Differential effects of thyroid status on regional H2O2 production in slow- and fast-twitch muscle of ducklings

Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

Volumn 183, Issue 1, 2013, Pages 135-143

  Rey, Benjamin ^a,b   Roussel, Damien ^a   Rouanet, Jean Louis ^a   Duchamp, Claude ^a  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITY OF THE WITWATERSRAND   (South Africa)

Author keywords

Birds; Cold acclimation; Mitochondria; Reactive oxygen species; Thyroid status

Indexed keywords

AVES;

EID: 84871891094     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-012-0692-5     Document Type: Article

References (38)

1. Adhihetty PJ, Ljubicic V, Menzies KJ, Hood DA (2005) Differential susceptibility of subsarcolemmal and intermyofibrillar mitochondria to apoptotic stimuli. Am J Physiol Cell Physiol 289: C994-C1001.
2. Anderson EJ, Neufer PD (2006) Type II skeletal myofibers possess unique properties that potentiate mitochondrial H(2)O(2) generation. Am J Physiol Cell Physiol 290: C844-C851.
3. Brand MD (2000) Uncoupling to survive? The role of mitochondrial inefficiency in ageing. Exp Gerontol 35: 811-820.
4. Chanseaume E, Malpuech-Brugere C, Patrac V, Bielicki G, Rousset P, Couturier K, Salles J, Renou JP, Boirie Y, Morio B (2006) Diets high in sugar, fat, and energy induce muscle type-specific adaptations in mitochondrial functions in rats. J Nutr 136: 2194-2200.
5. Cogswell AM, Stevens RJ, Hood DA (1993) Properties of skeletal muscle mitochondria isolated from subsarcolemmal and intermyofibrillar regions. Am J Physiol Cell Physiol 264: C383-C389.
6. Cohen AA, McGraw KJ, Robinson WD (2009) Serum antioxidant levels in wild birds vary in relation to diet, season, life history strategy, and species. Oecologia 161: 673-683.
7. Costantini D, Dell'ariccia G, Lipp HP (2008a) Long flights and age affect oxidative status of homing pigeons (Columba livia). J Exp Biol 211: 377-381.
8. Costantini D, Fanfani A, Dell'Omo G (2008b) Effects of corticosteroids on oxidative damage and circulating carotenoids in captive adult kestrel (Falco tinnunculus). J Comp Physiol B 178: 829-835.
9. Duchamp C, Barre H, Rouanet JL, Lanni A, Cohen-Adad F, Berne G, Brebion P (1991) Nonshivering thermogenesis in king penguin chicks. I. Role of skeletal muscle. Am J Physiol Regul Integr Comp Physiol 261: R1438-R1445.
10. Duchamp C, Chatonnet J, Dittmar A, Barre H (1993) Increased role of skeletal muscle in the calorigenic response to glucagon of cold-acclimated ducklings. Am J Physiol Regul Integr Comp Physiol 265: R1084-R1091.
11. Ferreira R, Vitorino R, Alves RM, Appell HJ, Powers SK, Duarte JA, Amado F (2010) Subsarcolemmal and intermyofibrillar mitochondria proteome differences disclose functional specializations in skeletal muscle. Proteomics 10: 3142-3154.
12. Goglia F, Lanni A, Duchamp C, Rouanet JL, Barre H (1993) Effect of cold acclimation on oxidative capacity and respiratory properties of liver and muscle mitochondria in ducklings, Cairina moschata. Comp Biochem Physiol 106: 95-101.
13. Holmes DJ, Fluckiger R, Austad SN (2001) Comparative biology of aging in birds: an update. Exp Gerontol 36: 869-883.
14. Horak P, Zilmer M, Saks L, Ots I, Karu U, Zilmer K (2006) Antioxidant protection, carotenoids and the costs of immune challenge in greenfinches. J Exp Biol 209: 4329-4338.
15. Hulbert AJ, Faulks S, Buttemer WA, Else PL (2002) Acyl composition of muscle membranes varies with body size in birds. J Exp Biol 205: 3561-3569.
16. Iossa S, Lionetti L, Mollica MP, Crescenzo R, Botta M, Samec S, Dulloo AG, Liverini G (2001) Differences in proton leak kinetics, but not in UCP3 protein content, in subsarcolemmal and intermyofibrillar skeletal muscle mitochondria from fed and fasted rats. FEBS Lett 505: 53-56.
17. Judge S, Jang YM, Smith A, Selman C, Phillips T, Speakman JR, Hagen T, Leeuwenburgh C (2005) Exercise by lifelong voluntary wheel running reduces subsarcolemmal and interfibrillar mitochondrial hydrogen peroxide production in the heart. Am J Physiol Regul Integr Comp Physiol 289: R1564-R1572.
18. Korshunov SS, Skulachev VP, Starkov AA (1997) High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 416: 15-18.
19. Lambert AJ, Boysen HM, Buckingham JA, Yang T, Podlutsky A, Austad SN, Kunz TH, Buffenstein R, Brand MD (2007) Low rates of hydrogen peroxide production by isolated heart mitochondria associate with long maximum lifespan in vertebrate homeotherms. Aging Cell 6: 607-618.
20. Ljubicic V, Hood DA (2008) Kinase-specific responsiveness to incremental contractile activity in skeletal muscle with low and high mitochondrial content. Am J Physiol Endocrinol Metab 295: E195-E204.
21. Lombardi A, Damon M, Vincent A, Goglia F, Herpin P (2000) Characterisation of oxidative phosphorylation in skeletal muscle mitochondria subpopulations in pig: a study using top-down elasticity analysis. FEBS Lett 475: 84-88.
22. Lopez-Torres M, Romero M, Barja G (2000) Effect of thyroid hormones on mitochondrial oxygen free radical production and DNA oxidative damage in the rat heart. Mol Cell Endocrinol 168: 127-134.
23. Mollica MP, Lionetti L, Crescenzo R, D'Andrea E, Ferraro M, Liverini G, Iossa S (2006) Heterogeneous bioenergetic behaviour of subsarcolemmal and intermyofibrillar mitochondria in fed and fasted rats. Cell Mol Life Sci 63: 358-366.
24. Mujahid A, Yoshiki Y, Akiba Y, Toyomizu M (2005) Superoxide radical production in chicken skeletal muscle induced by acute heat stress. Poult Sci 84: 307-314.
25. Mujahid A, Sato K, Akiba Y, Toyomizu M (2006) Acute heat stress stimulates mitochondrial superoxide production in broiler skeletal muscle, possibly via downregulation of uncoupling protein content. Poult Sci 85: 1259-1265.
26. Picard M, Hepple RT, Burelle Y (2012) Mitochondrial functional specialization in glycolytic and oxidative muscle fibers: tailoring the organelle for optimal function. Am J Physiol Cell Physiol 302: C629-C641.
27. Rey B, Roussel D, Romestaing C, Belouze M, Rouanet JL, Desplanches D, Sibille B, Servais S, Duchamp C (2010) Up-regulation of avian uncoupling protein in cold-acclimated and hyperthyroid ducklings prevents reactive oxygen species production by skeletal muscle mitochondria. BMC Physiol 10: 5.
28. Rey B, Roussel D, Teulier L, Eyenga P, Degletagne C, Belouze M, Duchamp C (2011) Functional argument for the existence of an avian nitric oxide synthase in muscle mitochondria: effect of cold acclimation. FEBS Lett 585: 173-177.
29. Roussel D, Rouanet JL, Duchamp C, Barre H (1998) Effects of cold acclimation and palmitate on energy coupling in duckling skeletal muscle mitochondria. FEBS Lett 439: 258-262.
30. Roussel D, Chainier F, Rouanet J, Barre H (2000) Increase in the adenine nucleotide translocase content of duckling subsarcolemmal mitochondria during cold acclimation. FEBS Lett 477: 141-144.
31. Servais S, Couturier K, Koubi H, Rouanet JL, Desplanches D, Sornay-Mayet MH, Sempore B, Lavoie JM, Favier R (2003) Effect of voluntary exercise on H2O2 release by subsarcolemmal and intermyofibrillar mitochondria. Free Radic Biol Med 35: 24-32.
32. Silva JE (1995) Thyroid hormone control of thermogenesis and energy balance. Thyroid 5: 481-492.
33. Simonides WS, van Hardeveld C (2008) Thyroid hormone as a determinant of metabolic and contractile phenotype of skeletal muscle. Thyroid 18: 205-216.
34. Stowe DF, Camara AK (2009) Mitochondrial reactive oxygen species production in excitable cells: modulators of mitochondrial and cell function. Antioxid Redox Signal 11: 1373-1414.
35. Suarez RK (1992) Hummingbird flight: sustaining the highest mass-specific metabolic rates among vertebrates. Experientia 48: 565-570.
36. Toyomizu M, Ueda M, Sato S, Seki Y, Sato K, Akiba Y (2002) Cold-induced mitochondrial uncoupling and expression of chicken UCP and ANT mRNA in chicken skeletal muscle. FEBS Lett 529: 313-318.
37. Venditti P, Puca A, Di Meo S (2003a) Effect of thyroid state on rate and sites of H2O2 production in rat skeletal muscle mitochondria. Arch Biochem Biophys 411: 121-128.
38. Venditti P, Puca A, Di Meo S (2003b) Effects of thyroid state on H2O2 production by rat heart mitochondria: sites of production with complex I- and complex II-linked substrates. Horm Metab Res 35: 55-61.