Skip to main content
Log in

Effect of photoperiod and acclimation temperature on nonshivering thermogenesis and GDP-binding of brown fat mitochondria in the Djungarian hamsterPhodopus s. sungorus

  • Heart, Circulation, Respiration and Blood; Environmental and Exercise Physiology
  • Published:
Pflügers Archiv - European Journal of Physiology Aims and scope Submit manuscript

Abstract

Acclimation to short photoperiod at 23° C constantT a causedP. sungorus to improve their NST capacity from 752 to 1,082 mW. Chronic cold exposure in short photoperiod further enhanced the NST capacity, reaching a maximum level of 1,573 mW at −5° C acclimation temperature. Improvements in NST capacity were always accompanied by an increase in brown fat mitochondrial mass and GDP-binding of brown fat mitochondria, in proportion with the cold load applied during temperature acclimation (23°, 15°, 5°, −5° C). Brown fat mitochondrial protein increased from 7.41 mg (23° CT a, long photoperiod) through 21.6 mg (23° CT a, short photoperiod) and 81.6 mg (−5° CT a, short photoperiod). This ∼10-fold increase was accompanied by a ∼35-fold increase in GDP-binding (2.0, 7.3 and 71.6 nmol GDP bound, respectively), demonstrating that the increase in capacity for uncoupled respiration in brown fat is of primary significance for thermogenic acclimation to cold as well as to short photoperiod.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

Cox:

cytochrome c oxidase

GDP:

guanosine-5-diphosphate

NST:

nonshivering thermogenesis

K-Tes:

potassium salt of N-tris-(hydroxymethyl)-methyl-2-amino-ethane-sulfonic-acid

T a :

ambient temperatures

U:

units of enzyme activity (μmol min at 25° C

References

  • Ashwell M, Jennings G, Richard D, Stirling DM, Trayhurn P (1983) Effect of acclimation temperature on the concentration of the mitochondrial uncoupling protein measured by radioimmunoassay in mouse brown adipose tissue. FEBS Lett 161:108–112

    Article  CAS  PubMed  Google Scholar 

  • Böckler H, Steinlechner S, Heldmaier G (1982) Complete cold substitution of noradrenaline-induced thermogenesis in the Djungarian hamster,Phodopus sungorus. Experientia 38:261–262

    Article  PubMed  Google Scholar 

  • Figala J, Hoffmann K, Goldau G (1973) Zur Jahresperiodik beim Dsungarischen ZwerghamsterPhodopus sungorus PALLAS. Oecologia 12:89–118

    Article  Google Scholar 

  • Foster DO, Frydman ML (1978) Nonshivering thermogenesis in the rat. II. Measurements of blood flow with microspheres point to brown adipose tissue as the dominant site of the calorigenesis induced by noradrenaline. Can J Physiol 56:110–122

    CAS  Google Scholar 

  • Heldmaier G (1971) Zitterfreie Wärmebildung und Körpergröße bei Säugetieren. Z Vergl Physiol 73:222–248

    Article  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 156:237–245

    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, Seidl K (1985) Plasma free fatty acid levels during cold-induced and noradrenaline-induced nonshivering thermogenesis in the Djungarian hamster. J Comp Physiol 155:679–684

    CAS  Google Scholar 

  • Heldmaier G, Steinlechner S, Rafael J, Vsiansky P (1981) Photoperiodic control and effects of melatonin on nonshivering thermogenesis and brown adipose tissue. Science 212:917–919

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Heldmaier G, Steinlechner S, Rafael J, Latteier B (1982b) Photoperiod and ambient temperature as environmental cues for seasonal thermogenic adaptation in the Djungarian hamster,Phodopus sungorus. Int J Biometeor 26:339–345

    Article  CAS  Google Scholar 

  • Heldmaier G, Böckler H, Buchberger A, Lynch GR, Puchalski W, Steinlechner S, Wiesinger H (1985) Seasonal acclimation and thermogenesis. In: Gilles R (ed) Circulation, respiration and metabolism. Springer, Berlin Heidelberg New York, pp 490–501

    Google Scholar 

  • Heldmaier G, Böckler H, Buchberger A, Klaus S, Puchalski W, Steinlechner S, Wiesinger H (1986) Seasonal variation of thermogenesis. In: Heller HC, Mussachia XJ, Wang LCH (eds) Living in the cold: physiological and biochemical adaptations. Elsevier, Amsterdam New York, pp 361–372

    Google Scholar 

  • Himms-Hagen J (1986) Brown adipose tissue and cold-acclimation. In: Trayhurn P, Nicholls DG (eds) Brown adipose tissue. Arnold, London Melbourne, pp 867–104

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Lynch GR, White SE, Grundel R, Berger MS (1978) Effects of photoperiod, melatonin administration and thyroid block on spontaneous daily torpor and temperature regulation in the white-footed mouse,Peromyscus leucopus. J Comp Physiol 125:157–163

    CAS  Google Scholar 

  • Nedergaard J, Cannon B (1984) Thermogenic mitochondria. In: Ernster L (ed) Bioenergetics. Elsevier, Amsterdam New York, pp 291–314

    Google Scholar 

  • Nicholls DG (1977) The effective proton conductance of the inner membrane of mitochondria from brown adipose tissue. Dependency on proton electrochemical potential gradient. Eur J Biochem 77:349–356

    Article  CAS  PubMed  Google Scholar 

  • Nicholls DG (1982) Bioenergetics. An introduction to the chemiosmotic theory. Academic Press, New York London

    Google Scholar 

  • Nicholls DG, Locke RM (1984) Thermogenic mechanisms in brown fat. Physiol Rev 64:1–64

    CAS  PubMed  Google Scholar 

  • Nicholls DG, Cunningham SA, Rial E (1986) The bioenergetic mechanisms of brown adipose tissue mitochondria. In: Trayhurn P, Nicholls DG (eds) Brown adipose tissue. Arnold, London Melbourne, pp 86–104

    Google Scholar 

  • Puchalski W, Böckler 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 

  • Rafael J (1983) Cytochrome c oxidase. In: Bergmeyer HU (ed) Methods of enzymatic analysis, vol 3. Verlag Chemie, Weinheim, pp 266–273

    Google Scholar 

  • Rafael J, Vsiansky P (1985) Photoperiodic control of the thermogenic capacity in brown adipose tissue of the Djungarian hamster. J Therm Biol 10:167–170

    Article  CAS  Google Scholar 

  • Rafael J, Vsiansly P, Heldmaier G (1985a) Seasonal adaptation of brown adipose tissue in the Djungarian hamster. J Comp Physiol 155:521–528

    CAS  Google Scholar 

  • Rafael J, Vsiansky P, Heldmaier G (1985b) Increased contribution of brown adipose tissue to nonshivering thermogenesis in the Djungarian hamster during cold-adaptation. J Comp Physiol 155:717–722

    CAS  Google Scholar 

  • Rial E, Nicholls DG (1983) The regulation of the proton conductance of brown fat mitochondria. Identification of functional and nonfunctional nucleotide-binding sites. FEBS Lett 161:282–288

    Article  Google Scholar 

  • Rial E, Nicholls DG (1984) The mitochondrial uncoupling protein from guinea-pig brown adipose tissue. Synchronous increase in structural and functional parameters during cold-adaptation. Biochem J 222:685–693

    CAS  PubMed  Google Scholar 

  • Riequier D, Bouillaud F (1986) The brown adipose tissue mitochondrial uncoupling protein. In: Trayhurn P, Nicholls DG (eds) Brown adipose tissue. Arnold, London Melbourne, pp 86–104

    Google Scholar 

  • Rothwell NJ, Stock MJ (1980) Similarities between cold- and diet-induced thermogenesis in the rat. Can J Physiol Pharmacol 58:842–848

    Google Scholar 

  • Rothwell NJ, Stock MJ (1986) Brown adipose tissue and diet-induced thermogenesis. In: Trayhurn P, Nicholls DG (eds) Brown adipose tissue. Arnold, London Melbourne, pp 269–298

    Google Scholar 

  • Smith RE, Horwitz BA (1969) Brown fat and thermogenesis. Physiol Rev 49:330–425

    CAS  PubMed  Google Scholar 

  • Steinlechner S, Heldmaier G, Becker H (1983) The seasonal cycle of body weight in the Djungarian hamster: photoperiodic control and the influence of starvation and melatonin. Oecologia 60:401–405

    Article  Google Scholar 

  • Sundin U (1981) GDP binding to rat brown fat mitochondria: effects of thyroxine at different ambient temperatures. Am J Physiol 241:C134–C139

    CAS  PubMed  Google Scholar 

  • Trayhurn P (1980) Fatty acid synthesis in brown adipose tissue in relation the whole body synthesis in the cold-acclimated golden hamster (Mesocricetus auratus). Biochim Biophys Acta 620:10–17

    CAS  PubMed  Google Scholar 

  • Trayhurn P, Richard D, Jennings G, Ashwell M (1983) Adaptive changes in the concentration of the mitochondrial uncoupling protein in brown adipose tissue of hamsters acclimated at different temperatures. Biosci Rep 3:1077–1984

    Article  CAS  PubMed  Google Scholar 

  • Trayhurn P, Ashwell M, Jennings G, Richard D, Stirling DM (1987) Effect of warm or cold exposure on GDP binding and uncoupling protein in rat brown fat. Am J Physiol 252:E237–243

    CAS  PubMed  Google Scholar 

  • Weiner J (1987) Maximum energy assimilation rates in the Djungarian hamster (Phodopus sungorus). Oecologia 72:297–302

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wiesinger, H., Heldmaier, G. & Buchberger, A. Effect of photoperiod and acclimation temperature on nonshivering thermogenesis and GDP-binding of brown fat mitochondria in the Djungarian hamsterPhodopus s. sungorus . Pflugers Arch. 413, 667 (1989). https://doi.org/10.1007/BF00581818

Download citation

  • Received:

  • Revised:

  • Accepted:

  • DOI: https://doi.org/10.1007/BF00581818

Key words

Navigation