Molecular cloning of lamprey uncoupling protein and assessment of its uncoupling activity using a yeast heterologous expression system

Mitochondrion

Volumn 10, Issue 1, 2010, Pages 54-61

  Wang, Chen ^a   Sun, Guoxun ^a   Chen, Kun ^a   Lv, Zhiyuan ^a   Peng, Shiming ^a   Jiang, Xueyuan ^a   Xiang, Yang ^a   Zhang, Chenyu ^a  

^a NANJING UNIVERSITY   (China)

Author keywords

Lamprey; Molecular cloning; UCP; Uncoupling activity; Yeast expression system

Indexed keywords

GUANOSINE DIPHOSPHATE; UNCOUPLING PROTEIN; UNCOUPLING PROTEIN 1; UNCOUPLING PROTEIN 2; UNCOUPLING PROTEIN 3;

ARTICLE; CONTROLLED STUDY; HETEROLOGOUS EXPRESSION; LAMPREY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTON TRANSPORT; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CLONING, MOLECULAR; HUMANS; ION CHANNELS; KINETICS; LAMPREYS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; OXYGEN CONSUMPTION; PROTONS; RATS; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT;

PETROMYZONTIDAE; RATTUS; SACCHAROMYCES CEREVISIAE;

EID: 70450284460     PISSN: 15677249     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mito.2009.09.003     Document Type: Article

References (35)

1. 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
2. Arsenijevic D., Onuma H., Pecqueur C., Raimbault S., Manning B.S., Miroux B., Couplan E., Alves-Guerra M.-C., Goubern M., Surwit R., Bouillaud F., Richard D., Collins S., and Ricquier D. Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production. Nat. Genet. 26 (2000) 435-439
3. Boss O., Samec S., PaoloniGiacobino A., Rossier C., Dulloo A., Seydoux J., Muzzin P., and Giacobino J.P. Uncoupling protein-3: A new member of the mitochondrial carrier family with tissue-specific expression. FEBS Lett. 408 (1997) 39-42
4. Boss O., Hagen T., and Lowell B.B. Uncoupling proteins 2 and 3: potential regulators of mitochondrial energy metabolism. Diabetes 49 (2000) 143-156
5. Brand M.D., Brindle K.M., Buckingham J.A., Harper J.A., Rolfe D.F., and Stuart J.A. The significance and mechanism of mitochondrial proton conductance. Int. J. Obes. Relat. Metab. Disord. 23 (1999) S4-S11
6. Brand M.D., Affourtit C., Esteves T.C., Green K., Lambert A.J., Miwa S., Pakay J.L., and Parker N. Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins. Free Rad. Bio. Med. 37 (2004) 755-767
7. Cannon B., and Nedergaard J.A.N. Brown adipose tissue: function and physiological significance. Physiol. Rev. 84 (2004) 277-359
8. Echtay K.S., Roussel D., St-Pierre J., Jekabsons M.B., Cadenas S., Stuart J.A., Harper J.A., Roebuck S.J., Morrison A., Pickering S., Clapham J.C., and Brand M.D. Superoxide activates mitochondrial uncoupling proteins. Nature 415 (2002) 96-99
9. Echtay K.S., Esteves T.C., Pakay J.L., Jekabsons M.B., Lambert A.J., Portero-Otõân M., Pamplona R., Vidal-Puig A.J., Wang S., Roebuck S.J., and Brand M.D. A signalling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling. EMBO J. 22 (2003) 4103-4110
10. Escriva H., Manzon L., Youson J., and Laudet V. Analysis of lamprey and hagfish genes reveals a complex history of gene duplications during early vertebrate evolution. Mol. Biol. Evol. 19 (2002) 1440-1450
11. Esteves T.C., Echtay K.S., Jonassen T., Clarke C.F., and Brand M.D. Ubiquinone is not required for proton conductance by uncoupling protein 1 in yeast mitochondria. Biochem. J. 379 (2004) 309-315
12. Esteves T.C., Parker N., and Brand M.D. Synergy of fatty acid and reactive alkenal activation of proton conductance through uncoupling protein 1 in mitochondria. Biochem. J. 395 (2006) 619-628
13. Fleury C., Neverova M., Collins S., Raimbault S., Champigny O., LeviMeyrueis C., Bouillaud F., Seldin M.F., Surwit R.S., Ricquier D., and Warden C.H. Uncoupling protein-2: a novel gene linked to obesity and hyperinsulinemia. Nat. Genet. 15 (1997) 269-272
14. Harper J.A., Stuart J.A., Jekabsons M.B., Roussel D., Brindle K.M., Dickinson K., Jones R.B., and Brand M.D. Artifactual uncoupling by uncoupling protein 3 in yeast mitochondria at the concentrations found in mouse and rat skeletal-muscle mitochondria. Biochem. J. 36 (2002) 49-56
15. Jaburek M., Varecha M., Gimeno R.E., Dembski M., Jezek P., Zhang M., Burn P., Tartaglia L.A., and Garlid K.D. Transport function and regulation of mitochondrial uncoupling proteins 2 and 3. J. Biol. Chem. 274 (1999) 26003-26007
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. Jastroch M., Wuertz S., Kloas W., and Klingenspor M. Uncoupling protein 1 in fish uncovers an ancient evolutionary history of mammalian nonshivering thermogenesis. Physiol. Genomics 22 (2005) 150-156
18. Laloi M., Klein M., Riesmeier J.W., Müller-Röber B., Fleury C., Bouillaud F., and Ricquier D. A plant cold-induced uncoupling protein. Nature 389 (1997) 135-136
19. Murdza-Inglis D.L., Patel H.V., Freeman K.B., Jezek P., Orosz D.E., and Garlid K.D. Functional reconstitution of rat uncoupling protein following its high level expression in yeast. J. Biol. Chem. 266 (1991) 11871-11875
20. Murphy M.P., Echtay K.S., Blaikie F.H., Asin-Cayuela J., Cochemé 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., and 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 α-phenyl-N-tert-butylnitrone. J. Biol. Chem. 278 (2003) 48534-48545
21. Nicholls D.G., and Locke R.M. Thermogenic mechanisms in brown fat. Physiol. Rev. 64 (1984) 1-64
22. Osorio J., and Retaux S. The lamprey in evolutionary studies. Dev. Genes Evol. 218 (2008) 221-235
23. Porras A., Peñas M., Fernández M., and Benito M. Development of the uncoupling protein in the rat brown-adipose tissue during the perinatal period. Eur. J. Biochem. 187 (1990) 671-675
24. Rial E., González-Barroso 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
25. 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. Bioenerg. Biomembr. 34 (2002) 165-176
26. Saito S., Saito C.T., and Shingai R. Adaptive evolution of the uncoupling protein 1 gene contributed to the acquisition of novel nonshivering thermogenesis in ancestral eutherian mammals. Gene 408 (2008) 37-44
27. Stuart J.A., Harper J.A., Brindle K.M., Jekabsons M.B., and Brand M.D. A mitochondrial uncoupling artifact can be caused by expression of uncoupling protein 1 in yeast. Biochem. J. 356 (2001) 779-789
28. Stuart J.A., Harper J.A., Brindle K.M., Jekabsons M.B., and Brand M.D. Physiological levels of mammalian uncoupling protein 2 do not uncouple yeast mitochondria. J. Biol. Chem. 276 (2001) 18633-18639
29. 2+ uniport. Nat. Cell Biol. 9 (2007) 445-452
30. Vidal-Puig A.J., Grujic D., Zhang C.Y., Hagen T., Boss O., Ido Y., Szczepanik A., Wade J., Mootha V., Cortright R., Muoio D.M., and Lowell B.B. Energy metabolism in uncoupling protein 3 gene knockout mice. J. Biol. Chem. 275 (2000) 16258-16266
31. Vozza A., Blanco E., Palmieri L., and Palmieri F. Identification of the mitochondrial GTP/GDP transporter in Saccharomyces cerevisiae. J. Biol. Chem. 279 (2004) 20850-20857
32. Walker J.E., and Runswick M.J. The mitochondrial transport protein superfamily. J. Bioenerg. Biomembr. 25 (1993) 435-446
33. Yu X.X., Mao W.G., Zhong A., Schow P., Brush J., Sherwood S.W., Adams S.H., and Pan G.H. Characterization of novel UCP5/BMCP1 isoforms and differential regulation of UCP4 and UCP5 expression through dietary or temperature manipulation. FASEB J. 14 (2000) 1611-1618
34. Zhang C.Y., Hagen T., Mootha V.K., Slieker L.J., and Lowell B.B. Assessment of uncoupling activity of uncoupling protein 3 using a yeast heterologous expression system. FEBS Lett. 449 (1999) 129-134
35. Zhang C.Y., Baffy G., Perret P., Krauss S., Peroni O., Grujic D., Hagen T., Vidal-Puig A.J., Boss O., Kim Y.B., Zheng X.X., Wheeler M.B., Shulman G.I., Chan C.B., and Lowell B.B. Uncoupling protein-2 negatively regulates insulin secretion and is a major link between obesity, beta cell dysfunction, and type 2 diabetes. Cell 105 (2001) 745-755