Synaptic vesicle proteins and early endosomes in cultured hippocampal neurons: differential effects of Brefeldin A in axon and dendrites

doi:10.1083/jcb.122.6.1207

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Synaptic vesicle proteins and early endosomes in cultured hippocampal neurons: differential effects of Brefeldin A in axon and dendrites

O Mundigl, M Matteoli, L Daniell, A Thomas-Reetz, A Metcalf, R Jahn and P De Camilli
Howard Hughes Medical Institute, Yale University School of Medicine, New Haven, Connecticut 06510.

The pathways of synaptic vesicle (SV) biogenesis and recycling are still poorly understood. We have studied the effects of Brefeldin A (BFA) on the distribution of several SV membrane proteins (synaptophysin, synaptotagmin, synaptobrevin, p29, SV2 and rab3A) and on endosomal markers to investigate the relationship between SVs and the membranes with which they interact in cultured hippocampal neurons developing in isolation. In these neurons, SV proteins are detected as punctate immunoreactivity that is concentrated in axons but is also present in perikarya and dendrites. In the same neurons, the transferrin receptor, a well established marker of early endosomes, is selectively concentrated in perikarya and dendrites. In the perikaryal- dendritic region, BFA induced a dramatic tubulation of transferrin receptors as well as a cotubulation of the bulk of synaptophysin. Synaptotagmin, synaptobrevin, p29 and SV2 immunoreactivities retained a primarily punctate distribution. No tubulation of rab3A was observed. In axons, BFA did not produce any obvious alteration of the distribution of SV proteins, nor of peroxidase- or Lucifer yellow- labeled early endosomes. The selective effect of BFA on dendritic membranes suggests the existence of functional differences between the endocytic systems in dendrites and axons. Cotubulation of transferrin receptors and synaptophysin in the perikaryal-dendritic region is consistent with a functional interconnection between the traffic of SV proteins and early endosomes. The heterogeneous effects of BFA on SV proteins in this cell region indicates that SV proteins are differentially sorted upon exit from the TGN and are coassembled into SVs at the cell periphery.
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Burns, M.E., Sasaki, T., Takai, Y., Augustine, G.J. (1998). Rabphilin-3A: A Multifunctional Regulator of Synaptic Vesicle Traffic. JGP 111: 243-255 [Abstract] [Full Text]
Lledo, P., Zhang, X., Südhof, T. C., Malenka, R. C., Nicoll, R. A. (1998). Postsynaptic Membrane Fusion and Long-Term Potentiation. Science 279: 399-403 [Abstract] [Full Text]
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West, A. E., Neve, R. L., Buckley, K. M. (1997). Targeting of the Synaptic Vesicle Protein Synaptobrevin in the Axon of Cultured Hippocampal Neurons: Evidence for Two Distinct Sorting Steps. JCB 139: 917-927 [Abstract] [Full Text]
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Ringstad, N., Nemoto, Y., De Camilli, P. (1997). The SH3p4/Sh3p8/SH3p13 protein family: Binding partners for synaptojanin and dynamin via a Grb2-like Src homology 3�domain. Proc. Natl. Acad. Sci. USA 94: 8569-8574 [Abstract] [Full Text]
Schmidt, A., Hannah, M. J., Huttner, W. B. (1997). Synaptic-like Microvesicles of Neuroendocrine Cells Originate from a Novel Compartment That Is Continuous with the Plasma Membrane and Devoid of Transferrin Receptor. JCB 137: 445-458 [Abstract] [Full Text]
Wilson, J. M., Colton, T. L. (1997). Targeting of an Intestinal Apical Endosomal Protein to Endosomes in Nonpolarized Cells. JCB 136: 319-330 [Abstract] [Full Text]
Marquez-Sterling, N. R., Lo, A. C.�Y., Sisodia, S. S., Koo, E. H. (1997). Trafficking of Cell-Surface beta -Amyloid Precursor Protein: Evidence that a Sorting Intermediate Participates in Synaptic Vesicle Recycling. J. Neurosci. 17: 140-151 [Abstract] [Full Text]
Kraszewski, K., Daniell, L., Mundigl, O., De Camilli, P. (1996). Mobility of Synaptic Vesicles in Nerve Endings Monitored by Recovery from Photobleaching of Synaptic Vesicle-Associated Fluorescence. J. Neurosci. 16: 5905-5913 [Abstract] [Full Text]
Galli, T., McPherson, P. S., De Camilli, P. (1996). The V(0) Sector of the V-ATPase, Synaptobrevin, and Synaptophysin Are Associated on Synaptic Vesicles in a Triton X-100-resistant, Freeze-thawing Sensitive, Complex. J. Biol. Chem. 271: 2193-2198 [Abstract] [Full Text]
Chang, S., Hemmings, H. C. Jr., Aderem, A. (1996). Stimulus-dependent Phosphorylation of MacMARCKS, a Protein Kinase C Substrate, in Nerve Termini and PC12 Cells. J. Biol. Chem. 271: 1174-1178 [Abstract] [Full Text]
Sofer, A, Schwarzmann, G, Futerman, A. (1996). The internalization of a short acyl chain analogue of ganglioside GM1 in polarized neurons. J. Cell Sci. 109: 2111-2119 [Abstract]
Buxbaum, E, Woodman, P. (1995). Selective action of uncoating ATPase towards clathrin-coated vesicles from brain. J. Cell Sci. 108: 1295-1306 [Abstract]
Baurfend, R., David, C., Galli, T., McPherson, P.S., Takei, K., De Camilli, P. (1995). Molecular Mechanisms in Synaptic Vesicle Endocytosis. Cold Spring Harb Symp Quant Biol 60: 397-404 [Abstract]
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