Developmental regulation of the intracellular Ca2+ sensitivity of vesicle fusion and Ca2+-secretion coupling at the rat calyx of Held

Journal of Physiology

Volumn 587, Issue 12, 2009, Pages 3009-3023

  Kochubey, Olexiy ^a   Han, Yunyun ^a   Schneggenburger, Ralf ^a  

^a EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CALCIUM CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUDITORY NERVOUS SYSTEM; CALCIUM CELL LEVEL; CALCIUM CURRENT; CALYX OF HELD SYNAPSE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; NEUROTRANSMITTER RELEASE; NONHUMAN; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPSE VESICLE; ACTION POTENTIAL AMPLITUDE; CALYX OF HELD; CELL FUSION; CELL VACUOLE; CHEMICAL PARAMETERS; EXCITATORY POSTSYNAPTIC POTENTIAL; GLUTAMATERGIC SYNAPSE; HEARING; NERVOUS SYSTEM DEVELOPMENT; PRESYNAPTIC NERVE; PROTEIN LOCALIZATION; SENSITIVITY ANALYSIS;

ACTION POTENTIALS; AGING; ANIMALS; AUDITORY PATHWAYS; BRAIN STEM; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; DATA INTERPRETATION, STATISTICAL; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIALS; NEUROTRANSMITTER AGENTS; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; SYNAPTIC VESICLES;

EID: 67649639270     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2009.172387     Document Type: Article

References (53)

1. Augustine GJ, Adler EM & Charlton MP (1991). The calcium signal for transmitter secretion from presynaptic nerve terminals. Ann N Y Acad Sci 635, 365-381.
2. 2+ signal. Nat Neurosci 8, 426-434.
3. Bollmann JH, Sakmann B & Borst JG (2000). Calcium sensitivity of glutamate release in a calyx-type terminal. Science 289, 953-957.
4. Borst JG & Sakmann B (1998). Calcium current during a single action potential in a large presynaptic terminal of the rat brainstem. J Physiol 506, 143-157.
5. Borst JG & Sakmann B (1999). Effect of changes in action potential shape on calcium currents and transmitter release in a calyx-type synapse of the rat auditory brainstem. Philos Trans R Soc Lond B Biol Sci 354, 347-355.
6. Brandt A, Khimich D & Moser T (2005). Few Ca V 1.3 channels regulate the exocytosis of a synaptic vesicle at the hair cell ribbon synapse. J Neurosci 25, 11577-11585.
7. 2+ sensors promotes fast and efficient transmitter release at a cortical GABAergic synapse. Neuron 57, 536-545.
8. Chuhma N, Koyano K & Ohmori H (2001). Synchronisation of neurotransmitter release during postnatal development in a calyceal presynaptic terminal of rat. J Physiol 530, 93-104.
9. Fedchyshyn MJ & Wang LY (2005). Developmental transformation of the release modality at the calyx of Held synapse. J Neurosci 25, 4131-4140.
10. 2+ dependent and lacks a direct influence of presynaptic membrane potential. Proc Natl Acad Sci U S A 100, 15200-15205.
11. 2+-binding proteins calretinin and parvalbumin at the calyx of Held of rats and mice. Eur J Neurosci 20, 1473-1482.
12. Futai K, Okada M, Matsuyama K & Takahashi T (2001). High-fidelity transmission acquired via a developmental decrease in NMDA receptor expression at an auditory synapse. J Neurosci 21, 3342-3349.
13. Geal-Dor M, Freeman S, Li G & Sohmer H (1993). Development of hearing in neonatal rats: Air and bone conducted ABR thresholds. Hear Res 69, 236-242.
14. Gentile L & Stanley EF (2005). A unified model of presynaptic release site gating by calcium channel domains. Eur J Neurosci 21, 278-282.
15. 2+ channels. Neuron 34, 411-423.
16. Hoffpauir BK, Grimes JL, Mathers PH & Spirou GA (2006). Synaptogenesis of the calyx of Held: Rapid onset of function and one-to-one morphological innervation. J Neurosci 26, 5511-5523.
17. 2+-triggered exocytosis in presynaptic terminals. Neuron 17, 501-512.
18. Iwasaki S, Momiyama A, Uchitel OD & Takahashi T (2000). Developmental changes in calcium channel types mediating central synaptic transmission. J Neurosci 20, 59-65.
19. Iwasaki S & Takahashi T (2001). Developmental regulation of transmitter release at the calyx of Held in rat auditory brainstem. J Physiol 534, 861-871.
20. Jewett DL & Romano MN (1972). Neonatal development of auditory system potentials averaged from the scalp of rat and cat. Brain Res 36, 101-115.
21. Joshi I & Wang L-Y (2002). Developmental profiles of glutamate receptors and synaptic transmission at a single synapse in the mouse auditory brainstem. J Physiol 540, 861-873.
22. Kaeser PS & Sudhof TC (2005). RIM function in short- and long-term synaptic plasticity. Biochem Soc Trans 33, 1345-1349.
23. Kandler K & Friauf E (1993). Pre- and postnatal development of efferent connections of the cochlear nucleus in the rat. J Comp Neurol 328, 161-184.
24. 2+ channels. Nat Neurosci 10, 691-701.
25. 2+ sensor for vesicle fusion. Nature 435, 497-501.
26. Meinrenken C, Borst JGG & Sakmann B (2002). Calcium secretion coupling at calyx of Held governed by nonuniform channel-vesicle topography. J Neurosci 22, 1648-1667.
27. 2+-current facilitation to paired-pulse facilitation of transmitter release at the rat calyx of Held. J Physiol 586, 5503-5520.
28. 2+ binding in bovine chromaffin cells. Biophys J 75, 1635-1647.
29. ++ signals. Cell Calcium 24, 345-357.
30. Neher E & Sakaba T (2001). Combining deconvolution and noise analysis for the estimation of transmitter release rates at the calyx of Held. J Neurosci 21, 444-461.
31. Price GD & Trussell LO (2007). Good players left on the sidelines: why some synaptic vesicles don't get in the game. Neuron 53, 471-473.
32. 2+ channels with the presynaptic proteins syntaxin and SNAP-25. Proc Natl Acad Sci U S A 93, 7363-7368.
33. Rodriguez-Contreras A, van Hoeve JS, Habets RL, Locher H & Borst JG (2008). Dynamic development of the calyx of Held synapse. Proc Natl Acad Sci U S A 105, 5603-5608.
34. Sakaba T (2006). Roles of the fast-releasing and the slowly releasing vesicles in synaptic transmission at the calyx of Held. J Neurosci 26, 5863-5871.
35. Sakaba T & Neher E (2001). Quantitative relationship between transmitter release and calcium current at the calyx of Held synapse. J Neurosci 21, 462-476.
36. Schneggenburger R & Neher E (2000). Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406, 889-893.
37. Schneggenburger R & Neher E (2005). Presynaptic calcium and control of vesicle fusion. Curr Opin Neurobiol 15, 266-274.
38. Schwarz G (1978). Estimating the dimension of a model. Ann Statist 6, 461-464.
39. Sheng ZH, Rettig J, Takahashi M & Catterall WA (1994). Identification of a syntaxin-binding site on N-type calcium channels. Neuron 13, 1303-1313.
40. Steinert JR, Kopp-Scheinpflug C, Baker C, Challiss RA, Mistry R, Haustein MD, Griffin SJ, Tong H, Graham BP & Forsythe ID (2008). Nitric oxide is a volume transmitter regulating postsynaptic excitability at a glutamatergic synapse. Neuron 60, 642-656.
41. 2+-sensor model for neurotransmitter release in a central synapse. Nature 450, 676-682.
42. Taschenberger H, Leao RM, Rowland KC, Spirou GA & von Gersdorff H (2002). Optimizing synaptic architecture and efficiency for high-frequency transmission. Neuron 36, 1127-1143.
43. Taschenberger H, Scheuss V & Neher E (2005). Release kinetics, quantal parameters and their modulation during short-term depression at a developing synapse in the rat CNS. J Physiol 568, 513-537.
44. Taschenberger H & von Gersdorff H (2000). Fine-tuning an auditory synapse for speed and fidelity: Developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J Neurosci 20, 9162-9173.
45. Trussell LO (1999). Synaptic mechanisms for coding timing in auditory neurons. Annu Rev Physiol 61, 477-496.
46. 2+-dependent steps leading to secretion in chromaffin cells from mouse adrenal slices. Neuron 28, 537-545.
47. von Gersdorff H, Schneggenburger R, Weis S & Neher E (1997). Presynaptic depression at a calyx synapse: The small contribution of metabotropic glutamate receptors. J Neurosci 17, 8137-8146.
48. 2+ channels determines fast neurotransmitter release. Neuron 53, 563-575.
49. Wang L-Y, Neher E & Taschenberger H (2008). Synaptic vesicles in mature calyx of Held synapses sense higher nanodomain calcium concentrations during action potential-evoked glutamate release. J Neurosci 28, 14450-14458.
50. Wölfel M, Lou X & Schneggenburger R (2007). A mechanism intrinsic to the vesicle fusion machinery determines fast and slow transmitter release at a large CNS synapse. J Neurosci 27, 3198-3210.
51. Wu LG, Westenbroek RE, Borst JGG, Catterall WA & Sakmann B (1999). Calcium channel types with distinct presynaptic localization couple differentially to transmitter release in single calyx-type synapses. J Neurosci 19, 726-736.
52. 2+ current and its efficacy in triggering transmitter release at the developing calyx of Held synapse. J Neurosci 26, 5698-5708.
53. Yoshikami D, Bagabaldo Z & Olivera BM (1989). The inhibitory effects of omega-conotoxins on Ca channels and synapses. Ann N Y Acad Sci 560, 230-248.