Gβγ interferes with Ca2+-dependent binding of synaptotagmin to the soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) complex

Molecular Pharmacology

Volumn 72, Issue 5, 2007, Pages 1210-1219

  Yoon, Eun Ja ^a   Gerachshenko, Tatyana ^b   Spiegelberg, Bryan D ^a   Alford, Simon ^b   Hamm, Heidi E ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN BETA GAMMA SUBUNIT; SEROTONIN; SNARE PROTEIN; SYNAPTOTAGMIN; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; CALCIUM; G PROTEIN BETA GAMMA; G-PROTEIN BETA GAMMA; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN GAMMA SUBUNIT; SYNAPTOBREVIN 2; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNAPTOTAGMIN I; SYNTAXIN 1;

ARTICLE; DRUG INHIBITION; EXOCYTOSIS; NEUROTRANSMISSION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; ANIMAL; CATTLE; DRUG EFFECT; GENETICS; LAMPREY; METABOLISM; SPINAL CORD; SYNAPSE;

ANIMALS; CALCIUM; CATTLE; EXOCYTOSIS; GTP-BINDING PROTEIN BETA SUBUNITS; GTP-BINDING PROTEIN GAMMA SUBUNITS; LAMPREYS; SEROTONIN; SNARE PROTEINS; SPINAL CORD; SYNAPSES; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25; SYNAPTOTAGMIN I; SYNTAXIN 1; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2;

EID: 35548980544     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.107.039446     Document Type: Article

References (40)

1. Adler EM, Augustine GJ, Duffy SN, and Charlton MP (1991) Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse. J Neurosci 11:1496-1507.
2. Bai J, Wang CT, Richards DA, Jackson MB, and Chapman ER (2004) Fusion pore dynamics are regulated by synaptotagmin*t-SNARE interactions. Neuron 41:929-942.
3. Bennett MK, Calakos N, and Scheller RH (1992) Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science 257:255-259.
4. Blackmer T, Larsen EC, Bartleson C, Kowalchyk JA, Yoon EJ, Preininger AM, Alford S, Hamm HE, and Martin TF (2005) G protein betagamma directly regulates SNARE protein fusion machinery for secretory granule exocytosis. Nat Neurosci 8:421-425.
5. 2+ entry. Science 292:293-297.
6. Blanton MG, Lo Turco JJ, and Kriegstein AR (1989) Whole cell recording from neurons in slices of reptilian and mammalian cerebral cortex. J Neurosci Methods 30:203-210.
7. 2+ regulates the interaction between synaptotagmin and syntaxin 1. J Biol Chem 270:23667-23671.
8. Chen XK, Wang LC, Zhou Y, Cai Q, Prakriya M, Duan KL, Sheng ZH, Lingle C, and Zhou Z (2005) Activation of GPCRs modulates quantal size in chromaffin cells through G(betagamma) and PKC. Nat Neurosci 8:1160-1168.
9. Chen YA, Scales SJ, Jagath JR, and Scheller RH (2001) A discontinuous SNAP-25 C-terminal coil supports exocytosis. J Biol Chem 276:28503-28508.
10. 2+ and drives membrane fusion. Cell 97:165-174.
11. Elhamdani A, Azizi F, and Artalejo CR (2006) Double patch clamp reveals that transient fusion (kiss-and-run) is a major mechanism of secretion in calf adrenal chromaffin cells: high calcium shifts the mechanism from kiss-and-run to complete fusion. J Neurosci 26:3030-3036.
12. Elhamdani A, Palfrey HC, and Artalejo CR (2001) Quantal size is dependent on stimulation frequency and calcium entry in calf chromaffin cells. Neuron 31:819-830.
13. Ferrer-Montiel AV, Gutierrez LM, Apland JP, Canaves JM, Gil A, Viniegra S, Biser JA, Adler M, and Montal M (1998) The 26-mer peptide released from SNAP-25 cleavage by botulinum neurotoxin E inhibits vesicle docking. FEBS Lett 435:84-88.
14. Fukuda M (2002) Vesicle-associated membrane protein-2/synaptobrevin binding to synaptotagmin I promotes O-glycosylation of synaptotagmin I. J Biol Chem 277:30351-30358.
15. Gerachshenko T, Blackmer T, Yoon EJ, Bartleson C, Hamm HE, and Alford S (2005) Gbetagamma acts at the C terminus of SNAP-25 to mediate presynaptic inhibition. Nat Neurosci 8:597-605.
16. 2+-dependent binding of synaptotagmin to SNARE complexes. J Biol Chem 275:6328-6336.
17. 2+-triggered exocytosis. J Cell Biol 172:281-293.
18. Harata NC, Choi S, Pyle JL, Aravanis AM, and Tsien RW (2006) Frequency-dependent kinetics and prevalence of kiss-and-run and reuse at hippocampal synapses studied with novel quenching methods. Neuron 49:243-256.
19. 2+ channels by G-protein beta gamma subunits. Nature 380:258-262, 1996.
20. Ikeda SR (1996) Voltage-dependent modulation of N-type calcium channels by G-protein beta gamma subunits. Nature 380:255-258.
21. Jarvis SE, Barr W, Feng ZP, Hamid J, and Zamponi GW (2002) Molecular determinants of syntaxin 1 modulation of N-type calcium channels. J Biol Chem 277:44399-44407.
22. Man-Son-Hing H, Zoran MJ, Lukowiak K, and Haydon PG(1989). A neuromodulator of synaptic transmission acts on the secretory apparatus as well as on ion channels. Nature 341:237-239.
23. Margittai M, Otto H, and Jahn R (1999) A stable interaction between syntaxin 1a and synaptobrevin 2 mediated by their transmembrane domains. FEBS Lett 446:40-44.
24. Maximov A and Sudhof TC (2005) Autonomous function of synaptotagmin 1 in triggering synchronous release independent of asynchronous release. Neuron 48:547-554.
25. Mazzoni MR, Malinski JA, and Hamm HE (1991) Structural analysis of rod GTP-binding protein, Gt. Limited proteolytic digestion pattern of Gt with four proteases defines monoclonal antibody epitope. J Biol Chem 266:14072-14081.
26. Morimoto T, Popov S, Buckley KM, and Poo MM (1995) Calcium-dependent transmitter secretion from fibroblasts: modulation by synaptotagmin I. Neuron 15:689-696.
27. Perin MS, Fried VA, Mignery GA, Jahn R, and Sudhof TC (1990) Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C. Nature 345:260-263.
28. Phillips WJ and Cerione RA (1991) Labeling of the beta gamma subunit complex of transducin with an environmentally sensitive cysteine reagent. Use of fluorescence spectroscopy to monitor transducin subunit interactions. J Biol Chem 266:11017-11024.
29. Photowala H, Blackmer T, Schwartz E, Hamm HE, and Alford S (2006) G protein beta{gamma}-subunits activated by serotonin mediate presynaptic inhibition by regulating vesicle fusion properties. Proc Natl Acad Sci U S A 103:4281-4286.
30. Rizo J, Chen X, and Arac D (2006) Unraveling the mechanisms of synaptotagmin and SNARE function in neurotransmitter release. Trends Cell Biol.
31. Schiavo G, Stenbeck G, Rothman JE, and Sollner TH (1997) Binding of the synaptic vesicle v-SNARE, synaptotagmin, to the plasma membrane t-SNARE, SNAP-25, can explain docked vesicles at neurotoxin-treated synapses. Proc Natl Acad Sci U S A 94:997-1001.
32. 2+-independent miniature endplate potentials by phorbol ester and adenosine in frog. Br J Pharmacol 145:954-962.
33. Silinsky EM (1984) On the mechanism by which adenosine receptor activation inhibits the release of acetylcholine from motor nerve endings. J Physiol 346:243-256.
34. Sollner T, Bennett MK, Whiteheart SW, Scheller RH, and Rothman JE (1993) A protein assembly disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75:409-418.
35. Sorensen JB, Wiederhold K, Muller EM, Milosevic I, Nagy G, de Groot BL, Grubmuller H, and Fasshauer D (2006) Sequential N- to C-terminal SNARE complex assembly drives priming and fusion of secretory vesicles. EMBO J 25:955-966.
36. Takahashi M, Freed R, Blackmer T, and Alford S (2001) Calcium influx-independent depression of transmitter release by 5-HT at lamprey spinal cord synapses. J Physiol 532:323-336.
37. 2+ triggers two sequential steps in regulated exocytosis in rat PC-12 cells: fusion pore opening and fusion pore dilation. J Physiol 570:295-307.
38. Wang CT, Grishanin R, Earles CA, Chang PY, Martin TF, Chapman ER, and Jackson MB (2001) Synaptotagmin modulation of fusion pore kinetics in regulated exocytosis of dense-core vesicles. Science 294:1111-1115.
39. Wickelgren WO (1977) Physiological and anatomical characteristics of reticulospinalneurones in lamprey. J Physiol 270:89-114.
40. Yoshihara M and Littleton JT (2002) Synaptotagmin I functions as a calcium sensor to synchronize neurotransmitter release. Neuron 36:897-908.