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J. Biol. Chem., Vol. 277, Issue 46, 44431-44439, November 15, 2002
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From the We have previously demonstrated
intracellular degradation of the heparan sulfate side chains in
recycling glypican-1 by heparanase and by deaminative cleavage at
N-unsubstituted glucosamine with nitric oxide derived from
intrinsic nitrosothiols (see Ding, K., Mani, K., Cheng, F., Belting, M. and Fransson, L.-Å. (2002) J. Biol. Chem. 277, 33353-33360). To determine where and in what order events take place,
we have visualized, by using confocal laser-scanning immunofluorescence
microscopy, glypican-1 variants in unperturbed cells or arrested at
various stages of processing. In unperturbed proliferating cells,
glypican-1 was partly S-nitrosylated. Intracellular
glypican-1 was enriched in endosomes, colocalized significantly with
GM-1 ganglioside, caveolin-1, and Rab9-positive endosomes, and carried
side chains rich in N-unsubstituted glucosamine residues.
However, such residues were scarce in cell surface glypican-1. Brefeldin A-arrested glypican-1, which was
non-S-nitrosylated and carried side chains rich in
N-unsubstituted glucosamines, colocalized extensively with
caveolin-1 but not with Rab9. Suramin, which inhibits heparanase,
induced the appearance of S-nitrosylated glypican-1 in caveolin-1-rich compartments. Inhibition of deaminative cleavage did not prevent heparanase from generating heparan sulfate oligosaccharides that colocalized strongly with caveolin-1.
Growth-quiescent cells displayed extensive NO-dependent
deaminative cleavage of heparan sulfate-generating
anhydromannose-terminating fragments that were partly associated with
acidic vesicles. Proliferating cells generated such fragments during
polyamine uptake. We conclude that recycling glypican-1 that is
associated with caveolin-1-containing endosomes undergoes sequential
N-desulfation/N-deacetylation, heparanase
cleavage, S-nitrosylation, NO release, and deaminative cleavage of its side chains in conjunction with polyamine uptake.
Nitric Oxide-dependent Processing of Heparan Sulfate
in Recycling S-Nitrosylated Glypican-1 Takes Place in
Caveolin-1-containing Endosomes*
,,¶,, and
Department of Cell and Molecular Biology,
Lund University, BMC C13, SE-221 84, Lund, Sweden and the
§ Department of Cell Biology, Free University of Amsterdam,
Van der Boechorststraat 7, 1081 BT, Amsterdam, The Netherlands
*
This work was supported by grants from the Swedish Science
Council (VR-M and VR-NaTe), the Cancer Fund, the Strategic Research Fund (Glycoconjugates in Biological Systems (to F. C.)), the
WennerGren, Kock, and Österlund Foundations, Xylogen AB, and the
Medical Faculty of Lund University.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.
To whom correspondence should be addressed: Dept. of Cell and
Molecular Biology, Lund University, BMC C13, SE-221 84, Lund, Sweden. Tel.: 46-46-222-8573; Fax: 46-46-222-3128; E-mail:
lars-ake.fransson@medkem.lu.se.
Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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