Control of synaptic vesicle endocytosis by an extracellular signalling molecule

Nature Communications

Volumn 4, Issue , 2013, Pages

  Smillie, Karen J ^a   Pawson, Jonathan ^a   Perkins, Emma M ^a   Jackson, Mandy ^a   Cousin, Michael A ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; DYNAMIN I; GLYCOGEN SYNTHASE KINASE 3;

BRAIN; ENZYME ACTIVITY; INHIBITION; MOLECULAR ANALYSIS; SIGNALING; VESICLE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVITY; INHIBITION KINETICS; INTRACELLULAR SIGNALING; NERVE CELL CULTURE; NEUROTRANSMISSION; NONHUMAN; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; RAT; REPOLARIZATION; SIGNAL TRANSDUCTION; SYNAPSE VESICLE;

ANIMALS; BIOLOGICAL TRANSPORT; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELLS, CULTURED; CHROMONES; DYNAMIN I; ENDOCYTOSIS; ENZYME INHIBITORS; FEMALE; GLYCOGEN SYNTHASE KINASE 3; HIPPOCAMPUS; MALE; MORPHOLINES; NEUROTRANSMITTER AGENTS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES;

EID: 84884155949     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3394     Document Type: Article

References (46)

1. Miller, R. J. Presynaptic receptors. Annu. Rev. Pharmacol. Toxicol. 38, 201-227 (1998).
2. Granseth, B., Odermatt, B., Royle, S. J. & Lagnado, L. Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron 51, 773-786 (2006).
3. Zhu, Y., Xu, J. & Heinemann, S. F. Two pathways of synaptic vesicle retrieval revealed by single-vesicle imaging. Neuron 61, 397-411 (2009).
4. Clayton, E. L., Evans, G. J. & Cousin, M. A. Bulk synaptic vesicle endocytosis is rapidly triggered during strong stimulation. J. Neurosci. 28, 6627-6632 (2008).
5. Kasprowicz, J. et al. Inactivation of clathrin heavy chain inhibits synaptic recycling but allows bulk membrane uptake. J. Cell Biol. 182, 1007-1016 (2008).
6. Heerssen, H., Fetter, R. D. & Davis, G. W. Clathrin dependence of synapticvesicle formation at the Drosophila neuromuscular junction. Curr. Biol. 18, 401-409 (2008).
7. Cheung, G. & Cousin, M. A. Adaptor protein complexes 1 and 3 are essential for generation of synaptic vesicles from activity-dependent bulk endosomes. J. Neurosci. 32, 6014-6023 (2012).
8. Clayton, E. L. & Cousin, M. A. The molecular physiology of activity-dependent bulk endocytosis of synaptic vesicles. J. Neurochem. 111, 901-914 (2009).
9. Clayton, E. L. et al. Dynamin I phosphorylation by GSK3 controls activitydependent bulk endocytosis of synaptic vesicles. Nat. Neurosci. 13, 845-851 (2010).
10. Evans, G. J. & Cousin, M. A. Activity-dependent control of slow synaptic vesicle endocytosis by cyclin-dependent kinase 5. J. Neurosci. 27, 401-411 (2007).
11. Yoshii, A. & Constantine-Paton, M. Postsynaptic BDNF-TrkB signaling in synapse maturation, plasticity, and disease. Dev. Neurobiol. 70, 304-322 (2010).
12. Minichiello, L. TrkB signalling pathways in LTP and learning. Nat. Rev. Neurosci. 10, 850-860 (2009).
13. Cross, D. A., Alessi, D. R., Cohen, P., Andjelkovich, M. & Hemmings, B. A. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378, 785-789 (1995).
14. Smillie, K. J. & Cousin, M. A. Akt/PKB controls the activity-dependent bulk endocytosis of synaptic vesicles. Traffic 13, 1004-1011 (2012).
15. Gao, W. Q., Zheng, J. L. & Karihaloo, M. Neurotrophin-4/5 (NT-4/5) and brain-derived neurotrophic factor (BDNF) act at later stages of cerebellar granule cell differentiation. J. Neurosci. 15, 2656-2667 (1995).
16. Segal, R. A., Pomeroy, S. L. & Stiles, C. D. Axonal growth and fasciculation linked to differential expression of BDNF and NT3 receptors in developing cerebellar granule cells. J. Neurosci. 15, 4970-4981 (1995).
17. Ramirez, D. M., Khvotchev, M., Trauterman, B. & Kavalali, E. T. Vti1a identifies a vesicle pool that preferentially recycles at rest and maintains spontaneous neurotransmission. Neuron 73, 121-134 (2012).
18. Shupliakov, O. et al. Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science 276, 259-263 (1997).
19. Chen, Y. et al. Formation of an endophilin-Ca2\+ channel complex is critical for clathrin-mediated synaptic vesicle endocytosis. Cell 115, 37-48 (2003).
20. Koh, T. W. et al. Eps15 and Dap160 control synaptic vesicle membrane retrieval and synapse development. J. Cell Biol. 178, 309-322 (2007).
21. Zucker, R. S. & Regehr, W. G. Short-term synaptic plasticity. Annu. Rev. Physiol. 64, 355-405 (2002).
22. Cousin, M. A. & Evans, G. J. Activation of silent and weak synapses by cAMPdependent protein kinase in cultured cerebellar granule neurons. J. Physiol. 589, 1943-1955 (2011).
23. Clayton, E. L. et al. The phospho-dependent dynamin-syndapin interaction triggers activity-dependent bulk endocytosis of synaptic vesicles. J. Neurosci. 29, 7706-7717 (2009).
24. Cheung, G., Jupp, O. J. & Cousin, M. A. Activity-dependent bulk endocytosis and clathrin-dependent endocytosis replenish specific synaptic vesicle pools in central nerve terminals. J. Neurosci. 30, 8151-8161 (2010).
25. Hartmann, M., Heumann, R. & Lessmann, V. Synaptic secretion of BDNF after high-frequency stimulation of glutamatergic synapses. EMBO J. 20, 5887-5897 (2001).
26. Brigadski, T., Hartmann, M. & Lessmann, V. Differential vesicular targeting and time course of synaptic secretion of the mammalian neurotrophins. J. Neurosci. 25, 7601-7614 (2005).
27. Matsuda, N. et al. Differential activity-dependent secretion of brain-derived neurotrophic factor from axon and dendrite. J. Neurosci. 29, 14185-14198 (2009).
28. Nagappan, G. et al. Control of extracellular cleavage of ProBDNF by high frequency neuronal activity. Proc. Natl Acad. Sci. USA 106, 1267-1272 (2009).
29. Lohof, A. M., Ip, N. Y. & Poo, M. M. Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF. Nature 363, 350-353 (1993).
30. Kang, H. & Schuman, E. M. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267, 1658-1662 (1995).
31. Carmignoto, G., Pizzorusso, T., Tia, S. & Vicini, S. Brain-derived neurotrophic factor and nerve growth factor potentiate excitatory synaptic transmission in the rat visual cortex. J. Physiol. 498(Pt 1): 153-164 (1997).
32. Li, Y. X. et al. Expression of a dominant negative TrkB receptor, T1, reveals a requirement for presynaptic signaling in BDNF-induced synaptic potentiation in cultured hippocampal neurons. Proc. Natl Acad. Sci. USA 95, 10884-10889 (1998).
33. Li, Y. X., Zhang, Y., Lester, H. A., Schuman, E. M. & Davidson, N. Enhancement of neurotransmitter release induced by brain-derived neurotrophic factor in cultured hippocampal neurons. J. Neurosci. 18, 10231-10240 (1998).
34. Jovanovic, J. N., Czernik, A. J., Fienberg, A. A., Greengard, P. & Sihra, T. S. Synapsins as mediators of BDNF-enhanced neurotransmitter release. Nat. Neurosci. 3, 323-329 (2000).
35. Figurov, A., Pozzo-Miller, L. D., Olafsson, P., Wang, T. & Lu, B. Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature 381, 706-709 (1996).
36. Tanaka, T., Saito, H. & Matsuki, N. Inhibition of GABAA synaptic responses by brain-derived neurotrophic factor (BDNF) in rat hippocampus. J. Neurosci. 17, 2959-2966 (1997).
37. Frerking, M., Malenka, R. C. & Nicoll, R. A. Brain-derived neurotrophic factor (BDNF) modulates inhibitory, but not excitatory, transmission in the CA1 region of the hippocampus. J. Neurophysiol. 80, 3383-3386 (1998).
38. Sala, R. et al. Nerve growth factor and brain-derived neurotrophic factor increase neurotransmitter release in the rat visual cortex. Eur. J. Neurosci. 10, 2185-2191 (1998).
39. Valente, P. et al. Site-specific synapsin I phosphorylation participates in the expression of post-tetanic potentiation and its enhancement by BDNF. J. Neurosci. 32, 5868-5879 (2012).
40. Yano, H. et al. BDNF-mediated neurotransmission relies upon a myosin VI motor complex. Nat. Neurosci. 9, 1009-1018 (2006).
41. Furutani, K., Okubo, Y., Kakizawa, S. & Iino, M. Postsynaptic inositol 1,4,5-trisphosphate signaling maintains presynaptic function of parallel fiber-Purkinje cell synapses via BDNF. Proc. Natl Acad. Sci. USA 103, 8528-8533 (2006).
42. Peineau, S. et al. LTP inhibits LTD in the hippocampus via regulation of GSK3beta. Neuron 53, 703-717 (2007).
43. Koch, D. et al. Proper synaptic vesicle formation and neuronal network activity critically rely on syndapin I. EMBO J. 30, 4955-4969 (2011).
44. Koyama, R. & Ikegaya, Y. To BDNF or not to BDNF: that is the epileptic hippocampus. Neuroscientist 11, 282-287 (2005).
45. Tan, T. C. et al. Cdk5 is essential for synaptic vesicle endocytosis. Nat. Cell Biol. 5, 701-710 (2003).
46. Wenzel, E. M. et al. Key physiological parameters dictate triggering of activitydependent bulk endocytosis in hippocampal synapses. PLoS. One 7, e38188 (2012).