Abstract
Survival of small mammals in winter requires proper adjustments in physiology, behavior and morphology. The present study was designed to examine the changes in serum leptin concentration and the molecular basis of thermogenesis in seasonally acclimatized root voles (Microtus oeconomus) from the Qinghai-Tibetan plateau. In January root voles had lower body mass and body fat mass coupled with higher nonshivering thermogenesis (NST) capacity. Consistently, cytochrome c oxidase activity and mitochondrial uncoupling protein-1 (UCP1) protein contents in brown adipose tissues were higher in January as compared to that in July. Circulating level of serum leptin was significantly lower in winter and higher in July. Correlation analysis showed that serum leptin levels were positively related with body mass and body fat mass while negatively correlated with UCP1 protein contents. Together, these data provided further evidence for our previous findings that root voles from the Qinghai-Tibetan plateau mainly depend on higher NST coupled with lower body mass to enhance winter survival. Further, fat deposition was significantly mobilized in cold winter and leptin was potentially involved in the regulation of body mass and thermogenesis in root voles. Serum leptin might act as a starvation signal in winter and satiety signal in summer.
Similar content being viewed by others
References
Abelenda M, Ledesma A, Rial E, Puerta M (2003) Leptin administration to cold-acclimated rats reduces both food intake and brown adipose tissue thermogenesis. J Therml Biol 28:525–530
Barbara C, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84:277–359
Berthoud (2005) A new role for leptin as a direct satiety signal from the stomach. Am J Physiol Regul Integr Comp Physiol 288:796–797
Bing C, Frankish HM, Pickavance L, Wang Q, Hopkins DFC, Stock MJ, Williams G. (1998) Hyperphagia in cold-exposed rats is accompanied by decreased plasma leptin but unchanged hypothalamic NPY. Am J Physiol Regul Integr Comp Physiol 274:R62–R68
Bozinovic F, Gallardo PA, Visser RH, Corte´s A (2003) Seasonal acclimatization in water flux rate, urine osmolality and kidney water channels in free-living degus: molecular mechanisms, physiological processes and ecological implications. J Exp Biol 206:2959–2966
Bozinovic F, Bacigalupe LD, Vasquez RA, Visser GH, Veloso C, Kenagy G.J (2004) Cost of living in free-ranging degus (Octodon degus): seasonal dynamics of energy expenditure. Comp Biochem Physiol A 137:597–604
Brunhoff CK, Galbreath E, Fedorov VB, Cook JA, Jaarola M (2003) Holarctic phylogeography of the root vole ( Microtus oeconomus ): implications for late Quaternary biogeography of high latitudes. Mol Ecol 12:957–968
Buckley CA, Schneider JE (2003) Peptides that Regulate Food Intake Food hoarding is increased by food deprivation and decreased by leptin treatment in Syrian hamsters. Am J Physiol Regul Integr Comp Physiol 285:R1021–R1029
Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84(1):277–359
Commins SP, Watson PM, Frampton IC, Gettys TW (2001) Leptin selectively reduces white adipose tissue in mice via a UCP1-dependent mechanism in brown adipose tissue. Am J Physiol Endocrinol Metab 280:E372–E377
Dijk G.V (2001) The role of leptin in the regulation of energy balance and adiposity. J Neuroendocrinol (13):913–921
Feist DD, Feist CF (1986) Effect of cold, short day and melatonin on thermogenesis, body weight and reproductive organs in Alaskan red-backed voles. J Comp Physiol B 156:741–746
Friedman JM, Halaas JL (1998) Leptin and the regulation of body weight in mammals. Nature 395:763–770
Haim A (1996) Food and energy intake, non-shivering thermogenesis and daily rhythm of body temperature in the bushy-tailed gerbil Sekeetamys calurus: The role of photoperiod manipulations. J Therm Biol 21(1):37–42
Heldmaier G (1971) Zitterfreie wärmebildung und körpergröße bei säugetieren. Z Vergl Physiologie 73:222–248
Heldmaier G, Steinlechner S, Rafael J (1982) Nonshivering thermogenesisand cold resistance during seasonal acclimatization in the Djungarian hamster. J Comp Physiol B 149:1–9
Janskey L (1973) Non-shievering thermogenesis and its thermoregulatory significance. Biol Rev 48:85–132
Jefimow M, Wojciechowski M, Tegowska E (2004a) Seasonal changes in the thermoregulation of laboratory golden hamsters during acclimation to seminatural outdoor conditions. Comp Biochem Physiol A 139(3):379–388
Jefimow M, Wojciechowski M, Tegowska E (2004b) Seasonal and daily changes in the capacity for nonshivering thermogenesis in the golden hamsters housed under semi-natural conditions. Comp Biochem Physiol A 137(2):297–309
Jia XX, Sun RY (1986) Characteristics of the resting metabolic rate of the root vole at high altitude. Acta Zool Sinica 32: 280–287 (In Chinese with English summary )
Johnson MS, Onorato DP, Gower BA, Nagy TR (2004) Weight change affects serum leptin and corticosterone in the collared lemming. Gen Comp Endocrinol 136(1):30–36
Klause S, Heldmaier G, Ricquier D (1988) Seasonal acclimation of blank voles and wood mice: noshievering thermogenesis and thermogenic properties of brown adipose tissue mitochondria. J Comp Physiol B 158:157–164
Klingenspor M, Dickopp A, Heldmaier G, Klaus S (1996) Short photoperiod reduces leptin gene expression in white and brown adipose tissue of Djungarian hamster. FEBS Letts 399:290–294
Klingenspor M, Niggemann H, Heldmaier G. (2000) Modulation of leptin sensititivity by short photoperiod acclimation in the Djungarian hamster Phodopus sungorus . J Comp Physiol B 170:37–43
Krauss S, Zhang CY, Lowell BB (2005) The mitochondrial uncoupling-protein homologues. Nat Rev Mol Cell Biol 6:248–261
Kronfeld-Schor N, Haim A, Dayan T, Zisapel N, Klingenspor M, Heldmaier G. (2000) Seasonal thermogenic acclimation of diurnally and nocturnally active desert spiny mice. Physiol Biochem Zool 73(1):37–44
Li QF, Sun RY, Huang CX, Wang ZK, Liu XT, Hou JJ (2001) Cold adaptive thermogenesis in small mammals from different geographical zones of China. Comp Biochem Physiol A 129:949–961
Li XS (2005) Mechanism of body mass regulation and thermogenesis in Brandt’s voles and Mongolian gerbils. Ph.D Dissertation. Institute of Zoology, the Chinese Academy of Sciences
Li XS, Wang DH (2005a) Regulation of body weight and thermogenesis in seasonally acclimatized Brandt’s voles (Microtus brandti). Horm Behav 48(3):321–328
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
Li YN, Zhao XQ, Cao GM, Zhao L, Wang QX (2004) Analysis on climates and vegetation productivity background at Haibei Alpine Meadow Ecosystem Research Station. Plateau Metrol 23(4):558–567 (In Chinese with English summary)
Lowry OH, Rosbrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin-phenol reagents. J Biol Chem 193:265
Lynch GR (1973) Seasonal changes in thermogenesis, organ weights, and body composition in the whited-footed mouse, Peromyscus leucopus. Oecologia (Berl) 13:363–376
Nagy TR, Gower BA, Stetson MH (1995) Endocrine correlates of seasonal body mass dynamics in the collared lemming Dicrostonyx groenlandicus. Am Zool 35:246–258
Nespolo RF, Bacigalupe LD, Rezende EL, Bozinovic F (2001) When nonshivering thermogenesis equals maximum metabolic rate: thermal acclimation and phenotypic plasticity of fossorial Spalacopus cyanus (Rodentia). Physiol Biochem Zool 74:325–332
Nicholls DG, Locke RM (1984) Thermogenic mechanisms in brown fat. Physiol Rev 64:1–64
Paracchini V, Pedotti P, Taioli E (2005) Genetics of leptin and obesity: a huge review. Am J Epidemiol 162(2):101–114
Praun CV, Burkert M, Gessner M, Klingenspor M (2001) Tissue specific expression and cold-induced mRNA levels of uncoupling proteins in the Djungarian hamster. Physiol Biochem Zool 74(2):203–211
Ricquier D, Bouilloud F (2000) The uncoupling protein homologues: UCP1, UCP2, UCP3, StUCP and AtUCP. Biochem J 345:161–179
Rousseau K, Atcha Z, Loudon ASI (2003) Leptin and seasonal mammals. J Neuroendo 15:409–414
Scantlebury M, Oosthuizen MK, Speakman JR, Jackson CR, Bennett NC (2005) Seasonal energetics of the Hottentot golden mole at 1500 m altitude. Physiol Behav 84(5):739–745
Scarpace PJ, Matheny M, Pollock BH, Tumer N (1997) Leptin increases uncoupling protein expression and energy expenditure. Am J Physiol Endocrinol Metab 273:E226–E230
Wang DH, Wang ZW (1989) Strategies for survival of small mammals in a cold environment I. Seasonal variations in the weight and structure of brown adipose tissue in Ochotona curzoniae and Microtus oeconomus. Acta Theriol Sinica 9:176–185 (In Chinese with English summary)
Wang DH, Wang ZW (1996) Seasonal variations in thermogenesis and energy requirements of plateau pikas Ochotona curzoniae and root voles Microtus oeconomus. Acta Theriol 41(3):225–236
Wang DH, Wang ZW (2000) Metabolism and thermoregulation in root vole (Microtus oeconomus) from the Qinghai-Tibetan Plateau. Mamm Biol 65:15–20
Wang DH, Sun RY, Wang ZW (1996) Maximum energy assimilation rate in the root voles (Microtus oeconomus). Acta Zool Sinica 42(1):35–41 (In Chinese with English summary)
Wang DH, Sun RY, Wang ZW, Liu JS (1999) Effects of temperature and photoperiod on thermogenesis in plateau pikas (Ochotona curzoniae) and root voles (Microtus oeconomus). J Comp Physiol B 169(1):77–83
Wang DH, Wang ZW, Feng Y (1991) Strategies for survival of small mammals in a cold alpine environment. Thermoregulation of Ochotona cansus and adaptive convergence of small mammals to cold and high altitude. Alpine Meadow Ecosystem 3:125–137 (In Chinese with English summary)
Wang ZW, Zeng JX, Han YC (1979) Studies on the metabolism rates of the mouse hare (Ochotona curzoniae) and the mole rat (Myospalax fontanierii). Acta Zool Sinica 25(1):75–85 (In Chinese with English summary)
Wunder BA, Dobkin DS, Gettinger RT (1977) Shifts of thermogenesis in the prairie vole (Microtus ochrogaster): strategies for survival in a seasonal environment. Oecologia 29:11–26
Zeng JX, Wang ZW, Han YC (1981) On the daily activity rhythm of five small mammals. Acta Theriol Sinica 1:189–197 (In Chinese with English summary)
Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM (1994) Positional cloning of the mouse obese gene and it’s human homologue. Nature 372:425–432
Zhang ZQ (2005) Seasonal changes in thermogenesis, energy budgets and immune function in Mongolian gerbils (Meriones unguiculatus). Ph.D Dissertation. Institute of Zoology, the Chinese Academy of Sciences
Zhao ZJ, Wang DH (2005) Short photoperiod enhances thermogenic capacity in Brandt’s voles. Physiol Behav 85(2):143–149
Acknowledgments
We wish to thank Ying-Nian Li, Northwest Plateau Institute of Biology, the Chinese Academy of Sciences, for helping catch the animals. Thanks to Dr. Martin Klingenspor, Department of Biology, Philipps-University Marburg, Germany, for providing the hamster UCP1 antibody. Thanks to all the members of Animal Physiological Ecology Group, Institute of Zoology of the Chinese Academy of Sciences, for helping the experiments. This study was financially supported by the National Natural Science Foundation of China (No. 30430140 and No. 30170151) and the Chinese Academy of Sciences (No. KSCX2-SW-103) to DHW.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by I.D. Hume
Rights and permissions
About this article
Cite this article
Wang, JM., Zhang, YM. & Wang, DH. Seasonal regulations of energetics, serum concentrations of leptin, and uncoupling protein 1 content of brown adipose tissue in root voles (Microtus oeconomus) from the Qinghai-Tibetan plateau. J Comp Physiol B 176, 663–671 (2006). https://doi.org/10.1007/s00360-006-0089-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-006-0089-4