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Cdk5 in Presynapses

  • Fan-Yan Wei
  • Kazuhito Tomizawa
Chapter

Abstract

Recent studies have explored the indispensable roles of Cdk5 in presynapse. Presynapse is the structure in which neurotransmitter-containing synaptic vesicles are fused to the synaptic membrane and recycled to internal compartments via exocytosis and endocytosis, respectively. Cdk5 is involved in the regulation of the exocytosis and endocytosis of synaptic vesicles.

Keywords

Synaptic Vesicle Presynaptic Terminal Presynaptic Membrane Loop Domain Reserve Pool 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Bahler, M. and Greengard, P. (1987). Synapsin I bundles F-actin in a phosphorylation-dependent manner. Nature 326, 704–707.PubMedCrossRefGoogle Scholar
  2. Bauerfeind, R., Takei, K., and De, C.P. (1997). Amphiphysin I is associated with coated endocytic intermediates and undergoes stimulation-dependent dephosphorylation in nerve terminals. J. Biol. Chem. 272, 30984–30992.PubMedCrossRefGoogle Scholar
  3. Benfenati, F., Neyroz, P., Bahler, M., Masotti, L., and Greengard, P. (1990). Time-resolved fluorescence study of the neuron-specific phosphoprotein synapsin I. Evidence for phosphorylation-dependent conformational changes. J. Biol. Chem. 265, 12584–12595.PubMedGoogle Scholar
  4. Bhaskar, K., Shareef, M.M., Sharma, V.M., Shetty, A.P., Ramamohan, Y., Pant, H.C., Raju, T.R., and Shetty, K.T. (2004). Co-purification and localization of Munc18-1 (p67) and Cdk5 with neuronal cytoskeletal proteins. Neurochem. Int. 44, 35–44.PubMedCrossRefGoogle Scholar
  5. Cho, S. and Meriney, S.D. (2006). The effects of presynaptic calcium channel modulation by roscovitine on transmitter release at the adult frog neuromuscular junction. Eur. J. Neurosci. 23, 3200–3208.PubMedCrossRefGoogle Scholar
  6. Cremona, O., Di, P.G., Wenk, M.R., Luthi, A., Kim, W.T., Takei, K., Daniell, L., Nemoto, Y., Shears, S.B., Flavell, R.A., McCormick, D.A., and De, C.P. (1999). Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 99, 179–188.PubMedCrossRefGoogle Scholar
  7. Czernik, A.J., Pang, D.T., and 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. U.S.A. 84, 7518–7522.PubMedCrossRefGoogle Scholar
  8. De, C.P., Cameron, R., and Greengard, P. (1983a). 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.CrossRefGoogle Scholar
  9. De, C.P., Emr, S.D., McPherson, P.S., and Novick, P. (1996). Phosphoinositides as regulators in membrane traffic. Science 271, 1533–1539.CrossRefGoogle Scholar
  10. De, C.P., Harris, S.M., Jr., Huttner, W.B., and Greengard, P. (1983b). 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.CrossRefGoogle Scholar
  11. Earnest, S., Khokhlatchev, A., Albanesi, J.P., and Barylko, B. (1996). Phosphorylation of dynamin by ERK2 inhibits the dynamin-microtubule interaction. FEBS Lett. 396, 62–66.PubMedCrossRefGoogle Scholar
  12. Fletcher, A.I., Shuang, R., Giovannucci, D.R., Zhang, L., Bittner, M.A., and Stuenkel, E.L. (1999). Regulation of exocytosis by cyclin-dependent kinase 5 via phosphorylation of Munc18. J. Biol. Chem. 274, 4027–4035.PubMedCrossRefGoogle Scholar
  13. Floyd, S.R., Porro, E.B., Slepnev, V.I., Ochoa, G.C., Tsai, L.H., and De, C.P. (2001). Amphiphysin 1 binds the cyclin-dependent kinase (cdk) 5 regulatory subunit p35 and is phosphorylated by cdk5 and cdc2. J. Biol. Chem. 276, 8104–8110.PubMedCrossRefGoogle Scholar
  14. Fujita, Y., Sasaki, T., Fukui, K., Kotani, H., Kimura, T., Hata, Y., Sudhof, T.C., Scheller, R.H., and Takai, Y. (1996). Phosphorylation of Munc-18/n-Sec1/rbSec1 by protein kinase C: its implication in regulating the interaction of Munc-18/n-Sec1/rbSec1 with syntaxin. J. Biol. Chem. 271, 7265–7268.PubMedCrossRefGoogle Scholar
  15. Grabs, D., Slepnev, V.I., Songyang, Z., David, C., Lynch, M., Cantley, L.C., and De, C.P. (1997). The SH3 domain of amphiphysin binds the proline-rich domain of dynamin at a single site that defines a new SH3 binding consensus sequence. J. Biol. Chem. 272, 13419–13425.PubMedCrossRefGoogle Scholar
  16. Greengard, P., Valtorta, F., Czernik, A.J., and Benfenati, F. (1993). Synaptic vesicle phosphoproteins and regulation of synaptic function. Science 259, 780–785.PubMedCrossRefGoogle Scholar
  17. Hata, Y., Slaughter, C.A., and Sudhof, T.C. (1993b). Synaptic vesicle fusion complex contains unc-18 homologue bound to syntaxin. Nature 366, 347–351.CrossRefGoogle Scholar
  18. Hata, Y., Slaughter, C.A., and Sudhof, T.C. (1993a). Synaptic vesicle fusion complex contains unc-18 homologue bound to syntaxin. Nature 366, 347–351.CrossRefGoogle Scholar
  19. Hosoya, H., Komatsu, S., Shimizu, T., Inagaki, M., Ikegami, M., and Yazaki, K. (1994). Phosphorylation of dynamin by cdc2 kinase. Biochem. Biophys. Res. Commun. 202, 1127–1133.PubMedCrossRefGoogle Scholar
  20. Huttner, W.B. and Greengard, P. (1979). Multiple phosphorylation sites in protein I and their differential regulation by cyclic AMP and calcium. Proc. Natl. Acad. Sci. U.S.A. 76, 5402–5406.PubMedCrossRefGoogle Scholar
  21. Huttner, W.B., Schiebler, W., Greengard, P., and De, C.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.PubMedCrossRefGoogle Scholar
  22. Johnson, E.M., Maeno, H., and Greengard, P. (1971). Phosphorylation of endogenous protein of rat brain by cyclic adenosine 3′,5′-monophosphate-dependent protein kinase. J. Biol. Chem. 246, 7731–7739.PubMedGoogle Scholar
  23. Jovanovic, J.N., Benfenati, F., Siow, Y.L., Sihra, T.S., Sanghera, J.S., Pelech, S.L., Greengard, P., and Czernik, A.J. (1996). Neurotrophins stimulate phosphorylation of synapsin I by MAP kinase and regulate synapsin I-actin interactions. Proc. Natl. Acad. Sci. U.S.A. 93, 3679–3683.PubMedCrossRefGoogle Scholar
  24. Jovanovic, J.N., Sihra, T.S., Nairn, A.C., Hemmings, H.C., Jr., Greengard, P., and Czernik, A.J. (2001). Opposing changes in phosphorylation of specific sites in synapsin I during Ca2+-dependent glutamate release in isolated nerve terminals. J. Neurosci. 21, 7944–7953.PubMedGoogle Scholar
  25. Krueger, B.K., Forn, J., and Greengard, P. (1977). Depolarization-induced phosphorylation of specific proteins, mediated by calcium ion influx, in rat brain synaptosomes. J. Biol. Chem. 252, 2764–2773.PubMedGoogle Scholar
  26. Lackner, M.R., Nurrish, S.J., and Kaplan, J.M. (1999). Facilitation of synaptic transmission by EGL-30 Gqalpha and EGL-8 PLCbeta: DAG binding to UNC-13 is required to stimulate acetylcholine release. Neuron 24, 335–346.PubMedCrossRefGoogle Scholar
  27. Lee, S.Y., Wenk, M.R., Kim, Y., Nairn, A.C., and De, C.P. (2004). Regulation of synaptojanin 1 by cyclin-dependent kinase 5 at synapses. Proc. Natl. Acad. Sci. U.S.A. 101, 546–551.PubMedCrossRefGoogle Scholar
  28. Liang, S., Wei, F.Y., Wu, Y.M., Tanabe, K., Abe, T., Oda, Y., Yoshida, Y., Yamada, H., Matsui, H., Tomizawa, K., and Takei, K. (2007). Major Cdk5-dependent phosphorylation sites of amphiphysin 1 are implicated in the regulation of the membrane binding and endocytosis. J. Neurochem 102,1466–1476.Google Scholar
  29. Marks, B., Stowell, M.H., Vallis, Y., Mills, I.G., Gibson, A., Hopkins, C.R., and McMahon, H.T. (2001). GTPase activity of dynamin and resulting conformation change are essential for endocytosis. Nature 410, 231–235.PubMedCrossRefGoogle Scholar
  30. Matsubara, M., Kusubata, M., Ishiguro, K., Uchida, T., Titani, K., and Taniguchi, H. (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.PubMedCrossRefGoogle Scholar
  31. McPherson, P.S., Garcia, E.P., Slepnev, V.I., David, C., Zhang, X., Grabs, D., Sossin, W.S., Bauerfeind, R., Nemoto, Y., and De, C.P. (1996). A presynaptic inositol-5-phosphatase. Nature 379, 353–357.PubMedCrossRefGoogle Scholar
  32. Misura, K.M., Scheller, R.H., and Weis, W.I. (2000). Three-dimensional structure of the neuronal-Sec1-syntaxin 1a complex. Nature 404, 355–362.PubMedCrossRefGoogle Scholar
  33. Nguyen, C. and Bibb, J.A. (2003). Cdk5 and the mystery of synaptic vesicle endocytosis. J. Cell Biol. 163, 697–699.PubMedCrossRefGoogle Scholar
  34. Novick, P., Field, C., and Schekman, R. (1980). Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell 21, 205–215.PubMedCrossRefGoogle Scholar
  35. Powell, K.A., Valova, V.A., Malladi, C.S., Jensen, O.N., Larsen, M.R., and Robinson, P.J. (2000). Phosphorylation of dynamin I on Ser-795 by protein kinase C blocks its association with phospholipids. J. Biol. Chem. 275, 11610–11617.PubMedCrossRefGoogle Scholar
  36. Robinson, P.J., Sontag, J.M., Liu, J.P., Fykse, E.M., Slaughter, C., McMahon, H., and Sudhof, T.C. (1993). Dynamin GTPase regulated by protein kinase C phosphorylation in nerve terminals. Nature 365, 163–166.PubMedCrossRefGoogle Scholar
  37. Rosales, J.L., Ernst, J.D., Hallows, J., and Lee, K.Y. (2004). GTP-dependent secretion from neutrophils is regulated by Cdk5. J. Biol. Chem. 279, 53932–53936.PubMedCrossRefGoogle Scholar
  38. Rosales, J.L., Nodwell, M.J., Johnston, R.N., and Lee, K.Y. (2000). Cdk5/p25(nck5a) interaction with synaptic proteins in bovine brain. J. Cell Biochem. 78, 151–159.PubMedCrossRefGoogle Scholar
  39. Schiebler, W., Jahn, R., Doucet, J.P., Rothlein, J., and Greengard, P. (1986). Characterization of synapsin I binding to small synaptic vesicles. J. Biol. Chem. 261, 8383–8390.PubMedGoogle Scholar
  40. Sihra, T.S., Wang, J.K., Gorelick, F.S., and Greengard, P. (1989). Translocation of synapsin I in response to depolarization of isolated nerve terminals. Proc. Natl. Acad. Sci. U.S.A. 86, 8108–8112.PubMedCrossRefGoogle Scholar
  41. Solomaha, E., Szeto, F.L., Yousef, M.A., and Palfrey, H.C. (2005). Kinetics of Src homology 3 domain association with the proline-rich domain of dynamins: specificity, occlusion, and the effects of phosphorylation. J. Biol. Chem. 280, 23147–23156.PubMedCrossRefGoogle Scholar
  42. Takahashi, S., Ohshima, T., Cho, A., Sreenath, T., Iadarola, M.J., Pant, H.C., Kim, Y., Nairn, A.C., Brady, R.O., Greengard, P., and Kulkarni, A.B. (2005). Increased activity of cyclin-dependent kinase 5 leads to attenuation of cocaine-mediated dopamine signaling. Proc. Natl. Acad. Sci. U.S.A. 102, 1737–1742.PubMedCrossRefGoogle Scholar
  43. Tan, T.C., Valova, V.A., Malladi, C.S., Graham, M.E., Berven, L.A., Jupp, O.J., Hansra, G., McClure, S.J., Sarcevic, B., Boadle, R.A., Larsen, M.R., Cousin, M.A., and Robinson, P.J. (2003). Cdk5 is essential for synaptic vesicle endocytosis. Nat. Cell Biol. 5, 701–710.PubMedCrossRefGoogle Scholar
  44. Tomizawa, K., Ohta, J., Matsushita, M., Moriwaki, A., Li, S.T., Takei, K., and Matsui, H. (2002). Cdk5/p35 regulates neurotransmitter release through phosphorylation and downregulation of P/Q-type voltage-dependent calcium channel activity. J. Neurosci. 22, 2590–2597.PubMedGoogle Scholar
  45. Tomizawa, K., Sunada, S., Lu, Y.F., Oda, Y., Kinuta, M., Ohshima, T., Saito, T., Wei, F.Y., Matsushita, M., Li, S.T., Tsutsui, K., Hisanaga, S., Mikoshiba, K., Takei, K., and Matsui, H. (2003). Cophosphorylation of amphiphysin I and dynamin I by Cdk5 regulates clathrin-mediated endocytosis of synaptic vesicles. J. Cell Biol. 163, 813–824.PubMedCrossRefGoogle Scholar
  46. Valtorta, F., Greengard, P., Fesce, R., Chieregatti, E., and Benfenati, F. (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.PubMedGoogle Scholar
  47. Verhage, M., Maia, A.S., Plomp, J.J., Brussaard, A.B., Heeroma, J.H., Vermeer, H., Toonen, R.F., Hammer, R.E., van den Berg, T.K., Missler, M., Geuze, H.J., and Sudhof, T.C. (2000). Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 287, 864–869.PubMedCrossRefGoogle Scholar
  48. Xin, X., Ferraro, F., Back, N., Eipper, B.A., and Mains, R.E. (2004). Cdk5 and Trio modulate endocrine cell exocytosis. J. Cell Sci. 117, 4739–4748.PubMedCrossRefGoogle Scholar
  49. Yan, Z., Chi, P., Bibb, J.A., Ryan, T.A., and Greengard, P. (2002). Roscovitine: a novel regulator of P/Q-type calcium channels and transmitter release in central neurons. J. Physiol 540, 761–770.PubMedCrossRefGoogle Scholar
  50. Yang, B., Steegmaier, M., Gonzalez, L.C., Jr., and Scheller, R.H. (2000). nSec1 binds a closed conformation of syntaxin1A. J. Cell Biol. 148, 247–252.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  1. 1.Department of PhysiologyOkayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences2-5-1 Shikata-choJapan

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