Synaptotagmin-IV modulates synaptic function and long-term potentiation by regulating BDNF release

Nature Neuroscience

Volumn 12, Issue 6, 2009, Pages 767-776

  Dean, Camin ^a   Liu, Huisheng ^a   Dunning, F Mark ^a   Chang, Payne Y ^a   Jackson, Meyer B ^a   Chapman, Edwin R ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; SYNAPTOTAGMIN; SYNAPTOTAGMIN IV; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; HIPPOCAMPUS; LONG TERM POTENTIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPSE VESICLE;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; DENDRITES; DOWN-REGULATION; EXOCYTOSIS; HIPPOCAMPUS; LONG-TERM POTENTIATION; MICE; MICE, KNOCKOUT; NEURONS; NEUROTRANSMITTER AGENTS; PRESYNAPTIC TERMINALS; SYNAPTIC POTENTIALS; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES; SYNAPTOTAGMINS;

EID: 67349113528     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn.2315     Document Type: Article

References (50)

1. Chapman, E.R. How does synaptotagmin trigger neurotransmitter release? Annu. Rev. Biochem. 77, 615-641 (2008).
2. 2+ sensor for neurotransmitter release. Trends Neurosci. 26, 413-422 (2003).
3. 2+ concentration to SNARE-mediated membrane fusion. Mol. Biol. Cell 16, 4755-4764 (2005).
4. Hui, E. et al. Three distinct kinetic groupings of the synaptotagmin family: candidate sensors for rapid and delayed exocytosis. Proc. Natl. Acad. Sci. USA 102, 5210-5214 (2005).
5. Bhalla, A., Chicka, M.C. & Chapman, E.R. Analysis of the synaptotagmin family during reconstituted membrane fusion: uncovering a class of inhibitory isoforms. J. Biol. Chem. 283, 21799-21807 (2008).
6. 2+ sensors for fast release that specify distinct presynaptic properties in subsets of neurons. Neuron 54, 567-581 (2007).
7. Vician, L. et al. Synaptotagmin IV is an immediate early gene induced by depolarization in PC12 cells and in brain. Proc. Natl. Acad. Sci. USA 92, 2164-2168 (1995).
8. Ibata, K., Fukuda, M., Hamada, T., Kabayama, H. & Mikoshiba, K. Synaptotagmin IV is present at the Golgi and distal parts of neurites. J. Neurochem. 74, 518-526 (2000).
9. Chapman, E.R., Desai, R.C., Davis, A.F. & Tornehl, C.K. Delineation of the oligomerization, AP-2 binding and synprint binding region of the C2B domain of synaptotagmin. J. Biol. Chem. 273, 32966-32972 (1998).
10. Wang, C.T. et al. Different domains of synaptotagmin control the choice between kiss- and-run and full fusion. Nature 424, 943-947 (2003).
11. Wang, C.T. et al. Synaptotagmin modulation of fusion pore kinetics in regulated exocytosis of dense-core vesicles. Science 294, 1111-1115 (2001).
12. Ahras, M., Otto, G.P. & Tooze, S.A. Synaptotagmin IV is necessary for the maturation of secretory granules in PC12 cells. J. Cell Biol. 173, 241-251 (2006).
13. Zhang, Q., Fukuda, M., Van Bockstaele, E., Pascual, O. & Haydon, P.G. Synaptotagmin IV regulates glial glutamate release. Proc. Natl. Acad. Sci. USA 101, 9441-9446 (2004).
14. Zhang, Z., Bhalla, A., Dean, C., Chapman, E.R. & Jackson, M.B. Synaptotagmin IV: a multifunctional regulator of peptidergic nerve terminals. Nat. Neurosci. 12, 163-171 (2009).
15. Osborne, S.L., Herreros, J., Bastiaens, P.I. & Schiavo, G. Calcium-dependent oligomerization of synaptotagmins I and II. Synaptotagmins I and II are localized on the same synaptic vesicle and heterodimerize in the presence of calcium. J. Biol. Chem. 274, 59-66 (1999).
16. Ting, J.T., Kelley, B.G. & Sullivan, J.M. Synaptotagmin IV does not alter excitatory fast synaptic transmission or fusion pore kinetics in mammalian CNS neurons. J. Neurosci. 26, 372-380 (2006).
17. Ibata, K. et al. Non-polarized distribution of synaptotagmin IV in neurons: evidence that synaptotagmin IV is not a synaptic vesicle protein. Neurosci. Res. 43, 401-406 (2002).
18. Berton, F. et al. Synaptotagmin I and IV define distinct populations of neuronal transport vesicles. Eur. J. Neurosci. 12, 1294-1302 (2000).
19. Littleton, J.T., Serano, T.L., Rubin, G.M., Ganetzky, B. & Chapman, E.R. Synaptic function modulated by changes in the ratio of synaptotagmin I and IV. Nature 400, 757-760 (1999).
20. 2+ binding in the C(2)A domain. Nature 418, 336-340 (2002).
21. Pawlu, C., DiAntonio, A. & Heckmann, M. Postfusional control of quantal current shape. Neuron 42, 607-618 (2004).
22. Yoshihara, M., Adolfsen, B., Galle, K.T. & Littleton, J.T. Retrograde signaling by Syt 4 induces presynaptic release and synapse-specific growth. Science 310, 858-863 (2005).
23. Ferguson, G.D., Anagnostaras, S.G., Silva, A.J. & Herschman, H.R. Deficits in memory and motor performance in synaptotagmin IV mutant mice. Proc. Natl. Acad. Sci. USA 97, 5598-5603 (2000).
24. Ferguson, G.D., Wang, H., Herschman, H.R. & Storm, D.R. Altered hippocampal short-term plasticity and associative memory in synaptotagmin IV (-/-)mice. Hippocampus 14, 964-974 (2004).
25. Denovan-Wright, E.M., Newton, R.A., Armstrong, J.N., Babity, J.M. & Robertson, H.A. Acute administration of cocaine, but not amphetamine, increases the level of synaptotagmin IV mRNA in the dorsal striatum of rat. Brain Res. Mol. Brain Res. 55, 350-354 (1998).
26. Peng, W. et al. Synaptotagmin I and IV are differentially regulated in the brain by the recreational drug 3,4-methylene dioxymethamphetamine (MDMA). Brain Res. Mol. Brain Res. 108, 94-101 (2002).
27. Poo, M.M. Neurotrophins as synaptic modulators. Nat. Rev. Neurosci. 2, 24-32 (2001).
28. Zemelman, B.V., Nesnas, N., Lee, G.A. & Miesenbock, G. Photochemical gating of heterologous ion channels: remote control over genetically designated populations of neurons. Proc. Natl. Acad. Sci. USA 100, 1352-1357 (2003).
29. Balkowiec, A. & Katz, D.M. Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons. J. Neurosci. 22, 10399-10407 (2002).
30. Tyler, W.J. & Pozzo-Miller, L.D. BDNF enhances quantal neurotransmitter release and increases the number of docked vesicles at the active zones of hippocampal excitatory synapses. J. Neurosci. 21, 4249-4258 (2001).
31. Tyler, W.J. et al. BDNF increases release probability and the size of a rapidly recycling vesicle pool within rat hippocampal excitatory synapses. J. Physiol. (Lond.) 574, 787-803 (2006).
32. Zakharenko, S.S. et al. Presynaptic BDNF required for a presynaptic but not post-synaptic component of LTP at hippocampal CA1-CA3 synapses. Neuron 39, 975-990 (2003).
33. Chen, G., Kolbeck, R., Barde, Y.A., Bonhoeffer, T. & Kossel, A. Relative contribution of endogenous neurotrophins in hippocampal long-term potentiation. J. Neurosci. 19, 7983-7990 (1999).
34. Kang, H., Welcher, A.A., Shelton, D. & Schuman, E.M. Neurotrophins and time: different roles for TrkB signaling in hippocampal long-term potentiation. Neuron 19, 653-664 (1997).
35. Rutherford, L.C., Nelson, S.B. & Turrigiano, G.G. BDNF has opposite effects on the quantal amplitude of pyramidal neuron and interneuron excitatory synapses. Neuron 21, 521-530 (1998).
36. Chang, P.Y. & Jackson, M.B. Heterogeneous spatial patterns of long-term potentiation in hippocampal slices. J. Physiol. (Lond.) 576, 427-443 (2006).
37. Levine, E.S., Crozier, R.A., Black, I.B. & Plummer, M.R. Brain-derived neurotrophic factor modulates hippocampal synaptic transmission by increasing N-methyl-d-aspartic acid receptor activity. Proc. Natl. Acad. Sci. USA 95, 10235-10239 (1998).
38. Caldeira, M.V. et al. BDNF regulates the expression and the synaptic delivery of AMPA receptor subunits in hippocampal neurons. J. Biol. Chem. 282, 12619-12628 (2007).
39. Aicardi, G. et al. Induction of long-term potentiation and depression is reflected by corresponding changes in secretion of endogenous brain-derived neurotrophic factor. Proc. Natl. Acad. Sci. USA 101, 15788-15792 (2004).
40. Aravanis, A.M., Pyle, J.L. & Tsien, R.W. Single synaptic vesicles fusing transiently and successively without loss of identity. Nature 423, 643-647 (2003).
41. Richards, D.A., Bai, J. & Chapman, E.R. Two modes of exocytosis at hippocampal synapses revealed by rate of FM1-43 efflux from individual vesicles. J. Cell Biol. 168, 929-939 (2005).
42. Kovalchuk, Y., Hanse, E., Kafitz, K.W. & Konnerth, A. Postsynaptic induction of BDNF-mediated long-term potentiation. Science 295, 1729-1734 (2002).
43. Gärtner, A. et al. Hippocampal long-term potentiation is supported by presynaptic and postsynaptic tyrosine receptor kinase B-mediated phospholipase Cgamma signaling. J. Neurosci. 26, 3496-3504 (2006).
44. Perrais, D., Kleppe, I.C., Taraska, J.W. & Almers, W. Recapture after exocytosis causes differential retention of protein in granules of bovine chromaffin cells. J. Physiol. (Lond.) 560, 413-428 (2004).
45. Bohnert, S. & Schiavo, G. Tetanus toxin is transported in a novel neuronal compartment characterized by a specialized pH regulation. J. Biol. Chem. 280, 42336-42344 (2005).
46. Deinhardt, K. et al. Rab5 and Rab7 control endocytic sorting along the axonal retrograde transport pathway. Neuron 52, 293-305 (2006).
47. Lu, Y., Christian, K. & Lu, B. BDNF: A key regulator for protein synthesis-dependent LTP and long-term memory? Neurobiol. Learn. Mem. 89, 312-323 (2008).
48. Shakiryanova, D., Tully, A. & Levitan, E.S. Activity-dependent synaptic capture of transiting peptidergic vesicles. Nat. Neurosci. 9, 896-900 (2006).
49. Tarsa, L. & Goda, Y. Synaptophysin regulates activity-dependent synapse formation in cultured hippocampal neurons. Proc. Natl. Acad. Sci. USA 99, 1012-1016 (2002).
50. Hartmann, M., Heumann, R. & Lessmann, V. Synaptic secretion of BDNF after high-frequency stimulation of glutamatergic synapses. EMBO J. 20, 5887-5897 (2001).