pp. 326-330 Maxwell, D.P., Nickels, R., McIntosh, L., Evidence of mitochondrial involvement in the transduction of signals required for the induction of genes associated with pathogen attack and senescence (2002) Plant J., 29, pp. 269-279 Maxwell, D.P., Wang, Y., McIntosh, L., The alternative oxidase lowers mitochondrial reactive oxygen species production in plant cells (1999) Proc Natl Acad Sci USA, 96, pp. 8271-8276 McIntosh, L., Eichler, T., Gray, G., Maxwell, D., Nickels, R., Wang, Y., Biochemical and genetic controls exerted by plant mitochondria (1998) Biochim. Biophys. Acta, 1365, pp. 278-284 Meeuse, B.J.D., Thermogenic respiration in aroids (1975) Annu. Rev. Plant Physiol., 26, pp. 117-126 Meeuse, B.J.D., Buggeln, R.G., Time, space, light and darkness in the metabolic flare-up of the Sauromatum appendix (1969) Acta Bot. Neerl., 18, pp. 159-172 Milani, G., Jarmuszkiewicz, W., Sluse-Goffart, C.M., Schreiber, A.Z., Vercesi, A.E., Sluse, F.E., Respiratory chain network in mitochondria of Candida parapsilosis: ADP/O appraisal of the multiple electron pathways (2001) FEBS Lett., 508, pp. 231-235 Millar, A.H., Bergersen, F.J., Day, D.A., Oxygen affinity of terminal oxidases in soybean mitochondria (1994) Plant Physiol. Biochem., 32, pp. 847-852 Millar, A.H., Wiskich, J.T., Whelan, J., Day, D.A., Organic acid activation of the alternative oxidase of plant mitochondria (1993) FEBS Lett., 329, pp. 259-262 Minagawa, N., Koga, S., Nakano, M., Sakajo, S., Yoshimoto, A., Possible involvement of superoxide anion in the induction of cyanide-resistant respiration in Hansenula anomala (1992) FEBS Lett., 302, pp. 217-219 Minagawa, N., Sakajo, S., Yoshimoto, A., Effects of unsaturated fatty acids on cyanide-resistant respiration of mitochondria isolated from Hansenula anomala (1992) Biosci. Biotechnol. Biochem., 56, pp. 1342-1343 Mitchell, P., Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism (1961) Naturwissenschaften, 191, pp. 144-148 Møller, I.M., Plant mitochondria and oxidative stress: Electron Transport, NADPH Turnover, and Metabolism of Reactive Oxygen Species (2001) Annu. Rev. Plant Physiol. Plant Mol. Biol., 52, pp. 561-591 Moore, A.L., Umbach, A.L., Siedow, J.N., Structure-function relationships of the alternative oxidase of plant mitochondria: A model of the active site (1995) J. Bioenerg. Biomembr., 27, pp. 367-377 Moore, A.L., Siedow, J.N., The regulation and nature of the cyanide resistant alternative oxidase of plant mitochondria (1991) Biochem. Biophys. Acta, 1059, pp. 121-140 Moore, A.L., Dry, I.B., Wiskich, J.T., Measurement of the redox state of the ubiquinone pool in plant mitochondria (1988) FEBS Lett., 235, pp. 76-80 Moynihan, M.R., Ordentlich, A., Raskin, I., Chilling-Induced Heat Evolution in Plants (1995) Plant Physiol., 108, pp. 995-999 Murayama, S., Handa, H., Isolation and characterization of cDNAs encoding mitochondrial uncoupling proteins in wheat: Wheat UCP genes are not regulated by low temperature (2000) Mol. Gen. Genet., 264, pp. 112-118 Murphy, M.P., Brand, M.D., The stoichiometry of charge translocation by cytochrome c oxidase and the cytochrome bc 1 complex of mitochondria at high membrane potential (1988) Eur. J. Biochem., 173, pp. 645-651 Murphy, M.P., Echtay, K.S., Blaikie, F.H., Asin-Cayuela, J., Cocheme, H.M., Green, K., Buckingham, J.A., Brand, M.D., Superoxide activates uncoupling proteins by generating carbon-centered radicals and initiating lipid peroxidation: Studies using a mitochondria- targeted spin trap derived from alpha-phenyl-N-tert-butylnitrone (2003) J. Biol. Chem., 278, pp. 48534-48545 Nantes, I.L., Fagian, M.M., Catisti, R., Arruda, P., Maia, I.G., Vercesi, A.E., Low temperature and aging-promoted expression of PUMP in potato tuber mitochondria (1999) FEBS Lett., 457, pp. 103-106 Nicholls, D.G., Hamster brown-adipose-tissue mitochondria. Purine nucleotide control of the ion conductance of the inner membrane, the nature of the nucleotide binding site (1976) Eur. J. Biochem., 62, pp. 223-228 Nicholls, D.G., Locke, R.M., Thermogenic mechanisms in brown fat (1984) Physiol. Rev., 64, pp. 1-64 Ordog, S.H., Higgins, V.J., Vanlerberghe, G.C., Mitochondrial alternative oxidase is not a critical component of plant viral resistance but may play a role in the hypersensitive response (2002) Plant Physiol., 129, pp. 1858-1865 Parsons, H.L., Yip, J.Y.H., Vanlerberghe, G.C., Increased respiratory restriction during phosphate-limited growth in transgenic tobacco cells lacking alternative oxidase (1999) Plant Physiol., 121, pp. 1309-1320 Pinhero, R.G., Rao, M.V., Paliyath, G., Murr, D.P., Fletcher, R.A., Changes in Activities of Antioxidant Enzymes and Their Relationship to Genetic and Paclobutrazol-Induced Chilling Tolerance of Maize Seedlings (1997) Plant Physiol., 114, pp. 695-704 Popov, V.N., Simonian, R.A., Skulachev, V.P., Starkov, A.A., Inhibition of the alternative oxidase stimulates H2O2 production in plant mitochondria (1997) FEBS Lett., 415, pp. 87-90 Purvis, A.C., Shewfelt, R.L., Does the alternative pathway ameliorate chilling injury in sensitive plant-tissues? (1993) Physiol. Plant., 88, pp. 712-718 Rafael, J., Pampel, I., Wang, X., Effect of pH and MgCl2 on the binding of purine nucleotides to the uncoupling protein in membrane particles from brown fat mitochondria (1994) Eur. J. Biochem., 223, pp. 971-980 Raskin, I., Ehmann, A., Melander, W.R., Meeuse, B.J.D., Salicylic acid: A natural inducer of heat production in arum lilies (1987) Science, 237, pp. 1601-1602 Raskin, I., Turner, I.M., Melander, W.R., Regulation of heat production in the inflorescences of an Arum lily by endogenous salicylic acid (1989) Proc. Natl. Acad. Sci. USA, 86, pp. 2214-2218 Rawsthorne, S., Larue, T.A., Metabolism under microaerobic conditions of mitochondria from cowpea nodules (1986) Plant Physiol., 81, pp. 1097-1102 Rhoads, D.M., McIntosh, L., Isolation and characterization of a cDNA clone encoding an alternative oxidase protein of Sauromatum guttatum (Schott) (1991) Proc. Natl. Acad. Sci. USA, 88, pp. 2122-2126 Ribas-Carbo, M., Berry, J.A., Azcon-Bieto, J., Siedow, J.N., The reaction of the plant mitochondrial cyanide-resistant alternative oxidase with oxygen (1994) Biochim. Biophys. Acta, 1188, pp. 205-212 Ricquier, D., Bouillaud, F., The uncoupling protein homologues: UCP1, UCP2, UCP3, StUCP and AtUCP (2000) Biochem J., 345, pp. 161-179 Ricquier, D., Bouillaud, F., Mitochondrial uncoupling proteins: From mitochondria to the regulation of energy balance (2000) J Physiol., 529, pp. 3-10 Ricquier, D., Kader, J.-C., Mitochondrial protein alteration in active brown fat: A soidum dodecyl sulfate-polyacrylamide gel electrophoretic study (1976) Biochem. Biophys. Res. Commun., 73, pp. 577-583 Sakajo, S., Minagawa, N., Komiyama, T., Yoshimoto, A., Molecular cloning of cDNA for antimycin A-inducible mRNA and its role in cyanide-resistant respiration in Hansenula anomala (1991) Biochim. Biophys. Acta, 1090, pp. 102-108 Sanchis, D., Fleury, C., Chomiki, N., Goubern, M., Huang, Q., Neverova, M., Gregoire, F., Ricquier, D., BMCP1, a novel mitochondrial carrier with high expression in the central nervous system of humans and rodents, and respiration uncoupling activity in recombinant yeast (1998) J. Biol. Chem., 273, pp. 34611-34615 Sato, Y., Murakami, T., Funatsuki, H., Matsuba, S., Saruyama, H., Tanida, M., Heat shock-mediated APX gene expression and protection against chilling injury in rice seedlings (2001) J. Exp. Bot., 52, pp. 145-151 Schonbaum, G.R., Bonner, W.D., Storey, B.T., Bahr, J.T., Specific inhibition of the cyanide-insensitive respiratory pathway in plant mitochondria by hydroxamic acids (1971) Plant Physiol., 47, pp. 124-128 Seymour, R.S., White, C.R., Gibernau, M., Environmental biology: Heat reward for insect pollinators (2003) Nature, 426, pp. 243-244 Siedow, J.N., Umbach, A.L., Plant mitochondrial electron transfer and molecular biology (1995) Plant Cell, 7, pp. 821-831 Simon, M., Adam, G., Rapatz, W., Spevak, W., Ruis, H., The Saccharomyces cerevisiae ADR1 gene is a positive regulator of transcription of genes encoding peroxisomal proteins (1991) Mol. Cell Biol., 11, pp. 699-704 Skulachev, V.P., Uncoupling: New approaches to an old problem of bioenergetics (1998) Biochim. Biophys. Acta, 1363, pp. 100-124 Sluse, F.E., Jarmuszkiewicz, W., Alternative oxidase in the branched mitochondrial respiratory network: An overview on structure, function, regulation, and role (1998) Braz. J. Med. Biol. Res., 31, pp. 733-747 Sluse, F.E., Jarmuszkiewicz, W., Activity and functional interaction of alternative oxidase and uncoupling protein in mitochondria from tomato fruit (2000) Braz. J. Med. Biol. Res., 33, pp. 259-268 Sluse, F.E., Jarmuszkiewicz, W., Uncoupling proteins outside the animal and plant kingdoms: Functional and evolutionary aspects (2002) FEBS Lett., 510, pp. 117-120 Sluse, F.E., Almeida, A.M., Jarmuszkiewicz, W., Vercesi, A.E., Free fatty acids regulate the uncoupling protein and alternative oxidase activities in plant mitochondria (1998) FEBS Lett, 433, pp. 237-234 Smith, A.M., Ratcliffe, R.G., Sweetlove, L.J., Activation and function of mitochondrial uncoupling protein in plants (2004) J. Biol. Chem., 279, pp. 51944-51952 Stuart, J.A., Harper, J.A., Brindle, K.M., Brand, M.D., Uncoupling protein 2 from carp and zebrafish, ectothermic vertebrates (1999) Biochim. Biophys. Acta, 1413, pp. 50-54 Talbot, D.A., Duchamp, C., Rey, B., Hanuise, N., Rouanet, J.L., Sibille, B., Brand, M.D., Uncoupling protein and ATP/ADP carrier increase mitochondrial proton conductance after cold adaptation of king penguins (2004) J. Physiol., 558, pp. 123-135 Tai, P.Y.P., Lentini, R.S., Freeze Damage of Florida Sugarcane (1998) Sugarcane Handbook, pp. 1-3. , (Anderson D. L. Ed.), Ed. 1. Florida Cooperative Extension Service, University of Florida, Florida Uemura, S.A., Luo, S., Moreno, S.N.J., Docampo, R., Oxidative Phosphorylation, Ca2+ Transport, and Fatty Acid-induced Uncoupling in Malaria Parasites Mitochondria (2000) J. Biol. Chem., 275, pp. 9709-9715 Umbach, A.L., Siedow, J.N., Covalent and non-covalent dimers of the cyanide-resistant alternative oxidase protein in higher plant mitochondria and their relationship to enzyme activity (1993) Plant Physiol., 103, pp. 845-854 Umbach, A.L., Wiskich, J.T., Siedow, J.N., Regulation of alternative oxidase kinetics by pyruvate and intermolecular disulfide bond redox status in soybean seedling mitochondria (1994) FEBS Lett., 348, pp. 181-184 Van Der Straeten, D., Chaerle, L., Sharkov, G., Lambers, H., Van Montagu, M., Salicylic acid enhances the activity of the alternative pathway of respiration in tobacco leaves and induces thermogenicity (1995) Planta, 196, pp. 412-419 Vanlerberghe, G.C., McIntosh, L., Signals Regulating the Expression of the Nuclear Gene Encoding Alternative Oxidase of Plant Mitochondria (1996) Plant Physiol., 111, pp. 589-595 Vanlerberghe, G.C., McIntosh, L., Alternative oxidase: From gene to function (1997) Annu. Rev. Plant Physiol. Plant Mol. Biol., 48, pp. 703-734 Vanlerberghe, G.C., Day, D.A., Wiskich, J.T., Vanlerberghe, A.E., McIntosh, L., Alternative oxidase activity in tobacco leaf mitochondria: Dependence on tricarboxylic acid cycle-mediated redox regulation and pyruvate activation (1995) Plant Physiol., 109, pp. 353-361 Vanlerberghe, G.C., McIntosh, L., Alternative oxidase: From gene to function (1997) Annu. Rev. Plant Physiol. Plant Mol. Biol., 48, pp. 703-734 Vanlerberghe, G.C., Vanlerberghe, A.E., McIntosh, L., Molecular genetic alteration of plant respiration (silencing and overexpression of alternative oxidase in transgenic tobacco) (1994) Plant Physiol., 106, pp. 1503-1510 Vanlerberghe, G.C., Robson, C.A., Yip, J.Y.H., Induction of Mitochondrial Alternative Oxidase in Response to a Cell Signal Pathway Down-Regulating the Cytochrome Pathway Prevents Programmed Cell Death (2002) Plant Physiol., 129, pp. 1829-1842 Vercesi, A.E., The discovery of an uncoupling mitochondrial protein in plants (2001) Biosci. Rep., 21, pp. 195-200 Vercesi, A.E., Martins, I.S., Silva, M.A.P., Leite, H.M.F., Cuccovia, I.M., Chaimovich, H., PUMPing plants (1995) Nature, 375, p. 24 Vercesi, A.E., Chaimovich, H., Cuccovia, I.M., A plant uncoupling mitochondrial protein, PUMP (1997) Rec. Res. Devel. Plant Physiol., 1, pp. 85-91 Vercesi, A.E., Ježek, P., Costa, A.D.T., Kowaltowski, A.J., Maia, I.G., Arruda, P., Moller, I.M., Glaser, E., A plant uncoupling mitochondrial protein (1998) Plant Mitochondria: From Gene to Function., pp. 435-440. , Backhuys Publishers Leiden, The Netherlands Vianna, C.R., Hagen, T., Zhang, C.-Y., Bachman, E., Boss, O., Gereben, B., Moriscot, A.S., Bianco, A.C., Cloning and functional characterization of an uncoupling protein homolog in hummingbirds (2001) Physiol. Genomics, 5, pp. 137-145 Wagner, A.M., Moore, A.L., Structure and function of the plant alternative oxidase: Its putative role in the oxygen defence mechanism (1997) Biosci. Rep., 17, pp. 319-333 Wagner, A.M., Wagner, M.J., Changes in mitochondrial respiratory chain components of petunia cells during culture in the presence of antimycin a (1997) Plant Physiol., 115, pp. 617-622 Watanabe, A., Nakazono, M., Tsutsumi, N., Hirai, A., AtUCP2: A novel isoform of the mitochondrial uncoupling protein of Arabidopsis thaliana (1999) Plant Cell Physiol., 40, pp. 1160-1166 Watanabe, A., Hirai, A., Two uncoupling protein genes of rice (Oryza sativa L.): Molecular study reveals the defects in the pre-mRNA processing for the heat-generating proteins of the subtropical cereal (2002) Planta, 215, pp. 90-100 Yip, J.Y.H., Vanlerberghe, G.C., Mitochondrial alternative oxidase acts to dampen the generation of active oxygen species during a period of rapid respiration induced to support a high rate of nutrient uptake (2001) Physiol. Plant., 112, pp. 327-333 Zhou, D.B., Solomos, T., Effect of hypoxia on sugar accumulation, respiration, activities of amylase and starch phosphorylase, and induction of alternative oxidase and acid invertase during storage of potato tubers (Solanum tuberosum cultivar Russet Burbank) at 1°C (1998) Physiol. Plant., 104, pp. 255-265