Mitochondrial metabolism in hibernation and daily torpor: A review

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

Volumn 178, Issue 7, 2008, Pages 811-827

  Staples, James F ^a   Brown, Jason C L ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Hibernation; Mitochondria; Oxidative phosphorylation; Proton leak; Torpor

Indexed keywords

ANIMAL; BASAL METABOLIC RATE; BODY TEMPERATURE; BREATHING; HIBERNATION; LIVER MITOCHONDRION; METABOLISM; MITOCHONDRIAL MEMBRANE; PHYSIOLOGY; REVIEW;

ANIMALS; BASAL METABOLISM; BODY TEMPERATURE; HIBERNATION; MITOCHONDRIA, LIVER; MITOCHONDRIAL MEMBRANES; RESPIRATION;

AVES; MAMMALIA;

EID: 49349102919     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-008-0282-8     Document Type: Review

References (117)

1. ZG Amerkhanov MV Yegorova OV Markova EN Mokhova 1996 Carboxyatractylate- and cyclosporin A-sensitive uncoupling in liver mitochondria of ground squirrels during hibernation and arousal Biochem Mol Biol Int 38 863 870
2. ML Augee DJ Pehowich JK Raison LCH Wang 1984 Seasonal and temperature-related changes in mitochondrial membranes associated with torpor in the mammalian hibernator Spermophilus richardsonii Biochim Biophys Acta 776 27 36
3. J Barger MD Brand BM Barnes BB Boyer 2003 Tissue-specific depression of mitochondrial proton leak and substrate oxidation in hibernating arctic ground squirrels Am J Physiol 284 R1306 R1313
4. JL Barger BM Barnes BB Boyer 2006 Regulation of UCP1 and UCP3 in arctic ground squirrels and relation with mitochondrial proton leak J Appl Physiol 101 339 347
5. T Bishop J St-Pierre MD Brand 2002 Primary causes of decreased mitochondrial oxygen consumption during metabolic depression in snail cells Am J Physiol Regul Integr Comp Physiol 282 R372 R382
6. 2S induces a suspended animation-like state in mice Science 308 518
7. BB Boyer BM Barnes BB Lowell D Grujic 1998 Differential regulation of uncoupling protein gene homologues in multiple tissues of hibernating ground squirrels Am J Physiol 275 R1232 R1238
8. MD Brand JL Pakay A Ocloo J Kokoszka DC Wallace PS Brookes EJ Cornwall 2005 The basal proton conductance of mitochondria depends on adenine nucleotide translocase content Biochem J 392 353 362
9. RM Brigham CD Inanuzzo N Hamilton MB Fenton 1990 Histochemical and biochemical plasticity of muscle fibers in the little brown bat (Myotis lucifugus) J Comp Physiol B 160 183 186
10. GE Bronnikov SO Vingradova VS Mezentseva 1990 Changes in kinetics of ATP-synthase and in concentrations of adenine nucleotides in ground squirrel liver mitochondria during hibernation Comp Biochem Physiol 97B 411 415
11. SPJ Brooks KB Storey 1992 Mechanisms of glycolytic control during hibernation in the ground squirrel Spermophilus lateralis J Comp Physiol B 162 23 28
12. JCL Brown AR Gerson JF Staples 2007 Mitochondrial metabolism during daily torpor in the dwarf Siberian hamster: the role of active regulated changes and passive thermal effects Am J Physiol Regul Integr Comp Physiol 293 R1833 R1845
13. NN Brustovetsky EI Mayevsky EV Grishina VG Gogvadze ZG Amerkhanov 1989 Regulation of the rate of respiration and oxidative phosphorylation in liver mitochondria from hibernating ground squirrels, Citellus undulatus Comp Biochem Physiol 94B 537 541
14. NN Brustovetsky ZG Amerkhanov EY Popova AA Konstantinov 1990 Reversible inhibition of electron transfer in the ubiquinol cytochrome c reductase segment of the mitochondrial respiratory chain in hibernating ground squirrels Fed Eur Biochem Soc 263 73 76
15. N Brustovetsky M Egorova D Gnutov V Gogvadze E Mokhova V Skulachev 1992 Thermoregulatory, carboxyatractylate-sensitive uncoupling in heart and skeletal muscle mitochondria of the ground squirrel correlates with the level of free fatty acids FEBS Lett 305 15 17
16. 2 Comp Biochem Physiol 102B 635 638
17. LC Buck BM Barnes 2000 Effects of ambient temperature on metabolic rate, respiratory quotient, and torpor in an arctic hibernator Am J Physiol 279 R255 R262
18. S Cadenas JA Buckingham S Samec J Seydoux N Din AG Dulloo MD Brand 1999 UCP2 and UCP3 rise in starved rat skeletal muscle but mitochondrial proton conductance is unchanged FEBS Lett 462 257 260
19. H Carey MT Andrews SL Martin 2003 Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature Physiol Rev 83 1153 1181
20. RRJ Chaffee ET Pengelley JR Allen RE Smith 1966 Biochemistry of brown fat and liver of hibernating golden-mantled ground squirrels (Citellus lateralis) Can J Physiol Pharmacol 44 217 223
21. M Chamberlin 2004 Top-down control analysis of the effect of temperature on ectotherm oxidative phosphorylation Am J Physiol 287 R794 R800
22. B Chance GR Williams 1956 The respiratory chain and oxidative phosphorylation Adv Enzymol 17 65 134
23. 2+ -ATPase of a hibernator, the ground squirrel (Spermophilus richardsonii) Comp Biochem Physiol 60B 433 439
24. MB Diaz M Lange G Heldmaier M Klingenspor 2004 Depression of transcription and translation during daily torpor in the Djungarian hamster (Phodopus sungorus) J Comp Physiol B 174 495 502
25. W Droge 2002 Free radicals in the physiological control of cell function Physiol Rev 82 47 95
26. S Dufour N Rousse P Canioni P Diolez 1996 Top-down control analysis of temperature effect on oxidative phosphorylation Biochem J 314 743 751
27. KS Echtay MP Murphy RAJ Smith DA Talbot MD Brand 2002 Superoxide activates mitochondrial uncoupling protein 2 from the matrix side J Biol Chem 277 47129 47135
28. KS Echtay D Roussel J St-Pierre MB Jekabsons S Cadenas JA Stuart JA Harper SJ Roebuck A Morrison S Pickering JC Clapham MD Brand 2002 Superoxide activates mitochondrial uncoupling proteins Nature 415 96 99
29. SF Eddy P Morin KB Storey 2006 Differential expression of selected mitochondrial genes in hibernating little brown bats, Myotis lucifugus J Exp Zool Part A Comp Exp Biol 305A 620 630
30. JW Elrod JW Calvert J Morrison JE Doeller DW Kraus L Tao X Jiao R Scalia L Kiss C Szabo H Kimura C-W Chow DJ Lefer 2007 Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function Proc Natl Acad Sci 104 15560 15565
31. C Entenman PD Ackerman J Walsh XJ Musacchia 1975 Effect of incubation temperature on hepatic palmitate metabolism in rats, hamsters and ground squirrels Comp Biochem Physiol 50B 51 54
32. A Fahlman JM Storey KB Storey 2000 Gene up-regulation in heart during mammalian hibernation Cryobiology 40 332 342
33. + transport in mitochondria during hibernation Comp Biochem Physiol 82B 191 195
34. GL Florant HC Heller 1977 CNS regulation of body temperature in euthermic and hibernating marmots (Marmota flaviventris) Am J Physiol Regul Integr Comp Physiol R232 R203 208
35. ML Fonda GH Herbener RW Cuddihee 1983 Biochemical and morphometric studies of heart, liver and skeletal muscle from the hibernating, arousing and aroused big brown bat, Eptesicus fuscus Comp Biochem Physiol 76B 355 363
36. CL Frank 1992 The influence of dietary fatty acids on hibernation by golden-mantled ground squirrels (Spermophlilus lateralis) Physiol Zool 65 906 920
37. CL Frank 1994 Polyunsaturate content and diet selection by ground squirrels (Spermophilus lateralis) Ecology 75 458 463
38. CL Frank KB Storey 1995 The optimal depot fat composition for hibernation by golden-mantled ground squirrels (Spermophilus lateralis) J Comp Physiol B 164 536 542
39. Frank CL, Storey KB (1996) The effect of unsaturate content on hibernation. In: Geiser F, Hulbert AJ, Nichol SC (eds) Adaptations to the cold. University of New England Press, Armidale NSW, pp 211-216
40. KU Frerichs CB Smith M Brenner DJ DeGarcia GS Krause L Marrone TE Dever JM Hallenback 1998 Suppression of protein synthesis in brain during hibernation involves inhibition of protein initiation and elongation Proc Natl Acad Sci 95 14511 14516
41. T Furono T Kanno K Arita M Asami T Utsumi Y Doi M Inoue K Utsumi 2001 Roles of long chain fatty acids and carnitine in mitochondrial membrane permeability transition Biochem Pharmacol 62 1039 1046
42. WA Galster PR Morrison 1975 Gluconeogenesis in arctic ground squirrels between periods of hibernation Am J Physiol 228 325 330
43. SC Gehnrich JR Aprille 1988 Hepatic gluconeogenesis and mitochondrial function during hibernation Comp Biochem Physiol 91B 11 16
44. F Geiser 1988 Reduction of metabolism during hibernation and daily torpor in mammals and birds: temperature effect or physiological inhibition? J Comp Physiol 158 25 37
45. F Geiser 1991 The effect of unsaturated and saturated dietary lipids on the pattern of daily torpor and the fatty acid composition of tissues and membranes of the deer mouse (Peromyscus maniculatus) J Comp Physiol B 161 590 597
46. F Geiser 2004 Metabolic rate and body temperature reduction during hibernation and daily torpor Ann Rev Physiol 66 239 273
47. F Geiser GJ Kenagy 1987 Polyunsaturated lipid diet lengthens torpor and reduces body temperature in a hibernator Am J Physiol 252 R897 R901
48. F Geiser BM McAllan GJ Kenagy 1994 The degree of dietary fatty acid unsaturation affects torpor patterns and lipid composition of a hibernator J Comp Physiol 164 299 305
49. Gerson AR, Brown JCL, Thomas R, Bernards MA, Staples JF (2008) Effects of dietary polyunsaturated fatty acids on mitochondrial metabolism in mammalian hibernation. J Exp Biol (in press)
50. C Giulivi K Kato CE Cooper 2006 Nitric oxide regulation of mitochondrial oxygen consumption I: cellular physiology Am J Physiol Cell Physiol 291 C1225 C1231
51. A Groen R Wanders H Westerhoff R van der Meer J Tager 1982 Quantification of the contribution of various steps to the control of mitochondrial respiration J Biol Chem 257 2754 2757
52. M Guppy P Withers 1999 Metabolic depression in animals: physiological perspectives and biochemical generalizations Biol Rev 74 1 40
53. RP Hafner MJ Leake MD Brand 1989 Hypothyroidism in rats decreases mitochondrial inner membrane cation permeability FEBS Lett 248 175 178
54. RP Hafner GC Brown MD Brand 1990 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
55. X Han H Cheng DJ Mancuso RW Gross 2004 Caloric restriction results in phospholipid depletion, membrane remodeling, and triacylglycerol accumulation in murine myocardium Biochemistry 43 15584 15594
56. HJ Harlow CL Frank 2001 The role of dietary fatty acids in the evolution of spontaneous and facultative hibernation patterns in prairie dogs J Comp Physiol B 171 77 84
57. M-E Harper MD Brand 1993 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
58. Heldmaier G, Elvert R (2004) How to enter torpor: thermodynamic and physiological mechanisms of metabolic depression. In: Barnes BM, Carey HV (eds) Life in the cold. University of Alaska Fairbanks, Fairbanks, pp 185-198
59. G Heldmaier K Seidl 1985 Plasma free fatty acid levels during cold-induced and noradrenaline-induced nonshivering thermogenesis in the Djungarian hamster J Comp Physiol B 155 679 684
60. G Heldmaier M Klingenspor M Werneyer GJ Lampi SPJ Brooks KB Storey 1999 Metabolic adjustments during daily torpor in the Djungarian hamster Am J Physiol 276 E896 E906
61. HC Heller GW Colliver 1974 CNS regulation of body temperature during hibernation Am J Physiol 227 583 589
62. Heller HC, Colliver GW, Beard J (1977) Thermoregulation during entrance into hibernation. Pflugers Arch 369
63. DS Hittel KB Storey 2002 Differential expression of mitochondria-encoded genes in a hibernating mammal J Exp Biol 205 1625 1631
64. Hochachka PW, Somero GN (2002) Biochemical adaptation. Oxford University Press, New York
65. BA Horwitz L Nelson 1968 Effect of temperature on mitochondrial respiration in a hibernator (Myotis austroriparius) and a non-hibernator (Rattus rattus) Comp Biochem Physiol 24 385 394
66. MH Kim K Park BJ Gwag N Jung YK Oh H Shin I Choi 2000 Seasonal biochemical plasticity of a flight muscle in a bat, Murina leucogaster Comp Biochem Physiol 126A 245 250
67. SC Leary CN Lyons AG Rosenberger JS Ballantyne J Stillman CD Moyes 2003 Fiber-type differences in muscle mitochondrial profiles Am J Physiol 285 R817 R826
68. C Liu JL Frehn AD Laporta 1969 Liver and brown fat mitochondrial response to cold in hibernators and nonhibernators J Appl Physiol 27 83 89
69. +-ATPase activity by reversible phosphorylation during hibernation Biochem Biophys Res Comm 254 424 429
70. AW Martin FA Fuhrman 1955 The relationship between summated tissue respiration and metabolic rate in the mouse and dog Physiol Zool 28 18 28
71. SL Martin GD Maniero C Carey SC Hand 1999 Reversible depression of oxygen consumption in isolated liver mitochondria during hibernation Physiol Biochem Zool 72 255 264
72. McKechnie AE, Lovegrove BG (2002) Avian facultative hypothermic responses: a review. The Condor: 705-724
73. EJ McMurchie MY Abeywardena JS Charnock RA Gibson 1983 Differential modulation of rat heart mitochondrial membrane-associated enzymes by dietary lipid Biochim Biophys Acta 760 13 24
74. EJ McMurchie MY Abeywardena JS Charnock RA Gibson 1983 The effect of dietary lipids on the thermotropic behaviour of rat liver and heart mitochondrial membrane lipids Biochim Biophys Acta 734 114 124
75. MP Meyer P Morrison 1960 Tissue respiration and hibernation in the thirteen-lined ground squirrel, Spermophilus tridecemlineatus Bull Mus Comp Zool 124 406 420
76. R Milner L Wang P Trayhurn 1989 Brown fat thermogenesis during hibernation and arousal in Richardson's ground squirrel Am J Physiol 256 R42 R48
77. D Mountassif M Kabine N Latruffe MS El Kebbaj 2007 Prehibernation and hibernation effects on the D-3-hydroxybutyrate dehydrogenase of the heavy and light mitochondria from liver jerboa (Jaculus orientalis) and related metabolism Biochimie 89 1019 1028
78. HM Muleme AC Walpole JF Staples 2006 Mitochondrial metabolism in hibernation: metabolic suppression, temperature effects, and substrate preferences Physiol Biochem Zool 79 474 483
79. SE Nizielski CJ Billington AS Levine 1989 Brown fat GDP binding and circulating metabolites during hibernation and arousal Am J Physiol 257 R536 R541
80. KR Olson RA Dombkowski MJ Russell MM Doellman SK Head NL Whitfield JA Madden 2006 Hydrogen sulfide as an oxygen sensor/transducer in vertebrate hypoxic vasoconstriction and hypoxic vasodilation J Exp Biol 209 4011 4023
81. PG Osborne B Gao M Hashimoto 2004 Determination in vivo of newly synthesized gene expression in hamsters during phases of the hibernation cycle Japan J Physiol 54 295 305
82. S Papa AM Sardanelli S Scacco Z Technikova-Dobrova 1999 cAMP-dependent protein kinase and phosphoproteins in mammalian mitochondria An extension of the cAMP-mediated intracellular signal transduction. FEBS Lett 444 245 249
83. DJ Pehowich 1994 Modification of skeletal muscle sarcoplasmic reticulum fatty acyl composition during arousal from hibernation Comp Biochem Physiol 109B 571 578
84. DJ Pehowich 1999 Thyroid hormone status and membrane n-3 fatty acid content influence mitochondrial proton leak Biochim Biophys Acta 1411 192 200
85. 2+ uptake and oxygen consumption in liver mitochondria from a hibernator Physiol Zool 60 114 120
86. DJ Pehowich LCH Wang 1984 Seasonal changes in mitochondrial succinate dehydrogenase activity in a hibernator, Spermophilus richardsonii J Comp Physiol 154 495 501
87. DJ Pehowich PM Macdonald RN McElhaney AR Cossins LCH Wang 1988 Calorimetric and spectroscopic studies of lipid thermotropic phase behavior in liver inner mitochondrial membranes from a mammalian hibernator Biochem 27 4632 4638
88. WS Platner DG Steffen G Tempel XJ Musacchia 1976 Mitochondrial membrane liver fatty acids of liver and heart of the euthermic and hibernating ground squirrel (Citellus tridecemlineatus) Comp Biochem Physiol 53A 279 283
89. E Quagliariello F Palmieri 1968 Control of succinate oxidation by succinate-uptake by rat-liver mitochondria Eur J Biochem 4 20 27
90. JJ Ramsey K Hagopian TM Kenny EK Koomson L Bevilacqua R Weindruch M-E Harper 2004 Proton leak and hydrogen peroxide production in liver mitochondria from energy restricted rats Am J Physiol 286 E31 E40
91. Roberts JC, Chaffee RR (1972) Suppression of mitochondrial respiration in hibernation and its reversal in arousal. In: Smith RE, Shields JC, Hannon PP, Horwitz BA (eds) Proceedings of the international symposium on environmental physiology: bioenergetics and temperature regulation. FASEB, Bethesda, pp 101-107
92. DFS Rolfe GC Brown 1997 Cellular energy utilization and molecular origin of standard metabolic rate in mammals Physiol Rev 77 731 758
93. DFS Rolfe JMB Newman JA Buckingham MG Clark MD Brand 1999 Contribution of mitochondrial proton leak to respiration rate in working skeletal muscle and liver and to SMR Am J Physiol Cell Physiol 276 C692 C699
94. S Scacco R Vergari RC Scarpulla Z Tchnikova-Dobrova A Sardanelli R Lambo V Lorusso S Papa 2000 cAMP-dependent phosphorylation of the nuclear encoded 18-KDa (IP) subunit of respiratory complex I and activation of the complex in serum -starved mouse fibroblast cultures J Biol Chem 275 17587 17582
95. CD Schaefer JF Staples 2006 Mitochondrial metabolism in mammalian cold-acclimation: magnitude and mechanisms of fatty-acid uncoupling J Therm Biol 31 355 361
96. AL Shug S Ferguson E Shrago RF Burlington 1971 Changes in respiratory control and cytochromes in liver mitochondria during hibernation Biochim Biophys Acta 226 309 312
97. RA Simonyan M Jiminez RB Ceddia JP Giacobino P Muzzin VP Skulachev 2001 Cold-induced changes in the energy coupling and the UCP3 level in rodent skeletal muscles Biochim Biophys Acta 1505 271 279
98. BD Snapp HC Heller 1981 Suppression of metabolism during hibernation in ground squirrels (Citellus lateralis) Physiol Zool 54 297 307
99. JR Speakman DA Talbot C Selman S Snart JS McLaren P Redman E Krol DM Jackson MS Johnson MD Brand 2004 Uncoupled and surviving: individual mice with metabolism have greater mitochondrial uncoupling and live longer Aging Cell 3 87 95
100. KB Storey JM Storey 2004 Metabolic rate depression in animals: transcriptional and translational controls Biol Rev 79 207 233
101. J St-Pierre MD Brand RG Boutilier 2000 The effect of metabolic depression on proton leak rate in mitochondria from hibernating frogs J Exp Biol 203 1469 1476
102. JA Stuart TE Gillis JS Ballantyne 1998 Compositional correlates of metabolic depression in the mitochondrial membranes of estivating snails Am J Physiol 275 R1977 R1982
103. JA Stuart TE Gillis JS Ballantyne 1998 Remodeling of phopsholipid fatty acids in mitiochondrial membranes of estivating snails Lipids 33 787 793
104. U Sundin G Moore J Nedergaard B Cannon 1987 Thermogenin amount and activity in hamster brown fat mitochondria: effect of cold acclimation Am J Physiol 252 R822 R832
105. SJ Swoap M Rathvon M Gutilla 2007 AMP does not induce torpor Am J Physiol Regul Integr Comp Physiol 293 R468 R473
106. BJ Thatcher KB Storey 2001 Glutamate dehydrogenase from liver of euthermic and hibernating Richardson's ground squirrels: evidence for two distinct enzyme forms Biochem Cell Biol 79 11 19
107. Ø Tøien KL Drew ML Chao ME Rice 2001 Ascorbate dynamics and oxygen consumption during arousal from hibernation in Arctic ground squirrels Am J Physiol 281 R572 R583
108. M Toyomizu M Ueda S Sato Y Seki K Sato Y Akiba 2002 Cold-induced mitochondrial uncoupling and expression of chicken UCP and ANT mRNA in chicken skeletal muscle FEBS Lett 529 313 318
109. F van Breukelen SL Martin 2001 Translational initiation is uncoupled from elongation at 18°C during mammalian hibernation Am J Physiol Regul Integr Comp Physiol 281 R1374 R1379
110. F van Breukelen SL Martin 2002 Reversible depression of transcription during hibernation J Comp Physiol B 172 355 361
111. F van Breukelen N Sonenberg SL Martin 2004 Seasonal and state-dependent changes of eIF4E and 4E-BP1 during mammalian hibernation: implications for the control of translation during torpor Am J Physiol Regul Integr Comp Physiol 287 R349 R353
112. GP Volpato R Searles Y Binglan M Scherrer-Crosbie KD Bloch F Ichinose WM Zapol 2008 Inhaled hydrogen sulfide-a rapidly reversible inhibitor of cardiac and metabolic function in the mouse Anesthesiology 108 659 668
113. LCH Wang 1979 Time patterns and metabolic rates in natural torpor in the Richardson's ground squirrel Can J Zool 57 149 155
114. SJ Wickler BA Horwitz KS Kott 1987 Muscle function in hibernating hamsters: a natural analog to bed rest? J Therm Biol 12 163 166
115. SJ Wickler DF Hoyt F van Breukelen 1991 Disuse atrophy in the hibernating golden-mantled ground squirrel, Spermophilus lateralis Am J Physiol 261 R1214 R1217
116. 2 regulation in the hibernating thirteen-lined ground squirrel Cell Mol Biol Lett 12 621 632
117. ME Yacoe 1983 Adjustments of metabolic pathways in the pectoralis muscle of the bat, Eptesicus fuscus, related to carbohydrate sparing during hibernation Physiol Zool 56 648 658