Cdk5 is essential for synaptic vesicle endocytosis

Nature Cell Biology

Volumn 5, Issue 8, 2003, Pages 701-710

  Tan, Timothy C ^a   Valova, Valentina A ^a   Malladi, Chandra S ^a   Graham, Mark E ^a   Berven, Leise A ^a   Jupp, Orla J ^f   Hansra, Gurdip ^a   McClure, Sonya J ^b   Sarcevic, Boris ^c   Boadle, Ross ^d   Larsen, Martin R ^e   Cousin, Michael A ^f   Robinson, Phillip J ^a  

^a CHILDREN'S MEDICAL RESEARCH INSTITUTE   (Australia)

^b ROYAL HOSPITAL FOR WOMEN   (Australia)

^c GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d WESTMEAD HOSPITAL   (Australia)

^e MACQUARIE UNIVERSITY   (Australia)

^f UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIPHYSIN; CALCINEURIN; CYCLIN DEPENDENT KINASE 5; CYCLIN DEPENDENT KINASE INHIBITOR; DEPHOSPHIN; DYNAMIN; PROTEIN; PROTEIN KINASE; SERINE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENDOCYTOSIS; IN VITRO STUDY; IN VIVO STUDY; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SYNAPSE VESICLE;

AMINO ACID MOTIFS; ANIMALS; CYCLIN-DEPENDENT KINASE 5; CYCLIN-DEPENDENT KINASES; DYNAMIN I; ENDOCYTOSIS; ENZYME INHIBITORS; MONOMERIC CLATHRIN ASSEMBLY PROTEINS; NERVE TISSUE PROTEINS; NEURONS; PEPTIDES; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN KINASE C-ALPHA; PURINES; RATS; RECOMBINANT FUSION PROTEINS; SERINE; SHEEP; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SYNAPSES; SYNAPTIC VESICLES; SYNAPTOSOMES;

EID: 0042490494     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb1020     Document Type: Article

References (50)

1. Liu, J. P., Sim, A. T. R. & Robinson, P. J. Calcineurin inhibition of dynamin I GTPase activity coupled to nerve terminal depolarization. Science 265, 970-973 (1994).
2. Marks, B. & McMahon, H. T. Calcium triggers calcineurin-dependent synaptic vesicle recycling in mammalian nerve terminals. Curr. Biol. 8, 740-749 (1998).
3. Cousin, M. A., Tan, T. C. & Robinson, P. J. Protein phosphorylation is required for endocytosis in nerve terminals. Potential role for the dephosphins dynamin I and synaptojanin, but not AP180 or amphiphysin. J. Neurochem. 76, 105-116 (2001).
4. Cousin, M. A. Synaptic vesicle endocytosis: calcium works overtime in the nerve terminal. Mol. Neurobiol. 22, 115-128 (2000).
5. Cousin, M. A. & Robinson, P. J. The dephosphins: Dephosphorylation by calcineurin triggers synaptic vesicle endocytosis. Trends Neurosci. 24, 659-665 (2001).
6. 2 synthesizing enzyme at the synapse. Neuron 32, 79-88 (2001).
7. Powell, K. A. et al. Phosphorylation of dynamin I on Ser-795 by protein kinase C blocks its association with phospholipids. J. Biol. Chem. 275, 11610-11617 (2000).
8. Marks, B. et al. GTPase activity of dynamin and resulting conformation change are essential for endocytosis. Nature 410, 231-235 (2001).
9. Shupliakov, O. et al. Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science 276, 259-263 (1997).
10. 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).
11. Robinson, P. J. Dephosphin, a 96,000 dalton substrate of protein kinase C in synaptosomal cytosol is phosphorylated in intact synaptosomes. FEBS Lett. 282, 388-392 (1991).
12. Robinson, P. J. et al. Dynamin GTPase regulated by protein kinase C phosphorylation in nerve terminals. Nature 365, 163-166 (1993).
13. Hosoya, H. et al. Phosphorylation of dynamin by cdc2 kinase. Biochem. Biophys. Res. Commun. 202, 1127-1133 (1994).
14. Earnest, S., Khokhlatchev, A., Albanesi, J. P. & Barylko, B. Phosphorylation of dynamin by ERK2 inhibits the dynamin-microtubule interaction. FEBS Lett. 396, 62-66 (1996).
15. Chen-Hwang, M.-C., Chen, H.-R., Elzinga, M. & Hwang, Y.-W. Dynamin is a minibrain kinase/Dyrk1A substrate. J. Biol. Chem. 277, 17597-17604 (2002).
16. Songyang, Z. et al. A structural basis for substrate specificities of protein Ser/Thr kinases: primary sequence preference of casein kinases I and II, NIMA, phosphorylase kinase, calmodulin-dependent kinase II, CDK5, and Erk1. Mol. Cell. Biol. 16, 6486-6493 (1996).
17. Tomizawa, K. et al. Cdk5/p35 regulates neurotransmitter release through phosphorylation and downregulation of P/Q-type voltage-dependent calcium channel activity. J. Neurosci. 22, 2590-2597 (2002).
18. Matsubara, M. et al. 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 (1996).
19. Shuang, R. Q. et al. Regulation of Munc-18 syntaxin 1A interaction by cyclin-dependent kinase 5 in nerve endings. J. Biol. Chem. 273, 4957-4966 (1998).
20. Floyd, S. R. et al. Amphiphysin binds the cdk5 regulatory subunit p35 and is phosphorylated by cdk5 and cdc2. J. Biol. Chem. 276, 8104-8110 (2001).
21. Hill, E., van der, K. J., Downes, C. P. & Smythe, E. The role of dynamin and its binding partners in coated pit invagination and scission. J. Cell Biol. 152, 309-324 (2001).
22. Grabs, D. et al. 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 (1997).
23. Meijer, L. et al. Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. Eur. J. Biochem. 243, 527-536 (1997).
24. Davies, S. P., Reddy, H., Caivano, M. & Cohen, P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351, 95-105 (2000).
25. Cousin, M. A. et al. Synapsin I-associated phosphatidylinositol 3-kinase mediates synaptic vesicle delivery to the readily releasable pool. J. Biol. Chem. (cited 16 May 2003) DOI: 10.1074/jbc.M302386200 (2003).
26. Rosales, J. L., Nodwell, M. J., Johnston, R. N. & Lee, K. Y. Cdk5/p25(nck5a) interaction with synaptic proteins in bovine brain. J. Cell. Biochem. 78, 151-159 (2000).
27. 2+ inhibition of dynamin arrests synaptic vesicle recycling at the active zone. J. Neurosci. 20, 949-957 (2000).
28. Koenig, J. H. & Ikeda, K. Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J. Neurosci. 9, 3844-3860 (1989).
29. 2+-sensitive phospholipid-binding protein with very high affinity for protein kinase C. J. Biol. Chem. 269, 21043-21050 (1994).
30. Robinson, P. J. Differential stimulation of protein kinase C activity by phorbol ester or calcium/phosphatidylserine in vitro and in intact synaptosomes. J. Biol. Chem. 267, 21637-21644 (1992).
31. Robinson, P. J., Liu, J. P., Powell, K. A., Fykse, E. M. & Südhof, T. C. Phosphorylation of dynamin I and synaptic vesicle recycling. Trends Neurosci. 17, 348-353 (1994).
32. Dhavan, R., Tsai, L. H. & Tsai, L. H. A decade of cdk5. Nature Rev. Mol. Cell Biol. 2, 749-759 (2001).
33. Ohshima, T. et al. Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proc. Natl Acad. Sci. USA 93, 11173-11178 (1996).
34. Kwon, Y. T., Tsai, L. H. & Crandall, J. E. Callosal axon guidance defects in p35(-/-) mice. J. Comp. Neurol. 415, 218-229 (1999).
35. Tsai, L. H., Takahashi, T., Caviness, V. S. J. & Harlow, E. Activity and expression pattern of cyclin-dependent kinase 5 in the embryonic mouse nervous system. Development 119, 1029-1040 (1993).
36. Bibb, J. A. et al. Effects of chronic exposure to cocaine are regulated by the neuronal protein Cdk5. Nature 410, 376-380 (2001).
37. Fletcher, A. I. et al. Regulation of exocytosis by cyclin-dependent kinase 5 via phosphorylation of munc 18. J. Biol. Chem. 274, 4027-4035 (1999).
38. Li, B. S. et al. Regulation of NMDA receptors by cyclin-dependent kinase-5. Proc. Natl Acad. Sci. USA 98, 12742-12747 (2001).
39. Yan, Z., Chi, P., Bibb, J. A., Ryan, T. A. & Greengard, P. Roscovitine: a novel regulator of P/Q-type calcium channels and transmitter release in central neurons. J. Physiol. 540, 761-770 (2002).
40. Nicholls, D. G. The glutamatergic nerve terminal. Eur. J. Biochem. 212, 613-631 (1993).
41. Wilde, A. & Brodsky, F. M. In vivo phosphorylation of adaptors regulates their interaction with clathrin. J. Cell Biol. 135, 635-645 (1996).
42. Kariya, K. et al. Regulation of complex formation of POB1/epsin/adaptor protein complex 2 by mitotic phosphorylation. J. Biol. Chem. 275, 18399-18406 (2000).
43. Slepnev, V. I., Ochoa, G. C., Butler, M. H., Grabs, D. & DeCamilli, P. Role of phosphorylation in regulation of the assembly of endocytic coat complexes. Science 281, 821-824 (1998).
44. Rasmussen, R. K., Rusak, J., Price, G., Robinson, P. J. & Dorow, D. S. Mixed lineage kinase 2-SH3 domain binds dynamin and greatly enhances GTPase activation by phospholipid. Biochem. J. 335, 119-124 (1998).
45. Negash, S., Wang, H. S., Gao, C., Ledee, D. & Zelenka, P. Cdk5 regulates cell-matrix and cell-cell adhesion in lens epithelial cells. J. Cell Sci. 115, 2109-2117 (2002).
46. van den Heuvel, S. & Harlow, E. Distinct roles for cyclin-dependent kinases in cell cycle control. Science 262, 2050-2054 (1993).
47. Stowell, M. H., Marks, B., Wigge, P. & McMahon, H. T. Nucleotide-dependent conformational changes in dynamin: evidence for a mechanochemical molecular spring. Nature Cell Biol. 1, 27-32 (1999).
48. Wang, L.-H., Südhof, T. C. & Anderson, R. G. The appendage domain of α-adaptin is a high-affinity binding site for dynamin. J. Biol. Chem. 270, 10079-10083 (1995).
49. 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).
50. Zhou, W., Merrick, B. A., Khaledi, M. G. & Tomer, K. B. Detection and sequencing of phosphopeptides affinity bound to immobilized metal ion beads by matrix-assisted laser desorption/ionization mass spectrometry. J. Am. Soc. Mass Spectrom. 11, 273-282 (2000).