Physiological increases in uncoupling protein 3 augment fatty acid oxidation and decrease reactive oxygen species production without uncoupling respiration in muscle cells

Diabetes

Volumn 54, Issue 8, 2005, Pages 2343-2350

  Darcy MacLellan, J ^a   Gerrits, Martin F ^a   Gowing, Adrienne ^a   Smith, Peter J S ^b   Wheeler, Michael B ^c   Harper, Mary Ellen ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b MARINE BIOLOGICAL LABORATORY   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2,4 DINITROPHENOL; FATTY ACID; GREEN FLUORESCENT PROTEIN; INSULIN; OXYGEN; PALMITIC ACID; REACTIVE OXYGEN METABOLITE; UNCOUPLING PROTEIN 3;

ADENOVIRUS; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MUSCLE CELL; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; WESTERN BLOTTING;

ANIMALS; CARRIER PROTEINS; CELL LINE; DINITROPHENOLS; FATTY ACIDS; GENE EXPRESSION; GLUCOSE; ION CHANNELS; MEMBRANE POTENTIALS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MUSCLE CELLS; MUSCLE, SKELETAL; OXIDATION-REDUCTION; OXYGEN CONSUMPTION; PALMITIC ACID; RATS; REACTIVE OXYGEN SPECIES; TRANSFECTION;

EID: 23644434842     PISSN: 00121797     EISSN: None     Source Type: Journal    
DOI: 10.2337/diabetes.54.8.2343     Document Type: Article

References (49)

1. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstrale M, Laurila E: PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34:267-273, 2003
2. Patti ME, Butte AJ, Crunkhorn S, Cusi K, Berria R, Kashyap S, Miyazaki Y, Kohane I, Costello M, Saccone R: Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1. Proc Natl Acad Sci USA 100:8466-8471, 2003
3. Schrauwen P, Hesselink MK, Blaak EE, Borghouts LB, Schaart G, Saris WH, Keizer HA: Uncoupling protein 3 content is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes 50:2870-2873, 2001
4. Kozak LP, Harper ME: Mitochondrial uncoupling proteins in energy expenditure. Annu Rev Nutr 20:339-363, 2000
5. Nedergaard J, Golozoubova V, Matthais A, Asadi A, Jacobsson A, Cannon B: UCP1: the only protein able to mediate adaptive non-shivering thermogenesis and metabolic inefficiency. Biochim Biophys Acta 1504:82-106, 2001
6. Harper ME, Himms-Hagen J: Mitochondrial efficiency: lessons learned from transgenic mice. Biochim Biophys Acta 1504:159-172, 2001
7. Enerbäck S, Jacobsson A, Simpson EM, Guerra C, Yamashita H, Harper ME, Kozak LP: Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese. Nature 387:90-94, 1997
8. Liu X, Rossmeisl M, McClaine J, Riachi M, Harper ME, Kozak LP: Paradoxical resistance to diet-induced obesity in UCP1-deficient mice. J Clin Invest 111:399-407, 2003
9. Fleury C, Neverova M, Collins S, Raimbault S, Champigny O, Levi-Meyrueis C, Bouillaud F, Seldin MF, Surwit RS, Ricquier D: Uncoupling protein-2: a novel gene linked to obesity and hyperinsulinemia. Nat Genet 15:269-272, 1997
10. Gimeno RE, Dembski M, Weng X, Deng N, Shyjan AW, Gimeno CJ, Iris F, Ellis SJ, Woolf EA, Tartaglia LA: Cloning and characterization of an uncoupling protein homolog: a potential molecular mediator of human thermogenesis. Diabetes 46:900-906, 1997
11. Boss O, Samec S, Paoloni-Giacobino A, Rosier C, Dulloo A, Seydoux J, Muzzin P, Giacobino JP: Uncoupling protein-3: a new member of the mitochondrial carrier family with tissue-specific expression. FEBS Lett 408:39-42, 1997
12. Vidal-Puig A, Solanes G, Grujic D, Flier JS, Lowell BB: UCP3: an uncoupling protein homologue expressed preferentially and abundantly in skeletal muscle and brown adipose tissue. Biochem Biophys Res Commun 235:79-82, 1997
13. Pecqueur C, Alves-Guerra M-C, Gelly C, Lévi-Meyrueis C, Couplan E, Collins S, Ricquier D, Bouillaud F, Miroux B: Uncoupling protein 2, in vivo distribution, induction upon oxidative stress, and evidence for translational regulation. J Biol Chem 276:8705-8712, 2001
14. Arserujevic D, Onuma H, Pecqueur C, Raimbault S, Manning BS, Miroux B, Couplan E, Alves-Guerra MC, Goubern M, Surwit R: Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production. Nat Genet.26:435-439, 2000
15. Harper ME, Antoniou A, Villalobos-Menuey E, Russo A, Trauger R, Vendemelio M, George A, Bartholomew R, Carlo D, Shaikh A: Characterization of a novel metabolic strategy used by drug-resistant tumor cells. FASEB J 16:1550-1557, 2002
16. Chan CB, Saleh MC, Koshlan V, Wheeler MB: Uncoupling protein 2 and islet function. Diabetes 53:8136-8142, 2004
17. Vincent AM, Olzmann JA, Brownlee M, Sivitz WI, Russell JW: Uncoupling proteins prevent glucose-induced neuronal oxidative stress and programmed cell death. Diabetes 53:726-734, 2004
18. Argyropoulos G, Harper ME: Uncoupling proteins and thermoregulation. J Appl Physiol 92:2187-2198, 2002
19. Cadenas S, Buckingham JA, Samec S, Seydoux J, Din N, Dulloo AG, Brand MD: UCP2 and UCP3 rise in starved rat skeletal muscle but mitochondrial proton conductance is unchanged. FEBS Lett 462:257-260, 1999
20. -/- and wild-type mice. Am J Physiol Endocrinol Metab 281:E975-E982, 2001
21. Stuart JA, Cadenas S, Jekabsons MB, Roussel D, Brand MD: Mitochondrial proton leak and the uncoupling protein 1 homologues. Biochim Biophys Acta 1504:144-158, 2001
22. Stuart JA, Harper JA, Brindle KM, Jekabsons MB, Brand MD: Physiological levels of mammalian uncoupling protein 2 do not uncouple yeast mitochondria. J Biol Chem 276:18633-18639, 2001
23. Du X-L, Edelstein D, Rossetti L, Fantus IG, Goldberg H, Ziyadeh F, Wu J, Brownlee M: Hyperglycemia-induced mitochondrial Superoxide overpro-duction activates the hexosamine pathway and induces plasminogen activator inhibitor-1 expression by increasing Sp1 glycosylation. Proc Natl Acad Sci U S A 97:12222-12226, 2000
24. Brownlee M: Biochemistry and molecular cell biology of diabetic complications. Nature 414:813-820, 2001
25. Miwa S, St-Pierre J, Partridge L, Brand MD: Superoxide and hydrogen peroxide production by Drosophila mitochondria. Free Radic Biol MeA 35:938-948, 2003
26. Huppertz C, Fischer BM, Kim YB, Kotani K, Vidal-Puig A, Slieker LJ, Sloop KW, Lowell BB, Kahn BB: Uncoupling protein 3 (UCP3) stimulates glucose uptake in muscle cells through a phosphoinositide 3-kinase-dependent mechanism. J Biol Chem 276:12520-12529, 2001
27. Roduit R, Nolan C, Alarcon C, Moore P, Barbeau A, Delghingaro-Augusto V, Przybykowski E, Morin J, Masse F, Massie B: A role for the malonyl-CoA/long- chain acyl-CoA pathway of lipid signaling in the regulation of insulin secretion in response to both fuel and nonfuel stimuli. Diabetes 53:1007-1019, 2004
28. Land SC, Porterfield DM, Sanger RH, Smith PJS: The serf-referencing oxygen-selective microelectrode: detection of transmembrane oxygen flux from single cells. J Exp Biol 202:211-218, 1999
29. Porterfield DM, Corkey RF, Sanger RH, Tornheim K, Smith PJ, Corkey BE: Oxygen consumption oscillates in single clonal pancreatic β-cells (HIT). Diabetes 49:1511-1516, 2000
30. Jung SK, Gorski W, Aspinwall CW, Kauri LM, Kennedy RT: Oxygen microsensor and its application to single cells and mouse pancreatic islets. Anal Chem 71:3642-3649, 1999
31. Jaburek M, Varecha M, Gimeno RE, Dembski M, Jezek P, Zhang M, Burn P, Tartaglia LA, Garlid KD: Transport function and regulation of mitochondrial uncoupling proteins 2 and 3. J Biol Chem 274:26003-26007, 1999
32. Acin A, Rodriguez M, Rique H, Canet E, Boutin JA, Galizzi JP: Cloning and characterization of the 5′ flanking region of the human uncoupling protein 3 (UCP3) gene. Biochem Biophys Res Commun 258:278-283, 1999
33. Weigle DS, Selfridge LE, Schwartz MW, Seeley RJ, Cummings DE, Havel PJ, Kuijper JL, BeltrandelRio H: Elevated free fatty acids induce uncoupling protein 3 expression in muscle: a potential explanation for the effect of fasting. Diabetes 47:298-302, 1998
34. Boss O, Hagen T, Lowell BB: Uncoupling proteins 2 and 3: potential regulators of mitochondrial energy metabolism. Diabetes 49:143-156, 2000
35. Himms-Hagen J, Harper ME: Physiological role of UCP3 may be export of fatty acids from mitochondria when fatty acid oxidation predominates: an hypothesis. Exp Biol Med 226:78-84, 2001
36. Eaton S: Current Views of Fatty Acid Oxidation and Ketogenesis: From Organelles to Point Mutations. New York, Kluwer Academic/Plenum Publishers, 1999
37. Hunt MC, Nousiainen SE, Huttunen MK, Orii KE, Svensson LT, Alexson SE: Peroxisome proliferator-induced long chain acyl-CoA thioesterases comprise a highly conserved novel multi-gene family involved in lipid metabolism. J Biol Chem 274:34317-34326, 1999
38. Moore GB, Himms-Hagen J, Harper ME, Clapham JC: Overexpression of UCP-3 in skeletal muscle of mice results in increased expression of mitochondrial thioesterase mRNA. Biochem Biophys Res Commun 283: 785-790, 2001
39. Stavinoha MA, RaySpellicy JW, Essop MF, Graveleau C, Abel ED, Hart-Sailors ML, Mersmann HJ, Bray MS, Young ME: Evidence for mitochondrial thioesterase 1 as a peroxisome proliferator-activated receptor-α-regulated gene in cardiac and skeletal muscle. Am J Physiol Endocrinol Metab 287:E878-E887, 2004
40. Schrauwen P, Saris WH, Hesselink MK: An alternative function for human uncoupling protein 3: protection of mitochondria against accumulation of nonesterifled fatty acids. FASEB J 15:2497-2502, 2001
41. Clapham JC, Arch JR, Chapman H, Haynes A, Lister C, Moore GB, Piercy V, Carter SA, Lehner I, Smith SA: Mice overexpressing human uncoupling protein-3 in skeletal muscle are hyperphagic and lean. Nature 406:415-418, 2000
42. Vidal-Puig AJ, Grujic D, Zhang CY, Hagen T, Boss O, Ido Y, Szczepanik A, Wade J, Mootha V, Cortright R: Energy metabolism in uncoupling protein 3 gene knockout mice. J Biol Chem 275:16258-16266, 2000
43. Echtay KS, Esteves TC, Pakay JL, Jekabsons MB, Lambert AJ, Portero-Otin M, Pamplona R, Vidal-Puig AJ, Wang S, Roebuck SJ: A signalling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling. EMBO J 22:4103-4110, 2003
44. Goglia F, Skulachev VP: A function for novel uncoupling proteins: antioxidant defense of mitochondrial matrix by translocating fatty acid peroxides from the inner to the outer membrane leaflet. FASEB J 17:1585-1591, 2003
45. Echtay KS, Roussel D, St-Pierre J, Jekabsons MB, Cadenas S, Stuart JA, Harper JA, Roebuck SJ, Morrison A, Pickering S: Superoxide activates mitochondrial uncoupling proteins. Nature 415:96-99, 2002
46. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP: Normalizing mitochondrial Superoxide production blocks three pathways of hyperglycaemic damage. Nature 404:787-790, 2000
47. Argyropoulos G, Brown AM, Willi SM, Zhu J, He Y, Reitman M, Gevao SM, Spruill I, Garvey WT: Effects of mutations in the human uncoupling protein 3 gene on the respiratory quotient and fat oxidation in severe obesity and type 2 diabetes. J Clin Invest 102:1345-1351, 1998
48. Chung WK, Luke A, Cooper RS, Rotini C, Vidal-Puig A, Rosenbaum M, Chua M, Solanes G, Zheng M, Zhao L: Genetic and physiologic analysis of the role of uncoupling protein 3 in human energy homeostasis. Diabetes 48:1890-1895, 1999
49. Bezaire V, Spriet LL, Campbell S, Sabet N, Gerrits M, Bonen A, Harper M-E: Constitutive UCP3 overexpression at physiological levels increases mouse skeletal muscle capacity for fatty acid transport and oxidation. FASEB J 19:977-979, 2005