Modeling the impact of store-operated Ca2+ entry on intracellular Ca2+ oscillations.

Calcium (Ca2+) oscillations play fundamental roles in various cell signaling processes and have been the subject of numerous modeling studies. Here we have implemented a general mathematical model to simulate the impact of store-operated Ca2+ entry on intracellular Ca2+ oscillations. In addition, we have compared two different models of the inositol 1,4,5-trisphosphate (IP3) receptor (IP3R) and their influences on intracellular Ca2+ oscillations. Store-operated Ca2+ entry following Ca2+ depletion of endoplasmic reticulum (ER) is an important component of Ca2+ signaling. We have developed a phenomenological model of store-operated Ca2+ entry via store-operated Ca2+ (SOC) channels, which are activated upon ER Ca2+ depletion. The depletion evokes a bi-phasic Ca2+ signal, which is also produced in our mathematical model. The IP3R is an important regulator of intracellular Ca2+ signals. This IP3 sensitive Ca2+ channel is also regulated by Ca2+. We apply two IP3R models, the Mak-McBride-Foskett model and the De Young and Keizer model, with significantly different channel characteristics. Our results show that the two separate IP3R models evoke intracellular Ca2+ oscillations with different frequencies and amplitudes. Store-operated Ca2+ entry affects the oscillatory behavior of these intracellular Ca2+ oscillations. The IP3 threshold is altered when store-operated Ca2+ entry is excluded from the model. Frequencies and amplitudes of intracellular Ca2+ oscillations are also altered without store-operated Ca2+ entry. Under certain conditions, when intracellular Ca2+ oscillations are absent, excluding store-operated Ca2+ entry induces an oscillatory response. These findings increase knowledge concerning store-operated Ca2+ entry and its impact on intracellular Ca2+ oscillations.

[1]  H. Brismar,et al.  Ouabain, a steroid hormone that signals with slow calcium oscillations , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[2]  M. Berridge,et al.  Capacitative calcium entry. , 1995, The Biochemical journal.

[3]  D. Clapham,et al.  Acceleration of intracellular calcium waves in Xenopus oocytes by calcium influx. , 1993, Science.

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

[5]  Roger Y. Tsien,et al.  Emptying of intracellular Ca2+ stores releases a novel small messenger that stimulates Ca2+ influx , 1993, Nature.

[6]  R. Penner,et al.  Store depletion and calcium influx. , 1997, Physiological reviews.

[7]  J Rinzel,et al.  Sensing and refilling calcium stores in an excitable cell. , 1997, Biophysical journal.

[8]  M. Falcke.  Reading the patterns in living cells —the physics of ca2+ signaling , 2004 .

[9]  K. Venkatachalam,et al.  The cellular and molecular basis of store-operated calcium entry , 2002, Nature Cell Biology.

[10]  J. Putney,et al.  A model for receptor-regulated calcium entry. , 1986, Cell calcium.

[11]  J. Putney,et al.  Store-operated calcium channels. , 2005, Physiological reviews.

[12]  S. Snyder,et al.  Inositol 1,4,5-trisphosphate receptors as signal integrators. , 2004, Annual review of biochemistry.

[13]  L. Loew,et al.  An image-based model of calcium waves in differentiated neuroblastoma cells. , 2000, Biophysical journal.

[14]  W. Stühmer,et al.  Ca2+ oscillations and Ca2+ influx in Xenopus oocytes expressing a novel 5‐hydroxytryptamine receptor. , 1993, The Journal of physiology.

[15]  M. Takahashi,et al.  Functional Properties of the Type-3 InsP3 Receptor in 16HBE14o− Bronchial Mucosal Cells* , 1998, The Journal of Biological Chemistry.

[16]  T. Pozzan,et al.  Role of capacitative calcium entry on glutamate‐induced calcium influx in type‐I rat cortical astrocytes , 2001, Journal of neurochemistry.

[17]  J. Putney,et al.  Activation of calcium entry by the tumor promoter thapsigargin in parotid acinar cells. Evidence that an intracellular calcium pool and not an inositol phosphate regulates calcium fluxes at the plasma membrane. , 1989, The Journal of biological chemistry.

[18]  R. Patterson,et al.  Store-Operated Ca2+ Entry Evidence for a Secretion-like Coupling Model , 1999, Cell.

[19]  M Fill,et al.  Isoform-specific function of single inositol 1,4,5-trisphosphate receptor channels. , 1998, Biophysical journal.

[20]  K. Mikoshiba,et al.  Cell Signaling Microdomain with Na,K-ATPase and Inositol 1,4,5-Trisphosphate Receptor Generates Calcium Oscillations* , 2003, Journal of Biological Chemistry.

[21]  F. Bäckhed,et al.  α-Haemolysin of uropathogenic E. coli induces Ca 2+ oscillations in renal epithelial cells , 2000, Nature.

[22]  Don-On Daniel Mak,et al.  Inositol 1,4,5-tris-phosphate activation of inositol tris-phosphate receptor Ca2+ channel by ligand tuning of Ca2+ inhibition , 1998 .

[23]  Upinder S Bhalla,et al.  Simulations of inositol phosphate metabolism and its interaction with InsP(3)-mediated calcium release. , 2002, Biophysical journal.

[24]  J. Putney,et al.  Mechanisms of capacitative calcium entry. , 2001, Journal of cell science.

[25]  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.

[26]  James Watras,et al.  Bell-shaped calcium-response curves of lns(l,4,5)P3- and calcium-gated channels from endoplasmic reticulum of cerebellum , 1991, Nature.

[27]  A. Parekh,et al.  Ca2+ store dynamics determines the pattern of activation of the store‐operated Ca2+ current ICRAC in response to InsP3 in rat basophilic leukaemia cells , 2000, The Journal of physiology.

[28]  Jeanette Hellgren Kotaleski,et al.  mGluR-Mediated calcium oscillations in the lamprey: a computational model , 2004, Neurocomputing.

[29]  R Heinrich,et al.  Intercellular Ca2+ wave propagation through gap-junctional Ca2+ diffusion: a theoretical study. , 2001, Biophysical journal.

[30]  R. Dolmetsch,et al.  Signaling between intracellular Ca2+ stores and depletion-activated Ca2+ channels generates [Ca2+]i oscillations in T lymphocytes , 1994, The Journal of general physiology.

[31]  Leslie M Loew,et al.  Computational cell biology: spatiotemporal simulation of cellular events. , 2002, Annual review of biophysics and biomolecular structure.

[32]  K. Mikoshiba,et al.  Distinct Roles of Inositol 1,4,5-Trisphosphate Receptor Types 1 and 3 in Ca2+ Signaling* , 2004, Journal of Biological Chemistry.

[33]  Barbara E. Ehrlich,et al.  Type III InsP3 receptor channel stays open in the presence of increased calcium , 1998, Nature.

[34]  Rachel J Errington,et al.  A mathematical model predicts that calreticulin interacts with the endoplasmic reticulum Ca(2+)-ATPase. , 2002, Biophysical journal.

[35]  J. Sneyd,et al.  Models of the inositol trisphosphate receptor. , 2005, Progress in biophysics and molecular biology.

[36]  E Bornberg-Bauer,et al.  Switching from simple to complex oscillations in calcium signaling. , 2000, Biophysical journal.

[37]  A. Goldbeter.  Computational approaches to cellular rhythms , 2002, Nature.

[38]  G. Barritt,et al.  Evidence that Ca2+-release-activated Ca2+ channels in rat hepatocytes are required for the maintenance of hormone-induced Ca2+ oscillations. , 2003, Biochemical Journal.

[39]  R M Nerem,et al.  A mathematical model of cytosolic calcium dynamics in human umbilical vein endothelial cells. , 1996, The American journal of physiology.

[40]  M. Berridge,et al.  Calcium signalling: dynamics, homeostasis and remodelling , 2003, Nature reviews. Molecular cell biology.