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Synaptic Vesicle Proteins: Targets and Routes for Botulinum Neurotoxins

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Botulinum Neurotoxins

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 364))

Abstract

Synaptic vesicles (SV) are key organelles of neuronal communication. SV are responsible for the storage of neurotransmitters, which are released by Ca2+-dependent exocytosis. After release and interaction with postsynaptic receptors, transmitters rapidly diffuse out of the synaptic cleft and are sequestered by plasma membrane transporters (in some cases following enzymatic conversion). SVs undergo endocytosis and are refilled by specific vesicular transmitter transporters different in the various neuronal subtypes. Besides these differences, SVs in general are equipped with a remarkable common set of proteins. Botulinum neurotoxins (BoNTs) inhibit neurotransmitter release from almost all types of neurons by cleaving proteins required for membrane fusion localized either to SVs (synaptobrevin) or to the plasma membrane (SNAP-25 and syntaxin) depending on the BoNT serotype. To enter the neuronal cytoplasm, BoNTs specifically interact with the luminal domain of SV proteins (synaptotagmin or SV2, depending on serotype) transiently exposed during exocytotic membrane fusion and occurring in almost every neuron. Thus, the highly specific interaction with luminal domains of SV proteins commonly expressed on all SV types is one reason why BoNTs exhibit such a high neuronal specificity but attack almost every neuron type.

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Abbreviations

BoNTs:

Botulinum neurotoxin

ClC3:

Chloride exchanger 3

Habc:

N-terminal a-helical domain of syntaxin

HC:

Heavy chain

LC:

Light chain

SNAP:

Soluble N-ethylmaleimide-sensitive factor attachment protein

SNARE:

SNAP receptor) complex

SNAP-25:

Synaptosomal-associated protein of 25 kDa

SV:

Synaptic vesicle

SV2:

Synaptic vesicle glycoprotein 2

Syt:

Synaptotagmin

TI-VAMP:

Tetanus toxin insensitive VMAP

VAMP:

Vesicle-associated membrane protein

V-ATPase:

Vacuolar proton ATPase

VGLUT:

Vesicular glutamate transporter

VGAT:

Vesicular GABA transporter

VMAT:

Vesicular monoamine transporter

References

  • Aguado F, Majo G, Ruiz-Montasell B, Llorens J, Marsal J, Blasi J (1999) Syntaxin 1A and 1B display distinct distribution patterns in the rat peripheral nervous system. Neuroscience 88:437–446

    Article  PubMed  CAS  Google Scholar 

  • Ahnert-Hilger G, Jahn R (2011) CLC-3 spices up GABAergic synaptic vesicles. Nat Neurosci 14:405–407

    Article  PubMed  CAS  Google Scholar 

  • Antonin W, Holroyd C, Tikkanen R, Honing S, Jahn R (2000) The R-SNARE endobrevin/VAMP-8 mediates homotypic fusion of early endosomes and late endosomes. Mol Biol Cell 11:3289–3298

    PubMed  CAS  Google Scholar 

  • Bajjalieh SM, Peterson K, Shinghal R, Scheller RH (1992) SV2, a brain synaptic vesicle protein homologous to bacterial transporters. Science 257:1271–1273

    Article  PubMed  CAS  Google Scholar 

  • Bajjalieh SM, Peterson K, Linial M, Scheller RH (1993) Brain contains two forms of synaptic vesicle protein 2. Proc Natl Acad Sci USA 90:2150–2154

    Article  PubMed  CAS  Google Scholar 

  • Bajjalieh SM, Frantz GD, Weimann JM, McConnell SK, Scheller RH (1994) Differential expression of synaptic vesicle protein 2 (SV2) isoforms. J Neurosci 14:5223–5235

    PubMed  CAS  Google Scholar 

  • Bark C, Bellinger FP, Kaushal A, Mathews JR, Partridge LD, Wilson MC (2004) Developmentally regulated switch in alternatively spliced SNAP-25 isoforms alters facilitation of synaptic transmission. J Neurosci 24:8796–8805

    Article  PubMed  CAS  Google Scholar 

  • Becher A, Drenckhahn A, Pahner I, Margittai M, Jahn R, Ahnert-Hilger G (1999) The synaptophysin-synaptobrevin complex: a hallmark of synaptic vesicle maturation. J Neurosci 19:1922–1931

    PubMed  CAS  Google Scholar 

  • Bennett MK, Garcia-Arraras JE, Elferink LA, Peterson K, Fleming AM, Hazuka CD, Scheller RH (1993) The syntaxin family of vesicular transport receptors. Cell 74:863–873

    Article  PubMed  CAS  Google Scholar 

  • Berton F, Iborra C, Boudier JA, Seagar MJ, Marqueze B (1997) Developmental regulation of synaptotagmin I, II, III, and IV mRNAs in the rat CNS. J Neurosci 17:1206–1216

    PubMed  CAS  Google Scholar 

  • Bragina L, Candiracci C, Barbaresi P, Giovedi S, Benfenati F, Conti F (2007) Heterogeneity of glutamatergic and GABAergic release machinery in cerebral cortex. Neuroscience 146:1829–1840

    Article  PubMed  CAS  Google Scholar 

  • Chang WP, Sudhof TC (2009) SV2 renders primed synaptic vesicles competent for Ca2+-induced exocytosis. J Neurosci 29:883–897

    Article  PubMed  CAS  Google Scholar 

  • Chapman ER (2008) How does synaptotagmin trigger neurotransmitter release? Annu Rev Biochem 77:615–641

    Article  PubMed  CAS  Google Scholar 

  • Christie MP, Whitten AE, King GJ (2012) Low-resolution solution structures of Munc18: syntaxin protein complexes indicate an open binding mode driven by the Syntaxin N-peptide. Proc Natl Acad Sci USA 109:9816–9821

    Article  PubMed  CAS  Google Scholar 

  • Coco S, Raposo G, Martinez S (1999) Subcellular localization of tetanus neurotoxin-insensitive vesicle-associated membrane protein (VAMP)/VAMP7 in neuronal cells: evidence for a novel membrane compartment. J Neurosci 19:9803–9812

    PubMed  CAS  Google Scholar 

  • Danglot L, Zylbersztejn K, Petkovic M (2012) Absence of TI-VAMP/Vamp7 leads to increased anxiety in mice. J Neurosci 32:1962–1968

    Article  PubMed  CAS  Google Scholar 

  • Dardou D, Dassesse D, Cuvelier L, Deprez T, De Ryck M, Schiffmann SN (2011) Distribution of SV2C mRNA and protein expression in the mouse brain with a particular emphasis on the basal ganglia system. Brain Res 1367:130–145

    Article  PubMed  CAS  Google Scholar 

  • de Wit H, Walter AM, Milosevic I, Gulyas-Kovacs A, Riedel D, Sorensen JB, Verhage M (2009) Synaptotagmin-1 docks secretory vesicles to syntaxin-1/SNAP-25 acceptor complexes. Cell 138:935–946

    Article  PubMed  Google Scholar 

  • Deak F, Schoch S, Liu X, Sudhof TC, Kavalali ET (2004) Synaptobrevin is essential for fast synaptic-vesicle endocytosis. Nat Cell Biol 6:1102–1108

    Article  PubMed  CAS  Google Scholar 

  • Delgado-Martinez I, Nehring RB, Sorensen JB (2007) Differential abilities of SNAP-25 homologs to support neuronal function. J Neurosci 27:9380–9391

    Article  PubMed  CAS  Google Scholar 

  • Dong M, Yeh F, Tepp WH, Dean C, Johnson EA, Janz R, Chapman ER (2006) SV2 is the protein receptor for botulinum neurotoxin A. Science 312:592–596

    Article  PubMed  CAS  Google Scholar 

  • Ferguson GD, Anagnostaras SG, Silva AJ, Herschman HR (2000) Deficits in memory and motor performance in synaptotagmin IV mutant mice. Proc Natl Acad Sci USA 97:5598–5603

    Article  PubMed  CAS  Google Scholar 

  • Foran PG, Mohammed N, Lisk GO, Nagwaney S, Lawrence GW, Johnson E, Smith L, Aoki KR, Dolly JO (2003) Evaluation of the therapeutic usefulness of botulinum neurotoxin B, C1, E, and F compared with the long lasting type A. Basis for distinct durations of inhibition of exocytosis in central neurons. J Biol Chem 278:1363–1371

    Article  PubMed  CAS  Google Scholar 

  • Galli T, Zahraoui A, Vaidyanathan VV, Raposo G, Tian JM, Karin M, Niemann H, Louvard D (1998) A novel tetanus neurotoxin-insensitive vesicle-associated membrane protein in SNARE complexes of the apical plasma membrane of epithelial cells. Mol Biol Cell 9:1437–1448

    PubMed  CAS  Google Scholar 

  • Geppert M, Archer BT 3rd, Sudhof TC (1991) Synaptotagmin II a novel differentially distributed form of synaptotagmin. J Biol Chem 266:13548–13552

    PubMed  CAS  Google Scholar 

  • Gerber SH, Rah JC, Min SW (2008) Conformational switch of syntaxin-1 controls synaptic vesicle fusion. Science 321:1507–1510

    Article  PubMed  CAS  Google Scholar 

  • Gibbins IL, Jobling P, Teo EH, Matthew SE, Morris JL (2003) Heterogeneous expression of SNAP-25 and synaptic vesicle proteins by central and peripheral inputs to sympathetic neurons. J Comp Neurol 459:25–43

    Article  PubMed  CAS  Google Scholar 

  • Gordon SL, Leube RE, Cousin MA (2011) Synaptophysin is required for synaptobrevin retrieval during synaptic vesicle endocytosis. J Neurosci 31:14032–14036

    Article  PubMed  CAS  Google Scholar 

  • Gras C, Amilhon B, Lepicard EM (2008) The vesicular glutamate transporter VGLUT3 synergizes striatal acetylcholine tone. Nat Neurosci 11:292–300

    Article  PubMed  CAS  Google Scholar 

  • Gronborg M, Pavlos NJ, Brunk I, Chua JJ, Münster-Wandowski A, Riedel D, Ahnert-Hilger G, Urlaub H, Jahn R (2010) Quantitative comparison of glutamatergic and GABAergic synaptic vesicles unveils selectivity for few proteins including MAL2, a novel synaptic vesicle protein. J Neurosci 30:2–12

    Article  PubMed  CAS  Google Scholar 

  • Grumelli C, Corradini I, Matteoli M, Verderio C (2010) Intrinsic calcium dynamics control botulinum toxin a susceptibility in distinct neuronal populations. Cell Calcium 47:419–424

    Article  PubMed  CAS  Google Scholar 

  • Gustavsson N, Lao Y, Maximov A (2008) Impaired insulin secretion and glucose intolerance in synaptotagmin-7 null mutant mice. Proc Natl Acad Sci USA 105:3992–3997

    Article  PubMed  CAS  Google Scholar 

  • Han GA, Malintan NT, Collins BM, Meunier FA, Sugita S (2010) Munc18-1 as a key regulator of neurosecretion. J Neurochem 115:1–10

    Article  PubMed  CAS  Google Scholar 

  • Hinz B, Becher A, Mitter D, Schulze K, Heinemann U, Draguhn A, Ahnert-Hilger G (2001) Activity-dependent changes of the presynaptic synaptophysin-synaptobrevin complex in adult rat brain. Eur J Cell Biol 80:615–619

    Article  PubMed  CAS  Google Scholar 

  • Hnasko TS, Chuhma N, Zhang H, Goh GY, Sulzer D, Palmiter RD, Rayport S, Edwards RH (2010) Vesicular glutamate transport promotes dopamine storage and glutamate corelease in vivo. Neuron 65:643–656

    Article  PubMed  CAS  Google Scholar 

  • Holt M, Varoqueaux F, Wiederhold K, Takamori S, Urlaub H, Fasshauer D, Jahn R (2006) Identification of SNAP-47, a novel Qbc-SNARE with ubiquitous expression. J Biol Chem 281:17076–17083

    Article  PubMed  CAS  Google Scholar 

  • Humeau Y, Doussau F, Grant NJ, Poulain B (2000) How botulinum and tetanus neurotoxins block neurotransmitter release. Biochimie 82:427–446

    Article  PubMed  CAS  Google Scholar 

  • Ibata K, Hashikawa T, Tsuboi T, Terakawa S, Liang F, Mizutani A, Fukuda M, Mikoshiba K (2002) Non-polarized distribution of synaptotagmin IV in neurons: evidence that synaptotagmin IV is not a synaptic vesicle protein. Neurosci Res 43:401–406

    Article  PubMed  CAS  Google Scholar 

  • Janz R, Sudhof TC (1999) SV2C is a synaptic vesicle protein with an unusually restricted localization: anatomy of a synaptic vesicle protein family. Neuroscience 94:1279–1290

    Article  PubMed  CAS  Google Scholar 

  • Karvar S, Zhu L, Crothers J Jr, Wong W, Turkoz M, Forte JG (2005) Cellular localization and stimulation-associated distribution dynamics of syntaxin-1 and syntaxin-3 in gastric parietal cells. Traffic 6:654–666

    Article  PubMed  CAS  Google Scholar 

  • Kwon SE, Chapman ER (2011) Synaptophysin regulates the kinetics of synaptic vesicle endocytosis in central neurons. Neuron 70:847–854

    Article  PubMed  CAS  Google Scholar 

  • Li JY, Jahn R, Dahlstrom A (1994) Synaptotagmin I is present mainly in autonomic and sensory neurons of the rat peripheral nervous system. Neuroscience 63:837–850

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Sugiura Y, Lin W (2011) The role of synaptobrevin1/VAMP1 in Ca2+-triggered neurotransmitter release at the mouse neuromuscular junction. J Physiol 589:1603–1618

    Article  PubMed  CAS  Google Scholar 

  • Lynch BA, Lambeng N, Nocka K, Kensel-Hammes P, Bajjalieh SM, Matagne A, Fuks B (2004) The synaptic vesicle protein SV2A is the binding site for the antiepileptic drug levetiracetam. Proc Natl Acad Sci USA 101:9861–9866

    Article  PubMed  CAS  Google Scholar 

  • Martens H, Weston MC, Boulland JL (2008) Unique luminal localization of VGAT-C terminus allows for selective labeling of active cortical GABAergic synapses. J Neurosci 28:13125–13131

    Article  PubMed  CAS  Google Scholar 

  • Matteoli M, Pozzi D, Grumelli C, Condliffe SB, Frassoni C, Harkany T, Verderio C (2009) The synaptic split of SNAP-25: different roles in glutamatergic and GABAergic neurons? Neuroscience 158:223–230

    Article  PubMed  CAS  Google Scholar 

  • Morgans CW, Kensel-Hammes P, Hurley JB, Burton K, Idzerda R, McKnight GS, Bajjalieh SM (2009) Loss of the Synaptic Vesicle Protein SV2B results in reduced neurotransmission and altered synaptic vesicle protein expression in the retina. PLoS ONE 4:e5230

    Article  PubMed  Google Scholar 

  • Pan PY, Cai Q, Lin L, Lu PH, Duan S, Sheng ZH (2005) SNAP-29-mediated modulation of synaptic transmission in cultured hippocampal neurons. J Biol Chem 280:25769–25779

    Article  PubMed  CAS  Google Scholar 

  • Pang ZP, Melicoff E, Padgett D, Liu Y, Teich AF, Dickey BF, Lin W, Adachi R, Sudhof TC (2006) Synaptotagmin-2 is essential for survival and contributes to Ca2+ triggering of neurotransmitter release in central and neuromuscular synapses. J Neurosci 26:13493–13504

    Article  PubMed  CAS  Google Scholar 

  • Perin MS, Brose N, Jahn R, Sudhof TC (1991) Domain structure of synaptotagmin (p65). J Biol Chem 266:623–629

    PubMed  CAS  Google Scholar 

  • Raingo J, Khvotchev M, Liu P (2012) VAMP4 directs synaptic vesicles to a pool that selectively maintains asynchronous neurotransmission. Nat Neurosci 15:738–745

    Article  PubMed  CAS  Google Scholar 

  • Raptis A, Torrejon-Escribano B, de Gomez Aranda I, Blasi J (2005) Distribution of synaptobrevin/VAMP 1 and 2 in rat brain. J Chem Neuroanat 30:201–211

    Article  PubMed  CAS  Google Scholar 

  • Ravichandran V, Chawla A, Roche PA (1996) Identification of a novel syntaxin- and synaptobrevin/VAMP-binding protein, SNAP-23, expressed in non-neuronal tissues. J Biol Chem 271:13300–13303

    Article  PubMed  CAS  Google Scholar 

  • Reisinger C, Yelamanchili SV, Hinz B, Mitter D, Becher A, Bigalke H, Ahnert-Hilger G (2004) The synaptophysin/synaptobrevin complex dissociates independently of neuroexocytosis. J Neurochem 90:1–8

    Article  PubMed  CAS  Google Scholar 

  • Rhee JS, Li LY, Shin OH, Rah JC, Rizo J, Sudhof TC, Rosenmund C (2005) Augmenting neurotransmitter release by enhancing the apparent Ca2+ affinity of synaptotagmin 1. Proc Natl Acad Sci USA 102:18664–18669

    Article  PubMed  CAS  Google Scholar 

  • Riazanski V, Deriy LV, Shevchenko PD, Le B, Gomez EA, Nelson DJ (2011) Presynaptic CLC-3 determines quantal size of inhibitory transmission in the hippocampus. Nat Neurosci 14:487–494

    Article  PubMed  CAS  Google Scholar 

  • Rose AJ, Jeppesen J, Kiens B, Richter EA (2009) Effects of contraction on localization of GLUT4 and v-SNARE isoforms in rat skeletal muscle. Am J Physiol Regul Integr Comp Physiol 297:R1228–R1237

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Montasell B, Aguado F, Majo G, Chapman ER, Canals JM, Marsal J, Blasi J (1996) Differential distribution of syntaxin isoforms 1A and 1B in the rat central nervous system. Eur J Neurosci 8:2544–2552

    Article  PubMed  CAS  Google Scholar 

  • Rummel A, Hafner K, Mahrhold S (2009) Botulinum neurotoxins C, E and F bind gangliosides via a conserved binding site prior to stimulation-dependent uptake with botulinum neurotoxin F utilising the three isoforms of SV2 as second receptor. J Neurochem 110:1942–1954

    Article  PubMed  CAS  Google Scholar 

  • Sakaba T, Stein A, Jahn R, Neher E (2005) Distinct kinetic changes in neurotransmitter release after SNARE protein cleavage. Science 309:491–494

    Article  PubMed  CAS  Google Scholar 

  • Schiavo G, Matteoli M, Montecucco C (2000) Neurotoxins affecting neuroexocytosis. Physiol Rev 80:717–766

    PubMed  CAS  Google Scholar 

  • Schmitt U, Tanimoto N, Seeliger M, Schaeffel F, Leube RE (2009) Detection of behavioral alterations and learning deficits in mice lacking synaptophysin. Neuroscience 162:234–243

    Article  PubMed  CAS  Google Scholar 

  • Schoch S, Deak F, Konigstorfer A, Mozhayeva M, Sara Y, Sudhof TC, Kavalali ET (2001) SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science 294:1117–1122

    Article  PubMed  CAS  Google Scholar 

  • Seal RP, Akil O, Yi E (2008) Sensorineural deafness and seizures in mice lacking vesicular glutamate transporter 3. Neuron 57:263–275

    Article  PubMed  CAS  Google Scholar 

  • Spiwoks-Becker I, Vollrath L, Seeliger MW, Jaissle G, Eshkind LG, Leube RE (2001) Synaptic vesicle alterations in rod photoreceptors of synaptophysin-deficient mice. Neuroscience 107:127–142

    Article  PubMed  CAS  Google Scholar 

  • Steegmaier M, Yang B, Yoo JS, Huang B, Shen M, Yu S, Luo Y, Scheller RH (1998) Three novel proteins of the syntaxin/SNAP-25 family. J Biol Chem 273:34171–34179

    Article  PubMed  CAS  Google Scholar 

  • Stobrawa SM, Breiderhoff T, Takamori S (2001) Disruption of ClC-3, a chloride channel expressed on synaptic vesicles, leads to a loss of the hippocampus. Neuron 29:185–196

    Article  PubMed  CAS  Google Scholar 

  • Südhof TC (2012) The presynaptic active zone. Neuron 75:11–25

    Article  PubMed  CAS  Google Scholar 

  • Sutton RB, Fasshauer D, Jahn R, Brunger AT (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 a resolution. Nature 395:347–353

    Article  PubMed  CAS  Google Scholar 

  • Takamori S, Holt M, Stenius K (2006) Molecular anatomy of a trafficking organelle. Cell 127:831–846

    Article  PubMed  CAS  Google Scholar 

  • van den Bogaart G, Thutupalli S, Risselada JH (2011) Synaptotagmin-1 may be a distance regulator acting upstream of SNARE nucleation. Nat Struct Mol Biol 18:805–812

    Article  PubMed  Google Scholar 

  • Vennekate W, Schroder S, Lin CC, van den Bogaart G, Grunwald M, Jahn R, Walla PJ (2012) Cis- and trans-membrane interactions of synaptotagmin-1. Proc Natl Acad Sci USA 109:11037–11042

    Article  PubMed  CAS  Google Scholar 

  • Verderio C, Rossetto O, Grumelli C, Frassoni C, Montecucco C, Matteoli M (2006) Entering neurons: botulinum toxins and synaptic vesicle recycling. EMBO Rep 7:995–999

    Article  PubMed  CAS  Google Scholar 

  • Verderio C, Grumelli C, Raiteri L (2007) Traffic of botulinum toxins A and E in excitatory and inhibitory neurons. Traffic 8:142–153

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Wang L, Iordanov H, Swietlicki EA, Zheng Q, Jiang S, Tang Y, Levin MS, Rubin DC (2006) Epimorphin(-/-) mice have increased intestinal growth, decreased susceptibility to dextran sodium sulfate colitis, and impaired spermatogenesis. J Clin Invest 116:1535–1546

    Article  PubMed  CAS  Google Scholar 

  • Washbourne P, Thompson PM, Carta M (2002) Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat Neurosci 5:19–26

    PubMed  CAS  Google Scholar 

  • Watson RT, Pessin JE (2001) Transmembrane domain length determines intracellular membrane compartment localization of syntaxins 3, 4, and 5. Am J Physiol Cell Physiol 281:C215–C223

    PubMed  CAS  Google Scholar 

  • Xu J, Mashimo T, Sudhof TC (2007) Synaptotagmin-1, -2, and -9: Ca2+ sensors for fast release that specify distinct presynaptic properties in subsets of neurons. Neuron 54:567–581

    Article  PubMed  CAS  Google Scholar 

  • Xue M, Craig TK, Shin OH, Li L, Brautigam CA, Tomchick DR, Sudhof TC, Rosenmund C, Rizo J (2010) Structural and mutational analysis of functional differentiation between synaptotagmins-1 and -7. PLoS One 5

    Google Scholar 

  • Yang C, Mora S, Ryder JW, Coker KJ, Hansen P, Allen LA, Pessin JE (2001) VAMP3 null mice display normal constitutive, insulin- and exercise-regulated vesicle trafficking. Mol Cell Biol 21:1573–1580

    Article  PubMed  CAS  Google Scholar 

  • Yao J, Nowack A, Kensel-Hammes P, Gardner RG, Bajjalieh SM (2010) Cotrafficking of SV2 and synaptotagmin at the synapse. J Neurosci 30:5569–5578

    Article  PubMed  CAS  Google Scholar 

  • Yelamanchili SV, Reisinger C, Becher A, Sikorra S, Bigalke H, Binz T, Ahnert-Hilger G (2005) The C-terminal transmembrane region of synaptobrevin binds synaptophysin from adult synaptic vesicles. Eur J Cell Biol 84:467–475

    Article  PubMed  CAS  Google Scholar 

  • Zander JF, Munster-Wandowski A, Brunk I, Pahner I, Gomez-Lira G, Heinemann U, Gutierrez R, Laube G, Ahnert-Hilger G (2010) Synaptic and vesicular coexistence of VGLUT and VGAT in selected excitatory and inhibitory synapses. J Neurosci 30:7634–7645

    Article  PubMed  CAS  Google Scholar 

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Ahnert-Hilger, G., Münster-Wandowski, A., Höltje, M. (2012). Synaptic Vesicle Proteins: Targets and Routes for Botulinum Neurotoxins. In: Rummel, A., Binz, T. (eds) Botulinum Neurotoxins. Current Topics in Microbiology and Immunology, vol 364. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-33570-9_8

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