Mitochondrial uncoupling prevents cold-induced oxidative stress: A case study using UCP1 knockout mice

Journal of Experimental Biology

Volumn 217, Issue 4, 2014, Pages 624-630

  Stier, Antoine ^a,b   Bize, Pierre ^c,e   Habold, Caroline ^a,b   Bouillaud, Frederic ^d   Massemin, Sylvie ^a,b   Criscuolo, Francois ^a,b  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b INSTITUT DE RECHERCHES SUBATOMIQUES   (France)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

^d INSTITUT COCHIN   (France)

^e UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Cold; Mitochondria; Nonshivering thermogenesis; Oxidative stress; Reactive oxygen species; Uncoupling protein

Indexed keywords

ION CHANNEL; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL UNCOUPLING PROTEIN; REACTIVE OXYGEN METABOLITE; UNCOUPLING PROTEIN;

ANIMAL; ARTICLE; C57BL MOUSE; COLD; COLD SHOCK RESPONSE; FEMALE; GENETICS; KNOCKOUT MOUSE; MALE; METABOLISM; MITOCHONDRION; MOUSE; NONSHIVERING THERMOGENESIS; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PHYSIOLOGY; THERMOGENESIS;

COLD; MITOCHONDRIA; NONSHIVERING THERMOGENESIS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; UNCOUPLING PROTEIN;

ANIMALS; COLD-SHOCK RESPONSE; FEMALE; ION CHANNELS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; OXIDATIVE STRESS; OXYGEN CONSUMPTION; REACTIVE OXYGEN SPECIES; THERMOGENESIS;

EID: 84893927142     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.092700     Document Type: Article

References (46)

1. Aydin, J., Shabalina, I. G., Place, N., Reiken, S., Zhang, S.-J., Bellinger, A. M., Nedergaard, J., Cannon, B., Marks, A. R., Bruton, J. D. et al. (2008). Nonshivering thermogenesis protects against defective calcium handling in muscle. FASEB J 22, 3919-3924.
2. Barja, G. (2007). Mitochondrial oxygen consumption and reactive oxygen species production are independently modulated: Implications for aging studies. Rejuvenation Res. 10, 215-224.
3. Beckman, K. B. and Ames, B. N. (1998). The free radical theory of aging matures. Physiol. Rev. 78, 547-581.
4. Boström, P., Wu, J., Jedrychowski, M. P., Korde, A., Ye, L., Lo, J. C., Rasbach, K. A., Boström, E. A., Choi, J. H., Long, J. Z. et al. (2012). A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481, 463-468.
5. Brand, M. D. (2000). Uncoupling to survive? The role of mitochondrial inefficiency in ageing. Exp. Gerontol. 35, 811-820.
6. Caldeira da Silva, C. C., Cerqueira, F. M., Barbosa, L. F., Medeiros, M. H. and Kowaltowski, A. J. (2008). Mild mitochondrial uncoupling in mice affects energy metabolism, redox balance and longevity. Aging Cell 7, 552-560.
7. Cannon, B. and Nedergaard, J. (2004). Brown adipose tissue: Function and physiological significance. Physiol. Rev. 84, 277-359.
8. Cannon, B., Hedin, A. and Nedergaard, J. (1982). Exclusive occurrence of thermogenin antigen in brown adipose tissue. FEBS Lett. 150, 129-132.
9. Divakaruni, A. S. and Brand, M. D. (2011). The regulation and physiology of mitochondrial proton leak. Physiology (Bethesda) 26, 192-205.
10. Dlasková, A., Clarke, K. J. and Porter, R. K. (2010). The role of UCP 1 in production of reactive oxygen species by mitochondria isolated from brown adipose tissue. Bioenergetics 1797, 1470-1476.
11. Gates, A. C., Bernal-Mizrachi, C., Chinault, S. L., Feng, C., Schneider, J. G., Coleman, T., Malone, J. P., Townsend, R. R., Chakravarthy, M. V. and Semenkovich, C. F. (2007). Respiratory uncoupling in skeletal muscle delays death and diminishes age-related disease. Cell Metab. 6, 497-505.
12. Golden, T. R. and Melov, S. (2001). Mitochondrial DNA mutations, oxidative stress, and aging. Mech. Ageing Dev. 122, 1577-1589.
13. Golozoubova, V., Hohtola, E., Matthias, A., Jacobsson, A., Cannon, B. and Nedergaard, J. (2001). Only UCP1 can mediate adaptive nonshivering thermogenesis in the cold. FASEB J 15, 2048-2050.
14. Harman, D. (1956). Aging: A theory based on free radical and radiation chemistry. J. Gerontol. 11, 298-300.
15. Holloszy, J. O. and Smith, E. K. (1986). Longevity of cold-exposed rats: A reevaluation of the 'rate-of-living theory'. J. Appl. Physiol. 61, 1656-1660.
16. Janský, L. (1973). Non-shivering thermogenesis and its thermoregulatory significance. Biol. Rev. Camb. Philos. Soc. 48, 85-132.
17. Kaushik, S. and Kaur, J. (2003). Chronic cold exposure affects the antioxidant defense system in various rat tissues. Clin. Chim. Acta 333, 69-77.
18. Klingenberg, M. (1990). Mechanism and evolution of the uncoupling protein of brown adipose tissue. Trends Biochem. Sci. 15, 108-112.
19. Klingenspor, M. (2003). Cold-induced recruitment of brown adipose tissue thermogenesis. Exp. Physiol. 88, 141-148.
20. Lambert, A. J. and Brand, M. D. (2009). Reactive oxygen species production by mitochondria. Methods Mol. Biol. 554, 165-181.
21. McArdle, A., Pattwell, D., Vasilaki, A., Griffiths, R. D. and Jackson, M. J. (2001). Contractile activity-induced oxidative stress: Cellular origin and adaptive responses. Am. J. Physiol. 280, C621-C627.
22. Meyer, C. W., Willershäuser, M., Jastroch, M., Rourke, B. C., Fromme, T., Oelkrug, R., Heldmaier, G. and Klingenspor, M. (2010). Adaptive thermogenesis and thermal conductance in wild-type and UCP1-KO mice. Am. J. Physiol. 299, R1396- R1406.
23. Mookerjee, S. A., Divakaruni, A. S., Jastroch, M. and Brand, M. D. (2010). Mitochondrial uncoupling and lifespan. Mech. Ageing Dev. 131, 463-472.
24. Murphy, M. P. (2009). How mitochondria produce reactive oxygen species. Biochem. J. 417, 1-13.
25. Nicholls, D. G., Ferguson, S. J. and Ferguson, S. (2002). Bioenergetics, 3rd edn. London; San Diego, CA: Elsevier Academic Press.
26. Oelkrug, R. (2013). New Perspectives on the Significance of Brown Adipose Tissue in Mammals. PhD thesis.
27. Oelkrug, R., Kutschke, M., Meyer, C. W., Heldmaier, G. and Jastroch, M. (2010). Uncoupling protein 1 decreases superoxide production in brown adipose tissue mitochondria. J. Biol. Chem. 285, 21961-21968.
28. Ortega-Molina, A., Efeyan, A., Lopez-Guadamillas, E., Muñoz-Martin, M., Gómez- López, G., Cañamero, M., Mulero, F., Pastor, J., Martinez, S., Romanos, E. et al. (2012). Pten positively regulates brown adipose function, energy expenditure, and longevity. Cell Metab. 15, 382-394.
29. Ouellet, V., Labbé, S. M., Blondin, D. P., Phoenix, S., Guérin, B., Haman, F., Turcotte, E. E., Richard, D. and Carpentier, A. C. (2012). Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans. J. Clin. Invest. 122, 545-552.
30. Pearl, R. (1928). The Rate of Living. London: University of London Press.
31. Petrovic, V., Buzadzic, B., Korac, A., Vasilijevic, A., Jankovic, A., Micunovic, K. and Korac, B. (2008). Antioxidative defence alterations in skeletal muscle during prolonged acclimation to cold: Role of L-arginine/NO-producing pathway. J. Exp. Biol. 211, 114-120.
32. Ricquier, D. and Bouillaud, F. (2000). The uncoupling protein homologues: Ucp1, UCP2, UCP3, StUCP and AtUCP. Biochem. J. 345, 161-179.
33. Salin, K., Luquet, E., Rey, B., Roussel, D. and Voituron, Y. (2012a). Alteration of mitochondrial efficiency affects oxidative balance, development and growth in frog (Rana temporaria) tadpoles. J. Exp. Biol. 215, 863-869.
34. Salin, K., Roussell, D., Rey, B. and Voituron, Y. (2012b). David and Goliath: A mitochondrial coupling problem? J. Exp. Zool. 317, 283-293.
35. Selman, C., Grune, T., Stolzing, A., Jakstadt, M., McLaren, J. S. and Speakman, J. R. (2002). The consequences of acute cold exposure on protein oxidation and proteasome activity in short-tailed field voles, Microtus agrestis. Free Radic. Biol. Med. 33, 259-265.
36. Selman, C., McLaren, J. S., Collins, A. R., Duthie, G. G. and Speakman, J. R. (2008). The impact of experimentally elevated energy expenditure on oxidative stress and lifespan in the short-tailed field vole Microtus agrestis. Proc. Biol. Sci. 275, 1907-1916.
37. Shabalina, I. G. and Nedergaard, J. (2011). Mitochondrial ('mild') uncoupling and ROS production: Physiologically relevant or not? Biochem. Soc. Trans. 39, 1305-1309.
38. Shabalina, I. G., Petrovic, N., Kramarova, T. V., Hoeks, J., Cannon, B. and Nedergaard, J. (2006). UCP1 and defense against oxidative stress. 4-Hydroxy-2- nonenal effects on brown fat mitochondria are uncoupling protein 1-independent. J. Biol. Chem. 281, 13882-13893.
39. Speakman, J. R. and Selman, C. (2011). The free-radical damage theory: Accumulating evidence against a simple link of oxidative stress to ageing and lifespan. Bioessays 33, 255-259.
40. Speakman, J. R., Talbot, D. A., Selman, C., Snart, S., McLaren, J. S., Redman, P., Krol, E., Jackson, D. M., Johnson, M. S. and Brand, M. D. (2004). Uncoupled and surviving: Individual mice with high metabolism have greater mitochondrial uncoupling and live longer. Aging Cell 3, 87-95.
41. St-Pierre, J., Buckingham, J. A., Roebuck, S. J. and Brand, M. D. (2002). Topology of superoxide production from different sites in the mitochondrial electron transport chain. J. Biol. Chem. 277, 44784-44790.
42. Stier, A., Reichert, S., Massemin, S., Bize, P. and Criscuolo, F. (2012). Constraint and cost of oxidative stress on reproduction: Correlative evidence in laboratory mice and review of the literature. Front. Zool. 9, 37.
43. Topp, H., Lengger, C., Schöch, G., Werner, J. and Mietzsch, E. (2000). Renal excretion of 8-oxo-7,8-dihydro-2?-deoxyguanosine in Wistar rats with increased O(2) consumption due to cold stress. Arch. Biochem. Biophys. 376, 328-332.
44. Ukropec, J., Anunciado, R. P., Ravussin, Y., Hulver, M. W. and Kozak, L. P. (2006). UCP1-independent thermogenesis in white adipose tissue of cold-acclimated Ucp1- /- mice. J. Biol. Chem. 281, 31894-31908.
45. Vaanholt, L. M., Daan, S., Schubert, K. A. and Visser, G. H. (2009). Metabolism and aging: Effects of cold exposure on metabolic rate, body composition, and longevity in mice. Physiol. Biochem. Zool. 82, 314-324.
46. Venditti, P., De Rosa, R., Portero-Otin, M., Pamplona, R. and Di Meo, S. (2004). Cold-induced hyperthyroidism produces oxidative damage in rat tissues and increases susceptibility to oxidants. Int. J. Biochem. Cell Biol. 36, 1319-1331.