Comparison of Models for IP3 Receptor Kinetics Using Stochastic Simulations

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Hituri, Katri ^a   Linne, Marja Leena ^a  

^a TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; CALCIUM; INOSITOL 1,4,5 TRISPHOSPHATE;

ALGORITHM; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; GILLESPIE STOCHASTIC SIMULATION ALGORITHM; MATHEMATICAL COMPUTING; MATHEMATICAL PARAMETERS; MEAN OPEN AND CLOSED TIME; OPEN AND CLOSED TIME DISTRIBUTION; OPEN PROBABILITY; PROCESS DEVELOPMENT; PROCESS MODEL; PROTEIN DETERMINATION; PROTEIN FUNCTION; STEADY STATE; STOCHASTIC MODEL; BIOLOGICAL MODEL; CHANNEL GATING; KINETICS; METABOLISM; PROBABILITY; STATISTICS;

CALCIUM; INOSITOL 1,4,5-TRISPHOSPHATE; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; ION CHANNEL GATING; KINETICS; MODELS, NEUROLOGICAL; PROBABILITY; STOCHASTIC PROCESSES;

EID: 84876060574     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059618     Document Type: Article

References (85)

1. Libersat F, Duch C, (2004) Mechanisms of dendritic maturation. Mol Neurobiol 29: 303-320.
2. Michaelsen K, Lohmann C, (2010) Calcium dynamics at developing synapses: mechanisms and functions. Eur J Neurosci 32: 218-223.
3. Banerjee S, Hasan G, (2005) The InsP3 receptor: its role in neuronal physiology and neurodegeneration. Bioessays 27: 1035-1047.
4. Foskett J, (2010) Inositol trisphosphate receptor Ca2+ release channels in neurological diseases. Pflugers Arch Eur J Physiol 460: 481-494.
5. Bliss T, Collingridge G, (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31-39.
6. Franks KM, Sejnowski TJ, (2002) Complexity of calcium signaling in synaptic spines. BioEssays 24: 1130-1144.
7. Ogasawara H, Doi T, Kawato M, (2008) Systems biology perspectives on cerebellar long-term depression. Neurosignals 16: 300-317.
8. Collingridge G, Peineau S, Howland J, Wang Y, (2010) Long-term depression in the CNS. Nature Rev Neurosci 11: 459-473.
9. Citri A, Malenka R, (2008) Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology 33: 18-41.
10. Sharp A, Nucifora Jr. F, Blondel O, Sheppard C, Zhang C, et al. (1999) Differential cellular expression of isoforms of inositol 1,4,5-triphosphate receptors in neurons and glia in brain. J Comp Neurol 406: 207-220.
11. Ito M, (2002) The molecular organization of cerebellar long-term depression. Nature Rev Neurosci 3: 896-902.
12. Foskett JK, White C, Cheung KH, Mak DOD, (2007) Inositol trisphosphate receptor Ca2+ release channels. Physiol Rev 87: 593-658.
13. Llano I, DiPolo R, Marty A, (1994) Calcium-induced calcium release in cerebellar Purkinje cells. Neuron 12: 663-673.
14. Barbara J, (2002) IP3-dependent calcium-induced calcium release mediates bidirectional calcium waves in neurones: functional implications for synaptic plasticity. Biochim Biophys Acta - Proteins & Proteomics 1600: 12-18.
15. Ehrlich B, Watras J, (1988) Inositol 1,4,5-trisphosphate activates a channel from smooth muscle sarcoplasmic reticulum. Nature 336: 583-586.
16. Bezprozvanny I, Watras J, Ehrlich B, (1991) Bell-shaped calcium-response curves of Ins(1,4,5)P3- and calcium-gated channels from endoplasmic reticulum of cerebellum. Nature 351: 751-754.
17. Watras J, Bezprozvanny I, Ehrlich B, (1991) Inositol 1,4,5-trisphosphate-gated channels in cerebellum: presence of multiple conductance states. J Neurosci 11: 3239.
18. Bezprozvanny I, Ehrlich B, (1994) Inositol (1,4,5)-trisphosphate (InsP3)-gated Ca channels from cerebellum: conduction properties for divalent cations and regulation by intraluminal calcium. J Gen Phys 104: 821-856.
19. Kaftan E, Ehrlich B, Watras J, (1997) Inositol 1,4,5-trisphosphate (InsP3) and calcium interact to increase the dynamic range of InsP3 receptor-dependent calcium signaling. J Gen Physiol 110: 529-538.
20. Moraru I, Kaftan E, Ehrlich B, Watras J, (1999) Regulation of type 1inositol 1,4,5-trisphosphategated calcium channels by InsP3 and calcium. Simulation of single shannel kinetics based on ligand binding and electrophysiological analysis. J Gen Physiol 113: 837-849.
21. Maeda N, Kawasaki T, Nakade S, Yokota N, Taguchi T, et al. (1991) Structural and functional characterization of inositol 1,4,5-trisphosphate receptor channel from mouse cerebellum. J Biol Chem 266: 1109-1116.
22. Kaznacheyeva E, Lupu VD, Bezprozvanny I, (1998) Single-channel properties of inositol (1,4,5)- trisphosphate receptor heterologously expressed in HEK-293 cells. J Gen Physiol 111: 847-856.
23. Dellis O, Dedos S, Tovey S, Taufiq-Ur-Rahman, Dubel S, et al. (2006) Ca2+ entry through plasma membrane IP3 receptors. Science 313: 229.
24. Wagner I, Larry E, Joseph S, Yule D, (2008) Regulation of single inositol 1,4,5-trisphosphate receptor channel activity by protein kinase a phosphorylation. J Physiol 586: 3577-3596.
25. Wagner I, Larry E, Yule D, (2012) Differential regulation of the InsP3 receptor type-1 and-2 single channel properties by InsP3, Ca2+ and ATP. J Physiol 590: 3245-3259.
26. Mak D, Foskett J, (1994) Single-channel inositol 1,4,5-trisphosphate receptor currents revealed by patch clamp of isolated Xenopus oocyte nuclei. J Biol Chem 269: 29375-29378.
27. Marchenko S, Yarotskyy V, Kovalenko T, Kostyuk P, Thomas R, (2005) Spontaneously active and InsP3-activated ion channels in cell nuclei from rat cerebellar Purkinje and granule neurones. J Physiol 565: 897-910.
28. Marchenko S, Thomas R, (2006) Nuclear Ca2+ signalling in cerebellar Purkinje neurons. The Cerebellum 5: 36-42.
29. Skupin A, Falcke M, Taylor C, (2009) Clustering of InsP3 receptors by InsP3 retunes their regulation by InsP3 and Ca2+. Nature 458: 655-659.
30. Mak D, McBride S, Foskett J, (2001) ATP regulation of recombinant type 3 inositol 1, 4, 5- trisphosphate receptor gating. J Gen Physiol 117: 447-456.
31. Fujiwara A, Hirose K, Yamazawa T, Iino M, (2001) Reduced IP3 sensitivity of IP3 receptor in Purkinje neurons. Neuroreport 12: 2647-2651.
32. Dufour J, Arias I, Turner T, (1997) Inositol 1,4,5-trisphosphate and calcium regulate the calcium channel function of the hepatic inositol 1,4,5-trisphosphate receptor. J Biol Chem 272: 2675-2681.
33. Marchant JS, Taylor CW, (1997) Cooperative activation of IP3 receptors by sequential binding of IP3 and Ca2+ safeguards against spontaneous activity. Curr Biol 7: 510-518.
34. Adkins C, Taylor C, (1999) Lateral inhibition of inositol 1,4,5-trisphosphate receptors by cytosolic Ca2+. Curr Biol 9: 1115-1118.
35. Doi T, Kuroda S, Michikawa T, Kawato M, (2005) Inositol 1,4,5-trisphosphate-dependent Ca2+ threshold dynamics detect spike timing in cerebellar Purkinje cells. J Neurosci 25: 950-961.
36. Sneyd J, Falcke M, Dufour J, Fox C, (2004) A comparison of three models of the inositol trisphosphate receptor. Prog Biophys Mol Biol 85: 121-140.
37. Eungdamrong N, Iyengar R, (2004) Modeling cell signaling networks. Biol Cell 96: 355-362.
38. Hellgren Kotaleski J, Blackwell K, (2010) Modelling the molecular mechanisms of synaptic plasticity using systems biology approaches. Nat Rev Neurosci 11: 239-251.
39. Sneyd J, Falcke M, (2005) Models of the inositol trisphosphate receptor. Prog Biophys Mol Biol 89: 207-245.
40. Falcke M, (2003) On the role of stochastic channel behavior in intracellular Ca2+ dynamics. Biophys J 84: 42-56.
41. De Young G, Keizer J, (1992) A single-pool inositol 1,4,5-trisphosphate-receptor-based model for agonist-stimulated oscillations in Ca2+ concentration. Proc Natl Acad Sci USA 89: 9895-9899.
42. LeBeau A, Yule D, Groblewski G, Sneyd J, (1999) Agonist-dependent phosphorylation of the inositol 1, 4, 5-trisphosphate receptor. J Gen Physiol 113: 851.
43. Tang Y, Stephenson J, Othmer H, (1996) Simplification and analysis of models of calcium dynamics based on IP3-sensitive calcium channel kinetics. Biophys J 70: 246-263.
44. Mak D, McBride S, Foskett J, (2003) Spontaneous channel activity of the inositol 1,4,5-trisphosphate (InsP3) receptor (InsP3R). Application of allosteric modeling to calcium and InsP3 regulation of InsP3R single-channel gating. J Gen Physiol 122: 583.
45. Shuai JW, Yang DP, Pearson JE, Rüdiger S, (2009) An investigation of models of the IP3R channel in Xenopus oocyte. Chaos 19: 037105.
46. Schuster S, Marhl M, Hofer T, (2002) Modelling of simple and complex calcium oscillations. Eur J Biochem 269: 1333-1355.
47. Turner TE, Schnell S, Burrage K, (2004) Stochastic approaches for modelling in vivo reactions. Comp Biol Chem 28: 165-178.
48. Barrio M, Burrage K, Leier A, Tian T, (2006) Oscillatory regulation of Hes1: discrete stochastic delay modelling and simulation. PLOS Comp Biol 2: e117.
49. Hituri K, Achard P, Wils S, Linne ML, De Schutter E (2008) Stochastic modeling of inositol-1,4,5- trisphophate receptors in Purkinje cell spine. In: Proceedings of the 5th TICSP Workshop on Computation Systems Biology (WCSB 2008). Leipzig, Germany, pp. 57-60.
50. Choi T, Maurya M, Tartakovsky D, Subramaniam S, (2010) Stochastic hybrid modeling of intracellular calcium dynamics. J Chem Phys 133: 165101.
51. Gillespie DT, (1976) A general method for numerical simulating the stochastic time evolution of coupled chemical reactions. J Comp Phys 22: 403-434.
52. Sneyd J, Dufour J, (2002) A dynamic model of the type-2 inositol trisphosphate receptor. Proc Natl Acad Sci USA 99: 2398-2403.
53. Swillens S, Champeil P, Combettes L, Dupont G, (1998) Stochastic simulation of a single inositol 1,4,5-trisphosphate-sensitive Ca2+ channel reveals repetitive openings during 'blip-like' Ca2+ transients. Cell calcium 23: 291-302.
54. Haeri H, Hashemianzadeh S, Monajjemi M, (2007) A kinetic Monte Carlo simulation study of inositol 1,4,5-trisphosphate receptor (IP3R) calcium release channel. Comp Biol Chem 31: 99-109.
55. Othmer HG, Tang Y (1993) Oscillations and waves in a model of InsP3-controlled calcium dynamics, London: Plenum Press, volume 259 of Experimental and Theoretical Advances in Biological Pattern Formation. pp. 277-300.
56. Dawson A, Lea E, Irvine R, (2003) Kinetic model of the inositol trisphosphate receptor that shows both steady-state and quantal patterns of Ca2+ release from intracellular stores. Biochem J 370: 621.
57. Fraiman D, Dawson SP, (2004) A model of IP3 receptor with a luminal calcium binding site: stochastic simulations and analysis. Cell Calcium 35: 403-413.
58. Wils S, De Schutter E, (2009) STEPS: Modeling and simulating complex reaction-diffusion systems with Python. Front Neuroinform 3: 165-178.
59. Hepburn I, Chen W, Wils S, De Schutter E, (2012) STEPS: efficient simulation of stochastic reaction-diffusion models in realistic morphologies. BMC Syst Biol 6: 1752-0509.
60. Mishra J, Bhalla U, (2002) Simulations of inositol phosphate metabolism and its interaction with InsP3-mediated calcium release. Biophys J 83: 1298-1316.
61. Sachs F, Qin F, Palade P, (1995) Models of Ca2+ release channel adaptation. Science 267: 2010-2011.
62. Taylor CW, da Fonseca PC, Morris EP, (2004) IP3 receptors: the search for structure. Trends Biochem Sci 29: 210-219.
63. Khodakhah K, Ogden D, (1995) Fast activation and inactivation of inositol trisphosphate-evoked Ca2+ release in rat cerebellar Purkinje neurones. J Physiol 487: 343.
64. Gillespie DT, (1977) Exact stochastic simulation of coupled chemical reactions. J Phys Chem 81: 2340-2361.
65. MATLAB (2011) version 7.13.0.564 (R2011b). Natick, Massachusetts: The MathWorks Inc.
66. Diambra L, Guisoni N, (2005) Modeling stochastic Ca2+ release from a cluster of IP3-sensitive receptors. Cell Calcium 37: 321-332.
67. Fraiman D, Dawson SP, (2004) Erratum to "a model of IP3 receptor with a luminal calcium binding site: stochastic simulations and analysis". Cell Calcium 36: 445.
68. De Schutter E, (2008) Why are computational neuroscience and systems biology so separate? PLOS Comp Biol 4: e1000078.
69. Gin E, Falcke M, Wagner L, Yule D, Sneyd J, (2009) Markov chain Monte Carlo fitting of singlechannel data from inositol trisphosphate receptors. J Theor Biol 257: 460-474.
70. Gin E, Falcke M, Wagner L, et al. (2009) A kinetic model of the inositol trisphosphate receptor based on single-channel data. Biophysical journal 96: 4053.
71. Gin E, Wagner L, Yule D, Sneyd J, (2009) Inositol trisphosphate receptor and ion channel models based on single-channel data. Chaos 19: 037104.
72. Siekmann I, Wagner L, Yule D, Fox C, Bryant D, et al. (2011) MCMC estimation of Markov models for ion channels. Biophys J 100: 1919-1929.
73. Amari S, Beltrame F, Bjaalie J, Dalkara T, De Schutter E, et al. (2002) Neuroinformatics: the integration of shared databases and tools towards integrative neuroscience. J Integr Neurosci 1: 117-128.
74. Cannon R, Howell F, Goddard N, De Schutter E, (2002) Non-curated distributed databases for experimental data and models in neuroscience. Network: Computation in Neural Systems 13: 415-428.
75. De Schutter E (2010) Data publishing and scientific journals: The future of the scientific paper in a world of shared data. Neuroinformatics: 1-3.
76. Ranjan R, Khazen G, Gambazzi L, Ramaswamy S, Hill S,et al. (2011) Channelpedia: an integrative and interactive database for ion channels. Front Neuroinform 5.
77. Cannon R, O'Donnell C, Nolan M, (2010) Stochastic ion channel gating in dendritic neurons: Morphology dependence and probabilistic synaptic activation of dendritic spikes. PLOS Comp Biol 6: e1000886.
78. White J, Klink R, Alonso A, Kay A, (1998) Noise from voltage-gated ion channels may influence neuronal dynamics in the entorhinal cortex. J Neurophysiol 80: 262.
79. Steinmetz P, Manwani A, Koch C, London M, Segev I, (2000) Subthreshold voltage noise due to channel fluctuations in active neuronal membranes. J Comput Neurosci 9: 133-148.
80. Saarinen A, Linne ML, Yli-Harja O, (2008) Stochastic differential equation model for cerebellar granule cell excitability. PLOS Comp Biol 4(2): e1000004.
81. Faisal A, Laughlin S, (2007) Stochastic simulations on the reliability of action potential propagation in thin axons. PLOS Comp Biol 3: e79.
82. Skupin A, Kettenmann H, Falcke M, (2010) Calcium signals driven by single channel noise. PLOS Comp Biol 6: e1000870.
83. Wilkinson D, (2007) Bayesian methods in bioinformatics and computational systems biology. Brief Bioinform 8: 109.
84. Girolami M, (2008) Bayesian inference for differential equations. Theor Comput Sci 408: 4-16.
85. Penny W, Stephan K, Daunizeau J, Rosa M, Friston K, et al. (2010) Comparing families of dynamic causal models. PLOS Comp Biol 6: e1000709.