Mitochondrial metabolism during daily torpor in the dwarf Siberian hamster: Role of active regulated changes and passive thermal effects

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 293, Issue 5, 2007, Pages

  Brown, Jason C L ^a   Gerson, Alexander R ^a   Staples, James F ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Oxidative phosphorylation; Phodopus sungorus; Proton conductance; Top down elasticity analysis

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; LETHARGY; LIVER MITOCHONDRION; METABOLIC RATE; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PHODOPUS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TEMPERATURE DEPENDENCE;

ADENOSINE DIPHOSPHATE; ANIMALS; BODY TEMPERATURE REGULATION; BODY WEIGHT; CITRATE (SI)-SYNTHASE; CRICETINAE; HIBERNATION; KINETICS; MEMBRANE POTENTIALS; MITOCHONDRIA, LIVER; NADH DEHYDROGENASE; OXIDATION-REDUCTION; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PHODOPUS; PHOTOPERIOD; SUCCINATE CYTOCHROME C OXIDOREDUCTASE; TEMPERATURE;

EID: 36049014906     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00310.2007     Document Type: Article

References (72)

1. Ainscow EK, Brand MD. The responses of rat hepatocytes to glucagon and adrenaline: application of quantified elasticity analysis. Eur J Biochem 265: 1043-1055, 1999.
2. Arnold W. Social thermoregulation during hibernation in alpine marmots (Marmota marmota). J Comp Physiol [B] 158: 151-156, 1988.
3. Barger JL, Brand MD, Barnes BM, Boyer BB. Tissue-specific depression of mitochondrial proton leak and substrate oxidation in hibernating arctic ground squirrels. Am J Physiol Regul Integr Comp Physiol 284: R1306-R1313, 2003.
4. Bishop T, St-Pierre J, Brand MD. Primary causes of decreased mitochondrial oxygen consumption during metabolic depression in snail cells. Am J Physiol Regul Integr Comp Physiol 282: R372-R382, 2002.
5. Brand MD, Harper ME, Taylor HC. Control of the effective P/O ratio of oxidative phosphorylation in liver mitochondria and hepatocytes. Biochem J 291: 739-748, 1993.
6. Brand MD, Chien LF, Diolez P. Experimental discrimination between proton leak and redox slip during mitochondrial electron transport. Biochem J 297: 27-29, 1994.
7. Brand MD, Chien LF, Ainscow EK, Rolfe DFS, Porter RK. The causes and functions of mitochondrial proton leak. Biochim Biophys Acta 1187: 132-139, 1994.
8. Brand MD. Top-down elasticity analysis and its application to energy metabolism in isolated mitochondria and intact cells. Mol Cell Biochem 184: 13-20, 1998.
9. Brand MD, Pakay JL, Ocloo A, Kokoszka J, Wallace DC, Brookes PS. The basal proton conductance of mitochondria depends on adenine nucleotide translocase content. Biochem J 392: 353-362, 2005.
10. + leak and ROS generation: an odd couple. Free Radic Biol Med 38: 12-23, 2005.
11. Brustovetsky NN, Amerkhanov ZG, Popova EY, Konstantinov AA. 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, 1990.
12. Buttgereit F, Grant A, Muller M. The effects of methylprednisolone on oxidative phosphorylation in concanavalin-A-stimulated thymocytes: top down elasticity analysis and control analysis. Eur J Biochem 223: 513-519, 1994.
13. Cadenas E. Biochemistry of oxygen toxicity. Annu Rev Biochem 58: 79-110, 1989.
14. Chamberlin ME. Top-down control analysis of the effect of temperature on ecotherm oxidative phosphorylation. Am J Physiol Regul Integr Comp Physiol 287: R794-R800, 2004.
15. Dark J, Miller DR, Licht P, Zucker I. Glucoprivation counteracts effects of testosterone on daily torpor in Siberian hamsters. Am J Physiol Regul Integr Comp Physiol 270: R398-R403, 1996.
16. Demura M, Kamo N, Kobatake Y. Binding of lipophilic cations to the liposomal membrane: thermodynamic analysis. Biochim Biophys Acta 903: 303-308, 1987.
17. Diaz MB, Lange M, Heldmaier G, Klingenspor M. Depression of transcription and translation during daily torpor in the Djungarian hamster (Phodopus sungorus). J Comp Physiol [B] 174: 495-502, 2004.
18. Dufour S, Rousse N, Canioni P, Diolez P. Top-down control analysis of temperature effect on oxidative phosphorylation. Biochem J 314: 743-751, 1996.
19. Duong CA, Sepulveda CA, Graham JB, Dickson KA. Mitochondrial proton leak rates in the slow, oxidative myotomal muscle and liver of the endothermic shortfin mako shark (Isurus oxyrinchus) and the ectothermic blue shark (Prionace glauca) and leopard shark (Triakis semifasciata). J Exp Biol 209: 2678-2685, 2006.
20. + transport in mitochondria during hibernation. Comp Biochem Physiol B 82: 191-195, 1985.
21. Florant GL, Heller HC. CNS regulation of body temperature in euthermic and hibernating marmots (Marmota flaviventris). Am J Physiol Regul Integr Comp Physiol 232: R203-R208, 1977.
22. Frerichs KU, Smith CB, Brenner M, DeGracia DJ, Krause GS, Marrone L, Dever TE, Hallenbeck JM. Suppression of protein synthesis in brain during hibernation involves inhibition of protein initiation and elongation. Proc Natl Acad Sci USA 95: 14511-14516, 1998.
23. Gehnrich SC, Aprille JR. Hepatic gluconeogenesis and mitochondrial function during hibernation. Comp Biochem Physiol B 91: 11-16, 1988.
24. Geiser F. Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu Rev Physiol 66: 239-274, 2004.
25. Grivennikova VG, Kapustin AN, Vinogradov AD. Catalytic activity of NADH-ubiquinone oxidoreductase (complex I) in intact mitochondria: evidence for the slow active/deactive transition. J Biol Chem 276: 9038-9044, 2001.
26. Groen AK, Wanders RJA, Westerhoff HV, van der Meer R, Tager JM. Quantification of the contribution of various steps to the control of mitochondrial respiration. J Biol Chem 257: 2754-2757, 1982.
27. Guderley H, Turner N, Else PL, Hulbert AJ. Why are some mitochondria more powerful than others: insights from comparisons of muscle mitochondria from three terrestrial vertebrates. Comp Biochem Physiol B 142: 172-180, 2005.
28. Gutman M. Modulation of mitochondrial succinate dehydrogenase activity, mechanism and function. Mol Cell Biochem 20: 41-60, 1978.
29. Guppy M, Withers P. Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol Rev 74: 1-40, 1999.
30. Hafner RP, Brown GC, Brand MD. Analysis of the control of respiration rate, phosphorylation rate, proton leak rate and protonmotive force in isolated mitochondria using the "top-down" approach of metabolic control theory. Eur J Biochem 188: 313-319, 1990.
31. Halestrap AP. The regulation of the matrix volume of mammalian mitochondria in vivo and in vitro and its role in the control of mitochondrial metabolism. Biochim Biophys Acta 973: 335-382, 1989.
32. Harper ME, Brand MD. The quantitative contributions of mitochondrial proton leak and ATP turnover reactions to the changed respiration rates of hepatocytes from rats of different thyroid status. J Biol Chem 268: 14850-14860, 1993.
33. Harper ME, Brand MD. Use of top-down elasticity analysis to identify sites of thyroid hormone-induced thermogenesis. Proc Soc Exp Biol Med 208: 228-237, 1995.
34. Heldmaier G, Steinlechner S. Seasonal pattern and energetics of short daily torpor in the Djungarian hamster, Phodopus sungorus. Oecologia 48: 265-270, 1981.
35. Heldmaier G, Ruf T. Body temperature and metabolic rate during natural hypothermia in endotherms. J Comp Physiol [B] 162: 696-706, 1992.
36. Heldmaier G, Klingenspor M, Werneyer M, Lampi BJ, Brooks SPJ, Storey KB. Metabolic adjustments during daily torpor in the Djungarian hamster. Am J Physiol Endocrinol Metab 276: E896-E906, 1999.
37. Heldmaier G, Elvert R. How to enter torpor: thermodynamic and physiological mechanisms of metabolic depression. In: Life in the Cold: Evolution, Mechanisms, Adaptations, and Application, edited by Barnes BM, Carey HV. Fairbanks, AK: University of Alaska Press, 2004.
38. Hiebert SM, Fulkerson EK, Lindermayer KT, McClure SD. Effect of temperature on preference for dietary unsaturated fatty acids in the Djungarian hamster (Phodopus sungorus). Can J Zool 78: 1361-1368, 2000.
39. Humphries MM, Thomas DW, Kramer DL. The role of energy availability in mammalian hibernation: a cost-benefit approach. Physiol Biochem Zool 76: 165-179, 2003.
40. Hwang YT, Larivière S, Messier F. Energetic consequences and ecological significance of heterothermy and social thermoregulation in striped skunks (Mephitis mephitis). Physiol Biochem Zool 80: 138-145.
41. Jefimow M, Wojciechowski M, Masuda A, Oishi T. Correlation between torpor frequency and capacity for nonshivering thermogenesis in the Siberian hamster (Phodopus sungorus). J Therm Biol 29: 641-647, 2004.
42. Kayser EB, Sedensky MM, Morgan PG, Hoppel CL. Mitochondrial oxidative phosphorylation is defective in the long-lived mutant clk-1. J Biol Chem 279: 54479-54486, 2004.
43. Kemp TS. The origin of mammalian endothermy: a paradigm for the evolution of complex biological structure. Zool J Linnean Soc 147: 473-488, 2006.
44. Lombardi A, Lanni A, Moreno M, Brand MD, Goglia F. Effect of 3,5-di-iodo-L-thyronine on the mitochondrial energy-transduction apparatus. Biochem J 330: 521-526, 1998.
45. Lyman CP, O'Brien RC, Greene GC, Papafrangos ED. Hibernation and longevity in the Turkish hamster, Mesocricetus brandti. Science 212: 668-670, 1981.
46. Lyman CP, Willis JS, Malan A, Wang LCH. Hibernation and torpor in mammals and birds. New York: Academic, 1982.
47. +-ATPase activity by reversible phosphorylation in hibernation. Biochem Biophys Res Commun 254: 424-429, 1999.
48. Marcinkeviciute A, Mildaziene V, Crumm S, Demin O, Hoek JB, Kholodenko B. Kinetics and control of oxidative phosphorylation in rat liver mitochondria after chronic ethanol feeding. Biochem J 349: 519-526, 2000.
49. Martin AW, Fuhrman FA. The relationship between summated tissue respiration and metabolic rate in the mouse and dog. Physiol Zool 28: 18-34, 1955.
50. Martin SM, Maniero GD, Carey C, Hand SC. Reversible depression of oxygen consumption in isolated liver mitochondria during hibernation. Physiol Biochem Zool 72: 255-264, 1999.
51. Mildaziene V, Nauciene Z, Baniene R, Grigiene J. Multiple effects of 2,2′,5,5′-tetrachlorobiphenyl on oxidative phosphorylation in rat liver mitochondria. Toxicol Sci 65: 220-227, 2002.
52. Muleme HM, Walpole AC, Staples JF. Mitochondrial metabolism in hibernation: metabolic suppression, temperature effects, and substrate preferences. Physiol Biochem Zool 79: 474-483, 2006.
53. Ortmann S, Heldmaier G. Regulation of body temperature and energy requirements of hibernating Alpine marmots (Marmota marmota). Am J Physiol Regul Integr Comp Physiol 278: R698-R704, 2000.
54. Papa S, Sardanelli AM, Scacco S, Petruzzella V, Technikova-Dobrova Z, Vergari R, Signorile A. The NADH: ubiquinone oxidoreductase (complex I) of the mammalian respiratory chain and the cAMP cascade. J Bioenerg Biomembr 34: 1-10, 2002.
55. Pehowich DJ, Wang LCH. Seasonal changes in mitochondrial succinate dehydrogenase activity in a hibernator, Spermophilus richardsonii. J Comp Physiol [B] 154: 495-501, 1984.
56. +-pumps in mitochondria: on the nature of "leaks". Eur J Biochem 117: 389-394, 1981.
57. Porter RK, Hulbert AJ, Brand MD. Allometry of mitochondria proton leak: influence of membrane surface area and fatty acid composition. Am J Physiol Regul Integr Comp Physiol 271: R1550-R1560, 1996.
58. 2 solubility in aqueous media determined by a kinetic method. Anal Biochem 145: 406-418, 1985.
59. Rolfe DFS, Brand MD. The physiological significance of mitochondrial proton leak in animal cells and tissues. Biosci Rep 17: 9-16, 1997.
60. Rolfe DFS, Hulbert AJ, Brand MD. 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, 1994.
61. Rolfe DFS, Brown GC. Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77: 731-758, 1997.
62. Rottenberg H. Metabolic potential and surface potential in mitochondria: uptake and binding of lipophilic cations. J Membr Biol 81: 127-138, 1984.
63. 10 and energy metabolism during daily torpor and hibernation in rodents. J Comp Physiol [B] 159: 667-675, 1990.
64. Stahl WR. Organ weights in primates and other mammals. Science 150: 1039-1042, 1965.
65. St-Pierre J, Brand MD, Boutilier RG. The effect of metabolic depression on proton leak rate in mitochondria from hibernating frogs. J Exp Biol 203: 1469-1476, 2000.
66. Sutherland BA, Shaw OM, Clarkson AN, Jackson DM, Sammut IA, Appleton I. Neuroprotective effects of (-)-epigallocatechin gallate after hypoxia-ischemia-induced brain damage: novel mechanisms of action. FASEB J 19: 258-260, 2005.
67. Takaki M, Nakahara H, Kawatani Y, Utsumi K, Suga H. No suppression of respiratory function of mitochondria isolated from the hearts of anesthetized rats with high-dose pentobarbital sodium. Jpn J Physiol 47: 87-92, 1997.
68. Toien O, Drew KL, Chao ML, Rice ME. Ascorbate dynamics and oxygen consumption during arousal from hibernation in Arctic ground squirrels. Am J Physiol Regul Integr Comp Physiol 281: R572-R583, 2001.
69. Trounce IA, Kim YL, Jun AS, Wallace DC. Assessment of mitochondrial oxidative phosphorylation in patient muscle biopsies, lymphoblasts, and transmitochondrial cell lines. Methods Enzymol 264: 484-509, 1996.
70. Van Voorhies WA. Metabolism and lifespan. Exp Gerontol 36: 55-64, 2001.
71. Wilkinson GS, South JM. Life history, ecology and longevity in bats. Aging Cell 1: 124-131, 2002.
72. Wu BJ, Hulbert AJ, Storlien LH, Else PL. Membrane lipids and sodium pumps of cattle and crocodiles: an experimental test of the membrane pacemaker theory of metabolism. Am J Physiol Regul Integr Comp Physiol 287: R633-R641, 2004.