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Molecular Organization and Assembly of the Presynaptic Active Zone of Neurotransmitter Release

  • Anna FejtovaEmail author
  • Eckart D. Gundelfinger
Chapter
Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 43)

Abstract

At chemical synapses, neurotransmitter is released at a restricted region of the presynaptic plasma membrane, called the active zone. At the active zone, a matrix of proteins is assembled, which is termed the presynaptic grid or cytomatrix at the active zone (CAZ). Components of the CAZ are thought to localize and organize the synaptic vesicle cycle, a series of membrane trafficking events underlying regulated neurotransmitter exocytosis. This review is focused on a set of specific proteins involved in the structural and functional organization of the CAZ. These include the multi-domain Rab3-effector proteins RIM1α and RIM2α; Bassoon and Piccolo, two multi-domain CAZ scaffolding proteins of enormous size; as well as members of the CAST/ERC family of CAZ-specific structural proteins. Studies on ribbon synapses of retinal photoreceptor cells have fostered understanding the molecular design of the CAZ. In addition, the analysis of the delivery pathways for Bassoon and Piccolo to presynaptic sites during development has produced new insights into assembly mechanisms of brain synapses during development. Based on these studies, the active zone transport vesicle hypothesis was formulated, which postulates that active zones, at least in part, are pre-assembled in neuronal cell bodies and transported as so-called Piccolo-Bassoon transport vesicles (PTVs) to sites of synaptogenesis. Several PTVs can fuse on demand with the presynaptic membrane to rapidly form an active zone.

Keywords

Active Zone Molecular Organization Ribbon Synapse Synaptic Ribbon Presynaptic Active Zone 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

C1 domain

conserved domain 1 of protein kinase C

C2 domain

conserved domain 2 of protein kinase C

CAST

CAZ-associated structural protein

CAZ

cytomatrix assembled at the active zone

CtBP

C-terminal binding protein (or connected to Bassoon and Piccolo)

DAG

diacylglycerol

ERC

ELKS-Rab6-interacting molecule-CAST

GIT

protein interacting with G-protein-coupled receptor kinases

PBH domain

Piccolo-Bassoon homology domain

PDZ

PSD-95-Discs large-ZO-1 domain

PSD

postsynaptic density

PTV

Piccolo-Bassoon transport vesicle

RIM

Rab3-interacting molecule

RIM-BP

RIM-binding protein

SV

synaptic vesicle

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Notes

Acknowledgments

Work on active zone function and assembly in the authors' lab is supported by the Deutsche Forschungsgemeinschaft, the European Commission (SynScaff), the Swiss National Fonds, the Fonds der Chemischen Industrie and the Max Planck Prize awarded by the Alexander von Humboldt Foundation and the Max Planck Society.

References

  1. 1.
    Ahmari SE, Buchanan J, Smith SJ (2000) Assembly of presynaptic active zones from cytoplasmic transport packets. Nat Neurosci 3:445–451 PubMedCrossRefGoogle Scholar
  2. 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 PubMedCrossRefGoogle Scholar
  3. 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 PubMedCrossRefGoogle Scholar
  4. 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 PubMedCrossRefGoogle Scholar
  5. 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 PubMedCrossRefGoogle Scholar
  6. 6.
    Brose N, Rosenmund C, Rettig J (2000) Regulation of transmitter release by Unc-13 and its homologues. Curr Opin Neurobiol 10:303–311 PubMedCrossRefGoogle Scholar
  7. 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 PubMedGoogle Scholar
  8. 8.
    Castillo PE, Schoch S, Schmitz F, Sudhof TC, Malenka RC (2002) RIM1alpha is required for presynaptic long-term potentiation. Nature 415:327–330 PubMedCrossRefGoogle Scholar
  9. 9.
    Chapman ER (2002) Synaptotagmin: a Ca(2+) sensor that triggers exocytosis? Nat Rev Mol Cell Biol 3:498–508 PubMedCrossRefGoogle Scholar
  10. 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 PubMedCrossRefGoogle Scholar
  11. 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 PubMedCrossRefGoogle Scholar
  12. 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 PubMedCrossRefGoogle Scholar
  13. 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 PubMedCrossRefGoogle Scholar
  14. 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 PubMedCrossRefGoogle Scholar
  15. 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 PubMedCrossRefGoogle Scholar
  16. 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 PubMedCrossRefGoogle Scholar
  17. 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 PubMedGoogle Scholar
  18. 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 PubMedCrossRefGoogle Scholar
  19. 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 PubMedCrossRefGoogle Scholar
  20. 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 PubMedCrossRefGoogle Scholar
  21. 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 PubMedCrossRefGoogle Scholar
  22. 22.
    Fuchs PA, Glowatzki E, Moser T (2003) The afferent synapse of cochlear hair cells. Curr Opin Neurobiol 13:452–458 PubMedCrossRefGoogle Scholar
  23. 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 PubMedCrossRefGoogle Scholar
  24. 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 PubMedGoogle Scholar
  25. 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 PubMedCrossRefGoogle Scholar
  26. 26.
    Garner CC, Kindler S, Gundelfinger ED (2000) Molecular determinants of presynaptic active zones. Curr Opin Neurobiol 10:321–327 PubMedCrossRefGoogle Scholar
  27. 27.
    Garner CC, Zhai RG, Gundelfinger ED, Ziv NE (2002) Molecular mechanisms of CNS synaptogenesis. Trends Neurosci 25:243–251 PubMedCrossRefGoogle Scholar
  28. 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 PubMedCrossRefGoogle Scholar
  29. 29.
    Gray EG (1963) Electron microscopy of presynaptic organelles of the spinal cord. J Anat 97:101–106 PubMedGoogle Scholar
  30. 30.
    Gundelfinger ED, Kessels MM, Qualmann B (2003) Temporal and spatial coordination of exocytosis and endocytosis. Nat Rev Mol Cell Biol 4:127–139 PubMedCrossRefGoogle Scholar
  31. 31.
    Gundelfinger ED, Altrock WD, Fejtova A (2005) Active zone. In: Hirokawa N, Takahashi M (eds) Encyclopedic reference of neuroscience. Springer Google Scholar
  32. 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 PubMedCrossRefGoogle Scholar
  33. 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 PubMedCrossRefGoogle Scholar
  34. 34.
    Jahn R, Lang T, Sudhof TC (2003) Membrane fusion. Cell 112:519–533 PubMedCrossRefGoogle Scholar
  35. 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 PubMedCrossRefGoogle Scholar
  36. 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 PubMedCrossRefGoogle Scholar
  37. 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 PubMedCrossRefGoogle Scholar
  38. 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 PubMedCrossRefGoogle Scholar
  39. 39.
    Koch H, Hofmann K, Brose N (2000) Definition of Munc13-homology-domains and characterization of a novel ubiquitously expressed Munc13 isoform. Biochem J 349:247–253 PubMedCrossRefGoogle Scholar
  40. 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 PubMedCrossRefGoogle Scholar
  41. 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 PubMedCrossRefGoogle Scholar
  42. 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 PubMedCrossRefGoogle Scholar
  43. 43.
    Murthy VN, De Camilli P (2003) Cell biology of the presynaptic terminal. Annu Rev Neurosci 26:701–728 PubMedCrossRefGoogle Scholar
  44. 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 PubMedCrossRefGoogle Scholar
  45. 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 PubMedCrossRefGoogle Scholar
  46. 46.
    Pfenninger K, Akert K, Moor H, Sandri C (1972) The fine structure of freeze-fractured presynaptic membranes. J Neurocytol 1:129–149 PubMedCrossRefGoogle Scholar
  47. 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 PubMedCrossRefGoogle Scholar
  48. 48.
    Reim K, Mansour M, Varoqueaux F, McMahon HT, Sudhof TC, Brose N, Rosenmund C (2001) Complexins regulate a late step in Ca2+-dependent neurotransmitter release. Cell 104:71–81 PubMedCrossRefGoogle Scholar
  49. 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 diacylglycerol-induced augmentation of transmitter release is mediated by Munc13s and not by PKCs. Cell 108:121–133 PubMedCrossRefGoogle Scholar
  50. 50.
    Rosenmund C, Rettig J, Brose N (2003) Molecular mechanisms of active zone function. Curr Opin Neurobiol 13:509–519 PubMedCrossRefGoogle Scholar
  51. 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 PubMedCrossRefGoogle Scholar
  52. 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 PubMedCrossRefGoogle Scholar
  53. 53.
    Scheiffele P (2003) Cell-cell signaling during synapse formation in the CNS. Annu Rev Neurosci 26:485–508 PubMedCrossRefGoogle Scholar
  54. 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 PubMedCrossRefGoogle Scholar
  55. 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 PubMedCrossRefGoogle Scholar
  56. 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 PubMedCrossRefGoogle Scholar
  57. 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 PubMedCrossRefGoogle Scholar
  58. 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 PubMedCrossRefGoogle Scholar
  59. 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 PubMedCrossRefGoogle Scholar
  60. 60.
    Sterling P, Matthews G (2005) Structure and function of ribbon synapses. Trends Neurosci 28:20–29 PubMedCrossRefGoogle Scholar
  61. 61.
    Sudhof TC (1995) The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375:645–653 PubMedCrossRefGoogle Scholar
  62. 62.
    Sudhof TC (2000) The synaptic vesicle cycle revisited. Neuron 28:317–320 PubMedCrossRefGoogle Scholar
  63. 63.
    Sudhof TC (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27:509–547 PubMedCrossRefGoogle Scholar
  64. 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 PubMedCrossRefGoogle Scholar
  65. 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 CrossRefGoogle Scholar
  66. 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 CrossRefGoogle Scholar
  67. 67.
    Vaughn JE (1989) Fine structure of synaptogenesis in the vertebrate central nervous system. Synapse 3:255–285 PubMedCrossRefGoogle Scholar
  68. 68.
    von Gersdorff H (2001) Synaptic ribbons: versatile signal transducers. Neuron 29:7–10 CrossRefGoogle Scholar
  69. 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 PubMedCrossRefGoogle Scholar
  70. 70.
    Wang Y, Sudhof TC (2003) Genomic definition of RIM proteins: evolutionary amplification of a family of synaptic regulatory proteins. Genomics 81:126–137 PubMedCrossRefGoogle Scholar
  71. 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 PubMedCrossRefGoogle Scholar
  72. 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 PubMedCrossRefGoogle Scholar
  73. 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 PubMedCrossRefGoogle Scholar
  74. 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 PubMedCrossRefGoogle Scholar
  75. 75.
    Zhai RG, Bellen HJ (2004) The architecture of the active zone in the presynaptic nerve terminal. Physiology (Bethesda) 19:262–270 Google Scholar
  76. 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 PubMedCrossRefGoogle Scholar
  77. 77.
    Zhen M, Jin Y (1999) The liprin protein SYD-2 regulates the differentiation of presynaptic termini in C. elegans. Nature 401:371–375 PubMedGoogle Scholar
  78. 78.
    Ziv NE, Garner CC (2004) Cellular and molecular mechanisms of presynaptic assembly. Nat Rev Neurosci 5:385–399 PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2006

Authors and Affiliations

  1. 1.Leibniz Institute for NeurobiologyDepartment of Neurochemistry and Molecular BiologyMagdeburgGermany

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