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Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
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The role of lipid binding for the targeting of synaptic proteins into synaptic vesicles

  • Jang, Deok-Jin (National Creative Research Initiative Center for Memory, Department of Biological Sciences, College of Natural Sciences, Seoul National University) ;
  • Park, Soo-Won (National Creative Research Initiative Center for Memory, Department of Biological Sciences, College of Natural Sciences, Seoul National University) ;
  • Kaang, Bong-Kiun (National Creative Research Initiative Center for Memory, Department of Biological Sciences, College of Natural Sciences)
  • Published : 2009.01.31
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Abstract

Synaptic vesicles (SVs) are key structures for synaptic transmission in neurons. Numerous membrane-associated proteins are sorted from the Golgi complex to the axon and the presynaptic terminal. Protein-protein and protein-lipid interactions are involved with SV targeting in neurons. Interestingly, many SV proteins have lipid binding capability, primarily with either cholesterol or phosphoinositides (PIs). As examples, the major SV protein synaptophysin can bind to cholesterol, a major lipid component in SVs, while several other SV proteins, including synaptotagmin, can bind to PIs. Thus, lipid-protein binding plays a key role for the SV targeting of synaptic proteins. In addition, numerous SV proteins can be palmitoylated. Palmitoylation is thought to be another synaptic targeting signal. Here, we briefly describe the relationship between lipid binding and SV targeting.

Keywords

References

  1. Bonanomi, D., Benfenati, F. and Valtorta, F. (2006) Protein sorting in the synaptic vesicle life cycle, Prog. Neurobiol. 80, 177-217 https://doi.org/10.1016/j.pneurobio.2006.09.002
  2. Takamori, S., Holt, M., Stenius, K., Lemke, E. A., Gronborg, M., Riedel, D., Urlaub, H., Schenck, S., Brugger, B., Ringler, P., Muller, S. A., Rammner, B., Grater, F., Hub, J. S., De Groot, B. L., Mieskes, G., Moriyama, Y., Klingauf, J., Grubmuller, H., Heuser, J., Wieland, F. and Jahn, R. (2006) Molecular anatomy of a trafficking organelle. Cell 127, 831-846 https://doi.org/10.1016/j.cell.2006.10.030
  3. Park, H., Lee, J. A., Lee, C., Kim, M. J., Chang, D. J., Kim, H., Lee, S. H., Lee, Y. S. and Kaang, B. K. (2005) An Aplysia type 4 phosphodiesterase homolog localizes at the presynaptic terminals of Aplysia neuron and regulates synaptic facilitation. J. Neurosci. 25, 9037-9045 https://doi.org/10.1523/JNEUROSCI.1989-05.2005
  4. Rohrbough, J. and Broadie, K. (2005) Lipid regulation of the synaptic vesicle cycle. Nat. Rev. Neurosci. 6, 139-150 https://doi.org/10.1038/nrn1608
  5. Santos, M. S., Li, H. and Voglmaier, S. M. (2008) Synaptic vesicle protein trafficking at the glutamate synapse. Neuroscience (in press)
  6. Mundigl, O., Matteoli, M., Daniell, L., Thomas-Reetz, A., Metcalf, A., Jahn, R. and De Camilli, P. (1993) Synaptic vesicle proteins and early endosomes in ultured hippocampal neurons: differential effects of Brefeldin A in axon and dendrites. J. Cell Biol. 122, 1207-1221 https://doi.org/10.1083/jcb.122.6.1207
  7. Mills, I. G., Jones, A. T. and Clague, M. J. (1998) Involvement of the endosomal autoantigen EEA1 in homotypic fusion of early endosomes. Curr. Biol. 8, 881-884 https://doi.org/10.1016/S0960-9822(07)00351-X
  8. Pfrieger, F. W. (2003) Role of cholesterol in synapse formation and function. Biochim. Biophys. Acta 1610, 271-280 https://doi.org/10.1016/S0005-2736(03)00024-5
  9. Di Paolo, G. and De Camilli, P. (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443, 651-657 https://doi.org/10.1038/nature05185
  10. Wood, W. G., Schroeder, F., Avdulov, N. A., Chochina, S. V. and Igbavboa, U. (1999) Recent advances in brain cholesterol dynamics: transport, domains, and Alzheimer's disease. Lipids 34, 225-234 https://doi.org/10.1007/s11745-999-0357-9
  11. Thiele, C., Hannah, M. J., Fahrenholz, F. and Huttner, W. B. (2000) Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nat. Cell Biol. 2, 42-49 https://doi.org/10.1038/71366
  12. Nagler, K., Mauch, D. H. and Pfrieger, F. W. (2001) Gliaderived signals induce synapse formation in neurones of the rat central nervous system. J. Physiol. 533, 665-679 https://doi.org/10.1111/j.1469-7793.2001.00665.x
  13. Wasser, C. R., Ertunc, M., Liu, X. and Kavalali, E. T. (2007) Cholesterol-dependent balance between evoked and spontaneous synaptic vesicle recycling. J. Physiol. 579, 413-429 https://doi.org/10.1113/jphysiol.2006.123133
  14. Pennuto, M., Bonanomi, D., Benfenati, F. and Valtorta, F. (2003) Synaptophysin I controls the targeting of VAMP2/synaptobrevin II to synaptic vesicles. Mol. Biol. Cell 14, 4909-4919 https://doi.org/10.1091/mbc.E03-06-0380
  15. Daly, C. and Ziff, E. B. (2002) Ca2+-dependent formation of a dynamin-synaptophysin complex: potential role in synaptic vesicle endocytosis. J. Biol. Chem. 277, 9010-9015 https://doi.org/10.1074/jbc.M110815200
  16. Hanada, K., Kumagai, K., Yasuda, S., Miura, Y., Kawano, M., Fukasawa, M. and Nishijima, M. (2003) Molecular machinery for non-vesicular trafficking of ceramide. Nature 426, 803-809 https://doi.org/10.1038/nature02188
  17. Guo, J., Wenk, M. R., Pellegrini, L., Onofri, F., Benfenati, F. and De Camilli, P. (2003) Phosphatidylinositol 4-kinase type IIalpha is responsible for the phosphatidylinositol 4-kinase activity associated with synaptic vesicles. Proc. Natl. Acad. Sci. U.S.A. 100, 3995-4000 https://doi.org/10.1073/pnas.0230488100
  18. McPherson, P. S., Garcia, E. P., Slepnev, V. I., David, C., Zhang, X., Grabs, D., Sossin, W. S., Bauerfeind, R., Nemoto, Y. and De Camilli, P. (1996) A presynaptic inositol-5-phosphatase. Nature 379, 353-357 https://doi.org/10.1038/379353a0
  19. Watt, S. A., Kular, G., Fleming, I. N., Downes, C. P. and Lucocq, J. M. (2002) Subcellular localization of phosphatidylinositol 4,5-bisphosphate using the pleckstrin homology domain of phospholipase C delta1. Biochem. J. 363, 657-666 https://doi.org/10.1042/0264-6021:3630657
  20. Schiavo, G., Gu, Q. M., Prestwich, G. D., Sollner, T. H. and Rothman, J. E. (1996) Calcium-dependent switching of the specificity of phosphoinositide binding to synaptotagmin. Proc. Natl. Acad. Sci. U.S.A. 93, 13327-13332 https://doi.org/10.1073/pnas.93.23.13327
  21. Barylko, B., Gerber, S. H., Binns, D. D., Grichine, N., Khvotchev, M., Sudhof, T. C. and Albanesi, J. P. (2001) A novel family of phosphatidylinositol 4-kinases conserved from yeast to humans. J. Biol. Chem. 276, 7705-7708 https://doi.org/10.1074/jbc.C000861200
  22. Chang, S., Daniell, L., Arioka, M., Martin, T. F. and De Camilli, P. (2001) PIP kinase Igamma is the major PI(4,5) P(2) synthesizing enzyme at the synapse. Neuron 32, 79-88 https://doi.org/10.1016/S0896-6273(01)00456-1
  23. Di Paolo, G., Moskowitz, H. S., Gipson, K., Wenk, M. R., Voronov, S., Obayashi, M., Flavell, R., Fitzsimonds, R. M., Ryan, T. A. and De Camilli, P. (2004) Impaired PtdIns (4,5)P2 synthesis in nerve terminals produces defects in synaptic vesicle trafficking. Nature 431, 415-422 https://doi.org/10.1038/nature02896
  24. El-Husseini Ael, D. and Bredt, D. S. (2002) Protein palmitoylation: a regulator of neuronal development and function. Nat. Rev. Neurosci. 3, 791-802 https://doi.org/10.1038/nrn940
  25. El-Husseini Ael, D., Craven, S. E., Brock, S. C. and Bredt, D. S. (2001) Polarized targeting of peripheral membrane proteins in neurons. J. Biol. Chem. 276, 44984-44992 https://doi.org/10.1074/jbc.M103049200
  26. Kanaani, J., el-Husseini Ael, D., Aguilera-Moreno, A., Diacovo, J. M., Bredt, D. S. and Baekkeskov, S. (2002) A combination of three distinct trafficking signals mediates axonal targeting and presynaptic clustering of GAD65. J. Cell Biol. 158, 1229-1238 https://doi.org/10.1083/jcb.200205053
  27. McCabe, J. B. and Berthiaume, L. G. (2001) N-terminal protein acylation confers localization to cholesterol, sphingolipid-enriched membranes but not to lipid rafts/caveolae. Mol. Biol. Cell 12, 3601-3617 https://doi.org/10.1091/mbc.12.11.3601
  28. Hannah, M. J., Weiss, U. and Huttner, W. B. (1998) Differential extraction of proteins from paraformaldehyde- fixed cells: lessons from synaptophysin and other membrane proteins. Methods 16, 170-181 https://doi.org/10.1006/meth.1998.0664

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