Toward understanding the mechanism of ion transport activity of neuronal uncoupling proteins UCP2, UCP4, and UCP5

Biochemistry

Volumn 51, Issue 19, 2012, Pages 4004-4014

  Hoang, Tuan ^a,b   Smith, Matthew D ^a,b   Jelokhani Niaraki, Masoud ^a,b  

^a WILFRID LAURIER UNIVERSITY   (Canada)

^b UNIVERSITY OF GUELPH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; ANION TRANSPORT; BIOCHEMICAL STUDIES; CARDIOLIPINS; CENTRAL NERVOUS SYSTEMS; FUNCTIONAL PROPERTIES; ION TRANSPORTS; LIPID MEMBRANES; LOW LEVEL; PHYSIOLOGICAL FUNCTIONS; PURINE NUCLEOTIDES; STRUCTURE-FUNCTION RELATIONSHIP; TRANSMEMBRANES; TRANSPORT ACTIVITY; UNCOUPLING PROTEINS;

AMINO ACIDS; CHLORINE COMPOUNDS; CIRCULAR DICHROISM SPECTROSCOPY; ESCHERICHIA COLI; PHOSPHOLIPIDS; PHYSIOLOGY; PROTEINS; PROTONS; TRANSPORT PROPERTIES;

IONS;

CARDIOLIPIN; CHLORIDE; FATTY ACID; PROTON; UCP4 PROTEIN; UCP5 PROTEIN; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN; UNCOUPLING PROTEIN 2;

AMINO ACID SEQUENCE; ARTICLE; CIRCULAR DICHROISM; COMPARATIVE STUDY; CONTROLLED STUDY; ESCHERICHIA COLI; HUMAN; ION TRANSPORT; PRIORITY JOURNAL; PROTEIN ISOLATION;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CARDIOLIPINS; CHLORIDES; CIRCULAR DICHROISM; ESCHERICHIA COLI; ION CHANNELS; ION TRANSPORT; LIPOSOMES; MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL PROTEINS; NERVE TISSUE PROTEINS; NEURONS; PROTEIN CONFORMATION; PROTONS; RECOMBINANT PROTEINS;

ESCHERICHIA COLI;

EID: 84861134135     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3003378     Document Type: Article

References (53)

1. Krauss, S., Zhang, C. Y., and Lowell, B. B. (2005) The mitochondrial uncoupling protein homologs Nat. Rev. Mol. Cell Biol. 6, 248-261
2. Echtay, K. S. (2007) Mitochondrial uncoupling proteins: What is their physiological role? Free Radical Biol. Med. 43, 1351-1371
3. Berardi, M. J., Shih, W. M., Harrison, S. C., and Chou, J. J. (2011) Mitochondrial uncoupling protein 2 structure determined by NMR molecular fragment searching Nature 476, 109-113
4. Andrews, Z. B., Diano, S., and Horvath, T. L. (2005) Mitochondrial uncoupling proteins in the CNS: In support of function and survival Nat. Rev. Neurosci. 6, 829-840
5. 10 J. Biol. Chem. 278, 25825-25831
6. + transporters and highly nucleotide sensitive when activated by coenzyme Q (ubiquinone) Proc. Natl. Acad. Sci. U.S.A. 98, 1416-1421
7. Jezek, P. and Urbankova, E. (2000) Specific sequence motifs of mitochondrial uncoupling proteins IUBMB Life 49, 63-70
8. Mao, W., Yu, X. X., Zhong, A., Li, W., Brush, J., Sherwood, S. W., Adams, S. H., and Pan, G. (1999) UCP4, a novel brain-specific mitochondrial protein that reduces membrane potential in mammalian cells FEBS Lett. 443, 326-330
9. Zhang, M., Wang, B., Ni, N. Y. H., Liu, F., Fei, L., Pan, X. Q., Guo, M., Chen, R. H., and Guo, X. R. (2006) Overexpression of uncoupling protein 4 promotes proliferation and inhibits apoptosis and differentiation of preadipocytes Life Sci. 79, 1428-1435
10. Sanchis, D., Fleury, C., Chomiki, N., Goubern, M., Huang, Q., Neverova, M., Gregoire, F., Easlick, J., Raimbault, S., Levi-Meyrueis, C., Miroux, B., Collins, S., Seldin, M., Richard, D., Warden, C., Bouillaud, F., and 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
11. Fridell, Y. W. C., Sanchez-Blanco, A., Silvia, B. A., and Helfand, S. L. (2004) Functional characterization of a Drosophila mitochondrial uncoupling protein J. Bioenerg. Biomembr. 36, 219-228
12. Yu, X. X., Mao, W., Zhong, A., Schow, P., Brush, J., Sherwood, S. W., Adams, S. H., and Pan, G. (2000) Characterization of novel UCP5/BMCP1 isoforms and differential regulation of UCP4 and UCP5 expression through dietary or temperature manipulation FASEB J. 14, 1611-1618
13. Ledesma, A., Lacoba, M. G., and Rial, E. (2002) The mitochondrial uncoupling proteins Genome Biol. 3, 3015.1-3015.9
14. Kim-Han, J. S., Reichert, S. A., Quick, K. L., and Dugan, L. L. (2001) BMCP1: A mitochondrial uncoupling protein in neurons which regulates mitochondrial function and oxidant production J. Neurochem. 79, 658-668
15. Mattson, M. P. and Liu, D. (2003) Mitochondrial potassium channels and uncoupling proteins in synaptic plasticity and neuronal cell death Biochem. Biophys. Res. Commun. 304, 539-549
16. + and dopamine-induced oxidative stress, mitochondrial depolarization, and ATP deficiency in neurons, and is interlinked with UCP2 expression Free Radical Biol. Med. 46, 810-820
17. + and dopamine toxicity Free Radical Biol. Med. 49, 1023-1035
18. Nury, H., Dahout-Gonzalez, C., Trezeguet, V., Lauquin, G., Brandolin, G., and Pebay-Peyroula, E. (2005) Structural basis for lipid-mediated interactions between mitochondrial ADP/ATP carrier monomers FEBS Lett. 579, 6031-6036
19. Kagan, V. E., Tyurin, V. A., Jiang, J., Tyurina, Y. Y., Ritov, V. B., Amoscato, A. A., Osipov, A. N., Belikova, N. A., Karpalov, A. A., Kini, V., Vlasova, I. I., Zhao, Q., Zou, M., Di, P., Svistunenko, D. A., Kurnikov, I. V., and Borisenko, G. G. (2005) Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors Nat. Chem. Biol. 1, 223-232
20. 31P nuclear magnetic resonance spectroscopy J. Biol. Chem. 265, 19434-19440
21. Pfeiffer, K., Gohli, V., Stuart, R. A., Hunte, C., Brandt, U., Greenberg, M. L., and Schagger, H. (2003) Cardiolipin stabilizes respiratory chain supercomplexes J. Biol. Chem. 278, 52873-52880
22. Haines, T. H. (2009) A new look at cardiolipin Biochim. Biophys. Acta 1788, 1997-2002
23. Klingenberg, M. (2009) Cardiolipin and mitochondrial carriers Biochim. Biophys. Acta 1788, 2048-2058
24. Ivanova, M. V., Hoang, T., McSorley, F. R., Krnac, G., Smith, M. D., and Jelokhani-Niaraki, M. (2010) A comparative study on conformation and ligand binding of the neuronal uncoupling proteins Biochemistry 49, 512-521
25. Jelokhani-Niaraki, M., Ivanova, M. V., McIntyre, B. L., Newman, C. L., McSorley, F. R., Young, E. K., and Smith, M. D. (2008) A CD study of uncoupling protein-1 and its transmembrane and matrix-loop domains Biochem. J. 411, 593-603
26. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951) Protein measurement with the folin phenol reagent J. Biol. Chem. 193, 265-275
27. Whitmore, L. and Wallace, B. A. (2004) Dichroweb: An online server for protein secondary structure analyses from circular dichroism spectroscopic data Nucleic Acids Res. 32, W668-W673
28. Lees, J. G., Miles, A. J., Wien, F., and Wallace, B. A. (2006) A reference database for circular dichroism spectroscopy covering fold and secondary structure space Bioinformatics 22, 1955-1962
29. Orosz, D. E. and Garlid, K. D. (1993) A sensitive new fluorescence assay for measuring proton transport across liposomal membranes Anal. Biochem. 210, 7-15
30. Poirot, O., O'Toole, E., and Notredame, C. (2003) Tcoffee@igs: A web server for computing, evaluating and combining multiple sequence alignments Nucleic Acids Res. 31, 3503-3506
31. Notredame, C., Higgins, D. G., and Heringa, J. (2000) T-Coffee: A novel method for fast and accurate multiple sequence alignment J. Mol. Biol. 302, 205-217
32. Sali, A., Potteron, L., Yuan, F., Vlijimen, H. V., and Karplus, M. (1995) Evaluation of comparative protein folding by MODELLER Proteins 23, 318-326
33. DeLano, W. L. (2002) PyMOL, DeLano Scientific, San Carlos, CA.
34. Echtay, K. S., Winkler, E., Bienengraeber, M., and Klingenberg, M. (2000) Site-directed mutagenesis identifies residues in uncoupling protein (UCP1) involved in three different functions Biochemistry 39, 3311-3317
35. Klingenberg, M. and Echtay, K. S. (2001) Uncoupling proteins: The issues from a biochemist point of view Biochim. Biophys. Acta 1504, 128-143
36. Garlid, K. D., Orosz, D. E., Modriansky, M., Vassanelli, S., and Jezek, P. (1996) On the mechanism of fatty acid-induced proton transport by mitochondrial uncoupling protein J. Biol. Chem. 271, 2615-2620
37. Huang, S. G. and Klingenberg, M. (1996) Chloride channel properties of the uncoupling protein from brown adipose tissue mitochondria: A patch-clamp study Biochemistry 35, 16806-16814
38. Yamaguchi, H., Jelokhani-Niaraki, M., and Kodama, H. (2004) Second transmembrane domain of human uncoupling protein 2 is essential for its anion channel formation FEBS Lett. 577, 299-304
39. Mao, D. and Wallace, B. A. (1984) Differential light scattering and absorption flattening optical effects are minimal in the circular dichroism spectra of small unilamellar vesicles Biochemistry 23, 2667-2673
40. Acehan, D., Malhotra, A., Xu, Y., Ren, M., Stokes, D. L., and Schlame, M. (2011) Cardiolipin affects the supramolecular organization of ATP synthase in mitochondria Biophys. J. 100, 2184-2192
41. Smorodchenko, A., Ruppercht, A., Sarilova, I., Ninnemann, O., Brauer, A. U., Franke, K., Schumacher, S., Techritz, S., Nitsch, R., Schuelke, M., and Pohl, E. E. (2009) Comparative analysis of uncoupling protein 4 distribution in various tissues under physiological conditions and during development Biochim. Biophys. Acta 1788, 2309-2319
42. Sauer, H., Wartenberg, M., and Hescheler, J. (2001) Reactive oxygen species as intracellular messengers during cell growth and differentiation Cell. Physiol. Biochem. 11, 173-186
43. Echtay, K. S., Bienengraeber, M., and Klingenberg, M. (2001) Role of intrahelical arginine residues in functional properties of uncoupling protein (UCP1) Biochemistry 40, 5243-5248
44. Mende, P., Kolbe, H. V., Kadenbach, B., Stipani, I., and Palmieri, F. (1982) Reconstitution of the isolated phosphate-transport system of pig-heart mitochondria Eur. J. Biochem. 128, 91-95
45. 31P nuclear magnetic resonance Biochemistry 24, 3821-3826
46. Kadenbach, B., Mende, P., Kolbe, H. V., Stipani, I., and Palmieri, F. (1982) The mitochondrial phosphate carrier has essential requirement for cardiolipin FEBS Lett. 139, 109-112
47. Hoffman, B., Stockl, A., Schlame, M., Beyer, K., and Klingenberg, M. (1994) The reconstituted ADP/ATP carrier activity has an absolute requirement for cardiolipin as shown in cysteine mutants J. Biol. Chem. 269, 1940-1944
48. Noel, H. and Pande, S. V. (1986) An essential requirement of cardiolipin for mitochondrial carnitine acylcarnitine translocase activity. Lipid requirement of carnitine acylcarnitine translocase Eur. J. Biochem. 155, 99-102
49. Modriansky, M., Murdza-Inglis, D. L., Patel, H. V., Freeman, K. B., and Garlid, K. D. (1997) Identification by site-directed mutagenesis of three arginines in uncoupling protein that are essential for nucleotide binding and inhibition J. Biol. Chem. 272, 24759-24762
50. Robinson, A. J., Overy, C., and Kunji, E. R. S. (2008) The mechanism of transport by mitochondrial carriers based on analysis of symmetry Proc. Natl. Acad. Sci. U.S.A. 105, 17766-17771
51. Nury, H., Dahout-Gonzalez, C., Trezeguet, V., Lauquin, G., Brandolin, G., and Pebay-Peyroula, E. (2006) Relations between structure and function of the mitochondrial ADP/ATP carrier Annu. Rev. Biochem. 75, 713-741
52. Bamber, L., Harding, M., Monne, M., Slotboom, D.-J., and Kunji, E. R. S. (2007) The yeast mitochondrial ADP/ATP carrier functions as a monomer in mitochondrial membranes Proc. Natl. Acad. Sci. U.S.A. 104, 10830-10834
53. Nury, H., Manon, F., Arnou, B., Maire, M., Pebay-Peyroula, E., and Ebel, C. (2008) Mitochondrial bovine ADP/ATP carrier in detergent is predominantly monomeric but also forms multimeric species Biochemistry 47, 12319-12331