Postsynaptic synaptotagmins mediate AMPA receptor exocytosis during LTP

Nature

Volumn 544, Issue 7650, 2017, Pages 316-321

  Wu, Dick ^a   Bacaj, Taulant ^a   Morishita, Wade ^a   Goswami, Debanjan ^a   Arendt, Kristin L ^a   Xu, Wei ^a,b   Chen, Lu ^a   Malenka, Robert C ^a   Südhof, Thomas C ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; SYNAPTOTAGMIN; SYNAPTOTAGMIN I; SYNAPTOTAGMIN VII; UNCLASSIFIED DRUG; CALCIUM;

CELLS AND CELL COMPONENTS; GENE EXPRESSION; LEARNING; LONG-TERM CHANGE; MEMORY; MUTATION; NERVOUS SYSTEM; PROTEIN; RODENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; EXOCYTOSIS; FEMALE; HIPPOCAMPAL CA1 REGION; LONG TERM POTENTIATION; MALE; MOUSE; NEWBORN; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; ANIMAL; CYTOLOGY; GENETICS; METABOLISM; MUTATION; PHYSIOLOGY; PROTEIN TRANSPORT; SYNAPSE; SYNAPTIC TRANSMISSION;

MUS;

ANIMALS; CA1 REGION, HIPPOCAMPAL; CALCIUM; EXOCYTOSIS; FEMALE; LONG-TERM POTENTIATION; MALE; MICE; MUTATION; PROTEIN TRANSPORT; PYRAMIDAL CELLS; RECEPTORS, AMPA; SYNAPSES; SYNAPTIC TRANSMISSION; SYNAPTOTAGMINS;

EID: 85017463238     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature21720     Document Type: Article

References (46)

1. Bliss, T. V. & Collingridge, G. L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39 (1993).
2. Malenka, R. C. & Bear, M. F. LTP and LTD: an embarrassment of riches. Neuron 44, 5-21 (2004).
3. Huganir, R. L. & Nicoll, R. A. AMPARs and synaptic plasticity: the last 25 years. Neuron 80, 704-717 (2013).
4. Morris, R. G. NMDA receptors and memory encoding. Neuropharmacology 74, 32-40 (2013).
5. Opazo, P. & Choquet, D. A three-step model for the synaptic recruitment of AMPA receptors. Mol. Cell. Neurosci. 46, 1-8 (2011).
6. Makino, H. & Malinow, R. AMPA receptor incorporation into synapses during LTP: the role of lateral movement and exocytosis. Neuron 64, 381-390 (2009).
7. Granger, A. J., Shi, Y., Lu, W., Cerpas, M. & Nicoll, R. A. LTP requires a reserve pool of glutamate receptors independent of subunit type. Nature 493, 495-500 (2013).
8. Lledo, P. M., Zhang, X., Südhof, T. C., Malenka, R. C. & Nicoll, R. A. Postsynaptic membrane fusion and long-term potentiation. Science 279, 399-403 (1998).
9. Ahmad, M. et al. Postsynaptic complexin controls AMPA receptor exocytosis during LTP. Neuron 73, 260-267 (2012).
10. Jurado, S. et al. LTP requires a unique postsynaptic SNARE fusion machinery. Neuron 77, 542-558 (2013).
11. Südhof, T. C. Neurotransmitter release: the last millisecond in the life of a synaptic vesicle. Neuron 80, 675-690 (2013).
12. Reim, K. et al. Complexins regulate the Ca2+ sensitivity of the synaptic neurotransmitter release machinery. Cell 104, 71-81 (2001).
13. Maximov, A., Tang, J., Yang, X., Pang, Z. P. & Südhof, T. C. Complexin controls the force transfer from SNARE complexes to membranes in fusion. Science 323, 516-521 (2009).
14. Geppert, M. et al. Synaptotagmin I: a major Ca2+ sensor for transmitter release at a central synapse. Cell 79, 717-727 (1994).
15. Wen, H. et al. Distinct roles for two synaptotagmin isoforms in synchronous and asynchronous transmitter release at zebrafish neuromuscular junction. Proc. Natl Acad. Sci. USA 107, 13906-13911 (2010).
16. Bacaj, T. et al. Synaptotagmin-1 and synaptotagmin-7 trigger synchronous and asynchronous phases of neurotransmitter release. Neuron 80, 947-959 (2013).
17. Bacaj, T. et al. Synaptotagmin-1 and -7 are redundantly essential for maintaining the capacity of the readily-releasable pool of synaptic vesicles. PLoS Biol. 13, e1002267 (2015).
18. Schonn, J. S., Maximov, A., Lao, Y., Südhof, T. C. & Sørensen, J. B. Synaptotagmin-1 and -7 are functionally overlapping Ca2+ sensors for exocytosis in adrenal chromaffin cells. Proc. Natl Acad. Sci. USA 105, 3998-4003 (2008).
19. Xu, W. et al. Distinct neuronal coding schemes in memory revealed by selective erasure of fast synchronous synaptic transmission. Neuron 73, 990-1001 (2012).
20. Zhou, Q. et al. Architecture of the synaptotagmin-SNARE machinery for neuronal exocytosis. Nature 525, 62-67 (2015).
21. Wyllie, D. J., Manabe, T. & Nicoll, R. A. A rise in postsynaptic Ca2+ potentiates miniature excitatory postsynaptic currents and AMPA responses in hippocampal neurons. Neuron 12, 127-138 (1994).
22. Kato, H. K., Watabe, A. M. & Manabe, T. Non-Hebbian synaptic plasticity induced by repetitive postsynaptic action potentials. J. Neurosci. 29, 11153-11160 (2009).
23. Kang, H. & Schuman, E. M. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267, 1658-1662 (1995).
24. Harward, S. C. et al. Autocrine BDNF-TrkB signalling within a single dendritic spine. Nature 538, 99-103 (2016).
25. Arendt, K. L. et al. Calcineurin mediates homeostatic synaptic plasticity by regulating retinoic acid synthesis. Proc. Natl Acad. Sci. USA 112, E5744-E5752 (2015).
26. Dudek, S. M. & Bear, M. F. Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-d-aspartate receptor blockade. Proc. Natl Acad. Sci. USA 89, 4363-4367 (1992).
27. Zamanillo, D. et al. Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science 284, 1805-1811 (1999).
28. Lu, W. et al. Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron 29, 243-254 (2001).
29. Passafaro, M., Piëch, V. & Sheng, M. Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat. Neurosci. 4, 917-926 (2001).
30. Lin, D. T. & Huganir, R. L. PICK1 and phosphorylation of the glutamate receptor 2 (GluR2) AMPA receptor subunit regulates GluR2 recycling after NMDA receptor-induced internalization. J. Neurosci. 27, 13903-13908 (2007).
31. Kwon, O. B., Longart, M., Vullhorst, D., Hoffman, D. A. & Buonanno, A. Neuregulin-1 reverses long-term potentiation at CA1 hippocampal synapses. J. Neurosci. 25, 9378-9383 (2005).
32. Lee, J., Guan, Z., Akbergenova, Y. & Littleton, J. T. Genetic analysis of synaptotagmin C2 domain specificity in regulating spontaneous and evoked neurotransmitter release. J. Neurosci. 33, 187-200 (2013).
33. Rosenmund, C. & Stevens, C. F. Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16, 1197-1207 (1996).
34. Malinow, R., Schulman, H. & Tsien, R. W. Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. Science 245, 862-866 (1989).
35. Malenka, R. C. et al. An essential role for postsynaptic calmodulin and protein kinase activity in long-term potentiation. Nature 340, 554-557 (1989).
36. Silva, A. J., Stevens, C. F., Tonegawa, S. & Wang, Y. Deficient hippocampal long-term potentiation in α -calcium-calmodulin kinase II mutant mice. Science 257, 201-206 (1992).
37. Thiagarajan, T. C., Piedras-Renteria, E. S. & Tsien, R. W. α - and β CaMKII. Inverse regulation by neuronal activity and opposing effects on synaptic strength. Neuron 36, 1103-1114 (2002).
38. Pang, Z. P., Cao, P., Xu, W. & Südhof, T. C. Calmodulin controls synaptic strength via presynaptic activation of calmodulin kinase II. J. Neurosci. 30, 4132-4142 (2010).
39. Chetkovich, D. M., Chen, L., Stocker, T. J., Nicoll, R. A. & Bredt, D. S. Phosphorylation of the postsynaptic density-95 (PSD-95)/discs large/zona occludens-1 binding site of stargazin regulates binding to PSD-95 and synaptic targeting of AMPA receptors. J. Neurosci. 22, 5791-5796 (2002).
40. Opazo, P. et al. CaMKII triggers the diffusional trapping of surface AMPARs through phosphorylation of stargazin. Neuron 67, 239-252 (2010).
41. Maximov, A. et al. Genetic analysis of synaptotagmin-7 function in synaptic vesicle exocytosis. Proc. Natl Acad. Sci. USA 105, 3986-3991 (2008).
42. Xu, J., Pang, Z. P., Shin, O. H. & Südhof, T. C. Synaptotagmin-1 functions as a Ca2+ sensor for spontaneous release. Nat. Neurosci. 12, 759-766 (2009).
43. Tang, J. et al. A complexin/synaptotagmin 1 switch controls fast synaptic vesicle exocytosis. Cell 126, 1175-1187 (2006).
44. Maximov, A., Pang, Z. P., Tervo, D. G. & Südhof, T. C. Monitoring synaptic transmission in primary neuronal cultures using local extracellular stimulation. J. Neurosci. Methods 161, 75-87 (2007).
45. Gähwiler, B. H., Capogna, M., Debanne, D., McKinney, R. A. & Thompson, S. M. Organotypic slice cultures: a technique has come of age. Trends Neurosci. 20, 471-477 (1997).
46. Aoto, J., Martinelli, D. C., Malenka, R. C., Tabuchi, K. & Südhof, T. C. Presynaptic neurexin-3 alternative splicing trans-synaptically controls postsynaptic AMPA receptor trafficking. Cell 154, 75-88 (2013).