Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro

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Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro

J Gruenberg, G Griffiths and KE Howell
European Molecular Biology Laboratory, Heidelberg, Federal Republic of Germany.

We have investigated two aspects of membrane traffic at early stages of endocytosis: membrane fusion and microtubule-dependent transport. As a marker, we have used the trans-membrane glycoprotein G of vesicular stomatitis virus implanted into the plasma membrane and then internalized for different times at 37 degrees C. The corresponding endosomal fractions were immunoisolated using the cytoplasmic domain of the G protein as antigen. These fractions were then used in an in vitro assay to quantify the efficiency of fusion between endosomal vesicles. To identify the vesicular partners of the fusion, these in vitro studies were combined with in vivo biochemical and morphological experiments. Internalized molecules were delivered to early endosomal elements, which corresponded to a network of tubular and tubulovesicular structures. Rapid recycling back to the plasma membrane and routing to late stages of the pathway occurred from these early endosomal elements. These elements exhibited a high and specific fusion activity with each other in vitro, suggesting that individual elements of the early endosomal compartment interact with each other in vivo. After their appearance in the early endosome, the molecules destined to be degraded were observed at the next stage of the pathway in distinct spherical vesicles (0.5 micron diam) and then in late endosomes and lysosomes. When the microtubules were depolymerized with nocodazole, endocytosis proceeded as in control cells. However, internalized molecules remained in the spherical vesicles and did not appear in late endosomes or lysosomes. These spherical vesicles had relatively little fusion activity with each other or with early endosomal elements in vitro. Our observations suggest that the spherical vesicles mediate transport between the early endosome and late endosomes and that this process requires intact microtubules.
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Rojo, M., Pepperkok, R., Emery, G., Kellner, R., Stang, E., Parton, R. G., Gruenberg, J. (1997). Involvement of the Transmembrane Protein p23 in Biosynthetic Protein Transport. JCB 139: 1119-1135 [Abstract] [Full Text]
Gu, F., Aniento, F., Parton, R. G., Gruenberg, J. (1997). Functional Dissection of COP-I Subunits in the Biogenesis of Multivesicular Endosomes. JCB 139: 1183-1195 [Abstract] [Full Text]
Ward, D. M., Leslie, J. D., Kaplan, J. (1997). Homotypic Lysosome Fusion in Macrophages: Analysis Using an In Vitro Assay. JCB 139: 665-673 [Abstract] [Full Text]
Kumar, A., Wetzler, E., Berger, M. (1997). Isolation and Characterization of Complement Receptor Type 1�(CR1) Storage Vesicles From Human Neutrophils Using Antibodies to the Cytoplasmic Tail of CR1. Blood 89: 4555-4565 [Abstract] [Full Text]
Turner, M. D., Plutner, H., Balch, W. E. (1997). A Rab GTPase Is Required for Homotypic Assembly of the Endoplasmic Reticulum. J. Biol. Chem. 272: 13479-13483 [Abstract] [Full Text]
Presley, J. F., Mayor, S., McGraw, T. E., Dunn, K. W., Maxfield, F. R. (1997). Bafilomycin A1 Treatment Retards Transferrin Receptor Recycling More than Bulk Membrane Recycling. J. Biol. Chem. 272: 13929-13936 [Abstract] [Full Text]
Blocker, A., Severin, F. F., Burkhardt, J. K., Bingham, J. B., Yu, H., Olivo, J.-C., Schroer, T. A., Hyman, A. A., Griffiths, G. (1997). Molecular Requirements for Bi-directional Movement of Phagosomes Along Microtubules. JCB 137: 113-129 [Abstract] [Full Text]