A novel fast mechanism for GPCR-mediated signal transduction - Control of neurotransmitter release

Journal of Cell Biology

Volumn 192, Issue 1, 2011, Pages 137-151

  Kupchik, Yonatan M ^a   Barchad Avitzur, Ofra ^a   Wess, Jürgen ^b   Ben Chaim, Yair ^a,c   Parnas, Itzchak ^a   Parnas, Hanna ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; CADMIUM; CALCIUM ION; CARBACHOL; G PROTEIN COUPLED RECEPTOR; MAGNESIUM ION; MUSCARINIC M2 RECEPTOR; NEUROTRANSMITTER; TETRODOTOXIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CURRENT; CALCIUM TRANSPORT; CONTROLLED STUDY; MOUSE; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; OOCYTE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VOLTAGE CLAMP; XENOPUS;

ACETYLCHOLINE; ALLOSTERIC REGULATION; ANIMALS; CALCIUM; CALCIUM SIGNALING; CARBACHOL; EXCITATORY POSTSYNAPTIC POTENTIALS; GALLAMINE TRIETHIODIDE; ION CHANNEL GATING; MICE; NEUROTRANSMITTER AGENTS; OOCYTES; PHOTOLYSIS; RECEPTOR, MUSCARINIC M2; SIGNAL TRANSDUCTION; TIME FACTORS; XENOPUS;

EID: 78651335929     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201007053     Document Type: Article

References (62)

1. Andreu, R., and E.F. Barrett. 1980. Calcium dependence of evoked transmitter release at very low quantal contents at the frog neuromuscular junction. J. Physiol. 308:79-97.
2. Ben-Chaim, Y., O. Tour, N. Dascal, I. Parnas, and H. Parnas. 2003. The M2 muscarinic G-protein-coupled receptor is voltage-sensitive. J. Biol. Chem. 278:22482-22491. doi:10.1074/jbc.M301146200
3. Ben-Chaim, Y., B. Chanda, N. Dascal, F. Bezanilla, I. Parnas, and H. Parnas. 2006. Movement of 'gating charge' is coupled to ligand binding in a G-protein-coupled receptor. Nature. 444:106-109. doi:10.1038/nature05259
4. Bezanilla, F., and C.M. Armstrong. 1977. Inactivation of the sodium channel. I. Sodium current experiments. J. Gen. Physiol. 70:549-566. doi:10.1085/jgp.70.5.549 (Pubitemid 8239321)
5. Blackmer, T., E.C. Larsen, C. Bartleson, J.A. Kowalchyk, E.J. Yoon, A.M. Preininger, S. Alford, H.E. Hamm, and T.F. Martin. 2005. G protein beta-gamma directly regulates SNARE protein fusion machinery for secretory granule exocytosis. Nat. Neurosci. 8:421-425.
6. Bollmann, J.H., and B. Sakmann. 2005. Control of synaptic strength and timing by the release-site Ca2+ signal. Nat. Neurosci. 8:426-434.
7. Bollmann, J.H., B. Sakmann, and J.G. Borst. 2000. Calcium sensitivity of glutamate release in a calyx-type terminal. Science. 289:953-957. doi:10.1126/science.289.5481.953
8. Brigant, J.L., and A. Mallart. 1982. Presynaptic currents in mouse motor endings. J. Physiol. 333:619-636.
9. Calakos, N., and R.H. Scheller. 1996. Synaptic vesicle biogenesis, docking, and fusion: a molecular description. Physiol. Rev. 76:1-29.
10. Conn, P.J., A. Christopoulos, and C.W. Lindsley. 2009. Allosteric modulators of GPCRs: a novel approach for the treatment of CNS disorders. Nat. Rev. Drug Discov. 8:41-54. doi:10.1038/nrd2760
11. Daeffler, L., A. Chahdi, J.P. Gies, and Y. Landry. 1999. Inhibition of GTPase activity of Gi proteins and decreased agonist affinity at M2 muscarinic acetylcholine receptors by spermine and methoctramine. Br. J. Pharmacol. 127:1021-1029. doi:10.1038/sj.bjp.0702625
12. Dascal, N. 1997. Signalling via the G protein-activated K+ channels. Cell. Signal. 9:551-573. doi:10.1016/S0898-6568(97)00095-8
13. Dascal, N., and I. Lotan. 1992. Expression of exogenous ion channels and neurotransmitter receptors in RNA-injected Xenopus oocytes. In Methods in Molecular Neurobiology. A. Longstaff and P. Revest, editors. Humana Press, Totowa, NJ. 205-225.
14. Datyner, N.B., and P.W. Gage. 1980. Phasic secretion of acetylcholine at a mammalian neuromuscular junction. J. Physiol. 303:299-314.
15. Del Castillo, J., and B. Katz. 1954. The effect of magnesium on the activity of motor nerve endings. J. Physiol. 124:553-559.
16. Dodge, F.A. Jr., and R. Rahamimoff. 1967. Co-operative action a calcium ions in transmitter release at the neuromuscular junction. J. Physiol. 193:419-432.
17. Dolphin, A.C. 1998. Mechanisms of modulation of voltage-dependent calcium channels by G proteins. J. Physiol. 506:3-11. doi:10.1111/j.1469-7793.1998. 003bx.x
18. Dudel, J. 1981. The effect of reduced calcium on quantal unit current and release at the crayfish neuromuscular junction. Pflugers Arch. 391:35-40. doi:10.1007/BF00580691
19. Dudel, J. 1990. Inhibition of Ca2+ inflow at nerve terminals of frog muscle blocks facilitation while phasic transmitter release is still considerable. Pflugers Arch. 415:566-574. doi:10.1007/BF02583507
20. Felmy, F., E. Neher, and R. Schneggenburger. 2003a. Probing the intracellular calcium sensitivity of transmitter release during synaptic facilitation. Neuron. 37:801-811. doi:10.1016/S0896-6273(03)00085-0
21. Felmy, F., E. Neher, and R. Schneggenburger. 2003b. The timing of phasic transmitter release is Ca2+-dependent and lacks a direct influence of presynaptic membrane potential. Proc. Natl. Acad. Sci. USA. 100:15200-15205. doi:10.1073/pnas.2433276100
22. Gether, U. 2000. Uncovering molecular mechanisms involved in activation of G protein-coupled receptors. Endocr. Rev. 21:90-113. doi:10.1210/er.21.1.90
23. Gomeza, J., H. Shannon, E. Kostenis, C. Felder, L. Zhang, J. Brodkin, A. Grinberg, H. Sheng, and J. Wess. 1999. Pronounced pharmacologic deficits in M2 muscarinic acetylcholine receptor knockout mice. Proc. Natl. Acad. Sci. USA. 96:1692-1697. doi:10.1073/pnas.96.4.1692
24. Gregory, K.J., P.M. Sexton, and A. Christopoulos. 2007. Allosteric modulation of muscarinic acetylcholine receptors. Curr. Neuropharmacol. 5:157-167. doi:10.2174/157015907781695946
25. Hamm, H.E. 1998. The many faces of G protein signaling. J. Biol. Chem. 273:669-672. doi:10.1074/jbc.273.2.669
26. Hochner, B., H. Parnas, and I. Parnas. 1991. Effects of intra-axonal injection of Ca2+ buffers on evoked release and on facilitation in the crayfish neuromuscular junction. Neurosci. Lett. 125:215-218. doi:10.1016/0304-3940(91) 90032-O
27. Ilouz, N., L. Branski, J. Parnis, H. Parnas, and M. Linial. 1999. Depolarization affects the binding properties of muscarinic acetylcholine receptors and their interaction with proteins of the exocytic apparatus. J. Biol. Chem. 274:29519-29528. doi:10.1074/jbc.274.41.29519
28. Jakubík, J., L. Bacáková, V. Lisá, E.E. el-Fakahany, and S. Tucek. 1996. Activation of muscarinic acetylcholine receptors via their allosteric binding sites. Proc. Natl. Acad. Sci. USA. 93:8705-8709. doi:10.1073/pnas.93.16.8705
29. Katz, B., and R. Miledi. 1965. The measurement of synaptic delay, and the time course of acetylcholine release at the neuromuscular junction. Proc. R. Soc. Lond., B, Biol. Sci. 161:483-495. doi:10.1098/rspb.1965.0016
30. Katz, B., and R. Miledi. 1978. A re-examination of curare action at the motor endplate. Proc. R. Soc. Lond., B, Biol. Sci. 203:119-133. doi:10.1098/rspb.1978.0096
31. Kew, J.N.C., J.M. Ducarre, M.C. Pflimlin, V. Mutel, and J.A. Kemp. 2001. Activity-dependent presynaptic autoinhibition by group II metabotropic glutamate receptors at the perforant path inputs to the dentate gyrus and CA1. Neuropharmacology. 40:20-27. doi:10.1016/S0028-3908(00)00118-0
32. Khanin, R., H. Parnas, and L. Segel. 1997. "First step" negative feedback accounts for inhibition of fast neurotransmitter release. J. Theor. Biol. 188:261-276. doi:10.1006/jtbi.1997.0480
33. Kupchik, Y.M., G. Rashkovan, L. Ohana, T. Keren-Raifman, N. Dascal, H. Parnas, and I. Parnas. 2008. Molecular mechanisms that control initiation and termination of physiological depolarization-evoked transmitter release. Proc. Natl. Acad. Sci. USA. 105:4435-4440. doi:10.1073/pnas.0708540105
34. Lee, N.H., and E.E. el-Fakahany. 1991. Allosteric antagonists of the muscarinic acetylcholine receptor. Biochem. Pharmacol. 42:199-205. doi:10.1016/0006-2952(91)90703-8
35. Linial, M., N. Ilouz, and H. Parnas. 1997. Voltage-dependent interaction between the muscarinic ACh receptor and proteins of the exocytic machinery. J. Physiol. 504:251-258. doi:10.1111/j.1469-7793.1997.251be.x
36. Llinás, R., I.Z. Steinberg, and K. Walton. 1981. Presynaptic calcium currents in squid giant synapse. Biophys. J. 33:289-321. doi:10.1016/S0006-3495(81)84898-9
37. Loiacono, R., J. Stephenson, J. Stevenson, and F. Mitchelson. 1993. Multiple binding sites for nicotine receptor antagonists in inhibiting [3H](-)-nicotine binding in rat cortex. Neuropharmacology. 32:847-853. doi:10.1016/0028-3908(93)90139-T
38. Lustig, C., H. Parnas, and L.A. Segel. 1989. Neurotransmitter release: development of a theory for total release based on kinetics. J. Theor. Biol. 136:151-170. doi:10.1016/S0022-5193(89)80222-X
39. Martin, A.R. 1966. Quantal nature of synaptic transmission. Physiol. Rev. 46:51.
40. Milburn, T., N. Matsubara, A.P. Billington, J.B. Udgaonkar, J.W. Walker, B.K. Carpenter, W.W. Webb, J. Marque, W. Denk, J.A. McCray, et al. 1989. Synthesis, photochemistry, and biological activity of a caged photolabile acetylcholine receptor ligand. Biochemistry. 28:49-55. doi:10.1021/bi00427a008
41. Mitchelson, F. 1988. Muscarinic receptor differentiation. Pharmacol. Ther. 37:357-423. doi:10.1016/0163-7258(88)90005-8
42. Murthy, V.N., and P. De Camilli. 2003. Cell biology of the presynaptic terminal. Annu. Rev. Neurosci. 26:701-728. doi:10.1146/annurev.neuro.26.041002. 131445
43. Neher, E., and T. Sakaba. 2008. Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron. 59:861-872. doi:10.1016/j. neuron.2008.08.019
44. Ohana, L., O. Barchad, I. Parnas, and H. Parnas. 2006. The metabotropic glutamate G-protein-coupled receptors mGluR3 and mGluR1a are voltage-sensitive. J. Biol. Chem. 281:24204-24215. doi:10.1074/jbc.M513447200
45. Pan, B., and R.S. Zucker. 2009. A general model of synaptic transmission and short-term plasticity. Neuron. 62:539-554. doi:10.1016/j.neuron.2009.03.025
46. Parnas, H., and I. Parnas. 2007. The chemical synapse goes electric: Ca2+- and voltage-sensitive GPCRs control neurotransmitter release. Trends Neurosci. 30:54-61. doi:10.1016/j.tins.2006.12.001
47. Parnas, I., and H. Parnas. 2010. Control of neurotransmitter release: From Ca2+ to voltage dependent G-protein coupled receptors. Pflugers Arch. 460:975-990. doi:10.1007/s00424-010-0872-7
48. Parnas, H., L. Segel, J. Dudel, and I. Parnas. 2000. Autoreceptors, membrane potential and the regulation of transmitter release. Trends Neurosci. 23:60-68. doi:10.1016/S0166-2236(99)01498-8
49. Parnas, H., J.C. Valle-Lisboa, and L.A. Segel. 2002. Can the Ca2+ hypothesis and the Ca2+-voltage hypothesis for neurotransmitter release be reconciled? Proc. Natl. Acad. Sci. USA. 99:17149-17154. doi:10.1073/pnas. 242549999
50. Parnas, H., I. Slutsky, G. Rashkovan, I. Silman, J. Wess, and I. Parnas. 2005. Depolarization initiates phasic acetylcholine release by relief of a tonic block imposed by presynaptic M2 muscarinic receptors. J. Neurophysiol. 93:3257-3269. doi:10.1152/jn.01131.2004
51. Peleg, S., D. Varon, T. Ivanina, C.W. Dessauer, and N. Dascal. 2002. G(alpha)(i) controls the gating of the G protein-activated K(+) channel, GIRK. Neuron. 33:87-99. doi:10.1016/S0896-6273(01)00567-0
52. Schneggenburger, R., and E. Neher. 2000. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature. 406:889-893. doi:10.1038/35022702
53. Schneggenburger, R., and E. Neher. 2005. Presynaptic calcium and control of vesicle fusion. Curr. Opin. Neurobiol. 15:266-274. doi:10.1016/j.conb.2005. 05.006
54. Slutsky, I., H. Parnas, and I. Parnas. 1999. Presynaptic effects of muscarine on ACh release at the frog neuromuscular junction. J. Physiol. 514:769-782. doi:10.1111/j.1469-7793.1999.769ad.x
55. Slutsky, I., I. Silman, I. Parnas, and H. Parnas. 2001. Presynaptic M(2) muscarinic receptors are involved in controlling the kinetics of ACh release at the frog neuromuscular junction. J. Physiol. 536:717-725. doi:10.1111/j.1469- 7793.2001.00717.x
56. Slutsky, I., G. Rashkovan, H. Parnas, and I. Parnas. 2002. Ca2+-independent feedback inhibition of acetylcholine release in frog neuromuscular junction. J. Neurosci. 22:3426-3433.
57. Slutsky, I., J. Wess, J. Gomeza, J. Dudel, I. Parnas, and H. Parnas. 2003. Use of knockout mice reveals involvement of M2-muscarinic receptors in control of the kinetics of acetylcholine release. J. Neurophysiol. 89:1954-1967. doi:10.1152/jn.00668.2002
58. Stefani, E., and F. Bezanilla. 1998. Cut-open oocyte voltage-clamp technique. Methods Enzymol. 293:300-318. doi:10.1016/S0076-6879(98)93020-8
59. Sudhof, T.C. 2004. The synaptic vesicle cycle. Annu. Rev. Neurosci. 27:509-547. doi:10.1146/annurev.neuro.26.041002.131412
60. Wonnacott, S. 1997. Presynaptic nicotinic ACh receptors. Trends Neurosci. 20:92-98. doi:10.1016/S0166-2236(96)10073-4
61. Yusim, K., H. Parnas, and L. Segel. 1999. Theory of fast neurotransmitter release control based on voltage-dependent interaction between autoreceptors and proteins of the exocytotic machinery. Bull. Math. Biol. 61:701-725. doi:10.1006/bulm.1999.0107
62. Zohar, A., N. Dekel, B. Rubinsky, and H. Parnas. 2010. New mechanism for voltage induced charge movement revealed in GPCRs - theory and experiments. PLoS One. 5:e8752. doi:10.1371/journal.pone.0008752