Rab11 Regulates the Compartmentalization of Early Endosomes Required for Efficient Transport from Early Endosomes to the Trans-Golgi Network

doi:10.1083/jcb.151.6.1207

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Published online 11 December 2000. doi:10.1083/jcb.151.6.1207

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© The Rockefeller University Press, 0021-9525/2000//1207 $5.00
The Journal of Cell Biology, Volume 151, Number 6, , 2000 1207-1220

Original Article

Rab11 Regulates the Compartmentalization of Early Endosomes Required for Efficient Transport from Early Endosomes to the Trans-Golgi Network

Mona Wilcke^a, Ludger Johannes^a, Thierry Galli^a, Véronique Mayau^b, Bruno Goud^a, and Jean Salamero^a

^a UMR CNRS 144, Laboratoire Mécanismes Moléculaires du Transport Intracellulaire, Institut Curie, F-75248 Paris Cedex 05, France
^b Unité de Génétique Somatique, URA CNRS 1960, Institut Pasteur, 75724 Paris Cedex 15, France
Molecular Biology and Genomics, Department of Biology, Pharmacia Corporation, S-112 87 Stockholm, Sweden.46-8-618588246-8-6958610

mona.wilcke{at}eu.pnu.com

Several GTPases of the Rab family, known to be regulators ofmembrane traffic between organelles, have been described andlocalized to various intracellular compartments. Rab11 has previouslybeen reported to be associated with the pericentriolar recyclingcompartment, post-Golgi vesicles, and the trans-Golgi network(TGN). We compared the effect of overexpression of wild-typeand mutant forms of Rab11 on the different intracellular transportsteps in the endocytic/degradative and the biosynthetic/exocyticpathways in HeLa cells. We also studied transport from endosomesto the Golgi apparatus using the Shiga toxin B subunit (STxB)and TGN38 as reporter molecules. Overexpression of both Rab11wild-type (Rab11wt) and mutants altered the localization ofthe transferrrin receptor (TfR), internalized Tf, the STxB,and TGN38. In cells overexpressing Rab11wt and in a GTPase-deficientRab11 mutant (Rab11Q70L), these proteins were found in vesiclesshowing characteristics of sorting endosomes lacking cellubrevin(Cb). In contrast, they were redistributed into an extendedtubular network, together with Cb, in cells overexpressing adominant negative mutant of Rab11 (Rab11S25N). This tubularizedcompartment was not accessible to Tf internalized at temperatures<20°C, suggesting that it is of recycling endosomal origin.Overexpression of Rab11wt, Rab11Q70L, and Rab11S25N also inhibitedSTxB and TGN38 transport from endosomes to the TGN. These resultssuggest that Rab11 influences endosome to TGN trafficking primarilyby regulating membrane distribution inside the early endosomalpathway.

Key Words: Rab11 • intracellular trafficking • endosomes • Shiga toxin • TGN38

T. Galli's present address is UMR CNSR 144, Membrane Trafficand Neuronal Plasticity, Institut Curie, F-75248 Paris Cedex05, France.

Abbreviations used in this paper: CI-M6P, cation-independentM6P; Cb, human cellubrevin; HA, hemagglutinin; Ii, MHC classII–associated invariant chain; M6P, mannose-6-phosphate;MHC, major histocompatibility complex; SEAP, secreted alkalinphosphatase; STxB, Shiga toxin B subunit; STxB-sulf, STxB withsulfation sites; Tf, transferrin; TfR, Tf receptor; TRITC, tetramethylrhodamine isothiocyanate; VSV, vesicular stomatis virus.

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Hickson, G. R.X., Matheson, J., Riggs, B., Maier, V. H., Fielding, A. B., Prekeris, R., Sullivan, W., Barr, F. A., Gould, G. W. (2003). Arfophilins Are Dual Arf/Rab 11 Binding Proteins That Regulate Recycling Endosome Distribution and Are Related to Drosophila Nuclear Fallout. Mol. Biol. Cell 14: 2908-2920 [Abstract] [Full Text]
Dollar, G., Struckhoff, E., Michaud, J., Cohen, R. S. (2003). Rab11 polarization of the Drosophila oocyte: a novel link between membrane trafficking, microtubule organization, and oskar mRNA localization and translation. Development 129: 517-526 [Abstract] [Full Text]
Mannova, P., Forstova, J. (2003). Mouse Polyomavirus Utilizes Recycling Endosomes for a Traffic Pathway Independent of COPI Vesicle Transport. J. Virol. 77: 1672-1681 [Abstract] [Full Text]
Grimberg, E., Peng, Z., Hammel, I., Sagi-Eisenberg, R. (2003). Synaptotagmin III is a critical factor for the formation of the perinuclear endocytic recycling compartment and determination of secretory granules size. J. Cell Sci. 116: 145-154 [Abstract] [Full Text]
van Dam, E. M., ten Broeke, T., Jansen, K., Spijkers, P., Stoorvogel, W. (2002). Endocytosed Transferrin Receptors Recycle via Distinct Dynamin and Phosphatidylinositol 3-Kinase-dependent Pathways. J. Biol. Chem. 277: 48876-48883 [Abstract] [Full Text]
Meyers, J. M., Prekeris, R. (2002). Formation of Mutually Exclusive Rab11 Complexes with Members of the Family of Rab11-interacting Proteins Regulates Rab11 Endocytic Targeting and Function. J. Biol. Chem. 277: 49003-49010 [Abstract] [Full Text]
Wulfkuhle, J. D., Sgroi, D. C., Krutzsch, H., McLean, K., McGarvey, K., Knowlton, M., Chen, S., Shu, H., Sahin, A., Kurek, R., Wallwiener, D., Merino, M. J., Petricoin, E. F. III, Zhao, Y., Steeg, P. S. (2002). Proteomics of Human Breast Ductal Carcinoma in Situ. Cancer Res. 62: 6740-6749 [Abstract] [Full Text]
Holtta-Vuori, M., Tanhuanpaa, K., Mobius, W., Somerharju, P., Ikonen, E. (2002). Modulation of Cellular Cholesterol Transport and Homeostasis by Rab11. Mol. Biol. Cell 13: 3107-3122 [Abstract] [Full Text]
Lindsay, A. J., McCaffrey, M. W. (2002). Rab11-FIP2 Functions in Transferrin Recycling and Associates with Endosomal Membranes via Its COOH-terminal Domain. J. Biol. Chem. 277: 27193-27199 [Abstract] [Full Text]
Johannes, L. (2002). The Epithelial Cell Cytoskeleton and Intracellular Trafficking: I. Shiga toxin B-subunit system: retrograde transport, intracellular vectorization, and more. Am. J. Physiol. Gastrointest. Liver Physiol. 283: G1-G7 [Abstract] [Full Text]
Zeigerer, A., Lampson, M. A., Karylowski, O., Sabatini, D. D., Adesnik, M., Ren, M., McGraw, T. E. (2002). GLUT4 Retention in Adipocytes Requires Two Intracellular Insulin-regulated Transport Steps. Mol. Biol. Cell 13: 2421-2435 [Abstract] [Full Text]
Savina, A., Vidal, M., Colombo, M. I. (2002). The exosome pathway in K562 cells is regulated by Rab11. J. Cell Sci. 115: 2505-2515 [Abstract] [Full Text]
Lindsay, A. J., Hendrick, A. G., Cantalupo, G., Senic-Matuglia, F., Goud, B., Bucci, C., McCaffrey, M. W. (2002). Rab Coupling Protein (RCP), a Novel Rab4 and Rab11 Effector Protein. J. Biol. Chem. 277: 12190-12199 [Abstract] [Full Text]
Rosenfeld, J. L., Moore, R. H., Zimmer, K.-P., Alpizar-Foster, E., Dai, W., Zarka, M. N., Knoll, B. J. (2002). Lysosome proteins are redistributed during expression of a GTP-hydrolysis-defective rab5a. J. Cell Sci. 114: 4499-4508 [Abstract] [Full Text]
Jeffries, T. R., Morgan, G. W., Field, M. C. (2002). A developmentally regulated Rab11 homologue in Trypanosoma brucei is involved in recycling processes. J. Cell Sci. 114: 2617-2626 [Abstract] [Full Text]
Inaba, T., Nagano, Y., Nagasaki, T., Sasaki, Y. (2002). Distinct Localization of Two Closely Related Ypt3/Rab11 Proteins on the Trafficking Pathway in Higher Plants. J. Biol. Chem. 277: 9183-9188 [Abstract] [Full Text]
Mallard, F., Tang, B. L., Galli, T., Tenza, D., Saint-Pol, A., Yue, X., Antony, C., Hong, W., Goud, B., Johannes, L. (2002). Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform. JCB 156: 653-664 [Abstract] [Full Text]
Perez, F., Pernet-Gallay, K., Nizak, C., Goodson, H. V., Kreis, T. E., Goud, B. (2002). CLIPR-59, a new trans-Golgi/TGN cytoplasmic linker protein belonging to the CLIP-170 family. JCB 156: 631-642 [Abstract] [Full Text]
Lauvrak, S. U., Llorente, A., Iversen, T.-G., Sandvig, K. (2002). Selective regulation of the Rab9-independent transport of ricin to the Golgi apparatus by calcium. J. Cell Sci. 115: 3449-3456 [Abstract] [Full Text]
Tarabal, O., Caldero, J., Llado, J., Oppenheim, R. W., Esquerda, J. E. (2001). Long-Lasting Aberrant Tubulovesicular Membrane Inclusions Accumulate in Developing Motoneurons after a Sublethal Excitotoxic Insult: A Possible Model for Neuronal Pathology in Neurodegenerative Disease. J. Neurosci. 21: 8072-8081 [Abstract] [Full Text]
Prekeris, R., Davies, J. M., Scheller, R. H. (2001). Identification of a Novel Rab11/25 Binding Domain Present in Eferin and Rip Proteins. J. Biol. Chem. 276: 38966-38970 [Abstract] [Full Text]
Mallard, F., Tang, B. L., Galli, T., Tenza, D., Saint-Pol, A., Yue, X., Antony, C., Hong, W., Goud, B., Johannes, L. (2002). Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform. JCB 156: 653-664 [Abstract] [Full Text]