Uncoupling protein-3 sensitizes cells to mitochondrial-dependent stimulus of apoptosis

Journal of Cellular Physiology

Volumn 201, Issue 2, 2004, Pages 294-304

  Dejean, Laurent ^a   Ćamara, Yolanda ^a   Sibille, Brigitte ^b   Solanes, Gemma ^a   Villarroya, Francesc ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b UNIVERSITÉ LYON 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE DIPHOSPHATE; PROTEIN BAX; PROTEIN BCL 2; UNCOUPLING PROTEIN 3;

APOPTOSIS; ARTICLE; CHANNEL GATING; HUMAN; HUMAN CELL; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSITIZATION;

APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, WESTERN; CARRIER PROTEINS; CASPASE 3; CASPASE 9; CASPASES; CELL RESPIRATION; CYTOCHROMES C; ENERGY METABOLISM; ENZYME ACTIVATION; GENE EXPRESSION; GUANOSINE DIPHOSPHATE; HUMANS; ION CHANNELS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-BCL-2; TRANSFECTION;

EID: 4644301489     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.20048     Document Type: Article

References (54)

1. Antonsson B. 2001. Bax and other pro-apoptotic Bcl-2 family "killer-proteins" and their victim the mitochondrion. Cell Tissue Res 306:347-361.
2. Armstrong JS, Steinauer KK, French J, Killoran PL, Walleczek J, Kochanski J, Knox SJ. 2001. Bcl-2 inhibits apoptosis induced by mitochondrial uncoupling but does not prevent mitochondrial transmembrane depolarization. Exp Cell Res 262:170-179.
3. Arsenijevic D, Onuma H, Pecqueur C, Raimbault S, Manning BS, Miroux B, Couplan E, Alves-Guerra MC, Goubern M, Surwit R, Bouillaud F, Richard D, Collins S, Ricquier D. 2000. Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production. Nat Genet 26:435-439.
4. Bing C, Brown M, King P, Collins P, Tisdale MJ, Williams G. 2000. Increased gene expression of brown fat uncoupling protein (UCP)1 and skeletal muscle UCP2 and UCP3 in MAC16-induced cancer cachexia. Cancer Res 60:2405-2410.
5. Bishopric NH, Andreka P, Slepak T, Webster KA. 2001. Molecular mechanisms of apoptosis in the cardiac myocyte. Curr Opin Pharmacol 1:141-150.
6. Boss O, Samec S, Paoloni-Giacobino A, Dossier C, Dulloo A, Seydoux J, Muzzin P, Giacobino JP. 1997. Uncoupling protein-3: A new member of the mitochondrial carrier family with tissue-specific expression. FEBS Lett 408:39-42.
7. Brun S, Carmona MC, Mampel T, Vinas O, Giralt M, Iglesias R, Villarroya F. 1999. Uncoupling protein-3 gene expression in skeletal muscle during development is regulated by nutritional factors that alter circulating non-esterified fatty acids. FEBS Lett 453:205-209.
8. Chauvin C, De Oliveira F, Ronot X, Mousseau M, Leverve X, Fontaine E. 2001. Rotenone inhibits the mitochondrial permeability transition-induced cell death in U937 and KB cells. J Biol Chem 276:41394-41398.
9. De Giorgi F, Lartigue L, Bauer MK, Schubert A, Grimm S, Hanson GT, Remington SJ, Youle RJ, Ichas F. 2002. The permeability transition pore signals apoptosis by directing Bax translocation and multimerization. FASEB J 16:607-609.
10. Diano S, Matthews RT, Patrylo P, Yang L, Beal MF, Barnstable CJ, Horvath TL. 2003. Uncoupling protein 2 prevents neuronal death including that occuring during seizures. A mechism for preconditioning. Endocrinology 144:5014-5021.
11. Dirks A, Leeuwenburgh C. 2002. Apoptosis in skeletal muscle with aging. Am J Physiol Regul Integr Comp Physiol 282:R519-R527.
12. Dispersyn G, Nuydens R, Connors R, Borgers M, Geerts H. 1999. Bcl-2 protects against FCCP-induced apoptosis and mitochondrial membrane potential depolarization in PC12 cells. Biochim Biophys Acta 1428:357-371.
13. Dupuis L, di Scala F, Rene F, de Tapia M, Oudart H, Pradat PF, Meininger V, Loeffler JP. 2003. Up-regulation of mitochondrial uncoupling protein 3 reveals an early muscular metabolic defect in amyotrophic lateral sclerosis. FASEB J 17:2091-2093.
14. Echtay KS, Winkler E, Frischmuth K, Klingenberg M. 2001. Uncoupling proteins 2 and 3 are highly active H(+) transporters and highly nucleotide sensitive when activated by coenzyme Q (ubiquinone). Proc Natl Acad Sci USA 98:1416-1421.
15. Echtay KS, Roussel D, St-Pierre J, Jekabsons MB, Cadenas S, Stuart JA, Harper JA, Roebuck SJ, Morrison A, Pickering S, Clapham JC, Brand MD. 2002. Superoxide activates mitochondrial uncoupling proteins. Nature 415:96-99.
16. Enerback S, Jacobsson A, Simpson EM, Guerra C, Yamashita H, Harper ME, Kozak LP. 1997. Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese. Nature 387:90-94.
17. Fink BD, Hong YS, Mathahs MM, Scholz TD, Dillon JS, Sivitz WI. 2002. UCP2-dependent proton leak in isolated mammalian mitochondria. J Biol Chem 277:3918-3925.
18. Fontaine E, Eriksson O, Ichas F, Bernardi P. 1998. Regulation of the permeability transition pore in skeletal muscle mitochondria. Modulation by electron flow through the respiratory chain complex I. J Biol Chem 273:12662-12668.
19. Guerini D, Prati E, Desai U, Nick HP, Flammer R, Gruninger S, Cumin F, Kaleko M, Connelly S, Chiesi M. 2002. Uncoupling of protein-3 induces an uncontrolled uncoupling of mitochondria after expression in muscle derived L6 cells. Eur J Biochem 269:1373-1381.
20. Gupta S. 2001. Molecular steps of tumor necrosis factor receptor-mediated apoptosis. Curr Mol Med 1:317-324.
21. Herrera B, Fernández M, Alvarez AM, Roncero C, Benito M, Gil J, Fabregat I. 2001. Activation of caspases occurs downstream from radical oxygen species production, Bcl-xL down-regulation, and early cytochrome C release in apoptosis induced by transforming growth factor beta in rat fetal hepatocytes. Hepatology 34:548-556.
22. Hesselink MK, Greenhaff PL, Constantin-Teodosiu D, Hultman E, Saris WH, Nieuwlaat R, Schaart G, Kornips E, Schrauwen P. 2003. Increased uncoupling protein 3 content does not affect mitochondrial function in human skeletal muscle in vivo. J Clin Invest 111:479-486.
23. Huang X, Zhai D, Huang Y. 2001. Dependence of permeability transition pore opening and cytochrome C release from mitochondria on mitochondria energetic status. Mol Cell Biochem 224:1-7.
24. Jiang S, Cai J, Wallace DC, Jones DP. 1999. Cytochrome c-mediated apoptosis in cells lacking mitochondrial DNA. Signaling pathway involving release and caspase 3 activation is conserved. J Biol Chem 274:29905-29911.
25. Klingenberg M. 1974. Nicotinamide adenine dinucleotides (NAD, NADP, NADH, NADPH) spectrophotometric and fluorimetric methods. In: Bergmeyer HU, editor. Methods of enzymatic analysis. New York, London: Academic Press. pp 2045-2059.
26. Kroemer G, Reed JC. 2000. Mitochondrial control of cell death. Nat Med 6:513-519.
27. Kuida K. 2000. Caspase-9. Int J Biochem Cell Biol 32:121-124.
28. Linsinger G, Wilhelm S, Wagner H, Hacker G. 1999. Uncouplers of oxidative phosphorylation can enhance a Fas death signal. Mol Cell Biol 19:3299-3311.
29. Masaki T, Yoshimatsu H, Chiba S, Hidaka S, Tajima D, Kakuma T, Kurokawa M, Sakata T. 1999. Tumor necrosis factor-alpha regulates in vivo expression of the rat UCP family differentially. Biochim Biophys Acta 1436:585-592.
30. Mattiasson G, Shamloo M, Gido G, Mathi K, Tomasevic G, Yi S, Warden CH, Castilho RF, Melcher T, Gonzalez-Zulueta M, Nikolich K, Wieloch T. 2003. Uncoupling protein-2 prevents neuronal death and diminishes brain dysfunction after stroke and brain trauma. Nat Med 9:1062-1068.
31. Mills EM, Xu D, Fergusson MM, Combs CA, Xu Y, Finkel T. 2002. Regulation of cellular oncosis by uncoupling protein 2. J Biol Chem 277:27385-27392.
32. Nedergaard J, Cannon B. 2003. The 'novel' 'uncoupling' proteins UCP2 and UCP3: what do they really do? Pros and cons for suggested functions. Exp Physiol 88:65-84.
33. Nicholls DG, Cunningham SA, Rial E. 1989. The bioenergetic mechanisms of brown adipose tissue mitochondria. In: Trayhurn P, Nicholls DG, editors. Brown adipose tissue. London: Edward Arnold. pp 55-85.
34. Nishimura G, Proske RJ, Doyama H, Higuchi M. 2001. Regulation of apoptosis by respiration: Cytochrome c release by respiratory substrates. FEBS Lett 505:399-404.
35. Nomura M, Shimizu S, Sugiyama T, Narita M, Ito T, Matsuda H, Tsujimoto Y. 2003. 14-3-3 interacts directly with and negatively regulates pro-apoptotic Bax. J Biol Chem 278:2058-2065.
36. Ouhabi R, Boue-Grabot M, Mazat JP. 1998. Mitochondrial ATP synthesis in permeabilized cells: Assessment of the ATP/O values in situ. Anal Biochem 263:169-175.
37. Pedraza N, Solanes G, Carmona MC, Iglesias R, Vinas O, Mampel T, Vazquez M, Giralt M, Villarroya F. 2000. Impaired expression of the uncoupling protein-3 gene in skeletal muscle during lactation: Fibrates and troglitazone reverse lactation-induced downregulation of the uncoupling protein-3 gene. Diabetes 49:1224-1230.
38. Penzo D, Tagliapietra C, Colonia R, Petronilli V, Bernardi P. 2002. Effects of fatty acids on mitochondria: Implications for cell death. Biochim Biophys Acta 1555:160-165.
39. Pierrat B, Ito M, Hinz W, Simonen M, Erdmann D, Chiesi M, Heim J. 2000. Uncoupling proteins 2 and 3 interact with members of the 14.3.3 family. Eur J Biochem 267:2680-2687.
40. Polster BM, Basanez G, Young M, Suzuki M, Fiskum G. 2003. Inhibition of Bax-induced cytochrome c release from neural cell and brain mitochondria by dibucaine and propanolol. J Neuroscience 23:2735-2743.
41. Ravagnan L, Roumier T, Kroemer G. 2002. Mitochondria, the killer organelles and their weapons. J Cell Physiol 192:131-177.
42. Ricquier D, Bouillaud F. 2000. The uncoupling protein homologues: UCP1, UCP2, UCP3, StUCP, and AtUCP. Biochem J 345:161-179.
43. Sandri M, Carraro U. 1999. Apoptosis of skeletal muscles during development and disease. Int J Biochem Cell Biol 31:1373-1390.
44. Schrauwen P. 2002. Skeletal muscle uncoupling protein 3 (UCP3): Mitochondrial uncoupling protein in search of a function. Curr Opin Clin Nutr Metab Care 5:265-270.
45. Stoetzer OJ, Pogrebniak A, Pelka-Fleischer R, Hasmann M, Hiddemann W, Nuessler V. 2002. Modulation of apoptosis by mitochondrial uncouplers: Apoptosis-delaying features despite intrinsic cytotoxicity. Biochem Pharmacol 63:471-483.
46. Subramanian RR, Masters SC, Zhang H, Fu H. 2001. Functional conservation of 14-3-3 isoforms in inhibiting bad-induced apoptosis. Exp Cell Res 271:142-151.
47. Sun X, Wray CC, Tian X, Hasselgren PO, Lu J. 2003. The expression of uncoupling protein-3 is upregulated in skeletal muscle during sepsis. Am J Physiol Endocrinol Metab 285:E512-E520.
48. Van Hemert MJ, Steensma HY, Van Exuden GP. 2001. 14-3-3 proteins: Key regulators of cell division, signalling, and apoptosis. Bioessays 23:936-946.
49. Vidal-Puig A, Solanes G, Grujic D, Flier JS, Lowell BB. 1997. UCP3: An uncoupling protein homologue expressed preferentially and abundantly in skeletal muscle and brown adipose tissue. Biochem Biophys Res Commun 235:79-82.
50. Vieira HL, Haouzi D, El Hamel C, Jacotot E, Belzacq AS, Brenner C, Kroemer G. 2000. Permeabilization of the mitochondrial inner membrane during apoptosis: Impact of the adenine nucleotide translocator. Cell Death Differ 7:1146-1154.
51. Villani G, Greco M, Papa S, Attardi G. 1998. Low reserve of cytochrome c oxidase capacity in vivo in the respiratory chain of a variety of human cell types. J Biol Chem 48:31829-31836.
52. Voehringer DW, Hirschberg DL, Xiao J, Lu Q, Roederer M, Lock CB, Herzenberg LA, Steinman L, Herzenberg LA. 2000. Gene microarray identification of redox and mitochondrial elements that control resistance or sensitivity to apoptosis. Proc Natl Acad Sci USA 97:2680-2685.
53. Zackova M, Skobisova E, Urbankova E, Jezek P. 2003. Activating omega-6 polyunsaturated fatty acids and inhibitory purine nucleotides are high affinity ligands for novel mitochondrial uncoupling proteins UCP2 and UCP3. J Biol Chem 278:20761-20769.
54. Zhang CY, Baffy G, Pret P, Krauss S, Peroni O, Grujic D, Hagen T, Vidal-Puig AJ, Boss O, Kim YB, Zheng XX, Wheeler MB, Shulman GI, Chan CB, Lowell BB. 2001. Uncoupling protein-2 negatively regulates insulin secretion and is a major link between obesity, beta cell dysfunction, and type 2 diabetes. Cell 105:745-755.