CaV2.1 (P/Q channel) interaction with synaptic proteins is essential for depolarization-evoked release

Channels

Volumn 4, Issue 4, 2010, Pages

  Cohen Kutner, Moshe ^a   Nachmanni, Daphna ^a   Atlas, Daphne ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Capacitance; Exocytosis; P Q channel; Synaptic transmission; Synaptotagmin; Syntaxin

Indexed keywords

BOTULINUM TOXIN; CYSTEINE; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; MULTIPROTEIN COMPLEX; SYNAPTOBREVIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNAPTOTAGMIN I; SYNTAXIN 1A; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CHANNEL GATING; CYTOSOLIC FRACTION; DEPOLARIZATION; HUMAN; HUMAN CELL; NEURONAL CHANNELOPATHY; NONHUMAN; OOCYTE; SYNAPSE; XENOPUS;

EID: 77956466889     PISSN: 19336950     EISSN: 19336969     Source Type: Journal    
DOI: 10.4161/chan.4.4.12130     Document Type: Article

References (66)

1. Katz B, Miledi R. The timing of calcium action during neuromuscular transmission. J Physiol 1967; 189:535-44.
2. 2+ sensor of fast neurotransmitter release. Cell Mol Neurobiol 2001; 21:717-31.
3. Jarvis SE, Zamponi GW. Masters or slaves? Vesicle release machinery and the regulation of presynaptic calcium channels. Cell Calcium 2005; 37:483-8.
4. 2+ channel/syntaxin interaction. J Neurosci 1997; 17:6647-56.
5. 2+ channels. Neuron 1996; 17:781-8.
6. 2+ channel is functionally coupled to the exocytotic machinery. Proc Natl Acad Sci USA 1999; 96:248-53.
7. Ji J, Yang SN, Huang X, Li X, Sheu L, Diamant N, et al. Modulation of L-type Ca(2+) channels by distinct domains within SNAP-25. Diabetes 2002; 51:1425-36.
8. Fasshauer D, Otto H, Eliason WK, Jahn R, Brunger AT. Structural changes are associated with soluble N-ethylmaleimide-sensitive fusion protein attachment protein receptor complex formation. J Biol Chem 1997; 272:28036-41.
9. Heuser JE, Reese TS. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol 1973; 57:315-44.
10. Mennerick S, Matthews G. Ultrafast exocytosis elicited by calcium current in synaptic terminals of retinal bipolar neurons. Neuron 1996; 17:1241-9.
11. Stanley EF. Presynaptic calcium channels and the transmitter release mechanism. Ann N Y Acad Sci 1993; 681:368-72.
12. Cohen R, Schmitt BM, Atlas D. Molecular identification and reconstitution of depolarization-induced exocytosis monitored by membrane capacitance. Biophys J 2005; 89:4364-73.
13. Hagalili Y, Bachnoff N, Atlas D. The voltage-gated Ca(2+) channel is the Ca(2+) sensor protein of secretion. Biochemistry 2008; 47:13822-30.
14. Atlas D. Signaling role of the voltage-gated calcium channel as the molecular 'ON/OFF'-switch of secretion. Cell Signal.
15. 2+ channels mediating synaptic transmission at the calyx of Held of mice. J Physiol 2005; 568:199-209.
16. 2+ channels in the mammalian central nervous system. Trends Neurosci 1992; 15:351-5.
17. Stea A, Tomlinson WJ, Soong TW, Bourinet E, Dubel SJ, Vincent SR, Snutch TP. Localization and functional properties of a rat brain alpha1A calcium channel reflect similarities to neuronal Q- and P-type channels. Proc Natl Acad Sci USA 1994; 91:10576-80.
18. Wu LG, Saggau P. Pharmacological identification of two types of presynaptic voltage-dependent calcium channels at CA3-CA1 synapses of the hippocampus. J Neurosci 1994; 14:5613-22.
19. Takahashi T, Momiyama A. Different types of calcium channels mediate central synaptic transmission. Nature 1993; 366:156-8.
20. Regehr WG, Mintz IM. Participation of multiple calcium channel types in transmission at single climbing fiber to Purkinje cell synapses. Neuron 1994; 12:605-13.
21. Wang G, Dayanithi G, Newcomb R, Lemos JR. An R-type Ca(2+) current in neurohypophysial terminals preferentially regulates oxytocin secretion. J Neurosci 1999; 19:9235-41.
22. Meinrenken CJ, Borst JG, Sakmann B. Calcium secretion coupling at calyx of held governed by non-uniform channel-vesicle topography. J Neurosci 2002; 22:1648-67.
23. Cohen R, Marom M, Atlas D. Depolarization-evoked secretion requires two vicinal transmembrane cysteines of syntaxin 1A. PLoS One 2007; 2:1273.
24. Sandoz G, Bichet D, Cornet V, Mori Y, Felix R, De Waard M. Distinct properties and differential beta subunit regulation of two C-terminal isoforms of the P/Q-type Ca(2+)-channel alpha(1A) subunit. Eur J Neurosci 2001; 14:987-97.
25. Hanson PI, Heuser JE, Jahn R. Neurotransmitter release - four years of SNARE complexes. Curr Opin Neurobiol 1997; 7:310-5.
26. 2+ channels. EMBO J 1996; 15:4100-10.
27. Wiser O, Tobi D, Trus M, Atlas D. Synaptotagmin restores kinetic properties of a syntaxin-associated N-type voltage sensitive calcium channel. FEBS Lett 1997; 404:203-7.
28. Sutton KG, McRory JE, Guthrie H, Murphy TH, Snutch TP. P/Q-type calcium channels mediate the activity-dependent feedback of syntaxin-1A. Nature 1999; 401:800-4.
29. Bezprozvanny I, Scheller RH, Tsien RW. Functional impact of syntaxin on gating of N-type and Q-type calcium channels. Nature 1995; 378:623-6.
30. Sollner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, Tempst P, Rothman JE. SNAP receptors implicated in vesicle targeting and fusion. Nature 1993; 362:318-24.
31. Cohen R, Atlas D. R-type voltage-gated Ca(2+) channel interacts with synaptic proteins and recruits synaptotagmin to the plasma membrane of Xenopus oocytes. Neuroscience 2004; 128:831-41.
32. Aleu J, Blasi J, Solsona C, Marsal J. Calcium-dependent acetylcholine release from Xenopus oocytes: simultaneous ionic currents and acetylcholine release recordings. Eur J Neurosci 2002; 16:1442-8.
33. 2+ channels and their role in neurotransmitter release. Cell Calcium 1998; 24:307-23.
34. 2+ channels - integration centers for neuronal signaling pathways. Trends Neurosci 2006; 29:617-24.
35. 2+ and assembly with the core SNARE complex onto membranes. Neuron 1999; 24:363-76.
36. 2+ channels: a functional patchwork. Trends Neurosci 2003; 26:683-7.
37. V2.3 calcium channels control second-phase insulin release. J Clin Invest 2005; 115:146-54.
38. Baldelli P, Hernandez-Guijo JM, Carabelli V, Novara M, Cesetti T, Andres-Mateos E, et al. Direct and remote modulation of L-channels in chromaffin cells: distinct actions on alpha1C and alpha1D subunits? Mol Neurobiol 2004; 29:73-96.
39. + channels: tuning beta-cell excitability with syntaxin-1A and other exocytotic proteins. Endocr Rev 2007; 28:653-63.
40. Spafford JD, Zamponi GW. Functional interactions between presynaptic calcium channels and the neurotransmitter release machinery. Curr Opin Neurobiol 2003; 13:308-14.
41. 2+ channel gating. Proc Natl Acad Sci USA 2000; 97:13943-8.
42. Sheng ZH, Rettig J, Takahashi M, Catterall WA. Identification of a syntaxin-binding site on N-type calcium channels. Neuron 1994; 13:1303-13.
43. Kaneko S, Cooper CB, Nishioka N, Yamasaki H, Suzuki A, Jarvis SE, et al. Identification and characterization of novel human Ca(v)2.2 (alpha1B) calcium channel variants lacking the synaptic protein interaction site. J Neurosci 2002; 22:82-92.
44. Cena V, Nicolas GP, Sanchez-Garcia P, Kirpekar SM, Garcia AG. Pharmacological dissection of receptor-associated and voltage-sensitive ionic channels involved in catecholamine release. Neuroscience 1983; 10:1455-62.
45. 2+ channel trigger secretion with different efficacies in chromaffin cells. Nature 1994; 367:72-6.
46. Garcia AG, Garcia-De-Diego AM, Gandia L, Borges R, Garcia-Sancho J. Calcium signaling and exocytosis in adrenal chromaffin cells. Physiol Rev 2006; 86:1093-131.
47. 2+ channels with the presynaptic proteins syntaxin and SNAP-25. Proc Natl Acad Sci USA 1996; 93:7363-8.
48. Sakurai T, Westenbroek RE, Rettig J, Hell J, Catterall WA. Biochemical properties and subcellular distribution of the BI and rbA isoforms of alpha1A subunits of brain calcium channels. J Cell Biol 1996; 134:511-28.
49. 2+ channels by SNAP-25, syntaxin and synaptotagmin. Nat Neurosci 1999; 2:939-41.
50. Atlas D. Functional and physical coupling of voltage-sensitive calcium channels with exocytotic proteins: ramifications for the secretion mechanism. J Neurochem 2001; 77:972-85.
51. Bergsman JB, Tsien RW. Syntaxin modulation of calcium channels in cortical synaptosomes as revealed by botulinum toxin C1. J Neurosci 2000; 20:4368-78.
52. Stanley EF. The calcium channel and the organization of the presynaptic transmitter release face. Trends Neurosci 1997; 20:404-9.
53. Jarvis SE, Zamponi GW. Distinct molecular determinants govern syntaxin 1A-mediated inactivation and G-protein inhibition of N-type calcium channels. J Neurosci 2001; 21:2939-48.
54. Tobi D, Wiser O, Trus M, Atlas D. N-type voltage-sensitive calcium channel interacts with syntaxin, synaptotagmin and SNAP-25 in a multiprotein complex. Receptors Channels 1998; 6:89-98.
55. Stanley EF. Syntaxin I modulation of presynaptic calcium channel inactivation revealed by botulinum toxin C1. Eur J Neurosci 2003; 17:1303-5.
56. 2+ sensor protein of stimulus-secretion coupling in pancreatic beta cells. Biochemistry 2007; 46:14461-7.
57. Stanley EF, Mirotznik RR. Cleavage of syntaxin prevents G-protein regulation of presynaptic calcium channels. Nature 1997; 385:340-3.
58. Bai J, Wang CT, Richards DA, Jackson MB, Chapman ER. Fusion pore dynamics are regulated by synaptotagmin*t-SNARE interactions. Neuron 2004; 41:929-42.
59. Rickman C, Jimenez JL, Graham ME, Archer DA, Soloviev M, Burgoyne RD, Davletov B. Conserved prefusion protein assembly in regulated exocytosis. Mol Biol Cell 2006; 17:283-94.
60. Kuo W, Herrick DZ, Ellena JF, Cafiso DS. The calcium-dependent and calcium-independent membrane binding of synaptotagmin 1: two modes of C2B binding. J Mol Biol 2009; 387:284-94.
61. Chapman ER. How does synaptotagmin trigger neurotransmitter release? Annu Rev Biochem 2008; 77:615-41.
62. 2+-evoked secretion in Xenopus oocytes monitored by membrane capacitance. Methods Mol Biol 2008; 440:269-82.
63. Hibino H, Pironkova R, Onwumere O, Vologodskaia M, Hudspeth AJ, Lesage F. RIM binding proteins (RBPs) couple Rab3-interacting molecules (RIMs) to voltage-gated Ca(2+) channels. Neuron 2002; 34:411-23.
64. Lang T, Jahn R. Core proteins of the secretory machinery. Handb Exp Pharmacol 2008; 107-27.
65. Thomas DM, Elferink LA. Functional analysis of the C2A domain of synaptotagmin 1: implications for calcium-regulated secretion. J Neurosci 1998; 18:3511-20.
66. Schmitt BM, Koepsell H. An improved method for real-time monitoring of membrane capacitance in Xenopus laevis oocytes. Biophys J 2002; 82:1345-57.