N type Ca2+ channels and RIM scaffold protein covary at the presynaptic transmitter release face but are components of independent protein complexes

Neuroscience

Volumn 140, Issue 4, 2006, Pages 1201-1208

  Khanna, R ^a   Li, Q ^a   Sun, L ^a,b   Collins, T J ^a   Stanley, E F ^a  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

Author keywords

active zone; calcium channel; cytomatrix; RIM; scaffold; synaptic vesicle

Indexed keywords

BINDING PROTEIN; CALCIUM CHANNEL N TYPE; MUNC 13 PROTEIN; RAB3 INTERACTING MOLECULE; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; AVIAN PROTEIN; CACNA1B PROTEIN, MOUSE; GUANINE NUCLEOTIDE BINDING PROTEIN; RAB PROTEIN;

ANIMAL TISSUE; ARTICLE; CILIARY GANGLION; CONTROLLED STUDY; CORRELATION ANALYSIS; EMBRYO; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; SYNAPSE; SYNAPTOSOME; ANIMAL; BRAIN; CHEMISTRY; CHICK EMBRYO; COMPARATIVE STUDY; METABOLISM; SECRETION;

ANIMALS; AVIAN PROTEINS; BRAIN; CALCIUM CHANNELS, N-TYPE; CHICK EMBRYO; GTP-BINDING PROTEINS; NEUROTRANSMITTER AGENTS; PRESYNAPTIC TERMINALS; RAB3A GTP-BINDING PROTEIN; SYNAPTOSOMES;

EID: 33745662597     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2006.04.053     Document Type: Article

References (40)

1. Betz A., Thakur P., Junge H.J., Ashery U., Rhee J.S., Scheuss V., Rosenmund C., Rettig J., and Brose N. Functional interaction of the active zone proteins Munc13-1 and RIM1 in synaptic vesicle priming. Neuron 30 (2001) 183-196
2. Calakos N., Schoch S., Sudhof T.C., and Malenka R.C. Multiple roles for the active zone protein RIM1alpha in late stages of neurotransmitter release. Neuron 42 (2004) 889-896
3. Coppola T., Magnin-Luthi S., Perret-Menoud V., Gattesco S., Schiavo G., and Regazzi R. Direct interaction of the Rab3 effector RIM with Ca2+ channels, SNAP-25, and synaptotagmin. J Biol Chem 276 (2001) 32756-32762
4. Dulubova I., Lou X., Lu J., Huryeva I., Alam A., Schneggenburger R., Sudhof T.C., and Rizo J. A Munc13/RIM/Rab3 tripartite complex. from priming to plasticity?. EMBO J 24 (2005) 2839-2850
5. Gentile L., and Stanley E.F. A unified model of presynaptic release site gating by calcium channel domains. Eur J Neurosci 21 (2005) 278-282
6. Haydon P.G., Henderson E., and Stanley E.F. Localization of individual calcium channels at the release face of a presynaptic nerve terminal. Neuron 13 (1994) 1275-1280
7. Heuser J.E., Reese T.S., and Landis D.M.D. Functional changes in frog neuromuscular junctions studied with freeze fracture. J Neurocytol 3 (1974) 109-131
8. Hibino H., Pironkova R., Onwumere O., Vologodskaia M., Hudspeth A.J., and Lesage F. RIM binding proteins (RBPs) couple Rab3-interacting molecules (RIMs) to voltage-gated Ca(2+) channels. Neuron 34 (2002) 411-423
9. Huttner W.B., Schiebler W., Greengard P., and De C.P. Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J Cell Biol 96 (1983) 1374-1388
10. Kaeser P.S., and Sudhof T.C. RIM function in short- and long-term synaptic plasticity. Biochem Soc Trans 33 (2005) 1345-1349
11. Khanna R., Sun L., Li Q., Guo L., and Stanley E.F. Long splice variant N type calcium channels are clustered at presynaptic transmitter release sites without modular adaptor proteins. Neuroscience 138 (2006) 1115-1125
12. Koushika S.P., Richmond J.E., Hadwiger G., Weimer R.M., Jorgensen E.M., and Nonet M.L. A post-docking role for active zone protein Rim. Nat Neurosci 4 (2001) 997-1005
13. Li Q., Lau A., Morris T.J., Guo L., Fordyce C.B., and Stanley E.F. A syntaxin 1, Galpha(o), and N-type calcium channel complex at a presynaptic nerve terminal. analysis by quantitative immunocolocalization. J Neurosci 24 (2004) 4070-4081
14. Llinas R., Sugimori M., and Silver R.B. Microdomains of high calcium concentration in a presynaptic terminal. Science 256 (1992) 677-679
15. Llinas R.R., Steinberg I.Z., and Walton K. Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse. Biophys J 33 (1981) 323-351
16. Maximov A., and Bezprozvanny I. Synaptic targeting of N-type calcium channels in hippocampal neurons. J Neurosci 22 (2002) 6939-6952
17. Mirotznik R.R., Zheng X., and Stanley E.F. G-protein types involved in calcium channel inhibition at a presynaptic nerve terminal. J Neurosci 20 (2000) 7614-7621
18. Morris T.J., and Stanley E.F. A simple method for immunocytochemical staining with multiple rabbit polyclonal antibodies. J Neurosci Methods 127 (2003) 149-155
19. Nishimune H., Sanes J.R., and Carlson S.S. A synaptic laminin-calcium channel interaction organizes active zones in motor nerve terminals. Nature (Lond) 432 (2004) 580-587
20. Photowala H., Freed R., and Alford S. Location and function of vesicle clusters, active zones and Ca2+ channels in the lamprey presynaptic terminal. J Physiol 569 Pt1 (2005) 119-135
21. Pumplin D.W., Reese T.S., and Llinas R. Are the presynaptic membrane particles the calcium channels?. Proc Natl Acad Sci U S A 78 (1981) 7210-7213
22. Robitaille R., Adler E.M., and Charlton M.P. Strategic location of calcium channels at transmitter release sites of frog neuromuscular synapses. Neuron 5 (1990) 773-779
23. Schoch S., Castillo P.E., Jo T., Mukherjee K., Geppert M., Wang Y., Schmitz F., Malenka R.C., and Sudhof T.C. RIM1alpha forms a protein scaffold for regulating neurotransmitter release at the active zone. Nature (Lond) 415 (2002) 321-326
24. Smith S.J., Buchanan J., Osses L.R., Charlton M.P., and Augustine G.J. The spatial distribution of calcium signals in squid presynaptic terminals. J Physiol (Lond) 472 (1993) 573-593
25. Stanley E.F. Calcium currents in a vertebrate presynaptic nerve terminal. the chick ciliary ganglion calyx. Brain Res 505 (1989) 341-345
26. Stanley E.F. Single calcium channels on a cholinergic presynaptic nerve terminal. Neuron 7 (1991) 585-591
27. Stanley E.F. The calcium channel and the organization of the presynaptic transmitter release face. Trends Neurosci 20 (1997) 404-409
28. Stanley E.F., and Atrakchi A.H. Calcium currents recorded from a vertebrate presynaptic nerve terminal are resistant to the dihydropyridine nifedipine. Proc Natl Acad Sci U S A 87 (1990) 9683-9687
29. Stanley E.F., and Goping G. Characterization of a calcium current in a vertebrate cholinergic presynaptic nerve terminal. J Neurosci 11 (1991) 985-993
30. Stanley E.F., and Mirotznik R.R. Cleavage of syntaxin prevents G-protein regulation of presynaptic calcium channels. Nature (Lond) 385 (1997) 340-343
31. Sudhof T.C. The synaptic vesicle cycle. Annu Rev Neurosci 27 (2004) 509-547
32. 2+ channel clusters persist at isolated presynaptic terminals. Eur J Neurosci 23 (2006) 1391-1396
33. Sun X.P., and Stanley E.F. An ATP-activated, ligand gated ion channel on a cholinergic presynaptic nerve terminal. Proc Natl Acad Sci U S A 93 (1996) 1859-1863
34. Wachman E.S., Poage R.E., Stiles J.R., Farkas D.L., and Meriney S.D. Spatial distribution of calcium entry evoked by single action potentials within the presynaptic active zone. J Neurosci 24 (2004) 2877-2885
35. Wang Y., Liu X., Biederer T., and Sudhof T.C. A family of RIM-binding proteins regulated by alternative splicing. Implications for the genesis of synaptic active zones. Proc Natl Acad Sci U S A 99 (2002) 14464-14469
36. Wang Y., Okamoto M., Schmitz F., Hofmann K., and Südhof T.C. Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion. Nature (Lond) 388 (1997) 593-598
37. Wang Y., and Sudhof T.C. Genomic definition of RIM proteins. evolutionary amplification of a family of synaptic regulatory proteins (small star, filled). Genomics 81 (2003) 126-137
38. Wang Y., Sugita S., and Sudhof T.C. The RIM/NIM family of neuronal C2 domain proteins. Interactions with Rab3 and a new class of Src homology 3 domain proteins. J Biol Chem 275 (2000) 20033-20044
39. Yawo H., and Chuhma N. omega-Conotoxin-sensitive and -resistant transmitter release from the chick ciliary presynaptic terminal. J Physiol (Lond) 477 (1994) 437-448
40. Zhai R.G., and Bellen H.J. The architecture of the active zone in the presynaptic nerve terminal. Physiology (Bethesda) 19 (2004) 262-270