Skip to main content

Synaptic Vesicle Membrane Traffic and the Cycle of Rab3

  • Chapter
GTPases in Biology I

Part of the book series: Handbook of Experimental Pharmacology ((HEP,volume 108 / 1))

Abstract

Neurons are highly specialized cells which process and transmit information. Information is transferred between neurons via small molecules, the neurotransmitters. Neurotransmitters are stored in synaptic vesicles and are released by Ca2+-dependent exocytosis upon activation of the presynaptic cell (for reviews see Smith and Augustine 1988; De Camilli and Jahn 1990; Südhof and Jahn 1991).

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Araki S, Kikuchi A, Hata Y, Isomura M, Takai Y (1990) Regulation of reversible binding of smgp25A, a ras p21 like GTP-binding protein, to synaptic plasma membranes and vesicles by its specific regulatory protein, GDP dissociation inhibitor (GDI). J Biol Chem 265:13007–13015

    PubMed  CAS  Google Scholar 

  • Ayala J, Olofsson B, Tavitian A, Prochiantz A (1989) Developmental and regional regulation of rab3: a new brain specific ras-like gene. J Neurosci Res 22:241–246

    Article  PubMed  CAS  Google Scholar 

  • Balch WE (1990) Small GTP-binding proteins in vesicular transport. TIBS 15:473–477

    PubMed  Google Scholar 

  • Bourne HR, Sanders DA, McCormick F (1990) The GTPase superfamily: a conserved switch for diverse cell functions. Nature 348:125–132

    Article  PubMed  CAS  Google Scholar 

  • Burstein ES, Macara IG (1992) Characterization of a guanine nucleotide-releasing factor and a GTPase-activating protein that are specific for the ras-related protein p25 rab3A. Proc Natl Acad Sci USA 89: 1154–1158

    Article  PubMed  CAS  Google Scholar 

  • Burstein ES, Linko-Stentz K, Lu Z, Macara IG (1991) Regulation of the GTPase activity of the ras-like protein p25 rab3A evidence for a rab3A-specific GAP. J Biol Chem 266:2689–2692

    PubMed  CAS  Google Scholar 

  • Casey PJ, Thissen JA, Moolmaw JF (1991) Enzymatic modification of proteins with a geranylgeranyl isoprenoid. Proc Natl Acad Sci USA 88:8631–8635

    Article  PubMed  CAS  Google Scholar 

  • Ceccarelli B, Hurlbut WP (1980) Vesicle hypothesis of the release of quanta of acetylcholine. Physiol Rev 60:396–441

    PubMed  CAS  Google Scholar 

  • Chavrier P, Gorvel JP, Stelzer E, Simons K, Gruenberg J, Zerial M (1991) Hypervariable C-terminal domain of rab proteins acts as a targeting signal. Nature 353:769–772

    Article  PubMed  CAS  Google Scholar 

  • Darchen F, Zahraoui A, Hammel F, Monteils MP, Tavitian A, Scherman D (1990) Association of the GTP-binding protein Rab3A with bovine adrenal chromaffin granules. Proc Natl Acad Sci USA 87:5692–5696

    Article  PubMed  CAS  Google Scholar 

  • De Camilli P, Jahn R (1990) Pathways to regulated exocytosis in neurons. Annu Rev Physiol 52:625–645

    Article  PubMed  Google Scholar 

  • Farnsworth CC, Kawata M, Yoshida Y, Takai Y, Gelb MH, Glomset JA (1991) C terminus of the small GTP-binding protein smgp25A contains two geranylgeranylated cysteine residues and a methyl ester. Proc Natl Acad Sci USA 88:6196–6200

    Article  PubMed  CAS  Google Scholar 

  • Fischer von Mollard G, Mignery G, Baumert M, Perkin MS, Hanson TJ, Burger PM, Jahn R, Südhof TC (1990) Rab3 is a small GTP-binding protein exclusively localized to synaptic vesicles. Proc Natl Acad Sci USA 87:1988–1992

    Article  Google Scholar 

  • Fischer von Mollard G, Südhof TC, Jahn R (1991) A small GTP-binding protein dissociates from synaptic vesicles during exocytosis. Nature 349:79–81

    Article  Google Scholar 

  • Gallwitz D, Donath C, Sander C (1983) A yeast gene encoding a protein homologous to the human c-has/bas proto-oncogene product. Nature 306:704–707

    Article  PubMed  CAS  Google Scholar 

  • Griffiths G, Gruenberg J (1991) The arguments for pre-existing early and late endosomes. TICB 1:5–9

    CAS  Google Scholar 

  • Hancock JF, Magee AI, Childs JE, Marshall CJ (1989) All ras proteins are polyisoprenylated but only some are palmitoylated. Cell 57:1167–1177

    Article  PubMed  CAS  Google Scholar 

  • Heuser JE, Reese TS (1973) Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol 57:315–344

    Article  PubMed  CAS  Google Scholar 

  • Horiuchi H, Kawata M, Katayama M, Yoshida Y, Musha T, Ando S, Takai Y (1991) A novel prenyltransferase for a small GTP-binding protein having a C-terminal Cys-Ala-Cys structure. J Biol Chem 266:16981–16984

    PubMed  CAS  Google Scholar 

  • Jaentzko A, Zimmermann H, Volknandt W (1989) Intraneuronal distribution of a synaptic vesicle membrane protein: antibody binding sites at axonal membrane compartments and trans-Golgi network and accumulation at nodes of ranvier. Neuroscience 32:65–77

    Article  Google Scholar 

  • Johnston PA, Archer BT, Robinson K, Mignery GA, Jahn R, Südhof TC (1991) Rab3A attachment to the synaptic vesicle membrane mediated by a conserved polyisoprenylated carboxy-terminal sequence. Neuron 7:101–109

    Article  PubMed  CAS  Google Scholar 

  • Khosravi-Far R, Lutz R, Cox AD, Conroy L, Bourne JR, Sinensky M, Balch WE, Buss JE, Der CJ (1991) Isoprenoid modification of rab proteins terminating on CC or CXC motifs. Proc Natl Acad Sci USA 88:6264–6268

    Article  PubMed  CAS  Google Scholar 

  • Kikuchi A, Yamashita T, Kawata M, Yamamoto K, Ikeda K, Tanimoto T, Takai Y (1988) Purification and characterization of a novel GTP-binding protein with a molecular weight of 24000 from bovine brain membranes. J Biol Chem 263:2897–2904

    PubMed  CAS  Google Scholar 

  • Kim S, Kikuchi A, Mizoguchi A, Takai Y (1989) Intrasynaptosomal distribution of the ras, rho and smg-25A GTP-binding proteins in bovine brain. Mol Brain Res 6:167–176

    Article  PubMed  CAS  Google Scholar 

  • Kinsella BT, Maltese WA (1992) rab GTP-binding proteins with three different carboxyl-terminal cysteine motifs are modified in vivo by 20-carbon isoprenoids. J Biol Chem 267:3940–3945

    PubMed  CAS  Google Scholar 

  • Kinsella, BT, Erdman RA, Maltese WA (1991) Posttranslational modification of Ha-ras p21 by farnesyl versus geranylgeranyl isoprenoids is determined by the COOH-terminal amino acid. Proc Natl Acad Sci USA 88:8934

    Article  PubMed  CAS  Google Scholar 

  • Matsuda K, Sakamoto C, Nakano O, Konda Y, Matozaki T, Wada K, Kasuga M, Mizoguchi A, Kikuchi A, Takai Y (1992) Distribution of smg p25A and smg p21s, ras p21-like guanine nucleotide-binding proteins, in the rat stomach. Am J Physiol 262:G69–G73

    PubMed  CAS  Google Scholar 

  • Matsui Y, Kikuchi A, Kondo J, Hishida T, Teranishi Y, Takai Y (1988) Nucleotide and deduced amino acid sequences of a GTP-binding protein family with molecular weights of 25000 from bovine brain. J Biol Chem 263:11071–11074

    PubMed  CAS  Google Scholar 

  • Matsui Y, Kikuchi A, Araki S, Hata S, Kondo J, Teranishi Y, Takai Y (1990) Molecular cloning and characterization of a novel type of regulatory protein (GDI) for smg p25A, a ras p21-like GTP-binding protein. Mol Cell Biol 10:4116–4122

    PubMed  CAS  Google Scholar 

  • Matteoli M, Takei K, Cameron R, Hurlbut P, Johnston PA, Südhof TC, Jahn R, De Camilli P (1991) Association of rab3A with synaptic vesicles at late stages of the secretory pathway. J Cell Biol 115:625–633

    Article  PubMed  CAS  Google Scholar 

  • Maycox PR, Link E, Reetz A, Morris SA, Jahn R (1992) Clathrin-coated vesicles in nervous tissue are involved primarily in synaptic vesicle recycling. J Cell Biol 118:1379–1388

    Article  PubMed  CAS  Google Scholar 

  • Mizoguchi A, Kim S, Ueda T, Takai Y (1989) Tissue distribution of smgp25A, a ras p21-like GTP-binding protein, studied by use of a specific monoclonal antibody. Biochem Biophys Res Commun 162:1438–1445

    Article  PubMed  CAS  Google Scholar 

  • Ngsee JK, Miller K, Wendland B, Scheller RH (1990) Multiple GTP-binding proteins from cholinergic synaptic vesicle. J Neurosci 10:317–322

    PubMed  CAS  Google Scholar 

  • Olofsson B, Chardin P, Touchot N, Zahraoui A, Tavitian A (1988) Expression or the ras-related rallA, rhol2 and rab genes in adult mouse tissue. Oncogene 3:231–234

    PubMed  CAS  Google Scholar 

  • Pfeffer SR (1992) GTP-binding proteins in intracellular transport. TICB 2:41–46

    CAS  Google Scholar 

  • Regnier-Vigouroux A, Tooze SA, Huttner WB (1991) Newly synthesized synaptophysin is transported to synaptic-like microvesicles via constitutive secretory vesicles and the plasma membrane. EMBO J 10:3589–3601

    PubMed  CAS  Google Scholar 

  • Rothman JE, Orci L (1990) Movement of proteins through the Golgi stack: a molecular dissection of vesicular transport. FASEB J 4:1460–1468

    PubMed  CAS  Google Scholar 

  • Salminen A, Novick PJ (1987) A ras-like protein is required for a post-Golgi event in yeast. Cell 49:527–538

    Article  PubMed  CAS  Google Scholar 

  • Sano K, Kikuchi A, Matsui Y, Teranishi Y, Takai Y (1989) Tissue-specific expression of a novel GTP-binding protein (smg p25A) mRNA and its increase by nerve growth factor and cyclic AMP in rat pheochromocytoma PC-12 cells. Biochem Biophys Res Commun 158:377–385

    Article  PubMed  CAS  Google Scholar 

  • Sasaki T, Kikuchi A, Araki S, Hata Y, Isomura M, Kuroda S, Takai Y (1990) Purification and characterization from bovine brain cytosol of a protein that inhibits the dissociation of GDP from and the subsequent binding of GTP to smg p25A, a ras p21 like GTP-binding protein. J Biol Chem 265:2333–2337

    PubMed  CAS  Google Scholar 

  • Sasaki T, Kaibuchi K, Kabcenell A, Novick PJ, Takai Y (1991) A mammalian inhibitory GDP/GTP exchange protein (GDP dissociation inhibitor) for smgp25A is active on the yeast sec4 protein. Mol Cell Biol 11:2909

    PubMed  CAS  Google Scholar 

  • Schnefel S, Zimmermann P, Pröfrock A, Jahn R, Aktories K, Hinsch KD, Haase W, Schulz I (1992) Multiple small and high molecular weight GTP-binding proteins in zymogen granule membranes of rat pancreatic acinar cells. Cell Physiol Biochem 2:77–89

    Article  CAS  Google Scholar 

  • Seabra MC, Goldstein JC, Südhof TC, Brown MS (1992) Rab Geranylgeranyl transferase: a multisubunit enzyme that prenylates GTP-binding terminating in Cys-X-Cys or Cys-Cys. J Biol Chem 267:14497–14503

    PubMed  CAS  Google Scholar 

  • Smith SJ, Augustine GJ (1988) Calcium ions, active zones and synaptic transmitter release. TINS 11:458–464

    PubMed  CAS  Google Scholar 

  • Südhof TC, Jahn R (1991) Proteins of synaptic vesicles involved in exocytosis and membrane recycling. Neuron 6:665–677

    Article  PubMed  Google Scholar 

  • Volknandt W, Pevsner J, Elferink LA, Schilling J, Scheller RH (1991) A synaptic vesicle specific GTP-binding protein from ray electric organ. Mol Brain Res 11:283–290

    Article  PubMed  CAS  Google Scholar 

  • Zahraoui A, Touchet N, Chardin P, Tavitian A (1988) Complete coding sequences of the ras related rab 3 and 4 cDNAs. Nucleic Acid Res 16:1204

    Article  PubMed  CAS  Google Scholar 

  • Zahraoui A, Touchet N, Chardin P, Tavitian A (1989) The human rab genes encode a family of GTP-binding proteins related to yeast YPT1 and sec4 products involved in secretion. J Biol Chem 264:12394–12401

    PubMed  CAS  Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1993 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

von Mollard, G.F., Südhof, T.C., Jahn, R. (1993). Synaptic Vesicle Membrane Traffic and the Cycle of Rab3. In: Dickey, B.F., Birnbaumer, L. (eds) GTPases in Biology I. Handbook of Experimental Pharmacology, vol 108 / 1. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-78267-1_31

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-78267-1_31

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-78269-5

  • Online ISBN: 978-3-642-78267-1

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics