Differential regulation of spontaneous and evoked neurotransmitter release at central synapses

Current Opinion in Neurobiology

Volumn 21, Issue 2, 2011, Pages 275-282

  Ramirez, Denise MO ^a   Kavalali, Ege T ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; DNA METHYLTRANSFERASE; METABOTROPIC RECEPTOR 2; SNARE PROTEIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNAPTOTAGMIN I; VOLTAGE GATED CALCIUM CHANNEL;

CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CHOLESTEROL SYNTHESIS; ENDOCYTOSIS; EXCITATORY POSTSYNAPTIC POTENTIAL; EXOCYTOSIS; NERVE POTENTIAL; NEUROMODULATION; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPSE VESICLE; SYNAPTOSOME;

ANIMALS; BRAIN; HUMANS; NEUROTRANSMITTER AGENTS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 79955655872     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2011.01.007     Document Type: Review

References (77)

1. Deák F., Liu X., Khvotchev M., Li G., Kavalali E.T., Sugita S., Südhof T.C. Alpha-latrotoxin stimulates a novel pathway of Ca2+-dependent synaptic exocytosis independent of the classical synaptic fusion machinery. J Neurosci 2009, 29:8639-8648.
2. Chung C., Deák F., Kavalali E.T. Molecular substrates mediating lanthanide-evoked neurotransmitter release in central synapses. J Neurophysiol 2008, 100:2089-2100.
3. Sharma G., Vijayaraghavan S. Modulation of presynaptic store calcium induces release of glutamate and postsynaptic firing. Neuron 2003, 38:929-939.
4. Fatt P., Katz B. Spontaneous subthreshold activity at motor nerve endings. J Physiol 1952, 117:109-128.
5. Wasser C.R., Kavalali E.T. Leaky synapses: regulation of spontaneous neurotransmission in central synapses. Neuroscience 2009, 158:177-188.
6. Kavalali ET, Chung C, Khvotchev M, Leitz J, Nosyreva E, Raingo J, Ramirez DMO. Spontaneous Neurotransmission: an independent pathway for neuronal signaling? Physiology (Bethesda), in press.
7. Carter A.G., Regehr W.G. Quantal events shape cerebellar interneuron firing. Nat Neurosci 2002, 5:1309-1318.
8. Otmakhov N., Shirke A.M., Malinow R. Measuring the impact of probabilistic transmission on neuronal output. Neuron 1993, 10:1101-1111.
9. Sutton M.A., Wall N.R., Aakalu G.N., Schuman E.M. Regulation of dendritic protein synthesis by miniature synaptic events. Science 2004, 304:1979-1983.
10. Sutton M.A., Ito H.T., Cressy P., Kempf C., Woo J.C., Schuman E.M. Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis. Cell 2006, 125:785-799.
11. Sutton M.A., Taylor A.M., Ito H.T., Pham A., Schuman E.M. Postsynaptic decoding of neural activity: eEF2 as a biochemical sensor coupling miniature synaptic transmission to local protein synthesis. Neuron 2007, 55:648-661.
12. Aoto J., Nam C.I., Poon M.M., Ting P., Chen L. Synaptic signaling by all-trans retinoic acid in homeostatic synaptic plasticity. Neuron 2008, 60:308-320.
13. Chung C., Kavalali E.T. Seeking a function for spontaneous neurotransmission. Nat Neurosci 2006, 9:989-990.
14. Atasoy D., Ertunc M., Moulder K.L., Blackwell J., Chung C., Su J., Kavalali E.T. Spontaneous and evoked glutamate release activates two populations of NMDA receptors with limited overlap. J Neurosci 2008, 28:10151-10166.
15. Zenisek D. Vesicle association and exocytosis at ribbon and extraribbon sites in retinal bipolar cell presynaptic terminals. Proc Natl Acad Sci USA 2008, 105:4922-4927.
16. Lee M.C., Yasuda R., Ehlers M.D. Metaplasticity at single glutamatergic synapses. Neuron 2010, 66:859-870.
17. Jakawich S.K., Nasser H.B., Strong M.J., McCartney A.J., Perez A.S., Rakesh N., Carruthers C.J., Sutton M.A. Local presynaptic activity gates homeostatic changes in presynaptic function driven by dendritic BDNF synthesis. Neuron 2010, 68:1143-1158.
18. Sara Y., Virmani T., Deak F., Liu X., Kavalali E.T. An isolated pool of vesicles recycles at rest and drives spontaneous neurotransmission. Neuron 2005, 45:563-573.
19. Fredj N.B., Burrone J. A resting pool of vesicles is responsible for spontaneous vesicle fusion at the synapse. Nat Neurosci 2009, 12:751-758.
20. Chung C., Barylko B., Leitz J., Liu X., Kavalali E.T. Acute dynamin inhibition dissects synaptic vesicle recycling pathways that drive spontaneous and evoked neurotransmission. J Neurosci 2010, 30:1363-1376.
21. Mathew S.S., Pozzo-Miller L., Hablitz J.J. Kainate modulates presynaptic GABA release from two vesicle pools. J Neurosci 2008, 28:725-731.
22. Groemer T.W., Klingauf J. Synaptic vesicles recycling spontaneously and during activity belong to the same vesicle pool. Nat Neurosci 2007, 10:145-147.
23. Hua Y., Sinha R., Martineau M., Kahms M., Klingauf J. A common origin of synaptic vesicles undergoing evoked and spontaneous fusion. Nat Neurosci 2010, 13:1451-1453.
24. Wilhelm B.G., Groemer T.W., Rizzoli S.O. The same synaptic vesicles drive active and spontaneous release. Nat Neurosci 2010, 13:1454-1456.
25. Hablitz J.J., Mathew S.S., Pozzo-Miller L. GABA vesicles at synapses: are there 2 distinct pools?. Neuroscientist 2009, 15:218-224.
26. Wasser C.R., Ertunc M., Liu X., Kavalali E.T. Cholesterol-dependent balance between evoked and spontaneous synaptic vesicle recycling. J Physiol 2007, 579:413-429.
27. Zamir O., Charlton M.P. Cholesterol and synaptic transmitter release at crayfish neuromuscular junctions. J Physiol 2006, 571:83-99.
28. Lipscombe D., Kongsamut S., Tsien R.W. Alpha-adrenergic inhibition of sympathetic neurotransmitter release mediated by modulation of N-type calcium-channel gating. Nature 1989, 340:639-642.
29. Missler M., Zhang W., Rohlmann A., Kattenstroth G., Hammer R.E., Gottmann K., Südhof T.C. Alpha-neurexins couple Ca2+ channels to synaptic vesicle exocytosis. Nature 2003, 423:939-948.
30. Dittman J.S., Regehr W.G. Contributions of calcium-dependent and calcium-independent mechanisms to presynaptic inhibition at a cerebellar synapse. J Neurosci 1996, 16:1623-1633.
31. Blackmer T., Larsen E.C., Takahashi M., Martin T.F., Alford S., Hamm H.E. G protein betagamma subunit-mediated presynaptic inhibition: regulation of exocytotic fusion downstream of Ca2+ entry. Science 2001, 292:293-297.
32. Sakaba T., Neher E. Direct modulation of synaptic vesicle priming by GABA(B) receptor activation at a glutamatergic synapse. Nature 2003, 424:775-778.
33. Malenka R.C., Madison D.V., Nicoll R.A. Potentiation of synaptic transmission in the hippocampus by phorbol esters. Nature 1986, 321:175-177.
34. Lou X., Scheuss V., Schneggenburger R. Allosteric modulation of the presynaptic Ca2+ sensor for vesicle fusion. Nature 2005, 435:497-501.
35. Virmani T., Ertunc M., Sara Y., Mozhayeva M., Kavalali E.T. Phorbol esters target the activity-dependent recycling pool and spare spontaneous vesicle recycling. J Neurosci 2005, 25:10922-10929.
36. Swartz K.J., Merritt A., Bean B.P., Lovinger D.M. Protein kinase C modulates glutamate receptor inhibition of Ca2+ channels and synaptic transmission. Nature 1993, 361:165-168.
37. Waters J., Smith S.J. Phorbol esters potentiate evoked and spontaneous release by different presynaptic mechanisms. J Neurosci 2000, 20:7863-7870.
38. Glitsch M. Selective inhibition of spontaneous but not Ca2+-dependent release machinery by presynaptic group II mGluRs in rat cerebellar slices. J Neurophysiol 2006, 96:86-96.
39. Taniguchi N., Takada N., Kimura F., Tsumoto T. Actions of brain-derived neurotrophic factor on evoked and spontaneous EPSCs dissociate with maturation of neurones cultured from rat visual cortex. J Physiol 2000, 527:579-592.
40. Nelson E.D., Kavalali E.T., Monteggia L.M. Activity-dependent suppression of miniature neurotransmission through the regulation of DNA methylation. J Neurosci 2008, 28:395-406.
41. Nosyreva E., Kavalali E.T. Activity-dependent augmentation of spontaneous neurotransmission during endoplasmic reticulum stress. J Neurosci 2010, 30:7358-7368.
42. Pratt K.G., Zhu P., Watari H., Cook D.G., Sullivan J.M. A novel role for γ-secretase: selective regulation of spontaneous neurotransmitter release from hippocampal neurons. J Neurosci 2011, 31:899-906.
43. Tu H., Nelson O., Bezprozvanny A., Wang Z., Lee S.F., Hao Y.H., Serneels L., De Strooper B., Yu G., Bezprozvanny I. Presenilins form ER Ca2+ leak channels, a function disrupted by familial Alzheimer's disease-linked mutations. Cell 2006, 126:981-993.
44. Zhang C., Wu B., Beglopoulos V., Wines-Samuelson M., Zhang D., Dragatsis I., Südhof T.C., Shen J. Presenilins are essential for regulating neurotransmitter release. Nature 2009, 460:632-636.
45. Pan Z.H., Segal M.M., Lipton S.A. Nitric oxide-related species inhibit evoked neurotransmission but enhance spontaneous miniature synaptic currents in central neuronal cultures. Proc Natl Acad Sci U S A 1996, 93:15423-15428.
46. Murthy V.N., Stevens C.F. Reversal of synaptic vesicle docking at central synapses. Nat Neurosci 1999, 2:503-507.
47. Prange O., Murphy T.H. Correlation of miniature synaptic activity and evoked release probability in cultures of cortical neurons. J Neurosci 1999, 19:6427-6438.
48. Mozhayeva M.G., Sara Y., Liu X., Kavalali E.T. Development of vesicle pools during maturation of hippocampal synapses. J Neurosci 2002, 22:654-665.
49. Shen W., Wu B., Zhang Z., Dou Y., Rao Z.R., Chen Y.R., Duan S. Activity-induced rapid synaptic maturation mediated by presynaptic cdc42 signaling. Neuron 2006, 50:401-414.
50. Wittenmayer N., Körber C., Liu H., Kremer T., Varoqueaux F., Chapman E.R., Brose N., Kuner T., Dresbach T. Postsynaptic Neuroligin1 regulates presynaptic maturation. Proc Natl Acad Sci USA 2009, 106:13564-13569.
51. Llano I., Gonzalez J., Caputo C., Lai F.A., Blayney L.M., Tan Y.P., Marty A. Presynaptic calcium stores underlie large-amplitude miniature IPSCs and spontaneous calcium transients. Nat Neurosci 2000, 3:1256-1265.
52. Abenavoli A., Forti L., Bossi M., Bergamaschi A., Villa A., Malgaroli A. Multimodal quantal release at individual hippocampal synapses: evidence for no lateral inhibition. J Neurosci 2002, 22:6336-6346.
53. Popescu I.R., Morton L.A., Franco A., Di S., Ueta Y., Tasker J.G. Synchronized bursts of miniature inhibitory postsynaptic currents. J Physiol 2010, 588:939-951.
54. Glitsch M.D. Spontaneous neurotransmitter release and Ca(2+)-How spontaneous is spontaneous neurotransmitter release?. Cell Calcium 2008, 43:9-15.
55. Xu J., Pang Z.P., Shin O.H., Sudhof T.C. Synaptotagmin-1 functions as a Ca(2+) sensor for spontaneous release. Nat Neurosci 2009, 12:759-766.
56. Groffen A.J., Martens S., Diez Arazola R., Cornelisse L.N., Lozovaya N., de Jong A.P., Goriounova N.A., Habets R.L., Takai Y., Borst J.G., et al. Doc2b is a high-affinity Ca2+ sensor for spontaneous neurotransmitter release. Science 2010, 327:1614-1618.
57. Sun J., Pang Z.P., Qin D., Fahim A.T., Adachi R., Südhof T.C. A dual-Ca2+-sensor model for neurotransmitter release in a central synapse. Nature 2007, 450:676-682.
58. Peters J.H., McDougall S.J., Fawley J.A., Smith S.M., Andresen M.C. Primary afferent activation of thermosensitive TRPV1 triggers asynchronous glutamate release at central neurons. Neuron 2010, 65:657-669.
59. Maximov A., Shin O.H., Liu X., Sudhof T.C. Synaptotagmin-12, a synaptic vesicle phosphoprotein that modulates spontaneous neurotransmitter release. J Cell Biol 2007, 176:113-124.
60. Jahn R., Scheller R.H. SNAREs-engines for membrane fusion. Nat Rev Mol Cell Biol 2006, 7:631-643.
61. Sudhof T.C., Rothman J.E. Membrane fusion: grappling with SNARE and SM proteins. Science 2009, 323:474-477.
62. Schoch S., Deak F., Konigstorfer A., Mozhayeva M., Sara Y., Sudhof T.C., Kavalali E.T. SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science 2001, 294:1117-1122.
63. Washbourne P., Thompson P.M., Carta M., Costa E.T., Mathews J.R., Lopez-Benditó G., Molnár Z., Becher M.W., Valenzuela C.F., Partridge L.D., Wilson M.C. Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat Neurosci 2002, 5:19-26.
64. Bronk P., Deak F., Wilson M.C., Liu X., Sudhof T.C., Kavalali E.T. Differential effects of SNAP-25 deletion on Ca2+-dependent and Ca2+-independent neurotransmission. J Neurophysiol 2010, 98:794-806.
65. Hua S.Y., Raciborska D.A., Trimble W.S., Charlton M.P. Different VAMP/synaptobrevin complexes for spontaneous and evoked transmitter release at the crayfish neuromuscular junction. J Neurophysiol 1998, 80:3233-3246.
66. Takamori S., Holt M., Stenius K., Lemke E.A., Grønborg M., Riedel D., Urlaub H., Schenck S., Brügger B., Ringler P., et al. Molecular anatomy of a trafficking organelle. Cell 2006, 127:831-846.
67. Antonin W., Riedel D., von Mollard G.F. The SNARE Vti1a-beta is localized to small synaptic vesicles and participates in a novel SNARE complex. J Neurosci 2000, 20:5724-5732.
68. Muzerelle A., Alberts P., Martinez-Arca S., Jeannequin O., Lafaye P., Mazié J.C., Galli T., Gaspar P. Tetanus neurotoxin-insensitive vesicle-associated membrane protein localizes to a presynaptic membrane compartment in selected terminal subsets of the rat brain. Neuroscience 2003, 122:59-75.
69. Scheuber A., Rudge R., Danglot L., Raposo G., Binz T., Poncer J.C., Galli T. Loss of AP-3 function affects spontaneous and evoked release at hippocampal mossy fiber synapses. Proc Natl Acad Sci U S A 2006, 103:16562-16567.
70. Deak F., Shin O.H., Kavalali E.T., Sudhof T.C. Structural determinants of synaptobrevin 2 function in synaptic vesicle fusion. J Neurosci 2006, 26:6668-6676.
71. Weber J.P., Reim K., Sørensen J.B. Opposing functions of two sub-domains of the SNARE-complex in neurotransmission. EMBO J 2010, 29:2477-2490.
72. Maximov A., Tang J., Yang X., Pang Z.P., Südhof T.C. Complexin controls the force transfer from SNARE complexes to membranes in fusion. Science 2009, 323:516-521.
73. Rizzoli S.O., Betz W.J. Synaptic vesicle pools. Nat Rev Neurosci 2005, 6:57-69.
74. Koenig J.H., Ikeda K. Contribution of active zone subpopulation of vesicles to evoked and spontaneous release. J Neurophysiol 1999, 81:1495-1505.
75. Vanden Berghe P., Klingauf J. Synaptic vesicles in rat hippocampal boutons recycle to different pools in a use-dependent fashion. J Physiol 2006, 572:707-720.
76. Holt M., Riedel D., Stein A., Schuette C., Jahn R. Synaptic vesicles are constitutively active fusion machines that function independently of Ca2+. Curr Biol 2008, 18:715-722.
77. Sutton M.A., Schuman E.M. Partitioning the synaptic landscape: distinct microdomains for spontaneous and spike-triggered neurotransmission. Sci Signal 2009, 2:pe19.