Preferences help
enabled [disable] Abstract
Number of results
2001 | 48 | 1 | 145-155
Article title

Uncoupling proteins in mitochondria of plants and some microorganisms.

Title variants
Languages of publication
Uncoupling proteins, members of the mitochondrial carrier family, are present in mitochondrial inner membrane and mediate free fatty acid-activated, purine-nucleotide-inhibited H+ re-uptake. Since 1995, it has been shown that the uncoupling protein is present in many higher plants and some microorganisms like non-photosynthetic amoeboid protozoon, Acanthamoeba castellanii and non-fermentative yeast Candida parapsilosis. In mitochondria of these organisms, uncoupling protein activity is revealed not only by stimulation of state 4 respiration by free fatty acids accompanied by decrease in membrane potential (these effects being partially released by ATP and GTP) but mainly by lowering ADP/O ratio during state 3 respiration. Plant and microorganism uncoupling proteins are able to divert very efficiently energy from oxidative phosphorylation, competing for ΔμH+ with ATP synthase. Functional connection and physiological role of uncoupling protein and alternative oxidase, two main energy-dissipating systems in plant-type mitochondria, are discussed.
Physical description
  • Department of Bioenergetics, Institute of Molecular Biology and Biotechnology, Adam Mickiewicz University, Poznań, Poland
  • 1. Mitchell, P. (1961) Coupling of phosphorylation to electron and proton transfer by a chemiosmotic type of mechanism. Nature 191, 144-148.
  • 2. Stuart, J.A., Brindle, K.M., Harper, J.A. & Brand, M.D. (2000) Mitochondrial proton leak and uncoupling proteins. J. Bioenerg. Biomembr. 31, 517-525.
  • 3. Mackenzie, S. & McIntosh, L. (1999) Higher plant mitochondria. Plant Cell 11, 571-585.
  • 4. Vercesi, A.E., Martins, I.S., Silva, M.A.P., Leite, H.M.F., Cuccovia, I.M. & Chaimovich, H. (1995) PUMPing plants. Nature 375, 24.
  • 5. Laloi, M. (1999) Plant mitochondrial carriers: An overview. Cell. Mol. Life Sci. 56, 918-944.
  • 6. Klingenberg, M. (1990) Mechanism and evolution of the uncoupling protein of brown adipose tissue. Trends Biochem. Sci. 15, 108-112.
  • 7. Nicholls, D.G. & Rial, E. (1999) A history of the first uncoupling protein, UCP1. J. Bioenerg. Biomembr. 31, 399-418.
  • 8. Fleury, C., Neverova, M., Collins, S., Raimbault, S., Champigny, O., Levi-Meyrueis, C., Boillaud, F., Seldin, M.F., Surwit, R.S., Ricquier, D. & Warden, C.H. (1997) Uncoupling protein-2: A novel gene linked to obesity and hyperinsulinemia. Nat. Genet. 15, 269-272.
  • 9. Boss, O., Samec, S., Paolonigiacobino, A., Rossier, C., Dulloo, A., Seydoux, J., Muzzin, P. & Giacobino, J.-P. (1997) Uncoupling protein-3: A new member of the mitochondrial carrier family with tissue-specific expression. FEBS Lett. 408, 39-42.
  • 10. Vidal-Puig, A., Solanes, G., Grujic, D., Flier, J.S. & Lowell, B.B. (1997) UCP3: An uncoupling protein homologue expressed preferentially and abundantly in skeletal muscle and brown adipose tissue. Biochem. Biophys. Res. Commun. 235, 79-82.
  • 11. Mao, W.G., Yu, X.X., Zhong, A., Li, W.L., Brush, J., Sherwood, S.W., Adams, S.H. & Pan, G. (1999) UCP4, a novel brain-specific mitochondrial protein that reduces membrane potential in mammalian cells. FEBS Lett. 443, 326-330.
  • 12. Sanchis, D., Fleury, Ch., Chomiki, N., Goubern, M., Huang, Q. L., Neverova, M., Grégoire, F., Easlick, J., Raimbault, S., Lévi-Meyrueis, C., Miroux, B., Collins, S., Seldin, M., Richard, D., Warden, C., Bouillaud, F. & Ricquier, D. (1998) BMCP1, a novel mitochondrial carrier with high expression in the central nervous system of humans and rodents, and respiration uncoupling activity in recombinant yeast. J. Biol. Chem. 273, 34611-34615.
  • 13. Ježek, P., Costa, A.D.T. & Vercesi, A.E. (1997) Reconstituted plant uncoupling mitochondrial protein allows for proton translocation via fatty acid cycling mechanism. J. Biol. Chem. 272, 24272-24278.
  • 14. Ježek, P., Engstová, H., Žačková, M., Vercesi, A.E., Costa, D.T., Arruda, P. & Garlid, P. (1998) Fatty acid cycling mechanism and mitochondrial uncoupling proteins. Biochim. Biophys. Acta 1365, 319-327.
  • 15. Laloi, M., Klein, M., Riesmeier, J.W., Muller-Rober, B., Fleury, C., Bouillaud, F. & Ricquier, D. (1997) A plant cold-induced uncoupling protein. Nature 389, 135-136.
  • 16. Maia, I.G., Benedetti, C.E., Leite, A., Turcinelli, S.R., Vercesi, A.E. & Arruda, P. (1998) AtPUMP: An Arabidopsis gene encoding a plant uncoupling mitochondrial protein. FEBS Lett. 429, 403-406.
  • 17. Watanabe, A., Nakazano, M., Tsutsumi, N. & Hirai, A. (1999) AtUCP2: A novel isoform of the mitochondrial uncoupling protein of Arabidopsis thaliana. Plant Cell Physiol. 40, 1160-1166.
  • 18. Jarmuszkiewicz, W., Sluse-Goffart, C.M., Hryniewiecka, L. & Sluse, F.E. (1999) Identification and characterization of a protozoan uncoupling protein in Acanthamoeba castellanii. J. Biol. Chem. 274, 23198-23202.
  • 19. Gray, M.W., Burger, G. & Lang, B.F. (1999) Mitochondrial evolution. Science 283, 1476-1481.
  • 20. Jarmuszkiewicz, W., Milani, G., Fortes, F., Schreiber, A.Z., Sluse, F.E. & Vercesi, A.E. (2000) First evidence and characterization of an uncoupling protein in fungi kingdom: CpUCP of Candida parapsilosis. FEBS Lett. 467, 145-149.
  • 21. Uyemura, S.A., Luo, S., Moreno, S.N.J. & Docampo, R. (2000) Oxidative phosphorylation, Ca2+ transport, and fatty acid-induced uncoupling in malaria parasites mitochondria. J. Biol. Chem. 275, 9709-9715.
  • 22. Ricquier, D. & Bouillaud, F. (2000) The uncoupling protein homologues: UCP1, UCP2, UCP3, StUCP and AtUCP. Biochem. J. 345, 161-179.
  • 23. Ježek, P. & Urbanková, E. (2000) Specific sequence motifs of mitochondrial uncoupling proteins. IUBMB Life, 49, 63-70.
  • 24. Winkler, E. & Klingenberg, M. (1994) Effect of fatty acids on H+ transport activity of the reconstituted uncoupling protein. J. Biol. Chem. 269, 2508-2515.
  • 25. Skulachev, V.P. (1991) Fatty acid circuit as a physiological mechanism of uncoupling of oxidative phosphorylation. FEBS Lett. 264, 246-248.
  • 26. Garlid, K.D., Orosz, D.E., Modriansky, M., Vassanelli, S. & Ježek, P. (1996) On the mechanism of fatty acid-induced proton transport by mitochondrial uncoupling protein. J. Biol. Chem. 271, 2615-2620.
  • 27. Skulachev, V.P. (1998) Uncoupling: New approaches to an old problem of bioenergetics. Biochim. Biophys. Acta, 1363, 100-124.
  • 28. Andreyev, A.Y., Bondareva, T.O., Dedukhova, V.I., Mokhova, E.N., Skulachev, V.P., Tsofina, L.M., Volkov, N.L. & Vygodina, T.V. (1989) The ATP/ADP-antiporter is involved in the uncoupling effect of fatty acids on mitochondria. Eur. J. Biochem. 182, 585-592.
  • 29. Smartsev, V.N., Mokhova, E.N. & Skulachev, V.P. (1997) The pH-dependent reciprocal changes in contribution of ADP/ATP antiporter and aspartate/glutamate antiporter to the fatty acid-induced uncoupling. FEBS Lett. 412, 179-182.
  • 30. Więckowski, M. & Wojtczak, L. (1997) Involvement of the dicarboxylate carrier in the protonophoric action of long-chain fatty acids in mitochondria. Biochem. Biophys. Res. Commun. 232, 414-417.
  • 31. Žaűková, M., Krämer, R. & Ježek, P. (2000) Interaction of mitochondrial phosphate carrier with fatty acids and hydrophobic phosphate analogs. Int. J. Biochem. Cell Biol. 32, 499-508.
  • 32. Almeida, A.M., Jarmuszkiewicz, W., Khomsi, H., Arruda, P., Vercesi, A.E. & Sluse, F.E. (1999) Cyanide-resistant, ATP synthesis-sustained, and uncoupling protein-sustained respiration during postharvest ripening of tomato fruit. Plant Physiol. 119, 1323-1329.
  • 33. Ježek, P., Costa, A.D.T. & Vercesi, A.E. (1996) Evidence for anion-translocating plant uncoupling mitochondrial protein in potato mitochondria. J. Biol. Chem. 271, 32743-32748.
  • 34. Jarmuszkiewicz, W., Almeida, A.M., Sluse-Goffart, C.M., Sluse, F.E. & Vercesi, A.E. (1998) Linoleic acid-induced activity of plant uncoupling mitochondrial protein in purified tomato fruit mitochondria during resting, phosphorylating, and progressively uncoupled respiration. J. Biol. Chem. 273, 34882-34886.
  • 35. Saviani, E.E., da Silva, A. & Martins, I.S. (1998) Role of F1F0-ATP synthase and uncoupling protein in mitochondrial respiratory uncoupling of ripened avocado fruits. Plant Physiol. Biochem. 36, 575- 582.
  • 36. Pastore, D., Fratianni, A., Pede, S.D. & Passarella, S. (2000) Effects of fatty acids, nucleotides and reactive species on durum wheat mitochondria. FEBS Lett. 470, 88-92.
  • 37. Saviani, E.E., da Silva, A., Jr. & Martins, I.S. (1997) Photoaffinity labelling of the uncoupling protein from potato tuber mitochondria. Plant Physiol. Biochem. 35, 701-706.
  • 38. Jarmuszkiewicz, W., Almeida, A.M., Vercesi, A.E., Sluse, F.E. & Sluse-Goffart, C.M. (2000) Proton re-uptake partitioning between uncoupling protein and ATP synthase during benzohydroxamic acid-resistant state 3 respiration in tomato fruit mitochondria. J. Biol. Chem. 275, 13315-13320.
  • 39. Jarmuszkiewicz, W., Hryniewiecka, L., Sluse- Goffart, C.M. & Sluse, F.E. (2000) Efficiency of Acanthamoeba castellanii uncoupling protein in energy-dissipating processes; in Animating the Cellular Map (Hofmeyr, J.-H., Rohwer, J.M., Snoep, J.L., eds.) pp. 119-123, Stellenbosch University Press.
  • 40. Jarmuszkiewicz, W., Sluse-Goffart, C.M., Hryniewiecka, L., Michejda, J. & Sluse, F.E. (1998) Electron partitioning between the two branching quinol-oxidizing pathways in Acanthamoeba castellanii mitochondria during steady-state state 3 respiration. J. Biol. Chem. 273, 10174-10180.
  • 41. Sluse, F.E., Jarmuszkiewicz, W., Almeida, A.M., Vercesi, A.E., Hryniewiecka, L. & Sluse-Goffart, C.M. (1998) Determination of actual contributions of energy-dissipating pathways in mitochondrial respiration: the ADP/O method; in Plant Mitochondria: from Gene to Function (Möller, I.M., Gardestrom, P., Glimelius, K., Glaser, E., eds.) pp. 519-523, Backhuys Publishers, Leiden.
  • 42. Sluse, F.E., Jarmuszkiewicz, W., Almeida, A.M., Vercesia, A.E. & Sluse-Goffart, C.M. (2000) Proton partitioning between ATP synthase and uncoupling protein during cytochrome pathway state 3 respiration in tomato fruit mitochondria; in Animating the Cellular Map (Hofmeyr, J.-H., Rohwer, J.M., Snoep, J.L., eds.) pp. 135-140, Stellenbosch University Press.
  • 43. Vanlerberghe, G.C. & McIntosh, L. (1997) Alternative oxidase: From gene to function. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 703-734.
  • 44. Kay, C.J. & Palmer, J.M. (1985) Solubilization of the alternative oxidase of cuckoo-pint (Arum maculatum) mitochondria. Biochem. J. 228, 309- 318.
  • 45. Minagawa, N., Sakajo, S. & Yoshimoto, A. (1992) Effects of unsaturated fatty acids on CN-resistant respiration of mitochondria isolated from Hansenula anomala. Biosci. Biotechnol. Biochem. 56, 1342-1343.
  • 46. Sluse, F.E., Almeida, A.M., Jarmuszkiewicz, W. & Vercesi, A.E. (1998) Free fatty acids regulate the uncoupling protein and alternative oxidase activities in plant mitochondria. FEBS Lett. 433, 237-240.
  • 47. Kumar, S., Patil, B.C. & Sinha, S.K. (1990) Cyanide-resistant respiration is involved in temperature rise in ripening mangoes. Biochem. Biophys. Res. Commun. 168, 818-822.
  • 48. Kumar, S. & Sinha, S.K. (1992) Alternative respiration and heat production in ripening banana fruits (Musa paradisiaca var. Mysore Kadali). J. Exp. Bot. 43, 1639-1642.
  • 49. Gueclue, J., Paulin, A. & Soudain, P. (1989) Changes in polar lipids during ripening and senescence of cherry tomato (Lycopersicn esculentum): Relation to climacteric and ethylene increases. Plant Physiol. 77, 413-419.
  • 50. Rouet-Mayer, M.A., Valentova, O., Simond-Cote, E., Daussant, J. & ThPvenot, C. (1995) Critical analysis of phospholipid hydrolyzing activities in ripening tomato fruits: Study by spectrofluorimetry and high-performance liquid chromatography. Lipids 30, 739-746.
  • 51. Sluse, F.E. & Jarmuszkiewicz, W. (2000) Activity and functional interaction of alternative oxidase and uncoupling protein in mitochondria from tomato fruit. Braz. J. Med. Biol. Res. 33, 259-268.
  • 52. Meeuse, B.D.J. (1975) Thermogenic respiration in Aroids. Annu. Rev. Plant Physiol. 26, 117-126.
  • 53. Elthon, T.E., Stewart, C.E., McCoy, C.A. & Bonner, W.D., Jr. (1986) Alternative respiratory path capacity in plant mitochondria: Effect of growth temperature, the electrochemical gradient, and assay pH. Plant Physiol. 80, 378-383.
  • 54. Duque, P. & Arrabaca, J.D. (1999) Respiratory metabolism during cold storage of apple friuit. II. Alternative oxidase is induced at the climacteric. Physiol. Plant. 107, 24-31.
  • 55. Nantes, I.L., Fagian, M.M., Catisti, R., Arruda, P., Maia, I.G. & Vercesi, A.E. (1999) Low temperature and aging-promoted expression of PUMP in potato tuber mitochondria. FEBS Lett. 457, 103-106.
  • 56. Jarmuszkiewicz, W., Sluse-Goffart, C.M., Vercesi, A.E. & Sluse, F.E. (2000) Alternative oxidase and uncoupling protein: Thermogenesis versus cell energy balance. Biosci. Rep. (in press).
  • 57. Sluse, F.E. & Jarmuszkiewicz, W. (2000) Dynamics of H+ fluxes in mitochondrial membrane; in Handbook of Plant Growth: pH as a Master Variable in Plant Growth (Rengel, Z., ed.) Marcel Dekker, Inc. New York (in press).
  • 58. Purvis, A.C. & Shewfelt, R.L. (1993) Does the alternative pathway ameliorate chilling injury sensitive plant tissues? Physiol. Plant. 88, 712-718.
  • 59. Purvis, A.C. (1997) Role of the alternative oxidase in limiting superoxide production by plant mitochondria. Physiol. Plant. 100, 165-170.
  • 60. Wagner, A.M. & Moore, A.L. (1997) Structure and function of the plant alternative oxidase: Its role in the oxygen defence mechanism. Biosci. Rep. 17, 319-333.
  • 61. Popov, V.N., Simonian, R.A., Skulachev, V.P. & Starcov, A.A. (1997) Inhibition of the alternative oxidase stimulates H2O2 production in plant mitochondria. FEBS Lett. 415, 87-90.
  • 62. Maxwell, D.P., Wang, Y. & McIntosh, L. (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc. Natl. Acad. Sci. U.S.A. 96, 8271-8276.
  • 63. Kowaltowski, A.J., Costa, A.D.T. & Vercesi, A.E. (1998) Activation of the potato plant uncoupling mitochondrial protein inhibits reactive oxygen species generation by the respiratory chain. FEBS Lett. 425, 213-216.
  • 64. Casolo, V., Braidot, E., Chiandussi, E., Macri, F. & Vianello, A. (2000) The role of mild uncoupling and non-coupled respiration in the regulation of hydrogen peroxide generation by plant mitochondria. FEBS Lett. 474, 53-57.
Document Type
Publication order reference
YADDA identifier
JavaScript is turned off in your web browser. Turn it on to take full advantage of this site, then refresh the page.