Abstract
To examine the effects of low ambient temperature and thyroid hormones on the energy metabolism of the striped hamster (Cricetulus barabensis), adult male striped hamsters were kept at 30 °C, or acclimated to 5 °C, for 4 weeks. During this time, hamsters were treated with a synthetic thyroxine, levothyroxine sodium (LTS), the antithyroid drug methimazole, or saline solution (control). Hamster’s food intake, basal metabolic rate (BMR), non-shivering thermogenesis (NST), thyroid hormones, body fat content, mitochondrial state-4 respiration, cytochrome c oxidase, and uncoupling protein 1 (UCP1) gene expression in brown adipose tissue (BAT), were measured. Both acclimation to 5 °C and LTS increased serum levels of triiodothyronine, which was associated with increased food and energy intake and BMR. Interestingly, although acclimation to 5 °C also increased NST and UCP1 gene expression in BAT, and decreased body fat content, these changes were not induced by LTS treatment. Finally, exposure to 5 °C reduced the effects of LTS on energy intake and expenditure in specific metabolic markers and organs. Together, these data illustrate that ambient temperature and thyroid hormones can have both independent, and interactive, effects on the metabolic changes in striped hamsters induced by cold acclimation.
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Alvarez-Crespo M, Csikasz RI, Martínez-Sánchez N, Diéguez C, Cannon B, Nedergaard J, López M (2016) Essential role of UCP1 modulating the central effects of thyroid hormones on energy balance. Mol Metab 5:271–282. https://doi.org/10.1016/j.molmet.2016.01.008
Bank JHH, Kemmling J, Rijntjes E, Wirth EK, Herwig A (2015) Thyroid hormone status affects expression of daily torpor and gene transcription in Djungarian hamsters (Phodopus sungorus). Horm Behav 75:120–129. https://doi.org/10.1016/j.yhbeh.2015.09.006
Banta MR, Holcombe DW (2002) The effects of thyroxine on metabolism and water balance in a desert-dwelling rodent, Merriam’s kangaroo rat (Dipodomys merriami). J Comp Physiol B 172:17–25. https://doi.org/10.1007/s003600100222
Bartness TJ, Demas GE, Song CK (2002) Seasonal changes in adiposity: the roles of the photoperiod, melatonin and other hormones, and sympathetic nervous system. Exp Biol Med 227:363–376. https://doi.org/10.1177/153537020222700601
Bernal J (2002) Action of thyroid hormone in brain. J Endocrinol Investig 25:268–288. https://doi.org/10.1007/BF03344003
Bianco AC, McAninch EA (2013) The role of thyroid hormone and brown adipose tissue in energy homoeostasis. Lancet Diabetes Endocrinol 1:250–258. https://doi.org/10.1016/S2213-8587(13)70069-X
Bianco AC, Silva JE (1987) Intracellular conversion of thyroxine to triiodothyronine is required for the optimal thermogenic function of brown adipose tissue. J Clin Investig 79:295–300. https://doi.org/10.1172/JCI112798
Bize P, Lowe I, Lehto Hurlimann M, Heckel G (2018) Effects of the mitochondrial and nuclear genomes on nonshivering thermogenesis in a wild derived rodent. Integr Comp Biol 77:1–12. https://doi.org/10.1093/icb/icy072
Broeders EP, Vijgen GH, Havekes B, Bouvy ND, Mottaghy FM, Kars M, Schaper NC, Schrauwen P, Brans B, van Marken Lichtenbelt WD (2016) Thyroid hormone activates brown adipose tissue and increases non-shivering thermogenesis—a cohort study in a group of thyroid carcinoma patients. PloS One 11:e0145049. https://doi.org/10.1371/journal.pone.0145049
Brown JHGJ, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789. https://doi.org/10.1890/03-9000
Cannon B, Nedergaard J (2001) Respiratory and thermogenic capacities of cells and mitochondria from brown and white adipose tissue. Methods Mol Biol 155:295–303. https://doi.org/10.1385/1-59259-231-7:295
Charlot K, Faure C, Antoine-Jonville S (2017) Influence of hot and cold environments on the regulation of energy balance following a single exercise session: a mini-review. Nutrients. https://doi.org/10.3390/nu9060592
Chen JF, Zhong WQ, Wang DH (2012) Seasonal changes in body mass, energy intake and thermogenesis in Maximowiczi’s voles (Microtus maximowiczii) from the Inner Mongolian grassland. J Comp Physiol B 182:275–285. https://doi.org/10.1007/s00360-011-0608-9
Chen K, Wang G, Zhao Z (2015) Effects of cold temperatures on energy metabolism, antioxidants and oxidative stress in striped hamsters. Acta Theriologica Sinica 35:412–421
Cheng SY, Leonard JL, Davis PJ (2010) Molecular aspects of thyroid hormone actions. Endocr Rev 31:139–170. https://doi.org/10.1210/er.2009-0007
Cioffi F, Senese R, Lanni A, Goglia F (2013) Thyroid hormones and mitochondria: with a brief look at derivatives and analogues. Mol Cell Endocrinol 379:51–61. https://doi.org/10.1016/j.mce.2013.06.006
Collin A, Cassy S, Buyse J, Decuypere E, Damon M (2005) Potential involvement of mammalian and avian uncoupling proteins in the thermogenic effect of thyroid hormones. Domest Anim Endocrinol 29:78–87. https://doi.org/10.1016/j.domaniend.2005.02.007
de Jonghe BC, Hayes MR, Banno R, Skibicka KP, Zimmer DJ, Bowen KA, Leichner TM, Alhadeff AL, Kanoski SE, Cyr NE, Nillni EA, Grill HJ, Bence KK (2011) Deficiency of PTP1B in POMC neurons leads to alterations in energy balance and homeostatic response to cold exposure. Am J Physiol Endocrinol Metab 300:E1002–E1011. https://doi.org/10.1152/ajpendo.00639.2010
Decuypere E, Van As P, Van Der Geyten S, Darras VM (2005) Thyroid hormone availability and activity in avian species: a review. Domest Anim Endocrinol 29:63–77. https://doi.org/10.1016/j.domaniend.2005.02.028
Fox CS, Pencina MJ, D’Agostino RB, Murabito JM, Seely EW, Pearce EN, Vasan RS (2008) Relations of thyroid function to body weight: cross-sectional and longitudinal observations in a community-based sample. Arch Intern Med 168:587–592. https://doi.org/10.1001/archinte.168.6.587
Galic S, Loh K, Murray-Segal L, Steinberg GR, Andrews ZB, Kemp BE (2018) AMPK signaling to acetyl-CoA carboxylase is required for fasting- and cold-induced appetite but not thermogenesis. eLife. https://doi.org/10.7554/eLife.32656
Gao Y, Lee WM, Cheng CY (2014) Thyroid hormone function in the rat testis. Front Endocrinol 5:188. https://doi.org/10.3389/fendo.2014.00188
German E, Hoffman-Goetz L (1986) The effect of cold acclimation and exercise training on cold tolerance in aged C57BL/6J mice. J Gerontol 41(4):453–459. https://doi.org/10.1093/geronj/41.4.453
Glanville EJ, Seebacher F (2010) Plasticity in body temperature and metabolic capacity sustains winter activity in a small endotherm (Rattus fuscipes). Comp Biochem Phys A 155:383–391. https://doi.org/10.1016/j.cbpa.2009.12.008
Gordon CJ (2012) Thermal physiology of laboratory mice: defining thermoneutrality. J Therm Biol 37:654–685. https://doi.org/10.1016/j.jtherbio.2012.08.004
Greg Kelly N (2006) Body temperature variability (part 1): a review of the history of body temperature and its variability due to site selection, biological rhythms, fitness, and aging. Altern Med Rev A J Clin Ther 11:278–293
Heldmaier G (1971) Nonshivering thermogenesis and body size in mammals. J Comp Physiol 73:222–248
Heldmaier G, Steinlechner S, Rafael J (1982) Nonshivering thermogenesis and cold resistance during seasonal acclimation in Djungarian hamster. J Comp Physiol 149:1–9
Iwen KASE, Brabant G (2013) Thyroid hormone and the metabolic syndrome. Eur Thyroid J 2:83–92. https://doi.org/10.1159/000351249
Jenni-Eiermann S, Jenni L, Piersma T (2002) Temporal uncoupling of thyroid hormones in red knots: T3 peaks in cold weather, T4 during moult. Journal Für Ornithologie 143:331–340. https://doi.org/10.1046/j.1439-0361.2002.02011.x
Jonas W, Lietzow J, Wohlgemuth F, Hoefig CS, Wiedmer P, Schweizer U, Kohrle J, Schurmann A (2015) 3,5-Diiodo-l-thyronine (3,5-t2) exerts thyromimetic effects on hypothalamus-pituitary-thyroid axis, body composition, and energy metabolism in male diet-induced obese mice. Endocrinology 156:389–399. https://doi.org/10.1210/en.2014-1604
Kaiyala KJ, Ogimoto K, Nelson JT, Schwartz MW, Morton GJ (2015) Leptin signaling is required for adaptive changes in food intake, but not energy expenditure, in response to different thermal conditions. PloS One 10:e0119391. https://doi.org/10.1371/journal.pone.0119391
Kim B (2008) Thyroid hormone as a determinant of energy expenditure and the basal metabolic rate. Thyroid 18:141–144. https://doi.org/10.1089/thy.2007.0266
Knudsen N, Laurberg P, Rasmussen LB, Bülow I, Perrild H, Ovesen L, Jørgensen T (2005) Small differences in thyroid function may be important for Body Mass Index and the occurrence of obesity in the population. J Clin Endocrinol Metab 90:4019–4024. https://doi.org/10.1210/jc.2004-2225
Lanni A, Moreno M, Lombardi A, Goglia F (2003) Thyroid hormone and uncoupling proteins. FEBS Lett 543:5–10. https://doi.org/10.1016/S0014-5793(03)00320-X
Li XS, Wang DH (2005a) Regulation of body weight and thermogenesis in seasonally acclimatized Brandt’s voles (Microtus brandti). Horm Behav 48:321–328. https://doi.org/10.1016/j.yhbeh.2005.04.004
Li XS, Wang DH (2005b) Seasonal adjustments in body mass and thermogenesis in Mongolian gerbils (Meriones unguiculatus): the roles of short photoperiod and cold. J Comp Physiol B 175:593–600. https://doi.org/10.1007/s00360-005-0022-2
Liu XT, Li QF, Huang CX, Sun RY (1997) Effects of thyroid status on cold-adaptive thermogenesis in Brandt’s vole, Microtus brandti. Physiol Zool 70:352–361. https://doi.org/10.1086/639613
Liu H, Wang DH, Wang ZW (2003) Energy requirements during reproduction in female Brandt’s voles (Microtus brandti). J Mamm 84:1410–1416. https://doi.org/10.1644/BRG-030
Liu JS, Chen YQ, Li M (2006) Thyroid hormones increase liver and muscle thermogenic capacity in the little buntings (Emberiza pusilla). J Therm Biol 31:386–393. https://doi.org/10.1016/j.jtherbio.2006.01.002
Liu JS, Yang M, Sun RY, Wang DH (2009) Adaptive thermogenesis in Brandt’s vole (Lasiopodomys brandti) during cold and warm acclimation. J Therm Biol 34:60–69. https://doi.org/10.1016/j.jtherbio.2008.11.001
Lovegrove BG (2000) The zoogeography of mammalian basal metabolic rate. Am Nat 156:201–219. https://doi.org/10.1086/303383
Lukaski HC, Hall CB, Marchello MJ (1992) Impaired thyroid hormone status and thermoregulation during cold exposure of zinc-deficient rats. Horm Metab Res 24:363–366. https://doi.org/10.1055/s-2007-1003336
Morrison SF (2016) Central control of body temperature. F1000 Res. https://doi.org/10.12688/f1000research.7958.1
Mozo J, Emre Y, Bouillaud F, Ricquier D, Criscuolo F (2005) Thermoregulation: what role for UCPs in mammals and birds? Biosci Rep 25:227–249. https://doi.org/10.1007/s10540-005-2887-4
Prusiner SB, Cannon B, Lindberg O (1968) Oxidative metabolism in cells isolated from brown adipose tissue. 1. Catecholamine and fatty acid stimulation of respiration. Eur J Biochem 6:15–22. https://doi.org/10.1111/j.1432-1033.1968.tb00413.x
Rashmi Mullur Y-YL, Brent GA (2014) Thyroid hormone regulation of metabolism. Physiol Rev 94:355–382. https://doi.org/10.1152/physrev.00030.2013.-Thyroid
Ravussin Y, Xiao C, Gavrilova O, Reitman ML (2014) Effect of intermittent cold exposure on brown fat activation, obesity, and energy homeostasis in mice. PloS One 9:e85876. https://doi.org/10.1371/journal.pone.0085876
Rawson RE, Concannon PW, Roberts PJ, Tennant BC (1998) Seasonal differences in resting oxygen consumption, respiratory quotient, and free thyroxine in woodchucks. Am J Physiol 274:R963–R969. https://doi.org/10.1152/ajpregu.1998.274.4.R963
Ribeiro MO, Carvalho SD, Schultz JJ, Chiellini G, Scanlan TS, Bianco AC, Brent GA (2001) Thyroid hormone-sympathetic interaction and adaptive thermogenesis are thyroid hormone receptor isoform-specific. J Clin Investig 108:97–105. https://doi.org/10.1172/JCI200112584
Santillo A, Burrone L, Falvo S, Senese R, Lanni A, Chieffi Baccari G (2013) Triiodothyronine induces lipid oxidation and mitochondrial biogenesis in rat Harderian gland. J Endocrinol 219:69–78. https://doi.org/10.1530/JOE-13-0127
Schreiber R, Diwoky C, Schoiswohl G, Feiler U, Wongsiriroj N, Abdellatif M, Kolb D, Hoeks J, Kershaw EE, Sedej S, Schrauwen P, Haemmerle G, Zechner R (2017) Cold-induced thermogenesis depends on ATGL-mediated lipolysis in cardiac muscle, but not brown adipose tissue. Cell Metab 26:753–763 e757. https://doi.org/10.1016/j.cmet.2017.09.004
Shi LL, Fan WJ, Zhang JY, Zhao XY, Tan S, Wen J, Cao J, Zhang XY, Chi QS, Wang DH, Zhao ZJ (2017) The roles of metabolic thermogenesis in body fat regulation in striped hamsters fed high-fat diet at different temperatures. Comp Biochem Phys A 212:35–44. https://doi.org/10.1016/j.cbpa.2017.07.002
Silva JE (2005) Thyroid hormone and the energetic cost of keeping body temperature. Biosci Rep 25:129–148. https://doi.org/10.1007/s10540-005-2882-9
Silva JE (2006) Thermogenic mechanisms and their hormonal regulation. Physiol Rev 86:435–464. https://doi.org/10.1152/physrev.00009.2005
Song Z, Wang D (2003) Metabolism and thermoregulation in the striped hamster Cricetulus barabensis. J Therm Biol 28:509–514. https://doi.org/10.1016/S0306-4565(03)00051-2
Swanson DL, Thomas NE (2007) The relationship of plasma indicators of lipid metabolism and muscle damage to overnight temperature in winter-acclimatized small birds. Comp Biochem Phys A 146:87–94. https://doi.org/10.1016/j.cbpa.2006.09.004
Tan S, Wen J, Shi LL, Wang CM, Wang GY, Zhao ZJ (2016) The increase in fat content in the warm-acclimated striped hamsters is associated with the down-regulated metabolic thermogenesis. Comp Biochem Phys A 201:162–172. https://doi.org/10.1016/j.cbpa.2016.07.013
Tata JR (1963) Inhibition of the biological action of thyroid hormones by actinomycin D and puromycin. Nature 197:1167–1168. https://doi.org/10.1038/1971167a0
Valente A, Jamurtas AZ, Koutedakis Y, Flouris AD (2015) Molecular pathways linking non-shivering thermogenesis and obesity: focusing on brown adipose tissue development. Biol Rev Camb Philos Soc 90:77–88. https://doi.org/10.1111/brv.12099
Vaughan MK, Little JC, Buzzell GR, Menendez-Pelaez A, Reiter RJ (1989) Natural decreasing temperature and photoperiod conditions or acute cold exposure affect circulating thyroid hormones, serum cholesterol and type II 5′-deiodinase in brown adipose tissue in the trumpet-tailed rat, Octodon degus. Biomed Res 10:469–474. https://doi.org/10.2220/biomedres.10.469
Wen J, Tan S, Qiao QG, Fan WJ, Huang YX, Cao J, Liu JS, Wang ZX, Zhao ZJ (2017) Sustained energy intake in lactating Swiss mice: a dual modulation process. J Exp Biol 220:2277–2286. https://doi.org/10.1242/jeb.157107
Wen J, Tan S, Wang DH, Zhao ZJ (2018) Variation of food availability affects male striped hamsters (Cricetulus barabensis) with different levels of metabolic rate. Integr Zool. https://doi.org/10.1111/1749-4877.12337
Worthmann A, John C, Ruhlemann MC, Baguhl M, Heinsen FA, Schaltenberg N, Heine M, Schlein C, Evangelakos I, Mineo C, Fischer M, Dandri M, Kremoser C, Scheja L, Franke A, Shaul PW, Heeren J (2017) Cold-induced conversion of cholesterol to bile acids in mice shapes the gut microbiome and promotes adaptive thermogenesis. Nat Med 23(7):839–849. https://doi.org/10.1038/nm.4357
Xu XM, Chi QS, Cao J, Zhao ZJ (2018) The effect of aggression I: the increases of metabolic cost and mobilization of fat reserves in male striped hamsters. Horm Behav 98:55–62. https://doi.org/10.1016/j.yhbeh.2017.12.015
Yen PM (2001) Physiological and molecular basis of thyroid hormone action. Physiol Rev 81:1097–1142. https://doi.org/10.1152/physrev.2001.81.3.1097
Zhang Z, Wang Z (1998) Ecology and management of rodent pests in agriculture. China Ocean Press, Beijing, pp 209–238. https://doi.org/10.1111/j.1749-4877.2007.00058.x
Zhang X, Zhao Z, Vasilieva N, Khrushchova A, Wang D (2015) Effects of short photoperiod on energy intake, thermogenesis, and reproduction in desert hamsters (Phodopus roborovskii). Integr Zool 10:207–215. https://doi.org/10.1111/1749-4877.12115
Zhang XY, Sukhchuluun G, Bo TB, Chi QS, Yang JJ, Chen B, Zhang L, Wang DH (2018) Huddling remodels gut microbiota to reduce energy requirements in a small mammal species during cold exposure. Microbiome 6(1):103. https://doi.org/10.1186/s40168-018-0473-9
Zhao ZJ, Wang DH (2007) Effects of diet quality on energy budgets and thermogenesis in Brandt’s voles. Comp Biochem Phys A 148:168–177. https://doi.org/10.1371/journal.pone.0084396
Zhao ZJ, Cao J, Meng XL, Li YB (2010a) Seasonal variations in metabolism and thermoregulation in the striped hamster (Cricetulus barabensis). J Therm Biol 35:52–57. https://doi.org/10.1016/j.jtherbio.2009.10.008
Zhao ZJ, Cao J, Liu ZC, Wang GY, Li LS (2010b) Seasonal regulations of resting metabolic rate and thermogenesis in striped hamster (Cricetulus barabensis). J Therm Biol 35:401–405. https://doi.org/10.1016/j.jtherbio.2010.08.005
Zhao ZJ, Chen KX, Liu YA, Wang CM, Cao J (2014a) Decreased circulating leptin and increased neuropeptide Y gene expression are implicated in food deprivation-induced hyperactivity in striped hamsters, Cricetulus barabensis. Horm Behav 65:355–362. https://doi.org/10.1016/j.yhbeh.2014.03.001
Zhao ZJ, Chi QS, Liu QS, Zheng WH, Liu JS, Wang DH (2014b) The shift of thermoneutral zone in striped hamster acclimated to different temperatures. PloS One. https://doi.org/10.1242/jeb.046821
Zheng WH, Fang YY, Jiang XH, Zhang GK, Liu JS (2010) Comparison of thermogenic character of liver and muscle in Chinese bulbul Pycnonotus sinensis between summer and winter. Zool Res 31:319–327. https://doi.org/10.3724/SP.J.1141.2010.03319
Zheng WH, Lin L, Liu JS, Pan H, Cao MT, Hu YL (2013) Physiological and biochemical thermoregulatory responses of chinese bulbuls Pycnonotus sinensis to warm temperature: phenotypic flexibility in a small passerine. J Therm Biol 38:240–246. https://doi.org/10.1016/j.jtherbio.2013.03.003
Zhou LM, Xia SS, Chen Q, Wang RM, Zheng WH, Liu JS (2016) Phenotypic flexibility of thermogenesis in the Hwamei (Garrulax canorus): responses to cold acclimation. Am J Physiol Regul Integr Comp Physiol 310(4):R330–R336. https://doi.org/10.1152/ajpregu.00259.2015
Zietak M, Kovatcheva-Datchary P, Markiewicz LH, Stahlman M, Kozak LP, Backhed F (2016) Altered microbiota contributes to reduced diet-induced obesity upon cold exposure. Cell Metab 23(6):1216–1223. https://doi.org/10.1016/j.cmet.2016.05.001
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This work was funded by Grants (no. 31670417) from the National Natural Science Foundation of China, and also partly supported by grants (no. Chinese IPM1704) from the State Key Laboratory of Integrated Management of Pest Insects and Rodents.
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Wen, J., Qiao, Qg., Zhao, Zj. et al. Effects of thyroid hormones and cold acclimation on the energy metabolism of the striped hamster (Cricetulus barabensis). J Comp Physiol B 189, 153–165 (2019). https://doi.org/10.1007/s00360-018-1197-7
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DOI: https://doi.org/10.1007/s00360-018-1197-7