Synapsin IIa controls the reserve pool of glutamatergic synaptic vesicles

Journal of Neuroscience

Volumn 28, Issue 43, 2008, Pages 10835-10843

  Gitler, Daniel ^a,b   Cheng, Qing ^a   Greengard, Paul ^c   Augustine, George J ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Alternative splice variants; Glutamatergic neurons; Neurotransmitter release; Synaptic physiology; Synaptic plasticity; Synaptic vesicle trafficking

Indexed keywords

DYE; GLUTAMIC ACID; N (3 TRIETHYLAMMONIUMPROPYL) 4 (6 (4 DIETHYLAMINO)PHENYL) HEXATRIENYL)PYRIDINIUM DIBROMIDE; SYNAPSIN; SYNAPSIN IIA; SYNAPTOBREVIN 2; UNCLASSIFIED DRUG; ENHANCED GREEN FLUORESCENT PROTEIN; FM 4 64; FM 4-64; GREEN FLUORESCENT PROTEIN; ISOPROTEIN; PYRIDINIUM DERIVATIVE; QUATERNARY AMMONIUM DERIVATIVE;

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; HIPPOCAMPUS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG EFFECT; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETIC TRANSFECTION; GENETICS; METABOLISM; METHODOLOGY; MOUSE MUTANT; NERVE CELL; NERVE CELL INHIBITION; PATCH CLAMP; PHYSIOLOGY; SYNAPSE; SYNAPTOSOME;

ANIMALS; CELLS, CULTURED; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; MICE; MICE, KNOCKOUT; NEURAL INHIBITION; NEURONS; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; PROTEIN ISOFORMS; PYRIDINIUM COMPOUNDS; QUATERNARY AMMONIUM COMPOUNDS; SYNAPSES; SYNAPSINS; SYNAPTIC VESICLES; TRANSFECTION; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2;

EID: 58149145791     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0924-08.2008     Document Type: Article

References (46)

1. Baldelli P, Fassio A, Valtorta F, Benfenati F (2007) Lack of synapsin I reduces the readily releasable pool of synaptic vesicles at central inhibitory synapses. J Neurosci 27:13520-13531.
2. 2+/calmodulin-dependent protein kinase II is a binding protein for synapsin I. Nature 359:417-420.
3. Betz A, Thakur P, Junge HJ, Ashery U, Rhee JS, Scheuss V, Rosenmund C, Rettig J, Brose N (2001) Functional interaction of the active zone proteins Munc13-1 and RIM1 in synaptic vesicle priming. Neuron 30:183-196.
4. Betz WJ (1970) Depression of transmitter release at the neuromuscular junction of the frog. J Physiol 206:629-644.
5. Chi P, Greengard P, Ryan TA (2001) Synapsin dispersion and reclustering during synaptic activity. Nat Neurosci 4:1187-1193.
6. Chi P, Greengard P, Ryan TA (2003) Synaptic vesicle mobilization is regulated by distinct synapsin I phosphorylation pathways at different frequencies. Neuron 38:69-78.
7. Dobrunz LE, Stevens CF (1997) Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18:995-1008.
8. Evergren E, Benfenati F, Shupliakov O (2007) The synapsin cycle: a view from the synaptic endocytic zone. J Neurosci Res 85:2648-2656.
9. Feng J, Chi P, Blanpied TA, Xu Y, Magarinos AM, Ferreira A, Takahashi RH, Kao HT, McEwen BS, Ryan TA, Augustine GJ, Greengard P (2002) Regulation of neurotransmitter release by synapsin III. J Neurosci 22:4372-4380.
10. Fernández-Alfonso T, Kwan R, Ryan TA (2006) Synaptic vesicles interchange their membrane proteins with a large surface reservoir during recycling. Neuron 51:179-186.
11. Ferreira A, Rapoport M (2002) The synapsins: beyond the regulation of neurotransmitter release. Cell Mol Life Sci 59:589-595.
12. Gaffield MA, Betz WJ (2007) Synaptic vesicle mobility in mouse motor nerve terminals with and without synapsin. J Neurosci 27:13691-13700.
13. Gitler D, Xu Y, Kao HT, Lin D, Lim S, Feng J, Greengard P, Augustine GJ (2004a) Molecular determinants of synapsin targeting to presynaptic terminals. J Neurosci 24:3711-3720.
14. Gitler D, Takagishi Y, Feng J, Ren Y, Rodriguiz RM, Wetsel WC, Greengard P, Augustine GJ (2004b) Different presynaptic roles of synapsins at excitatory and inhibitory synapses. J Neurosci 24:11368-11380.
15. Greengard P, Valtorta F, Czernik AJ, Benfenati F (1993) Synaptic vesicle phosphoproteins and regulation of synaptic function. Science 259:780-785.
16. Hilfiker S, Schweizer FE, Kao HT, Czernik AJ, Greengard P, Augustine GJ (1998) Two sites of action for synapsin domain E in regulating neurotransmitter release. Nat Neurosci 1:29-35.
17. Hilfiker S, Pieribone VA, Czernik AJ, Kao HT, Augustine GJ, Greengard P (1999) Synapsins as regulators of neurotransmitter release. Philos Trans R Soc Lond B Biol Sci 354:269-279.
18. Hilfiker S, Benfenati F, Doussau F, Nairn AC, Czernik AJ, Augustine GJ, Greengard P (2005) Structural domains involved in the regulation of transmitter release by synapsins. J Neurosci 25:2658-2669.
19. 2+ regulation. J Biol Chem 273:1425-1429.
20. Hosaka M, Südhof TC (1999) Homo- and heterodimerization of synapsins. J Biol Chem 274:16747-16753.
21. Hosaka M, Hammer RE, Südhof TC (1999) A phospho-switch controls the dynamic association of synapsins with synaptic vesicles. Neuron 24:377-387.
22. Humeau Y, Doussau F, Vitiello F, Greengard P, Benfenati F, Poulain B (2001) Synapsin controls both reserve and releasable synaptic vesicle pools during neuronal activity and short-term plasticity in Aplysia. J Neurosci 21:4195-4206.
23. Hvalby O, Jensen V, Kao HT, Walaas SI (2006) Synapsin-regulated synaptic transmission from readily releasable synaptic vesicles in excitatory hippocampal synapses in mice. J Physiol 571:75-82.
24. Kao HT, Porton B, Hilfiker S, Stefani G, Pieribone VA, DeSalle R, Greengard P (1999) Molecular evolution of the synapsin gene family. J Exp Zool 285:360-377.
25. Kao HT, Song HJ, Porton B, Ming GL, Hoh J, Abraham M, Czernik AJ, Pieribone VA, Poo MM, Greengard P (2002) A protein kinase A-dependent molecular switch in synapsins regulates neurite outgrowth. Nat Neurosci 5:431-437.
26. Kielland A, Erisir A, Walaas SI, Heggelund P (2006) Synapsin utilization differs among functional classes of synapses on thalamocortical cells. J Neurosci 26:5786-5793.
27. Li L, Chin LS, Shupliakov O, Brodin L, Sihra TS, Hvalby O, Jensen V, Zheng D, McNamara JO, Greengard P, Andersen P (1995) Impairment of synaptic vesicle clustering and of synaptic transmission, and increased seizure propensity, in synapsin I-deficient mice. Proc Natl Acad Sci U S A 92:9235-9239.
28. Li Z, Murthy VN (2001) Visualizing postendocytic traffic of synaptic vesicles at hippocampal synapses. Neuron 31:593-605.
29. 2+-calmodulin-dependent protein kinase II of transmitter release in squid giant synapse. J Physiol 436:257-282.
30. Lois C, Hong EJ, Pease S, Brown EJ, Baltimore D (2002) Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295:868-872.
31. Mozhayeva MG, Sara Y, Liu X, Kavalali ET (2002) Development of vesicle pools during maturation of hippocampal synapses. J Neurosci 22:654-665.
32. Murthy VN, Stevens CF (1998) Synaptic vesicles retain their identity through the endocytic cycle. Nature 392:497-501.
33. 2+-dependent neurotransmitter release. J Neurosci 24:8542-8550.
34. Pieribone VA, Shupliakov O, Brodin L, Hilfiker-Rothenfluh S, Czernik AJ, Greengard P (1995) Distinct pools of synaptic vesicles in neurotransmitter release. Nature 375:493-497.
35. Rizzoli SO, Betz WJ (2005) Synaptic vesicle pools. Nat Rev Neurosci 6:57-69.
36. Rosahl TW, Spillane D, Missler M, Herz J, Selig DK, Wolff JR, Hammer RE, Malenka RC, Südhof TC (1995) Essential functions of synapsins I and II in synaptic vesicle regulation. Nature 375:488-493.
37. Salin PA, Scanziani M, Malenka RC, Nicoll RA (1996) Distinct short-term plasticity at two excitatory synapses in the hippocampus. Proc Natl Acad Sci U S A 93:13304-13309.
38. Samigullin D, Bill CA, Coleman WL, Bykhovskaia M (2004) Regulation of transmitter release by synapsin II in the mouse motor terminal. J Physiol 23:23.
39. Siksou L, Rostaing P, Lechaire JP, Boudier T, Ohtsuka T, Fejtová A, Kao HT, Greengard P, Gundelfinger ED, Triller A, Marty S (2007) Three-dimensional architecture of presynaptic terminal cytomatrix. J Neurosci 27:6868-6877.
40. Stevens CF, Williams JH (2007) Discharge of the readily releasable pool with action potentials at hippocampal synapses. J Neurophysiol 98:3221-3229.
41. Südhof TC, Czernik AJ, Kao HT, Takei K, Johnston PA, Horiuchi A, Kanazir SD, Wagner MA, Perin MS, De Camilli P, Greengard P (1989) Synapsins: mosaics of shared and individual domains in a family of synaptic vesicle phosphoproteins. Science 245:1474-1480.
42. Takei Y, Harada A, Takeda S, Kobayashi K, Terada S, Noda T, Takahashi T, Hirokawa N (1995) Synapsin I deficiency results in the structural change in the presynaptic terminals in the murine nervous system. J Cell Biol 131:1789-1800.
43. Terada S, Tsujimoto T, Takei Y, Takahashi T, Hirokawa N (1999) Impairment of inhibitory synaptic transmission in mice lacking synapsin I. J Cell Biol 145:1039-1048.
44. Varoqueaux F, Sigler A, Rhee JS, Brose N, Enk C, Reim K, Rosenmund C (2002) Total arrest of spontaneous and evoked synaptic transmission but normal synaptogenesis in the absence of Munc13-mediated vesicle priming. Proc Natl Acad Sci U S A 99:9037-9042.
45. Wojcik SM, Rhee JS, Herzog E, Sigler A, Jahn R, Takamori S, Brose N, Rosenmund C (2004) An essential role for vesicular glutamate transporter 1 (VGLUT1) in postnatal development and control of quantal size. Proc Natl Acad Sci U S A 101:7158-7163.
46. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405.