Identification of the mitochondrial carrier that provides Yarrowia lipolytica with a fatty acid-induced and nucleotide-sensitive uncoupling protein-like activity

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1797, Issue 1, 2010, Pages 81-88

  Luévano Martínez, Luis A ^a   Moyano, Eva ^b   de Lacoba, Mario García ^b   Rial, Eduardo ^b   Uribe Carvajal, Salvador ^a  

^a INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

Energy dissipation; Heterologous expression; Mitochondria; UCP; Uncoupling protein; Yarrowia lipolytica; Yeast

Indexed keywords

CARRIER PROTEIN; DICARBOXYLIC ACID; FATTY ACID; FATTY ACID DERIVATIVE; GUANOSINE DIPHOSPHATE; LINOLEIC ACID; MITOCHONDRIAL PROTEIN; NUCLEOTIDE; NUCLEOTIDE DERIVATIVE; OXALOACETIC ACID; UNCOUPLING PROTEIN;

ARTICLE; BIOENERGY; COMPUTER MODEL; CONTROLLED STUDY; FUNGAL GENE; GROWTH CURVE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; STEADY STATE; YARROWIA LIPOLYTICA;

BIOLOGICAL TRANSPORT; FATTY ACIDS; GUANOSINE DIPHOSPHATE; ION CHANNELS; MEMBRANE POTENTIALS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; OXYGEN CONSUMPTION; PHYLOGENY; SUCCINATES; SULFATES; VANCOMYCIN; YARROWIA;

ANIMALIA; EUKARYOTA; FUNGI; PROTOZOA; SACCHAROMYCES CEREVISIAE; YARROWIA LIPOLYTICA;

EID: 71749101823     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2009.09.003     Document Type: Article

References (61)

1. Palmieri F. The mitochondrial transporter family (SLC25): physiological and pathological implications. Pflugers Arch. 447 (2004) 689-709
2. Bouillaud F., Couplan E., Pecqueur C., and Ricquier D. Homologues of the uncoupling protein from brown adipose tissue (UCP1): UCP2, UCP3, BMCP1 and UCP4. Biochim. Biophys. Acta 1504 (2001) 107-119
3. Rial E., and González-Barroso MM. Physiological regulation of the transport activity in the uncoupling proteins UCP1 and UCP2. Biochim. Biophys. Acta 1504 (2001) 70-81
4. Cannon B. Uncoupling proteins: a role in protection against reactive oxygen species-or not?. Biochim. Biophys. Acta 1757 (2006) 449-458
5. Echtay K.S. Mitochondrial uncoupling proteins-what is their physiological role?. Free Radic. Biol. Med. 43 (2007) 1351-1371
6. Krauss S., Zhang C.Y., and Lowell B.B. The mitochondrial uncoupling-protein homologues. Nat. Rev., Mol. Cell Biol. 6 (2005) 248-261
7. Vercesi A.E., Borecký J., Maia I.G., Arruda P., Cuccovia I.M., and Chaimovich H. Plant uncoupling mitochondrial proteins. Annu. Rev. Plant Biol. 57 (2006) 383-404
8. Negre-Salvayre A., Hirtz C., Carrera G., Cazenave R., Troly M., Salvayre R., Penicaud L., and Casteilla L. A role for uncoupling protein-2 as a regulator of mitochondrial hydrogen peroxide generation. FASEB J. 11 (1997) 809-815
9. Rial E., González-Barroso M.M., Fleury C., Iturrizaga S., Sanchis D., Jiménez-Jiménez J., Ricquier D., Goubern M., and Bouillaud F. Retinoids activate proton transport by the uncoupling proteins UCP1 and UCP2. EMBO J. 18 (1999) 5827-5833
10. Echtay K., Esteves T., Pakay J., Jekabsons M., Lambert A., Portero-Otín M., Pamplona R., Vidal-Puig A., Wang S., Roebuck S., and Brand M.D. A signalling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling. EMBO J. 22 (2003) 4103-4110
11. Brand M.D., Affourtit C., Esteves T.C., Green K., Lambert A.J., Miwa S., Pakay J., and Parker N. Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins. Free Radic Biol. Med. 37 (2004) 755-767
12. Esteves T.C., and Brand M.D. The reactions catalysed by the mitochondrial uncoupling proteins UCP2 and UCP3. Biochim. Biophys. Acta 1709 (2005) 34-44
13. Vercesi A.E., Martins I.S., Silva M.A., Leite H.M., Cuccovia I.M., and Chaimovich H. PUMPing plants. Nature 375 (1995) 24
14. Onda Y., Kato Y., Abe Y., Ito T., Morohashi M., Ito Y., Ichikawa M., Matsukawa K., Kakizaki Y., Koiwa H., and Ito K. Functional coexpression of the mitochondrial alternative oxidase and uncoupling protein underlies thermoregulation in the thermogenic florets of skunk cabbage. Plant Physiol. 146 (2008) 636-645
15. Jarmuszkiewicz W., Sluse-Goffart C.M., Hryniewiecka L., and Sluse F.E. Identification and characterization of a protozoan uncoupling protein in Acanthamoeba castellanii. J. Biol. Chem. 274 (1999) 23198-23202
16. Jarmuszkiewicz W., Milani G., Fortes F., Schreiber A.Z., Sluse F.E., and Vercesi A.E. First evidence and characterization of an uncoupling protein in fungi kingdom: CpUCP of Candida parapsilosis. FEBS Lett. 467 (2000) 145-149
17. Tudella V.G., Curti C., Soriani F.M., Santos A.C., and Uyemura S.A. In situ evidence of an alternative oxidase and an uncoupling protein in the respiratory chain of Aspergillus fumigatus. Int. J. Biochem. Cell Biol. 36 (2003) 162-172
18. Cavalheiro R.A., Fortes F., Borecký J., Faustinoni V.C., Schreiber A.Z., and Vercesi A.E. Respiration, oxidative phosphorylation, and uncoupling protein in Candida albicans. Braz. J. Med. Biol. Res. 37 (2004) 1455
19. Uyemura S.A., Luo S., Vieira M., Moreno S.N., and Docampo R. Oxidative phosphorylation and rotenone-insensitive malate- and NADH-quinone oxidoreductases in Plasmodium yoelii yoelii mitochondria in situ. J. Biol. Chem. 279 (2004) 385-393
20. Jarmuszkiewicz W., Behrendt M., Navet R., and 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. 532 (2002) 459-464
21. Uyemura S.A., Luo S., Moreno S.N., and Docampo R. Oxidative phosphorylation, Ca(2+) transport, and fatty acid-induced uncoupling in malaria parasites mitochondria. J. Biol. Chem. 275 (2000) 9709-9715
22. Jarmuszkiewicz W., Antos N., Swida A., Czarna M., and 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. 569 (2004) 178-184
23. Sluse F.E., and Jarmuszkiewicz W. Uncoupling proteins outside the animal and plant kingdoms: functional and evolutionary aspects. FEBS Lett. 510 (2002) 117-120
24. Czarna M., and Jarmuszkiewicz W. Activation of alternative oxidase and uncoupling protein lowers hydrogen peroxide formation in amoeba Acanthamoeba castellanii mitochondria. FEBS Lett. 579 (2005) 3136-3140
25. Guérin B., Labbe P., and Somlo M. Preparation of yeast mitochondria (Saccharomyces cerevisiae) with good P/O and respiratory control ratios. Methods Enzymol. 55 (1979) 149-159
26. Åkerman K.E.O., and Wikström M.K. Safranine as a probe of the mitochondrial membrane potential. FEBS Lett. 68 (1976) 191-197
27. Richieri G.V., Anel A., and Kleinfeld A.M. Interactions of long-chain fatty acids and albumin: determination of free fatty acid levels using the fluorescent probe ADIFAB. Biochemistry 32 (1993) 7574-7580
28. Palmieri L., Vozza A., Agrimi G., De Marco V., Runswick M.J., Palmieri F., and Walker J.E. Identification of the yeast mitochondrial transporter for oxaloacetate and sulfate. J. Biol. Chem. 274 (1999) 22184-22190
29. Rial E., and Zardoya R. Oxidative stress, thermogenesis and evolution of uncoupling proteins. J. Biol. 8 (2009) 58
30. Katoh K., and Toh H. Recent developments in the MAFFT multiple sequence alignment program. Brief. Bioinform. 9 (2008) 286-298
31. Guindon S., Gascuel O., and simple A. fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52 (2003) 696-704
32. Stamatakis A., Ludwig T., and Meier H. RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21 (2005) 456-463
33. Shimodaira H., and Hasegawa M. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17 (2001) 1246-1247
34. Linton J.D., and Rye A.L. The relationship between the energetic efficiency in different micro-organisms and the rate and type of metabolite overproduced. J. Ind. Microbiol. 4 (1989) 85-96
35. Linton J.D. Metabolite production and growth efficiency. Antoine van Leeuwenhoek 60 (1991) 293-311
36. Gallmetzer M., and Burgstaller W. Efflux of organic acids in Penicillium simplicissimum is an energy-spilling process, adjusting the catabolic carbon flow to the nutrient supply and the activity of catabolic pathways. Microbiology 148 (2002) 1143-1149
37. Barth G., and Gaillardin C. Physiology and genetics of the dimorphic fungus Yarrowia lipolytica. FEMS Microbiol. Rev. 19 (1997) 219-237
38. Athenstaedt K., Jolivet P., Boulard C., Zivy M., Negroni L., Nicaud J.M., and Chardot T. Lipid particle composition of the yeast Yarrowia lipolytica depends on the carbon source. Proteomics 6 (2006) 1450-1459
39. Weigle D.S., Selfridge L.E., Schwartz M.W., Seeley R.J., Cummings D.E., Havel P.J., Kuijper J.L., and Bertran del Rio H. Elevated free fatty acids induce uncoupling protein 3 expression in muscle, a potential explanation for the effect of fasting. Diabetes 47 (1998) 298-302
40. Bouillaud F. UCP2, not a physiologically relevant uncoupler but a glucose sparing switch impacting ROS production and glucose sensing. Biochim. Biophys. Acta 1787 (2009) 377-383
41. Skulachev V.P. "Mild" uncoupling of mitochondria. Biosci. Rep. 17 (1997) 347-366
42. Seifert E.L., Bézaire V., Estey C., and Harper M.E. Essential role for uncoupling protein-3 in mitochondrial adaptation to fasting but not in fatty acid oxidation or fatty acid anion export. J. Biol. Chem. 283 (2008) 25124-25131
43. Dujon B., Sherman D., Fischer G., Durrens P., Casaregola S., Lafontaine I., de Montigny J., Marck C., Neuveglise C., Talla E., Goffard N., Frangeul L., Aigle M., Anthouard V., Babour A., Barbe V., Barnay S., Blanchin S., Beckerich J.-M., Beyne E., Bleykasten C., Boisrame A., Boyer J., Cattolico L., Confanioleri F., de Daruvar A., Despons L., Fabre E., Fairhead C., Ferry-Dumazet H., Groppi A., Hantraye F., Hennequin C., Jauniaux N., Joyet P., Kachouri R., Kerrest A., Koszul R., Lemaire M., Lesur I., Ma L., Muller H., Nicaud J.-M., Nikolski M., Oztas S., Ozier-Kalogeropoulos O., Pellenz S., Potier S., Richard G.-F., Straub M.-L., Suleau A., Swennen D., Tekaia F., Wesolowski-Louvel M., Westhof E., Wirth B., Zeniou-Meyer M., Zivanovic I., Bolotin-Fukuhara M., Thierry A., Bouchier C., Caudron B., Scarpelli C., Gaillardin C., Weissenbach J., Wincker P., and Souciet J.-L. Genome evolution in yeasts. Nature 430 (2004) 35-44
44. Arechaga I., Raimbault S., Prieto S., Levi-Meyrueis C., Zaragoza P., Miroux B., Ricquier D., Bouillaud F., and Rial E. Cysteine residues are not essential for uncoupling protein function. Biochem. J. 296 (1993) 693-700
45. Roussel D., Harding M., Runswick M.J., Walker J.E., and Brand M.D. Does any yeast mitochondrial carrier have a native uncoupling protein function?. J. Bioener. Biomembr. 34 (2002) 165-176
46. Palmieri L., Lasorsa F.M., Vozza A., Agrimi G., Fiermonte G., Runswick M.J., Walker J.E., and Palmieri F. Identification and functions of new transporters in yeast mitochondria. Biochim. Biophys. Acta 1459 (2000) 363-369
47. Rial E., Aguirregoitia E., Jiménez-Jiménez J., and Ledesma A. Alkylsulfonates activate the uncoupling protein UCP1: implications for the transport mechanism. Biochim. Biophys. Acta 1608 (2004) 122-130
48. González-Barroso M.M., Fleury C., Bouillaud F., Nicholls D.G., and Rial E. The uncoupling protein UCP1 does not increase the proton conductance of the inner mitochondrial membrane by functioning as a fatty acid anion transporter. J. Biol. Chem. 273 (1998) 15528-15532
49. Borecky J., Nogueira F.T.S., de Oliveira K.A.P., Maia I.G., Vercesi A., and Arruda P. The plant energy-dissipating mitochondrial systems: depicting the genomic structure and the expression profiles of the gene families of uncoupling protein and alternative oxidase in monocots and dicots. J. Exp. Bot. 57 (2006) 849-864
50. Palmieri L., Picault N., Arrigoni R., Besin E., Palmieri F., and Hodges M. Molecular identification of the three Arabidopsis thaliana mitochondrial dicarboxylate carrier isoforms: organ distribution, bacterial expression, reconstitution into liposomes and functional characterization. Biochem. J. 410 (2008) 621-629
51. Jarmuszkiewicz W., Almeida A.M., Vercesi A.E., Sluse F.E., and 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. 273 (1998) 34882-34886
52. Jarmuszkiewicz W., Swida A., Czarna M., Antos N., Sluse-Goffart C.M., Sluse F.E., and Vercesi A.E. In phosphorylating Acanthamoeba castellanii mitochondria the sensitivity of uncoupling protein activity to GTP depends on the redox state of quinone. J. Bioener. Biomemb. 37 (2005) 97-107
53. Jarmuszkiewicz W., Sluse-Goffart C.M., Vercesi A.E., and Sluse F.E. Alternative oxidase and uncoupling protein: thermogenesis versus cell energy balance. Biosci. Rep. 21 (2001) 213-222
54. Cheng S., Clancy C.J., Zhang Z., Hao B., Wang W., Iczkowski K.A., Pfaller M.A., and Nguyen M.H. Uncoupling of oxidative phosphorylation enables Candida albicans to resist killing by phagocytes and persist in tissue. Cell. Microbiol. 9 (2007) 492-501
55. Barth G., and Gaillardin C. In: Wolf W.K. (Ed). Yarrowia lipolytica. pp. 313-388. In "Non-conventional Yeast in Biotechnology" Vol 1 (1996) Springer-Verlag, Berlin, Germany
56. Beopoulos A., Mrozova Z., Thevenieau F., Le Dall M.T., Hapala I., Papanikolaou S., Chardot T., and Nicaud J.M. Control of lipid accumulation in the yeast Yarrowia lipolytica. App. Environ. Microbiol. 74 (2008) 7779-7789
57. Mlíckova K., Roux E., Athenstaedt K., d'Andrea S., Daum G., Chardot T., and Nicaud J.M. Lipid accumulation, lipid body formation, and acyl coenzyme A oxidases of the yeast Yarrowia lipolytica. App. Environ. Microbiol. 70 (2004) 3918-3924
58. Maggio-Hall L.A., and Keller N.P. Mitochondrial beta-oxidation in Aspergillus nidulans. Mol. Microbiol. 54 (2005) 1173-1185
59. Feron G., Blin- Perrin C., Krasniewski I., Mauvais G., and Lherminier J. Metabolism of fatty acid in yeast: characterisation of beta-oxidation and ultrastructural changes in the genus Sporidiobolus sp. cultivated on ricinoleic acid methyl ester. FEMS Microbiol. Lett. 250 (2005) 63-69
60. Jastroch M., Buckingham J.A., Helwig M., Klingenspor M., and Brand M.D. Functional characterization of UCP1 in the common carp: uncoupling activity in liver mitochondria and cold-induced expression in the brain. J. Comp. Physiol. 177 (2007) 743-752
61. Jiménez-Jiménez J., Zardoya R., Ledesma A., García de Lacoba M., Zaragoza P., González-Barroso M.M., and Rial E. Evolutionarily distinct residues in the uncoupling protein UCP1 are essential for its characteristic basal proton conductance. J. Mol. Biol. 359 (2006) 1010-1022