Presynaptic release probability and readily releasable pool size are regulated by two independent mechanisms during posttetanic potentiation at the calyx of held synapse

Journal of Neuroscience

Volumn 28, Issue 32, 2008, Pages 7945-7953

  Jae, Sung Lee ^a   Kim, Myoung Hwan ^a,b   Ho, Won Kyung ^a   Lee, Suk Ho ^a  

^a Seoul National University College of Medicine   (South Korea)

^b Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

Author keywords

Calyx of held; Mitochondria; Myosin light chain kinase; Posttetanic potentiation; Readily releasable pool; Residual calcium

Indexed keywords

1 (5 IODO 1 NAPHTHALENESULFONYL)HEXAHYDRO 1H 1,4 DIAZEPINE; 2 [1 (3 AMIDINOTHIOPROPYL) 1H INDOL 3 YL] 3 (1 METHYL 1H INDOL 3 YL)MALEIMIDE; AMPA RECEPTOR; BLEBBISTATIN; CALCIUM ION; CALMIDAZOLIUM; CHELERYTHRINE; CYCLOTHIAZIDE; GAMMA DEXTRO GLUTAMYLGLYCINE; KYNURENIC ACID; LIDOCAINE ETHOBROMIDE; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN KINASE INHIBITOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN KINASE C INHIBITOR; SODIUM ION; TETRAPHENYLPHOSPHONIUM; CALCIUM; CALCIUM CHANNEL BLOCKING AGENT; CATION; MYOSIN LIGHT CHAIN KINASE; ORGANOPHOSPHORUS COMPOUND; PROTEIN KINASE C; PROTEIN KINASE INHIBITOR; RU 360; RUTHENIUM DERIVATIVE; SODIUM;

ANIMAL TISSUE; ARTICLE; CALCIUM BINDING; CALCIUM TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVATION; MITOCHONDRION; NEUROTRANSMISSION; NONHUMAN; PATCH CLAMP; POST TETANIC POTENTIATION; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION; ANIMAL; BRAIN STEM; DRUG ANTAGONISM; DRUG EFFECT; ELECTROSTIMULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; IN VITRO STUDY; METABOLISM; PHYSIOLOGY; PROBABILITY; SPRAGUE DAWLEY RAT; SYNAPTOSOME;

ANIMALS; BRAIN STEM; CALCIUM; CALCIUM CHANNEL BLOCKERS; ELECTRIC STIMULATION; ENZYME ACTIVATION; EXCITATORY POSTSYNAPTIC POTENTIALS; MITOCHONDRIA; MYOSIN-LIGHT-CHAIN KINASE; ONIUM COMPOUNDS; ORGANOPHOSPHORUS COMPOUNDS; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; PROBABILITY; PROTEIN KINASE C; PROTEIN KINASE INHIBITORS; RATS; RATS, SPRAGUE-DAWLEY; RUTHENIUM COMPOUNDS; SODIUM;

EID: 51149114631     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2165-08.2008     Document Type: Article

References (44)

1. Aiuchi T, Matsunaga M, Nakaya K, Nakamura Y (1985) Effects of probes of membrane potential on metabolism in synaptosome. Biochim Biophys Acta 843:20-24.
2. Awatramani GB, Price GD, Trussell LO (2005) Modulation of transmitter release by presynaptic resting potential and background calcium levels. Neuron 48:109-121.
3. Billups B, Forsythe ID (2002) Presynaptic mitochondrial calcium sequestration influences transmission at mammalian central synapses. J Neurosci 22:5840-5847.
4. Delaney KR, Tank DW (1994) A quantitative measurement of the dependence of short-term synaptic enhancement on presynaptic residual calcium. J Neurosci 14:5885-5902.
5. Delaney KR, Zucker RS, Tank DW (1989) Calcium in motor nerve terminals associated with posttetanic potentiation. J Neurosci 9:3558-3567.
6. Felmy F, Neher E, Schneggenburger R (2003) Probing the intracellular calcium sensitivity of transmitter release during synaptic facilitation. Neuron 37:801-811.
7. García-Chacón LE, Nguyen KT, David G, Barrett EF (2006) Extrusion of Ca2+ from mouse motor terminal mitochondria via a Na+/Ca2+ exchanger increases post-tetanic evoked release. J Physiol 574:663-675.
8. Gopalakrishna R, Chen ZH, Gundimeda U (1995) Modifications of cysteine-rich regions in protein kinase C induced by oxidant tumor promoters and enzyme-specific inhibitors. Methods Enzymol 252:132-146.
9. Habets RLP, Borst JGG (2005) Post-tetanic potentiation in the rat calyx of Held synapse. J Physiol 564:173-187.
10. Habets RLP, Borst JGG (2006) An increase in calcium influx contributes to post-tetanic potentiation at the rat calyx of Held synapse. J Neurophysiol 96:2868-2876.
11. Habets RLP, Borst JGG (2007) Dynamics of the readily releasable pool during post-tetanic potentiation in the rat calyx of Held synapse. J Physiol 581:467-478.
12. Hosoi N, Sakaba T, Neher E (2007) Quantitative analysis of calcium-dependent vesicle recruitment and its functional role at the calyx of Held synapse. J Neurosci 27:14286-14298.
13. Ishikawa T, Takahashi T (2001) Mechanisms underlying presynaptic facilitatory effect of cyclothiazide at the calyx of Held of juvenile rats. J Physiol 533:423-431.
14. Joshi I, Yang Y-M, Wang L-Y (2007) Coincident activation of metabotropic glutamate receptors and NMDA receptors (NMDARs) downregulates perisynaptic/extrasynaptic NMDARs and enhances high-fidelity neurotransmission at the developing calyx of Held synapse. J Neurosci 27:9989-9999.
15. Kamiya H, Zucker RS (1994) Residual Ca2+ and short-term synaptic plasticity. Nature 371:603-606.
16. Kamm KE, Stull JT (2001) Dedicated myosin light chain kinases with diverse cellular functions. J Biol Chem 276:4527-4530.
17. 2+ clearance at the calyx of Held. J Neurosci 25:6057-6065.
18. Kirichok Y, Krapivinsky G, Clapham DE (2004) The mitochondrial calcium uniporter is a highly selective ion channel. Nature 427:360-364.
19. Kopp-Scheinpflug C, Lippe WR, Dörrscheidt GJ, Rübsamen R (2003) The medial nucleus of the trapezoid body in the gerbil is more than a relay: comparison of pre- and postsynaptic activity. J Assoc Res Otolaryngol 4:1-23.
20. 2+ requirements and developmental regulation of posttetanic potentiation at the calyx of Held. J Neurosci 25:5127-5137.
21. Korogod N, Lou X, Schneggenburger R (2007) Posttetanic potentiation critically depends on an enhanced Ca2+ sensitivity of vesicle fusion mediated by presynaptic PKC. Proc Natl Acad Sci U S A 104:15923-15928.
22. Lee D, Lee KH, Ho WK, Lee SH (2007) Target cell-specific involvement of presynaptic mitochondria in post-tetanic potentiation at hippocampal mossy fiber synapses. J Neurosci 27:13603-13613.
23. Lukas TJ, Mirzoeva S, Slomczynska U, Watterson DM (1999) Identification of novel classes of protein kinase inhibitors using combinatorial peptide chemistry based on functional genomics knowledge. J Med Chem 42:910-919.
24. Mochida S, Kobayashi H, Matsuda Y, Yuda Y, Muramoto K, Nonomura Y (1994) Myosin II is involved in transmitter release at synapses formed between rat sympathetic neurons in culture. Neuron 13:1131-1142.
25. Moulder KL, Mennerick S (2005) Reluctant vesicles contribute to the total readily releasable pool in glutamatergic hippocampal neurons. J Neurosci 25:3842-3850.
26. Otis T, Zhang S, Trussell LO (1996) Direct measurement of AMPA receptor desensitization induced by glutamatergic synaptic transmission. J Neurosci 16:7496-7504.
27. Polo-Parada L, Plattner F, Bose C, Landmesser LT (2005) NCAM180 acting via a conserved C-terminal domain and MLCK is essential for effective transmission with repetitive stimulation. Neuron 46:917-931.
28. Regehr WG, Delaney KR, Tank DW (1994) The role of presynaptic calcium in short-term enhancement at the hippocampal mossy fiber synapse. J Neurosci 14:523-537.
29. Rozov A, Burnashev N, Sakmann B, Neher E (2001) Transmitter release modulation by intracellular Ca2+ buffers in facilitating and depressing nerve terminals of pyramidal cells in layer 2/3 of the rat neocortex indicates a target cell-specific difference in presynaptic calcium dynamics. J Physiol 531:807-826.
30. Ryan TA (1999) Inhibitors of myosin light chain kinase block synaptic vesicle pool mobilization during action potential firing. J Neurosci 19:1317-1323.
31. Sakaba T (2006) Roles of the fast-releasing and slowly releasing vesicles in synaptic transmission at the calyx of Held. J Neurosci 26:5863-5871.
32. Schneggenburger R, Meyer AC, Neher E (1999) Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 23:399-409.
33. Schneggenburger R, Sakaba T, Neher E (2002) Vesicle pools and short-term synaptic depression: lessons from a large synapse. Trends Neurosci 25:206-212.
34. Srinivasan G, Kim JH, von Gersdorff H (2008) The pool of fast releasing vesicles is augmented by myosin light chain kinase inhibition at the calyx of Held synapse. J Neurophysiol 99:1810-1824.
35. Stevens CF, Wesseling JF (1999) Augmentation is a potentiation of the exocytotic process. Neuron 22:139-146.
36. Takagishi Y, Futaki S, Itoh K, Espreafico EM, Murakami N, Murata Y, Mochida S (2005) Localization of myosin II and V isoforms in cultured rat sympathetic neurones and their potential involvement in presynaptic function. J Physiol 569:195-208.
37. Tang Y, Zucker RS (1997) Mitochondrial involvement in post-tetanic potentiation of synaptic transmission. Neuron 18:483-491.
38. Tokuoka H, Goda Y (2006) Myosin light chain kinase is not a regulator of synaptic vesicle trafficking during repetitive exocytosis in cultured hippocampal neurons. J Neurosci 26:11606-11614.
39. Toullec D, Pianetti P, Coste H, Bellevergue P, Grand-Perret T, Ajakane M, Baudet V, Boissin P, Boursier E, Loriolle F (1991) The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J Biol Chem 266:15771-15781.
40. Trussell LO, Zhang S, Raman IM (1993) Desensitization of AMPA receptors upon multiquantal neurotransmitter release. Neuron 10:1185-1196.
41. Verstreken P, Ly CV, Venken KJT, Koh T-W, Zhou Y, Bellen HJ (2005) Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 47:365-378.
42. Wingrove DE, Gunter TE (1986) Kinetics of mitochondrial calcium transport. II. A kinetic description of the sodium-dependent calcium efflux mechanism of liver mitochondria and inhibition by ruthenium red and by tetraphenylphosphonium. J Biol Chem 261:15166-15171.
43. Wong AYC, Graham BP, Billups B, Forsythe ID (2003) Distinguishing between presynaptic and postsynaptic mechanisms of short-term depression during action potential trains. J Neurosci 23:4868-4877.
44. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405.