Fusion Competent Synaptic Vesicles Persist upon Active Zone Disruption and Loss of Vesicle Docking

Neuron

Volumn 91, Issue 4, 2016, Pages 777-791

  Wang, Shan Shan H ^a   Held, Richard G ^a   Wong, Man Yan ^a   Liu, Changliang ^a   Karakhanyan, Aziz ^a   Kaeser, Pascal S ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN BASSOON; PROTEIN ELKS; PROTEIN MUNC13; PROTEIN PICCOLO; PROTEIN RIM; SCAFFOLD PROTEIN; SNARE PROTEIN; UNCLASSIFIED DRUG; ABC TRANSPORTER; ABCA4 PROTEIN, MOUSE; BSN PROTEIN, MOUSE; CARRIER PROTEIN; CYTOSKELETON PROTEIN; NERVE PROTEIN; NEUROPEPTIDE; PCLO PROTEIN, MOUSE; RAB6IP2 PROTEIN, MOUSE; RIM-BP3 PROTEIN, MOUSE; UNC13A PROTEIN, MOUSE;

ACTIVE ZONE DISRUPTION; ARTICLE; CALCIUM TRANSPORT; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; EXOCYTOSIS; KNOCKOUT MOUSE; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SYNAPSE VESICLE; SYNAPTIC VESICLE DOCKING; ANIMAL; CELL CULTURE; GENETICS; MEMBRANE FUSION; METABOLISM; NERVE ENDING; POSTSYNAPTIC DENSITY; SYNAPTIC MEMBRANE;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CARRIER PROTEINS; CELLS, CULTURED; CYTOSKELETAL PROTEINS; EXOCYTOSIS; MEMBRANE FUSION; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEUROPEPTIDES; POST-SYNAPTIC DENSITY; PRESYNAPTIC TERMINALS; SNARE PROTEINS; SYNAPTIC MEMBRANES; SYNAPTIC VESICLES;

EID: 84991108519     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2016.07.005     Document Type: Article

References (63)

1. Acuna, C., Liu, X., Gonzalez, A., Südhof, T.C., RIM-BPs mediate tight coupling of action potentials to Ca(2+)-triggered neurotransmitter release. Neuron 87 (2015), 1234–1247.
2. Andrews-Zwilling, Y.S., Kawabe, H., Reim, K., Varoqueaux, F., Brose, N., Binding to Rab3A-interacting molecule RIM regulates the presynaptic recruitment of Munc13-1 and ubMunc13-2. J. Biol. Chem. 281 (2006), 19720–19731.
3. Ariel, P., Ryan, T.A., Optical mapping of release properties in synapses. Front. Neural Circuits 4 (2010), 1–10.
4. Augustin, I., Rosenmund, C., Südhof, T.C., Brose, N., Munc13-1 is essential for fusion competence of glutamatergic synaptic vesicles. Nature 400 (1999), 457–461.
5. Bacaj, T., Wu, D., Burré, J., Malenka, R.C., Liu, X., Südhof, T.C., Synaptotagmin-1 and -7 are redundantly essential for maintaining the capacity of the readily-releasable pool of synaptic vesicles. PLoS Biol., 13, 2015, e1002267.
6. Betz, A., Thakur, P., Junge, H.J., Ashery, U., Rhee, J.S., Scheuss, V., Rosenmund, C., Rettig, J., Brose, N., Functional interaction of the active zone proteins Munc13-1 and RIM1 in synaptic vesicle priming. Neuron 30 (2001), 183–196.
7. Boyken, J., Grønborg, M., Riedel, D., Urlaub, H., Jahn, R., Chua, J.J., Molecular profiling of synaptic vesicle docking sites reveals novel proteins but few differences between glutamatergic and GABAergic synapses. Neuron 78 (2013), 285–297.
8. Bronk, P., Deák, F., Wilson, M.C., Liu, X., Südhof, T.C., Kavalali, E.T., Differential effects of SNAP-25 deletion on Ca2+ -dependent and Ca2+ -independent neurotransmission. J. Neurophysiol. 98 (2007), 794–806.
9. Couteaux, R., Pécot-Dechavassine, M., [Synaptic vesicles and pouches at the level of “active zones” of the neuromuscular junction]. C. R. Acad. Sci. Hebd. Seances Acad. Sci. D 271 (1970), 2346–2349.
10. Dai, Y., Taru, H., Deken, S.L., Grill, B., Ackley, B., Nonet, M.L., Jin, Y., SYD-2 Liprin-alpha organizes presynaptic active zone formation through ELKS. Nat. Neurosci. 9 (2006), 1479–1487.
11. Davydova, D., Marini, C., King, C., Klueva, J., Bischof, F., Romorini, S., Montenegro-Venegas, C., Heine, M., Schneider, R., Schröder, M.S., et al. Bassoon specifically controls presynaptic P/Q-type Ca(2+) channels via RIM-binding protein. Neuron 82 (2014), 181–194.
12. de Wit, H., Cornelisse, L.N., Toonen, R.F.G., Verhage, M., Docking of secretory vesicles is syntaxin dependent. PLoS ONE, 1, 2006, e126.
13. Deák, F., Schoch, S., Liu, X., Südhof, T.C., Kavalali, E.T., Synaptobrevin is essential for fast synaptic-vesicle endocytosis. Nat. Cell Biol. 6 (2004), 1102–1108.
14. Deng, L., Kaeser, P.S., Xu, W., Südhof, T.C., RIM proteins activate vesicle priming by reversing autoinhibitory homodimerization of Munc13. Neuron 69 (2011), 317–331.
15. Granseth, B., Odermatt, B., Royle, S.J., Lagnado, L., Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron 51 (2006), 773–786.
16. Hallermann, S., Fejtova, A., Schmidt, H., Weyhersmüller, A., Silver, R.A., Gundelfinger, E.D., Eilers, J., Bassoon speeds vesicle reloading at a central excitatory synapse. Neuron 68 (2010), 710–723.
17. 2+ channel density and vesicle docking at the presynaptic active zone. Neuron 69 (2011), 304–316.
18. Held, R.G., Liu, C., Kaeser, P.S., ELKS controls the pool of readily releasable vesicles at excitatory synapses through its N-terminal coiled-coil domains. eLife, 5, 2016, e14862.
19. Holderith, N., Lorincz, A., Katona, G., Rózsa, B., Kulik, A., Watanabe, M., Nusser, Z., Release probability of hippocampal glutamatergic terminals scales with the size of the active zone. Nat. Neurosci. 15 (2012), 988–997.
20. Imig, C., Min, S.W., Krinner, S., Arancillo, M., Rosenmund, C., Südhof, T.C., Rhee, J., Brose, N., Cooper, B.H., The morphological and molecular nature of synaptic vesicle priming at presynaptic active zones. Neuron 84 (2014), 416–431.
21. Jahn, R., Fasshauer, D., Molecular machines governing exocytosis of synaptic vesicles. Nature 490 (2012), 201–207.
22. Jockusch, W.J., Speidel, D., Sigler, A., Sørensen, J.B., Varoqueaux, F., Rhee, J.S., Brose, N., CAPS-1 and CAPS-2 are essential synaptic vesicle priming proteins. Cell 131 (2007), 796–808.
23. Kaeser, P.S., Regehr, W.G., Molecular mechanisms for synchronous, asynchronous, and spontaneous neurotransmitter release. Annu. Rev. Physiol. 76 (2014), 333–363.
24. Kaeser, P.S., Kwon, H.B., Chiu, C.Q., Deng, L., Castillo, P.E., Südhof, T.C., RIM1alpha and RIM1beta are synthesized from distinct promoters of the RIM1 gene to mediate differential but overlapping synaptic functions. J. Neurosci. 28 (2008), 13435–13447.
25. Kaeser, P.S., Deng, L., Chávez, A.E., Liu, X., Castillo, P.E., Südhof, T.C., ELKS2alpha/CAST deletion selectively increases neurotransmitter release at inhibitory synapses. Neuron 64 (2009), 227–239.
26. Kaeser, P.S., Deng, L., Wang, Y., Dulubova, I., Liu, X., Rizo, J., Südhof, T.C., RIM proteins tether Ca2+ channels to presynaptic active zones via a direct PDZ-domain interaction. Cell 144 (2011), 282–295.
27. Kaeser, P.S., Deng, L., Fan, M., Südhof, T.C., RIM genes differentially contribute to organizing presynaptic release sites. Proc. Natl. Acad. Sci. USA 109 (2012), 11830–11835.
28. Kaufmann, N., DeProto, J., Ranjan, R., Wan, H., Van Vactor, D., Drosophila liprin-alpha and the receptor phosphatase Dlar control synapse morphogenesis. Neuron 34 (2002), 27–38.
29. Kittel, R.J., Wichmann, C., Rasse, T.M., Fouquet, W., Schmidt, M., Schmid, A., Wagh, D.A., Pawlu, C., Kellner, R.R., Willig, K.I., et al. Bruchpilot promotes active zone assembly, Ca2+ channel clustering, and vesicle release. Science 312 (2006), 1051–1054.
30. Ko, J., Na, M., Kim, S., Lee, J.R., Kim, E., Interaction of the ERC family of RIM-binding proteins with the liprin-alpha family of multidomain proteins. J. Biol. Chem. 278 (2003), 42377–42385.
31. Koushika, S.P., Richmond, J.E., Hadwiger, G., Weimer, R.M., Jorgensen, E.M., Nonet, M.L., A post-docking role for active zone protein Rim. Nat. Neurosci. 4 (2001), 997–1005.
32. Lazarevic, V., Schöne, C., Heine, M., Gundelfinger, E.D., Fejtova, A., Extensive remodeling of the presynaptic cytomatrix upon homeostatic adaptation to network activity silencing. J. Neurosci. 31 (2011), 10189–10200.
33. Liu, K.S.Y., Siebert, M., Mertel, S., Knoche, E., Wegener, S., Wichmann, C., Matkovic, T., Muhammad, K., Depner, H., Mettke, C., et al. RIM-binding protein, a central part of the active zone, is essential for neurotransmitter release. Science 334 (2011), 1565–1569.
34. Liu, C., Bickford, L.S., Held, R.G., Nyitrai, H., Südhof, T.C., Kaeser, P.S., The active zone protein family ELKS supports Ca2+ influx at nerve terminals of inhibitory hippocampal neurons. J. Neurosci. 34 (2014), 12289–12303.
35. Lu, J., Machius, M., Dulubova, I., Dai, H., Südhof, T.C., Tomchick, D.R., Rizo, J., Structural basis for a Munc13-1 homodimer to Munc13-1/RIM heterodimer switch. PLoS Biol., 4, 2006, e192.
36. Miller, K.E., DeProto, J., Kaufmann, N., Patel, B.N., Duckworth, A., Van Vactor, D., Direct observation demonstrates that Liprin-alpha is required for trafficking of synaptic vesicles. Curr. Biol. 15 (2005), 684–689.
37. Morciano, M., Beckhaus, T., Karas, M., Zimmermann, H., Volknandt, W., The proteome of the presynaptic active zone: from docked synaptic vesicles to adhesion molecules and maxi-channels. J. Neurochem. 108 (2009), 662–675.
38. Müller, C.S., Haupt, A., Bildl, W., Schindler, J., Knaus, H.G., Meissner, M., Rammner, B., Striessnig, J., Flockerzi, V., Fakler, B., Schulte, U., Quantitative proteomics of the Cav2 channel nano-environments in the mammalian brain. Proc. Natl. Acad. Sci. USA 107 (2010), 14950–14957.
39. Müller, M., Liu, K.S.Y., Sigrist, S.J., Davis, G.W., RIM controls homeostatic plasticity through modulation of the readily-releasable vesicle pool. J. Neurosci. 32 (2012), 16574–16585.
40. Ohtsuka, T., Takao-Rikitsu, E., Inoue, E., Inoue, M., Takeuchi, M., Matsubara, K., Deguchi-Tawarada, M., Satoh, K., Morimoto, K., Nakanishi, H., Takai, Y., Cast: a novel protein of the cytomatrix at the active zone of synapses that forms a ternary complex with RIM1 and munc13-1. J. Cell Biol. 158 (2002), 577–590.
41. Patel, M.R., Lehrman, E.K., Poon, V.Y., Crump, J.G., Zhen, M., Bargmann, C.I., Shen, K., Hierarchical assembly of presynaptic components in defined C. elegans synapses. Nat. Neurosci. 9 (2006), 1488–1498.
42. Rizzoli, S.O., Betz, W.J., The structural organization of the readily releasable pool of synaptic vesicles. Science 303 (2004), 2037–2039.
43. Rosenmund, C., Stevens, C.F., Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16 (1996), 1197–1207.
44. Schikorski, T., Stevens, C.F., Morphological correlates of functionally defined synaptic vesicle populations. Nat. Neurosci. 4 (2001), 391–395.
45. Schoch, S., Gundelfinger, E.D., Molecular organization of the presynaptic active zone. Cell Tissue Res. 326 (2006), 379–391.
46. Schoch, S., Castillo, P.E., Jo, T., Mukherjee, K., Geppert, M., Wang, Y., Schmitz, F., Malenka, R.C., Südhof, T.C., RIM1alpha forms a protein scaffold for regulating neurotransmitter release at the active zone. Nature 415 (2002), 321–326.
47. Siksou, L., Varoqueaux, F., Pascual, O., Triller, A., Brose, N., Marty, S., A common molecular basis for membrane docking and functional priming of synaptic vesicles. Eur. J. Neurosci. 30 (2009), 49–56.
48. Spangler, S.A., Jaarsma, D., De Graaff, E., Wulf, P.S., Akhmanova, A., Hoogenraad, C.C., Differential expression of liprin-α family proteins in the brain suggests functional diversification. J. Comp. Neurol. 519 (2011), 3040–3060.
49. Spangler, S.A., Schmitz, S.K., Kevenaar, J.T., de Graaff, E., de Wit, H., Demmers, J., Toonen, R.F., Hoogenraad, C.C., Liprin-α2 promotes the presynaptic recruitment and turnover of RIM1/CASK to facilitate synaptic transmission. J. Cell Biol. 201 (2013), 915–928.
50. Südhof, T.C., The presynaptic active zone. Neuron 75 (2012), 11–25.
51. Südhof, T.C., Rothman, J.E., Membrane fusion: grappling with SNARE and SM proteins. Science 323 (2009), 474–477.
52. Sugie, A., Hakeda-Suzuki, S., Suzuki, E., Silies, M., Shimozono, M., Möhl, C., Suzuki, T., Tavosanis, G., Molecular remodeling of the presynaptic active zone of Drosophila photoreceptors via activity-dependent feedback. Neuron 86 (2015), 711–725.
53. Takao-Rikitsu, E., Mochida, S., Inoue, E., Deguchi-Tawarada, M., Inoue, M., Ohtsuka, T., Takai, Y., Physical and functional interaction of the active zone proteins, CAST, RIM1, and Bassoon, in neurotransmitter release. J. Cell Biol. 164 (2004), 301–311.
54. Thanawala, M.S., Regehr, W.G., Determining synaptic parameters using high-frequency activation. J. Neurosci. Methods 264 (2016), 136–152.
55. Varoqueaux, F., Sigler, A., Rhee, J.S., Brose, N., Enk, C., Reim, K., Rosenmund, C., Total arrest of spontaneous and evoked synaptic transmission but normal synaptogenesis in the absence of Munc13-mediated vesicle priming. Proc. Natl. Acad. Sci. USA 99 (2002), 9037–9042.
56. Wang, Y., Liu, X., Biederer, T., Südhof, T.C., A family of RIM-binding proteins regulated by alternative splicing: Implications for the genesis of synaptic active zones. Proc. Natl. Acad. Sci. USA 99 (2002), 14464–14469.
57. Watanabe, S., Rost, B.R., Camacho-Pérez, M., Davis, M.W., Söhl-Kielczynski, B., Rosenmund, C., Jorgensen, E.M., Ultrafast endocytosis at mouse hippocampal synapses. Nature 504 (2013), 242–247.
58. Weyhersmüller, A., Hallermann, S., Wagner, N., Eilers, J., Rapid active zone remodeling during synaptic plasticity. J. Neurosci. 31 (2011), 6041–6052.
59. Wyszynski, M., Kim, E., Dunah, A.W., Passafaro, M., Valtschanoff, J.G., Serra-Pagès, C., Streuli, M., Weinberg, R.J., Sheng, M., Interaction between GRIP and liprin-alpha/SYD2 is required for AMPA receptor targeting. Neuron 34 (2002), 39–52.
60. Zhen, M., Jin, Y., The liprin protein SYD-2 regulates the differentiation of presynaptic termini in C. elegans. Nature 401 (1999), 371–375.
61. Zucker, R.S., Regehr, W.G., Short-term synaptic plasticity. Annu. Rev. Physiol. 64 (2002), 355–405.
62. Zürner, M., Schoch, S., The mouse and human Liprin-alpha family of scaffolding proteins: genomic organization, expression profiling and regulation by alternative splicing. Genomics 93 (2009), 243–253.
63. Zürner, M., Mittelstaedt, T., tom Dieck, S., Becker, A., Schoch, S., Analyses of the spatiotemporal expression and subcellular localization of liprin-α proteins. J. Comp. Neurol. 519 (2011), 3019–3039.