Up-regulation of avian uncoupling protein in cold-acclimated and hyperthyroid ducklings prevents reactive oxygen species production by skeletal muscle mitochondria

BMC Physiology

Volumn 10, Issue 1, 2010, Pages

  Rey, Benjamin ^a,b   Roussel, Damien ^a,b   Romestaing, Caroline ^a,b   Belouze, Maud ^a,b   Rouanet, Jean Louis ^a,b   Desplanches, Dominique ^a,b   Sibille, Brigitte ^a,b   Servais, Stéphane ^a,b   Duchamp, Claude ^a,b  

^a UNIVERSITÉ DE LYON   (France)

^b Laboratoire de Physiologie Int&EACUTE grative Cellulaire et Mol&EACUTE culaire Villeurbanne   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; ION CHANNEL; LIOTHYRONINE; LIPID; MESSENGER RNA; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL UNCOUPLING PROTEIN; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

ACCLIMATIZATION; ANIMAL; ARTICLE; BLOOD; COLD; DUCK; ENERGY METABOLISM; GENETICS; GROWTH, DEVELOPMENT AND AGING; HYPERTHYROIDISM; MALE; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PATHOPHYSIOLOGY; PHYSIOLOGY; SKELETAL MUSCLE; SPECIES DIFFERENCE; UPREGULATION;

ACCLIMATIZATION; ANIMALS; COLD TEMPERATURE; DUCKS; ENERGY METABOLISM; GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; HYPERTHYROIDISM; ION CHANNELS; LIPIDS; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MUSCLE, SKELETAL; OXIDATIVE STRESS; OXYGEN CONSUMPTION; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; SPECIES SPECIFICITY; SUPEROXIDE DISMUTASE; TRIIODOTHYRONINE; UP-REGULATION;

EID: 77951607860     PISSN: None     EISSN: 14726793     Source Type: Journal    
DOI: 10.1186/1472-6793-10-5     Document Type: Article

References (57)

1. Mitochondria, oxygen free radicals, disease and ageing. S Raha BH Robinson, Trends Biochem Sci 2000 25 10 502 508 10.1016/S0968-0004(00)01674-1 11050436
2. Mitochondrial diseases in man and mouse. DC Wallace, Science 1999 283 5407 1482 1488 10.1126/science.283.5407.1482 10066162
3. Mitochondrial superoxide and aging: uncoupling-protein activity and superoxide production. MD Brand JA Buckingham TC Esteves K Green AJ Lambert S Miwa MP Murphy JL Pakay DA Talbot KS Echtay, Biochem Soc Symp 2004 71 203 213 15777023
4. Oxidative damage and mitochondrial decay in aging. MK Shigenaga TM Hagen BN Ames, Proc Natl Acad Sci USA 1994 91 23 10771 10778 10.1073/pnas.91.23.10771 7971961
5. The uncoupling protein homologues: UCP1, UCP2, UCP3, StUCP and AtUCP. D Ricquier F Bouillaud, Biochem J 2000 345 Pt 2 161 179 10.1042/0264-6021:3450161 10620491
6. Brown adipose tissue: function and physiological significance. B Cannon J Nedergaard, Physiol Rev 2004 84 1 277 359 10.1152/physrev.00015.2003 14715917
7. A history of the first uncoupling protein, UCP1. DG Nicholls E Rial, J Bioenerg Biomemb 1999 31 5 399 406 10.1023/A:1005436121005 (Pubitemid 30053954)
8. Uncoupling to survive? The role of mitochondrial inefficiency in ageing. MD Brand, Exp Gerontol 2000 35 6-7 811 820 10.1016/S0531-5565(00)00135-2 11053672
9. Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins. MD Brand C Affourtit TC Esteves K Green AJ Lambert S Miwa JL Pakay N Parker, Free Rad Biol Med 2004 37 6 755 767 10.1016/j. freeradbiomed.2004.05.034 15304252
10. Role of uncoupled and non-coupled oxidations in maintenance of safely low levels of oxygen and its one-electron reductants. VP Skulachev, Q Rev Biophys 1996 29 2 169 202 10.1017/S0033583500005795 8870073
11. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. SS Korshunov VP Skulachev AA Starkov, FEBS lett 1997 416 1 15 18 10.1016/S0014-5793(97)01159-9 9369223
12. Mitochondrial matrix reactive oxygen species production is very sensitive to mild uncoupling. S Miwa MD Brand, Biochem Soc Trans 2003 31 Pt 6 1300 1301 10.1042/BST0311300 14641047
13. Reactive oxygen species, mitochondria, apoptosis and aging. S Papa VP Skulachev, Mol Cell Biochem 1997 174 1-2 305 319 10.1023/A:1006873518427 9309704
14. Superoxide-mediated activation of uncoupling protein 2 causes pancreatic beta cell dysfunction. S Krauss CY Zhang L Scorrano LT Dalgaard J St-Pierre ST Grey BB Lowell, J Clin Invest 2003 112 12 1831 1842 14679178
15. Oxidative damage and phospholipid fatty acyl composition in skeletal muscle mitochondria from mice underexpressing or overexpressing uncoupling protein 3. MD Brand R Pamplona M Portero-Otin JR Requena SJ Roebuck JA Buckingham JC Clapham S Cadenas, Biochem J 2002 368 Pt 2 597 603 10.1042/BJ20021077 12193161
16. Activation of the potato plant uncoupling mitochondrial protein inhibits reactive oxygen species generation by the respiratory chain. AJ Kowaltowski AD Costa AE Vercesi, FEBS lett 1998 425 2 213 216 10.1016/S0014-5793(98)00231-2 9559650
17. A role for uncoupling protein-2 as a regulator of mitochondrial hydrogen peroxide generation. A Negre-Salvayre C Hirtz G Carrera R Cazenave M Troly R Salvayre L Penicaud L Casteilla, Faseb J 1997 11 10 809 815 9271366
18. Superoxide activates mitochondrial uncoupling proteins. KS Echtay D Roussel J St-Pierre MB Jekabsons S Cadenas JA Stuart JA Harper SJ Roebuck A Morrison S Pickering, et al. Nature 2002 415 6867 96 99 10.1038/415096a 11780125
19. A signalling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling. KS Echtay TC Esteves JL Pakay MB Jekabsons AJ Lambert M Portero-Otin R Pamplona AJ Vidal-Puig S Wang SJ Roebuck, et al. EMBO J 2003 22 16 4103 4110 10.1093/emboj/cdg412 12912909
20. Superoxide stimulates a proton leak in potato mitochondria that is related to the activity of uncoupling protein. MJ Considine M Goodman KS Echtay M Laloi J Whelan MD Brand LJ Sweetlove, J Biol Chem 2003 278 25 22298 22302 10.1074/jbc.M301075200 12672801
21. Superoxide activates a GDP-sensitive proton conductance in skeletal muscle mitochondria from king penguin (Aptenodytes patagonicus). DA Talbot N Hanuise B Rey JL Rouanet C Duchamp MD Brand, Biochem Biophys Res Commun 2003 312 4 983 988 10.1016/j.bbrc.2003.11.022 14651968
22. Avian UCP: the killjoy in the evolution of the mitochondrial uncoupling proteins. Y Emre C Hurtaud D Ricquier F Bouillaud J Hughes F Criscuolo, J Mol Evol 2007 65 4 392 402 10.1007/s00239-007-9020-1 17909695
23. Cold-induced enhancement of avian uncoupling protein expression, heat production, and triiodothyronine concentrations in broiler chicks. A Collin J Buyse P van As VM Darras RD Malheiros VM Moraes GE Reyns M Taouis E Decuypere, Gen Comp Endocrinol 2003 130 1 70 77 10.1016/S0016-6480(02)00571-3 12535627
24. An uncoupling protein homologue putatively involved in facultative muscle thermogenesis in birds. S Raimbault S Dridi F Denjean J Lachuer E Couplan F Bouillaud A Bordas C Duchamp M Taouis D Ricquier, Biochem J 2001 353 Pt 3 441 444 10.1042/0264-6021:3530441 11171038
25. Uncoupling protein and ATP/ADP carrier increase mitochondrial proton conductance after cold adaptation of king penguins. DA Talbot C Duchamp B Rey N Hanuise JL Rouanet B Sibille MD Brand, J Physiol Lond 2004 558 Pt 1 123 135 10.1113/jphysiol.2004.063768 15146050
26. Cold-induced mitochondrial uncoupling and expression of chicken UCP and ANT mRNA in chicken skeletal muscle. M Toyomizu M Ueda S Sato Y Seki K Sato Y Akiba, FEBS lett 2002 529 2-3 313 318 10.1016/S0014-5793(02)03395-1 12372620
27. Long-term fasting decreases mitochondrial avian UCP-mediated oxygen consumption in hypometabolic king penguins. B Rey LG Halsey V Dolmazon JL Rouanet D Roussel Y Handrich PJ Butler C Duchamp, Am J Physiol Regul Integr Comp Physiol 2008 295 1 92 R100 18495832
28. Endothermy in birds: underlying molecular mechanisms. I Walter F Seebacher, J Exp Biol 2009 212 Pt 15 2328 2336 10.1242/jeb.029009 19617425
29. Effects of dietary macronutrient content on energy metabolism and uncoupling protein mRNA expression in broiler chickens. A Collin RD Malheiros VM Moraes P Van As VM Darras M Taouis E Decuypere J Buyse, Br J Nutr 2003 90 2 261 269 10.1079/BJN2003910 12908886
30. Avian uncoupling protein expressed in yeast mitochondria prevents endogenous free radical damage. F Criscuolo M Gonzalez-Barroso Mdel Y Le Maho D Ricquier F Bouillaud, Proc Biol Sci 2005 272 1565 803 810 10.1098/rspb.2004.3044 15888413
31. Acute heat stress stimulates mitochondrial superoxide production in broiler skeletal muscle, possibly via downregulation of uncoupling protein content. A Mujahid K Sato Y Akiba M Toyomizu, Poult Sci 2006 85 7 1259 1265 16830867
32. Oxygen recovery up-regulates avian UCP and ANT in newly hatched ducklings. B Rey M Spee M Belouze A Girard J Prost D Roussel C Duchamp, J Comp Physiol B 2010 180 2 239 246 10.1007/s00360-009-0409-6 19816693
33. Possible role of avian uncoupling protein in down-regulating mitochondrial superoxide production in skeletal muscle of fasted chickens. T Abe A Mujahid K Sato Y Akiba M Toyomizu, FEBS lett 2006 580 20 4815 4822 10.1016/j.febslet.2006.07.070 16904672
34. Acute heat stress induces oxidative stress and decreases adaptation in young white leghorn cockerels by downregulation of avian uncoupling protein. A Mujahid Y Akiba M Toyomizu, Poult Sci 2007 86 2 364 371 17234852
35. Increased respiration in skeletal muscle mitochondria from cold-acclimated ducklings: uncoupling effects of free fatty acids. H Barré J Nedergaard B Cannon, Comp Biochem Physiol 1986 85 2 343 348 10.1016/0305-0491(86)90010-6
36. Skeletal muscle as the major site of nonshivering thermogenesis in cold-acclimated ducklings. C Duchamp H Barre, Am J Physiol Regul Integr Comp Physiol 1993 265 5 Pt 2 1076 R1083
37. Loose-coupled mitochondria in chronic glucagon-treated hyperthermic ducklings. H Barré G Berne P Brebion F Cohen-Adad JL Rouanet, Am J Physiol Regul Integr Comp Physiol 1989 256 6 Pt 2 1192 R1199
38. The proton leak across the mitochondrial inner membrane. MD Brand, Biochim Biophys Acta 1990 1018 2-3 128 133 10.1016/0005-2728(90)90232-S 2393654
39. The influence of respiration and ATP hydrolysis on the proton-electrochemical gradient across the inner membrane of rat-liver mitochondria as determined by ion distribution. DG Nicholls, Eur J Biochem/FEBS 1974 50 1 305 315 10.1111/j.1432-1033.1974.tb03899.x
40. Characteristics of mitochondrial proton leak and control of oxidative phosphorylation in the major oxygen-consuming tissues of the rat. DF Rolfe AJ Hulbert MD Brand, Biochim Biophys Acta 1994 1188 3 405 416 10.1016/0005-2728(94) 90062-0 7803454
41. Reptilian uncoupling protein: functionality and expression in sub-zero temperatures. B Rey B Sibille C Romestaing M Belouze D Letexier S Servais H Barre C Duchamp Y Voituron, J Exp Biol 2008 211 Pt 9 1456 1462 10.1242/jeb.012328 18424679
42. Superoxide production by NADH:ubiquinone oxidoreductase (complex I) depends on the pH gradient across the mitochondrial inner membrane. AJ Lambert MD Brand, Biochem J 2004 382 Pt 2 511 517 15175007
43. Methionine restriction decreases mitochondrial oxygen radical generation and leak as well as oxidative damage to mitochondrial DNA and proteins. A Sanz P Caro V Ayala M Portero-Otin R Pamplona G Barja, Faseb J 2006 20 8 1064 1073 10.1096/fj.05-5568com 16770005
44. Superoxide dismutase assays. L Flohe F Otting, Methods Enzymol 1984 105 93 104 full-text 6328209
45. Glutathione peroxidase and hydroperoxides. AL Tappel, Method Enzymol 1978 52 506 513 full-text
46. Cloning and functional characterization of an uncoupling protein homolog in hummingbirds. CR Vianna T Hagen CY Zhang E Bachman O Boss B Gereben AS Moriscot BB Lowell JE Bicudo AC Bianco, Physiol Genomics 2001 5 3 137 145 11285367
47. Production of endogenous matrix superoxide from mitochondrial complex I leads to activation of uncoupling protein 3. DA Talbot AJ Lambert MD Brand, FEBS lett 2004 556 1-3 111 115 10.1016/S0014-5793(03)01386-3 14706836
48. Cold acclimation or grapeseed oil feeding affects phospholipid composition and mitochondrial function in duckling skeletal muscle. F Chainier D Roussel B Georges R Meister JL Rouanet C Duchamp H Barre, Lipids 2000 35 10 1099 1106 10.1007/s11745-000-0625-8 11104016
49. Increased lipogenesis in isolated hepatocytes from cold-acclimated ducklings. E Bedu F Chainier B Sibille R Meister G Dallevet D Garin C Duchamp, Am J Physiol Regul Integr Comp Physiol 2002 283 5 1245 R1253 12376419
50. Effects of cold acclimation and palmitate on energy coupling in duckling skeletal muscle mitochondria. D Roussel JL Rouanet C Duchamp H Barre, FEBS lett 1998 439 3 258 262 10.1016/S0014-5793(98)01382-9 9845333
51. Functional relationship between MyoD and peroxisome proliferator- activated receptor-dependent regulatory pathways in the control of the human uncoupling protein-3 gene transcription. G Solanes N Pedraza R Iglesias M Giralt F Villarroya, Mol Endocrinol 2003 17 10 1944 1958 10.1210/me.2002-0395 12843208
52. Effects of environmental temperature on thyroid hormones in the barn owl (Tyto alba). A Klein M Kulcsar V Krizsik R Matics P Rudas J Torok G Huszenicza, Acta Vet Hung 2006 54 3 321 331 10.1556/AVet.54.2006.3.3 17020136
53. Cold-induced hyperthyroidism produces oxidative damage in rat tissues and increases susceptibility to oxidants. P Venditti R De Rosa M Portero-Otin R Pamplona S Di Meo, Int J Biochem Cell Biol 2004 36 7 1319 1331 10.1016/j.biocel.2003.11.005 15109575
54. Potential involvement of mammalian and avian uncoupling proteins in the thermogenic effect of thyroid hormones. A Collin S Cassy J Buyse E Decuypere M Damon, Domest Anim Endocrinol 2005 29 1 78 87 10.1016/j.domaniend.2005.02.007 15927767
55. Thyroid status, but not insulin status, affects expression of avian uncoupling protein mRNA in chicken. A Collin M Taouis J Buyse NB Ifuta VM Darras P Van As RD Malheiros VM Moraes E Decuypere, Am J Physiol Endocrinol Metab 2003 284 4 771 E777 12475757
56. Muscle-specific up-regulation of rat UCP3 mRNA expression by long-term hindlimb unloading. F Denjean D Desplanches J Lachuer F Cohen-Adad MH Mayet C Duchamp, Biochem Biophys Res Commun 1999 266 2 518 522 10.1006/bbrc.1999.1847 10600534
57. Effect of thyroid state on lipid peroxidation, antioxidant defences, and susceptibility to oxidative stress in rat tissues. P Venditti M Balestrieri S Di Meo T De Leo, J Endocrinol 1997 155 1 151 157 10.1677/joe.0.1550151 9390017