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

Sheff, David R., Daro, Elizabeth A., Hull, Michael, Mellman, Ira·1999·The Journal of Cell Biology
DOI 10.1083/jcb.145.1.123PMC PMC2148223
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Abstract

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.

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  • Previous studies have revealed heterogeneity in recycling of different receptors: LDLR is transported along a RAB11-mediated slow recycling pathway involving the endocytic recycling compartment, while TFR utilizes both RAB11- and RAB4-mediated rapid recycling pathways.

    “Previous studies have revealed heterogeneity in the recycling of different receptors, with some, including LDLR, transported along a RAB11-mediated slow recycling pathway involving the endocytic recycling compartment, while others, including TFR, utilize both RAB11- and RAB4-mediated rapid recycling pathways (20, 42, 43).”

    From The small GTPase RAB10 regulates endosomal recycling of the LDL receptor and transferrin receptor in hepatocytes (2022) · cites this paper as [43]

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  • Internalized receptors recycle to the plasma membrane via two distinct pathways: Rab4 regulates fast recycling from early endosomes to the cell surface, and Rab11 mediates slow recycling from perinuclear recycling vesicles to the plasma membrane.

    “Upon delivery to the early endosomes, internalized receptors then recycle to the plasma membrane via two distinct recycling pathways: Rab4 regulates fast recycling from early endosomes to the cell surface (Sheff et al., 1999), whereas Rab11 plays a role in slow recycling from perinuclear recycling vesicles back to the plasma membrane.”

    From BDNF-Dependent Recycling Facilitates TrkB Translocation to Postsynaptic Density during LTP via a Rab11-Dependent Pathway (2013) · cites this paper as Sheff et al., 1999

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Metadata

Authors
Sheff, D. R., Daro, E. A., Hull, M., & Mellman, I.
Affiliations
Department of Cell Biology, Yale University School of Medicine, New Haven, Connecticut 06520-8002
Venue
The Journal of Cell Biology
Publisher
Rockefeller University Press
Published
1999-04-05
Volume
145
Issue
1
Pages
123-139
ISSN
  • 0021-9525
  • 1540-8140
DOI
10.1083/jcb.145.1.123
PMC
PMC2148223
Cited by
399
References
2
Language
en

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