Isolation of Synaptic Vesicles from Mammalian Brain.

Brain Cellular compartment Centrifugation Neurotransmission Organelles Size exclusion chromatography Subcellular fractionation Synaptic vesicles Synaptosome Vesicles

Journal

Methods in molecular biology (Clifton, N.J.)
ISSN: 1940-6029
Titre abrégé: Methods Mol Biol
Pays: United States
ID NLM: 9214969

Informations de publication

Date de publication:
2022
Historique:
entrez: 31 1 2022
pubmed: 1 2 2022
medline: 1 4 2022
Statut: ppublish

Résumé

Synaptic vesicles (SVs) store neurotransmitters and undergo a fine-tuned regulatory and dynamic cycle of exo- and endocytosis, which is essential for neurotransmission at chemical synapses. The development of protocols for isolating SVs from biological extracts was a fundamental accomplishment since it allowed for characterizing the molecular properties of SVs using biochemical methods. In this chapter, we describe a modified procedure for isolating SVs from a few g of rodent brain and that can be completed within ~12 h. The protocol involves the preparation of isolated nerve terminals from which SVs are released by osmotic shock and then enriched via various centrifugation steps, followed by size exclusion chromatography as final purification step. The final vesicle fraction is 22-fold enriched in SVs over the starting material, and the final yield of SVs obtained using this protocol is approximately 20 μg of protein per gram of mouse brain. The degree of contamination by other organelles and particles monitored by morphology and immunolabeling compares well with that of the classical protocols.

Identifiants

pubmed: 35099797
doi: 10.1007/978-1-0716-1916-2_11
doi:

Substances chimiques

Neurotransmitter Agents 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

131-145

Informations de copyright

© 2022. The Author(s), under exclusive license to Springer Science+Business Media, LLC, part of Springer Nature.

Références

Rizo J, Xu J (2015) The synaptic vesicle release machinery. Annu Rev Biophys 44:339–367. https://doi.org/10.1146/annurev-biophys-060414-034057
doi: 10.1146/annurev-biophys-060414-034057 pubmed: 26098518
Jahn R, Fasshauer D (2012) Molecular machines governing exocytosis of synaptic vesicles. Nature 490(7419):201–207. https://doi.org/10.1038/nature11320
doi: 10.1038/nature11320 pubmed: 23060190 pmcid: 4461657
Rizzoli SO (2014) Synaptic vesicle recycling: steps and principles. EMBO J 33(8):788–822. https://doi.org/10.1002/embj.201386357
doi: 10.1002/embj.201386357 pubmed: 24596248 pmcid: 4194108
Sudhof TC (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27:509–547. https://doi.org/10.1146/annurev.neuro.26.041002.131412
doi: 10.1146/annurev.neuro.26.041002.131412 pubmed: 15217342
Takamori S, Holt M, Stenius K et al (2006) Molecular anatomy of a trafficking organelle. Cell 127(4):831–846. https://doi.org/10.1016/j.cell.2006.10.030
doi: 10.1016/j.cell.2006.10.030 pubmed: 17110340
Hell JW, Maycox PR, Stadler H et al (1988) Uptake of GABA by rat brain synaptic vesicles isolated by a new procedure. EMBO J 7(10):3023–3029
doi: 10.1002/j.1460-2075.1988.tb03166.x
Wolosker H, de Souza DO, de Meis L (1996) Regulation of glutamate transport into synaptic vesicles by chloride and proton gradient. J Biol Chem 271(20):11726–11731. https://doi.org/10.1074/jbc.271.20.11726
doi: 10.1074/jbc.271.20.11726 pubmed: 8662610
Farsi Z, Preobraschenski J, van den Bogaart G et al (2016) Single-vesicle imaging reveals different transport mechanisms between glutamatergic and GABAergic vesicles. Science 351(6276):981–984. https://doi.org/10.1126/science.aad8142
doi: 10.1126/science.aad8142 pubmed: 26912364
Preobraschenski J, Zander JF, Suzuki T et al (2014) Vesicular glutamate transporters use flexible anion and cation binding sites for efficient accumulation of neurotransmitter. Neuron 84(6):1287–1301. https://doi.org/10.1016/j.neuron.2014.11.008
doi: 10.1016/j.neuron.2014.11.008 pubmed: 25433636
Kiessling V, Ahmed S, Domanska MK et al (2013) Rapid fusion of synaptic vesicles with reconstituted target SNARE membranes. Biophys J 104(9):1950–1958. https://doi.org/10.1016/j.bpj.2013.03.038
doi: 10.1016/j.bpj.2013.03.038 pubmed: 23663838 pmcid: 3647153
Park Y, Hernandez JM, van den Bogaart G et al (2012) Controlling synaptotagmin activity by electrostatic screening. Nat Struct Mol Biol 19(10):991–997. https://doi.org/10.1038/nsmb.2375
doi: 10.1038/nsmb.2375 pubmed: 22940675 pmcid: 3465474
Holt M, Riedel D, Stein A et al (2008) Synaptic vesicles are constitutively active fusion machines that function independently of Ca
doi: 10.1016/j.cub.2008.04.069 pubmed: 18485705 pmcid: 2481520
Boyken J, Gronborg M, Riedel D et al (2013) Molecular profiling of synaptic vesicle docking sites reveals novel proteins but few differences between glutamatergic and GABAergic synapses. Neuron 78(2):285–297. https://doi.org/10.1016/j.neuron.2013.02.027
doi: 10.1016/j.neuron.2013.02.027 pubmed: 23622064
Gronborg M, Pavlos NJ, Brunk I et al (2010) Quantitative comparison of glutamatergic and GABAergic synaptic vesicles unveils selectivity for few proteins including MAL2, a novel synaptic vesicle protein. J Neurosci 30(1):2–12. https://doi.org/10.1523/JNEUROSCI.4074-09.2010
doi: 10.1523/JNEUROSCI.4074-09.2010 pubmed: 20053882 pmcid: 6632534
Hebb CO, Whittaker VP (1958) Intracellular distributions of acetylcholine and choline acetylase. J Physiol 142(1):187–196. https://doi.org/10.1113/jphysiol.1958.sp006008
doi: 10.1113/jphysiol.1958.sp006008 pubmed: 13564428 pmcid: 1356703
Michaelson IA, Whittaker VP, Laverty R et al (1963) Localization of acetylcholine, 5-Hydroxytryptamine and noradrenaline within subcellular particles derived from Guinea pig subcortical brain tissue. Biochem Pharmacol 12:1450–1453. https://doi.org/10.1016/0006-2952(63)90221-1
doi: 10.1016/0006-2952(63)90221-1 pubmed: 14096438
Whittaker VP, Michaelson IA, Kirkland RJ (1963) The separation of synaptic vesicles from disrupted nervending particles. Biochem Pharmacol 12:300–302. https://doi.org/10.1016/0006-2952(63)90156-4
doi: 10.1016/0006-2952(63)90156-4 pubmed: 14000416
De Robertis E, Rodriguez De Lores Arnaiz G, Pellegrino De Iraldi A (1962) Isolation of synaptic vesicles from nerve endings of the rat brain. Nature 194:794–795. https://doi.org/10.1038/194794a0
doi: 10.1038/194794a0
De Robertis E, Rodriguez De Lores Arnaiz G, Salganicoff L et al (1963) Isolation of synaptic vesicles and structural organization of the acetycholine system within brain nerve endings. J Neurochem 10:225–235. https://doi.org/10.1111/j.1471-4159.1963.tb05038.x
doi: 10.1111/j.1471-4159.1963.tb05038.x
Gray EG, Whittaker VP (1962) The isolation of nerve endings from brain: an electron-microscopic study of cell fragments derived by homogenization and centrifugation. J Anat 96:79–88
pubmed: 13901297 pmcid: 1244174
Huttner WB, Schiebler W, Greengard P et al (1983) Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J Cell Biol 96(5):1374–1388. https://doi.org/10.1083/jcb.96.5.1374
doi: 10.1083/jcb.96.5.1374 pubmed: 6404912
Nagy A, Baker RR, Morris SJ et al (1976) The preparation and characterization of synaptic vesicles of high purity. Brain Res 109(2):285–309. https://doi.org/10.1016/0006-8993(76)90531-x
doi: 10.1016/0006-8993(76)90531-x pubmed: 132227
Jahn R, Schiebler W, Ouimet C et al (1985) A 38,000-Dalton membrane protein (p38) present in synaptic vesicles. Proc Natl Acad Sci U S A 82(12):4137–4141. https://doi.org/10.1073/pnas.82.12.4137
doi: 10.1073/pnas.82.12.4137 pubmed: 3923488 pmcid: 397950
Jahn R, Sudhof TC (1993) Synaptic vesicle traffic: rush hour in the nerve terminal. J Neurochem 61(1):12–21. https://doi.org/10.1111/j.1471-4159.1993.tb03533.x
doi: 10.1111/j.1471-4159.1993.tb03533.x pubmed: 8515256
Ahmed S, Holt M, Riedel D et al (2013) Small-scale isolation of synaptic vesicles from mammalian brain. Nat Protoc 8(5):998–1009. https://doi.org/10.1038/nprot.2013.053
doi: 10.1038/nprot.2013.053 pubmed: 23619891
Maycox PR, Deckwerth T, Hell JW et al (1988) Glutamate uptake by brain synaptic vesicles. Energy dependence of transport and functional reconstitution in proteoliposomes. J Biol Chem 263(30):15423–15428
doi: 10.1016/S0021-9258(19)37605-7
Hell J, Jahn R (2006) Preparation of synaptic vesicles from mammalian brain. In: Cell biology, vol 2. Elsevier Inc., Amsterdam, pp 85–90. https://doi.org/10.1016/b978-012164730-8/50084-8
doi: 10.1016/b978-012164730-8/50084-8
Jahn R, Schiebler W, Greengard P (1984) A quantitative dot-immunobinding assay for proteins using nitrocellulose membrane filters. Proc Natl Acad Sci U S A 81(6):1684–1687. https://doi.org/10.1073/pnas.81.6.1684
doi: 10.1073/pnas.81.6.1684 pubmed: 6424121 pmcid: 344982
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680–685. https://doi.org/10.1038/227680a0
doi: 10.1038/227680a0 pubmed: 5432063 pmcid: 5432063

Auteurs

Marcelo Ganzella (M)

Laboratory of Neurobiology, Max-Planck-Institute for Biophysical Chemistry, Göttingen, Germany. marcelo.ganzella@mpibpc.mpg.de.

Momchil Ninov (M)

Laboratory of Neurobiology, Max-Planck-Institute for Biophysical Chemistry, Göttingen, Germany.
Bioanalytical Mass Spectrometry, Max-Planck-Institute for Biophysical Chemistry, Göttingen, Germany.

Dietmar Riedel (D)

Facility for Transmission Electron Microscopy, Max Planck Institute for Biophysical Chemistry, Göttingen, Germany.

Reinhard Jahn (R)

Laboratory of Neurobiology, Max-Planck-Institute for Biophysical Chemistry, Göttingen, Germany.
Georg-August University, Göttingen, Germany.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH