Role of Bassoon and Piccolo in Assembly and Molecular Organization of the Active Zone

Frontiers in Synaptic Neuroscience

Volumn 7, Issue , 2016, Pages

  Gundelfinger, Eckart D ^a,b,c,d   Reissner, Carsten ^e   Garner, Craig C ^d,f  

^a LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

^b Center for Behavioral Brain Science (CBBS)   (Germany)

^c OTTO VON GUERICKE UNIVERSITY   (Germany)

^d GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^e UNIVERSITY OF MÜNSTER   (Germany)

^f CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

actin dynamics; Aczonin; Bassoon; cytomatrix at the active zone; neurotransmitter release; Piccolo; synaptic vesicle; synapto nuclear signaling

Indexed keywords

EID: 84975487872     PISSN: None     EISSN: 16633563     Source Type: Journal    
DOI: 10.3389/fnsyn.2015.00019     Document Type: Review

References (127)

1. Ackermann F. Waites C. L. Garner C. C. (2015). Presynaptic active zones in invertebrates and vertebrates. EMBO Rep. 16, 923–938. 10.15252/embr.20154043426160654
2. Ahmari S. E. Buchanan J. Smith S. J. (2000). Assembly of presynaptic active zones from cytoplasmic transport packets. Nat. Neurosci. 3, 445–451. 10.1038/7481410769383
3. Ahmed S. Wittenmayer N. Kremer T. Hoeber J. Kiran Akula A. Urlaub H. et al. (2013). Mover is a homomeric phospho-protein present on synaptic vesicles. PLoS One 8:e63474. 10.1371/journal.pone.006347423723986
4. Akbergenova Y. Bykhovskaia M. (2009). Enhancement of the endosomal endocytic pathway increases quantal size. Mol. Cell. Neurosci. 40, 199–206. 10.1016/j.mcn.2008.10.00519026748
5. Altrock W. D. Tom Dieck S. Sokolov M. Meyer A. C. Sigler A. Brakebusch C. et al. (2003). Functional inactivation of a fraction of excitatory synapses in mice deficient for the active zone protein bassoon. Neuron 37, 787–800. 10.1016/s0896-6273(03)00088-612628169
6. Berman H. M. Westbrook J. Feng Z. Gilliland G. Bhat T. N. Weissig H. et al. (2000). The protein data bank. Nucleic Acids Res. 28, 235–242. 10.1093/nar/28.1.23510592235
7. Brandstatter J. H. Fletcher E. L. Garner C. C. Gundelfinger E. D. Wassle H. (1999). Differential expression of the presynaptic cytomatrix protein bassoon among ribbon synapses in the mammalian retina. Eur. J. Neurosci. 11, 3683–3693. 10.1046/j.1460-9568.1999.00793.x10564375
8. Bruckner J. J. Gratz S. J. Slind J. K. Geske R. R. Cummings A. M. Galindo S. E. et al. (2012). Fife, a Drosophila Piccolo-RIM homolog, promotes active zone organization and neurotransmitter release. J. Neurosci. 32, 17048–17058. 10.1523/JNEUROSCI.3267-12.201223197698
9. Bury L. A. Sabo S. L. (2011). Coordinated trafficking of synaptic vesicle and active zone proteins prior to synapse formation. Neural Dev. 6:24. 10.1186/1749-8104-6-2421569270
10. Cai Q. Pan P. Y. Sheng Z. H. (2007). Syntabulin-kinesin-1 family member 5B-mediated axonal transport contributes to activity-dependent presynaptic assembly. J. Neurosci. 27, 7284–7296. 10.1523/jneurosci.0731-07.200717611281
11. Carlson S. S. Valdez G. Sanes J. R. (2010). Presynaptic calcium channels and alpha3-integrins are complexed with synaptic cleft laminins, cytoskeletal elements and active zone components. J. Neurochem. 115, 654–666. 10.1111/j.1471-4159.2010.06965.x20731762
12. Cases-Langhoff C. Voss B. Garner A. M. Appeltauer U. Takei K. Kindler S. et al. (1996). Piccolo, a novel 420 kDa protein associated with the presynaptic cytomatrix. Eur. J. Cell Biol. 69, 214–223. 8900486
13. Cen X. Nitta A. Ibi D. Zhao Y. Niwa M. Taguchi K. et al. (2008). Identification of Piccolo as a regulator of behavioral plasticity and dopamine transporter internalization. Mol. Psychiatry 13, 451–463. 10.1038/sj.mp.400213218195717
14. Chalkley R. J. Thalhammer A. Schoepfer R. Burlingame A. L. (2009). Identification of protein O-GlcNAcylation sites using electron transfer dissociation mass spectrometry on native peptides. Proc. Natl. Acad. Sci. U S A 106, 8894–8899. 10.1073/pnas.090028810619458039
15. Chavrier P. Goud B. (1999). The role of ARF and Rab GTPases in membrane transport. Curr. Opin. Cell Biol. 11, 466–475. 10.1016/s0955-0674(99)80067-210449335
16. Chen J. Billings S. E. Nishimune H. (2011). Calcium channels link the muscle-derived synapse organizer laminin beta2 to Bassoon and CAST/Erc2 to organize presynaptic active zones. J. Neurosci. 31, 512–525. 10.1523/JNEUROSCI.3771-10.201121228161
17. Chinnadurai G. (2007). Transcriptional regulation by C-terminal binding proteins. Int. J. Biochem. Cell Biol. 39, 1593–1607. 10.1016/j.biocel.2007.01.02517336131
18. Cohen L. D. Zuchman R. Sorokina O. Müller A. Dieterich D. C. Armstrong J. D. et al. (2013). Metabolic turnover of synaptic proteins: kinetics, interdependencies and implications for synaptic maintenance. PLoS One 8:e63191. 10.1371/journal.pone.006319123658807
19. Corda D. Colanzi A. Luini A. (2006). The multiple activities of CtBP/BARS proteins: the Golgi view. Trends Cell Biol. 16, 167–173. 10.1016/j.tcb.2006.01.00716483777
20. Cosker K. E. Segal R. A. (2014). Neuronal signaling through endocytosis. Cold Spring Harb Perspect. Biol. 6:a020669. 10.1101/cshperspect.a02066924492712
21. Davydova D. Marini C. King C. Klueva J. Bischof F. Romorini S. et al. (2014). Bassoon specifically controls presynaptic P/Q-type Ca(2+) channels via RIM-binding protein. Neuron 82, 181–194. 10.1016/j.neuron.2014.02.01224698275
22. Deng L. Kaeser P. S. Xu W. Südhof T. C. (2011). RIM proteins activate vesicle priming by reversing autoinhibitory Homodimerization of Munc13. Neuron 69, 317–331. 10.1016/j.neuron.2011.01.00521262469
23. Dick O. Hack I. Altrock W. D. Garner C. C. Gundelfinger E. D. Brandstätter J. H. (2001). Localization of the presynaptic cytomatrix protein Piccolo at ribbon and conventional synapses in the rat retina: comparison with Bassoon. J. Comp. Neurol. 439, 224–234. 10.1002/cne.134411596050
24. Dick O. Tom Dieck S. Altrock W. D. Ammermuller J. Weiler R. Garner C. C. et al. (2003). The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron 37, 775–786. 10.1016/s0896-6273(03)00086-212628168
25. Dieni S. Matsumoto T. Dekkers M. Rauskolb S. Ionescu M. S. Deogracias R. et al. (2012). BDNF and its pro-peptide are stored in presynaptic dense core vesicles in brain neurons. J. Cell Biol. 196, 775–788. 10.1083/jcb.20120103822412021
26. Dieni S. Nestel S. Sibbe M. Frotscher M. Hellwig S. (2015). Distinct synaptic and neurochemical changes to the granule cell-CA3 projection in Bassoon mutant mice. Front. Synaptic Neurosci. 7:18. 10.3389/fnsyn.2015.0001826576722
27. Dresbach T. Hempelmann A. Spilker C. Tom Dieck S. Altrock W. D. Zuschratter W. et al. (2003). Functional regions of the presynaptic cytomatrix protein bassoon: significance for synaptic targeting and cytomatrix anchoring. Mol. Cell. Neurosci. 23, 279–291. 10.1016/s1044-7431(03)00015-012812759
28. Dresbach T. Torres V. Wittenmayer N. Altrock W. D. Zamorano P. Zuschratter W. et al. (2006). Assembly of active zone precursor vesicles: obligatory trafficking of presynaptic cytomatrix proteins Bassoon and Piccolo via a trans-Golgi compartment. J. Biol. Chem. 281, 6038–6047. 10.1074/jbc.m50878420016373352
29. Fairless R. Masius H. Rohlmann A. Heupel K. Ahmad M. Reissner C. et al. (2008). Polarized targeting of neurexins to synapses is regulated by their C-terminal sequences. J. Neurosci. 28, 12969–12981. 10.1523/JNEUROSCI.5294-07.200819036990
30. Fejtova A. Davydova D. Bischof F. Lazarevic V. Altrock W. D. Romorini S. et al. (2009). Dynein light chain regulates axonal trafficking and synaptic levels of Bassoon. J. Cell Biol. 185, 341–355. 10.1083/jcb.20080715519380881
31. Fenster S. D. Chung W. J. Zhai R. Cases-Langhoff C. Voss B. Garner A. M. et al. (2000). Piccolo, a presynaptic zinc finger protein structurally related to bassoon. Neuron 25, 203–214. 10.1016/s0896-6273(00)80883-110707984
32. Fenster S. D. Kessels M. M. Qualmann B. Chung W. J. Nash J. Gundelfinger E. D. et al. (2003). Interactions between Piccolo and the actin/dynamin-binding protein Abp1 link vesicle endocytosis to presynaptic active zones. J. Biol. Chem. 278, 20268–20277. 10.1074/jbc.m21079220012654920
33. Frank T. Rutherford M. A. Strenzke N. Neef A. Pangršič T. Khimich D. et al. (2010). Bassoon and the synaptic ribbon organize Ca(2)+ channels and vesicles to add release sites and promote refilling. Neuron 68, 724–738. 10.1016/j.neuron.2010.10.02721092861
34. 2+ sensor in pancreatic beta-cells. Involvement of cAMP-GEFII.Rim2.Piccolo complex in cAMP-dependent exocytosis. J. Biol. Chem. 277, 50497–50502. 10.1074/jbc.m21014620012401793
35. Furukawa-Hibi Y. Nitta A. Fukumitsu H. Somiya H. Furukawa S. Nabeshima T. et al. (2010). Overexpression of piccolo C2A domain induces depression-like behavior in mice. Neuroreport 21, 1177–1181. 10.1097/WNR.0b013e328341168520980930
36. Garcia J. Gerber S. H. Sugita S. Südhof T. C. Rizo J. (2004). A conformational switch in the Piccolo C2A domain regulated by alternative splicing. Nat. Struct. Mol. Biol. 11, 45–53. 10.1038/nsmb70714718922
37. Garner C. C. Kindler S. Gundelfinger E. D. (2000). Molecular determinants of presynaptic active zones. Curr. Opin. Neurobiol. 10, 321–327. 10.1016/s0959-4388(00)00093-310851173
38. Garner C. C. Zhai R. G. Gundelfinger E. D. Ziv N. E. (2002). Molecular mechanisms of CNS synaptogenesis. Trends Neurosci. 25, 243–251. 10.1016/s0166-2236(02)02152-511972960
39. Gerber S. H. Garcia J. Rizo J. Südhof T. C. (2001). An unusual C(2)-domain in the active-zone protein piccolo: implications for Ca(2+) regulation of neurotransmitter release. EMBO J. 20, 1605–1619. 10.1093/emboj/20.7.160511285225
40. Ghiglieri V. Sgobio C. Patassini S. Bagetta V. Fejtova A. Giampà C. et al. (2010). TrkB/BDNF-dependent striatal plasticity and behavior in a genetic model of epilepsy: modulation by valproic acid. Neuropsychopharmacology 35, 1531–1540. 10.1038/npp.2010.2320200504
41. Giniatullina A. Maroteaux G. Geerts C. J. Koopmans B. Loos M. Klaassen R. et al. (2015). Functional characterization of the PCLO p.Ser4814Ala variant associated with major depressive disorder reveals cellular but not behavioral differences. Neuroscience 300, 518–538. 10.1016/j.neuroscience.2015.05.04726045179
42. Gruber M. Lupas A. N. (2003). Historical review: another 50th anniversary—new periodicities in coiled coils. Trends Biochem. Sci. 28, 679–685. 10.1016/j.tibs.2003.10.00814659700
43. Gundelfinger E. D. Fejtova A. (2012). Molecular organization and plasticity of the cytomatrix at the active zone. Curr. Opin. Neurobiol. 22, 423–430. 10.1016/j.conb.2011.10.00522030346
44. Habas R. Kato Y. He X. (2001). Wnt/Frizzled activation of Rho regulates vertebrate gastrulation and requires a novel Formin homology protein Daam1. Cell 107, 843–854. 10.1016/s0092-8674(01)00614-611779461
45. Haeberle H. Fujiwara M. Chuang J. Medina M. M. Panditrao M. V. Bechstedt S. et al. (2004). Molecular profiling reveals synaptic release machinery in Merkel cells. Proc. Natl. Acad. Sci. U S A 101, 14503–14508. 10.1073/pnas.040630810115448211
46. Hagiwara A. Fukazawa Y. Deguchi-Tawarada M. Ohtsuka T. Shigemoto R. (2005). Differential distribution of release-related proteins in the hippocampal CA3 area as revealed by freeze-fracture replica labeling. J. Comp. Neurol. 489, 195–216. 10.1002/cne.2063315983999
47. Hallermann S. Fejtova A. Schmidt H. Weyhersmüller A. Silver R. A. Gundelfinger E. D. et al. (2010). Bassoon speeds vesicle reloading at a central excitatory synapse. Neuron 68, 710–723. 10.1016/j.neuron.2010.10.02621092860
48. Han Y. Kaeser P. S. Südhof T. C. Schneggenburger R. (2011). RIM determines Ca(2+) channel density and vesicle docking at the presynaptic active zone. Neuron 69, 304–316. 10.1016/j.neuron.2010.12.01421262468
49. Heyden A. Ionescu M. C. Romorini S. Kracht B. Ghiglieri V. Calabresi P. et al. (2011). Hippocampal enlargement in Bassoon-mutant mice is associated with enhanced neurogenesis, reduced apoptosis and abnormal BDNF levels. Cell Tissue Res. 346, 11–26. 10.1007/s00441-011-1233-321935677
50. Hibino H. Pironkova R. Onwumere O. Vologodskaia M. Hudspeth A. J. Lesage F. (2002). RIM binding proteins (RBPs) couple Rab3-interacting molecules (RIMs) to voltage-gated Ca(2+) channels. Neuron 34, 411–423. 10.1016/s0896-6273(02)00667-011988172
51. Higgs H. N. (2005). Formin proteins: a domain-based approach. Trends Biochem. Sci. 30, 342–353. 10.1016/j.tibs.2005.04.01415950879
52. Hübler D. Rankovic M. Richter K. Lazarevic V. Altrock W. D. Fischer K. D. et al. (2012). Differential spatial expression and subcellular localization of CtBP family members in rodent brain. PLoS One 7:e39710. 10.1371/journal.pone.003971022745816
53. Ivanova D. Dirks A. Montenegro-Venegas C. Schone C. Altrock W. D. Marini C. et al. (2015). Synaptic activity controls localization and function of CtBP1 via binding to Bassoon and Piccolo. EMBO J. 34, 1056–1077. 10.15252/embj.20148879625652077
54. 2+ channels from glucagon-like peptide-1 potentiation of insulin secretion in INS-1 cells via displacement from lipid rafts. J. Pharmacol. Exp. Ther. 330, 283–293. 10.1124/jpet.109.15067219351867
55. Jing Z. Rutherford M. A. Takago H. Frank T. Fejtova A. Khimich D. et al. (2013). Disruption of the presynaptic cytomatrix protein bassoon degrades ribbon anchorage, multiquantal release and sound encoding at the hair cell afferent synapse. J. Neurosci. 33, 4456–4467. 10.1523/JNEUROSCI.3491-12.201323467361
56. Jordan B. A. Kreutz M. R. (2009). Nucleocytoplasmic protein shuttling: the direct route in synapse-to-nucleus signaling. Trends Neurosci. 32, 392–401. 10.1016/j.tins.2009.04.00119524307
57. Jose M. Nair D. K. Altrock W. D. Dresbach T. Gundelfinger E. D. Zuschratter W. (2008). Investigating interactions mediated by the presynaptic protein bassoon in living cells by Foerster’s resonance energy transfer and fluorescence lifetime imaging microscopy. Biophys. J. 94, 1483–1496. 10.1529/biophysj.107.11167417933880
58. Juranek J. Mukherjee K. Rickmann M. Martens H. Calka J. Südhof T. C. et al. (2006). Differential expression of active zone proteins in neuromuscular junctions suggests functional diversification. Eur. J. Neurosci. 24, 3043–3052. 10.1111/j.1460-9568.2006.05183.x17156365
59. Kaeser P. S. Deng L. Fan M. Südhof T. C. (2012). RIM genes differentially contribute to organizing presynaptic release sites. Proc. Natl. Acad. Sci. U S A 109, 11830–11835. 10.1073/pnas.120931810922753485
60. Kähne T. Kolodziej A. Smalla K. H. Eisenschmidt E. Haus U. U. Weismantel R. et al. (2012). Synaptic proteome changes in mouse brain regions upon auditory discrimination learning. Proteomics 12, 2433–2444. 10.1002/pmic.20110066922696468
61. Kelley L. A. Sternberg M. J. (2009). Protein structure prediction on the web: a case study using the Phyre server. Nat. Protoc. 4, 363–371. 10.1038/nprot.2009.219247286
62. Kessels M. M. Engqvist-Goldstein A. E. Drubin D. G. Qualmann B. (2001). Mammalian Abp1, a signal-responsive F-actin-binding protein, links the actin cytoskeleton to endocytosis via the GTPase dynamin. J. Cell Biol. 153, 351–366. 10.1083/jcb.153.2.35111309416
63. Khimich D. Nouvian R. Pujol R. Tom Dieck S. Egner A. Gundelfinger E. D. et al. (2005). Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature 434, 889–894. 10.1038/nature0341815829963
64. Kim S. Ko J. Shin H. Lee J. R. Lim C. Han J. H. et al. (2003). The GIT family of proteins forms multimers and associates with the presynaptic cytomatrix protein Piccolo. J. Biol. Chem. 278, 6291–6300. 10.1074/jbc.m21228720012473661
65. Korber C. Horstmann H. Venkataramani V. Herrmannsdörfer F. Kremer T. Kaiser M. et al. (2015). Modulation of presynaptic release probability by the vertebrate-specific protein mover. Neuron 87, 521–533. 10.1016/j.neuron.2015.07.00126212709
66. Kovar D. R. (2006). Molecular details of formin-mediated actin assembly. Curr. Opin. Cell Biol. 18, 11–17. 10.1016/j.ceb.2005.12.01116364624
67. Kravchick D. O. Jordan B. A. (2015). Presynapses go nuclear! EMBO J. 34, 984–986. 10.15252/embj.20159133125762591
68. Kremer T. Kempf C. Wittenmayer N. Nawrotzki R. Kuner T. Kirsch J. et al. (2007). Mover is a novel vertebrate-specific presynaptic protein with differential distribution at subsets of CNS synapses. FEBS Lett. 581, 4727–4733. 10.1016/j.febslet.2007.08.07017869247
69. Langnaese K. Seidenbecher C. Wex H. Seidel B. Hartung K. Appeltauer U. et al. (1996). Protein components of a rat brain synaptic junctional protein preparation. Brain Res. Mol. Brain Res. 42, 118–122. 10.1016/s0169-328x(96)00147-78915587
70. Lazarevic V. Pothula S. Andres-Alonso M. Fejtova A. (2013). Molecular mechanisms driving homeostatic plasticity of neurotransmitter release. Front. Cell. Neurosci. 7:244. 10.3389/fncel.2013.0024424348337
71. Lazarevic V. Schöne C. Heine M. Gundelfinger E. D. Fejtova A. (2011). Extensive remodeling of the presynaptic cytomatrix upon homeostatic adaptation to network activity silencing. J. Neurosci. 31, 10189–10200. 10.1523/JNEUROSCI.2088-11.201121752995
72. Leal-Ortiz S. Waites C. L. Terry-Lorenzo R. Zamorano P. Gundelfinger E. D. Garner C. C. (2008). Piccolo modulation of synapsin1a dynamics regulates synaptic vesicle exocytosis. J. Cell Biol. 181, 831–846. 10.1083/jcb.20071116718519737
73. Limbach C. Laue M. M. Wang X. Hu B. Thiede N. Hultqvist G. et al. (2011). Molecular in situ topology of Aczonin/Piccolo and associated proteins at the mammalian neurotransmitter release site. Proc. Natl. Acad. Sci. U S A 108, E392–E401. 10.1073/pnas.110170710821712437
74. Liu W. Sato A. Khadka D. Bharti R. Diaz H. Runnels L. W. et al. (2008). Mechanism of activation of the Formin protein Daam1. Proc. Natl. Acad. Sci. U S A 105, 210–215. 10.1073/pnas.070727710518162551
75. Lucido A. L. Suarez Sanchez F. Thostrup P. Kwiatkowski A. V. Leal-Ortiz S. Gopalakrishnan G. et al. (2009). Rapid assembly of functional presynaptic boutons triggered by adhesive contacts. J. Neurosci. 29, 12449–12466. 10.1523/JNEUROSCI.1381-09.200919812321
76. Maas C. Torres V. I. Altrock W. D. Leal-Ortiz S. Wagh D. Terry-Lorenzo R. T. et al. (2012). Formation of Golgi-derived active zone precursor vesicles. J. Neurosci. 32, 11095–11108. 10.1523/JNEUROSCI.0195-12.201222875941
77. Magupalli V. G. Schwarz K. Alpadi K. Natarajan S. Seigel G. M. Schmitz F. (2008). Multiple RIBEYE-RIBEYE interactions create a dynamic scaffold for the formation of synaptic ribbons. J. Neurosci. 28, 7954–7967. 10.1523/JNEUROSCI.1964-08.200818685021
78. Mendoza Schulz A. Jing Z. Sánchez Caro J. M. Wetzel F. Dresbach T. Strenzke N. et al. (2014). Bassoon-disruption slows vesicle replenishment and induces homeostatic plasticity at a CNS synapse. EMBO J. 33, 512–527. 10.1002/embj.20138588724442636
79. Minerbi A. Kahana R. Goldfeld L. Kaufman M. Marom S. Ziv N. E. (2009). Long-term relationships between synaptic tenacity, synaptic remodeling and network activity. PLoS Biol. 7:e1000136. 10.1371/journal.pbio.100013619554080
80. Mukherjee K. Yang X. Gerber S. H. Kwon H. B. Ho A. Castillo P. E. et al. (2010). Piccolo and bassoon maintain synaptic vesicle clustering without directly participating in vesicle exocytosis. Proc. Natl. Acad. Sci. U S A 107, 6504–6509. 10.1073/pnas.100230710720332206
81. Müller C. S. Haupt A. Bildl W. Schindler J. Knaus H. G. Meissner M. et al. (2010). Quantitative proteomics of the Cav2 channel nano-environments in the mammalian brain. Proc. Natl. Acad. Sci. U S A 107, 14950–14957. 10.1073/pnas.100594010720668236
82. Munton R. P. Tweedie-Cullen R. Livingstone-Zatchej M. Weinandy F. Waidelich M. Longo D. et al. (2007). Qualitative and quantitative analyses of protein phosphorylation in naive and stimulated mouse synaptosomal preparations. Mol. Cell. Proteomics 6, 283–293. 10.1074/mcp.m600046-mcp20017114649
83. Nguyen T. H. Maucort G. Sullivan R. K. Schenning M. Lavidis N. A. McCluskey A. et al. (2012). Actin- and dynamin-dependent maturation of bulk endocytosis restores neurotransmission following synaptic depletion. PLoS One 7:e36913. 10.1371/journal.pone.003691322629340
84. Nishimune H. (2012). Active zones of mammalian neuromuscular junctions: formation, density and aging. Ann. N Y Acad. Sci. 1274, 24–32. 10.1111/j.1749-6632.2012.06836.x23252894
85. Nishimune H. Numata T. Chen J. Aoki Y. Wang Y. Starr M. P. et al. (2012). Active zone protein Bassoon co-localizes with presynaptic calcium channel, modifies channel function and recovers from aging related loss by exercise. PLoS One 7:e38029. 10.1371/journal.pone.003802922701595
86. Nishimune H. Sanes J. R. Carlson S. S. (2004). A synaptic laminin-calcium channel interaction organizes active zones in motor nerve terminals. Nature 432, 580–587. 10.1038/nature0311215577901
87. Panayotis N. Karpova A. Kreutz M. R. Fainzilber M. (2015). Macromolecular transport in synapse to nucleus communication. Trends Neurosci. 38, 108–116. 10.1016/j.tins.2014.12.00125534890
88. Podufall J. Tian R. Knoche E. Puchkov D. Walter A. M. Rosa S. et al. (2014). A presynaptic role for the cytomatrix protein GIT in synaptic vesicle recycling. Cell Rep. 7, 1417–1425. 10.1016/j.celrep.2014.04.05124882013
89. Popiolek M. Ross J. F. Charych E. Chanda P. Gundelfinger E. D. Moss S. J. et al. (2011). D-amino acid oxidase activity is inhibited by an interaction with bassoon protein at the presynaptic active zone. J. Biol. Chem. 286, 28867–28875. 10.1074/jbc.M111.26206321700703
90. Quiroz F. G. Chilkoti A. (2015). Sequence heuristics to encode phase behaviour in intrinsically disordered protein polymers. Nat. Mater. 14, 1164–1171. 10.1038/nmat441826390327
91. Regus-Leidig H. Fuchs M. Löhner M. Leist S. R. Leal-Ortiz S. Chiodo V. A. et al. (2014). In vivo knockdown of Piccolino disrupts presynaptic ribbon morphology in mouse photoreceptor synapses. Front. Cell. Neurosci. 8:259. 10.3389/fncel.2014.0025925232303
92. Regus-Leidig H. Ott C. Löhner M. Atorf J. Fuchs M. Sedmak T. et al. (2013). Identification and immunocytochemical characterization of Piccolino, a novel Piccolo splice variant selectively expressed at sensory ribbon synapses of the eye and ear. PLoS One 8:e70373. 10.1371/journal.pone.007037323936420
93. Richter K. Langnaese K. Kreutz M. R. Olias G. Zhai R. Scheich H. et al. (1999). Presynaptic cytomatrix protein bassoon is localized at both excitatory and inhibitory synapses of rat brain. J. Comp. Neurol. 408, 437–448. 10.1002/(sici)1096-9861(19990607)408:3<437::aid-cne9>3.0.co;2-510340516
94. Rostaing P. Real E. Siksou L. Lechaire J. P. Boudier T. Boeckers T. M. et al. (2006). Analysis of synaptic ultrastructure without fixative using high-pressure freezing and tomography. Eur. J. Neurosci. 24, 3463–3474. 10.1111/j.1460-9568.2006.05234.x17229095
95. Sauder J. M. Dunbrack R. L. Jr. (2000). Genomic fold assignment and rational modeling of proteins of biological interest. Proc. Int. Conf. Intell. Syst. Mol. Biol. 8, 296–306. 10977091
96. Schmitz F. Königstorfer A. Südhof T. C. (2000). RIBEYE, a component of synaptic ribbons: a protein’s journey through evolution provides insight into synaptic ribbon function. Neuron 28, 857–872. 10.1016/s0896-6273(00)00159-811163272
97. Schoch S. Gundelfinger E. D. (2006). Molecular organization of the presynaptic active zone. Cell Tissue Res. 326, 379–391. 10.1007/s00441-006-0244-y16865347
98. Scholz K. P. Miller R. J. (1995). Developmental changes in presynaptic calcium channels coupled to glutamate release in cultured rat hippocampal neurons. J. Neurosci. 15, 4612–4617. 7790927
99. Schröder M. S. Stellmacher A. Romorini S. Marini C. Montenegro-Venegas C. Altrock W. D. et al. (2013). Regulation of presynaptic anchoring of the scaffold protein Bassoon by phosphorylation-dependent interaction with 14–3-3 adaptor proteins. PLoS One 8:e58814. 10.1371/journal.pone.005881423516560
100. Shapira M. Zhai R. G. Dresbach T. Bresler T. Torres V. I. Gundelfinger E. D. et al. (2003). Unitary assembly of presynaptic active zones from Piccolo-Bassoon transport vesicles. Neuron 38, 237–252. 10.1016/s0896-6273(03)00207-112718858
101. 2+ channel in insulin granule exocytosis. J. Biol. Chem. 279, 7956–7961. 10.1074/jbc.m30906820014660679
102. 2+ signals in insulin granule exocytosis. Diabetes 53, S59–S62. 10.2337/diabetes.53.suppl_3.s5915561922
103. Siddiqui T. J. Craig A. M. (2011). Synaptic organizing complexes. Curr. Opin. Neurobiol. 21, 132–143. 10.1016/j.conb.2010.08.01620832286
104. Sigrist S. J. Schmitz D. (2011). Structural and functional plasticity of the cytoplasmic active zone. Curr. Opin. Neurobiol. 21, 144–150. 10.1016/j.conb.2010.08.01220832284
105. Siksou L. Rostaing P. Lechaire J. P. Boudier T. Ohtsuka T. Fejtová A. et al. (2007). Three-dimensional architecture of presynaptic terminal cytomatrix. J. Neurosci. 27, 6868–6877. 10.1523/jneurosci.1773-07.200717596435
106. Südhof T. C. (2012). The presynaptic active zone. Neuron 75, 11–25. 10.1016/j.neuron.2012.06.01222794257
107. Takao-Rikitsu E. Mochida S. Inoue E. Deguchi-Tawarada M. Inoue M. Ohtsuka T. et al. (2004). Physical and functional interaction of the active zone proteins, CAST, RIM1 and Bassoon, in neurotransmitter release. J. Cell Biol. 164, 301–311. 10.1083/jcb.20030710114734538
108. Tao-Cheng J. H. (2007). Ultrastructural localization of active zone and synaptic vesicle proteins in a preassembled multi-vesicle transport aggregate. Neuroscience 150, 575–584. 10.1016/j.neuroscience.2007.09.03117977664
109. tom Dieck S. Altrock W. D. Kessels M. M. Qualmann B. Regus H. Brauner D. et al. (2005). Molecular dissection of the photoreceptor ribbon synapse: physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex. J. Cell Biol. 168, 825–836. 10.1083/jcb.20040815715728193
110. tom Dieck S. Sanmarti-Vila L. Langnaese K. Richter K. Kindler S. Soyke A. et al. (1998). Bassoon, a novel zinc-finger CAG/glutamine-repeat protein selectively localized at the active zone of presynaptic nerve terminals. J. Cell Biol. 142, 499–509. 10.1083/jcb.142.2.4999679147
111. Trinidad J. C. Specht C. G. Thalhammer A. Schoepfer R. Burlingame A. L. (2006). Comprehensive identification of phosphorylation sites in postsynaptic density preparations. Mol. Cell. Proteomics 5, 914–922. 10.1074/mcp.t500041-mcp20016452087
112. Valente C. Luini A. Corda D. (2013). Components of the CtBP1/BARS-dependent fission machinery. Histochem. Cell Biol. 140, 407–421. 10.1007/s00418-013-1138-123996193
113. Vardinon-Friedman H. Bresler T. Garner C. C. Ziv N. E. (2000). Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron 27, 57–69. 10.1016/S0896-6273(00)00009-X
114. Vosseller K. Trinidad J. C. Chalkley R. J. Specht C. G. Thalhammer A. Lynn A. J. et al. (2006). O-linked N-acetylglucosamine proteomics of postsynaptic density preparations using lectin weak affinity chromatography and mass spectrometry. Mol. Cell. Proteomics 5, 923–934. 10.1074/mcp.t500040-mcp20016452088
115. Wagh D. A. Rasse T. M. Asan E. Hofbauer A. Schwenkert I. Dürrbeck H. et al. (2006). Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49, 833–844. 10.1016/j.neuron.2006.02.00816543132
116. Wagh D. Terry-Lorenzo R. Waites C. L. Leal-Ortiz S. A. Maas C. Reimer R. J. et al. (2015). Piccolo directs activity dependent F-actin assembly from presynaptic active Zones via Daam1. PLoS One 10:e0120093. 10.1371/journal.pone.012009325897839
117. Waites C. L. Craig A. M. Garner C. C. (2005). Mechanisms of vertebrate synaptogenesis. Annu. Rev. Neurosci. 28, 251–274. 10.1146/annurev.neuro.27.070203.14433616022596
118. Waites C. L. Garner C. C. (2011). Presynaptic function in health and disease. Trends Neurosci. 34, 326–337. 10.1016/j.tins.2011.03.00421596448
119. Waites C. L. Leal-Ortiz S. A. Andlauer T. F. Sigrist S. J. Garner C. C. (2011). Piccolo regulates the dynamic assembly of presynaptic F-actin. J. Neurosci. 31, 14250–14263. 10.1523/JNEUROSCI.1835-11.201121976510
120. Waites C. L. Leal-Ortiz S. A. Okerlund N. Dalke H. Fejtova A. Altrock W. D. et al. (2013). Bassoon and Piccolo maintain synapse integrity by regulating protein ubiquitination and degradation. EMBO J. 32, 954–969. 10.1038/emboj.2013.2723403927
121. Wang X. Hu B. Zieba A. Neumann N. G. Kasper-Sonnenberg M. Honsbein A. et al. (2009). A protein interaction node at the neurotransmitter release site: domains of Aczonin/Piccolo, Bassoon, CAST and rim converge on the N-terminal domain of Munc13–1. J. Neurosci. 29, 12584–12596. 10.1523/JNEUROSCI.1255-09.200919812333
122. Wang X. Kibschull M. Laue M. M. Lichte B. Petrasch-Parwez E. Kilimann M. W. (1999). Aczonin, a 550-kD putative scaffolding protein of presynaptic active zones, shares homology regions with Rim and Bassoon and binds profilin. J. Cell Biol. 147, 151–162. 10.1083/jcb.147.1.15110508862
123. Watanabe S. Liu Q. Davis M. W. Hollopeter G. Thomas N. Jorgensen N. B. et al. (2013a). Ultrafast endocytosis at Caenorhabditis elegans neuromuscular junctions. Elife 2:e00723. 10.7554/eLife.0072324015355
124. Watanabe S. Rost B. R. Camacho-Pérez M. Davis M. W. Söhl-Kielczynski B. Rosenmund C. et al. (2013b). Ultrafast endocytosis at mouse hippocampal synapses. Nature 504, 242–247. 10.1038/nature1280924305055
125. Zhai R. G. Vardinon-Friedman H. Cases-Langhoff C. Becker B. Gundelfinger E. D. Ziv N. E. et al. (2001). Assembling the presynaptic active zone: a characterization of an active one precursor vesicle. Neuron 29, 131–143. 10.1016/S0896-6273(01)00185-411182086
126. Zhou Q. Lai Y. Bacaj T. Zhao M. Lyubimov A. Y. Uervirojnangkoorn M. et al. (2015). Architecture of the synaptotagmin-SNARE machinery for neuronal exocytosis. Nature 525, 62–67. 10.1038/nature1497526280336
127. Ziv N. E. Fisher-Lavie A. (2014). Presynaptic and postsynaptic scaffolds: dynamics fast and slow. Neuroscientist 20, 439–452. 10.1177/107385841452332124609206