Mitochondrial uncoupling proteins in unicellular eukaryotes

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1797, Issue 6-7, 2010, Pages 792-799

  Jarmuszkiewicz, Wieslawa ^a   Woyda Ploszczyca, Andrzej ^a   Antos Krzeminska, Nina ^a   Sluse, Francis E ^b  

^a ADAM MICKIEWICZ UNIVERSITY   (Poland)

^b UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Amoeboid eukaryotes; Energy dissipation; Fungi; Mitochondria; Ubiquinone redox state; Uncoupling proteins

Indexed keywords

FATTY ACID; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PURINE NUCLEOTIDE; REACTIVE OXYGEN METABOLITE; UBIQUINONE; UNCOUPLING PROTEIN;

ACANTHAMOEBA CASTELLANII; BROWN ADIPOSE TISSUE; DICTYOSTELIUM DISCOIDEUM; ELECTROCHEMICAL ANALYSIS; ENERGY BALANCE; ENZYME ACTIVATION; ENZYME ACTIVITY; EUKARYOTE; LIPID PEROXIDATION; MEMBRANE POTENTIAL; MITOCHONDRION; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTON TRANSPORT; RESPIRATORY CHAIN; REVIEW; THERMOGENESIS;

ACANTHAMOEBA CASTELLANII; ADIPOSE TISSUE, BROWN; ANIMALS; EUKARYOTA; EVOLUTION, MOLECULAR; FATTY ACIDS, NONESTERIFIED; ION CHANNELS; LIPID PEROXIDATION; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; OXIDOREDUCTASES; PURINE NUCLEOTIDES; REACTIVE OXYGEN SPECIES; SPECIES SPECIFICITY; UBIQUINONE;

ACANTHAMOEBA CASTELLANII; EUKARYOTA; FUNGI; MAMMALIA; PROTISTA;

EID: 77953799076     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2009.12.005     Document Type: Review

References (69)

1. Jarmuszkiewicz W. Uncoupling proteins in mitochondria of plants and some microorganisms. Acta Biochem. Pol. 2001, 48:145-155.
2. Klingenberg M. Mechanism and evolution of the uncoupling protein of brown adipose tissue. Trends Biochem. Sci. 1990, 15:108-112.
3. Echtay K.S. Mitochondrial uncoupling proteins - what is their physiological role?. Free Rad. Biol. Med. 2007, 43:1351-1372.
4. Vercesi A.E., Borecky J., Maia I.D., Arruda P., Cuccovia I.M., Chaimovich H. Plant uncoupling mitochondrial proteins. Annu. Rev. Plant Biol. 2006, 57:383-404.
5. Hughes J., Criscuolo F. Evolutionary history of the UCP gene family: gene duplication and selection. BMC Evol. Biol. 2008, 8:306.
6. Sluse F.E., Jarmuszkiewicz W. Uncoupling proteins outside the animal and plant kingdoms: functional and evolutionary aspects. FEBS Lett. 2002, 510:117-120.
7. Jarmuszkiewicz W., Sluse-Goffart C.M., Hryniewiecka L., Sluse F.E. Identification and characterization of a protozoan uncoupling protein in Acanthamoeba castellanii. J. Biol. Chem. 1999, 274:23198-23202.
8. Gray M.W., Burger G., Lang B.F. Mitochondrial evolution. Science 1999, 283:1476-1481.
9. 2+ transport, and fatty acid-induced uncoupling in malaria parasites mitochondria. J. Biol. Chem. 2000, 275:9709-9715.
10. Uyemura S.A., Luo S., Viera M., Moreno S.N.J., Docampo R. Oxidative phosphorylation and rotenone-insensitive malate- and NADH-quinone oxidoreductases in Plasmodium yoelii yoelii mitochondria in situ. J. Biol. Chem. 2004, 279:385-393.
11. 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. FEBS Lett. 2000, 467:145-149.
12. Cavalheiro R.A., Fortes F., Borecky J., Faustinoni V.C., Schreiber A.Z., Vercesi A.E. Respiration, oxidative phosphorylation, and uncoupling protein in Candida albinicans. Braz. J. Med. Biol. Res. 2004, 37:1455-1461.
13. L.A. Luevano-Martinez, E. Moyano, M.G. de Lacoba, E. Rial, S. Uribe-Carvajal, Identification of the mitochondrial carrier that provides Yarrowia lipolytica with a fatty acid-induced and nucleotide-sensitive uncoupling protein-like activity, Biochim. Biophys. Acta 1797 (2010) 81-88.
14. Tudella V.G., Curti C., Soriani F.M., Santos A.C., Uyemura S.A. In situ evidence of an alternative oxidase and an uncoupling protein in the respiratory chain of Aspergilllus fumigatus. Int. J. Biochem. Cell Biol. 2003, 36:162-172.
15. 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. FEBS Lett. 2002, 532:459-464.
16. Roussel D., Harding M., Runswick M.J., Walker J.E., Brand M.D. Does any yeast mitochondrial carrier have a native uncoupling protein function?. J. Bioenerg. Biomembr. 2002, 34:165-176.
17. Palmieri L., Lasorsa F.M., Vozza A., Agrimi G., Fiermonte G., Runswick M.J., Walker J.E., Palmieri F. Identification and functions of new transporters in yeast mitochondria. Biochim. Biophys. Acta 2000, 1459:363-369.
18. Merchant S.S., Prochnik S.E., Vallon O., Harris E.H., Karpowicz S.J., et al. The Chlamydomonas, The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 2007, 318:245-250.
19. Swida A., Woyda-Ploszczyca A., Jarmuszkiewicz W. Redox state of quinone affects sensitivity of Acanthamoeba castellanii mitochondrial uncoupling protein to purine nucleotides. Biochem. J. 2008, 413:359-367.
20. Swida A., Czarna M., Woyda-Ploszczyca A., Kicinska A., Sluse F.E., Jarmuszkiewicz W. Fatty acid efficiency profile in uncoupling of Acanthamoeba castellanii mitochondria. J. Bioenerg. Biomembr. 2007, 39:109-115.
21. Pastore D., Fratianni A., Di Pede S., Passarela S. Effects of fatty acids, nucleotides and reactive oxygen species on durum wheat mitochondria. FEBS Lett. 2000, 470:88-92.
22. Winkler E., Klingenberg M. Effect of fatty acids on H+ transport activity of the reconstituted uncoupling protein. J. Biol. Chem. 1994, 269:2508-2515.
23. Klingenberg M., Huang S.-G. Structure and function of the uncoupling protein from brown adipose tissue. Biophys. Biochim. Acta 1999, 1415:271-296.
24. Avery S.V., Lloyd D., Harwood J.L.J. Changes in membrane fatty acid composition and delta12-desaturase activity during growth of Acanthamoeba castellanii in batch culture. J. Euk. Microbiol. 1994, 41:396-401.
25. Avery S.V., Harwood J.L., Lloyd D. Low-temperature-induced adaptations in fatty acid metabolism of Acanthamoeba castellanii cultures of different ages: relationship to changes in cell division, oxygen uptake and phagocytotic activity. Microbiology 1994, 140:2423-2431.
26. Jarmuszkiewicz W., Antos N., Swida A., Czarna M., Sluse F.E. The effect of growth at low temperature on the activity and expression of the uncoupling protein in Acanthamoeba castellanii mitochondria. FEBS Lett. 2004, 569:178-184.
27. Feron G., Blin-Perrin C., Krasniewski I., Mauvais G., Lherminier J. Metabolism of fatty acid in yeast: characterization of beta-oxidation and ultrastructural changes in the genus Sporidiobolus sp. cultivated on ricinoleic acid methyl ester. FEMS Microbiol. Lett. 2005, 250:63-69.
28. Graves L.B., Becker W.M. Beta-oxidation in glyoxysomes from Euglena. J. Euk. Micriobiol. 2007, 21:771-775.
29. Parsons M., Furuya T., Pal S., Kessler P. Biogenesis and function of peroxisomes and glycosomes. Mol. Biochem. Parasitol. 2001, 115:19-28.
30. Athenstaedt K., Jolivet P., Boulard C., Zivy M., Negroni L., Nicaud J.M., Chardot T. Lipid particle composition of the yeast Yarrowia lipolytica depends on the carbon source. Proteomics 2006, 6:1450-1459.
31. Andreyev A.Y., Bondareva T.O., Dedukhova V.I., Mokhova E.N., Skulachev V.P., Tsofina L.M., Volkov N.L., Vygodina T.V. The ATP/ADP-antiporter is involved in the uncoupling effect of fatty acids on mitochondria. Eur. J. Biochem. 1989, 182:585-592.
32. Samartsev V.N., Mokhova E.N., Skulachev V.P. The pH-dependent reciprocal changes in contribution of ADP/ATP antiporter and aspartate/glutamate antiporter to the fatty acid-induced uncoupling. FEBS Lett. 1997, 412:179-182.
33. Wieckowski M., Wojtczak L. Involvement of the dicarboxylate carrier in the protonophoric action of long-chain fatty acids in mitochondria. Biochem. Biophys. Res. Comm. 1997, 232:414-417.
34. Jarmuszkiewicz W., Czarna M., Sluse-Goffart C.M., Sluse F.E. The contribution of uncoupling protein and ATP synthase to state 3 respiration in Acanthamoeba castellanii mitochondria. Acta Biochim. Pol. 2004, 51:533-538.
35. Jarmuszkiewicz W., Almeida A.M., Sluse-Goffart C.M., Sluse F.E., Vercesi A.E. Linoleic acid-induced activity of plant uncoupling mitochondrial protein in purified tomato fruit mitochondria during resting, phosphorylating, and progressively uncoupled respiration. J. Biol. Chem. 1998, 273:34882-34886.
36. Jarmuszkiewicz W., Almeida A.M., Vercesi A.E., Sluse F.E., Sluse-Goffart C.M. Proton re-uptake partitioning between uncoupling protein and ATP synthase during benzohydroxamic acid-resistant state 3 respiration in tomato fruit mitochondria. J. Biol. Chem. 2000, 275:13315-13320.
37. 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 mitochondrial. J. Bioenerg. Biomembr. 2004, 36:493-502.
38. Swida-Barteczka A., Woyda-Ploszczyca A., Sluse F.E., Jarmuszkiewicz W. Uncoupling protein 1 inhibition by purine nucleotides is under control of the endogenous ubiquinone redox state. Biochem. J. 2009, 424:297-306.
39. Navet R., Douette P., Puttine-Marique F., Sluse-Goffart C.M., Jarmuszkiewicz W., Sluse F.E. Regulation of uncoupling protein activity in phosphorylating potato tuber mitochondria. FEBS Lett. 2005, 579:4437-4442.
40. Jarmuszkiewicz W., Swida A., Czarna M., Antos N., Sluse-Goffart C.M., Sluse F.E. In phosphorylating Acanthamoeba castellanii mitochondria the sensitivity of uncoupling protein activity to GTP depends on the redox state of quinone. J. Bioenerg. Biomembr. 2005, 37:97-107.
41. Rial E., Gonzalez-Barroso M.D.M., Fleury C., Iturrizaga S., Sanchis D., Jimenez-Jimenez J., Ricquier D., Goubern M., Bouilaud F. Retinoids activate proton transport by the uncoupling proteins UCP1 and UCP2. EMBO J. 1999, 18:5827-5833.
42. Smith A.M.O., Ratcliffe R.G., Sweetlove L.J. Activation and function of mitochondrial uncoupling protein in plants. J. Biol. Chem. 2004, 279:51944-51952.
43. Echtay K.S., Roussel D., St-Pierre J., Jekabson M.B., Cadenas S., Stuart J.A., Harper J.A., Roebuck S.J., Morrison A., Pickering S., Clapham J.C., Brand M.D. Superoxide activates mitochondrial uncoupling proteins. Nature 2002, 415:96-99.
44. 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. J. Biol. Chem. 2003, 278:22298-22302.
45. Echtay K.S., Esteves T.C., Pakay J.L., Jekabsons M.B., Lambert A.J., Portero-Otin M., Pamplona R., Vidal-Puig A., Wang S., Roebuck S.J., Brand M.D. A signaling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling. EMBO J. 2003, 22:4103-4110.
46. Sluse F.E., Jarmuszkiewicz W., Navet R., Douette P., Mathy G., Sluse-Goffart C.M. Mitochondrial UCPs: new insights into regulation and impact. Biochim. Biophys. Acta 2006, 1757:480-485.
47. Murphy M.P., Echtay K.S., Blaikie F.H., Asin-Cayuela J., Cocheme H.M., Green K., Buckingham J.A., Taylor E.R., Hurrell F., Hughes G., Miwa S., Cooper C.E., Svistunenko D.A., Smith R.A.J., 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. J. Biol. Chem. 2003, 278:48534-48545.
48. Esteves T.C., Brand M.D. The reactions catalysed by the mitochondrial uncoupling proteins UCP2 and UCP3. Biochim. Biophys. Acta 2005, 1709:35-44.
49. Siedow J.N., Umbach A.L. The mitochondrial cyanide-resistant oxidase: structural conservation and regulatory diversity. Biochim. Biophys. Acta 2000, 1459:432-439.
50. Jarmuszkiewicz W., Czarna M., Sluse F.E. Substrate kinetics of the Acanthamoeba castellanii alternative oxidase and effects of GMP. Biochim. Biophys. Acta 2005, 1708:71-78.
51. Woyda-Ploszczyca A.M., Sluse F.E., Jarmuszkiewicz W. Regulation of Acanthamoeba castellanii alternative oxidase activity by mutual exclusion of purine nucleotides; ATP's inhibitory effect. Biochim. Biophys. Acta 2009, 1787:264-271.
52. Milani G., Jarmuszkiewicz W., Sluse-Goffart C.M., Schreiber A.Z., Vercesi A.E., Sluse F.E. Respiratory network in mitochondria of Candida parapsilosis: ADP/O appraisal of the multiple electron pathways. FEBS Lett. 2001, 508:231-235.
53. Medentsev A.G., Arinbasarova A.Y., Golovchenko N.P., Akimenko V.K. Involvement of the alternative oxidase in respiration of Yarrowia lipolytica mitochondria is controlled by the activity of the cytochrome pathway. FEMS Yeast Res. 2002, 2:519-524.
54. Ott R., Chibale K., Anderson S., Chipeleme A., Chaudhuri M., Guerrah A., Colowick N., Hill G.C. Novel inhibitors of the trypanosome alternative oxidase inhibit Trypanosoma brucei brucei growth and respiration. Acta Trop. 2006, 100:172-184.
55. Colasante C., Diaz P.P., Clayton C., Voncken F. Mitochondrial carrier family inventory of Trypanosoma brucei brucei: identification, expression and subcellular localization. Mol. Bioch. Parasitol. 2009, 167:104-117.
56. 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. FEBS Lett. 1998, 433:237-240.
57. Minagawa N., Sakajo S., Yoshimoto A. Effects of unsaturated fatty acids on CN-resistant respiration of mitochondria isolated from Hansenula anomala. Biosci. Biotechnol. Biochem. 1992, 56:1342-1343.
58. Jarmuszkiewicz W., Sluse-Goffart C.M., Vercesi A.E., Sluse F.E. Alternative oxidase and uncoupling protein: thermogenesis versus cell energy balance. Biosci. Rep. 2001, 21:213-222.
59. Sluse F.E., Jarmuszkiewicz W. Activity and functional interaction of alternative oxidase and uncoupling protein in mitochondria from tomato fruit. Braz. J. Med. Biol. Res. 2000, 33:259-268.
60. Jarmuszkiewicz W., Czarna M., Swida A., Behrendt M. Uncoupling proteins in amoeboid eukaryotes, Acanthamoeba castellanii and Dictyostelium discoideum. Toxicol. Mech. Meth. 2004, 14:3-6.
61. Edwards S.W., Lloyd D. Changes in oxygen uptake rates, enzyme activities, cytochrome amounts and adenine nucleotide pool levels during growth of Acanthamoeba castellanii in batch culture. J. Gen. Microbiol. 1977, 102:135-144.
62. Czarna M., Sluse F.E., Jarmuszkiewicz W. Mitochondria function plasticity in Acanthamoeba castellanii during growth in batch culture. J. Bioenerg. Biomembr. 2007, 39:149-157.
63. Kicinska A., Swida A., Bednarczyk P., Koszela-Piotrowska I., Choma K., Dolowy K., Szewczyk A., Jarmuszkiewicz W. ATP-sensitive potassium channel in mitochondria of the eukaryotic microorganism, Acanthamoeba castellanii. J. Biol. Chem. 2007, 282(24):17433-17441.
64. Szewczyk A., Jarmuszkiewicz W., Kunz W.S. Mitochondrial potassium channels. IUBMB Life 2009, 61:134-143.
65. Jarmuszkiewicz W., Fraczyk O., Hryniewiecka L. Effect of growth at low temperature on the alternative pathway respiration in Acanthamoeba castellanii mitochondria. Acta Bioch. Pol. 2001, 48:729-737.
66. Skulachev V.P. Role of uncoupled and non-coupled oxidations in maintenance of safety low levels of oxygen and its one-electron reductants. Q. Rev. Biophys. 1996, 29:9895-9901.
67. Czarna M., Jarmuszkiewicz W. Activation of alternative oxidase and uncoupling protein lowers hydrogen peroxide formation in amoeba Acanthamoeba castellanii mitochondria. FEBS Lett. 2005, 579:3136-3140.
68. Jarmuszkiewicz W., Sluse-Goffart C.M., Hryniewiecka L., Michejda J., Sluse F.E. Electron partitioning between the two branching quinol-oxidizing pathways in Acanthamoeba castellanii mitochondria during steady-state state 3 respiration. J. Biol. Chem. 1998, 273:10174-10180.
69. Cheng S., Clancy C.J., Zhang Z., Hao B., Wang W., Iczkowski K.A., Pfaller M.A., Nguyen M.H. Uncoupling of oxidative phosphorylation enables Candida albinicans to resist killing by phagocytoses and persist in tissue. Cell. Microbiol. 2007, 9:492-501.