The role of synapsins in neuronal development

Cellular and Molecular Life Sciences

Volumn 67, Issue 9, 2010, Pages 1383-1396

  Fornasiero, Eugenio F ^a,b   Bonanomi, Dario ^a,b,d   Benfenati, Fabio ^b,c   Valtorta, Flavia ^a,b  

^a VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^b ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^c UNIVERSITY OF GENOA   (Italy)

^d SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Axon elongation; Cytoskeleton; Growth cone; Membrane trafficking; Nerve terminal; Neurotransmitter release; Synaptic vesicle

Indexed keywords

ACTIN; ISOPROTEIN; NEUROTRANSMITTER; PHOSPHOPROTEIN; PROTEIN KINASE; SYNAPSIN;

GENETIC CODE; GENETIC CONSERVATION; HUMAN; MOSAICISM; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NEUROTRANSMITTER RELEASE; NONHUMAN; ORTHOLOGY; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; ANIMAL; CHEMISTRY; CYTOLOGY; CYTOSKELETON; GENETICS; GROWTH CONE; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PHOSPHORYLATION; PHYSIOLOGY; SYNAPSE; ULTRASTRUCTURE;

INVERTEBRATA; MAMMALIA; VERTEBRATA;

ANIMALS; CYTOSKELETON; GROWTH CONES; HUMANS; NEUROGENESIS; NEURONS; PHOSPHORYLATION; PROTEIN ISOFORMS; SYNAPSES; SYNAPSINS; SYNAPTIC TRANSMISSION;

EID: 77952312857     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-009-0227-8     Document Type: Review

References (92)

1. P De Camilli F Benfenati F Valtorta P Greengard 1990 The synapsins Annu Rev Cell Biol 6 433 460 10.1146/annurev.cb.06.110190.002245 1980418
2. P Greengard F Valtorta AJ Czernik F Benfenati 1993 Synaptic vesicle phosphoproteins and regulation of synaptic function Science 259 780 785 10.1126/science.8430330 8430330
3. E Fdez S Hilfiker 2006 Vesicle pools and synapsins: new insights into old enigmas Brain Cell Biol 35 107 115 10.1007/s11068-007-9013-4 17957477 (Pubitemid 47630632)
4. P De Camilli R Cameron P Greengard 1983 Synapsin I (protein I), a nerve terminal-specific phosphoprotein. I. Its general distribution in synapses of the central and peripheral nervous system demonstrated by immunofluorescence in frozen and plastic sections J Cell Biol 96 1337 1354 10.1083/jcb.96.5.1337 6404910
5. P De Camilli SM Harris Jr WB Huttner P Greengard 1983 Synapsin I (protein I), a nerve terminal-specific phosphoprotein. II. Its specific association with synaptic vesicles demonstrated by immunocytochemistry in agarose-embedded synaptosomes J Cell Biol 96 1355 1373 10.1083/jcb.96.5.1355 6404911 (Pubitemid 13029639)
6. WB Huttner W Schiebler P Greengard P De Camilli 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 10.1083/jcb.96.5.1374 6404912 (Pubitemid 13029640)
7. F Benfenati M Bahler R Jahn P Greengard 1989 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 10.1083/jcb.108.5.1863 2497106 (Pubitemid 19130519)
8. 2+/calmodulin-dependent protein kinase II is a binding protein for synapsin I Nature 359 417 420 10.1038/359417a0 1328883
9. A Ferreira HT Kao J Feng M Rapoport P Greengard 2000 Synapsin III: developmental expression, subcellular localization, and role in axon formation J Neurosci 20 3736 3744 10804215
10. HT Kao P Li HM Chao S Janoschka K Pham J Feng BS McEwen P Greengard VA Pieribone B Porton 2008 Early involvement of synapsin III in neural progenitor cell development in the adult hippocampus J Comp Neurol 507 1860 1870 10.1002/cne.21643 18271024 (Pubitemid 351468205)
11. M Bahler P Greengard 1987 Synapsin I bundles F-actin in a phosphorylation-dependent manner Nature 326 704 707 10.1038/326704a0 3104800 (Pubitemid 17059791)
12. F Benfenati F Valtorta E Chieregatti P Greengard 1992 Interaction of free and synaptic vesicle-bound synapsin I with F-actin Neuron 8 377 386 10.1016/0896-6273(92)90303-U 1739463
13. F Valtorta P Greengard R Fesce E Chieregatti F Benfenati 1992 Effects of the neuronal phosphoprotein synapsin I on actin polymerization. I. Evidence for a phosphorylation-dependent nucleating effect J Biol Chem 267 11281 11288 1317863
14. P Baldelli A Fassio F Valtorta F Benfenati 2007 Lack of synapsin I reduces the readily releasable pool of synaptic vesicles at central inhibitory synapses J Neurosci 27 13520 13531 10.1523/JNEUROSCI.3151-07.2007 18057210 (Pubitemid 350255327)
15. F Valtorta F Benfenati P Greengard 1992 Structure and function of the synapsins J Biol Chem 267 7195 7198 1559963
16. PE Ceccaldi F Grohovaz F Benfenati E Chieregatti P Greengard F Valtorta 1995 Dephosphorylated synapsin I anchors synaptic vesicles to actin cytoskeleton: an analysis by videomicroscopy J Cell Biol 128 905 912 10.1083/jcb.128.5.905 7876313
17. TW Rosahl D Spillane M Missler J Herz DK Selig JR Wolff RE Hammer RC Malenka TC Sudhof 1995 Essential functions of synapsins I and II in synaptic vesicle regulation Nature 375 488 493 10.1038/375488a0 7777057
18. L Li LS Chin O Shupliakov L Brodin TS Sihra O Hvalby V Jensen D Zheng JO McNamara P Greengard P Andersen 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 10.1073/pnas.92.20.9235 7568108
19. D Gitler Y Takagishi J Feng Y Ren RM Rodriguiz WC Wetsel P Greengard GJ Augustine 2004 Different presynaptic roles of synapsins at excitatory and inhibitory synapses J Neurosci 24 11368 11380 10.1523/JNEUROSCI.3795-04.2004 15601943 (Pubitemid 39658272)
20. L Siksou P Rostaing JP Lechaire T Boudier T Ohtsuka A Fejtova HT Kao P Greengard ED Gundelfinger A Triller S Marty 2007 Three-dimensional architecture of presynaptic terminal cytomatrix J Neurosci 27 6868 6877 10.1523/JNEUROSCI. 1773-07.2007 17596435 (Pubitemid 47015888)
21. S Hilfiker FE Schweizer HT Kao AJ Czernik P Greengard GJ Augustine 1998 Two sites of action for synapsin domain E in regulating neurotransmitter release Nat Neurosci 1 29 35 10.1038/229 10195105
22. S Hilfiker F Benfenati F Doussau AC Nairn AJ Czernik GJ Augustine P Greengard 2005 Structural domains involved in the regulation of transmitter release by synapsins J Neurosci 25 2658 2669 10.1523/JNEUROSCI.4278-04.2005 15758176 (Pubitemid 40365177)
23. A Fassio D Merlo J Mapelli A Menegon A Corradi M Mete S Zappettini G Bonanno F Valtorta E D'Angelo F Benfenati 2006 The synapsin domain E accelerates the exo-endocytotic cycle of synaptic vesicles in cerebellar Purkinje cells J Cell Sci 119 4257 4268 10.1242/jcs.03194 17038543 (Pubitemid 44774032)
24. M Chiappalone S Casagrande M Tedesco F Valtorta P Baldelli S Martinoia F Benfenati 2009 Opposite changes in glutamatergic and GABAergic transmission underlie the diffuse hyperexcitability of synapsin I-deficient cortical networks Cereb Cortex 19 1422 1439 10.1093/cercor/bhn182 19020204
25. HT Kao B Porton S Hilfiker G Stefani VA Pieribone R DeSalle P Greengard 1999 Molecular evolution of the synapsin gene family J Exp Zool 285 360 377 10.1002/(SICI)1097-010X(19991215)285:4<360::AID-JEZ4>3.0.CO;2-3 10578110
26. L Esser CR Wang M Hosaka CS Smagula TC Sudhof J Deisenhofer 1998 Synapsin I is structurally similar to ATP-utilizing enzymes EMBO J 17 977 984 10.1093/emboj/17.4.977 9463376 (Pubitemid 28077652)
27. 2+ regulation J Biol Chem 273 1425 1429 10.1074/jbc.273.3.1425 9430678 (Pubitemid 28133662)
28. M Hosaka TC Sudhof 1999 Homo-and heterodimerization of synapsins J Biol Chem 274 16747 16753 10.1074/jbc.274.24.16747 10358015 (Pubitemid 29275121)
29. F Onofri M Messa V Matafora G Bonanno A Corradi A Bachi F Valtorta F Benfenati 2007 Synapsin phosphorylation by SRC tyrosine kinase enhances SRC activity in synaptic vesicles J Biol Chem 282 15754 15767 10.1074/jbc.M701051200 17400547 (Pubitemid 47093304)
30. VA Pieribone O Shupliakov L Brodin S Hilfiker-Rothenfluh AJ Czernik P Greengard 1995 Distinct pools of synaptic vesicles in neurotransmitter release Nature 375 493 497 10.1038/375493a0 7777058
31. D Gitler Y Xu HT Kao D Lin S Lim J Feng P Greengard GJ Augustine 2004 Molecular determinants of synapsin targeting to presynaptic terminals J Neurosci 24 3711 3720 10.1523/JNEUROSCI.5225-03.2004 15071120 (Pubitemid 38481129)
32. Monaldi I, Vassalli M, Bachi A, Millo E, Valtorta F, Raiteri R, Benfenati F, Fassio A (2009) The highly conserved synapsin domain E mediates synapsin dimerization and phospholipid vesicle clustering. Biochem J (in press)
33. EM Johnson T Ueda H Maeno P Greengard 1972 Adenosine 3′, 5-monophosphate-dependent phosphorylation of a specific protein in synaptic membrane fractions from rat cerebrum J Biol Chem 247 5650 5652 4341350
34. WB Huttner P Greengard 1979 Multiple phosphorylation sites in protein I and their differential regulation by cyclic AMP and calcium Proc Natl Acad Sci USA 76 5402 5406 10.1073/pnas.76.10.5402 228290 (Pubitemid 10231640)
35. AJ Czernik DT Pang P Greengard 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 10.1073/pnas.84.21.7518 3118371
36. JN Jovanovic F Benfenati YL Siow TS Sihra JS Sanghera SL Pelech P Greengard AJ Czernik 1996 Neurotrophins stimulate phosphorylation of synapsin I by MAP kinase and regulate synapsin I-actin interactions Proc Natl Acad Sci USA 93 3679 3683 10.1073/pnas.93.8.3679 8622996 (Pubitemid 26127596)
37. M Matsubara M Kusubata K Ishiguro T Uchida K Titani H Taniguchi 1996 Site-specific phosphorylation of synapsin I by mitogen-activated protein kinase and Cdk5 and its effects on physiological functions J Biol Chem 271 21108 21113 10.1074/jbc.271.35.21108 8702879 (Pubitemid 26292961)
38. 2+-dependent glutamate release in isolated nerve terminals J Neurosci 21 7944 7953 11588168
39. F Benfenati P Neyroz M Bahler L Masotti P Greengard 1990 Time-resolved fluorescence study of the neuron-specific phosphoprotein synapsin I. Evidence for phosphorylation-dependent conformational changes J Biol Chem 265 12584 12595 2115521
40. M Hosaka RE Hammer TC Sudhof 1999 A phospho-switch controls the dynamic association of synapsins with synaptic vesicles Neuron 24 377 387 10.1016/S0896-6273(00)80851-X 10571231 (Pubitemid 29508411)
41. W Schiebler R Jahn JP Doucet J Rothlein P Greengard 1986 Characterization of synapsin I binding to small synaptic vesicles J Biol Chem 261 8383 8390 3087973
42. F Torri Tarelli M Bossi R Fesce P Greengard F Valtorta 1992 Synapsin I partially dissociates from synaptic vesicles during exocytosis induced by electrical stimulation Neuron 9 1143 1153 10.1016/0896-6273(92)90072-L 1463610 (Pubitemid 23007184)
43. TS Sihra JK Wang FS Gorelick P Greengard 1989 Translocation of synapsin I in response to depolarization of isolated nerve terminals Proc Natl Acad Sci USA 86 8108 8112 10.1073/pnas.86.20.8108 2510160
44. R Llinas TL McGuinness CS Leonard M Sugimori P Greengard 1985 Intraterminal injection of synapsin I or calcium/calmodulin-dependent protein kinase II alters neurotransmitter release at the squid giant synapse Proc Natl Acad Sci USA 82 3035 3039 10.1073/pnas.82.9.3035 2859595 (Pubitemid 15097787)
45. R Llinas JA Gruner M Sugimori TL McGuinness P Greengard 1991 Regulation by synapsin I and Ca(2+)-calmodulin-dependent protein kinase II of the transmitter release in squid giant synapse J Physiol 436 257 282 1676419
46. JT Hackett SL Cochran LJ Greenfield Jr DC Brosius T Ueda 1990 Synapsin I injected presynaptically into goldfish mauthner axons reduces quantal synaptic transmission J Neurophysiol 63 701 706 2160524
47. RA Nichols TS Sihra AJ Czernik AC Nairn P Greengard 1990 Calcium/calmodulin-dependent protein kinase II increases glutamate and noradrenaline release from synaptosomes Nature 343 647 651 10.1038/343647a0 2154695 (Pubitemid 20075512)
48. RA Nichols TJ Chilcote AJ Czernik P Greengard 1992 Synapsin I regulates glutamate release from rat brain synaptosomes J Neurochem 58 783 785 10.1111/j.1471-4159.1992.tb09788.x 1345942
49. F Torri-Tarelli A Villa F Valtorta P De Camilli P Greengard B Ceccarelli 1990 Redistribution of synaptophysin and synapsin I during alpha-latrotoxin- induced release of neurotransmitter at the neuromuscular junction J Cell Biol 110 449 459 10.1083/jcb.110.2.449 1967610
50. P Chi P Greengard TA Ryan 2001 Synapsin dispersion and reclustering during synaptic activity Nat Neurosci 4 1187 1193 10.1038/nn756 11685225 (Pubitemid 33135623)
51. P Chi P Greengard TA Ryan 2003 Synaptic vesicle mobilization is regulated by distinct synapsin I phosphorylation pathways at different frequencies Neuron 38 69 78 10.1016/S0896-6273(03)00151-X 12691665 (Pubitemid 36423354)
52. TW Rosahl M Geppert D Spillane J Herz RE Hammer RC Malenka TC Sudhof 1993 Short-term synaptic plasticity is altered in mice lacking synapsin I Cell 75 661 670 10.1016/0092-8674(93)90487-B 7902212 (Pubitemid 23346365)
53. LS Chin L Li A Ferreira KS Kosik P Greengard 1995 Impairment of axonal development and of synaptogenesis in hippocampal neurons of synapsin I-deficient mice Proc Natl Acad Sci USA 92 9230 9234 10.1073/pnas.92.20.9230 7568107
54. Y Takei A Harada S Takeda K Kobayashi S Terada T Noda T Takahashi N Hirokawa 1995 Synapsin I deficiency results in the structural change in the presynaptic terminals in the murine nervous system J Cell Biol 131 1789 1800 10.1083/jcb.131.6.1789 8557745 (Pubitemid 26007975)
55. TA Ryan L Li LS Chin P Greengard SJ Smith 1996 Synaptic vesicle recycling in synapsin I knock-out mice J Cell Biol 134 1219 1227 10.1083/jcb.134.5.1219 8794863
56. S Terada T Tsujimoto Y Takei T Takahashi N Hirokawa 1999 Impairment of inhibitory synaptic transmission in mice lacking synapsin I J Cell Biol 145 1039 1048 10.1083/jcb.145.5.1039 10352020 (Pubitemid 29270061)
57. J Feng P Chi TA Blanpied Y Xu AM Magarinos A Ferreira RH Takahashi HT Kao BS McEwen TA Ryan GJ Augustine P Greengard 2002 Regulation of neurotransmitter release by synapsin III J Neurosci 22 4372 4380 12040043 (Pubitemid 37465653)
58. AJ Silva TW Rosahl PF Chapman Z Marowitz E Friedman PW Frankland V Cestari D Cioffi TC Sudhof R Bourtchuladze 1996 Impaired learning in mice with abnormal short-lived plasticity Curr Biol 6 1509 1518 10.1016/S0960-9822(96) 00756-7 8939606
59. A Corradi A Zanardi C Giacomini F Onofri F Valtorta M Zoli F Benfenati 2008 Synapsin-I-and synapsin-II-null mice display an increased age-dependent cognitive impairment J Cell Sci 121 3042 3051 10.1242/jcs.035063 18713831
60. D Samigullin CA Bill WL Coleman M Bykhovskaia 2004 Regulation of transmitter release by synapsin II in mouse motor terminals J Physiol 561 149 158 10.1113/jphysiol.2004.073494 15388780 (Pubitemid 39549472)
61. CC Garcia HJ Blair M Seager A Coulthard S Tennant M Buddles A Curtis JA Goodship 2004 Identification of a mutation in synapsin I, a synaptic vesicle protein, in a family with epilepsy J Med Genet 41 183 186 10.1136/jmg.2003. 013680 14985377
62. GL Cavalleri ME Weale KV Shianna R Singh JM Lynch B Grinton C Szoeke K Murphy P Kinirons D O'Rourke D Ge C Depondt KG Claeys M Pandolfo C Gumbs N Walley J McNamara JC Mulley KN Linney LJ Sheffield RA Radtke SK Tate SL Chissoe RA Gibson D Hosford A Stanton TD Graves MG Hanna K Eriksson AM Kantanen R Kalviainen TJ O'Brien JW Sander JS Duncan IE Scheffer SF Berkovic NW Wood CP Doherty N Delanty SM Sisodiya DB Goldstein 2007 Multicentre search for genetic susceptibility loci in sporadic epilepsy syndrome and seizure types: a case-control study Lancet Neurol 6 970 980 10.1016/S1474-4422(07)70247-8 17913586 (Pubitemid 47570022)
63. TL Fletcher P Cameron P De Camilli G Banker 1991 The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture J Neurosci 11 1617 1626 1904480
64. B Lu P Greengard MM Poo 1992 Exogenous synapsin I promotes functional maturation of developing neuromuscular synapses Neuron 8 521 529 10.1016/0896-6273(92)90280-Q 1312849
65. E Schaeffer J Alder P Greengard MM Poo 1994 Synapsin IIa accelerates functional development of neuromuscular synapses Proc Natl Acad Sci USA 91 3882 3886 10.1073/pnas.91.9.3882 8171006
66. R Dunia AA Herrera 1993 Synapse formation and elimination during growth of the pectoral muscle in Xenopus laevis J Physiol 469 501 509 8271210
67. S Cash RS Zucker MM Poo 1996 Spread of synaptic depression mediated by presynaptic cytoplasmic signalling Science 272 998 1001 10.1126/science.272. 5264.998 8638143
68. HQ Han P Greengard 1994 Remodeling of cytoskeletal architecture of non-neuronal cells induced by synapsin Proc Natl Acad Sci USA 91 8557 8561 10.1073/pnas.91.18.8557 8078922
69. A Ferreira KS Kosik P Greengard HQ Han 1994 Aberrant neurites and synaptic vesicle protein deficiency in synapsin II-depleted neurons Science 264 977 979 10.1126/science.8178158 8178158
70. A Ferreira LS Chin L Li LM Lanier KS Kosik P Greengard 1998 Distinct roles of synapsin I and synapsin II during neuronal development Mol Med 4 22 28 9513186
71. A Ferreira HQ Han P Greengard KS Kosik 1995 Suppression of synapsin II inhibits the formation and maintenance of synapses in hippocampal culture Proc Natl Acad Sci USA 92 9225 9229 10.1073/pnas.92.20.9225 7568106
72. A Ferreira L Li LS Chin P Greengard KS Kosik 1996 Postsynaptic element contributes to the delay in synaptogenesis in synapsin I-deficient neurons Mol Cell Neurosci 8 286 299 10.1006/mcne.1996.0064 9026316 (Pubitemid 27057152)
73. HT Kao HJ Song B Porton GL Ming J Hoh M Abraham AJ Czernik VA Pieribone MM Poo P Greengard 2002 A protein kinase A-dependent molecular switch in synapsins regulates neurite outgrowth Nat Neurosci 5 431 437 11976703
74. HE Murrey CI Gama SA Kalovidouris WI Luo EM Driggers B Porton LC Hsieh-Wilson 2006 Protein fucosylation regulates synapsin Ia/Ib expression and neuronal morphology in primary hippocampal neurons Proc Natl Acad Sci USA 103 21 26 10.1073/pnas.0503381102 16373512 (Pubitemid 43076098)
75. F Onofri S Giovedi P Vaccaro AJ Czernik F Valtorta P De Camilli P Greengard F Benfenati 1997 Synapsin I interacts with c-Src and stimulates its tyrosine kinase activity Proc Natl Acad Sci USA 94 12168 12173 10.1073/pnas.94.22.12168 9342381 (Pubitemid 27467861)
76. BA Tucker M Rahimtula KM Mearow 2008 Src and FAK are key early signalling intermediates required for neurite growth in NGF-responsive adult DRG neurons Cell Signal 20 241 257 10.1016/j.cellsig.2007.10.014 17999938 (Pubitemid 350138385)
77. HQ Han RA Nichols MR Rubin M Bahler P Greengard 1991 Induction of formation of presynaptic terminals in neuroblastoma cells by synapsin IIb Nature 349 697 700 10.1038/349697a0 1899916
78. F Valtorta N Iezzi F Benfenati B Lu MM Poo P Greengard 1995 Accelerated structural maturation induced by synapsin I at developing neuromuscular synapses of Xenopus laevis Eur J Neurosci 7 261 270 10.1111/j.1460-9568.1995.tb01062.x 7757263
79. S Giovedì F Darchen F Valtorta P Greengard F Benfenati 2004 Synapsin is a novel Rab3 effector protein on small synaptic vesicles. II. Functional effects of the Rab3A-synapsin I interaction J Biol Chem 279 43769 43779 10.1074/jbc.M404168200 15265868 (Pubitemid 39390682)
80. S Giovedì P Vaccaro F Valtorta F Darchen P Greengard G Cesareni F Benfenati 2004 Synapsin is a novel Rab3 effector protein on small synaptic vesicles. I. Identification and characterization of the synapsin I-Rab3 interactions in vitro and in intact nerve terminals J Biol Chem 279 43760 43768 10.1074/jbc.M403293200 15265865 (Pubitemid 39390681)
81. M Geppert B Ullrich DG Green K Takei L Daniels P De Camilli TC Sudhof RE Hammer 1994 Synaptic targeting domains of synapsin I revealed by transgenic expression in photoreceptor cells EMBO J 13 3720 3727 8070400
82. MA Gaffield WJ Betz 2007 Synaptic vesicle mobility in mouse motor nerve terminals with and without synapsin J Neurosci 27 13691 13700 10.1523/JNEUROSCI.3910-07.2007 18077680 (Pubitemid 350278251)
83. D Gitler Q Cheng P Greengard GJ Augustine 2008 Synapsin IIa controls the reserve pool of glutamatergic synaptic vesicles J Neurosci 28 10835 10843 10.1523/JNEUROSCI.0924-08.2008 18945891
84. TA Godenschwege D Reisch S Diegelmann K Eberle N Funk M Heisenberg V Hoppe J Hoppe BR Klagges JR Martin EA Nikitina G Putz R Reifegerste N Reisch J Rister M Schaupp H Scholz M Schwarzel U Werner TD Zars S Buchner E Buchner 2004 Flies lacking all synapsins are unexpectedly healthy but are impaired in complex behaviour Eur J Neurosci 20 611 622 10.1111/j.1460-9568.2004.03527.x 15255973 (Pubitemid 39036925)
85. NE Ziv CC Garner 2004 Cellular and molecular mechanisms of presynaptic assembly Nat Rev Neurosci 5 385 399 10.1038/nrn1370 15100721
86. P Forscher LK Kaczmarek JA Buchanan SJ Smith 1987 Cyclic AMP induces changes in distribution and transport of organelles within growth cones of Aplysia bag cell neurons J Neurosci 7 3600 3611 2824715
87. D Bonanomi A Menegon A Miccio G Ferrari A Corradi HT Kao F Benfenati F Valtorta 2005 Phosphorylation of synapsin I by cAMP-dependent protein kinase controls synaptic vesicle dynamics in developing neurons J Neurosci 25 7299 7308 10.1523/JNEUROSCI.1573-05.2005 16093379 (Pubitemid 41129801)
88. SL Sabo RA Gomes AK McAllister 2006 Formation of presynaptic terminals at predefined sites along axons J Neurosci 26 10813 10825 10.1523/JNEUROSCI.2052- 06.2006 17050720
89. F Onofri S Giovedi HT Kao F Valtorta L Bongiorno Borbone P De Camilli P Greengard F Benfenati 2000 Specificity of the binding of synapsin I to Src homology 3 domains J Biol Chem 275 29857 29867 10.1074/jbc.M006018200 10899172 (Pubitemid 32043871)
90. B Porton HT Kao P Greengard 1999 Characterization of transcripts from the synapsin III gene locus J Neurochem 73 2266 2271 10.1046/j.1471-4159.1999. 0732266.x 10582583
91. P Baldelli A Fassio A Corradi O Cremona F Valtorta F Benfenati 2005 Synapsins and neuroexocytosis: recent views from functional studies on synapsin null mutant mice Arch Ital Biol 143 113 126 16106992
92. CG Dotti CA Sullivan GA Banker 1988 The establishment of polarity by hippocampal neurons in culture J Neurosci 8 1454 1468 3282038