Home LiteratureArticle Details
PMID: 8922376 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Rab11 regulates recycling through the pericentriolar recycling endosome.

The Journal of cell biology ·Vol. 135 ·No. 4 ·1996-11-00 ·Pages 913-24

Ullrich O, Reinsch S, Urbé S, Zerial M, Parton RG

Abstract

Small GTPases of the rab family are crucial elements of the machinery that controls membrane traffic. In the present study, we examined the distribution and function of rab11. Rab11 was shown by confocal immunofluorescence microscopy and EM to colocalize with internalized transferrin in the pericentriolar recycling compartment of CHO and BHK cells. Expression of rab11 mutants that are preferentially in the GTP- or GDP-bound state caused opposite effects on the distribution of transferrin-containing elements; rab11-GTP expression caused accumulation of labeled elements in the perinuclear area of the cell, whereas rab11-GDP caused a dispersion of the transferrin labeling. Functional studies showed that the early steps of uptake and recycling for transferrin were not affected by overexpression of rab11 proteins. However, recycling from the later recycling endosome was inhibited in cells overexpressing the rab11-GDP mutant. Rab5, which regulates early endocytic trafficking, acted before rab11 in the transferrin-recycling pathway as expression of rab5-GTP prevented transport to the rab11-positive recycling endosome. These results suggest a novel role for rab11 in controlling traffic through the recycling endosome.

MeSH Terms
Animals Biological Transport/physiology CHO Cells/physiology Cell Compartmentation/physiology Centrioles/chemistry,enzymology,ultrastructure Cricetinae Endosomes/chemistry,enzymology,ultrastructure Escherichia coli/enzymology,genetics,ultrastructure GTP Phosphohydrolases/analysis,genetics,metabolism GTP-Binding Proteins/analysis,genetics,metabolism Gene Expression/physiology Guanosine Triphosphate/metabolism Kidney/cytology Microscopy, Immunoelectron Mutation/physiology Transferrin/metabolism rab GTP-Binding Proteins rab5 GTP-Binding Proteins
Chemicals
Transferrin Guanosine Triphosphate GTP Phosphohydrolases GTP-Binding Proteins rab11 protein rab GTP-Binding Proteins rab5 GTP-Binding Proteins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Ullrich O
European Molecular Biology Laboratory, Heidelberg, Germany.
Reinsch S
Urbé S
Zerial M
Parton R G
References (50)
50 references, click to expand
  1. Newly synthesized transferrin receptors can be detected in the endosome before they appear on the cell surface.
    J Biol Chem. 1995 May 5;270(18):10999-1003 PMID: 7738042
  2. Rab proteins and the road maps for intracellular transport.
    Neuron. 1993 Nov;11(5):789-99 PMID: 8240804
  3. Evidence for nonvectorial, retrograde transferrin trafficking in the early endosomes of HEp2 cells.
    J Cell Biol. 1995 Feb;128(4):549-61 PMID: 7860630
  4. Secretory granule and synaptic vesicle formation.
    Curr Opin Cell Biol. 1991 Aug;3(4):654-60 PMID: 1663373
  5. The small GTP-binding protein rab6 functions in intra-Golgi transport.
    J Cell Biol. 1994 Dec;127(6 Pt 1):1575-88 PMID: 7798313
  6. Isolation of a temperature-sensitive variant Chinese hamster ovary cell line with a morphologically altered endocytic recycling compartment.
    J Cell Physiol. 1993 Jun;155(3):579-94 PMID: 8491793
  7. Small GTP-binding protein associated with Golgi cisternae.
    Nature. 1990 Jun 7;345(6275):553-6 PMID: 2112230
  8. A novel class of clathrin-coated vesicles budding from endosomes.
    J Cell Biol. 1996 Jan;132(1-2):21-33 PMID: 8567724
  9. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments.
    Cell. 1990 Jul 27;62(2):317-29 PMID: 2115402
  10. Small GTP-binding proteins and their role in transport.
    Curr Opin Cell Biol. 1991 Aug;3(4):626-33 PMID: 1663370
  11. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway.
    Cell. 1992 Sep 4;70(5):715-28 PMID: 1516130
  12. Rab5a is a common component of the apical and basolateral endocytic machinery in polarized epithelial cells.
    Proc Natl Acad Sci U S A. 1994 May 24;91(11):5061-5 PMID: 8197185
  13. Quantification of low density lipoprotein and transferrin endocytic sorting HEp2 cells using confocal microscopy.
    J Cell Sci. 1994 Aug;107 ( Pt 8):2177-89 PMID: 7983176
  14. Cloning and subcellular localization of novel rab proteins reveals polarized and cell type-specific expression.
    J Cell Sci. 1994 Dec;107 ( Pt 12):3437-48 PMID: 7706395
  15. Association of three small GTP-binding proteins with cholinergic synaptic vesicles.
    FEBS Lett. 1993 Feb 8;317(1-2):53-6 PMID: 8428634
  16. Iterative fractionation of recycling receptors from lysosomally destined ligands in an early sorting endosome.
    J Cell Biol. 1989 Dec;109(6 Pt 2):3303-14 PMID: 2600137
  17. A general method for rapid site-directed mutagenesis using the polymerase chain reaction.
    Gene. 1990 Nov 30;96(1):125-8 PMID: 2265750
  18. Transport into and out of the Golgi complex studied by transfecting cells with cDNAs encoding horseradish peroxidase.
    J Cell Biol. 1994 Nov;127(3):641-52 PMID: 7962049
  19. The transmembrane segment of the human transferrin receptor functions as a signal peptide.
    EMBO J. 1986 Jul;5(7):1543-50 PMID: 3017701
  20. pH-induced microtubule-dependent redistribution of late endosomes in neuronal and epithelial cells.
    J Cell Biol. 1991 Apr;113(2):261-74 PMID: 2010463
  21. Movement of internalized ligand-receptor complexes along a continuous endosomal reticulum.
    Nature. 1990 Jul 26;346(6282):335-9 PMID: 2374607
  22. The response of the Golgi complex to microtubule alterations: the roles of metabolic energy and membrane traffic in Golgi complex organization.
    J Cell Biol. 1989 Nov;109(5):2081-8 PMID: 2681225
  23. Expression of Rab GTPases using recombinant vaccinia viruses.
    Methods Enzymol. 1995;257:155-64 PMID: 8583918
  24. Rab4 and cellubrevin define different early endosome populations on the pathway of transferrin receptor recycling.
    Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9559-64 PMID: 8790369
  25. Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis.
    EMBO J. 1994 Mar 15;13(6):1287-96 PMID: 8137813
  26. Intrinsic microtubule stability in interphase cells.
    J Cell Biol. 1994 Mar;124(6):985-96 PMID: 8132719
  27. Membrane transport in the endocytic pathway.
    Curr Opin Cell Biol. 1995 Aug;7(4):552-63 PMID: 7495576
  28. GTP-binding proteins in intracellular transport.
    Trends Cell Biol. 1992 Feb;2(2):41-6 PMID: 14731525
  29. The small GTP-binding protein rab4 is associated with early endosomes.
    Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):6313-7 PMID: 1906178
  30. From coiled tubules to a secretory canaliculus: a new model for membrane transformation and acid secretion by gastric parietal cells.
    Trends Cell Biol. 1996 Feb;6(2):49-53 PMID: 15157490
  31. The small GTP-binding protein rab4 controls an early sorting event on the endocytic pathway.
    Cell. 1992 Sep 4;70(5):729-40 PMID: 1516131
  32. 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. 1994 Jun;125(6):1265-74 PMID: 7515888
  33. Protein and cell membrane iodinations with a sparingly soluble chloroamide, 1,3,4,6-tetrachloro-3a,6a-diphrenylglycoluril.
    Biochem Biophys Res Commun. 1978 Feb 28;80(4):849-57 PMID: 637870
  34. Kinetics of internalization and recycling of transferrin and the transferrin receptor in a human hepatoma cell line. Effect of lysosomotropic agents.
    J Biol Chem. 1983 Aug 25;258(16):9681-9 PMID: 6309781
  35. Rab11, a small GTPase associated with both constitutive and regulated secretory pathways in PC12 cells.
    FEBS Lett. 1993 Nov 15;334(2):175-82 PMID: 8224244
  36. Rab GDP dissociation inhibitor as a general regulator for the membrane association of rab proteins.
    J Biol Chem. 1993 Aug 25;268(24):18143-50 PMID: 8349690
  37. Enrichment of rab11, a small GTP-binding protein, in gastric parietal cells.
    Am J Physiol. 1994 Aug;267(2 Pt 1):G187-94 PMID: 8074219
  38. Demonstration of an extensive trans-tubular network continuous with the Golgi apparatus stack that may function in glycosylation.
    Cell. 1985 Nov;43(1):287-95 PMID: 3000603
  39. Segregation of transferrin to a mildly acidic (pH 6.5) para-Golgi compartment in the recycling pathway.
    Cell. 1984 Jul;37(3):789-800 PMID: 6204769
  40. Microinjected antibodies against the cytoplasmic domain of vesicular stomatitis virus glycoprotein block its transport to the cell surface.
    EMBO J. 1986 May;5(5):931-41 PMID: 3013626
  41. Rab17, a novel small GTPase, is specific for epithelial cells and is induced during cell polarization.
    J Cell Biol. 1993 May;121(3):553-64 PMID: 8486736
  42. Microtubule-disrupting drugs blocked delivery of endocytosed transferrin to the cytocenter, but did not affect return of transferrin to plasma membrane.
    J Biochem. 1991 Apr;109(4):528-33 PMID: 1869507
  43. Communication of post-Golgi elements with early endocytic pathway: regulation of endoproteolytic cleavage of Semliki Forest virus p62 precursor.
    J Cell Sci. 1995 Jun;108 ( Pt 6):2465-75 PMID: 7673361
  44. Mapping the distribution of Golgi enzymes involved in the construction of complex oligosaccharides.
    J Cell Sci. 1995 Apr;108 ( Pt 4):1617-27 PMID: 7615680
  45. Associations of elements of the Golgi apparatus with microtubules.
    J Cell Biol. 1984 Sep;99(3):1092-100 PMID: 6381504
  46. Molecular cloning of YPT1/SEC4-related cDNAs from an epithelial cell line.
    Mol Cell Biol. 1990 Dec;10(12):6578-85 PMID: 2123294
  47. Localization of Rab family members in animal cells.
    Methods Enzymol. 1992;219:398-407 PMID: 1488012
  48. Rab GTPases in vesicular transport.
    Curr Opin Cell Biol. 1993 Aug;5(4):613-20 PMID: 8257602
  49. Internalization and processing of transferrin and the transferrin receptor in human carcinoma A431 cells.
    J Cell Biol. 1983 Aug;97(2):508-21 PMID: 6309862
  50. Biosynthetic transport of the asialoglycoprotein receptor H1 to the cell surface occurs via endosomes.
    Proc Natl Acad Sci U S A. 1995 Oct 24;92(22):10109-13 PMID: 7479735
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
DOI
10.1083/jcb.135.4.913
Published
1996-11-00
Pages
913-24
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2133374
Subset
IM
External Links
PubMed source DOI: 10.1083/jcb.135.4.913 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2