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J. Biol. Chem., Vol. 276, Issue 21, 18540-18550, May 25, 2001
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From the § Program in Membrane Biology & Renal Unit,
Massachusetts General Hospital, and Department of Medicine, Harvard
Medical School, Boston, Massachusetts, 02129-2020, the
Kidney proximal tubule epithelial cells have an
extensive apical endocytotic apparatus that is critical for the
reabsorption and degradation of proteins that traverse the glomerular
filtration barrier and that is also involved in the extensive recycling
of functionally important apical plasma membrane transporters. We show
here that an Arf-nucleotide exchange factor, ARNO
(ADP-ribosylation factor nucleotide
site opener) as well as Arf6 and Arf1 small GTPases are
located in the kidney proximal tubule receptor-mediated endocytosis
pathway, and that ARNO and Arf6 recruitment from cytosol to endosomes
is pH-dependent. In proximal tubules in situ,
ARNO and Arf6 partially co-localized with the V-ATPase in apical
endosomes in proximal tubules. Arf1 was localized both at the apical
pole of proximal tubule epithelial cells, but also in the Golgi. By Western blot analysis ARNO, Arf6, and Arf1 were detected both in
purified endosomes and in proximal tubule cytosol. A translocation assay showed that ATP-driven endosomal acidification triggered the
recruitment of ARNO and Arf6 from proximal tubule cytosol to endosomal
membranes. The translocation of both ARNO and Arf6 was reversed by
V-type ATPase inhibitors and by uncouplers of endosomal intralumenal
pH, and was correlated with the magnitude of intra-endosomal
acidification. Our data suggest that V-type ATPase-dependent acidification stimulates the selective
recruitment of ARNO and Arf6 to proximal tubule early endosomes. This
mechanism may play an important role in the pH-dependent
regulation of receptor-mediated endocytosis in proximal tubules
in situ.
Intra-endosomal pH-sensitive Recruitment of the
Arf-nucleotide Exchange Factor ARNO and Arf6 from Cytoplasm to Proximal
Tubule Endosomes*
,
,, Laboratory of Renal Biochemistry, L.C. Simard Research
Center, CHUM & GRTM, Université de Montréal,
Montréal, Québec, H2L4M1 Canada, the ¶ Centre
de Recherche en Rhumatologie et Immunologie, Centre de Recherche du
CHUL, Université Laval, Sainte-Foy, Québec, G1V4G2
Canada, and the Department of Cell Biology, University of
Virginia Health Sciences Center, Charlottesville, Virginia
22908
*
This work was supported by Medical Research Council of
Canada Grant MT-7875 (to V. M. and P. V.) and National
Institutes of Health Grants DK42956 (to D. B.) and DK38452 (to
D. A. A., V. M., J. E. C., and D. B.).The costs of publication of this
article were defrayed in part by the
payment of page charges. The article must therefore be hereby marked
"advertisement" in
accordance with 18 U.S.C. Section
1734 solely to indicate this fact.
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