The effect of metabolic depression on proton leak rate in mitochondria from hibernating frogs

Journal of Experimental Biology

Volumn 203, Issue 9, 2000, Pages 1469-1476

  St Pierre, J ^a   Brand, M D ^a,b   Boutilier, R G ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Electron transport chain; Frog; Hibernation; Hypoxia; Metabolic depression; Mitochondria; Normoxia; Proton conductance; Proton leak; Rana temporaria; Skeletal muscle; State 4

Indexed keywords

CARBONYL CYANIDE 4 (TRIFLUOROMETHOXY)PHENYLHYDRAZONE; PROTON; UNCOUPLING PROTEIN;

ANIMAL; ARTICLE; COLD; COMPARATIVE STUDY; DRUG EFFECT; ENERGY METABOLISM; FEMALE; FROG; HIBERNATION; KINETICS; LIVER MITOCHONDRION; MALE; METABOLISM; MUSCLE MITOCHONDRION; PHYSIOLOGY; RAT; WISTAR RAT;

ANIMALS; CARBONYL CYANIDE P-TRIFLUOROMETHOXYPHENYLHYDRAZONE; COLD; ENERGY METABOLISM; FEMALE; HIBERNATION; KINETICS; MALE; MITOCHONDRIA, LIVER; MITOCHONDRIA, MUSCLE; PROTONS; RANA TEMPORARIA; RATS; RATS, WISTAR; UNCOUPLING AGENTS;

EID: 0034076493     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (50)

1. Akhmerov, R. N. (1986). Qualitative difference in mitochondria of endothermic and ectothermic animals. FEBS Lett. 198, 251-255.
2. Barica, J. and Mathias, J. A. (1979). Oxygen depletion and winterkill risk in small prairie lakes under extended ice cover. J. Fish. Res. Bd Can. 36, 980-986.
3. Boutilier, R. G., Donohoe, P. H., Tattersall, G. J. and West, T. G. (1997). Hypometabolic homeostasis in overwintering aquatic amphibians. J. Exp. Biol. 200, 387-400.
4. Bradford, D. F. (1983). Winterkill, oxygen relations and energy metabolism of a submerged dormant amphibian. Rana muscosa. Ecology 64, 1171-1183.
5. Brand, M. D. (1990). The contribution of the leak of protons across the mitochondrial inner membrane to standard metabolic rate. J. theor. Biol. 145, 267-286.
6. Brand, M. D. (1994). The stoichiometry of proton pumping and ATP synthesis in mitochondria. Biochemist 16, 899-903.
7. Brand, M. D. (1995). Measurement of mitochondrial protonmotive force. In Bioenergetics - A Practical Approach (ed. G. C. Brown and C. E. Cooper), pp. 39-62. Oxford, UK: IRL Press.
8. Brand, M. D., Brindle, K. M., Buckingham, J. A., Harper, J. A., Rolfe, D. F. S. and Stuart, J. A. (1999). The significance and mechanism of mitochondrial proton conductance. Int. J. Obes. 23, S4-S11.
9. Brand, M. D., Chien, L. F. and Diolez, P. (1994a). Experimental discrimination between proton leak and redox slip during mitochondrial electron transport. Biochem. J. 297, 27-29.
10. Brand, M. D., Couture, P., Else, P. L., Withers, K. W. and Hulbert, A. J. (1991). Evolution of energy metabolism: proton permeability of the inner membrane of liver mitochondria is greater in a mammal than in a reptile. Biochem. J. 275, 81-86.
11. Brand, M. D., Couture, P. and Hulbert, A. J. (1994b). Liposomes from mammalian liver mitochondria are more polyunsaturated and leakier to protons than those from reptiles. Comp. Biochem. Physiol. 108B, 181-188.
12. Brand, M. D. and Murphy, M. P. (1987). Control of electron flux through the respiratory chain in mitochondria and cells. Biol. Rev. 62, 141-193.
13. Brookes, P. S., Buckingham, J. A., Tenreiro, A. M., Hulbert, A. J. and Brand, M. D. (1998). The proton permeability of the inner membrane of liver mitochondria from ectothermic and endothermic vertebrates and from obese rats: correlations with standard metabolic rate and phospholipid fatty acid composition. Comp. Biochem. Physiol. 119B, 325-334.
14. Brookes, P. S., Hulbert, A. J. and Brand, M. D. (1997a). The proton permeability of liposomes made from mitochondrial inner membrane phospholipids: no effect of fatty acid composition. Biochim. Biophys. Acta 1330, 157-164.
15. Brookes, P. S., Rolfe, D. F. S. and Brand, M. D. (1997b). The proton permeability of liposomes made from mitochondrial inner membrane phospholipids: comparison with isolated mitochondria. J. Membr. Biol. 155, 167-174.
16. Brooks, S. P. J. and Storey, K. B. (1997). Glycolytic controls in estivation and anoxia: a comparison of metabolic arrest in land and marine molluscs. Comp. Biochem. Physiol. 118A, 1103-1114.
17. Brustovetsky, N. N., Amerkhanov, Z. G., Popova, E. Y. and Konstantinov, (1990). Reversible inhibition of electron transfer in the ubiquinol cytochrome c reductase segment of the mitochondrial respiratory chain in hibernating ground squirrels. FEBS Lett. 263, 73-76.
18. Brustovetsky, N. N., Egorova, M. V., Iljasova, E. N. and Bakeeva, L. E. (1993). Relationship between structure and function of liver mitochondria from hibernating and active ground squirrels, Citellus undulatus. Comp. Biochem. Physiol. 106B, 125-130.
19. Brustovetsky, N. N., Mayevsky, E. I., Grishina, E. V., Gogvadze, V. G. and Amerkhanov, Z. G. (1989). Regulation of the rate of respiration and oxidative phosphorylation in liver mitochondria from hibernating ground squirrels, Citeilus undulatus. Comp. Biochem. Physiol. 94B, 537-541.
20. Canton, M., Luvisetto, S., Schmehl, I. and Azzone, G. F. (1995). The nature of mitochondrial respiration and discrimination between membrane and pump properties. Biochem. J. 310, 477-481.
21. Donohoe, P. H. and Boutilier, R. G. (1998). The protective effects of metabolic rate depression in hypoxic cold submerged frogs. Respir. Physiol. 111, 325-336.
22. Donohoe, P. H., West, T. G. and Boutilier, R. G. (1998) Respiratory, metabolic and acid-base correlates of aerobic metabolic rate reduction in overwintering frogs. Am. J. Physiol. 43, R704-R710.
23. Dufour, S., Rousse, N., Canioni, P. and Diolez, P. (1996) Top-down control analysis of temperature effect on oxidative phosphorylation. Biochem. J. 314, 743-751.
24. Gehnrich, S. C. and Aprille, J. R. (1988). Hepatic gluconeogenesis and mitochondrial function during hibernation. Comp. Biochem. Physiol. 91B, 11-16.
25. Gornall, A. G., Bardawill, C. J. and David, M. M. J. (1949). Determination of serum proteins by means of the biuret reaction. J. Biol. Chem. 177, 751-766.
26. Guppy, M., Fuery, C. J. and Flanigan, J. E. (1994). Biochemical principles of metabolic depression. Comp. Biochem. Physiol. 109B, 175-189.
27. Guppy, M. and Withers, P. (1999). Metabolic depression in animals; physiological perspectives and biochemical generalizations. Biol. Rev. 74, 1-40.
28. Hafner, R. P. and Brand, M. D. (1991). Effect of protonmotive force on the relative proton stoichiometries of the mitochondrial proton pumps. Biochem. J. 275, 75-80.
29. Hafner, R. P., Nobes, C. D., McGown, A. D. and Brand, M. D. (1988). Altered relationship between protonmotive force and respiration rate in non-phosphorylating liver mitochondria isolated from rats of different thyroid hormone status. Eur. J. Biochem. 178, 511-518.
30. Hand, S. C. and Hardewig, I. (1996). Downregulation of cellular metabolism during environmental stress: mechanisms and implications. Annu. Rev. Physiol. 58, 539-563.
31. Hillman, S. S., Lea, M. S. and Duerr, J. M. (1991). Osmotic effects on mitochondria from two species of amphibians, Bufo marinus and Rana catesbeiana. Physiol. Zool. 64, 1552-1560.
32. Hochachka, P. W., Land, S. C. and Buck, L. T. (1997). Oxygen sensing and signal transduction in metabolic defense against hypoxia: lessons from vertebrate facultative anaerobes. Comp. Biochem. Physiol. 118A, 23-29.
33. Hochachka, P. W. and Somero, G. N. (1984). Biochemical Adaptation. Princeton, NJ: Princeton University Press.
34. Kwast, K. E. and Hand, S. C. (1996). Acute depression of mitochondrial protein synthesis during anoxia: contributions of oxygen sensing, matrix acidification and redox state. J. Biol. Chem. 271, 7313-7319.
35. Liu, C. C., Frehn, J. L. and LaPorta, A. D. (1969). Liver and brown fat mitochondrial response to cold in hibernators and nonhibernators. J. Appl. Physiol. 27, 83-89.
36. Martin, S. L., Maniero, G. D., Carey, C. and Hand, S. C. (1999). Reversible depression of oxygen consumption in isolated liver mitochondria during hibernation. Physiol. Biochem. Zool. 72, 255-264.
37. Pehowich, D. J. and Wang, L. C. H. (1984). Seasonal changes in mitochondrial succinate dehydrogenase activity in a hibernator, Spermophilus richardsonii. J. Comp. Physiol. 154B, 495-501.
38. Pinder, A. W., Storey, K. B. and Ultsch, G. R. (1992). Estivation and hibernation. In Environmental Physiology of the Amphibians (ed. M. E. Feder and W. W. Burggren), pp. 250-274. Chicago: The University of Chicago Press.
39. + leak in mitochondria and its relevance to metabolic rate. Nature 362, 628-630.
40. Porter, R. K., Hulbert, A. J. and Brand, M. D. (1996). Allometry of mitochondrial proton leak: influence of membrane surface area and fatty acid composition. Am. J. Physiol. 271, R1550-R1560.
41. Ramsey, J. J., Johnson, D. E., Hossner, K. L. and Johnson, K. A. (1996). Metabolic rate, organ mass and mitochondrial proton leak variations in lean and obese rats. Comp. Biochem. Physiol. 113B, 461-466.
42. Rolfe, D. F. S. and Brand, M. D. (1996). Contribution of mitochondrial proton leak to skeletal muscle respiration and to standard metabolic rate. Am. J. Physiol. 271, C1380-C1389.
43. Rolfe, D. F. S. and Brown, G. C. (1997). Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol. Rev. 77, 731-758.
44. Rolfe, D. F. S., Hulbert, A. J. and Brand, M. D. (1994). Characteristics of mitochondrial proton leak and control of oxidative phosphorylation in the major oxygen-consuming tissues of the rat. Biochim. Biophys. Acta 1188, 405-416.
45. Rolfe, D. F. S., Newman, J. M. B., Buckingham, J. A., Clark, M. G. and Brand, M. D. (1999). Contribution of mitochondrial proton leak to respiration rate in working skeletal muscle and liver and to SMR. Am. J. Physiol. 276, C692-C699.
46. Staples, J. F. and Hochachka, P. W. (1997). Liver energy metabolism during hibernation in the golden-mantled ground squirrel, Spermophilus lateralis. Can. J. Zool. 74, 1059-1065.
47. Storey, K. B. (1997). Metabolic regulation in mammalian hibernation: enzyme and protein adaptations. Comp. Biochem. Physiol. 118A, 1115-1124.
48. Storey, K. B. and Storey, J. M. (1990). Metabolic rate depression and biochemical adaptation in anaerobiosis, hibernation and estivation. Q. Rev. Biol. 65, 145-174.
49. Stuart, J. A., Gillis, T. E. and Ballantyne, J. S. (1998a). Compositional correlates of metabolic depression in the mitochondrial membrane of estivating snails. Am. J. Physiol. 44, R1977-R1982.
50. Stuart, J. A., Gillis, T. E. and Ballantyne, J. S. (1998b). Remodeling of phospholipid fatty acids in mitochondrial membranes of estivating snails. Lipids 33, 787-793.