Arousal from hibernation and BAT thermogenesis against cold: Central mechanism and molecular basis

Journal of Thermal Biology

Volumn 27, Issue 6, 2002, Pages 503-515

  Hashimoto, Masaaki ^a   Gao, Bihu ^a   Kikuchi Utsumi, Kazue ^a   Ohinata, Hiroshi ^a   Osborne, Peter G ^a  

^a ASAHIKAWA MEDICAL COLLEGE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0036889292     PISSN: 03064565     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4565(02)00024-4     Document Type: Short Survey

References (118)

1. Andrews, M.T., Squire, T.L., Bowen, C.M., Rollins, M.B., 1998. Low-temperature carbon utilization is regulated by novel gene activity in the heart of a hibernating mammal. Proc. Natl. Acad. Sci. USA 95, 8392-8397.
2. Baffi, J.S., Palkovits, M., 2000. Fine topography of brain areas activated by cold stress. A fos immunohistochemical study in rats. Neuroendocrinology 72, 102-113.
3. Bamshad, M., Song, C.K., Bartness, T.J., 1999. CNS origins of the sympathetic nervous system outflow to brown adipose tissue. Am. J. Physiol. 276, R1569-R1578.
4. Barnes, B.M., 1989. Freeze avoidance in a mammal: Body temperatures below 0 degree c in an arctic hibernator. Science 244, 1593-1595.
5. Bester, H., Chapman, V., Besson, J.M., Bernard, J.F., 2000. Physiological properties of the lamina I spinoparabrachial neurons in the rat. J. Neurophysiol. 83, 2239-2259.
6. Bitting, L., Sutin, E.L., Watson, F.L., Leard, L.E., O'Hara, B.F., Holler, H.C., Kilduff, T.S., 1994. C-fos mRNA increases in the ground squirrel suprachiasmatic nucleus during arousal from hibernation. Neurosci. Lett. 165, 117-121.
7. Bocharova, L.S., Gordon, R., Arkhipov, V.I., 1992. Uridine uptake, RNA synthesis in the brain of torpid, awakened ground squirrels. Comp. Biochem. Physiol. B 101, 189-192.
8. Bouillaud, F., Couplan, E., Pecqueur, C., Ricquier, D., 2001. Homologues of the uncoupling protein from brown adipose tissue (UCP1): UCP2, UCP3, BMCP1, UCP4. Biochim. Biophys. Acta 1504, 107-119.
9. Boyer, B.B., Barnes, B.M., 1999. Molecular and metabolic aspects of mammalian hibernation. Bioscience 49, 713-724.
10. Boyer, B.B., Barnes, B.M., Lowell, B.B., Grujic, D., 1998. Differential regulation of uncoupling protein gene homologues in multiple tissues of hibernating ground squirrels. Am. J. Physiol. 275, R1232-R1238.
11. Bruce, D.S., Cope, G.W., Elam, T.R., Ruit, K.A., Oeltgen, P.R., Su, T.P., 1987. Opioids and hibernation. I. Effects of naloxone on bear HIT'S depression of guinea pig ileum contractility and on induction of summer hibernation in the ground squirrel. Life Sci. 41, 2107-2113.
12. Chatfield, P.O., Lyman, C.P., 1954. Subcortical electrical activity in the golden hamster during arousal from hibernation. Electroenceph. Clin. Neurophysiol. 6, 403-408.
13. Chen, Y., Matsushita, M., Nairn, A.C., Damuni, Z., Cai, D., Frerichs, K.U., Hallenbeck, J.M., 2001. Mechanisms for increased levels of phosphorylation of elongation factor-2 during hibernation in ground squirrels. Biochemistry 40, 11565-11570.
14. Colquhoun, E.Q., Hettiarchchi, M., Ye, J.M., Rattigen, S., Clark, M.G., 1990. Inhibition by vasodilators of noradrenaline and vasoconstrictor-mediated, but not skeletal muscle contraction-induced oxygen uptake in the perfused rat hindlimb; implications for non-shivering thermogenesis in muscle tissue. Gen. Pharmacol. 21, 141-148.
15. Dark, J., Kilduff, T.S., Heller, H.C., Licht, P., Zucker, I., 1990. Suprachiasmatic nuclei influence hibernation rhythms of golden-mantled ground squirrels. Brain Res. 509, 111-118.
16. Dawe, A.R., Spurrier, W.A., 1969. Hibernation induced in ground squirrels by blood transfusion. Science 163, 298-299.
17. Desautels, M., Dulos, R.A., 1988. Is adrenergic innervation essential for maintenance of UCP in hamster BAT mitochondria? Am. J. Physiol. 254, R1035-R1042.
18. Eckerman, P., Scharruhn, K., Horowitz, J.M., 1990. Effects of temperature and acid-base state on hippocampal population spikes in hamsters. Am. J. Physiol. 258, R1140-R1146.
19. Eldershaw, T.P.D., Ye, J., Clark, M.G., Colquhoun, E.Q., 1996. Vasoconstrictor-induced thermogenic switching in endotherm and ectotherm muscle. In: Geiser, F., Hulbert, A.J., Nicol, S.C. (Eds.), Adaptations in the Cold. University of New England Press, Armidale, pp. 311-317.
20. El Ouezzani, S., Lafon, P., Tramu, G., Magoul, R., 2001. Neuropeptide Y gene expression in the jerboa arcuate nucleus: Modulation by food deprivation and relationship with hibernation. Neurosci. Lett. 305, 21-24.
21. Enerbäck, S., Jacobsson, A., Simpson, E.M., Guerra, C., Yamashita, H., Harper, M.E., Kozak, L.P., 1997. Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese. Nature 387, 90-94.
22. Florant, G.L., Heller, H.C., 1977. CNS regulation of body temperature in euthermic and hibernating marmots (Marmota flaviventris). Am. J. Physiol. 232, R203-R208.
23. Foster, D.O., Frydman, M.L., 1978. Brown adipose tissue: The dominant site of nonshivering thermogenesis in the rat. Experientia Suppl. 32, 147-151.
24. Frerichs, K.U., Smith, C.B., Brenner, M., DeGracia, D.J., Krause, G.S., Marrone, L., Dever, T.E., Hallenbeck, J.M., 1998. Suppression of protein synthesis in brain during hibernation involves inhibition of protein initiation and elongation. Proc. Natl. Acad. Sci. USA 95, 14511-14516.
25. Gao, B., Kikuchi-Utsumi, K., Kuroshima, A., 2001. Effect of immobilization stress on the function of uncoupling protein1 in rats brown adipose tissue. Proceedings of the Australian Physiological and Pharmacological Society, Wollongong, Vol. 32, 38pp.
26. Goldman, S.S., Willis, J.S., 1973. Cold resistance of the brain during hibernation. II. Na-K-activated ATPase. Cryobiology 10, 218-224.
27. Grahn, D.A., Miller, J.D., Houng, V.S., Heller, H.C., 1994. Persistence of circadian rhythmicity in hibernating ground squirrels. Am. J. Physiol. 266, R1251-R1258.
28. Halvorson, I., Gregor, L., Thornhill, J.A., 1990. Brown adipose tissue thermogenesis is activated by electrical and chemical (L-glutamate) stimulation of the ventromedial hypothalamic nucleus in cold-acclimated rats. Brain Res. 522, 76-82.
29. Hammel, H.T., Dawson, T.J., Abrams, R.M., Andersen, H.J., 1968. Total calorimetric measurements on Citellus lateralis in hibernation. Physiol. Zool. 41, 341-357.
30. Hammel, H.T., Heller, H.C., Sharp, F.R., 1973. Probing the rostral brainstem of anesthetized, unanesthetized, and exercising dogs and of hibernating and euthermic ground squirrels. Fed. Proc. 32, 1588-1597.
31. Hashimoto, M., Kuroshima, A., 2001. CNS control of BAT thermogenesis in hibernating hamster. Jpn. J. Physiol. 51, S97.
32. Hashimoto, M., Arita, J., Shibata, M., 1998a. Electrical stimulation of the lower midbrain around retrorubral field decreases temperatures of brown fat and rectum in anesthetized Wistar rats. Neurosci. Lett. 246, 129-132.
33. Hashimoto, M., Arita, J., Shibata, M., 1998b. Microinjection of procaine into the midbrain around the retrorubral field facilitatesand electrical stimulation inhibits BAT heat production in the golden hamster. Jpn. J. Physiol. 48, S217.
34. Hashimoto, M., Schmid, H.A., Ohwatari, N., Pleschka, K., 1998c. Spontaneous activity of preoptic neurons in slice preparations of the hypothalamus of European hamsters (Cricetus cricetus) and Wistar rats under different states of hypothermia. Cryobiology 37, 254-262.
35. Hashimoto, M., Kuroshima, A., Arita, J., Shibata, M., 1999a. Brown fat temperature decrease by electrical stimulation of in and around retrorubral field in the golden hamster. J. Therm. Biol. 24, 347-350.
36. Hashimoto, M., Utsumi, K., Gao, B., Kuroshima, A., 1999b. Gene expression of uncoupling protein in syrian hamsters during hibernation. Jpn. J. Physiol. 49, S213.
37. Hashimoto, M., Kuroshima, A., Shibata, M., 2002. CNS regulation of BAT function and arousal from hibernation in hamsters. In: Moravec, J., Takeda, N., Singal, P.K. (Eds.), Adaptation Biology and Medicine. Narosa Publishing House, New Delhi, pp. 262-267.
38. Hayward, J.S., Lyman, C.P., 1967. Nonshivering heat production during arousal from hibernation and evidence for the contribution of brown fat. In: Fisher, K.C., Dawe, A.R., Lyman, C.P., Schönbaum, E., South, F.E. (Eds.), Mammalian Hibernation. Elsevier, New York, pp. 346-355.
39. Heldmaier, G., Buchberger, A., Seidle, K., 1983. Contribution of brown adipose tissue to thermoregulatory heat production in the Dhungarian hamster. J. Therm. Biol. 8, 413-415.
40. Heller, H.C., Colliver, G.W., 1974. CNS regulation of body temperature during hibernation. Am. J. Physiol. 227, 583-589.
41. Heller, H.C., Glotzbach, S.F., 1977. Thermoregulation during sleep and hibernation. Int. Rev. Physiol. 15, 147-188.
42. Heller, H.C., Hammel, H.T., 1972. CNS control of body temperature during hibernation. Comp. Biochem. Physiol. A 41, 349-359.
43. Heller, H.C., Colliver, G.W., Bread, J., 1977. Thermoregulation during entrance into hibernation. Pflügers Arch. 369, 55-59.
44. Himms-Hagen, J., 1984. Nonshivering thermogenesis. Brain Res. Bull. 12, 151-160.
45. Himms-Hagen, J., 1995. Does thermoregulatory feeding occur in newborn infants? A novel view of the role of brown adipose tissue thermogenesis in control of food intake. Obes. Res. 3, 361-369.
46. Hooper, D.C., Martin, S.M., Horowitz, J.M., 1985. Temperature effects on evoked potentials of hippocampal slices from euthermic chipmunks, hamsters and rats. J. Therm. Biol. 10, 35-40.
47. Horwitz, B.A., 1978. Neurohumoral regulation of nonshivering thermogenesis in mammals. In: Wang, L.C., Hudson, J.W. (Eds.), Strategies in Cold. Academic Press, New York, pp. 619-653.
48. Horowitz, J.M., Thomas, M.P., Eckerman, P., 1987. Thermal dependence of neural activity in the hamster hippocampal slice preparation. J. Therm. Biol. 12, 97-101.
49. Horton, N.D., Kaftani, D.J., Bruce, D.S., Bailey, E.C., Krober, A.S., Jones, J.R., Turker, M., Khattar, N., Su, T.P., Bolling, S.F., Oeltgen, P.R., 1998. Isolation and partial characterization of an opioid-like 88 kDa hibernation-related protein. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 119, 787-805.
50. Igelmund, P., Heinemann, U., 1995. Synaptic transmission and paired-pulse behaviour of CA1 pyramidal cells in hippo-campal slices from a hibernator at low temperature: Importance of ionic environment. Brain Res. 689, 9-20.
51. Imai-Matsumura, K., Matsumura, K., Nakayama, T., 1984. Involvement of ventromedial hypothalamus in brown adipose tissue thermogenesis induced by preoptic cooling in rats. Jpn. J. Physiol. 34, 939-943.
52. Kanosue, K., Hosono, T., Zhang, Y.H., Chen, X.M., 1998. Neuronal networks controlling thermoregulatory effectors. Prog. Brain. Res. 115, 49-62.
53. Kilduff, T.S., Sharp, F.R., Heller, H.C., 1982. [14C]2-deoxyglucose uptake in ground squirrel brain during hibernation. J. Neurosci. 2, 143-157.
54. Kilduff, T.S., Radeke, C.M., Randall, T.L., Sharp, F.R., Heller, H.C., 1989. Suprachiasmatic nucleus: Phase-dependent activation during the hibernation cycle. Am. J. Physiol. 257, R605-R612.
55. Kilduff, T.S., Miller, J.D., Radeke, C.M., Sharp, F.R., Heller, H.C., 1990. 14C-2-deoxyglucose uptake in the ground squirrel brain during entrance to and arousal from hibernation. J. Neurosci. 10, 2463-2475.
56. Klaus, S., Munzberg, H., Truloff, C., Heldmaier, G., 1998. Physiology of transgenic mice with brown fat ablation: Obesity is due to lowered body temperature. Am. J. Physiol. 274, R287-R293.
57. Klingenberg, M., 1999. Uncoupling protein-a useful energy dissipator. J. Bioenerg. Biomembr. 31, 419-430.
58. Klingenberg, M., Echtay, K.S., 2001. Uncoupling proteins: The issues from a biochemist point of view. Biochim. Biophys. Acta 1504, 128-143.
59. Kobayashi, A., Osaka, T., Inoue, S., 2001. Role of the parabrachial nucleus in the regulation of cold induced thermogenesis. Jpn. J. Physiol. 51, S261.
60. Kondo, N., Kondo, J., 1992. Identification of novel blood proteins specific for mammalian hibernation. J. Biol. Chem. 267, 473-478.
61. Kondo, N., Ohtsu, T., Sekijima, T., 2000. Molecular system controlling mammalian hibernation with circannual rhythm. In: Hayashi, N. (Ed.), Brain Hypothermia. Springer, Tokyo, pp. 29-36.
62. Kuroshima, A., 1993. Brown adipose tissue thermogenesis as physiological strategy for adaptation. Jpn. J. Physiol. 43, 117-139.
63. Kuroshima, A., Habara, Y., Uehara, A., Murazumi, K., Yahata, T., Ohno, T., 1984. Cross adaption between stress and cold in rats. Pflügers Arch. 402, 402-408.
64. Liu, X., Li, Q., Lin, Q., Sun, R., 2001. Uncoupling protein1 mRNA, mitochondrial GTP-binding, and T4 5′-deiodinase of brown adipose tissue in euthermic Daurian ground squirrel during cold exposure. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 128, 827-835.
65. Liu, X.T., Lin, Q.S., Li, Q.F., Huang, C.X., Sun, R.Y., 1998. Uncoupling protein mRNA, mitochondrial GTP-binding, and T4 5′-deiodinase activity of brown adipose tissue in Daurian ground squirrel during hibernation and arousal. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 120, 745-752.
66. Lowell, B.B., S-Susulic, V., Hamann, A., Lawitts, J.A., Himms-Hagen, J., Boyer, B.B., Kozak, L.P., Flier, J.S., 1993. Development of obesity in transgenic mice after genetic ablation of brown adipose tissue. Nature 366, 740-742.
67. Lyman, C.P., O'Brien, R.C., 1972. Sensitivity to low temperature in hibernating rodents. Am. J. Physiol. 222, 864-869.
68. McDonald, R.B., Horwitz, B.A., Hamilton, J.S., Stern, J.S., 1988. Cold- and norepinephrine-induced thermogenesis in younger and older Fischer 344 rats. Am. J. Physiol. 254, R457-R462.
69. Menendez, L., Bester, H., Besson, J.M., Bernard, J.F., 1996. Parabrachial area: Electrophysiological evidence for an involvement in cold nociception. J. Neurophysiol. 75, 2099-2116.
70. Mihailovic, L.T., 1972. Cortical and subcortical electrical activity in hibernation and hypothermia. In: South, F.E., Hannon, J.P., Willis, J.R., Pengelly, E.T., Alpert, N.R. (Eds.), Hibernation and Hypothermia, Perspectives and Challenges. Elsevier, Amsterdam, pp. 487-534.
71. Miller, J.D., Cao, V.H., Heller, H.C., 1994. Thermal effects on neuronal activity in suprachiasmatic nuclei of hibernators and nonhibernators. Am. J. Physiol. 266, R1259-R1266.
72. Mills, S.H., South, F.E., 1972. Central regulation of temperature in hibernation and normothermia. Cryobiology 9, 393-403.
73. Milner, R.E., Wang, L.C., Trayhurn, P., 1989. Brown fat thermogenesis during hibernation and arousal in Richardson's ground squirrel. Am. J. Physiol. 256, R42-R48.
74. Miyata, S., Ishiyama, M., Shido, O., Nakashima, T., Shibata, M., Kiyohara, T., 1995. Central mechanism of neural activation with cold acclimation of rats using Fos immunohistochemistry. Neurosci. Res. 22, 209-218.
75. Morimoto, A., Nakamori, T., Ono, T., Watanabe, T., Sakai, Y., Murakami, N., 1986. Changes in [14C]deoxyglucose incorporation into rat brain regions during heat-seeking behavior in the cold environment. Physiol. Behav. 38, 275-282.
76. Morrison, S.F., 1999. RVLM and raphe differentially regulate sympathetic outflows to splanchnic and brown adipose tissue. Am. J. Physiol. 276, R962-R973.
77. Morrison, S.F., 2001. Differential regulation of brown adipose and splanchnic sympathetic outflows in rat: Roles of raphe and rostral ventrolateral medulla neurons. Clin. Exp. Pharmacol. Physiol. 28, 138-143.
78. Morrison, S.F., Sved, A.F., Passerin, A.M., 1999. GABA-mediated inhibition of raphe pallidus neurons regulates sympathetic outflow to brown adipose tissue. Am. J. Physiol. 276, R290-R297.
79. Morrison, S.F., Ramamurthy, S., Young, J.B., 2000. Reduced rearing temperature augments responses in sympathetic outflow to brown adipose tissue. J. Neurosci. 20, 9264-9271.
80. Nedergaard, J., Cannon, B., 1990. Mammalian hibernation. Philos. Trans. R. Soc. London B Biol. Sci. 326, 669-685.
81. Nedergaard, J., Matthias, A., Golozoubova, V., Jacobsson, A., Cannon, B., 1999. UCP1: The original uncoupling protein- and perhaps the only one? New perspectives on UCP1, UCP2, and UCP3 in the light of the bioenergetics of the UCP1-ablated mice. J. Bioenerg. Biomembr. 31, 475-491.
82. Nedergaard, J., Golozoubova, V., Matthias, A., Asadi, A., Jacobsson, A., Cannon, B., 2001. UCP1: The only protein able to mediate adaptive non-shivering thermogenesis and metabolic inefficiency. Biochim. Biophys. Acta. 1504, 82-106.
83. Nizielski, S.E., Billington, C.J., Levine, A.S., 1989. Brown fat GDP binding and circulating metabolites during hibernation and arousal. Am. J. Physiol. 257, R536-R541.
84. Nizielski, S.E., Billington, C.J., Levine, A.S., 1995. Cold-induced alterations in uncoupling protein and its mRNA are seasonally dependent in ground squirrels. Am. J. Physiol. 269, R357-R364.
85. O'Hara, B.F., Watson, F.L., Srere, H.K., Kumar, H., Wiler, S.W., Welch, S.K., Bitting, L., Heller, H.C., Kilduff, T.S., 1999. Gene expression in the brain across the hibernation cycle. J. Neurosci. 19, 3781-3790.
86. Oeltgen, P.R., Bergmann, L.C., Spurrier, W.A., Jones, S.B., 1978. Isolation of a hibernation inducing trigger(s) from the plasma of hibernating woodchucks. Prep. Biochem. 8, 171-188.
87. Oeltgen, P.R., Walsh, J.W., Hamann, S.R., Randall, D.C., Spurrier, W.A., Myers, R.D., 1982. Hibernation "trigger": Opioid-like inhibitory action on brain function of the monkey. Pharmacol. Biochem. Behav. 17, 1271-1274.
88. Oklejewicz, M., Daan, S., Strijkstra, A.M., 2001. Temporal organisation of hibernation in wild-type and tau mutant Syrian hamsters. J. Comp. Physiol. B 171, 431-439.
89. Osborne, P.G., Hu, Y., Covey, D.N., Barnes, B.N., Katz, Z., Drew, K.L., 1999. Determination of striatal extracellular gamma-aminobutyric acid in non-hibernating and hibernating arctic ground squirrels using quantitative microdialysis. Brain Res. 839, 1-6.
90. Pakhotin, P.I., Pakhotina, I.D., Belousov, A.B., 1993. The study of brain slices from hibernating mammals in vitro and some approaches to the analysis of hibernation problems in vivo. Prog. Neurobiol. 40, 123-161.
91. Popov, V.I., Bocharova, L.S., 1992. Hibernation-induced structural changes in synaptic contacts between mossy fibres and hippocampal pyramidal neurons. Neuroscience 48, 53-62.
92. Popov, V.I., Bocharova, L.S., Bragin, A.G., 1992. Repeated changes of dendritic morphology in the hippocampus of ground squirrels in the course of hibernation. Neuroscience 48, 45-51.
93. Raths, P., Hensel, H., 1967. Cutane Thermoreceptoren bei Winterschlafern. Pflügers Arch. 293, 281-302.
94. Rothwell, N.J., 1989. Central control of brown adipose tissue. Proc. Nutr. Soc. 48, 197-206.
95. Rothwell, N.J., Stock, M.J., 1984. Effects of denervating brown adipose tissue on the responses to cold, hyperphagia and noradrenaline treatment in the rat. J. Physiol. 355, 457-463.
96. Rothwell, N.J., Stock, M.J., 1997. A role for brown adipose tissue in diet-induced thermogenesis. Obes. Res. 5, 650-656.
97. Ruby, N.F., Dark, J., Heller, H.C., Zucker, I., 1996. Ablation of suprachiasmatic nucleus alters timing of hibernation in ground squirrels. Proc. Natl. Acad. Sci. USA 93, 9864-9868.
98. Ruby, N.F., Dark, J., Heller, H.C., Zucker, I., 1998. Suprachiasmatic nucleus: role in circannual body mass and hibernation rhythms of ground squirrels. Brain Res. 782, 63-72.
99. Sallmen, T., Beckman, A.L., Stanton, T.L., Eriksson, K.S., Tarhanen, J., Tuomisto, L., Panula, P., 1999. Major changes in the brain histamine system of the ground squirrel citellus lateralis during hibernation. J. Neurosci. 19, 1824-1835.
100. Satinoff, E., 1967. Disruption of hibernation caused by hypothalamic lesions. Science 155, 1031-1033.
101. Shibata, M., Benzi, R.H., Seydoux, J., Girardier, L., 1987. Hyperthermia induced by pre-pontine knife-cut: Evidence for a tonic inhibition of non-shivering thermogenesis in anaesthetized rat. Brain Res. 436, 273-282.
102. Shibata, M., Iriki, M., Arita, J., Kiyohara, T., Nakashima, T., Miyata, S., Matsukawa, T., 1996. Procaine microinjection into the lower midbrain increases brown fat and body temperatures in anesthetized rats. Brain Res. 716, 171-179.
103. Shibata, M., Uno, T., Hashimoto, M., 1999a. Neurons in the lower midbrain tonically inhibit non-shivering thermogenesis through their influence on inferior olivery neurons in anesthetized rats. J. Therm. Biol. 24, 365-368.
104. Shibata, M., Uno, T., Hashimoto, M., 1999b. Disinhibition of lower midbrain neurons enhances non-shivering thermogenesis in anesthetized rats. Brain Res. 833, 242-250.
105. Soukri, A., Valverde, F., Hafid, N., Elkebbaj, M.S., Serrano, A., 1996. Occurrence of a differential expression of the glyceraldehyde-3-phosphate dehydrogenase gene in muscle and liver from euthermic and induced hibernating jerboa (Jaculus orientalis). Gene 181, 139-145.
106. Squire, T.L., Andrews, M.T., 2000. Genetic control of carbon utilization during hibernation: mechanistic considerations. In: Heldmaier, G., Klingenspor, M. (Eds.), Life in the Cold. Springer, Heidelberg, pp. 325-337.
107. Srere, H.K., Wang, L.C., Martin, S.L., 1992. Central role for differential gene expression in mammalian hibernation. Proc. Natl. Acad. Sci. USA 89, 7119-7123.
108. Stefl, B., Janovska, A., Hodny, Z., Rossmeisl, M., Horakova, M., Syrovy, I., Bemova, J., Bendlova, B., Kopecky, J., 1998. Brown fat is essential for cold-induced thermogenesis but not for obesity resistance in aP2-Ucp mice. Am. J. Physiol. 274, E527-E533.
109. Takamatsu, N., Ohba, K., Kondo, J., Kondo, N., Shiba, T., 1993. Hibernation-associated gene regulation of plasma proteins with a collagen-like domain in mammalian hibernators. Mol. Cell. Biol. 13, 1516-1521.
110. Tanaka, M., Tsuda, A., Ida, Y., Ushijima, I., Tsujimaru, S., Nagasaki, N., 1985. State-dependent effects of beta-endorphin on core temperature in stressed and non-stressed rats. Jpn. J. Pharmacol. 39, 395-397.
111. Trayhurn, P., Nicholls, D.G., 1986. Brown Adipose Tissue. Edwar Arnold, Baltimore.
112. Uno, T., Shibata, M., 2001. Role of inferior olive and thoracic IML neurons in nonshivering thermogenesis in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280, R536-R546.
113. Weidler, D.J., Earle, A.M., Myers, G.G., Sieck, G.C., 1974. Effect of hypothalamic lesions on temperature regulation in hibernating ground squirrels. Brain Res. 65, 175-179.
114. Wilson, B.E., Deeb, S., Florant, G.L., 1992. Seasonal changes in hormone-sensitive and lipoprotein lipase mRNA concentrations in marmot white adipose tissue. Am. J. Physiol. 262, R177-R181.
115. Wünnenberg, W., Merker, G., 1978. Control of non-shivering thermogenesis in a hibernator. Exp. Suppl. 32, 315-319.
116. Wünnenberg, W., Kuhnen, G., Laschefski-Sievers, R., 1986. CNS regulation of body temperature in hibernators and non-hibernators. In: Heller, H.C., Musacchia, X.J., Wang, L.C.H. (Eds.), Living in the Cold. Elsevier Science Publishing, New York, pp. 185-192.
117. Young, P., Wilson, S., Arch, J.R., 1984. Prolonged beta-adrenoceptor stimulation increases the amount of GDP-binding protein in brown adipose tissue mitochondria. Life Sci. 34, 1111-1117.
118. Zucker, I., Boshes, M., Dark, J., 1983. Suprachiasmatic nuclei influence circannual and circadian rhythms of ground squirrels. Am. J. Physiol. 244, R472-R480.