Developmental shift to a mechanism of synaptic vesicle endocytosis requiring nanodomain Ca2+

Nature Neuroscience

Volumn 13, Issue 7, 2010, Pages 838-844

  Yamashita, Takayuki ^a   Eguchi, Kohgaku ^a   Saitoh, Naoto ^b   von Gersdorff, Henrique ^c   Takahashi, Tomoyuki ^a,b  

^a OKINAWA INSTITUTE OF SCIENCE AND TECHNOLOGY GRADUATE UNIVERSITY   (Japan)

^b DOSHISHA UNIVERSITY   (Japan)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; CALCIUM CHANNEL; CALCIUM ION; CALMODULIN; GUANOSINE TRIPHOSPHATE;

ARTICLE; CELL MATURATION; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVATION; EXOCYTOSIS; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE VESICLE;

ANIMALS; AUDITORY PATHWAYS; BRAIN STEM; CALCINEURIN; CALCIUM; CALMODULIN; ELECTRIC CAPACITANCE; ENDOCYTOSIS; EXOCYTOSIS; MEMBRANE MICRODOMAINS; NEUROGENESIS; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; SYNAPTIC VESICLES; TIME FACTORS;

EID: 77954145400     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn.2576     Document Type: Article

References (48)

1. Heuser, J.E. & Reese, T.S. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57, 315-344 (1973).
2. 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).
3. 2+, GTP and dynamin, but not clathrin. Proc. Natl. Acad. Sci. USA 92, 8328-8332 (1995).
4. Neves, G., Gomis, A. & Lagnado, L. Calcium infux selects the fast mode of endocytosis in the synaptic terminal of retinal bipolar cells. Proc. Natl. Acad. Sci. USA 98, 15282-15287 (2001).
5. Beutner, D., Voets, T., Neher, E. & Moser, T. Calcium dependence of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse. Neuron 29, 681-690 (2001).
6. Wu, W., Xu, J., Wu, X.-S. & Wu, L.-G. Activity-dependent acceleration of endocytosis at a central synapse. J. Neurosci. 25, 11676-11683 (2005).
7. Hosoi, N., Holt, M. & Sakaba, T. Calcium-dependence of exo-and endocytotic coupling at a glutamatergic synapse. Neuron 63, 216-229 (2009).
8. 2+ and calmodulin initiates all forms of endocytosis during depolarization at a nerve terminal. Nat. Neurosci. 12, 1003-1010 (2009).
9. Renden, R. & von Gersdorff, H. Synaptic vesicle endocytosis at a CNS nerve terminal: faster kinetics at physiological temperatures and increased endocytotic capacity during maturation. J. Neurophysiol. 98, 3349-3359 (2007).
10. 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).
11. Balaji, J., Armbruster, M. & Ryan, T.A. Calcium control of endocytic capacity at a CNS synapse. J. Neurosci. 28, 6742-6749 (2008).
12. 2+] at the mouth of a calcium channel. J. Neurosci. 17, 6961-6973 (1997).
13. Augustine, G.J., Santamaria, F. & Tanaka, K. Local calcium signaling in neurons. Neuron 40, 331-346 (2003).
14. Jewett, D.L. & Romano, M.N. Neonatal development of auditory system potentials averaged from the scalp of rat and cat. Brain Res. 36, 101-115 (1972).
15. Borst, J.G.G. & Sakmann, B. Calcium infux and transmitter release in a fast CNS synapse. Nature 383, 431-434 (1996).
16. Fedchyshyn, M.J. & Wang, L.-Y. Developmental transformation of the release modality at the calyx of Held synapse. J. Neurosci. 25, 4131-4140 (2005).
17. Artalejo, C.R., Elhamdani, A. & Palfrey, H.C. Calmodulin is the divalent cation receptor for rapid endocytosis, but not exocytosis, in adrenal chromaffn cells. Neuron 16, 195-205 (1996).
18. Engisch, K.L. & Nowycky, M.C. Compensatory and excess retrieval: two types of endocytosis following single step depolarizations in bovine adrenal chromaffn cells. J. Physiol. (Lond.) 506, 591-608 (1998).
19. Chan, S.-A. & Smith, C. Physiological stimuli evoke two forms of endocytosis in bovine chromaffn cells. J. Physiol. (Lond.) 537, 871-885 (2001).
20. Marks, B. & McMahon, H.T. Calcium triggers calcineurin-dependent synaptic vesicle recycling in mammalian nerve terminals. Curr. Biol. 8, 740-749 (1998).
21. Cousin, M.A. & Robinson, P.J. The dephosphins: dephosphorylation by calcineurin triggers synaptic vesicle endocytosis. Trends Neurosci. 24, 659-665 (2001).
22. Slepnev, V.I., Ochoa, G.-C., Butler, M.H., Grabs, D. & De Camilli, P. Role of phosphorylation in regulation of the assembly of endocytic coat complexes. Science 281, 821-824 (1998).
23. Yamashita, T., Hige, T. & Takahashi, T. Vesicle endocytosis requires dynamin-dependent GTP hydrolysis at a fast CNS synapse. Science 307, 124-127 (2005).
24. Jockusch, W.J., Praefcke, G.J.K., McMahon, H.T. & Lagnado, L. Clathrin-dependent and clathrin-independent retrieval of synaptic vesicles in retinal bipolar cells. Neuron 46, 869-878 (2005).
25. Heidelberger, R. ATP is required at an early step in compensatory endocytosis in synaptic terminals. J. Neurosci. 21, 6467-6474 (2001).
26. Xu, J. et al. GTP-independent rapid and slow endocytosis at a central synapse. Nat. Neurosci. 11, 45-53 (2008).
27. Török, K. et al. Inhibition of calmodulin-activated smooth-muscle myosin light-chain kinase by calmodulin-binding peptides and fuorescent (phosphodiesterase-activating) calmodulin derivatives. Biochemistry 37, 6188-6198 (1998).
28. Nakamura, T., Yamashita, T., Saitoh, N. & Takahashi, T. Developmental changes in calcium/calmodulin-dependent inactivation of calcium currents at the rat calyx of Held. J. Physiol. (Lond.) 586, 2253-2261 (2008).
29. 2+ microdomains: new tools for understanding their roles in neurotransmitter release. Neuron 20, 389-399 (1998).
30. 2+-triggered synaptic vesicle exocytosis and clathrin-mediated endocytosis at a central synapse. Neuron 21, 607-616 (1998).
31. Roos, J. & Kelly, R.B. The endocytic machinery in nerve terminals surrounds sites of exocytosis. Curr. Biol. 9, 1411-1414 (1999).
32. Teng, H. & Wilkinson, R.S. Clathrin-mediated endocytosis near active zones in snake motor boutons. J. Neurosci. 20, 7986-7993 (2000).
33. Poskanzer, K.E., Marek, K.W., Sweeney, S.T. & Davis, G.W. Synaptotagmin 1 is necessary for compensatory synaptic vesicle endocytosis in vivo. Nature 426, 559-563 (2003).
34. Llinás, R.R., Sugimori, M., Moran, K.A., Moreira, J.E. & Fukuda, M. Vesicular reuptake inhibition by a synaptotagmin I C2B domain antibody at the squid giant synapse. Proc. Natl. Acad. Sci. USA 101, 17855-17860 (2004).
35. 2+-dependent formation of a dynamin-synaptophysin complex: potential role in synaptic vesicle endocytosis. J. Biol. Chem. 277, 9010-9015 (2002).
36. 2+ channel complex is critical for clathrin-mediated synaptic vesicle endocytosis. Cell 115, 37-48 (2003).
37. 2+ channel synprint site in synaptic vesicle endocytosis. J. Neurosci. 30, 655-660 (2010).
38. Xu, J. & Wu, L.-G. The decrease in the presynaptic calcium current is a major cause of short-term depression at a calyx-type synapse. Neuron 46, 633-645 (2005).
39. 2+ transients at the calyx of Held presynaptic terminal. Neurosci. Res. 58, S71 (2007).
40. 2+/calmodulin-dependent protein kinase II (CaMKII) is activated by calmodulin with two bound calciums. Proc. Natl. Acad. Sci. USA 103, 13968-13973 (2006).
41. 2+ signaling. Nat. Rev. Neurosci. 8, 182-193 (2007).
42. Kawasaki, F., Hazen, M. & Ordway, R.W. Fast synaptic fatigue in shibire mutants reveals a rapid requirement for dynamin in synaptic membrane traffcking. Nat. Neurosci. 3, 859-860 (2000).
43. Wu, Y., Kawasaki, F. & Ordway, R.W. Properties of short-term synaptic depression at larval neuromuscular synapses in wild-type and temperature-sensitive paralytic mutants of Drosophila. J. Neurophysiol. 93, 2396-2405 (2005).
44. Lou, X., Paradise, S., Ferguson, S.M. & De Camilli, P. Selective saturation of slow endocytosis at a giant glutamatergic central synapse lacking dynamin 1. Proc. Natl. Acad. Sci. USA 105, 17555-17560 (2008).
45. Newton, A.J., Kirchhausen, T. & Murthy, V.N. Inhibition of dynamin completely blocks compensatory synaptic vesicle endocytosis. Proc. Natl. Acad. Sci. USA 103, 17955-17960 (2006).
46. von Gersdorff, H. & Matthews, G. Inhibition of endocytosis by elevated internal calcium in a synaptic terminal. Nature 370, 652-655 (1994).
47. Wu, L.-G., Ryan, T.A. & Lagnado, L. Modes of vesicle retrieval at ribbon synapses, calyx-type synapses and small central synapses. J. Neurosci. 27, 11793-11802 (2007).
48. 1 receptor-mediated presynaptic inhibition at the calyx of Held of immature rats. J. Physiol. (Lond.) 553, 415-426 (2003).