Continuum simulations of acetylcholine diffusion with reaction-determined boundaries in neuromuscular junction models

Biophysical Chemistry

Volumn 127, Issue 3, 2007, Pages 129-139

  Cheng, Yuhui ^a   Suen, Jason K ^a   Radić, Zoran ^b   Bond, Stephen D ^c   Holst, Michael J ^b   McCammon, J Andrew ^a,b  

^a National Biomedical Computation Resource   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c University of Illinois at Urbana Champaign   (United States)

Author keywords

Finite element method; Reaction determined boundaries; Substrate inhibition; Synaptic transmission

Indexed keywords

ACETYLCHOLINE; ACETYLCHOLINESTERASE; NICOTINIC RECEPTOR;

ARTICLE; CHEMICAL REACTION; HYDROLYSIS; MOLECULAR DYNAMICS; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; PRIORITY JOURNAL; SIMULATION;

ACETYLCHOLINE; ACETYLCHOLINESTERASE; COMPUTER SIMULATION; DIFFUSION; HYDROLYSIS; MODELS, CHEMICAL; MODELS, NEUROLOGICAL; NEUROMUSCULAR JUNCTION; RECEPTORS, NICOTINIC; SYNAPSES; SYNAPTIC TRANSMISSION; TISSUE DISTRIBUTION;

EID: 33947372106     PISSN: 03014622     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bpc.2007.01.003     Document Type: Article

References (56)

1. Wathey J.C., Nass M.M., and Lester H.A. Numerical reconstruction of the quantal event at nicotinic synapses. Biophys. J. 27 1 (1979) 145-164
2. Friboulet A., and Thomas D. Reaction diffusion coupling in a structured system - application to the quantitative simulation of end-plate currents. J. Theor. Biol. 4 (1993) 441-455
3. Nagado T., Arimura K., Sonoda Y., Kurono A., Horikiri Y., Kameyama A., Kameyama M., Pongs O., and Osame M. Potassium current suppression in patients with peripheral nerve hyperexcitability. Brain 122 (1999) 2057-2066
4. Smit A.B., Syed N.I., Schaap D., van Minnen J., Klumperman J., Kits K.S., Lodder H., van der Schors R.C., van Elk R., Sorgedrager B., Brejc K., Sixma T.K., and Geraerts W.P.M. A glia-derived acetylcholine-binding protein that modulates synaptic transmission. Nature 411 6835 (2001) 261-268
5. Harel M., Kasher R., Nicolas A., Guss J.M., Balass M., Fridkin M., Smit A.B., Brejc K., Sixma T.K., Katchalski-katzir E., Sussman J.L., and Fuchs S. The binding site of acetylcholine receptor as visualized in the X-ray structure of a complex between alpha-bungarotoxin and a mimotope peptide. Neuron 32 2 (2001) 265-275
6. Sine S.M., and Engel A.G. Recent advances in cys-loop receptor structure and function. Nature 440 7083 (2006) 448-455
7. Miyazawa A., Fujiyoshi Y., and Unwin N. Structure and gating mechanism of the acetylcholine receptor pore. Nature 423 6943 (2003) 949-955
8. Unwin N. Structure and action of the nicotinic acetylcholine receptor explored by electron microscopy. FEBS Lett. 555 1 (2003) 91-95
9. Unwin N. Refined structure of the nicotinic acetylcholine receptor at 4 angstrom resolution. J. Mol. Biol. 346 4 (2005) 967-989
10. Taylor P. Anticholinesterase agents. In: Hardman j.G., Limbird L.E., Molinoff P.B., Ruddon R.W., and Gilman A.G. (Eds). The Pharmacological Basis of Therapeutics (1996), McGraw-Hill, New York 161-176
11. Shen T., Tai K., Henchman R., and McCammon J.A. Molecular dynamics of acetylcholinesterase. Acc. Chem. Res. 35 6 (2002) 332-340
12. Karlin A. Emerging structure of the nicotinic acetylcholine receptors. Nat. Rev. Neurosci. 3 2 (2002) 102-114
13. Bertram R. A simple model of transmitter release and facilitation. Neural. Comput. 9 3 (1997) 515-523
14. Bertram R., Sherman A., and Stanley E.F. Single-domain/bound calcium hypothesis of transmitter release and facilitation. J. Neurophysiol. 75 5 (1996) 1919-1931
15. Kruk P.J., Korn H., and Faber D.S. The effects of geometrical parameters on synaptic transmission: a Monte Carlo simulation study. Biophys. J. 73 6 (1997) 2874-2890
16. Wahl L.M., Pouzat C., and Stratford K.J. Monte Carlo simulation of fast excitatory synaptic transmission at a hippocampal synapse. J. Neurophysiol. 75 2 (1996) 597-608
17. Naka T., and Sakamoto N. Localization effects of acetylcholine release from a synaptic vesicle at the neuromuscular junction. Biosystems 51 2 (1999) 73-78
18. Ghaffari-farazi T., Liaw J.S., and Berger T.W. Consequence of morphological alterations on synaptic function. Neurocomputing 26-7 (1999) 17-27
19. Naka T. Evaluation of characteristic parameters for the neurotransmitter release mechanisms at the neuromuscular junction. Biosystems 49 2 (1999) 143-149
20. Naka T. Simulation analysis of the effects of the junctional folds on spontaneous generation of the miniature endplate current at neuromuscular junction. Math. Comput. Simul. 46 5-6 (1998) 631-639
21. Aharon S., Bercovier M., and Parnas H. Parallel computation enables precise description of Ca2+ distribution in nerve terminals. Bull. Math. Biol. 58 6 (1996) 1075-1097
22. Cooper R.L., Winslow J.L., Govind C.K., and Atwood H.L. Synaptic structural complexity as a factor enhancing probability of calcium-mediated transmitter release. J. Neurophysiol. 75 6 (1996) 2451-2466
23. Yamada W.M., and Zucker R.S. Time course of transmitter release calculated from simulations of a calcium diffusion-model. Biophys. J. 61 3 (1992) 671-682
24. 2+ diffusion on the time course of neurotransmitter release. Biophys. J. 55 5 (1989) 859-874
25. Zucker R.S., and Stockbridge N. Pre-synaptic calcium diffusion and the time courses of transmitter release and synaptic facilitation at the squid giant synapse. J. Neurosci. 3 6 (1983) 1263-1269
26. Axelsson O., and Baker V.A. Finite element solution of boundary value problems. Theory and Computation (1984), Academic Press, San Diego
27. Smart J.L., and McCammon J.A. Analysis of synaptic transmission in the neuro-muscular junction using a continuum finite element model. Biophys. J. 75 4 (1998) 1679-1688
28. Tai K., Bond S.D., Macmillan H.R., Baker N.A., Holst M.J., and McCammon J.A. Finite element simulations of acetylcholine diffusion in neuromuscular junctions. Biophys. J. 84 4 (2003) 2234-2241
29. Braess D. Finite Elements (1997), Cambridge University Press, Cambridge
30. Stiles J.R., and Bartol T.M. Monte Carlo methods for simulating realistic synaptic microphysiology using MCell. In: Schutter E.D. (Ed). Computational Neuroscience: Realistic Modeling for Experimentalists (2000), CRC Press Inc., New York 87-127
31. Stiles J.R., Bartol T.M., Salpeter M.M., and Sejnowski T.J. Synaptic variability: new insights from reconstructions and Monte Carlo simulations with MCell. In: Cowan W.M., Sudhof T.C., and Stevens C.F. (Eds). Synapses (2001), Johns Hopkins University Press, Baltimore, Maryland 681-731
32. Coggan J.S., Bartol T.M., Esquenazi E., Stiles J.R., Lamont S., Martone M.E., Berg D.K., Ellisman M.H., and Sejnowski T.J. Evidence for ectopic neurotransmission at a neuronal synapse. Science 309 5733 (2005) 446-451
33. Holst M. Adaptive numerical treatment of elliptic systems on manifolds. Adv. Comput. Math. 15 1-4 (2001) 139-191
34. Radić Z., Pickering N.A., Vellom D.C., Camp S., and Taylor P. 3 distinct domains in the cholinesterase molecule confer selectivity for acetyl-cholinesterase and butyrylcholinesterase inhibitors. Biochemistry 32 45 (1993) 12074-12084
35. Kovarik Z., Radić Z., Berman H.A., Simeon-rudolf V., Reiner E., and Taylor P. Acetylcholinesterase active centre and gorge conformations analysed by combinatorial mutations and enantiomeric phosphonates. Biochem. J. 373 (2003) 33-40
36. Radić Z., and Taylor P. Interaction kinetics of reversible inhibitors and substrates with acetylcholinesterase and its fasciculin 2 complex. J. Biol. Chem. 276 7 (2001) 4622-4633
37. Bourne Y., Taylor P., Radic Z., and Marchot P. Structural insights into ligand interactions at the acetylcholinesterase peripheral anionic site. EMBO J. 22 1 (2003) 1-12
38. Unwin N., Miyazawa A., Li J., and Fujiyoshi Y. Activation of the nicotinic acetyl-choline receptor involves a switch in conformation of the a subunits. J. Mol. Biol. 319 5 (2002) 1165-1176
39. Land B.R., Harris W.V., Salpeter E.E., and Salpeter M.M. Diffusion and binding constants for acetylcholine derived from the falling phase of miniature endplate currents. Proc. Natl. Acad. Sci. U. S. A. 81 5 (1984) 1594-1598
40. Grosman C., and Auerbach A. The dissociation of acetylcholine from open nicotinic receptor channels. Proc. Natl. Acad. Sci. U. S. A. 98 24 (2001) 14102-14107
41. Salamone F.N., Zhou M., and Auerbach A. A re-examination of adult mouse nicotinic acetylcholine receptor channel activation kinetics. J. Physiol. (Lond.) 516 2 (1999) 315-330
42. Grosman C., Salamone F.N., Sine S.M., and Auerbach A. The extracellular linker of muscle acetylcholine receptor channels is a gating control element. J. Gen. Physiol. 116 3 (2000) 327-339
43. Fucik S., and Kufner A. Nonlinear differential equations (1980), Elsevier Scientific Publishing Company, New York
44. Hackbusch W. Elliptic differential equations (1994), Springer-Verlag, Berlin, Germany
45. Holst M., Baker N., and Wang F. Adaptive multilevel finite element solution of the Poisson-Boltzmann equation I. algorithms and examples. J. Comput. Chem. 21 15 (2000) 1319-1342
46. Y.H. Cheng, J. Suen, D.Q. Zhang, S. Bond, Y.J. Zhang, Y.H. Song, N. Baker, C. Bajaj, M. Holst, J.A. McCammon. Finite element analysis of the time-dependent smoluchowski equation for acetylcholinesterase reaction rate calculations, Biophys. J. (in press).
47. Schöberl J. Netgen: an advancing front 2D/3D-mesh generator based on abstract rules. Comput. Visual Sci. 1 (1997) 41-52
48. Zhang D.Q., Suen J., Zhang Y.J., Song Y.H., Radić Z., Taylor P., Holst M.J., Bajaj C., Baker N.A., and Mccammon J.A. Tetrameric mouse acetyl-cholinesterase: continuum diffusion rate calculations by solving the steady-state Smoluchowski equation using finite element methods. Biophys. J. 88 3 (2005) 1659-1665
49. Akk G., and Auerbach A. Activation of muscle nicotinic acetylcholine receptor channels by nicotinic and muscarinic agonists. Br. J. Pharmacol. 128 7 (1999) 1467-1476
50. Schwartz J.H. Synaptic vesicles. In: Kandel E.R., Schwartz J.H., and Jessell T.M. (Eds). Principles of Neural Science (1991), Appleton and Lange, Norwalk, Connecticut 225-234
51. Zimmermann H. Synaptic Transmission: Cellular and Molecular Basis (1993), Thieme, Stuttgart, Germany
52. Südhof T.C., and Scheller R.H. Mechanism and regulation of neurotransmitter release. In: Cowan W.M., Südhof T.C., and Stevens C.F. (Eds). Synapses (2000), Johns Hopkins University Press, Baltimore, Maryland
53. Naka T., Shiba K., and Sakamoto N. A two-dimensional compartment model for the reaction-diffusion system of acetylcholine in the synaptic cleft at the neuromuscular junction. Biosystems 41 1 (1997) 17-27
54. Magleby K.L., and Terrar D.A. Factors affecting time course of decay of end-plate currents - possible cooperative action of acetylcholine on receptors at frog neuromuscular-junction. J. Physiol. (Lond.) 244 2 (1975) 467-495
55. Katz B., and Miledi R. Binding of acetylcholine to receptors and its removal from synaptic cleft. J. Physiol. (Lond.) 231 3 (1973) 549-574
56. Zhang Y.J., Bajaj C., and Sohn B.S. 3D finite element meshing from imaging data. Comput. Methods Appl. Mech. Eng. 194 48-49 (2005) 5083-5106