Structural domains involved in the regulation of transmitter release by synapsins

Journal of Neuroscience

Volumn 25, Issue 10, 2005, Pages 2658-2669

  Hilfiker, Sabine ^a,c,e   Benfenati, Fabio ^a,b   Doussau, Frédéric ^c,d,f   Nairn, Angus C ^a   Czernik, Andrew J ^a,g   Augustine, George J ^c,d   Greengard, Paul ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF GENOA   (Italy)

^c MARINE BIOLOGICAL LABORATORY   (United States)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

^e INSTITUTO DE PARASITOLOGÍA Y BIOMEDICINA LÓPEZ NEYRA   (Spain)

^f CNRS   (France)

^g PhosphoSolutions Inc   (United States)

Author keywords

Actin; Cytoskeleton; Depression; Neurotransmitter; Regulation; Release; Synapsin

Indexed keywords

ACTIN; SYNAPSIN;

ARTICLE; CYTOSKELETON; KINETICS; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; PHOSPHORYLATION; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; REGULATORY MECHANISM; SQUID; STRUCTURE ACTIVITY RELATION; SYNAPSE VESICLE;

AMINO ACID SEQUENCE; ANIMALS; CATTLE; EXCITATORY POSTSYNAPTIC POTENTIALS; LOLIGO; MOLECULAR SEQUENCE DATA; NEUROTRANSMITTER AGENTS; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, TERTIARY; RATS; STELLATE GANGLION; SYNAPSINS;

EID: 14944344943     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4278-04.2005     Document Type: Article

References (86)

1. Adams DJ, Takeda K, Umbach JA (1985) Inhibitors of calcium buffering depress evoked transmitter release at the squid giant synapse. J Physiol (Lond) 369:145-159.
2. Augustine GJ, Charlton MP, Smith SJ (1985) Calcium entry into voltage-clamped presynaptic terminals of squid. J Physiol (Lond) 367:143-162.
3. Bähler M, Greengard P (1987) Synapsin I bundles F-actin in a phosphorylation-dependent manner. Nature 326:704-707.
4. Bähler M, Benfenati F, Valtorta F, Czernik AJ, Greengard P (1989) Characterization of synapsin I fragments produced by cysteine-specific cleavage: a study of their interactions with F-actin. J Cell Biol 108:1841-1849.
5. Baines AJ, Bennett V (1985) Synapsin lisa spectrin-binding protein immunologically related to erythrocyte protein 4.1. Nature 315:410-413.
6. Baines AJ, Bennett V (1986) Synapsin I is a microtubule-bundling protein. Nature 319:145-147.
7. Benfenati F, Greengard P, Brunner J, Bähler M (1989a) Electrostatic and Hydrophobic interactions of synapsin I and synapsin I fragments with phospholipid bilayers. J Cell Biol 108:1851-1862.
8. Benfenati F, Bähler M, Jahn R, Greengard P (1989b) Interactions of synapsin I with small synaptic vesicles: distinct sites in synapsin I bind to vesicle phospholipids and vesicle proteins. J Cell Biol 108:1863-1872.
9. Benfenati F, Valtorta F, Chieregatti E, Greengard P (1992a) Interaction of free and synaptic vesicle-bound synapsin I with F-actin. Neuron 8:377-386.
10. 2+/calmodulin-dependent protein kinase II is a binding protein for synapsin I. Nature 359:417-420.
11. Benfenati F, Valtorta F, Neyroz P, Greengard P (1993a) Binding of synapsin I to synaptic vesicles: clues from the study of its interactions with liposomes. J Liposome Res 3:599-609.
12. Benfenati F, Valtorta F, Rossi MC, Onofri F, Sihra T, Greengard P (1993b) Interactions of synapsin I with phospholipids: possible role in synaptic vesicle clustering and in the maintenance of bilayer structures. J Cell Biol 123:1845-1855.
13. Bernstein BW, DeWit M, Bamburg JR (1998) Actin disassembles reversibly during electrically induced recycling of synaptic vesicles in cultured neurons. Brain Res Mol Brain Res 53:236-251.
14. Bloom O, Evergren E, Tomilin N, Kjaerulff O, Low P, Brodin L, Pieribone VA, Greengard P, Shupliakov A (2003) Colocalization of synapsin and actin during synaptic vesicle recycling. J Cell Biol 161:737-747.
15. Bommert K, Charlton MP, DeBello WM, Chin GJ, Betz H, Augustine GJ (1993) Inhibition of neurotransmitter release by C2-domain peptides implicates synaptotagmin in exocytosis. Nature 363:163-165.
16. Brautigam CA, Chelliah Y, Deisenhofer J (2004) Tetramerization and ATP binding by a protein comprising the A, B and C domains of rat synapsin I. J Biol Chem 279:11948-11956.
17. Burns ME, Sasaki T, Takai Y, Augustine GJ (1998) Rabphilin-3A: a multifunctional regulator of synaptic vesicle traffic. J Gen Physiol 111:243-255.
18. Ceccaldi PE, Grohovaz F, Benfenati F, Chieregatti E, Greengard P, Valtorta F (1995) Dephosphorylated synapsin I anchors synaptic vesicles to actin cytoskeleton: an analysis by videomicroscopy. J Cell Biol 128:905-912.
19. Chamberlain LH, Roth D, Morgan A, Burgoyne RD (1995) Distinct effects of α-SNAP, 14-3-3 proteins and calmodulin on priming and triggering of regulated exocytosis. J Cell Biol 130:1063-1070.
20. Cheetham JJ, Hilfiker S, Benfenati F, Weber T, Greengard P, Czernik AJ (2001) Identification of synapsin I peptides that insert into lipid membranes. Biochem J 354:57-66.
21. 2+-stimulated secretion by modulating membrane-attached exocytic machinery. J Biol Chem 274:26469-26476.
22. Chi P, Greengard P, Ryan TA (2001) Synapsin dispersion and reclustering during synaptic activity. Nat Neurosci 4:1187-1193.
23. 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.
24. Chilcote TJ, Siow YL, Schaeffer E, Greengard P, Thiel G (1994) Synapsin IIa bundles actin filaments. J Neurochem 63:1568-1571.
25. Cole JC, Villa BR, Wilkinson RS (2000) Disruption of actin impedes transmitter release in snake motor terminals. J Physiol (Lond) 525:579-586.
26. Czernik AJ, Pang DT, Greengard P (1987) Amino acid sequences surrounding the cAMP-dependent and calcium/calmodulin-dependent phosphorylation sites in rat and bovine synapsin I. Proc Natl Acad Sci USA 84:7518-7522.
27. DeBello WM, O'Connor V, Dresbach T, Whiteheart SW, Wang SS, Schweizer FE, Betz H, Rothman JE, Augustine GJ (1995) SNAP-mediated protein-protein interactions essential for neurotransmitter release. Nature 373:626-630.
28. De Camilli P, Benfenati F, Valtorta F, Greengard P (1990) The synapsins. Annu Rev Cell Biol 6:433-460.
29. Doussau F, Augustine GJ (2000) The actin cytoskeleton and neurotransmitter release: an overview. Biochimie 82:353-363.
30. Esser L, Wang C, Hosaka M, Smagula CS, Südhof TC, Deisenhofer J (1998) Synapsin I is structurally similar to ATP-utilizing enzymes. EMBO J 17:977-984.
31. 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.
32. Fesce R, Benfenati F, Greengard P, Valtorta F (1992) Effects of the neuronal phosphoprotein synapsin I on actin polymerization. J Biol Chem 267:11289-11299.
33. 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.
34. 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.
35. Greengard P, Valtorta F, Czernik AJ, Benfenati F (1993) Synaptic vesicle phosphoproteins and regulation of synaptic function. Science 259:780-785.
36. 2+- dependent interaction of calmodulin with the head domain of synapsin I. Biochem J 275:93-97.
37. Hemmings HC, Girault J-A, Williams KR, LoPresti MB, Greengard P (1989) ARPP-21, a cyclic AMP-regulated phosphoprotein (Mr = 21,000) enriched in dopamine-innervated brain regions. J Biol Chem 264:7726-7733.
38. Hess SD, Doroshenko PA, Augustine GJ (1993) A functional role for GTP-binding proteins in synaptic vesicle cycling. Science 259:1169-1172.
39. 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.
40. 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.
41. Hilfiker S, Czernik AJ, Greengard P, Augustine GJ (2001) Tonically active protein kinase A regulates neurotransmitter release at the squid giant synapse. J Physiol (Lond) 531:141-146.
42. 2+ regulation. J Biol Chem 273:1425-1429.
43. 2+. J Biol Chem 273:13371-13374.
44. Hosaka M, Hammer RE, Südhof TC (1999) A phospho-switch controls the dynamic association of synapsins with synaptic vesicles. Neuron 24:377-387.
45. 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.
46. Hunt JM, Bommert K, Charlton MP, Kistner A, Habermann E, Augustine GJ, Betz H (1994) A postdocking role for synaptobrevin in synaptic vesicle fusion. Neuron 12:1269-1279.
47. Hurley SL, Brown DL, Cheetham JJ (2004) Cytoskeletal interactions of synapsin I in non-neuronal cells. Biochem Biophys Res Commun 317:16-23.
48. Huttner WB, Greengard P (1979) Multiple phosphorylation sites in protein I and their differential regulation by cyclic AMP and calcium. Proc Natl Acad Sci USA 76:5402-5406.
49. Huttner WB, Schiebler W, Greengard P, De Camilli P (1983) Synapsin I (Protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J Cell Biol 96:1374-1388.
50. Job C, Lagnado L (1998) Calcium and protein kinase C regulate the actin cytoskeleton in the synaptic terminal of retinal bipolar cells. J Cell Biol 143:1661-1672.
51. Kaczmarek LK, Jennings KR, Strumwasser F, Nairn AC, Walter U, Wilson FD, Greengard P (1980) Microinjection of catalytic subunit of cyclic AMP-dependent protein kinase enhances calcium action potentials of bag cell neurons in cell culture. Proc Natl Acad Sci USA 77:7487-7491.
52. Kao HT, Porton B, Czernik AJ, Feng J, Yiu G, Haring M, Benfenati F, Greengard P (1998) A third member of the synapsin gene family. Proc Natl Acad Sci USA 95:4667-4672.
53. 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.
54. Klagges BR, Heimbeck G, Godenschwege TA, Hofbauer A, Pflugfelder GO, Reifegerste R, Reisch D, Schaupp M, Buchner S, Buchner E (1996) Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J Neurosci 16:3154-3165.
55. Kuromi H, Kidokoro Y (1998) Two distinct pools of synaptic vesicles in single presynaptic boutons in temperature-sensitive drosophila mutant, shibire. Neuron 20:917-925.
56. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
57. Li L, Chin LS, Shupliakov O, Brodin L, Sihra TS, Hvalby O, Jensen V, Zheng D, McNamara JO, Greengard P (1995) Impairment of synaptic vesicle clustering and of synaptic transmission, and increased seizure propensity, in synapsin I-deficient mice. Proc Natl Acad Sci USA 92:9235-9239.
58. Morales M, Colicos MA, Goda Y (2000) Actin-dependent regulation of neurotransmitter release at central synapses. Neuron 27:539-550.
59. 2+-dependent interaction with calmodulin is conserved in the synapsin family: identification of a high-affinity site. Biochemistry 36:11487-11495.
60. O'Connor V, Heuss C, DeBello WM, Dresbach T, Charlton MP, Hunt JH, Pellegrini LL, Hodel A, Burger MM, Betz H, Augustine GJ, Schaefer T (1997) Disruption of syntaxin-mediated protein interactions blocks neurotransmitter secretion. Proc Natl Acad Sci USA 94:12186-12191.
61. Parsons TD, Coorssen JR, Horstmann H, Almers W (1995) Docked granules, the exocytotic burst, and the need for ATP hydrolysis in endocrine cells. Neuron 15:1085-1096.
62. Petrucci T, Morrow JS (1987) Synapsin I: an actin-bundling protein under phosphorylation control. J Cell Biol 105:1355-1363.
63. Picciotto MR, Cohn JA, Bertuzzi G, Greengard P, Nairn AC (1992) Phosphorylation of the cystic fibrosis transmembrane conductance regulator. J Biol Chem 267:12742-12752.
64. Picciotto MR, Czernik AJ, Nairn AC (1993) Calcium/calmodulin-dependent protein kinase I. CDNA cloning and identification of autophosphorylation site. J Biol Chem 268:26512-26521.
65. 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.
66. Quetglas S, Iborra C, Sasakawa N, De Haro L, Kumakura K, Sato K, Leveque C, Seagar M (2002) Calmodulin and lipid binding to synaptobrevin regulates calcium-dependent exocytosis. EMBO J 21:3970-3979.
67. Rosahl TW, Geppert M, Spillane D, Herz J, Hammer RE, Malenka RC, Südhof TC (1993) Short-term synaptic plasticity is altered in mice lacking synapsin I. Cell 75:661-670.
68. Rosahl TW, Spillane D, Missler M, Herz J, Seling OK, Wolff JR, Hammer RE, Malenka RC, Südhof TC (1995) Essential functions of synapsins I and II in synaptic vesicle regulation. Nature 375:488-493.
69. Sanchez ME, Nuno CM, Buchanan J, Augustine GJ (1990) Contractions of the squid stellate ganglion. J Exp Biol 152:269-387.
70. Sankaranarayanan S, Atluri PP, Ryan TA (2003) Actin has a molecular scaffolding, not propulsive, role in presynaptic function. Nat Neurosci 6:127-134.
71. Sakaba T, Neher E (2003) Involvement of actin polymerization in vesicle recruitment at the calyx of Held synapse. J Neurosci 23:837-846.
72. Schiebler W, Jahn R, Doucet JP, Rothlein J, Greengard P (1986) Characterization of synapsin I binding to small synaptic vesicles. J Biol Chem 261:8383-8390.
73. Schikorski T, Stevens CF (1997) Quantitative ultrastructural analysis of hippocampal excitatory synapses. J Neurosci 17:5858-5867.
74. Schweizer FE, Dresbach T, DeBello WM, O'Connor V, Augustine GJ, Betz H (1998) Regulation of neurotransmitter release kinetics by NSF. Science 279:1203-1206.
75. Shupliakov O, Bloom O, Gustafsson JS, Kjaerulff O, Löw P, Tomilin N, Pieribone VA, Greengard P, Brodin L (2002) Impaired recycling of synaptic vesicles after acute perturbation of the presynaptic actin cytoskeleton. Proc Natl Acad Sci USA 99:14476-14481.
76. Sihra TS, Wang JK, Gorelick FS, Greengard P (1989) Translocation of synapsin I in response to depolarization of isolated nerve terminals. Proc Natl Acad Sci USA 86:8108-8112.
77. 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.
78. Swandulla D, Hans M, Zipser K, Augustine GJ (1991) Role of residual calcium in synaptic depression and posttetanic potentiation: fast and slow calcium signaling in nerve terminals. Neuron 7:915-926.
79. 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.
80. Tanaka T, Kato H, Nishioka T, Oda J (1992) Mutational and proteolytic studies on a flexible loop in glutathione synthetase from Escherichia coli B: the loop and arginine 233 are critical for the catalytic reaction. Biochemistry 31:2259-2265.
81. Thiel G, Südhof TC, Greengard P (1990) Synapsin II. Mapping of a domain in the NH2-terminal region which binds to small synaptic vesicles. J Biol Chem 265:16527-16533.
82. Torri-Tarelli F, Bossi M, Fesce R, Greengard P, Valtorta F (1992) Synapsin I partially dissociates from synaptic vesicles during exocytosis induced by electrical stimulation. Neuron 9:1143-1153.
83. Valtorta F, Greengard P, Fesce R, Chieregatti E, Benfenati F (1992) Effects of the neuronal phosphoprotein synapsin I on actin polymerization. J Biol Chem 267:11281-11288.
84. Walsh DA, Glass DB (1991) Utilization of the inhibitor protein of adenosine cyclic monophosphate-dependent protein kinase, and peptides derived from it, as tools to study adenosine cyclic monophosphate-mediated cellular processes. Methods Enzymol 201:304-316.
85. Walsh DA, Ashby CD, Gonzalez C, Calkins D, Fischer EH, Krebs EG (1971) Purification and characterization of a protein inhibitor of adenosine 3′,5′-monophosphate-dependent protein kinases. J Biol Chem 246:1977-1985.
86. Wang XH, Zheng JQ, Poo MM (1996) Effect of cytochalasin treatment in short-term synaptic plasticity at developing neuromuscular junctions in frogs. J Physiol (Lond) 491:187-195.