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J Biol Chem, Vol. 274, Issue 19, 13017-13024, May 7, 1999
From the Division of Cellular and Molecular Medicine, Glycobiology
Program, University of California, San Diego,
La Jolla, California 92093-0687
The proteoglycans of animal cells typically
contain one or more heparan sulfate or chondroitin sulfate chains.
These glycosaminoglycans assemble on a tetrasaccharide primer,
-GlcA
1,3Gal1,3Gal1,4Xyl-O-, attached to
specific serine residues in the core protein. Studies of Chinese
hamster ovary cell mutants defective in the first or second enzymes of
the pathway (xylosyltransferase and galactosyltransferase I) show that
the assembly of the primer occurs by sequential transfer of single
monosaccharide residues from the corresponding high energy nucleotide
sugar donor to the non-reducing end of the growing chain. In order to
study the other reactions involved in linkage tetrasaccharide assembly,
we have devised a powerful selection method based on induced resistance
to a mitotoxin composed of basic fibroblast growth factor-saporin. One
class of mutants does not incorporate 35SO4 and
[6-3H]GlcN into glycosaminoglycan chains. Incubation of
these cells with naphthol--D-xyloside
(Xyl-O-Np) resulted in accumulation of linkage region
intermediates containing 1 or 2 mol of galactose (Gal1,
4Xyl-O-Np and Gal1, 3Gal1,
4Xyl-O-Np) and sialic acid (Sia
2,3Gal1, 3Gal1,
4Xyl-O-Np) but not any GlcA-containing oligosaccharides.
Extracts of the mutants completely lacked UDP-glucuronic acid:Gal1,3Gal-R glucuronosyltransferase (GlcAT-I) activity, as
measured by the transfer of GlcA from UDP-GlcA to
Gal1,3Gal-O-naphthalenemethanol (<0.2
versus 3.6 pmol/min/mg). The mutation most likely lies in the structural gene encoding GlcAT-I since transfection of the mutant
with a cDNA for GlcAT-I completely restored enzyme activity and
glycosaminoglycan synthesis. These findings suggest that a single GlcAT
effects the biosynthesis of common linkage region of both heparan
sulfate and chondroitin sulfate in Chinese hamster ovary cells.
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