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

Wilcke, Mona, Johannes, Ludger, Galli, Thierry, Mayau, Véronique, Goud, Bruno, Salamero, Jean·2000·The Journal of Cell Biology

Abstract

Several GTPases of the Rab family, known to be regulators of membrane traffic between organelles, have been described and localized to various intracellular compartments. Rab11 has previously been reported to be associated with the pericentriolar recycling compartment, post-Golgi vesicles, and the trans-Golgi network (TGN). We compared the effect of overexpression of wild-type and mutant forms of Rab11 on the different intracellular transport steps in the endocytic/degradative and the biosynthetic/exocytic pathways in HeLa cells. We also studied transport from endosomes to the Golgi apparatus using the Shiga toxin B subunit (STxB) and TGN38 as reporter molecules. Overexpression of both Rab11 wild-type (Rab11wt) and mutants altered the localization of the transferrrin receptor (TfR), internalized Tf, the STxB, and TGN38. In cells overexpressing Rab11wt and in a GTPase-deficient Rab11 mutant (Rab11Q70L), these proteins were found in vesicles showing characteristics of sorting endosomes lacking cellubrevin (Cb). In contrast, they were redistributed into an extended tubular network, together with Cb, in cells overexpressing a dominant negative mutant of Rab11 (Rab11S25N). This tubularized compartment 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 inhibited STxB and TGN38 transport from endosomes to the TGN. These results suggest that Rab11 influences endosome to TGN trafficking primarily by regulating membrane distribution inside the early endosomal pathway.

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Research works printed but not linked: 68

  1. Antony, 1992, The small GTP-binding protein rab6p is distributed from medial Golgi to the trans-Golgi network as determined by a confocal microscopic approach, J. Cell Sci, 103, 785, 10.1242/jcs.103.3.785 · DOI
  2. Benli, 1996, Two GTPase isoforms, Ypt31p and Ypt32p, are essential for Golgi function in yeast, EMBO (Eur. Mol. Biol. Organ.) J., 15, 6460, 10.1002/j.1460-2075.1996.tb01037.x · DOI
  3. Bhakdi, 1993, A guide to the use of pore-forming toxins for controlled permeabilization of cell membranes, Med. Microbiol. Immunol, 182, 167, 10.1007/BF00219946 · DOI
  4. Bos, 1993, TGN38 is maintained in the trans-Golgi network by a tyrosine-containing motif in the cytoplasmic domain, EMBO (Eur. Mol. Biol. Organ.) J., 12, 2219, 10.1002/j.1460-2075.1993.tb05870.x · DOI
  5. Chapman, 1994, Retrieval of TGN proteins from the cell surface requires endosomal acidification, EMBO (Eur. Mol. Biol. Organ.) J., 13, 2305, 10.1002/j.1460-2075.1994.tb06514.x · DOI
  6. Chavrier, 1999, The role of ARF and Rab GTPases in membrane transport, Curr. Opin. Cell Biol., 11, 466, 10.1016/S0955-0674(99)80067-2 · DOI
  7. Chavrier, 1990, Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments, Cell, 62, 317, 10.1016/0092-8674(90)90369-P · DOI · Paper page
  8. Cole, 1995, Organization of organelles and membrane traffic by microtubules, Curr. Opin. Cell Biol., 7, 55, 10.1016/0955-0674(95)80045-X · DOI
  9. Colley, 1992, The signal anchor and stem regions of the beta-galactoside alpha 2,6-sialyltransferase may each act to localize the enzyme to the Golgi apparatus, J. Biol. Chem., 267, 7784, 10.1016/S0021-9258(18)42583-5 · DOI
  10. Cresswell, 1994, Assembly, transport, and function of MHC class II molecules, Annu. Rev. Immunol., 12, 259, 10.1146/annurev.iy.12.040194.001355 · DOI
  11. Dahdal, 1993, Specific sequences in the signal anchor of the beta-galactoside alpha-2,6-sialyltransferase are not essential for Golgi localization. Membrane flanking sequences may specify Golgi retention, J. Biol. Chem., 268, 26310, 10.1016/S0021-9258(19)74316-6 · DOI
  12. Fishman, 1987, A trans Golgi-derived exocytic coated vesicle can contain both newly synthesized cholinesterase and internalized transferrin, Cell., 48, 157, 10.1016/0092-8674(87)90366-7 · DOI
  13. Fuerst, 1986, Eukaryotic transcient-expression system based on recombinant vaccinia virus that synthetizes bacteriophage T7 RNA polymerase, Proc. Natl. Acad. Sci. USA, 83, 8122, 10.1073/pnas.83.21.8122 · DOI
  14. Galli, 1994, Tetanus toxin–mediated cleavage of cellubrevin impairs exocytosis of transferrin receptor–containing vesicles in CHO cells, J. Cell Biol., 125, 1015, 10.1083/jcb.125.5.1015 · DOI
  15. Galli, 1998, A novel tetanus neurotoxin-insensitive vesicle-associated membrane protein in SNARE complexes of the apical plasma membrane of epithelial cells, Mol. Biol. Cell., 9, 1437, 10.1091/mbc.9.6.1437 · DOI
  16. Ghosh, 1995, Evidence for nonvectorial retrograde transferrin trafficking in the early endosomes of HEp2 cells, J. Cell Biol., 128, 549, 10.1083/jcb.128.4.549 · DOI
  17. Ghosh, 1994, Quantification of low density lipoprootein and transferrin endocytic sorting in HEp2 cells using confocal microscopy, J. Cell Sci., 107, 2177, 10.1242/jcs.107.8.2177 · DOI · Paper page
  18. Ghosh, 1998, An endocytosed TGN38 chimeric protein is delivered to the TGN after trafficking through the endocytic recycling compartment in CHO cells, J. Cell Biol., 142, 923, 10.1083/jcb.142.4.923 · DOI
  19. Goldenring, 1994, Enrichment of rab11, a small GTP-binding protein, in gastric parietal cells, Am. J. Physiol., 267, G187
  20. Goud, 1990, Small GTP-binding protein associated with Golgi cisternae, Nature, 345, 553, 10.1038/345553a0 · DOI
  21. Gruenberg, 1989, Characterization of the early endosome and putative endocytic carrier vesicles in vivo with an assay of vesicle fusion in vitro, J. Cell Biol., 108, 1301, 10.1083/jcb.108.4.1301 · DOI
  22. Guy, 1982, Differential expression and serologically distinct subpopulations of human Ia antigens detected with monoclonal antibodies to Ia alpha and beta chains, Eur. J. Immunol, 12, 942, 10.1002/eji.1830121109 · DOI
  23. Hopkins, 1990, Movement of internalized ligand-receptor complexes along a continuous endosomal reticulum, Nature., 339, 335, 10.1038/346335a0 · DOI
  24. Hopkins, 1994, In migrating fibroblasts, recycling receptors are concentrated in narrow tubules in the pericentriolar area, and then routed to the plasma membrane of the leading lamella, J. Cell Biol., 125, 1265, 10.1083/jcb.125.6.1265 · DOI
  25. Humphrey, 1993, Localization of TGN38 to the trans-Golgi networkinvolvement of a cytoplasmic tyrosine–containing sequence, J. Cell Biol, 120, 1123, 10.1083/jcb.120.5.1123 · DOI
  26. Jasmin, 1989, Golgi apparatus in chick skeletal musclechanges in its distribution during end plate development and after denervation, Proc. Natl. Acad. Sci. USA., 86, 7218, 10.1073/pnas.86.18.7218 · DOI
  27. Jedd, 1997, Two new Ypt GTPases are required for exit from the yeast trans-Golgi compartment, J. Cell Biol, 137, 563, 10.1083/jcb.137.3.563 · DOI
  28. Johannes, 1998, Surfing on a retrograde wavehow does Shiga toxin reach the endoplasmic reticulum?, Trends Cell Biol, 8, 158, 10.1016/S0962-8924(97)01209-9 · DOI
  29. Johannes, 1997, Retrograde transport of KDEL-bearing B-subunit of Shiga toxin, J. Biol. Chem, 272, 19554, 10.1074/jbc.272.31.19554 · DOI
  30. Kornfeld, 1992, Structure and function of the mannose-6-phosphate/insulin-like growth factor receptors, Annu. Rev. Biochem., 61, 307, 10.1146/annurev.bi.61.070192.001515 · DOI
  31. Ladinsky, 1992, The trans-Golgi network can be dissected structurally and functionally from the cisternae of the Golgi complex by brefeldin A, Eur. J. Cell Biol, 59, 92
  32. Luzio, 1990, Identification, sequencing and expression of an integral membrane protein of the trans-Golgi network (TGN38), Biochem. J, 270, 97, 10.1042/bj2700097 · DOI
  33. Lutcke, 1993, Rab17, a novel small GTPase, is specific for epithelial cells and is induced during cell polarization, J. Cell Biol, 121, 553, 10.1083/jcb.121.3.553 · DOI
  34. Lutcke, 1994, Cloning and subcellular localization of novel rab proteins reveals polarized and cell type-specific expression, J. Cell Sci., 107, 3437, 10.1242/jcs.107.12.3437 · DOI
  35. Mallard, 1998, Direct pathway from early/recycling endosomes to the Golgi apparatus revealed through the study of shiga toxin B-fragment transport, J. Cell Biol, 143, 973, 10.1083/jcb.143.4.973 · DOI
  36. Martinez, 1994, The small GTP-binding protein rab6 functions in intra-Golgi transport, J. Cell Biol, 127, 1575, 10.1083/jcb.127.6.1575 · DOI
  37. Martinez, 1997, GTP-bound forms of rab6 induce the redistribution of Golgi proteins into the endoplasmic reticulum, Proc. Natl. Acad. Sci. USA., 94, 1828, 10.1073/pnas.94.5.1828 · DOI
  38. Mayor, 1993, Sorting of membrane components from endosomes and subsequent recycling to the cell surface occurs by a bulk flow process, J. Cell Biol, 121, 1257, 10.1083/jcb.121.6.1257 · DOI · Paper page
  39. McMahon, 1993, Cellubrevin is a ubiquitous tetanus-toxin substrate homologous to a putative synaptic vesicle fusion protein, Nature, 364, 346, 10.1038/364346a0 · DOI
  40. Niehrs, 1990, Purification and characterization of tyrosylprotein sulfotransferase, EMBO (Eur. Mol. Biol. Organ.) J., 9, 35, 10.1002/j.1460-2075.1990.tb08077.x · DOI
  41. Novick, 1997, The diversity of Rab proteins in vesicle transport, Curr. Opin. Cell Biol., 9, 496, 10.1016/S0955-0674(97)80025-7 · DOI
  42. Nuoffer, 1994, A GDP-bound of rab 1 inhibits protein export from the endoplasmic reticulum and transport between Golgi compartments, J. Cell Biol, 125, 225, 10.1083/jcb.125.2.225 · DOI
  43. O'Brien, 1992, Shiga toxinbiochemistry, genetics, mode of action, and role in pathogenesis, Curr. Top. Microbiol. Immunol., 180, 65
  44. Rabouille, 1995, Mapping the distribution of Golgi enzymes involved in the construction of complex oligosaccharides, J. Cell Sci., 108, 1617, 10.1242/jcs.108.4.1617 · DOI
  45. Ren, 1998, Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes, Proc. Natl. Acad. Sci. USA., 95, 6187, 10.1073/pnas.95.11.6187 · DOI · Paper page
  46. Reaves, 1993, TGN38/41 recycles between the cell surface and the TGNbrefeldin A affects its rate of return to the TGN, Mol. Biol. Cell, 4, 93, 10.1091/mbc.4.1.93 · DOI
  47. Riberdy, 1994, Transport and intracellular distribution of MHC class II molecules and associated invariant chain in normal and antigen-processing mutant cell lines, J. Cell Biol, 125, 1225, 10.1083/jcb.125.6.1225 · DOI
  48. Riederer, 1994, Lysosome biogenesis requires rab9 function and receptor recycling from endosomes to the trans-Golgi network, J. Cell Biol., 125, 573, 10.1083/jcb.125.3.573 · DOI
  49. Roth, 1985, Demonstration of an extensive trans-tubular network continuous with the Golgi apparatus stack that may function in glycosylation, Cell., 43, 287, 10.1016/0092-8674(85)90034-0 · DOI · Paper page
  50. Salamero, 1990, Mouse B lymphocyte specific endocytosis and recycling of MHC class II molecules, EMBO (Eur. Mol. Biol. Organ.) J., 9, 3489, 10.1002/j.1460-2075.1990.tb07557.x · DOI
  51. Salamero, 1996, Expression of major histocompatibility complex class II molecules in HeLa cells promotes the recruitment of AP-1 Golgi-specific assembly proteins on Golgi membranes, J. Biol. Chem, 271, 30318, 10.1074/jbc.271.48.30318 · DOI
  52. Sandvig, 1996, Endocytosis, intracellular transport, and cytotoxic action of Shiga toxin and ricin, Physiol. Rev., 76, 949, 10.1152/physrev.1996.76.4.949 · DOI
  53. Sandvig, 1991, Endocytosis and intracellular transport of the glycolipid-binding ligand Shiga toxin in polarized MDCK cells, J. Cell Biol, 113, 553, 10.1083/jcb.113.3.553 · DOI
  54. Sandvig, 1992, Retrograde transport of endocytosed Shiga toxin to the endoplasmic reticulum, Nature, 358, 510, 10.1038/358510a0 · DOI
  55. Saudrais, 1998, Intracellular pathway for the generation of functional MHC class II peptide complexes in immature human dendritic cells, J. Immunol, 160, 2597, 10.4049/jimmunol.160.6.2597 · DOI
  56. Sheff, 1999, The receptor recycling pathway contains two distinct populations of early endosomes with different sorting functions, J. Cell Biol, 145, 123, 10.1083/jcb.145.1.123 · DOI · Paper page
  57. Snider, 1985, Intracellular movement of cell surface receptors after endocytosisresialylation of asialo-transferrin receptor in human erythroleukemia cells, J. Cell Biol, 100, 826, 10.1083/jcb.100.3.826 · DOI
  58. Sönnichsen, 2000, Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11, J. Cell Biol., 149, 901, 10.1083/jcb.149.4.901 · DOI · Paper page
  59. Teter, 1998, Cellubrevin-targeted fluorescence uncovers heterogeneity in the recycling endosomes, J. Biol. Chem., 273, 19625, 10.1074/jbc.273.31.19625 · DOI
  60. Tisdale, 1996, Rab2 is essential for the maturation of pre-Golgi intermediates, J. Biol. Chem, 271, 29372, 10.1074/jbc.271.46.29372 · DOI
  61. Ullrich, 1996, Rab11 regulates recycling through the pericentriolar recycling endosome, J. Cell Biol, 135, 913, 10.1083/jcb.135.4.913 · DOI · Paper page
  62. Urbe, 1993, Rab11, a small GTPase associated with both constitutive and regulated secretory pathways in PC12 cells, FEBS Lett., 334, 175, 10.1016/0014-5793(93)81707-7 · DOI
  63. Van der Sluijs, 1991, The small GTP-binding protein rab4 is associated with early endosomes, Proc. Natl. Acad. Sci. USA., 88, 6313, 10.1073/pnas.88.14.6313 · DOI
  64. Van der Sluijs, 1992, The small GTP-binding protein rab4 controls an early sorting event on the endocytic pathway, Cell., 70, 729, 10.1016/0092-8674(92)90307-X · DOI
  65. Wei, 1998, GLUT4 and transferrin receptor are differentially sorted along the endocytic pathway in CHO cells, J. Cell Biol., 140, 565, 10.1083/jcb.140.3.565 · DOI
  66. Wong, 1993, The SXYQRL sequence in the cytoplasmic domain of TGN38 plays a major role in trans-Golgi network localization, J. Biol. Chem., 268, 22853, 10.1016/S0021-9258(18)41606-7 · DOI
  67. Yamashiro, 1984, Segregation of transferrin to a mildly acidic (pH 6.5) para-Golgi compartment in the recycling pathway, Cell., 37, 789, 10.1016/0092-8674(84)90414-8 · DOI
  68. Yoshimori, 1996, Different biosynthetic transport routes to the plasma membrane in BHK and CHO cells, J. Cell Biol, 133, 247, 10.1083/jcb.133.2.247 · DOI

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Metadata

Authors
Wilcke, M., Johannes, L., Galli, T., Mayau, V., Goud, B., & Salamero, J.
Affiliations
  • aUMR CNRS 144, Laboratoire Mécanismes Moléculaires du Transport Intracellulaire, Institut Curie, F-75248 Paris Cedex 05, France
  • bUnité de Génétique Somatique, URA CNRS 1960, Institut Pasteur, 75724 Paris Cedex 15, France
Venue
The Journal of Cell Biology
Published
2000-12-11
Volume
151
Issue
6
Pages
1207-1220
ISSN
  • 0021-9525
  • 1540-8140
Cited by
360
References
0
Language
en

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