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J Biol Chem, Vol. 274, Issue 8, 5185-5192, February 19, 1999
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From the The 3-O-sulfation of glucosamine
residues is an important modification during the biosynthesis of
heparan sulfate (HS). Our previous studies have led us to purify and
molecularly clone the heparan sulfate D-glucosaminyl
3-O-sulfotransferase (3-OST-1), which is the key enzyme
converting nonanticoagulant heparan sulfate (HSinact) to
anticoagulant heparan sulfate (HSact). In this study, we
expressed and characterized the full-length cDNAs of 3-OST-1
homologous genes, designated as 3-OST-2, 3-OST-3A, and
3-OST-3B as described in the accompanying paper (Shworak, N. W., Liu, J., Petros, L. M., Zhang, L., Kobayashi, M.,
Copeland, N. G., Jenkins, N. A., and Rosenberg, R. D. (1999)
J. Biol. Chem. 274, 5170-5184). All these cDNAs
were successfully expressed in COS-7 cells, and heparan sulfate
sulfotransferase activities were found in the cell extracts. We
demonstrated that 3-OST-2, 3-OST-3A, and
3-OST-3B are heparan sulfate D-glucosaminyl
3-O-sulfotransferases because the enzymes transfer sulfate
from adenosine 3'-phosphophate 5'-phospho-[35S]sulfate
([35S]PAPS) to the 3-OH position of glucosamine.
3-OST-3A and 3-OST-3B sulfate an identical
disaccharide. HSact conversion activity in the cell extract
transfected by 3-OST-1 was shown to be 300-fold greater than that in
the cell extracts transfected by 3-OST-2 and 3-OST-3A,
suggesting that 3-OST-2 and 3-OST-3A do not make
HSact. The results of the disaccharide analysis of the
nitrous acid-degraded [35S]HS suggested that 3-OST-2
transfers sulfate to GlcA2S-GlcNS and IdoA2S-GlcNS;
3-OST-3A transfers sulfate to IdoA2S-GlcNS. Our results
demonstrate that the 3-O-sulfation of glucosamine is
generated by different isoforms depending on the saccharide structures
around the modified glucosamine residue. This discovery has provided
evidence for a new cellular mechanism for generating a defined
saccharide sequence in structurally complex HS polysaccharide.
Department of Biology, Massachusetts
Institute of Technology, Cambridge, Massachusetts 02139, the
¶ Department of Medicine, Harvard Medical School, Beth Israel
Hospital, Boston, Massachusetts 02215, and the
Département de Chimie, Ecole Normale Superieure,
75231 Paris Cédex 05, France
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