Rab3 dissociation and clathrin-mediated endocytosis, two key steps in the exo-endocytotic pathway of large dense-cored vesicles in primary cultures of superior cervical ganglia

European Journal of Cell Biology

Volumn 74, Issue 3, 1997, Pages 217-229

  Annaert, Wim G ^a,b   Partoens, Peter ^a   Slembrouck, Dirk ^a   Bakker, Annette ^a   Jacob, Wim ^a   De Potter, Werner P ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Clathrin; Endocytosis; Exocytosis; Large dense cored vesicle; Noradrenergic neuron; Rab3; Superior cervical ganglion

Indexed keywords

ANTIMITOTIC AGENT; CLATHRIN; DOPAMINE BETA MONOOXYGENASE; ENZYME ANTIBODY; GUANINE NUCLEOTIDE BINDING PROTEIN; HORSERADISH PEROXIDASE; RAB PROTEIN; SYNAPTOTAGMIN;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL ULTRASTRUCTURE; COATED VESICLE; CONTROLLED STUDY; DENSITY GRADIENT CENTRIFUGATION; ENDOCYTOSIS; EXOCYTOSIS; FETUS; IMMUNOFLUORESCENCE; IMMUNOFLUORESCENCE TEST; MEMBRANE VESICLE; NERVE CELL CULTURE; NERVE CELL MEMBRANE STEADY POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SUPERIOR CERVICAL GANGLION; SWINE; SYMPATHETIC NERVE CELL;

ANIMALIA; ARMORACIA RUSTICANA; SUIDAE; SUS SCROFA;

EID: 0030666523     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (57)

1. Annaert, W. G., J. Quatacker, I. Llona, W. P. De Potter: Differences in the distribution of cytochrome b561 and synaptophysin in dog splenic nerve: a biochemical and immunocytochemical study. J. Neurochem. 62, 265-274 (1994).
2. Annaert, W. G., I. Llona, J. Quatacker, E. De Ritter, A. Weyns, W. P. De Potter: Subcellular localization of synaptophysin in noradrenergic nerve terminals: a biochemical and morphological study. Synapse 21, 65-76 (1995).
3. Bartfai, T., K. Iverfeldt, G. Fisone, P. A. Serfozo: Regulation of the release of coexisting neurotransmitters. Rev. Pharmacol. Toxicol. 28, 285-310 (1988).
4. Bauerfeind, R., A. Règnier-Vigouroux, T. Flatmark, W. B. Huttner: Selective storage of acetylcholine, but not catecholamines, in neuroendocrine synaptic-like microvesicles of early endosomal origin. Neuron 11, 105-121 (1993).
5. Bauerfeind, R., R. Jelinek, A. Hellwig, W. B. Huttner: Neurosecretory vesicles can be hybrids of synaptic vesicles and secretory granules. Proc. Natl. Acad. Sci. USA 92, 7342-7346 (1995).
6. Bradford, M. M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254 (1976).
7. Brose, N., A. G. Petrenko, T. C. Südhof, R. Jahn: Synaptotagmin: a Ca2+ sensor on the synaptic vesicle surface. Science 256, 1021-1025 (1992).
8. Bruns, D., R. Jahn: Real-time measurement of transmitter release from single synaptic vesicles. Nature 377, 62-65 (1995).
9. Cupers, P., A. Veithen, A. Kiss, P. Baudhuin, P. J. Courtoy: Clathrin polmyerization is not required for bulk-phase endocytosis in rat fetal fibroblasts. J. Cell Biol. 127, 725-735 (1994).
10. Darchen, F., J. Senyshyn, W. H. Brondyk, D. J. Taatjes, R. W. Holz, J. P. Henry, J. P. Denizot, I. G. Macara: The GTPase rab3a is associated with large dense-cored vesicles in bovine chromaffin cells and rat PC12 cells. J. Cell Sci. 108, 1639-1649 (1995).
11. De Camilli, P., R. Jahn: Pathways to regulated exocytosis in neurons. Annu. Rev. Physiol. 52, 625-645 (1990).
12. De Potter, W. P.: Peripheral sympathetic neurotransmission. Arscia Uitgaven N. V. Brussels, Belgium (1976).
13. De Potter, W. P., L. Dillen, W. A. Annaert, K. Tombeur, R. Berghmans, E. P. Coen: Evidence for the co-storage and co-release of neuropeptide Y and noradrenaline from large dense-cored vesicles in sympathetic nerves of the bovine vas deferens. Synapse 2, 157-162 (1988).
14. De Potter, W. P., P. Partoens, A. Schoups, I. Llona, E. P. Coen: Noradrenergic neurons release both noradrenaline and neuropeptides from a single pool: the large dense-cored vesicles. Synapse 25, 44-55 (1997).
15. Dillen, L., M. Claeys, W. P. De Potter. Determination of dopamine-β-hydroxylase in cerebrospinal fluid by high-performance liquid chromatography with electrochemical detection. J. Pharmacol. Methods 15, 51-63 (1986).
16. Fischer von Mollard, G. F., T. C. Südhof, R. Jahn: A small GTP-binding protein dissociates from synaptic vesicles during exocytosis. Nature 349, 79-81 (1991).
17. Fischer von Mollard, G. F., B. Stahl, A. Khokhlatchev, T. C. Südhof, R. Jahn: Rab3c is a synaptic vesicle protein that dissociates from synaptic vesicles after stimulation of exocytosis. J. Biol. Chem. 269, 10971-10974 (1994).
18. Gruenberg, J., G. Griffiths, K. E. Howell: Characterisation of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro. J. Cell Biol. 108, 1301-1316 (1989).
19. Heidelberger, R., C. Heinemann, E. Neher, G. Matthews: Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371, 513-515 (1994).
20. Heuser, J.: The role of coated vesicles in recycling of synaptic vesicle membrane. Cell Biol. Int. Rep. 13, 1063-1076 (1989).
21. Heuser, J., T. S. Reese: Evidence for the recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57, 315-344 (1973).
22. Higgins, D., P. J. Lein, D. J. Osterhout, M. I. Johnson: Tissue culture of mammalian autonomie neurons. In: G. Banker, K. Higgins (eds.): Culturing Nerve Cells, pp 177-205. MlT Press. Cambridge, MA 1991.
23. Hurtley, S. M.: Recycling of a secretory granule membrane protein after stimulated secretion. J. Cell Sc. 106, 649-656 (1993).
24. Jahn, R., P. De Camilli: Membrane proteins of synaptic vesicles: Markers for neurons and endocrine cells; Tools for the study of neurosecretion. In: M. Gratzl, K. Langley (eds.): Markers for Neural and Endocrine Cells: Molecular and Cell Biology, Diagnostic Applications. pp 25-92. VCH. Weinheim, Germany 1991.
25. Jena, B. P., F. D. Gumkowski, E. M. Konieczko, G. Fischer von Mollard, R. Jahn, J. D. Jamieson: Redistribution of a rab3-like GTP-binding protein from secretory granules to the Golgi-complex in pancreatic acinar cells during regulated exocytosis. J. Cell Biol. 124, 43-53 (1994).
26. Johannes, L., P. M. Lledo, M. Roa, J. D. Vincent, J. P. Henry, F. Darchen: The GTPase rab3a negatively controls calcium-dependent exocytosis in neuroendocrine cells. EMBO J. 13, 2029-2037 (1994).
27. Klein, R. L., A. K. Thureson-Klein: Noradrenergic vesicles. In: A. Lajtha (ed.): Handbook of Neurochemistry. pp 71-109. Plenum Press. New York 1984.
28. Laemmli, U. K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685 (1970).
29. Lagercrantz, H., D. F. Kirksey, R. L. Klein: On the development of sympathetic nerve trunk vesicles during axonal transport: density gradient analysis of dopamine-β-hydroxylase in bovine splenic nerve. J. Neurochem. 23, 769-773 (1974).
30. Leighton, F., B. Poole, P. Beaufay, P. Baudhuin, J. W. Coffey, S. Fowler, C. De Duve: The large-scale separation of peroxisomes, mitochondria and lysosomes from the livers of rats injected with Triton WR-1339. Improved isolation procedures, automated analysis, biochemical and morphological properties of fractions. J. Cell Biol. 37, 482-513 (1986).
31. Li, J.-Y., R. Jahn, A. Dahlström: Rab3a, a small GTP-binding protein, undergoes fast anterograde transport but not retrograde transport in neurons. Eur. J. Cell Biol. 67, 297-307 (1995).
32. Martelli, A. M., R. Bareggi, G. Baldini, P. E. Scherer, H. F. Lodish: Diffuse vesicular distribution of Rab3D in the polarized neuroendocrine cell line AtT-20. FEBS Lett. 368, 271-275 (1995).
33. Matteoli, M., C. Haimann, F. Torri-Tarelli, J. M. Polak, B. Ceccarelli, P. De Camilli: Differential effect of alpha-latrotoxin on exocytosis from small synaptic vesicles and from large dense-core vesicles containing calcitonin gene-related peptide at the frog neuromuscular junction. Proc. Natl. Acad. Sci. USA 85, 7366-7370 (1988).
34. Matteoli, M., K. Takei, P. Cameron, P. Hurlbut, P. A. Johnston, R. Jahn, T. C. Südhof, P. De Camilli: Association or rab3A with synaptic vesicles at late stages of the secretory pathway. J. Cell Biol. 115, 625-633 (1991).
35. Maycox, P. R., E. Link, A. Reetz, S. A. Morris, R. Jahn: Clathrin-coated vesicles in nervous tissue are involved primarily in synaptic vesicle recycling. J. Cell Biol. 118, 1379-1388 (1992).
36. Nordmann, J. J., J. C. Artault: Membrane retrieval following exocytosis in isolated neurosecretory nerve endings. Neuroscience 49, 201-207 (1992).
37. Patzak, A., H. Winkler: Exocytotic exposure and recycling of membrane antigens of chromaffin granules: Ultrastructural evaluation after immunolabelling. J. Cell Biol. 102, 510-515 (1986).
38. Phillips, J. H.: Chromaffin granule biogenesis and the exocytosis/ endocytosis cycle. In: I. Rosenheck, P. I. Lelkes (eds.): Stimulus-Secretion Coupling in Chromaffin Cells. pp 31-54. CRC Press Inc. Boca Raton, Florida 1987.
39. Règnier-Vigouroux, A., W. B. Huttner: Biogenesis of small synaptic vesicles and synaptic-like microvesicles. Neurochem. Res. 18, 59-64 (1993).
40. Rothman, J. E.: Mechanisms of intracellular protein transport. Nature 372, 55-63 (1994).
41. Scheller, R. H.: Membrane trafficking in the presynaptic nerve terminal. Neuron 14, 893-897 (1995).
42. Smith, A. D.: Proteins of vesicles from sympathetic axons: chemistry, immunoreactivity and release upon stimulation. Neurosci. Res. Prog. Bull. 8, 377-382 (1970).
43. Söllner, T., S. W. Whiteheart, M. Brunner, H. Erdjument-Bromage, H. Geromanos, P. Tempst, J. E. Rothman: SNAP receptors implicated in vesicle targeting and fusion. Nature 362, 318-324 (1993).
44. Söllner, T., M. K. Bennett, S. W. Whiteheart, R. H. Scheller, J. E. Rothman: A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation and fusion. Cell 75, 409-418 (1993).
45. Stahl, B., G. Fischer von Mollard, C. Walch-Solimena, R. Jahn: GTP cleavage by the small GTP-binding protein Rab3a is associated with exocytosis of synaptic vesicles induced by α-latrotoxin. J. Biol. Chem. 269, 24770-24776 (1994).
46. Südhof, T. C.: The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375, 645-653 (1995).
47. Takei, K., P. S. McPherson, S. L. Schmid, P. De Camilli: Tubular membrane invaginations coated by dnamin rings are induced by GTP-γs in nerve terminals. Nature 374, 186-190 (1995).
48. Takei, K., O. Mundigl, L. Daniell, P. De Camilli: The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin. J. Cell Biol. 133, 1237-1250 (1996).
49. Thureson-Klein, K., R. L. Klein: Exocytosis from neuronal large dense-cored vesicles. Int. Rev. Cytol. 121, 67-126 (1990).
50. Towbin, H., T. Staehelin, J. Gordon: Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 4350-4354 (1979).
51. Valentijn, J. A., D. Sengupta, F. D. Gumkowski, L. H. Tang, E. M. Konieczko, J. D. Jamieson: Rab3D localizes to secretory granules in rat pancreatic acinar cells. Eur. J. Cell Biol. 70, 33-41 (1996).
52. Walch-Solimena, C., K. Takei, M. L. Marek, K. Midyett, T. C. Südhof, P. De Camilli, R. Jahn: Synaptotagmin: a membrane constituent of neuropeptide-containing large dense-core vesicles. J. Neurosci. 13, 3895-3903 (1993).
53. Wang, J. M., P. Partoens, D. Callebaut, E. P. Coen, J. J. Martin, W. P. De Potter: Phenotypic plasticity and immunocytochemical evidence for ChAt and DβH colocalization in fetal pig superior cervical ganglion cells. Dev. Brain Res. 90, 17-23 (1995).
54. Weber, E., T. Jilling, K. L. Kirk: Distinct functional properties of rab3A and rab3B in PC12 neuroendocrine cells. J. Biol. Chem. 271, 6963-6971 (1996).
55. Winkler, H., R. Fischer-Colbrie: Common membrane proteins of chromaffin granules, endocrine and synaptic vesicles: properties, tissue distribution, membrane topography and regulation of synthesis. Neurochem. Int. 17, 245-262 (1990).
56. Yamazaki, T., D. J. Selkoe, E. H. Koo: Trafficking of cell surface amyloid precursor protein: retrograde and transcytotic transport in cultured neurons. J. Cell Biol. 129, 431-442 (1995).
57. Zhang, J. Z., B. A. Davletov, T. C. Südhof, R. G. W. Anderson: Synaptotagmin I is a high affinity receptor for clathrin AP-2: Implications for membrane recycling. Cell 78, 751-760 (1994).