Cold acclimation increases mitochondrial oxidative capacity without inducing mitochondrial uncoupling in goldfish white skeletal muscle

Biology Open

Volumn 2, Issue 1, 2013, Pages 82-87

  Dos Santos, Reinaldo Sousa ^a   Galina, Antonio ^a   Da Silva, Wagner Seixas ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Cold acclimation; Mitochondria; Skeletal muscle

Indexed keywords

EID: 84878655887     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.20122295     Document Type: Article

References (44)

1. Andreyev, A. Y., Bondareva, T. O., Dedukhova, V. I., Mokhova, E. N., Skulachev, V. P., Tsofina, L. M., Volkov, N. I. and Vygodina, T. V. (1989). The ATP/ADPantiporter is involved in the uncoupling effect of fatty acids on mitochondria. Eur. J. Biochem. 182, 585-592.
2. Battersby, B. J. and Moyes, C. D. (1998). Influence of acclimation temperature on mitochondrial DNA, RNA, and enzymes in skeletal muscle. Am. J. Physiol. 275, R905-R912.
3. Bicudo, J. E., Bianco, A. C. and Vianna, C. R. (2002). Adaptive thermogenesis in hummingbirds. J. Exp. Biol. 205, 2267-2273.
4. Brand, M. D. and Esteves, T. C. (2005). Physiological functions of the mitochondrial uncoupling proteins UCP2 and UCP3. Cell Metab. 2, 85-93.
5. Brand, M. D., Pakay, J. L., Ocloo, A., Kokoszka, J., Wallace, D. C., Brookes, P. S. and Cornwall, E. J. (2005). The basal proton conductance of mitochondria depends on adenine nucleotide translocase content. Biochem. J. 392, 353-362.
6. Bremer, K., Monk, C. T., Gurd, B. J. and Moyes, C. D. (2012). Transcriptional regulation of temperature-induced remodeling of muscle bioenergetics in goldfish. Am. J. Physiol. 303, R150-R158.
7. Cannon, B. and Nedergaard, J. (2011). Nonshivering thermogenesis and its adequate measurement in metabolic studies. J. Exp. Biol. 214, 242-253.
8. Chappell, J. B. and Perry, S. V. (1954). Biochemical and osmotic properties of skeletal muscle mitochondria. Nature 173, 1094-1095.
9. dos Santos, R. S., Diniz, L. P., Galina, A. and da-Silva, W. S. (2010). Characterization of non-cytosolic hexokinase activity in white skeletal muscle from goldfish (Carassius auratus L.) and the effect of cold acclimation. Biosci. Rep. 30, 413-423.
10. Egginton, S. and Johnston, I. A. (1984). Effects of acclimation temperature on routine metabolism muscle mitochondrial volume density and capillary supply in the elver (Anguilla anguilla L.). J. Therm. Biol. 9, 165-170.
11. Egginton, S. and Sidell, B. D. (1989). Thermal acclimation induces adaptive changes in subcellular structure of fish skeletal muscle. Am. J. Physiol. 256, R1-R9.
12. Gnaiger, E. (2001). Bioenergetics at low oxygen: dependence of respiration and phosphorylation on oxygen and adenosine diphosphate supply. Respir. Physiol. 128, 277-297.
13. Gnaiger, E., Kuznetsov, A. V., Schneeberger, S., Seiler, R., Brandacher, G., Steurer, W. and Margreiter, R. (2000). Mitochondria in the cold. In Life In The Cold (ed. G. Heldmaier and M. Klingenspor), pp. 431-442. Berlin: Springer.
14. Gracey, A. Y., Fraser, E. J., Li, W., Fang, Y., Taylor, R. R., Rogers, J., Brass, A. and Cossins, A. R. (2004). Coping with cold: An integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate. Proc. Natl. Acad. Sci. USA 101, 16970-16975.
15. Guderley, H. (2004). Metabolic responses to low temperature in fish muscle. Biol. Rev. Camb. Philos. Soc. 79, 409-427.
16. Guderley, H. and Johnston, I. I. (1996). Plasticity of fish muscle mitochondria with thermal acclimation. J. Exp. Biol. 199, 1311-1317.
17. Guderley, H. and Seebacher, F. (2011). Thermal acclimation, mitochondrial capacities and organ metabolic profiles in a reptile (Alligator mississippiensis). J. Comp. Physiol. B 181, 53-64.
18. Guderley, H., St Pierre, J., Couture, P. and Hulbert, A. J. (1997). Plasticity of the properties of mitochondria from rainbow trout red muscle with seasonal acclimatization. Fish Physiol. Biochem. 16, 531-541.
19. Harding, M. M., Anderberg, P. I. and Haymet, A. D. (2003). 'Antifreeze' glycoproteins from polar fish. Eur. J. Biochem. 270, 1381-1392.
20. Hazel, J. R. (1972a). The effect of temperature acclimation upon succinic dehydrogenase activity from the epaxial muscle of the common goldfish (Carassius auratus L)-I. Properties of the enzyme and the effect of lipid extraction. Comp. Biochem. Physiol. 43B, 837-861.
21. Hazel, J. R. (1972b). The effect of temperature acclimation upon succinic dehydrogenase activity from the epaxial muscle of the common goldfish (Carassius auratus L)-II. Lipid reactivation of the soluble enzyme. Comp. Biochem. Physiol. 43B, 863-882.
22. Hazel, J. R. and Prosser, C. L. (1974). Molecular mechanisms of temperature compensation in poikilotherms. Physiol. Rev. 54, 620-677.
23. Hochachka, P. W. and Somero, G. N. (2002). Cellular metabolism, regulation, and homeostasis. In Biochemical Adaptation: Mechanism And Process In Physiological Evolution, pp. 290-450. New York: Oxford University Press.
24. Johnston, I. A. and Dunn, J. (1987). Temperature acclimation and metabolism in ectotherms with particular reference to teleost fish. Symp. Soc. Exp. Biol. 41, 67-93.
25. Johnston, I. A. and Lucking, M. (1978). Temperature induced variation in the distribution of different types of muscle fibre in the goldfish (Carassius auratus). J. Comp. Physiol. 124B, 111-116.
26. Krauss, S., Zhang, C. Y. and Lowell, B. B. (2005). The mitochondrial uncouplingprotein homologues. Nat. Rev. Mol. Cell Biol. 6, 248-261.
27. Kuznetsov, A. V., Schneeberger, S., Seiler, R., Brandacher, G., Mark, W., Steurer, W., Saks, V., Usson, Y., Margreiter, R. and Gnaiger, E. (2004). Mitochondrial defects and heterogeneous cytochrome c release after cardiac cold ischemia and reperfusion. Am. J. Physiol. 286, H1633-H1641.
28. LeMoine, C. M., Genge, C. E. and Moyes, C. D. (2008). Role of the PGC-1 family in the metabolic adaptation of goldfish to diet and temperature. J. Exp. Biol. 211, 1448-1455.
29. Lowry, O. H., Rosebrough, N. J., Farr, A. L. and Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275.
30. Lucassen, M., Koschnick, N., Eckerle, L. G. and Pörtner, H. O. (2006). Mitochondrial mechanisms of cold adaptation in cod (Gadus morhua L.) populations from different climatic zones. J. Exp. Biol. 209, 2462-2471.
31. Makinen, M. W. and Lee, C. P. (1968). Biochemical studies of skeletal muscle mitochondria. I. Microanalysis of cytochrome content, oxidative and phosphorylative activities of mammalian skeletal muscle mitochondria. Arch. Biochem. Biophys. 126, 75-82.
32. McClelland, G. B., Craig, P. M., Dhekney, K. and Dipardo, S. (2006). Temperatureand exercise-induced gene expression and metabolic enzyme changes in skeletal muscle of adult zebrafish (Danio rerio). J. Physiol. 577, 739-751.
33. Nedergaard, J. and 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.
34. O'Brien, K. M. (2011). Mitochondrial biogenesis in cold-bodied fishes. J. Exp. Biol. 214, 275-285.
35. O'Brien, K. M. and Mueller, I. A. (2010). The unique mitochondrial form and function of Antarctic channichthyid icefishes. Integr. Comp. Biol. 50, 993-1008.
36. Orczewska, J. I., Hartleben, G. and O'Brien, K. M. (2010). The molecular basis of aerobic metabolic remodeling differs between oxidative muscle and liver of threespine sticklebacks in response to cold acclimation. Am. J. Physiol. 299, R352-R364.
37. Picard, M., Taivassalo, T., Ritchie, D., Wright, K. J., Thomas, M. M., Romestaing, C. and Hepple, R. T. (2011). Mitochondrial structure and function are disrupted by standard isolation methods. PLoS ONE 6, e18317.
38. Seebacher, F., Brand, M. D., Else, P. L., Guderley, H., Hulbert, A. J. and Moyes, C. D. (2010). Plasticity of oxidative metabolism in variable climates: molecular mechanisms. Physiol. Biochem. Zool. 83, 721-732.
39. Sidell, B. D. (1980). Responses of goldfish (Carassius auratus, L.) muscle to acclimation temperature: alterations in biochemistry and proportions of different fiber types. Physiol. Zool. 53, 98-107.
40. Somero, G. N. (2004). Adaptation of enzymes to temperature: searching for basic "strategies". Comp. Biochem. Physiol. 139B, 321-333.
41. Sperl, W., Skladal, D., Gnaiger, E., Wyss, M., Mayr, U., Hager, J. and Gellerich, F. N. (1997). High resolution respirometry of permeabilized skeletal muscle fibers in the diagnosis of neuromuscular disorders. Mol. Cell. Biochem. 174, 71-78.
42. Trzcionka, M., Withers, K. W., Klingenspor, M. and Jastroch, M. (2008). The effects of fasting and cold exposure on metabolic rate and mitochondrial proton leak in liver and skeletal muscle of an amphibian, the cane toad Bufo marinus. J. Exp. Biol. 211, 1911-1918.
43. Tyler, S. and Sidell, B. D. (1984). Changes in mitochondrial distribution and diffusion distances in muscle of goldfish upon acclimation to warm and cold temperatures. J. Exp. Zool. 232, 1-9.
44. van den Thillart, G. and Modderkolk, J. (1978). The effect of acclimation temperature on the activation energies of state III respiration and on the unsaturation of membrane lipids of goldfish mitochondria. Biochim. Biophys. Acta 510, 38-51.