Abstract
We calculate, using the first law of thermodynamics, the membrane heat fluxes during active transport of Ca2+ in the Ca2+-ATPase in leaky and intact vesicles, during ATP hydrolysis or synthesis conditions. The results show that the vesicle interior may cool down during hydrolysis and Ca2+-uptake, and heat up during ATP synthesis and Ca2+-efflux. The heat flux varies with the SERCA isoform. Electroneutral processes and rapid equilibration of water were assumed. The results are consistent with the second law of thermodynamics for the overall processes. The expression for the heat flux and experimental data, show that important contributions come from the enthalpy of hydrolysis for the medium in question, and from proton transport between the vesicle interior and exterior. The analysis give quantitative support to earlier proposals that certain, but not all, Ca2+-ATPases, not only act as Ca2+-pumps, but also as heat pumps. It can thus help explain why SERCA 1 type enzymes dominate in tissues where thermal regulation is important, while SERCA 2 type enzymes, with their lower activity and better ability to use the energy from the reaction to pump ions, dominate in tissues where this is not an issue.
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Notes
In an earlier article, Kjelstrup et al. (2005) related the calorimetric heat production, −J cal q erroneously to the system’s entropy production.
References
Alberty RA (2003) Thermodynamics of the hydrolysis of adenosine triphosphate as a function of temperature, pH, pMg, and ionic strength. J Phys Chem B 107:12324–12330
Arruda AP, da Silva W, Carvalho D, de Meis L (2003) Hyperthyroidism increases the uncoupled ATPase activity and heat production by the sarcoplasmic reticulum Ca2+-ATPase. Biochem J 372:375–753
Barata H, de Meis L (2002) Uncoupled ATP hydrolysis and thermogenetic activity of the sarcoplasmic reticulum Ca2+-ATPase. J Biol Chem 277:16868–16872
Bianconi ML (2003) Calorimetric determination of thermodynamic parameters of reaction reveals different enthalpic compensations of the yeast hexokinese isozymes. J Biol Chem 278:18709–18713
Caplan SR, Essig A (1983) Bioenergtics and linear non-equilibrium thermodynamics—the steady state. Harvard University Press, Cambridge
Dalton KA, Pilot JP, Mall S, East JM, Lee AG (1999) Anionic phospholipid decrease the rate of slippage on the Ca2+-ATPase of sacroplasmic reticulum. Biochem J 324:431–438
de Meis L, Martins OB, Alves EW (1980) Role of water on the synthesis of adenosine triphosphate by the sarcoplasmic reticulum adenosine triphosphate in the absence of a calcium ion gradient. Biochemistry 10:4252–4261
de Meis L, Inesi G (1982) ATP synthesis by sarcoplasmic reticulum ATPase following Ca2+, pH, temperature, and water activity jumps. J Biol Chem 257:1289–1294
de Meis L, Bianconi ML, Suzano VA (1997) Control of energy fluxes by the sarcoplasmic reticulum Ca2+-ATPase: ATP hydrolysis, ATP synthesis and heat production. FEBS Lett 406:201–204
de Meis L (2001) Uncoupled ATPase activity and heat production by the sarcoplasmic reticulum Ca2+-ATPase. J Biol Chem 276:25078–25087
de Meis L (2002) Ca2+-ATPases (SERCA): energy transduction and heat production in transport ATPases. Membrane Biol 188:1–9
de Meis L (2003) Brown adipose tissue Ca2+-ATPase. J Biol Chem 278:41856–41861
de Meis L, Oliveira GM, Arruda AP, Santos R, MAdeiro da Costa R, Benchimol M (2005) The thermogenic activity of rat brown adipose tissue and rabbit whilte muscle Ca2+-ATPase. Life 57:337–345
Fibich A, Janko K, Apell HJ (2007) Kinetics of proton binding to sarcoplasmic reticulum Ca-ATPase in the E1 state. Biophys J 93:3092–3104
Hauser K and Barth A (2007) Side-chain protonation and mobility in the sarcoplasmic reticulum Ca2+-ATPase: implications for proton countertransport and Ca2+ release. Biophys J 93:3259–3270
Honig JM (1995) Thermodynamics, 2nd edn. Academic Press, San Diego
Karjalainen EL, Hauser K, Barth A (2007) Proton paths in the sarcoplasmic reticulum Ca2+-ATPAse. Biochim et Biophys Acta 1767:1310–1318
Kjelstrup S, Rubi JM, Bedeaux D (2005) Energy dissipation in slipping biological pumps. Phys Chem Chem Phys 7:4009–4019
Mall S, Broadbridge R, Harrison SL, Gore MG, Lee AG, East JM (2006) The presence of sarcolipin results in increased heat production by Ca2+-ATPase. J Biol Chem 281:36597–36602
Møller JV, Juul B, le Maire M (1996) Structural organization, ion transport and energy transduction of P-type ATPases. Biochim Biophys Acta 1286:1–51
Nicholls D (1982) Bioenergtics, an introduction to chemiosmotic theory. Academic Press, London, pp 48–51
Obara K, Miyashita N, Xu C, Toyashima I, Sugita Y, Inesi G, Toyoshima C (2005) Structural role of countertransport revealed in Ca2+ pump crystal structure in the absence of Ca2+. Proc Natl Acad Sci USA 102(41):14489–14496
Olesen C, Picard M, Winther AML, Gyrup C, Morth JP, Oxvig C, Møller JV, Nissen P (2007) The structural basis of calcium transport by the calcium pump. Nature 450:1036–1042
Tinoco I, Jr, Sauer K, Wang J (1995) Physical chemistry. Principles and applications in biological sciences, 3rd edn. Prentice Hall, Englewood Cliffs, pp 29–31
Sandler S (2006) Chemical, biochemical and engineering thermodynamics, 4th edn. Wiley, New York
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The authors are grateful for support from Centre of Advanced Studies at the Norwegian Academy of Science and Letters, Oslo.
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Signe Kjelstrup and Dick Bedeaux on leave from Department of Chemistry, Norwegian University of Science and Technology, NO-7491, Trondheim, Norway. Jean-Marc Simon on leave from Institut Carnot de Bourgogne, UMR 5209 CNRS-Université de Bourgogne, F-21078, Dijon Cedex, France.
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Kjelstrup, S., de Meis, L., Bedeaux, D. et al. Is the Ca2+-ATPase from sarcoplasmic reticulum also a heat pump?. Eur Biophys J 38, 59–67 (2008). https://doi.org/10.1007/s00249-008-0358-0
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DOI: https://doi.org/10.1007/s00249-008-0358-0