Molecular organization and assembly of the presynaptic active zone of neurotransmitter release

Results and Problems in Cell Differentiation

Volumn 43, Issue , 2006, Pages 49-68

  Fejtova, Anna ^a   Gundelfinger, Eckart D ^a  

^a LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; CYTOSKELETON PROTEIN; NERVE PROTEIN;

BIOLOGICAL MODEL; BRAIN; CELL MEMBRANE; CHEMISTRY; CYTOLOGY; CYTOSKELETON; EXOCYTOSIS; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; REVIEW; SYNAPSE; SYNAPSE VESICLE; SYNAPTIC MEMBRANE; SYNAPTOSOME; TRANSPORT AT THE CELLULAR LEVEL; TRANSPORT VESICLE; ULTRASTRUCTURE;

BIOLOGICAL TRANSPORT; BRAIN; CELL MEMBRANE; CYTOSKELETAL PROTEINS; CYTOSKELETON; EXOCYTOSIS; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; NEUROTRANSMITTER AGENTS; PRESYNAPTIC TERMINALS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SYNAPSES; SYNAPTIC MEMBRANES; SYNAPTIC VESICLES; TRANSPORT VESICLES;

EID: 33749033079     PISSN: 00801844     EISSN: 18610412     Source Type: Book Series    
DOI: 10.1007/400_012     Document Type: Review

References (78)

1. Ahmari SE, Buchanan J, Smith SJ (2000) Assembly of presynaptic active zones from cytoplasmic transport packets. Nat Neurosci 3:445-451
2. Altrock WD, tom Dieck S, Sokolov M, Meyer AC, Sigler A, Brakebusch C, Fassler R, Richter K, Boeckers TM, Potschka H, Brandt C, Loscher W, Grimberg D, Dresbach T, Hempelmann A, Hassan H, Balschun D, Frey JU, Brandstatter JH, Garner CC, Rosenmund C, Gundelfinger ED (2003) Functional inactivation of a fraction of excitatory synapses in mice deficient for the active zone protein Bassoon. Neuron 37:787-800
3. Betz A, Thakur P, Junge HJ, Ashery U, Rhee JS, Scheuss V, Rosenmund C, Rettig J, Brose N (2001) Functional interaction of the active zone proteins Munc13-1 and RIM1 in synaptic vesicle priming. Neuron 30:183-196
4. Brandstatter JH, Fletcher EL, Garner CC, Gundelfinger ED, Wassle H (1999) Differential expression of the presynaptic cytomatrix protein Bassoon among ribbon synapses in the mammalian retina. Eur J Neurosci 11:3683-3693
5. Bresler T, Shapira M, Boeckers T, Dresbach T, Futter M, Garner CC, Rosenblum K, Gundelfinger ED, Ziv NE (2004) Postsynaptic density assembly is fundamentally different from presynaptic active zone assembly. J Neurosci 24:1507-1520
6. Brose N, Rosenmund C, Rettig J (2000) Regulation of transmitter release by Unc-13 and its homologues. Curr Opin Neurobiol 10:303-311
7. Cases-Langhoff C, Voss B, Garner AM, Appeltauer U, Takei K, Kindler S, Veh RW, De Camilli P, Gundelfinger ED, Garner CC (1996) Piccolo, a novel 420 kDa protein associated with the presynaptic cytomatrix. Eur J Cell Biol 69:214-223
8. Castillo PE, Schoch S, Schmitz F, Sudhof TC, Malenka RC (2002) RIM1alpha is required for presynaptic long-term potentiation. Nature 415:327-330
9. Chapman ER (2002) Synaptotagmin: A Ca(2+) sensor that triggers exocytosis? Nat Rev Mol Cell Biol 3:498-508
10. Coppola T, Magnin-Luthi S, Perret-Menoud V, Gattesco S, Schiavo G, Regazzi R (2001) Direct interaction of the Rab3 effector RIM with Ca2+ channels, SNAP-25, and synaptotagmin. J Biol Chem 276:32756-32762
11. Deguchi-Tawarada M, Inoue E, Takao-Rikitsu E, Inoue M, Ohtsuka T, Takai Y (2004) CAST2: Identification and characterization of a protein structurally related to the presynaptic cytomatrix protein CAST. Genes Cells 9:15-23
12. Dick O, Hack I, Altrock WD, Garner CC, Gundelfinger ED, Brandstatter JH (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
13. Dick O, tom Dieck S, Altrock WD, Ammermuller J, Weiler R, Garner CC, Gundelfinger ED, Brandstatter JH (2003) The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron 37:775-786
14. Dresbach T, Qualmann B, Kessels MM, Garner CC, Gundelfinger ED (2001) The presynaptic cytomatrix of brain synapses. Cell Mol Life Sci 58:94-116
15. Dresbach T, Hempelmann A, Spilker C, tom Dieck S, Altrock WD, Zuschratter W, Garner CC, Gundelfinger ED (2003) Functional regions of the presynaptic cytomatrix protein bassoon: Significance for synaptic targeting and cytomatrix anchoring. Mol Cell Neurosci 23:279-291
16. Dresbach T, Torres V, Wittenmayer N, Altrock WD, Zamorano P, Zuschratter W, Nawrotzki R, Ziv NE, Garner CC, Gundelfinger ED (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
17. Dunah AW, Hueske E, Wyszynski M, Hoogenraad CC, Jaworski J, Pak DT, Simonetta A, Liu G, Sheng M (2005) LAR receptor protein tyrosine phosphatases in the development and maintenance of excitatory synapses. Nat Neurosci 8:458-467
18. Fenster SD, Garner CC (2002) Gene structure and genetic localization of the PCLO gene encoding the presynaptic active zone protein Piccolo. Int J Dev Neurosci 20:161-171
19. Fenster SD, Kessels MM, Qualmann B, Chung WJ, Nash J, Gundelfinger ED, Garner CC (2003) Interactions between Piccolo and the actin/ dynamin-binding protein Abp1 link vesicle endocytosis to presynaptic active zones. J Biol Chem 278:20268-20277
20. Fenster SD, Chung WJ, Zhai R, Cases-Langhoff C, Voss B, Garner AM, Kaempf U, Kindler S, Gundelfinger ED, Garner CC (2000) Piccolo, a presynaptic zinc finger protein structurally related to bassoon. Neuron 25:203-214
21. Friedman HV, Bresler T, Garner CC, Ziv NE (2000) Assembly of new individual excitatory synapses: Time course and temporal order of synaptic molecule recruitment. Neuron 27:57-69
22. Fuchs PA, Glowatzki E, Moser T (2003) The afferent synapse of cochlear hair cells. Curr Opin Neurobiol 13:452-458
23. Fujimoto K, Shibasaki T, Yokoi N, Kashima Y, Matsumoto M, Sasaki T, Tajima N, Iwanaga T, Seino S (2002) Piccolo, a Ca2+ sensor in pancreatic beta-cells. Involvement of cAMP-GEFII.Rim2.Piccolo complex in cAMP-dependent exocytosis. J Biol Chem 277:50497-50502
24. Furusawa T, Moribe H, Kondoh H, Higashi Y (1999) Identification of CtBP1 and CtBP2 as corepressors of zinc finger-homeodomain factor deltaEF1. Mol Cell Biol 19:8581-8590
25. Garcia J, Gerber SH, Sugita S, Sudhof TC, Rizo J (2004) A conformational switch in the Piccolo C2A domain regulated by alternative splicing. Nat Struct Mol Biol 11:45-53
26. Garner CC, Kindler S, Gundelfinger ED (2000) Molecular determinants of presynaptic active zones. Curr Opin Neurobiol 10:321-327
27. Garner CC, Zhai RG, Gundelfinger ED, Ziv NE (2002) Molecular mechanisms of CNS synaptogenesis. Trends Neurosci 25:243-251
28. Gerber SH, Garcia J, Rizo J, Sudhof TC (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
29. Gray EG (1963) Electron microscopy of presynaptic organelles of the spinal cord. J Anat 97:101-106
30. Gundelfinger ED, Kessels MM, Qualmann B (2003) Temporal and spatial coordination of exocytosis and endocytosis. Nat Rev Mol Cell Biol 4:127-139
31. Gundelfinger ED, Altrock WD, Fejtova A (2005) Active zone. In: Hirokawa N, Takahashi M (eds) Encyclopedic reference of neuroscience. Springer
32. Harlow ML, Ress D, Stoschek A, Marshall RM, McMahan UJ (2001) The architecture of active zone material at the frog's neuromuscular junction. Nature 409:479-484
33. Hibino H, Pironkova R, Onwumere O, Vologodskaia M, Hudspeth AJ, Lesage F (2002) RIM binding proteins (RBPs) couple Rab3-interacting molecules (RIMs) to voltage-gated Ca(2+) channels. Neuron 34:411-423
34. Jahn R, Lang T, Sudhof TC (2003) Membrane fusion. Cell 112:519-533
35. Junge HJ, Rhee JS, Jahn O, Varoqueaux F, Spiess J, Waxham MN, Rosenmund C, Brose N (2004) Calmodulin and Munc13 form a Ca2+ sensor/effector complex that controls short-term synaptic plasticity. Cell 118:389-401
36. Khimich D, Nouvian R, Pujol R, Tom Dieck S, Egner A, Gundelfinger ED, Moser T (2005) Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature 434:889-894
37. Kim S, Ko J, Shin H, Lee JR, Lim C, Han JH, Altrock WD, Garner CC, Gundelfinger ED, Premont RT, Kaang BK, Kim E (2003) The GIT family of proteins forms multimers and associates with the presynaptic cytomatrix protein Piccolo. J Biol Chem 278:6291-6300
38. Ko J, Na M, Kim S, Lee JR, Kim E (2003) Interaction of the ERC family of RIM-binding proteins with the liprin-alpha family of multidomain proteins. J Biol Chem 278:42377-42385
39. Koch H, Hofmann K, Brose N (2000) De.nition of Munc13-homology-domains and characterization of a novel ubiquitously expressed Munc13 isoform. Biochem J 349:247-253
40. Koushika SP, Richmond JE, Hadwiger G, Weimer RM, Jorgensen EM, Nonet ML (2001) A post-docking role for active zone protein Rim. Nat Neurosci 4:997-1005
41. Lonart G, Schoch S, Kaeser PS, Larkin CJ, Sudhof TC, Linden DJ (2003) Phosphorylation of RIM1alpha by PKA triggers presynaptic long-term potentiation at cerebellar parallel fiber synapses. Cell 115:49-60
42. Martincic I, Peralta ME, Ngsee JK (1997) Isolation and characterization of a dual prenylated Rab and VAMP2 receptor. J Biol Chem 272:26991-26998
43. Murthy VN, De Camilli P (2003) Cell biology of the presynaptic terminal. Annu Rev Neurosci 26:701-728
44. Ohtsuka T, Takao-Rikitsu E, Inoue E, Inoue M, Takeuchi M, Matsubara K, Deguchi-Tawarada M, Satoh K, Morimoto K, Nakanishi H, Takai Y (2002) 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 158:577-590
45. Ozaki N, Shibasaki T, Kashima Y, Miki T, Takahashi K, Ueno H, Sunaga Y, Yano H, Matsuura Y, Iwanaga T, Takai Y, Seino S (2000) cAMP-GEFII is a direct target of cAMP in regulated exocytosis. Nat Cell Biol 2:805-811
46. Pfenninger K, Akert K, Moor H, Sandri C (1972) The fine structure of freeze-fractured presynaptic membranes. J Neurocytol 1:129-149
47. Phillips GR, Huang JK, Wang Y, Tanaka H, Shapiro L, Zhang W, Shan WS, Arndt K, Frank M, Gordon RE, Gawinowicz MA, Zhao Y, Colman DR (2001) The presynaptic particle web: Ultrastructure, composition, dissolution, and reconstitution. Neuron 32:63-77
48. 2+-dependent neurotransmitter release. Cell 104:71-81
49. Rhee JS, Betz A, Pyott S, Reim K, Varoqueaux F, Augustin I, Hesse D, Sudhof TC, Takahashi M, Rosenmund C, Brose N (2002) Beta phorbol ester- and diacylglycerolinduced augmentation of transmitter release is mediated by Munc13s and not by PKCs. Cell 108:121-133
50. Rosenmund C, Rettig J, Brose N (2003) Molecular mechanisms of active zone function. Curr Opin Neurobiol 13:509-519
51. Rosenmund C, Sigler A, Augustin I, Reim K, Brose N, Rhee JS (2002) Differential control of vesicle priming and short-term plasticity by Munc13 isoforms. Neuron 33:411-424
52. Schaeper U, Boyd JM, Verma S, Uhlmann E, Subramanian T, Chinnadurai G (1995) Molecular cloning and characterization of a cellular phosphoprotein that interacts with a conserved C-terminal domain of adenovirus E1A involved in negative modulation of oncogenic transformation. Proc Natl Acad Sci USA 92:10467-10471
53. Scheiffele P (2003) Cell-cell signaling during synapse formation in the CNS. Annu Rev Neurosci 26:485-508
54. Schmitz F, Konigstorfer A, Sudhof TC (2000) RIBEYE, a component of synaptic ribbons: A protein's journey through evolution provides insight into synaptic ribbon function. Neuron 28:857-872
55. Schoch S, Castillo PE, Jo T, Mukherjee K, Geppert M, Wang Y, Schmitz F, Malenka RC, Sudhof TC (2002) RIM1alpha forms a protein scaffold for regulating neurotransmitter release at the active zone. Nature 415:321-326
56. Serra-Pages C, Medley QG, Tang M, Hart A, Streuli M (1998) Liprins, a family of LAR transmembrane protein-tyrosine phosphatase-interacting proteins. J Biol Chem 273:15611-15620
57. Shapira M, Zhai RG, Dresbach T, Bresler T, Torres VI, Gundelfinger ED, Ziv NE, Garner CC (2003) Unitary assembly of presynaptic active zones from Piccolo-Bassoon transport vesicles. Neuron 38:237-252
58. Shibasaki T, Sunaga Y, Fujimoto K, Kashima Y, Seino S (2003) Interaction of ATP sensor, cAMP sensor, Ca2+ sensor, and voltage-dependent calcium channel in insulin granule exocytosis. J Biol Chem 279:7956-7961
59. Simsek-Duran F, Linden DJ, Lonart G (2004) Adapter protein 14-3-3 is required for a presynaptic form of LTP in the cerebellum. Nat Neurosci 7:1296-1298
60. Sterling P, Matthews G (2005) Structure and function of ribbon synapses. Trends Neurosci 28:20-29
61. Sudhof TC (1995) The synaptic vesicle cycle: A cascade of protein-protein interactions. Nature 375:645-653
62. Sudhof TC (2000) The synaptic vesicle cycle revisited. Neuron 28:317-320
63. Sudhof TC (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27:509-547
64. Takao-Rikitsu E, Mochida S, Inoue E, Deguchi-Tawarada M, Inoue M, Ohtsuka T, Takai Y (2004) Physical and functional interaction of the active zone proteins, CAST, RIM1, and Bassoon, in neurotransmitter release. J Cell Biol 164:301-311
65. tom Dieck S, Altrock WD, Kessels MM, Qualmann B, Regus H, Brauner D, Fejtova A, Bracko O, Gundelfinger ED, Brandstatter JH (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
66. tom Dieck S, Sanmarti-Vila L, Langnaese K, Richter K, Kindler S, Soyke A, Wex H, Smalla KH, Kampf U, Franzer JT, Stumm M, Garner CC, Gundelfinger ED (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
67. Vaughn JE (1989) Fine structure of synaptogenesis in the vertebrate central nervous system. Synapse 3:255-285
68. von Gersdorff H (2001) Synaptic ribbons: Versatile signal transducers. Neuron 29:7-10
69. Wang X, Kibschull M, Laue MM, Lichte B, Petrasch-Parwez E, Kilimann MW (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
70. Wang Y, Sudhof TC (2003) Genomic definition of RIM proteins: evolutionary amplification of a family of synaptic regulatory proteins. Genomics 81:126-137
71. Wang Y, Sugita S, Sudhof TC (2000) The RIM/NIM family of neuronal C2 domain proteins. Interactions with Rab3 and a new class of Src homology 3 domain proteins. J Biol Chem 275:20033-20044
72. Wang Y, Liu X, Biederer T, Sudhof TC (2002) A family of RIM-binding proteins regulated by alternative splicing: Implications for the genesis of synaptic active zones. Proc Natl Acad Sci USA 99:14464-14469
73. Wang Y, Okamoto M, Schmitz F, Hofmann K, Sudhof TC (1997) Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion. Nature 388:593-598
74. Weigert R, Silletta MG, Spano S, Turacchio G, Cericola C, Colanzi A, Senatore S, Mancini R, Polishchuk EV, Salmona M, Facchiano F, Burger KN, Mironov A, Luini A, Corda D (1999) CtBP/BARS induces fission of Golgi membranes by acylating lysophosphatidic acid. Nature 402:429-433
75. Zhai RG, Bellen HJ (2004) The architecture of the active zone in the presynaptic nerve terminal. Physiology (Bethesda) 19:262-270
76. Zhai RG, Vardinon-Friedman H, Cases-Langhoff C, Becker B, Gundelfinger ED, Ziv NE, Garner CC (2001) Assembling the presynaptic active zone: A characterization of an active one precursor vesicle. Neuron 29:131-143
77. Zhen M, Jin Y (1999) The liprin protein SYD-2 regulates the differentiation of presynaptic termini in C. elegans. Nature 401:371-375
78. Ziv NE, Garner CC (2004) Cellular and molecular mechanisms of presynaptic assembly. Nat Rev Neurosci 5:385-399