Effects of thyroid hormones and cold acclimation on the energy metabolism of the striped hamster (Cricetulus barabensis)

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.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. 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

    Article  CAS  PubMed  Google Scholar 

  3. 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

    Article  CAS  PubMed  Google Scholar 

  4. 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

    Article  CAS  Google Scholar 

  5. Bernal J (2002) Action of thyroid hormone in brain. J Endocrinol Investig 25:268–288. https://doi.org/10.1007/BF03344003

    Article  CAS  Google Scholar 

  6. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. 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

    Article  CAS  PubMed  Google Scholar 

  8. 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

    Article  Google Scholar 

  9. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. 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

    Article  Google Scholar 

  11. 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

    CAS  Article  PubMed  Google Scholar 

  12. 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

    Article  PubMed  PubMed Central  Google Scholar 

  13. 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

    Article  PubMed  Google Scholar 

  14. 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

    Google Scholar 

  15. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. 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

    Article  CAS  PubMed  Google Scholar 

  17. 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

    Article  CAS  PubMed  Google Scholar 

  18. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. 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

    Article  CAS  PubMed  Google Scholar 

  20. 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

    Article  PubMed  Google Scholar 

  21. 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

    Article  PubMed  PubMed Central  Google Scholar 

  22. 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

    Article  Google Scholar 

  23. 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

    Article  CAS  PubMed  Google Scholar 

  24. 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

    Article  CAS  Google Scholar 

  25. 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

    Article  Google Scholar 

  26. 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

    Google Scholar 

  27. Heldmaier G (1971) Nonshivering thermogenesis and body size in mammals. J Comp Physiol 73:222–248

    Google Scholar 

  28. Heldmaier G, Steinlechner S, Rafael J (1982) Nonshivering thermogenesis and cold resistance during seasonal acclimation in Djungarian hamster. J Comp Physiol 149:1–9

    Article  Google Scholar 

  29. Iwen KASE, Brabant G (2013) Thyroid hormone and the metabolic syndrome. Eur Thyroid J 2:83–92. https://doi.org/10.1159/000351249

    Article  PubMed  PubMed Central  Google Scholar 

  30. 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

    Article  Google Scholar 

  31. 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

    Article  CAS  PubMed  Google Scholar 

  32. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. 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

    Article  CAS  PubMed  Google Scholar 

  34. 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

    Article  CAS  PubMed  Google Scholar 

  35. 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

    Article  CAS  PubMed  Google Scholar 

  36. 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

    Article  PubMed  Google Scholar 

  37. 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

    Article  CAS  PubMed  Google Scholar 

  38. 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

    Article  CAS  PubMed  Google Scholar 

  39. 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

    Article  Google Scholar 

  40. 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

    Article  CAS  Google Scholar 

  41. 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

    Article  CAS  Google Scholar 

  42. Lovegrove BG (2000) The zoogeography of mammalian basal metabolic rate. Am Nat 156:201–219. https://doi.org/10.1086/303383

    Article  PubMed  Google Scholar 

  43. 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

    Article  CAS  PubMed  Google Scholar 

  44. Morrison SF (2016) Central control of body temperature. F1000 Res. https://doi.org/10.12688/f1000research.7958.1

    Article  Google Scholar 

  45. 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

    Article  CAS  PubMed  Google Scholar 

  46. 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

    Article  CAS  PubMed  Google Scholar 

  47. 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

    Article  PubMed  PubMed Central  Google Scholar 

  48. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. 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

    CAS  Article  PubMed  Google Scholar 

  50. 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

    Article  CAS  PubMed  Google Scholar 

  51. 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

    Article  CAS  PubMed  Google Scholar 

  52. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. 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

    Article  CAS  Google Scholar 

  54. 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

    Article  CAS  PubMed  Google Scholar 

  55. Silva JE (2006) Thermogenic mechanisms and their hormonal regulation. Physiol Rev 86:435–464. https://doi.org/10.1152/physrev.00009.2005

    Article  CAS  PubMed  Google Scholar 

  56. 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

    Article  Google Scholar 

  57. 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

    Article  CAS  Google Scholar 

  58. 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

    Article  CAS  Google Scholar 

  59. 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

    Article  CAS  PubMed  Google Scholar 

  60. 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

    Article  PubMed  Google Scholar 

  61. 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

    Article  CAS  Google Scholar 

  62. 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

    Article  PubMed  Google Scholar 

  63. 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

    Article  PubMed  Google Scholar 

  64. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. 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

    Article  PubMed  Google Scholar 

  66. 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

    Article  CAS  PubMed  Google Scholar 

  67. 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

    Google Scholar 

  68. 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

    Article  PubMed  Google Scholar 

  69. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. 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

    Article  CAS  Google Scholar 

  71. 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

    Article  Google Scholar 

  72. 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

    Article  Google Scholar 

  73. 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

    Article  CAS  PubMed  Google Scholar 

  74. 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

    Article  PubMed  PubMed Central  Google Scholar 

  75. 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

    CAS  Article  PubMed  Google Scholar 

  76. 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

    Article  Google Scholar 

  77. 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

    Article  PubMed  Google Scholar 

  78. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

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.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Jin-song Liu.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by G. Heldmaier.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 38 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Wen, J., Qiao, Q., Zhao, Z. 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

Download citation

Keywords

  • Thyroid hormones
  • Cold adaptation
  • Thermogenesis
  • Triiodothyronine
  • Thyroxine