[Ca2+] oscillations in a model of energy-dependent Ca2+ uptake by the endoplasmic reticulum.

Active Ca2+ transport in living cells necessitates controlled supply of metabolic energy. Direct coupling between sarco/endoplasmic reticulum (ER) Ca2+ ATPases (SERCA) and intracellular energy-generation sites has been well established experimentally. On the basis of these experimental findings we propose a pump-driven model to investigate complex dynamic properties of a cell system. The model describes the pump process both by the Ca2+ ATPase itself and by a suitable description of the glycolysis. The associated set of differential equations shows a rich behavior, the solutions ranging from simple periodic oscillations to complex patterns such as bursting and spiking. Recent experimental results on calcium oscillations in Xenopus laevis oocytes and on dynamic patterns of intracellular Ca2+ concentrations in electrically non-excitable cells are well described by corresponding theoretical results derived within the proposed model. The simulation results are further compared to spontaneous [Ca2+] oscillations in primitive endodermal cells.

[1]  L. de Meis,et al.  Glucose 6‐Phosphate and Fructose 1,6‐Bisphosphate Can Be Used as ATP‐Regenerating Systems by Cerebellum Ca2+‐Transport ATPase , 1999, Journal of neurochemistry.

[2]  L. Raeymaekers,et al.  Preferential support of Ca2+ uptake in smooth muscle plasma membrane vesicles by an endogenous glycolytic cascade , 1989, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[3]  D. Yule,et al.  Oscillations of cytosolic calcium in single pancreatic acinar cells stimulated by acetylcholine , 1988, FEBS letters.

[4]  A. Marks.  Intracellular calcium-release channels: regulators of cell life and death. , 1997, The American journal of physiology.

[5]  J. L. Hudson,et al.  Impact of mitochondrial Ca2+ cycling on pattern formation and stability. , 1999, Biophysical journal.

[6]  J. Weiss,et al.  The cytoplasm: no longer a well-mixed bag. , 2001, Circulation research.

[7]  K. Mikoshiba.  The InsP3 receptor and intracellular Ca2+ signaling , 1997, Current Opinion in Neurobiology.

[8]  A. Katz,et al.  Calcium transport ATPase of canine cardiac sarcoplasmic reticulum. A comparison with that of rabbit fast skeletal muscle sarcoplasmic reticulum. , 1976, The Journal of biological chemistry.

[9]  R. Gillies,et al.  Modulation of intracellular Ca2+ by glucose in MDCK cells: role of endoplasmic reticulum Ca(2+)-ATPase. , 1995, The American journal of physiology.

[10]  Peter Lipp,et al.  Calcium - a life and death signal , 1998, Nature.

[11]  T. Chay,et al.  Modelling receptor-controlled intracellular calcium oscillators. , 1991, Cell calcium.

[12]  D. Wilkie,et al.  The activity of creatine kinase in frog skeletal muscle studied by saturation-transfer nuclear magnetic resonance. , 1981, The Biochemical journal.

[13]  J. Hescheler,et al.  Spontaneous calcium oscillations in embryonic stem cell-derived primitive endodermal cells. , 1998, Experimental cell research.

[14]  P. Camacho,et al.  Increased frequency of calcium waves in Xenopus laevis oocytes that express a calcium-ATPase. , 1993, Science.

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

[16]  J. Keizer,et al.  A single-pool inositol 1,4,5-trisphosphate-receptor-based model for agonist-stimulated oscillations in Ca2+ concentration. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[17]  L. de Meis,et al.  Comparative data of Ca2+ transport in brain and skeletal muscle microsomes. , 1970, Journal of Biological Chemistry.

[18]  Ernesto Carafoli,et al.  Calcium signaling: A tale for all seasons , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[19]  A Goldbeter,et al.  Properties of intracellular Ca2+ waves generated by a model based on Ca(2+)-induced Ca2+ release. , 1994, Biophysical journal.

[20]  D. Allen,et al.  Characterization of oscillations of intracellular calcium concentration in ferret ventricular muscle. , 1984, The Journal of physiology.

[21]  M. Berridge,et al.  Cytosolic calcium oscillators , 1988, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[22]  S. Orrenius,et al.  Role of Ca2+ in toxic cell killing. , 1989, Trends in pharmacological sciences.

[23]  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.

[24]  U. Krause,et al.  Control of adenine nucleotide metabolism and glycolysis in vertebrate skeletal muscle during exercise , 1996, Experientia.

[25]  J. Keizer,et al.  On the roles of Ca2+ diffusion, Ca2+ buffers, and the endoplasmic reticulum in IP3-induced Ca2+ waves. , 1995, Biophysical journal.

[26]  P. Cobbold,et al.  Agonist-induced oscillations in cytoplasmic free calcium concentration in single rat hepatocytes. , 1987, Cell calcium.

[27]  H. Igarashi,et al.  Aging‐related changes in calcium oscillations in fertilized mouse oocytes , 1997, Molecular reproduction and development.

[28]  G. Inesi,et al.  Effect of diethyl ether on the adenosine triphosphatase activity and the calcium uptake of fragmented sarcoplasmic reticulum of rabbit skeletal muscle. , 1967, The Journal of biological chemistry.

[29]  A Goldbeter,et al.  Signal-induced Ca2+ oscillations: properties of a model based on Ca(2+)-induced Ca2+ release. , 1991, Cell calcium.

[30]  R Jacob,et al.  Calcium oscillations in electrically non-excitable cells. , 1990, Biochimica et biophysica acta.

[31]  M. Berman,et al.  Effects of pH, temperature, and calcium concentration on the stoichiometry of the calcium pump of sarcoplasmic reticulum. , 1984, The Journal of biological chemistry.

[32]  B. Ehrlich.  Functional properties of intracellular calcium-release channels , 1995, Current Opinion in Neurobiology.

[33]  L. de Meis,et al.  Pharmacological differentiation between intracellular calcium pump isoforms. , 1996, Molecular pharmacology.

[34]  S. Schrier.  Organization of enzymes in human erythrocyte membranes. , 1966, The American journal of physiology.

[35]  Martin Falcke,et al.  Modeling the dependence of the period of intracellular Ca2+ waves on SERCA expression. , 2003, Biophysical journal.

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

[37]  P. Gray.  Oscillations of free cytosolic calcium evoked by cholinergic and catecholaminergic agonists in rat parotid acinar cells. , 1988, The Journal of physiology.

[38]  M. Berridge,et al.  Localization and heterogeneity of agonist‐induced changes in cytosolic calcium concentration in single bovine adrenal chromaffin cells from video imaging of fura‐2. , 1989, The EMBO journal.

[39]  S. Schuster,et al.  Modelling of simple and complex calcium oscillations , 2002 .

[40]  T. Rink,et al.  Repetitive spikes in cytoplasmic calcium evoked by histamine in human endothelial cells , 1988, Nature.

[41]  G Inesi,et al.  Mechanism of calcium transport. , 1985, Annual review of physiology.

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

[43]  F. Di Virgilio,et al.  Identification, kinetic properties and intracellular localization of the (Ca(2+)-Mg2+)-ATPase from the intracellular stores of chicken cerebellum. , 1991, The Biochemical journal.

[44]  L. Becker,et al.  Functional coupling between glycolysis and sarcoplasmic reticulum Ca2+ transport. , 1995, Circulation research.

[45]  L. Stryer,et al.  Molecular model for receptor-stimulated calcium spiking. , 1988, Proceedings of the National Academy of Sciences of the United States of America.