Role of the sarcoplasmic reticulum Ca2+-ATPase on heat production and thermogenesis.

The sarcoplasmic reticulum of skeletal muscle retains a membrane bound Ca2+-ATPase which is able to interconvert different forms of energy. A part of the chemical energy released during ATP hydrolysis is converted into heat and in the bibliography it is assumed that the amount of heat produced during the hydrolysis of an ATP molecule is always the same, as if the energy released during ATP cleavage were divided in two non-interchangeable parts: one would be converted into heat, and the other used for Ca2+ transport. Data obtained in our laboratory during the past three years indicate that the amount of heat released during the hydrolysis of ATP may vary between 7 and 32 kcal/mol depending on whether or not a transmembrane Ca2+ gradient is formed across the sarcoplasmic reticulum membrane. Drugs such as heparin and dimethyl sulfoxide are able to modify the fraction of the chemical energy released during ATP hydrolysis which is used for Ca2+ transport and the fraction which is dissipated in the surrounding medium as heat.

[1]  P. Even,et al.  Ca(2+)‐dependent heat production under basal and near‐basal conditions in the mouse soleus muscle. , 1992, The Journal of physiology.

[2]  G. Shull,et al.  Functional comparisons between isoforms of the sarcoplasmic or endoplasmic reticulum family of calcium pumps. , 1992, The Journal of biological chemistry.

[3]  L. de Meis,et al.  Modulation by fatty acids of Ca2+ fluxes in sarcoplasmic-reticulum vesicles. , 1993, The Biochemical journal.

[4]  A. Bianco,et al.  Optimal response of key enzymes and uncoupling protein to cold in BAT depends on local T3 generation. , 1987, The American journal of physiology.

[5]  L. de Meis,et al.  ATP reversible Pi exchange and membrane phosphorylation in sarcoplasmic reticulum vesicles: activation by silver in the absence of a Ca2+ concentration gradient. , 1975, Biochemistry.

[6]  A. Galina,et al.  Ca2+ translocation and catalytic activity of the sarcoplasmic reticulum ATPase. Modulation by ATP, Ca2+, and Pi. , 1991, The Journal of biological chemistry.

[7]  W. Hasselbach,et al.  ATP synthesis by the reverse of the sarcoplasmic calcium pump , 1971, FEBS letters.

[8]  A M Prentice,et al.  Metabolic response to experimental overfeeding in lean and overweight healthy volunteers. , 1992, The American journal of clinical nutrition.

[9]  R. Wiesner,et al.  Biogenesis of thermogenic mitochondria in brown adipose tissue of Djungarian hamsters during cold adaptation. , 1996, The Biochemical journal.

[10]  D. Souza,et al.  Alteration of Ca2+ Fluxes in Brain Microsomes by K+ and Na+: Modulation by Sulfated Polysaccharides and Trifluoperazine , 1996, Journal of neurochemistry.

[11]  E. A. Sims,et al.  Expenditure and storage of energy in man. , 1987, The Journal of clinical investigation.

[12]  L. de Meis,et al.  Control of energy fluxes by the sarcoplasmic reticulum Ca2+‐ATPase: ATP hydrolysis, ATP synthesis and heat production , 1997, FEBS letters.

[13]  A Tremblay,et al.  The response to long-term overfeeding in identical twins. , 1990, The New England journal of medicine.

[14]  L. Dode,et al.  A sarco/endoplasmic reticulum Ca(2+)-ATPase 3-type Ca2+ pump is expressed in platelets, in lymphoid cells, and in mast cells. , 1994, The Journal of biological chemistry.

[15]  P. Boyer,et al.  A new concept for energy coupling in oxidative phosphorylation based on a molecular explanation of the oxygen exchange reactions. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[16]  L. DeMeis,et al.  Role of the Ca2+ concentration gradient in the adenosine 5'-triphosphate-inorganic phosphate exchange catalyzed by sarcoplasmic reticulum. , 1974 .

[17]  M. Fortea,et al.  Insight into the Uncoupling Mechanism of Sarcoplasmic Reticulum ATPase Using the Phosphorylating Substrate UTP* , 2000, The Journal of Biological Chemistry.

[18]  P. Bijlenga,et al.  Uncoupling Protein-3 Expression in Rodent Skeletal Muscle Is Modulated by Food Intake but Not by Changes in Environmental Temperature* , 1998, The Journal of Biological Chemistry.

[19]  L. Meis.  [13] Approaches to studying the mechanism of ATP synthesis in sarcoplasmic reticulum , 1988 .

[20]  H. Masuda,et al.  Phosphorylation of the sarcoplasmic reticulum membrane by orthophosphate. Inhibition by calcium ions. , 1973, Biochemistry.

[21]  G. Inesi,et al.  Variable Stoichiometric Efficiency of Ca2+ and Sr2+ Transport by the Sarcoplasmic Reticulum ATPase (*) , 1995, The Journal of Biological Chemistry.

[22]  L. de Meis,et al.  Functional interactions of catalytic site and transmembrane channel in the sarcoplasmic reticulum ATPase. , 1990, The Journal of biological chemistry.

[23]  L. de Meis,et al.  Intrinsic regulation of substrate fluxes and energy conservation in Ca2+‐ATPase , 1985, FEBS letters.

[24]  G Inesi,et al.  Regulation of steady state filling in sarcoplasmic reticulum. Roles of back-inhibition, leakage, and slippage of the calcium pump. , 1989, The Journal of biological chemistry.

[25]  L. de Meis,et al.  CHARACTERIZATION OF CALCIUM OXALATE AND CALCIUM PHOSPHATE DEPOSITS IN SARCOPLASMIC RETICULUM VESICLES , 1974, The Journal of cell biology.

[26]  M. Reitman,et al.  Uncoupling Protein-3 Is a Mediator of Thermogenesis Regulated by Thyroid Hormone, β3-Adrenergic Agonists, and Leptin* , 1997, The Journal of Biological Chemistry.

[27]  S. Engelender,et al.  Reaction Mechanism of the Sarcoplasmic Reticulum Ca2+-ATPase , 1997 .

[28]  L. Meis.  Control of heat production by the Ca2+-ATPase of rabbit and trout sarcoplasmic reticulum , 1998 .

[29]  W. Hasselbach,et al.  Activation of calcium efflux by ADP and inorganic phosphate , 1971, FEBS letters.

[30]  W. Dalton Dietrich,et al.  Small Differences in Intraischemic Brain Temperature Critically Determine the Extent of Ischemic Neuronal Injury , 1987, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[31]  L. Meis.  Fast efflux of Ca2+ mediated by the sarcoplasmic reticulum Ca2(+)-ATPase. , 1991 .

[32]  E. Dumonteil,et al.  Sarcoplasmic reticulum Ca(2+)-ATPase and ryanodine receptor in cold-acclimated ducklings and thermogenesis. , 1993, The American journal of physiology.

[33]  R. Goldberg,et al.  Thermodynamics of the hydrolysis of adenosine 5'-triphosphate to adenosine 5'-diphosphate. , 1986, The Journal of biological chemistry.

[34]  J. Levine,et al.  Role of nonexercise activity thermogenesis in resistance to fat gain in humans. , 1999, Science.

[35]  L. de Meis,et al.  On a possible mechanism of energy conservation in sarcoplasmic reticulum membrane. , 1976, The Journal of biological chemistry.

[36]  V. Skulachev.  Uncoupling: new approaches to an old problem of bioenergetics. , 1998, Biochimica et biophysica acta.

[37]  C. Tanford.  Twenty questions concerning the reaction cycle of the sarcoplasmic reticulum calcium pump. , 1984, CRC critical reviews in biochemistry.

[38]  B. Block,et al.  Thermogenesis in muscle. , 1994, Annual review of physiology.

[39]  O. Boss,et al.  The uncoupling proteins, a review. , 1998, European journal of endocrinology.

[40]  L. Janský.  Humoral thermogenesis and its role in maintaining energy balance. , 1995, Physiological reviews.

[41]  P. Larsen,et al.  Characterization of the Promoter of the Rat Sarcoplasmic Endoplasmic Reticulum Ca2+-ATPase 1 Gene and Analysis of Thyroid Hormone Responsiveness* , 1996, The Journal of Biological Chemistry.

[42]  L. de Meis,et al.  Ca2+ Release and Heat Production by the Endoplasmic Reticulum Ca2+-ATPase of Blood Platelets , 1999, The Journal of Biological Chemistry.

[43]  H. Masuda,et al.  Phosphorylation of the sarcoplasmic reticulum membrane by orthophosphate through two different reactions. , 1974, Biochemistry.

[44]  C. J. Gordon,et al.  Temperature regulation in laboratory mammals following acute toxic insult. , 1988, Toxicology.

[45]  C. van Hardeveld,et al.  Significance of cation transport in control of energy metabolism and thermogenesis. , 1991, Physiological reviews.

[46]  W. Hasselbach.  The reversibility of the sarcoplasmic calcium pump. , 1978, Biochimica et biophysica acta.

[47]  L. DeMeis.  The concept of energy-rich phosphate compounds: water, transport ATPases, and entropic energy. , 1993 .

[48]  N. Green,et al.  Amino-acid sequence of a Ca2+ + Mg2+ -dependent ATPase from rabbit muscle sarcoplasmic reticulum, deduced from its complementary DNA sequence , 1985, Nature.

[49]  L. Meis.  Uncoupled ATPase activity and heat production by the sarcoplasmic reticulum Ca2+-ATPase. Regulation by ADP. , 2001 .

[50]  A. S. Blix,et al.  Rapid brain cooling in diving ducks. , 1998, American journal of physiology. Regulatory, integrative and comparative physiology.

[51]  E. Dumonteil,et al.  Expression of sarcoplasmic reticulum Ca2+ transport proteins in cold-acclimating ducklings. , 1995, The American journal of physiology.

[52]  L. Meis.  Control of Heat Produced during ATP Hydrolysis by the Sarcoplasmic Reticulum Ca2+-ATPase in the Absence of A Ca2+Gradient , 1998 .

[53]  L. Meis.  Role of water in the energy of hydrolysis of phosphate compounds — energy transduction in biological membranes , 1989 .

[54]  Y. Sagara,et al.  Characterization of the inhibition of intracellular Ca2+ transport ATPases by thapsigargin. , 1992, The Journal of biological chemistry.

[55]  Herman Wolosker,et al.  Ligand-gated channel of the sarcoplasmic reticulum Ca2+ transport ATPase , 1995, Bioscience reports.

[56]  D. Nicholls,et al.  Thermogenic mechanisms in brown fat. , 1984, Physiological reviews.

[57]  L. Meis.  The sarcoplasmic reticulum: Transport and energy transduction , 1981 .

[58]  R. Tume,et al.  A new mechanism by which an H+ concentration gradient drives the synthesis of adenosine triphosphate, pH jump, and adenosine triphosphate synthesis by the Ca2+-dependnet adenosine triphosphatase of sarcoplasmic reticulum. , 1977, Biochemistry.

[59]  L. Meis.  ATP Synthesis and Heat Production during Ca2+ Efflux by Sarcoplasmic Reticulum Ca2+-ATPase , 2000 .

[60]  G. Elzinga,et al.  Heat produced by rabbit papillary muscle during anoxia and reoxygenation. , 1993, Circulation research.

[61]  L. de Meis,et al.  Uncoupling of muscle and blood platelets Ca2+ transport ATPases by heparin. Regulation by K+. , 1994, The Journal of biological chemistry.

[62]  G. Gould,et al.  A fast passive Ca2+ efflux mediated by the (Ca2+ + Mg2+)-ATPase in reconstituted vesicles. , 1987, Biochimica et biophysica acta.

[63]  O. Thastrup,et al.  The calcium mobilizing tumor promoting agent, thapsigargin elevates the platelet cytoplasmic free calcium concentration to a higher steady state level. A possible mechanism of action for the tumor promotion. , 1987, Biochemical and biophysical research communications.

[64]  L. DeMeis,et al.  Role of water, hydrogen ion, and temperature on the synthesis of adenosine triphosphate by the sarcoplasmic reticulum adenosine triphosphatase in the absence of a calcium ion gradient. , 1980 .

[65]  J. Lytton,et al.  Molecular cloning of cDNAs from human kidney coding for two alternatively spliced products of the cardiac Ca2+-ATPase gene. , 1988, The Journal of biological chemistry.

[66]  L. de Meis,et al.  Functional evidence of a transmembrane channel within the Ca2+ transport ATPase of sarcoplasmic reticulum , 1992, FEBS Letters.