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© The Rockefeller University Press, 0021-9525/1999//123 $5.00
The Journal of Cell Biology, Volume 145, Number 1, , 1999 123-139

The Receptor Recycling Pathway Contains Two Distinct Populations of Early Endosomes with Different Sorting Functions

Department of Cell Biology, Yale University School of Medicine, New Haven, Connecticut 06520-8002

Receptor recycling involves two endosome populations, peripheral early endosomes and perinuclear recycling endosomes. In polarized epithelial cells, either or both populations must be able to sort apical from basolateral proteins, returning each to its appropriate plasma membrane domain. However, neither the roles of early versus recycling endosomes in polarity nor their relationship to each other has been quantitatively evaluated. Using a combined morphological, biochemical, and kinetic approach, we found these two endosome populations to represent physically and functionally distinct compartments. Early and recycling endosomes were resolved on Optiprep gradients and shown to be differentially associated with rab4, rab11, and transferrin receptor; rab4 was enriched on early endosomes and at least partially depleted from recycling endosomes, with the opposite being true for rab11 and transferrin receptor. The two populations were also pharmacologically distinct, with AlF₄ selectively blocking export of transferrin receptor from recycling endosomes to the basolateral plasma membrane. We applied these observations to a detailed kinetic analysis of transferrin and dimeric IgA recycling and transcytosis. The data from these experiments permitted the construction of a testable, mathematical model which enabled a dissection of the roles of early and recycling endosomes in polarized receptor transport. Contrary to expectations, the majority (>65%) of recycling to the basolateral surface is likely to occur from early endosomes, but with relatively little sorting of apical from basolateral proteins. Instead, more complete segregation of basolateral receptors from receptors intended for transcytosis occurred upon delivery to recycling endosomes.

Key Words: sorting • endosomes • receptor recycling

Abbreviations used in this paper: dIgA, dimeric IgA; EE, early endosome; LE, late endosome; pIgR, polymeric immunoglobulin receptor; RE, recycling endosome; Tfn, transferrin.

Elizabeth A. Daro's current address is Immunex, 51 University St., Seattle, WA 98101.

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• 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]  
• Kolesnikova, L., Bugany, H., Klenk, H.-D., Becker, S. (2002). VP40, the Matrix Protein of Marburg Virus, Is Associated with Membranes of the Late Endosomal Compartment. J. Virol. 76: 1825-1838 [Abstract] [Full Text]  
• Peng, Z., Grimberg, E., Sagi-Eisenberg, R. (2002). Suppression of Synaptotagmin II restrains phorbolester-induced downregulation of protein kinase C{alpha} by diverting the kinase from a degradative pathway to the recycling endocytic compartment. J. Cell Sci. 115: 3083-3092 [Abstract] [Full Text]  
• de Wit, H., Lichtenstein, Y., Kelly, R. B., Geuze, H. J., Klumperman, J., van der Sluijs, P. (2001). Rab4 Regulates Formation of Synaptic-like Microvesicles from Early Endosomes in PC12 Cells. Mol. Biol. Cell 12: 3703-3715 [Abstract] [Full Text]  
• Wu, C., Lai, C.-F., Mobley, W. C. (2001). Nerve Growth Factor Activates Persistent Rap1 Signaling in Endosomes. J. Neurosci. 21: 5406-5416 [Abstract] [Full Text]  
• Wissel, H., Lehfeldt, A., Klein, P., Muller, T., Stevens, P. A. (2001). Endocytosed SP-A and surfactant lipids are sorted to different organelles in rat type II pneumocytes. Am. J. Physiol. Lung Cell. Mol. Physiol. 281: L345-L360 [Abstract] [Full Text]  
• Puertollano, R., Martinez-Menarguez, J. A., Batista, A., Ballesta, J., Alonso, M. A. (2001). An Intact Dilysine-like Motif in the Carboxyl Terminus of MAL Is Required for Normal Apical Transport of the Influenza Virus Hemagglutinin Cargo Protein in Epithelial Madin-Darby Canine Kidney Cells. Mol. Biol. Cell 12: 1869-1883 [Abstract] [Full Text]  
• Galan, J.-M., Wiederkehr, A., Seol, J. H., Haguenauer-Tsapis, R., Deshaies, R. J., Riezman, H., Peter, M. (2001). Skp1p and the F-Box Protein Rcy1p Form a Non-SCF Complex Involved in Recycling of the SNARE Snc1p in Yeast. Mol. Cell. Biol. 21: 3105-3117 [Abstract] [Full Text]  
• Straight, S. W., Chen, L., Karnak, D., Margolis, B. (2001). Interaction with mLin-7 Alters the Targeting of Endocytosed Transmembrane Proteins in Mammalian Epithelial Cells. Mol. Biol. Cell 12: 1329-1340 [Abstract] [Full Text]  
• Parker, J. S. L., Murphy, W. J., Wang, D., O'Brien, S. J., Parrish, C. R. (2001). Canine and Feline Parvoviruses Can Use Human or Feline Transferrin Receptors To Bind, Enter, and Infect Cells. J. Virol. 75: 3896-3902 [Abstract] [Full Text]  

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