Lipid regulation of the synaptic vesicle cycle

Nature Reviews Neuroscience

Volumn 6, Issue 2, 2005, Pages 139-150

  Rohrbough, Jeffrey ^a   Broadie, Kendal ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIPID; PROTEIN;

CELL MEMBRANE; EXOCYTOSIS; LIPID MEMBRANE; LIPID RAFT; LIPID VESICLE; MEMBRANE VESICLE; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; REVIEW; SYNAPSE VESICLE; SYNAPTIC MEMBRANE;

ANIMALS; ENDOCYTOSIS; ENZYMES; EXOCYTOSIS; LIPIDS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; PROTEIN TRANSPORT; SYNAPSES; SYNAPTIC VESICLES;

PANTHERA LEO;

EID: 13244275403     PISSN: 1471003X     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrn1608     Document Type: Review

References (142)

1. Sudhof, T. C. The synaptic vesicle cycle. Annu. Rev. Neurosci. 27, 509-547 (2004).
2. Cremona, O. et al. Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 99, 179-188 (1999).
3. Cremona, O. & De Camilli, P. Phosphoinositides in membrane traffic at the synapse. J. Cell Sci. 114, 1041-1052 (2001).
4. Martin, T. F. PI(4,5)P(2) regulation of surface membrane traffic. Curr. Opin. Cell Biol. 13, 493-499 (2001). An excellent, comprehensive review of PtdIns(4,5)P2 distribution, domain formation, protein interactions and regulation of vesicle fusion, endocytosis and trafficking.
5. Di Paolo, G. et al. Impaired PtdIns(4.5)P2 synthesis in nerve terminals produces defects in synaptic vesicle trafficking Nature 431, 415-422 (2004). This study investigated functional synaptic transmission properties in neurons cultured from PIPK1 γ-mutant mice to determine the effect of inhibiting activity-dependent synaptic PtdIns(4,5)P2 synthesis. PtdIns(4,5)P2-deficient neurons have smaller synaptic vesicle releasable pools, delayed endocytosis and greater synaptic depression, which is consistent with PtdIns(4,5)P2 synthesis regulating multiple synaptic vesicle cycle stages.
6. Osborne, S. L., Meunier, F. A. & Schiavo, G. Phosphoinositides as key regulators of synaptic function. Neuron 32, 9-12 (2001).
7. Wenk, M. R. & De Camilli, P. Protein-lipid interactions and pnosphoinositide metabolism in membrane traffic: insights from vesicle recycling in nerve terminals. Proc. Natl Acad. Sci. USA 101, 8262-8269 (2004).
8. Huttner, W. B. & Schmidt, A. Lipids, lipid modification and lipid-protein interaction in membrane budding and fission - insights from the roles of endophiln A1 and synaptophysin in synaptic vesicle endocytosis. Curr. Opin. Neurobiol. 10, 543-551 (2000).
9. Martin, T. F. Racing lipid rafts for synaptic-vesicle formation. Nature Cell Biol. 2, E9-E11 (2000).
10. Wu, L., Bauer, C. S., Zhen, X. G., Xie, C. & Yang, J. Dual regulation of voltage-gated calcium channels by PtdIns(4,5)P2. Nature 419, 947-952 (2002).
11. Aravamudan, B., Fergestad, T., Davis, W. S., Rodesch, C. K. & Broadie, K. Drosophila Unc-13 is essential for synaptic transmission. Nature Neurosci. 2, 965-971 (1999).
12. Augustin, I., Rosenmund, C., Sudhof, T. C. & Brose, N. Munc13-1 is essential for fusion competence of glutamatergic synaptic vesicles. Nature 400, 457-461 (1999).
13. Rhee, J. S. et al. β phorbolester-and diacylglycerol-induced augmentation of transmitter release is mediated by Munc13s and not by PKCs. Cell 108, 121-133 (2002).
14. Richmond, J. E., Davis, W. S. & Jorgensen, E. M. UNC-13 is required for synaptic vesicle fusion in C. elegans. Nature Neurosci 2, 959-964 (1999).
15. Martin, T. F. Prime movers of synaptic vesicle exocytosis. Neuron 34, 9-12 (2002).
16. Rosenmund, C. et al. Differential control of vesicle priming and short-term plasticity by Munc13 isoforms. Neuron 33, 411-424 (2002).
17. 2+ and inositol polyphosphate binding protein, in neurotransmitter release and neurite outgrowth. Chem. Phys. Lipids 98, 59-67 (1999).
18. Schiavo, G., Gu, Q. M., Prestwich, G. D., Sollner, T. H. & Rothman, J. E. Calcium-dependent switching of the specificity of phosphoinositide binding to synaptotagmin. Proc. Natl Acad. Sci. USA 93, 13327-13332 (1996).
19. Okamoto, M. & Sudhof, T. C. Mints, Mund 8-interacting proteins in synaptic vesicle exocytosis. J. Biol. Chem. 272, 31459-31464 (1997).
20. Jahn, R. & Grubmuller, H. Membrane fusion. Curr. Opin. Cell Biol. 14, 488-495 (2002).
21. Salaun, C., James, D. J. & Chamberlain, L. H. Lipid rafts and the regulation of exocytosis. Traffic 5, 255-264 (2004).
22. 2+-activated secretion. Nature 374, 173-177 (1995).
23. Cohen, J. S. & Brown, H. A. Phospholipases stimulate secretion in RBL mast cells. Biochemistry 40, 6589-6597 (2001).
24. Ivanova, P. T. et al. Electrospray ionization mass spectrometry analysis of changes in phospholipids in RBL-2H3 mastocytoma cells during degranulation. Proc. Natl Acad. Sci. USA 98, 7152-7157 (2001).
25. Staneva, G., Angelova, M. I. & Koumanov, K. Phospholipase A2 promotes raft budding and fission from giant liposomes. Chem. Phys. Lipids 129, 53-62 (2004).
26. Brown, W. J., Chambers, K. & Doody, A. Phospholipase A2 (PLA2) enzymes in membrane trafficking: mediators of membrane shape and function. Traffic 4, 214-221 (2003).
27. Wei, S. et al. Group IIA secretory phospholipase A2 stimulates exocytosis and neurotransmitter release in pheochromocytoma-12 cells and cultured rat hippocampal neurons. Neuroscience 121, 891-898 (2003).
28. Brown, F. D. et al. Phospholipase D1 localises to secretory granules and lysosomes and is plasma-membrane translocated on cellular stimulation. Curr. Biol. 8, 835-838 (1998).
29. Choi, W. S., Kim, Y. M., Combs, C., Frohman, M. A. & Beaven, M. A. Phospholipases D1 and D2 regulate different phases of exocytosis in mast cells. J. Immunol. 168, 5682-5689 (2002).
30. Vitale, N. et al. Phospholipase D1: a key factor for the exocytotic machinery in neuroendocrine cells. EMBO J. 20, 2424-2434 (2001).
31. Caumont, A. S., Galas, M. C., Vitale, N., Aunis, D. & Bader, M. F. Regulated exocytosis in chromaffin cells. Translocation of ARF6 stimulates a plasma membrane-associated phospholipase D. J. Biol. Chem. 273, 1373-1379 (1998).
32. Humeau, Y. et al. A role for phospholipase D1 in neurotransmitter release. Proc. Natl Acad. Sci. USA 98, 15300-15305 (2001).
33. Van Epps, H. A. et al. The zebrafish nrc mutant reveals a role for the polyphosphoinositide phosphatase synaptojanin 1 in cone photoreceptor ribbon anchoring. J. Neurosci. 24, 8641-8650 (2004).
34. Cousin, M. A. et al. Synapsin I-associated phosphatidylinositol 3-kinase mediates synaptic vesicle delivery to the readily releasable pool. J. Biol. Chem. 278, 29065-29071 (2003).
35. Guo, J. et al. Phosphatidylinositol 4-kinase type IIα is responsible for the phosphatidylinositol 4-kinase activity associated with synaptic vesicles. Proc. Natl Acad. Sci. USA 100, 3995-4000 (2003).
36. Huang, F. D., Matthies, H. J., Speese, S. D., Smith, M. A. & Broadie, K. Rolling blackout, a newly identified PIP(2)-DAG pathway lipase required for Drosophila phototransduction. Nature Neurosci. 7, 1070-1078 (2004). Genetic, biochemical and functional analyses in D. melanogaster indicate that RBO is a lipase in the PtdIns(4,5)P2-DAG pathway, which modulates PLC-dependent signalling and is required for phototransduction. Current, unpublished data in conditional mutants further shows that RBO is necessary for synaptic transmission, which indicates that a common lipid-signalling pathway may regulate both processes.
37. Hardie, R. C. Regulation of TRP channels via lipid second messengers. Annu. Rev. Physiol. 65, 735-759 (2003).
38. Hardie, R. C. Regulation of Drosophila TRP channels by lipid messengers. Novartis Found. Symp. 258, 160-167; discussion 167-171, 263-266 (2004).
39. Schmitt, H. & Meves, H. Modulation of neuronal calcium channels by arachidonic acid and related substances. J. Membr. Biol. 145, 233-244 (1995).
40. Meves, H. Modulation of ion channels by arachidonic add. Prog. Neurobiol. 43, 175-186 (1994).
41. Lesa, G. M. et al. Long chain polyunsaturated fatty acids are required for efficient neurotransmission in C. elegans. J. Cell Sci. 116, 4965-4975 (2003).
42. van Blitterswijk, W. J., van der Luit, A. H., Veldman, R. J., Verheij, M. & Borst, J. Ceramide: second messenger or modulator of membrane structure and dynamics? Biochem. J. 369, 199-211 (2003). This useful review discusses physical properties of ceramide that relate to its role in regulating lipid structure and curvature, raft formation and regulatory function, and vesicle formation and trafficking.
43. Tsui-Pierchala, B. A., Encinas, M., Milbrandt, J. & Johnson, E. M. Jr. Lipid rafts in neuronal signaling and function. Trends Neurosci. 25, 412-417 (2002).
44. Hering, H., Lin, C. C. & Sheng, M. Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability. J. Neurosci. 23, 3262-3271 (2003).
45. Cabrera-Poch, N., Sanchez-Ruiloba, L., Rodriguez-Martinez, M. & Iglesias, T. Lipid raft disruption triggers protein kinase C and Src-dependent protein kinase D activation and Kidins220 phosphorylation in neuronal cells. J. Biol. Chem. 279, 28592-28602 (2004).
46. Puri, V. et al. Cholesterol modulates membrane traffic along the endocytic pathway in sphingolipid-storage diseases. Nature Cell Biol. 1, 386-388 (1999).
47. Samuel, B. U. et al. The role of cholesterol and glycosylphosphatidylinositol-anchored proteins of erythrocyte rafts in regulating raft protein content and malarial infection. J. Biol. Chem. 276, 29319-29329 (2001).
48. Lang, T. et al. SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J. 20, 2202-2213 (2001). SNARE-mediated fusion of PC12 secretory vesicles occur in cholesterol-dependent raft-like clusters that localize syntaxin.
49. Deutsch, J. W. & Kelly R. B. Lipids of synaptic vesicles: relevance to the mechanism of membrane fusion. Biochemistry 20, 378-385 (1981).
50. Michaelson, D. M., Barkai, G. & Barenholz, Y. Asymmetry of lipid organization in cholinergic synaptic vesicle membranes. Biochem. J. 211, 155-162 (1983).
51. Benfenati, F., Greengard, P., Brunner, J. & Bahler, M. Electrostatic and hydrophobia interactions of synapsin I and synapsin I fragments with phospholipid bilayers. J. Cell Biol. 108, 1851-1862 (1989).
52. Thiele, C., Hannah, M. J., Fahrenholz, F. & Huttner, W. B. Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nature Cell Biol. 2, 42-49 (2000). This study identified synaptophysin as one of the main cholesterol-binding proteins through the use of photoactivatable cholesterol in PC12 cells. It also showed that synaptic-like vesicle formation is inhibited by cholesterol depletion and proposed that cholesterol-synaptophysin interactions are important for the organization of vesicle constituents and budding.
53. Mitter, D. et al. The synaptophysin/synaptobrevin interaction critically depends on the cholesterol content. J. Neurochem. 84, 35-42 (2003). Synaptophysin is a cholesterol-binding protein that forms a complex with the SNARE protein synaptobrevin. Pharmacological and genetic cholesterol perturbation reduced synaptophysin-synaptobrevin complex formation in non-neuronal cells as well as in hippocampal neurons, indicating that concentrated vesicle cholesterol levels facilitate SNARE complex formation.
54. Subtil, A. et al. Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc. Natl Acad. Sci. USA 96, 6775-6780 (1999).
55. Koudinov, A. R. & Koudinova, N. V. Cholesterol, synaptic function and Alzheimer's disease. Pharmacopsychiatry 36 (Suppl. 2), 3107-3112 (2003).
56. Taverna, E. et al. Role of lipid microdomains in P/Q-type calcium channel (Cav2.1) clustering and function in presynaptic membranes. J. Biol. Chem. 279, 5127-5134 (2004).
57. Chamberlain, L. H., Burgoyne, R. D. & Gould, G. W. SNARE proteins are highly enriched in lipid rafts in PC12 cells: implications for the spatial control of exocytosis. Proc. Natl Acad. Sci. USA 98, 5619-5624 (2001). In PC12 neurosecretory cells, the plasma membrane SNAREs are concentrated in detergent-insoluble lipid raft membranes, whereas the vesicular SNARE synaptobrevin is concentrated in a rafts of different composition, indicating that raft-SNARE interactions are important for regulated vesicle fusion.
58. Chamberlain, L. H. & Gould, G. W. The vesicle- and target-SNARE proteins that mediate Glut4 vesicle fusion are localized in detergent-insoluble lipid rafts present on distinct intracellular membranes. J. Biol. Chem. 277, 49750-49754 (2002).
59. Rozelle, A. L. et al. Phosphatidylinositol 4,5-bisphosphate induces actin-based movement of raft-enriched vesicles through WASP-Arp2/3. Curr. Biol. 10, 311-320 (2000).
60. Klopfenstein, D. R., Tomishige, M., Stuurman, N. & Vale, R. D. Role of phosphatidytinositol(4,5)bisphosphate organization in membrane transport by the Unc104 kinesin motor. Cell 109, 347-358 (2002).
61. Venkataraman, K, & Futerman, A. H. Ceramide as a second messenger: sticky solutions to sticky problems. Trends Cell Biol. 10, 408-412 (2000).
62. Liu, P. & Anderson, R. G. Compartmentalized production of ceramide at the cell surface. J. Biol. Chem. 270, 27179-27185 (1995).
63. Shinghal, R., Scheller, R. H. & Bajjalieh, S. M. Ceramide 1-phosphate phosphatase activity in brain. J. Neurochem. 61, 2279-2285 (1993).
64. Li, R., Blanchette-Mackie, E. J. & Ladisch, S. Induction of endocytic vesicles by exogenous C(6)-ceramide. J. Biol. Chem. 274, 21121-21127 (1999).
65. Chen, C. S. Rosenwald, A. G. & Pagano, R. E. Ceramide as a modulator of endocytosis. J. Biol. Chem. 270, 13291-13297 (1995).
66. Hartel, S., Fanani, M. L. & Maggio, B. Shape transitions and lattice structuring of ceramide-enriched domains generated by sphingomyelinase in lipid monolayers. Biophys. J. 15 Oct 2004 doi:10.152g/biophysj.104.048959.
67. Holopainen, J. M., Angelova, M. I. & Kinnunen, P. K. Vectorial budding of vesicles by asymmetrical enzymatic formation of ceramide in giant liposomes. Biophys. J. 78, 830-838 (2000).
68. Yoshimura, Y., Okino, N., Tani, M. & Ito, M. Molecular cloning and characterization of a secretory neutral ceramidase of Drosophila melanogaster. J. Biochem. (Tokyo) 132, 229-236 (2002).
69. Tani, M., Iida, H. & Ito, M. O-glycosylation of mucin-like domain retains the neutral ceramidase on the plasma membranes as a type II integral membrane protein. J. Biol. Chem. 278, 10523-10530 (2003).
70. Rohrbough, J. et al. Ceramidase regulates synaptic vesicle exocytosis and trafficking. J. Neurosci. 24, 7789-7803 (2004). D. melanogaster SLAB ceramidase mutant synapses have impaired synaptic vesicle priming/fusion and increased reserve pool synaptic vesicle tethering, indicating that the regulation of synaptic sphingolipids and raft environments has a role in synaptic vesicle exocytosis and trafficking.
71. Pagano, R. E., Puri, V. Dominguez, M. & Marks, D. L. Membrane traffic in sphingolipid storage diseases. Traffic 1, 807-815 (2000).
72. McMaster, C. R. Lipid metabolism and vesicle trafficking: more than just greasing the transport machinery. Biochem. Cell Biol. 79, 681-692 (2001).
73. Watanabe, R., Funato, K., Venkataraman, K., Futerman, A. H. & Riezman, H. Sphingolipids are required for the stable membrane association of glycosylphosphatidylinositol-anchored proteins in yeast. J. Biol. Chem. 277, 49538-49544 (2002).
74. Acharya, U., Mowen, M. B., Nagashima, K. & Acharya, J. K. Ceramidase expression facilitates membrane turnover and endocytosis of rhodopsin in photoreceptors. Proc. Natl Acad. Sci. USA 101, 1922-1926 (2004). The second of two important studies from this group showing that retinal ceramidase (SLAB) overexpression correspondingly reduced ceramide concentrations and facilitated membrane and protein recycling, which showed that the sphinolipid pathway mediated modulation of endocytosis.
75. Weimer, R. M. et al. Defects in synaptic vesicle docking in unc-18 mutarus. Nature Neurosci. 6, 1023-1030 (2003).
76. Voets, T. et al. Munc18-1 promotes large dense-core vesicle docking. Neuron 31, 581-591 (2001).
77. Richmond, J. E. & Broadie, K. S. The synaptic vesicle cycle: exocytosis and endocytosis in Drosophila and C. elegans. Curr. Opin. Neurobiol. 12, 499-507 (2002).
78. Kidokoro, Y. Roles of SNARE proteins and synaptotagmin I in synaptic transmission: studies at the Drosophila neuromuscular synapse. Neurosignals 12, 13-30 (2003).
79. Rietveld, A., Neutz, S., Simons, K. & Eaton, S. Association of sterol- and glycosylphosphatidylinositol-linked proteins with Drosophila raft lipid microdomains. J. Biol. Chim. 274, 12049-12054 (1999).
80. Jost, M., Simpson, F., Kavran, J. M., Lemmon, M. A. & Schmid, S. L. Phosphatidylinositol-4,5-bisphosphate is required for endocytic coated vesicle formation. Curr. Biol. 8, 1399-1402 (1998).
81. Krauss, M. et al. ARF6 stimulates clathrin/AP-2 recruitment to synaptic membranes by activating phosphatidylinositol phosphate kinase type 1γ. J. Cell Biol. 162, 113-124 (2003).
82. Arneson, L. S., Kunz, J., Anderson, R. A. & Traub, L. M. Coupled inositide phosphorylation and phospholipase D activation initiates clathrin-coat assembly on lysosomes. J. Biol. Chem. 274, 17794-17805 (1999).
83. Ford, M. G. et al. Simultaneous binding of PtdIns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science 291, 1051-1055 (2001).
84. Padron, D., Wang, Y. J., Yamamoto, M., Yin, H. & Roth, M. G. Phosphatidylinositol phosphate 5-kinase 1β recruits AP-2 to the plasma membrane and regulates rates of constitutive endocytosis. J. Cell Biol. 162, 693-701 (2003).
85. Gaidarov, I. & Keen, J. H. Phosphoinositide-AP-2 interactions required for targeting to plasma membrane clathrin-coated pits. J. Cell Biol. 146, 755-764 (1999).
86. Wenk, M. R. et al. PIP kinase 1γ is the major PI(4,5)P(2) synthesizing enzyme at the synapse. Neuron 32, 79-88 (2001). This report provides evidence that PtdIns(4,5)P2 synthesis and association with clathrin to promote synaptic vesicle endocytosis is antagonistically modulated by the actions of PIPK1γ, which synthesizes PtdIns(4,5)P2 and promotes clathrin binding, and synaptojanin phosphatase, which degrades PtdIns(4,5)P2, thereby allowing clathrin disassembly.
87. Farsad, K. et al. A putative role for intramolecular regulatory mechanisms in the adaptor function of amphiphysin in endocytosis. Neuropharmacology 45, 787-796 (2003).
88. Evergren, E. et al. Amphiphysin is a component of clathrin coats formed during synaptic vesicle recycling at the lamprey giant synapse. Traffic 5, 514-528 (2004).
89. Farge, E. Increased vesicle endocytosis due to an increase in the plasma membrane phosphatidyiserine concentration. Biophys. J. 69, 2501-2506 (1995).
90. Goni, F. M. & Alonso, A. Structure and functional properties of diacylglycerols in membranes. Prog. Lipid Res. 38, 1-48 (1999).
91. Reutens, A. T. & Begley, C. G. Endophilin-1: a multifunctional protein. Int. J. Biochem. Cell Biol. 34, 1173-1177 (2002).
92. Ringstad, N. et al. Endophilin/SH3p4 is required for the transition from early to late stages in clathrin-mediated synaptic vesicle endocytosis. Neuron 24, 143-154 (1999).
93. Schmidt, A. et al. Endophilin I mediates synaptic vesicle formation by transfer of arachidonate to lysophosphatidic acid. Nature 401, 133-141 (1999).
94. Verstreken, P. et al. Endophilin mutations block clathrin-mediated endocytosis but not neurotransmitter release. Cell 109, 101-112 (2002). See reference 107.
95. Farsad, K. et al. Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J. Cell Biol. 155, 193-200 (2001). An important study showing that purified endophilin is able to bind to, and generate curved membrane structures with similar geometry to budding synaptic vesicles. Endophilin's lipid restructuring activity is independent of a catalytic/enzymatic activity and is mediated by an NH2-terminal region BAR domain common to amphiphysin.
96. Peter, B. J. et al. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495-499 (2004).
97. Zimmerberg, J. & McLaughlin, S, Membrane curvature: how BAR domains bend bilayers. Curr. Biol. 14, R250-R252 (2004).
98. Ringstad, N., Nemoto, Y. & De Camili, P. The SH3p4/Sh3p8/SH3p13 protein family: binding partners for synaptojanin and dynamin via a Grb2-like Src homology 3 domain. Proc. Natl Acad. Sci. USA 94, 8569-8574 (1997).
99. Modregger, J., Schmidt, A. A., Ritter, B., Huttner, W. B. & Plomann, M. Characterization of Endophilin B1b, a brain-specific membrane-associated lysophosphatidic acid acyl transferase with properties distinct from endophilin A1. J. Biol. Chem. 278, 4160-4167 (2003).
100. Micheva, K. D., Ramjaun, A. R., Kay, B. K. & McPherson, P. S. SH3 domain-dependent interactions of endophilin with amphiphysin. FEBS Lett. 414, 308-312 (1997).
101. Lin, H. C., Barylko, B., Achiriloaie, M. & Albanesi, J. P. Phosphatidylinostol(4,5)-bisphosphate-dependent activation of dynamins I and II lacking the proline/arginine-rich domains. J. Biol. Chem. 272, 25999-26004 (1997).
102. Vallis, Y., Wigge, P., Marks, B., Evans, P. R. & McMahon, H. T. Importance of the pleckstrin homology domain of dynamin in clathrin-mediated endocytosis. Curr. Biol. 9, 257-260 (1999).
103. Achiriloaie, M., Barylko, B. & Albanesi, J. P. Essential role of the dynamin pleckstrin homology domain in receptor-mediated endocytosis. Mol. Cell. Biol. 19, 1410-1415 (1999).
104. Chung, J. K. et al. Synaptojanin inhibition of phospholipase D activity by hydrolysis of phosphatidylinositol 4,5-bisphosphate. J. Biol. Chem. 272, 15980-15985 (1997).
105. Lee, S. Y., Wenk, M. R., Kim, Y, Nairn, A. C. & De Camilli, P. Regulation of synaptojanin 1 by cyclin-dependent kinase 5 at synapses. Proc. Natl Acad. Sci. USA 101, 546-551 (2004).
106. Tan, T. C. et al. Cdk5 is essential for synaptic vesicle endocytosis. Nature Cell Biol. 5, 701-710 (2003).
107. Verstreken, P. et al. Synaptojanin is recruited by endophilin to promote synaptic vesicle uncoating. Neuron 40, 733-748 (2003). References 94 and 107 describe two studies in D. melanogaster. The first shows that endophilin is required for clathrin-dependent synaptic vesicle endocytosis and to maintain synaptic vesicle population, although it is not required for the transmission mediated by a small pool of vesicles released and cycled at the active zone. The second study investigates endophilin and synaptojanin, and shows that the proteins are colocalized in synaptic terminals, interact biochemically and function in the same pathway to regulate synaptic vesicle endocytosis and transmission.
108. Schuske, K. R. et al. Endophilin is required for synaptic vesicle endocytosis by localizing synaptojanin. Neuron 40, 749-762 (2003). This study showed that endo and synj mutants in C. elegans have almost indistinguishable endocytic and functional transmitter defects and function at the same trafficking steps. Furthermore, the results show that endophilin is required to stabilize synaptojanin synaptic localization.
109. Kim, W. T. et al. Delayed reentry of recycling vesicles into the fusion-competent synaptic vesicle pool in synaptojanin 1 knockout mice. Proc. Natl Acad. Sci. USA 99, 17143-17148 (2002).
110. Guichet, A. et al. Essential role of endophilin A in synaptic vesicle budding at the Drosophila neuromuscular junction. EMBO J. 21, 1661-1672 (2002).
111. Gad, H. et al. Fission and uncoating of synaptic clathrin-coated vesicles are perturbed by disruption of interactions with the SH3 domain of endophilin. Neuron 27, 301-312 (2000).
112. Harris, T. W., Hartwieg, E., Horvitz, H. R. & Jorgensen, E. M. Mutations in synaptojanin disrupt synaptic vesicle recycling. J. Cell Biol. 150, 589-600 (2000).
113. Kanzaki, M., Furukawa, M., Raab, W. & Pessin, J. E. Phosphatidylinositol 4,5-bisphosphate regulates adipocyte actin dynamics and GLUT4 vesicle recycling. J. Biol. Chem. 279, 30622-30633 (2004).
114. Takenawa, T. & Itoh, T. Phosphoinositides, key molecules for regulation of actin cytoskeletal organization and membrane traffic from the plasma membrane. Biochim. Biophys. Acta 1533, 190-206 (2001).
115. Romiti, E. et al. Localization of neutral ceramidase in caveolin-enriched light membranes of murine endothelial cells. FEBS Lett. 506, 163-168 (2001).
116. Acharya, U, et al. Modulating sphingolipid biosynthetic pathway rescues photoreceptor degeneration. Science 299, 1740-1743 (2003).
117. Kuromi, H. & Kidokoro, Y. Two distinct pools of synaptic vesicles in single presynaptic boutons in a temperature-sensitive Drosophila mutant, shibire. Neuron 20, 917-925 (1998).
118. Delgado, R., Maureira, C., Oliva, C., Kidokoro, Y. & Labarca, P. Size of vesicle pools, rates of mobilization, and recycling at neuromuscular synapses of a Drosophila mutant, shibire. Neuron 28, 941-953(2000).
119. Mozhayeva, M. G., Sara, Y. Liu, X. & Kavalali, E. T. Development of vesicle pools during maturation of hippocampal synapses. J. Neurosci. 22, 654-665 (2002).
120. Ceccaldi, P. E. et al. Dephosphorylated synapsin I anchors synaptic vesicles to actin cytoskeleton: an analysis by videomicroscopy. J. Cell Biol. 128, 905-912 (1995).
121. Dunaevsky, A. & Connor, E. A. F-actin is concentrated in nonrelease domains at frog neuromuscular junctions. J. Neurosci. 20, 6007-6012 (2000).
122. Humeau, Y. et al. Synapsin controls both reserve and releasable synaptic vesicle pools during neuronal activity and short-term plasticity in Aplysia. J. Neurosci. 21, 4195-4206 (2001).
123. Kuromi, H. & Kidokoro, Y. Tetanic stimulation recruits vesicles from reserve pool via a cAMP-mediated process in Drosophila synapses. Neuron 27, 133-143 (2000).
124. Bloom, O. et al. Colocalization of synapsin and actin during synaptic vesicle recycling. J. Cell Biol. 161, 737-747 (2003).
125. Morales, M., Colicos, M. A. & Goda, Y. Actin-dependent regulation of neurotransmitter release at central synapses. Neuron 27, 539-550 (2000).
126. Shupliakov, O. et al. Impaired recycling of synaptic vesicles after acute perturbation of the presynaptic actin cytoskeleton. Proc. Natl Acad. Sci. USA 99, 14476-14481 (2002).
127. Sankaranarayanan, S., Atluri, P. P. & Ryan, T. A. Actin has a molecular scaffolding, not propulsive, role in presynaptic function. Nature Neurosci. 6, 127-135 (2003).
128. Chi, P., Greengard, P. & Ryan, T. A. Synaptic vesicle mobilization is regulated by detinct synapsin I phosphorylation pathways at different frequencies. Neuron 38, 69-78 (2003). This study extends previous work showing that synapsin phosphorylation regulates its dissociation from the synaptic vesicle, thereby allowing the synaptic vesicle mobilization and release. The results indicate that several kinase and phosphorylation pathways are differentially activated at different levels of synaptic activity, allowing synapsin dispersal and vesicle mobilization to be correlated by multiple pathways activated at different levels of neuronal stimulation.
129. Angers, A. et al. Serotonin stimulates phosphorylation of Aplysia synapsin and alters its subcellular distribution in sensory neurons. J. Neurosci. 22, 5412-5422 (2002).
130. 2+-dependent glutamate release in isolated nerve terminals. J. Neurosci. 21, 7944-7953 (2001).
131. Chi, P., Greengard, P. & Ryan, T. A. Synapsin dispersion and reclustering during synaptic activity. Nature Neurosci. 4, 1187-1193 (2001).
132. Cheetham, J. J. et al. Identification of synapsin I peptides that insert into lipid membranes. Biochem. J. 354, 57-66 (2001).
133. Benfenati, F. et al. 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 (1993).
134. Benfenati, F., Valtorta, F., Chieregatti, E. & Greengard, P. Interaction of free and synaptic vesicle-bound synapsin I with F-actin. Neuron 8, 377-386 (1992).
135. Hosaka, M., Hammer, R. E. & Sudhof, T. C. A phospho-switch controls the dynamic association of synapsins with synaptic vesicles. Neuron 24, 377-387 (1999).
136. Fiumara, R. et al. Phosphorylation by cAMP-dependent protein kinase is essential for synapsin-induced enhancement of neurotransmitter release in invertebrate neurons. J. Cell Sci. 117, 5145-5154 (2004).
137. Chin, J., Angers, A., Cleary, L. J., Eskin, A. & Byrne, J. H. Transforming growth factor β1 alters synapsin distribution and modulates synaptic depression in Aplysia. J. Neurosci. 22, RC220 (2002).
138. Pagano, R. E. Endocytic trafficking of glycosphingolipids in sphingolipid storage diseases. Philos. Trans. R. Soc. Lond. B 358, 885-891 (2003).
139. Zanolari, B. et al. Sphingoid base synthesis requirement for endocytosis in Saccharomyces cerevisiae. EMBO J. 19, 2824-2833 (2000).
140. Benfenati, F., Bahler, M., Jahn, R. & Greengard, P. Interactions of synapsin I with small synaptic vesicles: distinct sites in synapsin I bind to vesicle phospholipids and vesicle proteins. J. Cell Biol. 108, 1863-1372 (1989).
141. Esch, S. W., Williams, T. D., Biswas, S., Chakrabarty, A. & Levine, S. M. Sphingolipid profile in the CNS of the twitcher (globoid cell leukodystrophy) mouse: a lipidomics approach. Cell. Mol. Biol. (Noisy-le-grand) 49, 779-787 (2003).
142. Forrester, J. S., Milne, S. B., Ivanova, P. T. & Brown, H. A. Computational lipidomics: a multiplexed analysis of dynamic changes in membrane lipid composition during signal transduction. Mol. Pharmacol. 65, 813-521 (2004).