Adjustments of Mitochondrial Energy Transduction in Response to Physiological and Environmental Challenge

Chapter

Abstract

The energy metabolism of animals is shaped by the ecological niche and requires adaptation and acclimatisation to physiological and environmental challenge. These adjustments are complex at different systemic levels and involve regulation of ATP homeostasis at the cellular level. Mitochondria are central to the conversion of nutrient to cellular energy (ATP). Mitochondrial ATP production is not fully efficient, flexible and allows a certain degree of plasticity for physiological adjustments. As a result of an inefficient energy transduction, by-products such as mitochondrial reactive oxygen species and heat are formed. Thus, a quantifiable knowledge on mitochondrial efficiency is required to understand the significance of mitochondrial adjustments for the biology and fitness of the animal. This chapter serves as a general introduction on the principles of mitochondrial energy transduction and efficiency, how to measure mitochondrial energy transduction in isolated mitochondria, reviews past efforts to elucidate adjustments of mitochondrial mechanisms and suggests future perspectives of mitochondrial bioenergetics in integrative and comparative physiology. In particular novel technologies, such as non-invasive measurement of oxygen consumption and membrane potential with fluorescent probes, allow the assessment of energy transduction in the living cell, therefore becoming the next stage to study mitochondrial energy metabolism.

Keywords

Mitochondrial Membrane Potential Brown Adipose Tissue Mitochondrial Reactive Oxygen Species Energy Transduction Cane Toad 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Affourtit C, Jastroch M, Brand MD (2011) Uncoupling protein-2 attenuates glucose-stimulated insulin secretion in INS-1E insulinoma cells by lowering mitochondrial reactive oxygen species. Free Rad Biol Med 50:609–616PubMedCrossRefGoogle Scholar
  2. Akerman KE, Wikström MK (1976) Safranine as a probe of the mitochondrial membrane potential. FEBS Lett 68(2):191–197PubMedCrossRefGoogle Scholar
  3. Birket MJ, Orr AL, Gerencser AA, Madden DT, Vitelli C, Swistowski A, Brand MD, Zeng X (2011) A reduction in ATP demand and mitochondrial activity with neural differentiation of human embryonic stem cells. J Cell Sci 124(Pt 3):348–358PubMedCrossRefGoogle Scholar
  4. Boutilier RG, St-Pierre J (2002) Adaptive plasticity of skeletal muscle energetics in hibernating frogs: mitochondrial proton leak during metabolic depression. J Exp Biol 205(Pt 15):2287–2296PubMedGoogle Scholar
  5. Brand MD (1995) Measurement of mitochondrial protonmotive force. In: Brown GC, Cooper CE (eds) Bioenergetics: a practical approach. Oxford University Press, Oxford, pp 39–62Google Scholar
  6. Brand MD (2010) The sites and topology of mitochondrial superoxide production. Exp Gerontol 45(7–8):466–472PubMedCrossRefGoogle Scholar
  7. Brand MD, Pakay JL, Ocloo A, Kokoszka J, Wallace DC, Brookes PS, Cornwall EJ (2005) The basal proton conductance of mitochondria depends on adenine nucleotide translocase content. Biochem J 392(Pt 2):353–362Google Scholar
  8. Brookes PS, Buckingham JA, Tenreiro AM, Hulbert AJ, Brand MD (1998) The proton permeability of the inner membrane of liver mitochondria from ectothermic and endothermic vertebrates and from obese rats: correlations with standard metabolic rate and phospholipid fatty acid composition. Comp Biochem Physiol B Biochem Mol Biol 119(2):325–334PubMedCrossRefGoogle Scholar
  9. Chance B, Williams GR (1955) Respiratory enzymes in oxidative phosphorylation. III. The steady state. J Biol Chem 217:409–427PubMedGoogle Scholar
  10. Estabrook R (1967) Mitochondrial respiratory control and the polarographic measurement of ADP:O ratios. Methods Enzymol 10:41–47CrossRefGoogle Scholar
  11. Jastroch M, Buckingham JA, Helwig M, Klingenspor M, Brand MD (2007) Functional characterisation of UCP1 in the common carp: uncoupling activity in liver mitochondria and cold-induced expression in the brain. J Comp Physiol B 177(7):743–752PubMedCrossRefGoogle Scholar
  12. 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(2):161–169PubMedGoogle Scholar
  13. Jastroch M, Withers KW, Stoehr S, Klingenspor M (2009) Mitochondrial proton conductance in skeletal muscle of a cold-exposed marsupial, Antechinus flavipes, is unlikely to be involved in adaptive nonshivering thermogenesis but displays increased sensitivity toward carbon-centered radicals. Physiol Biochem Zool 82(5):447–454PubMedCrossRefGoogle Scholar
  14. Jastroch M, Divakaruni AS, Mookerjee S, Treberg JR, Brand MD (2010) Mitochondrial proton and electron leaks. Essays Biochem 47:53–56PubMedCrossRefGoogle Scholar
  15. Keipert S, Klaus S, Heldmaier G, Jastroch M (2010) UCP1 ectopically expressed in murine muscle displays native function and mitigates mitochondrial superoxide production. Biochim Biophys Acta 1797:324–330PubMedCrossRefGoogle Scholar
  16. Kuznetsov AV, Veksler V, Gellerich FN, Saks V, Margreiter R, Kunz WS (2008) Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells. Nat Protoc 3:965–976PubMedCrossRefGoogle Scholar
  17. Marcinek DJ, Schenkman KA, Ciesielski WA, Conley KE (2004) Mitochondrial coupling in vivo in mouse skeletal muscle. Am J Physiol Cell Physiol 286:C457–C463PubMedCrossRefGoogle Scholar
  18. Martin SL, Maniero GD, Carey C, Hand SC (1999) Reversible depression of oxygen consumption in isolated liver mitochondria during hibernation. Physiol Biochem Zool 72:255–264PubMedCrossRefGoogle Scholar
  19. Mzilikazi N, Jastroch M, Meyer CW, Klingenspor M (2007) The molecular and biochemical basis of nonshivering thermogenesis in an African endemic mammal, Elephantulus myurus. Am J Physiol Regul Integr Comp Physiol 293(5):R2120–R2127PubMedCrossRefGoogle Scholar
  20. Nicholls DG (2006) Simultaneous monitoring of ionophore- and inhibitor-mediated plasma and mitochondrial membrane potential changes in cultured neurons. J Biol Chem 281(21):14864–14874PubMedCrossRefGoogle Scholar
  21. Nicholls DG, Ferguson SJ (2002) Bioenergetics 3. Academic Press, London, p 287Google Scholar
  22. Nicholls DG, Locke RM (1984) Thermogenic mechanisms in brown fat. Physiol Rev 64(1):1–64PubMedGoogle Scholar
  23. Nicholls DG, Darley-Usmar VM, Wu M, Jensen PB, Rogers GW, Ferrick DA (2010) Bioenergetic profile experiment using C2C12 myoblast cells. J Vis Exp (46), pii: 2511. doi: 10.3791/2511
  24. 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 285(29):21961–21968PubMedCrossRefGoogle Scholar
  25. Polymeropoulos ET, Heldmaier G, Frappell PB, McAllan BM, Withers KW, Klingenspor M, White CR, Jastroch M (2011a) Phylogenetic differences of mammalian basal metabolic rate are not explained by mitochondrial basal proton leak. Proc Biol Sci. doi: 10.1098/rspb.2011.0881
  26. Polymeropoulos ET, Jastroch M, Frappell PB (2011b) Absence of adaptive nonshivering thermogenesis in a marsupial, the fat-tailed dunnart (Sminthopsis crassicaudata). J Comp Physiol B. doi: 10.1007/s00360-011-0623-x
  27. Porter RK, Brand MD (1993) Body mass dependence of H+ leak in mitochondria and its relevance to metabolic rate. Nature 362(6421):628–630PubMedCrossRefGoogle Scholar
  28. Trzcionka M, Withers KW, Klingenspor M, Jastroch M (2008) The effects of fasting and cold exposure on metabolic rate and mitochondrial proton leak in liver and skeletal muscle of an amphibian, the cane toad Bufo marinus. J Exp Biol 211(Pt 12):1911–1918PubMedCrossRefGoogle Scholar
  29. Wu BJ, Hulbert AJ, Storlien LH, Else PL (2004) Membrane lipids and sodium pumps of cattle and crocodiles: an experimental test of the membrane pacemaker theory of metabolism. Am J Physiol Regul Integr Comp Physiol 287:R633–R641PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.German Research Center for Environmental Health (GmbH), Institute for Diabetes and Obesity, Helmholtz Zentrum MunichMunichGermany

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