Skip to main content
Springer Nature Link
Log in

Torpor patterns, arousal rates, and temporal organization of torpor entry in wildtype and UCP1-ablated mice

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

In eutherian mammals, uncoupling protein 1 (UCP1) mediated non-shivering thermogenesis from brown adipose tissue (BAT) provides a mechanism through which arousal from torpor and hibernation is facilitated. In order to directly assess the magnitude by which the presence or absence of UCP1 affects torpor patterns, rewarming and arousal rates within one species we compared fasting induced torpor in wildtype (UCP1+/+) and UCP1-ablated mice (UCP−/−). Torpor was induced by depriving mice of food for up to 48 h and by a reduction of ambient temperature (T a) from 30 to 18°C at four different time points after 18, 24, 30 and 36 h of food deprivation. In most cases, torpor bouts occurred within 20 min after the switch in ambient temperature (30–18°C). Torpor bouts expressed during the light phase lasted 3–6 h while significantly longer bouts (up to 16 h) were observed when mice entered torpor during the dark phase. The degree of hypometabolism (5–22 ml h−1) and hypothermia (19.5–26.7°C) was comparable in wildtype and UCP1-ablated mice, and both genotypes were able to regain normothermia. In contrast to wildtype mice, UCP1-ablated mice did not display multiple torpor bouts per day and their peak rewarming rates from torpor were reduced by 50% (UCP1+/+: 0.24 ± 0.08°C min−1; UCP1−/−: 0.12 ± 0.04°C min−1). UCP1-ablated mice therefore took significantly longer to rewarm from 25 to 32°C (39 vs. 70 min) and required 60% more energy for this process. Our results demonstrate the energetic benefit of functional BAT for rapid arousal from torpor. They also suggest that torpor entry and maintenance may be dependent on endogenous rhythms.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Abbreviations

BAT:

Brown adipose tissue

CET:

Central European time

NST:

Non-shivering thermogenesis

UCP:

Uncoupling protein

T a :

Ambient temperature

T b :

Body temperature

References

  • Barclay RM, Lausen CL, Hollis L (2001) What’s hot and what’s not: defining torpor in free-ranging birds and mammals. Can J Zool 79:1885–1890

    Article  Google Scholar 

  • Braulke LJ, Heldmaier G (2010) Torpor and ultradian rhythms require an intact signalling of the sympathetic nervous system. Cryobiology 60:198–203

    Article  CAS  PubMed  Google Scholar 

  • Brown JC, Staples JF (2010) Mitochondrial metabolism during fasting-induced daily torpor in mice. Biochim Biophys Acta 1797:476–486

    Article  CAS  PubMed  Google Scholar 

  • Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84:277–359

    Article  CAS  PubMed  Google Scholar 

  • Dikic D, Heldmaier G, Meyer CW (2008) Induced torpor in different strains of laboratory mice. In: Lovegrove BG, McKechnie AE (eds) Hypometabolism in animals: torpor. hibernation and cryobiology. Pietermaritzburg, University of KwaZulu-Natal, pp 223–230

    Google Scholar 

  • Ehrhardt N, Heldmaier G, Exner C (2005) Adaptive mechanisms during food restriction in Acomys russatus: the use of torpor for desert survival. J Comp Physiol [B] 175:193–200

    CAS  Google Scholar 

  • Enerback S, Jacobsson A, Simpson EM, Guerra C, Yamashita H, Harper ME, Kozak LP (1997) Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese. Nature 387:90–94

    Article  CAS  PubMed  Google Scholar 

  • Exner C, Hebebrand J, Remschmidt H, Wewetzer C, Ziegler A, Herpertz S, Schweiger U, Blum WF, Preibisch G, Heldmaier G, Klingenspor M (2000) Leptin suppresses semi-starvation induced hyperactivity in rats: implications for anorexia nervosa. Mol Psychiatry 5:476–481

    Article  CAS  PubMed  Google Scholar 

  • Foster DO, Frydman ML (1978) Brown adipose tissue: the dominant site of nonshivering thermogenesis in the rat. Experientia Suppl 32:147–151

    CAS  PubMed  Google Scholar 

  • Gavrilova O, Leon LR, Marcus-Samuels B, Mason MM, Castle AL, Refetoff S, Vinson C, Reitman ML (1999) Torpor in mice is induced by both leptin-dependent and -independent mechanisms. Proc Natl Acad Sci USA 96:14623–14628

    Article  CAS  PubMed  Google Scholar 

  • Geiser F (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu Rev Physiol 66:239–274

    Article  CAS  PubMed  Google Scholar 

  • Geiser F, Baudinette RV (1990) The relationship between body mass and rate of rewarming from hibernation and daily torpor in mammals. J Exp Biol 151:349–359

    CAS  PubMed  Google Scholar 

  • Golozoubova V, Cannon B, Nedergaard J (2006) UCP1 is essential for adaptive adrenergic nonshivering thermogenesis. Am J Physiol Endocrinol Metab 291:E350–E357

    Article  CAS  PubMed  Google Scholar 

  • Granneman JG, Burnazi M, Zhu Z, Schwamb LA (2003) White adipose tissue contributes to UCP1-independent thermogenesis. Am J Physiol Endocrinol Metab 285:E1230–E1236

    CAS  PubMed  Google Scholar 

  • Hayward JS, Lisson PA (1991) Evolution of brown fat: its absence in marsupials and monotremes. Can J Zool 70:171–179

    Article  Google Scholar 

  • Heldmaier G (1970) Die Thermogenese der Mausohrfledermaus (Myotis myotis) beim Erwachen aus dem Winterschlaf. Z Vergl Physiol 63:59–84

    Article  Google Scholar 

  • Heldmaier G (1975) Metabolic and thermoregulatory responses to heat and cold in the Djungarian hamster, Phodopus sungorus. J Comp Physiol 102:115–122

    Google Scholar 

  • Heldmaier G, Buchberger A (1985) Sources of heat during nonshivering thermogenesis in Djungarian hamsters: a dominant role of brown adipose tissue during cold adaptation. J Comp Physiol [B] 156:237–245

    CAS  Google Scholar 

  • Heldmaier G, Ruf T (1992) Body temperature and metabolic rate during natural hypothermia in endotherms. J Comp Physiol [B] 162:696–706

    CAS  Google Scholar 

  • Heldmaier G, Steinlechner S (1981) Seasonal control of energy requirements for thermoregulation in the Djungarian hamster (Phodopus sungorus), living in natural photoperiod. J Comp Physiol 142:429–437

    Google Scholar 

  • Heldmaier G, Ortmann S, Elvert R (2004) Natural hypometabolism during hibernation and daily torpor in mammals. Respir Physiol Neurobiol 141:317–329

    Article  PubMed  Google Scholar 

  • Hudson JW, Scott IM (1979) Daily torpor in the laboratory mouse, Mus musculus var. albino. Physiol Zool 52:205–218

    Google Scholar 

  • Jansky L (1973) Non-shivering thermogenesis and its thermoregulatory significance. Biol Rev 48:85–132

    CAS  PubMed  Google Scholar 

  • Jastroch M, Withers KW, Taudien S, Frappell PB, Helwig M, Fromme T, Hirschberg V, Heldmaier G, McAllan BM, Firth BT, Burmester T, Platzer M, Klingenspor M (2008) Marsupial uncoupling protein 1 sheds light on the evolution of mammalian nonshivering thermogenesis. Physiol Genomics 32:161–169

    CAS  PubMed  Google Scholar 

  • Jethwa PH, I’anson H, Warner A, Prosser HM, Hastings MH, Maywood ES, Ebling FJ (2008) Loss of prokineticin receptor 2 signaling predisposes mice to torpor. Am J Physiol Regul Integr Comp Physiol 294:R1968–R1979

    CAS  PubMed  Google Scholar 

  • Lovegrove BG, Koertner G, Geiser F (1999) The energetic cost of arousal from torpor in the marsupial Sminthopsis macroura: benefits of summer ambient temperature cycles. J Comp Physiol [B] 169:11–18

    CAS  Google Scholar 

  • Lyman CP, O’Brian RC (1986) Is brown fat necessary? In: Heller HC, Musacchia XJ, Wang LHC (eds) Living in the cold: physiological and biochemical adaptations. Elsevier, New York, pp 116–119

    Google Scholar 

  • McKechnie AE, Lovegrove BG (2001) Heterothermic responses in the speckled mousebird (Colius striatus). J Comp Physiol [B] 171:507–518

    CAS  Google Scholar 

  • McKechnie AE, Wolf BO (2004) The energetics of the rewarming phase of avian torpor. In: Barnes BM, Carey HV (eds) Life in the cold, evolution, mechanism, adaptation and application. Alaska University of Alaska Fairbanks, Institute of Arctic Biology, Fairbanks, pp 265–273

    Google Scholar 

  • Mzilikazi N, Lovegrove BG, Ribeiro MO (2002) Exogenous passive heating during torpor arousal in free-ranging rock elephant shrews, Elephantulus myurus. Oecologia 133:307–314

    Article  Google Scholar 

  • Nicol SC, Morrow G, Andersen NA (2008) Hibernation in monotremes: a review. In: Lovegrove BG, McKechnie AE (eds) Hypometabolism in animals: hibernation, torpor and cryobiology. University of KwaZulu-Natal, Pietermaritzburg, pp 251–262

    Google Scholar 

  • Nicol SC, Andersen NA, Arruda AP, Ruf T (2009) Rewarming rates of two large hibernators: comparison of a monotreme and a eutherian. J Therm Biol 34:155–159

    Article  Google Scholar 

  • Oelkrug R, Kutschke M, Meyer CW, Heldmaier G, Jastroch M (2010) Uncoupling protein 1 decreases superoxide production in brown adipose tissue mitochondria. J Biol Chem (PMID: 20466728)

  • Ootsuka Y, de Menezes RC, Zaretsky DV, Alimoradian A, Hunt J, Stefanidis A, Oldfield BJ, Blessing WW (2009) Brown adipose tissue thermogenesis heats brain and body as part of the brain-coordinated ultradian basic rest-activity cycle. Neuroscience 164:849–861

    Article  CAS  PubMed  Google Scholar 

  • Ortmann S, Heldmaier G, Schmid J, Ganzhorn JU (1997) Spontaneous daily torpor in Malagasy mouse lemurs. Naturwissenschaften 84:28–32

    Article  CAS  PubMed  Google Scholar 

  • Puchalski W, Bockler H, Heldmaier G, Langefeld M (1987) Organ blood flow and brown adipose tissue oxygen consumption during noradrenaline-induced nonshivering thermogenesis in the Djungarian hamster. J Exp Zool 242:263–271

    Article  CAS  PubMed  Google Scholar 

  • Rowlatt U, Mrosovsky N, Englisch A (1971) A comparative survey of brown fat in the neck and axilla of mammals at birth. Biol Neonate 17:53–83

    Article  CAS  PubMed  Google Scholar 

  • Ruby NF, Zucker I (1992) Daily torpor in the absence of the suprachiasmatic nucleus in Siberian hamsters. Am J Physiol 263:R353–R362

    CAS  PubMed  Google Scholar 

  • Scholander PF, Hock R, Walters V, Irving L (1950) Adaptation to cold in arctic and tropical mammals and birds in relation to body temperature insulation, and basal metabolic rate. Biol Bull 99:259–271

    Article  CAS  PubMed  Google Scholar 

  • Shabalina IG, Hoeks J, Kramarova TV, Schrauwen P, Cannon B, Nedergaard J (2010) Cold tolerance of UCP1-ablated mice: A skeletal muscle mitochondria switch toward lipid oxidation with marked UCP3 up-regulation not associated with increased basal, fatty acid- or ROS-induced uncoupling or enhanced GDP effects. Biochim Biophys Acta 1797(6–7):968–980

    CAS  PubMed  Google Scholar 

  • Stone GN, Purvis A (1992) Warm-up rates during arousal from torpor in heterothermic mammals: physiological correlates and a comparison with heterothermic insects. J Comp Physiol [B] 162:284–295

    CAS  Google Scholar 

  • Swoap SJ, Weinshenker D (2008) Norepinephrine controls both torpor initiation and emergence via distinct mechanisms in the mouse. PLoS One 3:e4038

    Google Scholar 

  • Swoap SJ, Gutilla MJ, Liles LC, Smith RO, Weinshenker D (2006) The full expression of fasting-induced torpor requires beta 3-adrenergic receptor signalling. J Neurosci 26:241–245

    Article  CAS  PubMed  Google Scholar 

  • Ukropec J, Anunciado RP, Ravussin Y, Hulver MW, Kozak LP (2006) UCP1-independent thermogenesis in white adipose tissue of cold-acclimated Ucp1−/− mice. J Biol Chem 281:31894–31908

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Kimura K, Inokuma K, Saito M, Kontani Y, Kobayashi Y, Mori N, Yamashita H (2006) Potential contribution of vasoconstriction to suppression of heat loss and homeothermic regulation in UCP1-deficient mice. Pflugers Arch 452:363–369

    Article  CAS  PubMed  Google Scholar 

  • Warnecke L, Geiser F (2010) The energetics of basking behaviour and torpor in a small marsupial exposed to simulated natural conditions. J Comp Physiol [B] 180:437–445

    Google Scholar 

  • Webb GP, Jagot SA, Jakobson ME (1982) Fasting-induced torpor in Mus musculus and its implications in the use of murine models for human obesity. Comp Biochem Physiol 72A:211–219

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by DFG (grant #HE-990 to GH and CWM).

Author information

Authors and Affiliations

  1. Department of Animal Physiology, Faculty of Biology, Philipps-Universität, Karl-von-Frisch Strasse 8, 35043, Marburg, Germany

    R. Oelkrug, G. Heldmaier & C. W. Meyer

Authors
  1. R. Oelkrug
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. G. Heldmaier
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. C. W. Meyer
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to C. W. Meyer.

Additional information

Communicated by H. V. Carey.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Oelkrug, R., Heldmaier, G. & Meyer, C.W. Torpor patterns, arousal rates, and temporal organization of torpor entry in wildtype and UCP1-ablated mice. J Comp Physiol B 181, 137–145 (2011). https://doi.org/10.1007/s00360-010-0503-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-010-0503-9

Keywords