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Distinct Membrane Domains on Endosomes in the Recycling Pathway Visualized by Multicolor Imaging of Rab4, Rab5, and Rab11

Sönnichsen, Birte, De Renzis, Stefano, Nielsen, Erik, Rietdorf, Jens, Zerial, Marino·2000·The Journal of Cell Biology

Abstract

Two endosome populations involved in recycling of membranes and receptors to the plasma membrane have been described, the early and the recycling endosome. However, this distinction is mainly based on the flow of cargo molecules and the spatial distribution of these membranes within the cell. To get insights into the membrane organization of the recycling pathway, we have studied Rab4, Rab5, and Rab11, three regulatory components of the transport machinery. Following transferrin as cargo molecule and GFP-tagged Rab proteins we could show that cargo moves through distinct domains on endosomes. These domains are occupied by different Rab proteins, revealing compartmentalization within the same continuous membrane. Endosomes are comprised of multiple combinations of Rab4, Rab5, and Rab11 domains that are dynamic but do not significantly intermix over time. Three major populations were observed: one that contains only Rab5, a second with Rab4 and Rab5, and a third containing Rab4 and Rab11. These membrane domains display differential pharmacological sensitivity, reflecting their biochemical and functional diversity. We propose that endosomes are organized as a mosaic of different Rab domains created through the recruitment of specific effector proteins, which cooperatively act to generate a restricted environment on the membrane.

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Crossref · 10.1083/jcb.149.4.901

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  • SNX17 is present on a subset of early endosomal structures that might define a distinct organelle in a mosaic of membrane domains characterized by the presence of EEA1, rab5, rab4, rab7 and rab11.

    “demonstrating that SNX17 is present on a subset of early endosomal structures that might define a distinct organelle in a mosaic of membrane domains characterized by the presence of EEA1, rab5, rab4, rab7 and rab11 (Sonnichsen et al ., 2000).”

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Research works printed but not linked: 49

  1. Besterman, 1981, Exocytosis of pinocytosed fluid in cultured cellskinetic evidence for rapid turnover and compartmentation, J. Cell Biol., 91, 716, 10.1083/jcb.91.3.716 · DOI
  2. Brown, 1993, ADP-ribosylation factor, a small GTP-dependent regulatory protein stimulates phospholipase D activity, Cell, 75, 1137, 10.1016/0092-8674(93)90323-I · DOI
  3. Bucci, 1992, The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway, Cell, 70, 715, 10.1016/0092-8674(92)90306-W · DOI
  4. Calhoun, 1998, Rab11a redistributes to apical secretory canaliculus during stimulation of gastric parietal cells, Am. J. Physiol., 275, C163, 10.1152/ajpcell.1998.275.1.C163 · DOI
  5. Chen, 1998, Rab11 is required for trans-Golgi network-to-plasma membrane transport and a preferential target for GDP dissociation inhibitor, Mol. Biol. Cell, 9, 3241, 10.1091/mbc.9.11.3241 · DOI
  6. Christoforidis, 1999, Phosphoinositide-3-kinases are Rab5 effectors, Nat. Cell Biol., 4, 249, 10.1038/12075 · DOI · Paper page
  7. Donaldson, 1992, Brefeldin A inhibits Golgi membrane-catalyzed exchange of guanine nucleotide onto ARF protein, Nature, 360, 350, 10.1038/360350a0 · DOI
  8. Dunn, 1989, Iterative fractionation of recycling receptors from lysosomally destined ligands in an early sorting endosome, J. Cell Biol, 109, 3303, 10.1083/jcb.109.6.3303 · DOI · Paper page
  9. Echard, 1998, Interaction of a Golgi-associated kinesin-like protein with Rab6, Science, 279, 580, 10.1126/science.279.5350.580 · DOI
  10. Ghosh, 1994, Quantification of low-density lipoprotein and transferrin endocytic sorting in Hep2 cells, J. Cell Biol., 128, 549, 10.1083/jcb.128.4.549 · DOI
  11. 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
  12. Gorvel, 1991, Rab5 controls early endosome fusion in vitro, Cell, 64, 915, 10.1016/0092-8674(91)90316-Q · DOI
  13. Griffiths, 1989, A quantitative analysis of the endocytic pathway in baby hamster kidney cells, J. Cell Biol, 109, 2703, 10.1083/jcb.109.6.2703 · DOI
  14. Gruenberg, 1995, Membrane transport in the endocytic pathway, Curr. Opin. Cell Biol., 7, 552, 10.1016/0955-0674(95)80013-1 · DOI
  15. Guo, 1999, The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis, EMBO (Eur. Mol. Biol. Organ.) J., 18, 1071, 10.1093/emboj/18.4.1071 · DOI
  16. Hopkins, 1983, Intracellular routing of transferrin and transferrin receptors in epidermoid carcinoma A431 cells, Cell, 35, 321, 10.1016/0092-8674(83)90235-0 · DOI
  17. Hopkins, 1990, Movement of internalized ligand-receptor complexes along a continuous endosomal reticulum, Nature, 346, 335, 10.1038/346335a0 · DOI
  18. Horiuchi, 1995, A GDP/GTP exchange-stimulatory activity for the Rab5–RabGDI complex on clathrin-coated vesicles from bovine brain, J. Biol. Chem., 270, 11257, 10.1074/jbc.270.19.11257 · DOI
  19. Horiuchi, 1997, A novel Rab5 GDP/GTP exchange factor complexed to Rabaptin-5 links nucleotide exchange to effector recruitment and function, Cell, 90, 1149, 10.1016/S0092-8674(00)80380-3 · DOI
  20. 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
  21. Lippincott-Schwartz, 1991, Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic, Cell, 67, 601, 10.1016/0092-8674(91)90534-6 · DOI
  22. Lütcke, 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
  23. 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
  24. McLauchlan, 1998, A novel role for Rab5-GDI in ligand sequestration into clathrin-coated pits, Curr. Biol, 8, 34, 10.1016/S0960-9822(98)70018-1 · DOI
  25. Mellman, 1996, Endocytosis and molecular sorting, Annu. Rev. Cell Dev. Biol., 12, 575, 10.1146/annurev.cellbio.12.1.575 · DOI
  26. Mills, 1998, Involvement of the endosomal autoantigen EEA1 in homotypic fusion of early endosomes, Curr. Biol., 8, 881, 10.1016/S0960-9822(07)00351-X · DOI
  27. Mu, 1995, EEA1, an early endosome-associated protein, J. Biol. Chem., 270, 13503, 10.1074/jbc.270.22.13503 · DOI
  28. Nielsen, 1999, Rab5 regulates motility of early endosomes on microtubules, Nat. Cell Biol., 1, 376, 10.1038/14075 · DOI
  29. Novick, 1997, The diversity of Rab proteins in vesicle transport, Curr. Opin. Cell Biol., 9, 496, 10.1016/S0955-0674(97)80025-7 · DOI
  30. Olkkonen, 1993, Molecular cloning and subcellular localization of 3 GTP-binding proteins of the rab subfamily, J. Cell Sci, 106, 1249, 10.1242/jcs.106.4.1249 · DOI
  31. Patki, 1997, Identification of an early endosomal protein regulated by phosphatidylinositol 3-kinase, Proc. Natl. Acad. Sci. USA, 94, 7326, 10.1073/pnas.94.14.7326 · DOI
  32. Pfeffer, 1994, Rab GTPasesmaster regulators of membrane trafficking, Curr. Opin. Cell Biol., 6, 522, 10.1016/0955-0674(94)90071-X · DOI
  33. 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
  34. Schmid, 1988, Two distinct subpopulations of endosomes involved in membrane recycling and transport to lysosomes, Cell, 52, 73, 10.1016/0092-8674(88)90532-6 · DOI
  35. Schu, 1993, Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting, Science, 260, 88, 10.1126/science.8385367 · DOI · Paper page
  36. Sheff, 1999, The 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
  37. Simonsen, 1998, EEA1 links phosphatidylinositol 3-kinase function to Rab5 regulation of endosome fusion, Nature, 394, 494, 10.1038/28879 · DOI · Paper page
  38. Sipe, 1987, High resolution acidification kinetics of transferrin in Balb/c 3T3 cellsexposure to pH 6 followed by temperature-sensitive alkalization during recycling, Proc. Natl. Acad. Sci. USA, 84, 7119, 10.1073/pnas.84.20.7119 · DOI
  39. Spiro, 1996, Wortmannin alters the transferrin receptor endocytic pathway in vivo and in vitro, Mol. Biol. Cell, 7, 355, 10.1091/mbc.7.3.355 · DOI
  40. Stoorvogel, 1996, A novel class of clathrin-coated vesicles budding from endosomes, J. Cell Biol, 132, 21, 10.1083/jcb.132.1.21 · DOI
  41. Tooze, 1992, In AtT20 and HeLa cells brefeldin A induces the fusion of tubular endosomes and changes their distribution and some of their endocytic properties, J. Cell Biol., 118, 813, 10.1083/jcb.118.4.813 · DOI
  42. Trischler, 1999, Biochemical analysis of distinct Rab5- and Rab11-positive endosomes along the transferrin pathway, J. Cell Sci., 112, 4773, 10.1242/jcs.112.24.4773 · DOI · Paper page
  43. Ullrich, 1996, Rab11 regulates recycling through the pericentriolar recycling endosome, J. Cell Biol., 135, 913, 10.1083/jcb.135.4.913 · DOI · Paper page
  44. 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
  45. 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
  46. Vitale, 1998, Distinct Rab-binding domains mediate the interaction of Rabaptin-5 with GTP-bound rab4 and rab5, EMBO (Eur. Mol. Biol. Organ.) J., 17, 1941, 10.1093/emboj/17.7.1941 · DOI
  47. White, 1998, Recycling of Golgi resident glycosyltransferases through the ER reveals a novel pathway and provides an explanation for nocodazole-induced Golgi scattering, J. Cell Biol., 143, 1505, 10.1083/jcb.143.6.1505 · DOI
  48. 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
  49. Zacchi, 1998, Rab17 regulates membrane trafficking through apical recycling endosomes in polarized epithelial cells, J. Cell Biol, 140, 1039, 10.1083/jcb.140.5.1039 · DOI

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Metadata

Authors
Sönnichsen, B., De Renzis, S., Nielsen, E., Rietdorf, J., & Zerial, M.
Venue
The Journal of Cell Biology
Published
2000-05-15
Volume
149
Issue
4
Pages
901-914
ISSN
  • 0021-9525
  • 1540-8140
Cited by
919
References
4
Language
en

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