CAMP modulates intracellular Ca2+ sensitivity of fast-releasing synaptic vesicles at the calyx of held synapse

Journal of Neurophysiology

Volumn 104, Issue 6, 2010, Pages 3250-3260

  Yao, Lijun ^a   Sakaba, Takeshi ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALCIUM CHANNEL; CYCLIC AMP; FORSKOLIN;

ALLOSTERISM; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CALCIUM CELL LEVEL; DEPOLARIZATION; NEUROTRANSMITTER RELEASE; NONHUMAN; PATCH CLAMP; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; SYNAPSE VESICLE;

1-METHYL-3-ISOBUTYLXANTHINE; ACTION POTENTIALS; ALLOSTERIC REGULATION; ANIMALS; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; COCHLEAR NUCLEUS; CYCLIC AMP; EGTAZIC ACID; EXCITATORY POSTSYNAPTIC POTENTIALS; FORSKOLIN; PATCH-CLAMP TECHNIQUES; PHOTOLYSIS; RATS; RATS, WISTAR; SECOND MESSENGER SYSTEMS; SYNAPTIC VESICLES;

EID: 78650883826     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00685.2010     Document Type: Article

References (50)

1. Bailey CH, Bartsch D, Kandel ER. Toward a molecular definition of long-term memory storage. Proc Natl Acad Sci USA 93: 13445-13452, 1996.
2. Barnes-Davies M, Forsythe ID. Pre- and postsynaptic glutamate receptors at a giant excitatory synapse in rat auditory brain stem slices. J Physiol 488: 387-406, 1995.
3. Basu J, Betz A, Brose N, Rosenmund C. Munc13-1 C1 domain activation lowers the energy barrier for synaptic vesicle fusion. J Neurosci 27: 1200-1210, 2007.
4. Beaumont V, Zucker RS. Enhancement of synaptic transmission by cyclic AMP modulation of presynaptic Ih channels. Nat Neurosci 3: 133-141, 2000.
5. Betz A, Thakur P, Junge HJ, Ashery U, Rhee JS, Scheuss V, Rosenmund C, Rettig J, Brose N. Functional interaction of the active zone proteins Munc13-1 and RIM1 in synaptic vesicle priming. Neuron 30: 183-196, 2001.
6. Bollmann JH, Sakmann B, Borst JG. Calcium sensitivity of glutamate release in a calyx-type terminal. Science 289: 953-957, 2000.
7. Borst JG, Sakmann B. Calcium influx and transmitter release in a fast CNS synapse. Nature 383: 431-434, 1996.
8. Byrne JH, Kandel ER. Presynaptic facilitation revisited: State and time dependence. J Neurosci 16: 425-435, 1996.
9. Capogna M, Gahwiler BH, Thompson SM. Presynaptic enhancement of inhibitory synaptic transmission by protein kinases A and C in the rat hippocampus in vitro. J Neurosci 15: 1249-1260, 1995.
10. Chavez-Noriega LE, Stevens CF. Increased transmitter release at excitatory synapses produced by direct activation of adenylate cyclase in rat hippocampal slices. J Neurosci 14: 310-317, 1994.
11. Chen C, Regehr WG. The mechanism of cAMP-mediated enhancement at a cerebellar synapse. J Neurosci 17: 8687-8694, 1997.
12. Eliasson L, Ma X, Renstrom E, Barg S, Berggren PO, Galvanovskis J, Gromada J, Jing X, Lundquist I, Salehi A, Sewing S, Rorsman P. SUR1 regulates PKA-independent cAMP-induced granule priming in mouse pancreatic B-cells. J Gen Physiol 121: 181-197, 2003.
13. Forsythe ID. Direct patch recording from identified presynaptic terminals mediating glutamatergic EPSCs in the rat CNS, in vitro. J Physiol 479: 381-387, 1994.
14. Gekel I, Neher E. Application of an Epac activator enhances neurotransmitter release at excitatory central synapses. J Neurosci 28: 7991-8002, 2008.
15. Goy MF, Kravitz EA. Cyclic AMP only partially mediates the actions of serotonin at lobster neuromuscular junctions. J Neurosci 9: 369-379, 1989.
16. 2+. Biophys J 67: 2546-2557, 1994.
17. Hori T, Takai Y, Takahashi T. Presynaptic mechanism for phorbol esterinduced synaptic potentiation. J Neurosci 19: 7262-7267, 1999.
18. Hosoi N, Sakaba T, Neher E. Quantitative analysis of calcium-dependent vesicle recruitment and it's functional role of the calyx of Held synapse. J Neurosci 27: 14286-14298, 2007.
19. Kaneko M, Takahashi T. Presynaptic mechanism underlying cAMP-dependent synaptic potentiation. J Neurosci 24: 5202-5208, 2004.
20. Kashima Y, Miki T, Shibasaki T, Ozaki N, Miyazaki M, Yano H, Seino S. Critical role of cAMP-GEFII-Rim2 complex in incretin-potentiated insulin secretion. J Biol Chem 276: 46046-46053, 2001.
21. Kondo S, Marty A. Protein kinase A-mediated enhancement of miniature IPSC frequency by noradrenaline in rat cerebellar stellate cells. J Physiol 498: 165-176, 1997.
22. 2+ chelators. J Neurophysiol 72: 825-830, 1994.
23. Llano I, Gerschenfeld HM. Beta-adrenergic enhancement of inhibitory synaptic activity in rat cerebellar stellate and Purkinje cells. J Physiol 468: 201-224, 1993.
24. 2+ sensor for vesicle fusion. Nature 435: 497-501, 2005.
25. 2+ and short-term facilitation. J Neurosci 27: 2261-2271, 2007.
26. Müller M, Goutman JD, Kochubey O, Schneggenburger R. Interaction between facilitation and depression at a large CNS synapse reveals mechanisms of short-term plasticity. J Neurosci 30: 2007-2016, 2010.
27. Neher E, Sakaba T. Combining deconvolution and noise analysis for the estimation of transmitter release rates at the calyx of held. J Neurosci 21: 444-461, 2001a.
28. Neher E, Sakaba T. Estimating transmitter release rates from postsynaptic current fluctuations. J Neurosci 21: 9638-9654, 2001b.
29. Neher E, Sakaba T. Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 59: 861-872, 2008.
30. Ozaki N, Shibasaki T, Kashima Y, Miki T, Takahashi K, Ueno H, Sunaga Y, Yano H, Matsuura Y, Iwanaga T, Takai Y, Seino S. cAMP-GEFII is a direct target of cAMP in regulated exocytosis. Nature cell biology 2: 805-811, 2000.
31. Rhee JS, Betz A, Pyott S, Reim K, Varoqueaux F, Augustin I, Hesse D, Sudhof TC, Takahashi M, Rosenmund C, Brose N. Beta phorbol esterand diacylglycerol-induced augmentation of transmitter release is mediated by Munc13s and not by PKCs. Cell 108: 121-133, 2002.
32. Sakaba T. Roles of the fast-releasing and the slowly releasing vesicles in synaptic transmission at the calyx of held. J Neurosci 26: 5863-5871, 2006.
33. Sakaba T, Neher E. Calmodulin mediates rapid recruitment of fast-releasing synaptic vesicles at a calyx-type synapse. Neuron 32: 1119-1131, 2001a.
34. Sakaba T, Neher E. Preferential potentiation of fast-releasing synaptic vesicles by cAMP at the calyx of Held. Proc Natl Acad Sci USA 98: 331-336, 2001b.
35. Sakaba T, Neher E. Quantitative relationship between transmitter release and calcium current at the calyx of held synapse. J Neurosci 21: 462-476, 2001c.
36. Sakaba T, Neher E. Direct modulation of synaptic vesicle priming by GABA(B) receptor activation at a glutamatergic synapse. Nature 424: 775-778, 2003.
37. Schlüter OM, Basu J, Sudhof TC, Rosenmund C. Rab3 superprimes synaptic vesicles for release: Implications for short-term synaptic plasticity. J Neurosci 26: 1239-1246, 2006.
38. Schneggenburger R, Meyer AC, Neher E. Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 23: 399-409, 1999.
39. Schneggenburger R, Neher E. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406: 889-893, 2000.
40. Schneggenburger R, Neher E. Presynaptic calcium and control of vesicle fusion. Curr Opin Neurobiol 15: 266-274, 2005.
41. Silinsky EM, Searl TJ. Phorbol esters and neurotransmitter release: More than just protein kinase C? Br J Pharmacol 138: 1191-1201, 2003.
42. Silva AJ, Kogan JH, Frankland PW, Kida S. CREB and memory. Annu Rev Neurosci 21: 127-148, 1998.
43. 2+- sensor model for neurotransmitter release in a central synapse. Nature 450: 676-682, 2007.
44. Trudeau LE, Emery DG, Haydon PG. Direct modulation of the secretory machinery underlies PKA-dependent synaptic facilitation in hippocampal neurons. Neuron 17: 789-797, 1996.
45. 2+ channels determines fast neurotransmitter release. Neuron 53: 563-575, 2007.
46. Weisskopf MG, Castillo PE, Zalutsky RA, Nicoll RA. Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP. Science 65: 1878-1882, 1994.
47. Wölfel M, Lou X, Schneggenburger R. A mechanism intrinsic to the vesicle fusion machinery determines fast and slow transmitter release at a large CNS synapse. J Neurosci 27: 3198-3210, 2007.
48. Wu LG, Borst JG. The reduced release probability of releasable vesicles during recovery from short-term synaptic depression. Neuron 23: 821-832, 1999.
49. 2+ sensor for spontaneous release. Nat Neurosci 12: 759-766, 2009.
50. Zucker RS, Regehr WG. Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405, 2002.