A Syntaxin 1, Gαo, and N-Type Calcium Channel Complex at a Presynaptic Nerve Terminal: Analysis by Quantitative Immunocolocalization

Journal of Neuroscience

Volumn 24, Issue 16, 2004, Pages 4070-4081

  Li, Qi ^a   Lau, Anthony ^a   Morris, Terence J ^a   Guo, Lin ^a   Fordyce, Christopher B ^a   Stanley, Elise F ^a  

^a UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

1B subunit; Cav2.2; Calcium channel; Colocalization; G o; G protein; Immunocytochemistry; Intensity correlation analysis; Intensity correlation quotient; MUNC18 1; n sec 1; N type; Presynaptic; Syntaxin; Transmitter release site

Indexed keywords

CALCIUM CHANNEL; CALCIUM CHANNEL N TYPE; GLUTATHIONE TRANSFERASE; GUANINE NUCLEOTIDE BINDING PROTEIN; SYNTAXIN; SYNTHETIC PEPTIDE; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; MEMBRANE ANTIGEN; MUNC18 PROTEIN; NERVE PROTEIN; STX1A PROTEIN, RAT; STXBP1 PROTEIN, RAT; SYNTAXIN 1; VESICULAR TRANSPORT PROTEIN;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; CHICKEN; FLUORESCENCE MICROSCOPY; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; NERVE CELL CULTURE; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; WESTERN BLOTTING; ANIMAL; ANTIBODY SPECIFICITY; BRAIN LEVEL; CELL CULTURE; CHEMISTRY; CHICK EMBRYO; IMMUNOHISTOCHEMISTRY; MACROMOLECULE; METABOLISM; METHODOLOGY; RAT; SYNAPTOSOME;

ANIMALS; ANTIBODY SPECIFICITY; ANTIGENS, SURFACE; BLOTTING, WESTERN; BRAIN CHEMISTRY; CALCIUM CHANNELS, N-TYPE; CELLS, CULTURED; CHICK EMBRYO; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; IMMUNOHISTOCHEMISTRY; MACROMOLECULAR SUBSTANCES; MUNC18 PROTEINS; NERVE TISSUE PROTEINS; PRESYNAPTIC TERMINALS; RATS; SYNTAXIN 1; VESICULAR TRANSPORT PROTEINS;

EID: 2142765951     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0346-04.2004     Document Type: Article

References (45)

1. Bergsman JB, Tsien RW (2000) Syntaxin modulation of calcium channels in cortical synaptosomes as revealed hy botulinum toxin C1. J Neurosci 20:4368-4378.
2. Bezprozvanny I, Scheller RH, Tsien RW (1995) Functional impact of syntaxin on gating of N-type and Q-type calcium channels. Nature(Lond) 378:623-626.
3. Bouvier JA, Charvin N, Boudier JL, Fathallah M, Tagaya M, Takahashi M, Seagar M (1996) Distribution of components of the SNARE complex in relation to transmitter release sites at the frog neuromuscular junction. Eur J Neurosci 8:545-552.
4. Brewer GJ (1997) Isolation and culture of adult rat hippocampal neurons. J Neurosci Methods 71:143-155.
5. Chen S, Zheng X, Schulze KL, Morris T, Bellen H, Stanley EF (2002) Enhancement of presynaptic calcium current by cysteine string current. J Physiol (Lond) 538:383-389.
6. David P, El Far O, Martin-Mouto N, Poupon MF, Takahashi M, Seagar MJ (1993) Expression of synaptotagmin and syntaxin associated with N-type calcium channels in small cell lung cancer. FEBS Lett 326:135-139.
7. Degtiar VE, Scheller RH, Tsien RW (2000) Syntaxin modulation of slow inactivation of N-type calcium channels. J Neurosci 20:4355-4367.
8. Dulubova I, Sugita S, Hill S, Hosaka M, Fernandez I, Sudhof TC, Rizo J (1999) A conformational switch in syntaxin during exocytosis: role of munc18. EMBO J 18:4372-4382.
9. Dulubova I, Yamaguchi T, Arac D, Li H, Huryeva I, Min SW, Rizo J, Sudhof TC (2003) Convergence and divergence in the mechanism of SNARE binding by Sec1/Munc18-like proteins. Proc Natl Acad Sci USA 100:32-37.
10. Fletcher CF, Tottene A, Lennon VA, Wilson SM, Dubel SJ, Paylor R, Hosford DA, Tessarollo L, McEnery MW, Pietrobon D, Copeland NG, Jenkins NA (2001) Dystonia and cerebellar a trophy in Cacnala null mice lacking P/Q calcium channel activity. FASEB J 15:1288-1290.
11. Garcia EP, McPherson PS, Chilcote TJ, Takei K, De Camilli P (1995) rbSec1A and B colocalize with syntaxin 1 and SNAP-25 throughout the axon, but are not in a stable complex with syntaxin. J Cell Biol 129:105-120.
12. 2+ channels coupled to acetylcholine release. Neuron 8:715-724.
13. Hata Y, Slaughter CA, Sudhof TC (1993) Synaptic vesicle fusion complex contains unc-18 homologue bound to syntaxin. Nature (Lond) 366:347-351.
14. Hata Y, Südhof TC (1995) A novel ubiquitous form of Munc-18 interacts with multiple syntaxins. Use of the yeast two-hybrid system to study interactions between proteins involved in membrane traffic. J Biol Chem 270:13022-13028.
15. Hille B (1994) Modulation of ion channels by G-protein coupled receptors. Trends Neurosci 17:531-533.
16. Ikeda SR, Dunlap K (1999) Voltage-dependent modulation of N-type calcium channels: role of G protein subunits. Adv Second Messenger Phosphoprotein Res 1999 131-151.
17. Jarvis SE, Zamponi GW (2001a) Distinct molecular determinants govern syntaxin 1A-mediated inactivation and G-protein inhibition of N-type calcium channels. J Neurosci 21:2939-2948.
18. 2+ channels, cytoplasmic messengers and proteins of the synaptic vesicle release complex. Trends Pharmacol Sci 22:519-525.
19. Kee Y, Lin RC, Hsu S-C, Scheller RH (1995) Distinct domains of syntaxin are required for synaptic vesicle fusion complex formation and dissociation. Neuron 14:991-998.
20. Lu Q, Dunlap K (1999) Cloning and functional expression of novel N-type Ca(2+) channel variants. J Biol Chem 274:34566-34575.
21. 2+ channels by Gβγ in chick sensory neurons. J Neurosci 21:2949-2957.
22. McEnery MW, Snowman AM, Snyder SH (1994) The association of endogenous Go alpha with the purified omega-conotoxin GVIA receptor. J Biol Chem 269:5-8.
23. 2+ channels is predominant isoform expressed in human neuroblastoma cell line IMR32. FEBS Lett 420:74-78.
24. Mirotznik RR, Zheng X, Stanley EF (2000) G-Protein types involved in calcium channel inhibition at a presynaptic nerve terminal. J Neurosci 20:7614-7621.
25. Misura KM, Scheller RH, Weis WI (2000) Three-dimensional structure of the neuronal-Sec1-syntaxin 1a complex. Nature (Lond) 404:355-362.
26. Morris TJ, Stanley EF (2003) A simple method for immunocytochemical staining with multiple rabbit polyclonal antibodies. J Neurosci Methods 127:149-155.
27. Pevsner J, Hsu S-C, Scheller RH (1994) n-Sec1: A neural-specific syntaxin-binding protein. Proc Natl Acad Sci USA 91:1445-1449.
28. Raciborska DA, Trimble WS, Charlton MP (1998) Presynaptic protein interactions in vivo: evidence from botulinum A, C, D, and E action at frog neuromuscular junction. Eur J Neurosci 10:2617-2628.
29. Saisu H, Ibaraki K, Yamaguchi T, Sekine Y, Abe T (1991) Monoclonal antibodies immunoprecipitating omega-conotoxin-sensitive calcium channel molecules recognize two novel proteins localized in the nervous system. Biochem Biophys Res Commun 181:59-66.
30. 2+. Biophys J 69:1847-1857.
31. Seagar M, Takahashi M (1998) Interactions between presynaptic calcium channels and proteins implicated in synaptic vesicle trafficking and exocytosis. J Bioenerg Biomembr 30:347-356.
32. Sheng Z-H, Rettig J, Takahashi M, Catterall WA (1994) Identification of a syntaxin-binding site on N-type calcium channels. Neuron 13:1303-1313.
33. Stanley EF (1991) Single calcium channels on a cholinergic presynaptic nerve terminal. Neuron 7:585-591.
34. Stanley EF (2003) Syntaxin I modulation of presynaptic calcium channel inactivation revealed by botulinum toxin C1. Eur J Neurosci 17:1303-1305.
35. Stanley EF, Atrakchi AH (1990) Calcium currents recorded from a vertebrate presynaptic nerve terminal are resistant to the dihydropyridine nifedipine. Proc Natl Acad Sci USA 87:9683-9687.
36. Stanley EF, Goping G (1991) Characterization of a calcium current in a vertebrate cholinergic presynaptic nerve terminal. J Neurosci 11:985-993.
37. Stanley EF, Mirotznik RR (1997) Cleavage of syntaxin prevents G-protein regulation of presynaptic calcium channels. Nature (Lond) 385:340-343.
38. Stanley EF, Reese TS, Wang GZ (2003) Molecular scaffold reorganization at the transmitter release site with vesicle exocytosis or botulinum toxin CI. Eur J Neurosci 18:2403-2407.
39. Sun XP, Stanley EF (1996) An ATP-activated, ligand gated ion channel on a cholinergic presynaptic nerve terminal. Proc Natl Acad Sci USA 93:1859-1863.
40. Takahashi T, Kajikawa Y, Tsujimoto T (1998) G-Protein-coupled modulation of presynaptic calcium currents and transmitter release by a GABAB receptor. J Neurosci 18:3138-3146.
41. Vance CL, Begg CM, Lee WL, Dubel SJ, Copeland TD, Sonnichsen FD, McEnery MW (1999) N-type calcium channel/syntaxin/SNAP-25 complex probed by antibodies to II-III intracellular loop of the alpha1B subunit. Neuroscience 90:665-676.
42. White MG, Crumling MA, Meriney SD (1997) Developmental changes in calcium current pharmacology and somatostatin inhibition in chick parasympathetic neurons. J Neurosci 17:6302-6313.
43. 2+ channels. EMBO J 15:4100-4110.
44. 2+ channels by adenosine autoreceptors. Nature (Lond) 365:256-258.
45. Yoshida A, Oho C, Omori A, Kuwahara R, Ito T, Takahashi M (1992) HPC-1 is associated with synaptotagmin and omega-conotoxin receptor. J Biol Chem 267:24925-24928.