The calcium sensor synaptotagmin 7 is required for synaptic facilitation

Nature

Volumn 529, Issue 7584, 2016, Pages 88-91

  Jackman, Skyler L ^a   Turecek, Josef ^a   Belinsky, Justine E ^a   Regehr, Wade G ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; SYNAPTOTAGMIN; SYNAPTOTAGMIN 7; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; SYT7 PROTEIN, MOUSE;

CALCIUM; EXPERIMENTAL STUDY; FACILITATION; LABORATORY METHOD; RODENT; SENSOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; FACILITATION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; MOUSE; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION; SYNAPTOSOME; THALAMOCORTICAL TRACT; ANIMAL; DEFICIENCY; FEMALE; GENETICS; MALE; METABOLISM; NERVE CELL; NERVE ENDING; SECRETION (PROCESS); SYNAPSE;

MUS;

ANIMALS; CALCIUM; CALCIUM SIGNALING; FEMALE; MALE; MICE; MICE, KNOCKOUT; NEURONAL PLASTICITY; NEURONS; NEUROTRANSMITTER AGENTS; PRESYNAPTIC TERMINALS; SYNAPSES; SYNAPTIC TRANSMISSION; SYNAPTOTAGMINS;

EID: 84953897650     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature16507     Document Type: Article

References (46)

1. Feng, T. P. Studies on the neuromuscular junction. XVIII. The local potentials around n-m junctions induced by single and multiple volleys. Chin. J. Physiol. 15, 367-404 (1940).
2. Zucker, R. S. & Regehr, W. G. Short-term synaptic plasticity. Annu. Rev. Physiol. 64, 355-405 (2002).
3. Abbott, L. F. & Regehr, W. G. Synaptic computation. Nature 431, 796-803 (2004).
4. Atluri, P. P. & Regehr, W. G. Determinants of the time course of facilitation at the granule cell to Purkinje cell synapse. J. Neurosci. 16, 5661-5671 (1996).
5. Bertram, R., Sherman, A. & Stanley, E. F. Single-domain/bound calcium hypothesis of transmitter release and facilitation. J. Neurophysiol. 75, 1919-1931 (1996).
6. Felmy, F., Neher, E. & Schneggenburger, R. Probing the intracellular calcium sensitivity of transmitter release during synaptic facilitation. Neuron 37, 801-811 (2003).
7. Südhof, T. C. A molecular machine for neurotransmitter release: synaptotagmin and beyond. Nature Med. 19, 1227-1231 (2013).
8. Matveev, V., Zucker, R. S. & Sherman, A. Facilitation through buffer saturation: Constraints on endogenous buffering properties. Biophys. J. 86, 2691-2709 (2004).
9. Blatow, M., Caputi, A., Burnashev, N., Monyer, H. & Rozov, A. Ca2+ buffer saturation underlies paired pulse facilitation in calbindin-D28k-containing terminals. Neuron 38, 79-88 (2003).
10. Mochida, S., Few, A. P., Scheuer, T. & Catterall, W. A. Regulation of presynaptic CaV2.1 channels by Ca2+ sensor proteins mediates short-term synaptic plasticity. Neuron 57, 210-216 (2008).
11. Sippy, T., Cruz-Martin, A., Jeromin, A. & Schweizer, F. E. Acute changes in short-term plasticity at synapses with elevated levels of neuronal calcium sensor-1. Nature Neurosci. 6, 1031-1038 (2003).
12. Tsujimoto, T., Jeromin, A., Saitoh, N., Roder, J. C. & Takahashi, T. Neuronal calcium sensor 1 and activity-dependent facilitation of P/Q-type calcium currents at presynaptic nerve terminals. Science 295, 2276-2279 (2002).
13. Müller, M., Felmy, F. & Schneggenburger, R. A limited contribution of Ca2+ current facilitation to paired-pulse facilitation of transmitter release at the rat calyx of Held. J. Physiol. (Lond.) 586, 5503-5520 (2008).
14. 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).
15. Li, C. et al. Ca2+-dependent and-independent activities of neural and non-neural synaptotagmins. Nature 375, 594-599 (1995).
16. Sugita, S. et al. Synaptotagmin VII as a plasma membrane Ca2+ sensor in exocytosis. Neuron 30, 459-473 (2001).
17. 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).
18. Bacaj, T. et al. Synaptotagmin-1 and synaptotagmin-7 trigger synchronous and asynchronous phases of neurotransmitter release. Neuron 80, 947-959 (2013).
19. Liu, H. et al. Synaptotagmin 7 functions as a Ca2+-sensor for synaptic vesicle replenishment. eLife 3, e01524 (2014).
20. Deschěnes, M. & Hu, B. Electrophysiology and pharmacology of the corticothalamic input to lateral thalamic nuclei: an intracellular study in the cat. Eur. J. Neurosci. 2, 140-152 (1990).
21. Lømo, T. Potentiation of monosynaptic EPSPs in the perforant path-dentate granule cell synapse. Exp. Brain Res. 12, 46-63 (1971).
22. Geiger, J. R. & Jonas, P. Dynamic control of presynaptic Ca2+ inflow by fast-inactivating K+ channels in hippocampal mossy fiber boutons. Neuron 28, 927-939 (2000).
23. Geppert, M. et al. Synaptotagmin I: a major Ca2+ sensor for transmitter release at a central synapse. Cell 79, 717-727 (1994).
24. Dingledine, R. & Somjen, G. Calcium dependence of synaptic transmission in the hippocampal slice. Brain Res. 207, 218-222 (1981).
25. Manabe, T. & Nicoll, R. A. Long-term potentiation: evidence against an increase in transmitter release probability in the CA1 region of the hippocampus. Science 265, 1888-1892 (1994).
26. Gustavsson, N.et al. Impaired insulin secretion and glucose intolerance in synaptotagmin-7 null mutant mice. Proc. Natl Acad. Sci. USA 105, 3992-3997 (2008).
27. Martinez, I. et al. Synaptotagmin VII regulates Ca2+-dependent exocytosis of lysosomes in fibroblasts. J. Cell Biol. 148, 1141-1150 (2000).
28. Klyachko, V. A. & Stevens, C. F. Excitatory and feed-forward inhibitory hippocampal synapses work synergistically as an adaptive filter of natural spike trains. PLoS Biol. 4, e207 (2006).
29. MacLeod, K. M., Horiuchi, T. K. & Carr, C. E. A role for short-term synaptic facilitation and depression in the processing of intensity information in the auditory brain stem. J. Neurophysiol. 97, 2863-2874 (2007).
30. Mongillo, G., Barak, O. & Tsodyks, M. Synaptic theory of working memory. Science 319, 1543-1546 (2008).
31. Chakrabarti, S. et al. Impaired membrane resealing and autoimmune myositis in synaptotagmin VII-deficient mice. J. Cell Biol. 162, 543-549 (2003).
32. Kim, J. H. et al. High cleavage efficiency of a 2A peptide derived from porcine teschovirus-1 in human cell lines, zebrafish and mice. PLoS ONE 6, e18556 (2011).
33. Zolotukhin, S. et al. Recombinant adeno-Associated virus purification using novel methods improves infectious titer and yield. Gene Ther. 6, 973-985 (1999).
34. Jackman, S. L., Beneduce, B. M., Drew, I. R. & Regehr, W. G. Achieving high-frequency optical control of synaptic transmission. J. Neurosci. 34, 7704-7714 (2014).
35. Kamiya, H., Shinozaki, H. & Yamamoto, C. Activation of metabotropic glutamate receptor type 2/3 suppresses transmission at rat hippocampal mossy fibre synapses. J. Physiol. (Lond.) 493, 447-455 (1996).
36. Zhao, M., Hollingworth, S. & Baylor, S. M. Properties of tri-And tetracarboxylate Ca2+ indicators in frog skeletal muscle fibers. Biophys. J. 70, 896-916 (1996).
37. Kreitzer, A. C. & Regehr, W. G. Modulation of transmission during trains at a cerebellar synapse. J. Neurosci. 20, 1348-1357 (2000).
38. Brenowitz, S. D. & Regehr, W. G. Calcium dependence of retrograde inhibition by endocannabinoids at synapses onto Purkinje cells. J. Neurosci. 23, 6373-6384 (2003).
39. Grynkiewicz, G., Poenie, M. & Tsien, R. Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450 (1985).
40. Sabatini, B. L. & Regehr, W. G. Detecting changes in calcium influx which contribute to synaptic modulation in mammalian brain slice. Neuropharmacology 34, 1453-1467 (1995).
41. Maravall, M., Mainen, Z. F., Sabatini, B. L. & Svoboda, K. Estimating intracellular calcium concentrations and buffering without wavelength ratioing. Biophys. J. 78, 2655-2667 (2000).
42. Sabatini, B. L. & Svoboda, K. Analysis of calcium channels in single spines using optical fluctuation analysis. Nature 408, 589-593 (2000).
43. Regehr, W. G. Short-term presynaptic plasticity. Cold Spring Harb. Perspect. Biol. 4, a005702 (2012).
44. Kaeser, P. S. & Regehr, W. G. Molecular mechanisms for synchronous, asynchronous, and spontaneous neurotransmitter release. Annu. Rev. Physiol. 76, 333-363 (2014).
45. Kamiya, H. & Zucker, R. S. Residual Ca2+ and short-term synaptic plasticity. Nature 371, 603-606 (1994).
46. Celio, M. R. Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35, 375-475 (1990).