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(Received for publication, March 29, 1996, and in revised form, July 3, 1996)
From the The cellular generation of proteoglycans with
anticoagulant heparan sulfate (HSPGact) is determined by
microsomal ``HSact conversion activity'' that functions
in concert with the sulfate donor 3
Volume 271, Number 43,
Issue of October 25, 1996
pp. 27072-27082
©1996 by The American Society for Biochemistry and Molecular Biology, Inc.
,§
,§
,§
and§
Department of Biology, Massachusetts
Institute of Technology, Cambridge, Massachusetts 02139 and the
§ Department of Medicine, Harvard Medical School, Beth
Israel Hospital, Boston, Massachusetts 02215
-phosphoadenosine 5-phosphosulfate
(PAPS) to convert nonanticoagulant heparan sulfate
(HSinact) to anticoagulant heparan sulfate
(HSact) (Shworak, N. W., Fritze, L. M. S., Liu, J., Butler,
L. D., and Rosenberg, R. D. (1996) J. Biol. Chem. 271, 27063-27071). Suspension cultures of L-33+ cells in
serum-free medium produce HSPGact and secrete
HSact conversion activity. The secreted protein
exhibiting HSact conversion activity was isolated by
subjecting large volumes of conditioned suspension culture medium to
heparin-AF Toyopearl affinity chromatography, Mono Q-FPLC, TSK
SW3000-HPLC, and 3,5-ADP-agarose affinity chromatography. The
final product was purified ~700,000-fold relative to cellular
material with a 5% overall recovery of HSact conversion
activity. The isolated protein migrated on SDS-polyacrylamide gel
electrophoresis as a broad band of Mr = 46,000 and co-migrated on nondenaturing acidic pH gel electrophoresis with
HSact conversion activity. The purified component was
identified as heparan sulfate D-glucosaminyl
3-O-sulfotransferase because it transferred sulfate from
[35S]PAPS to the 3-O-position of
D-glucosamine and D-glucosamine
6-O-sulfate of HSact precursor and
HSinact precursor to produce nearly equivalent amounts of
labeled HSact and HSinact. The exhaustive
modification of wild-type LTA cell [35S]HS with either
microsomal HSact conversion activity or purified enzyme
increased HSact content from 9 to ~36%, which indicates
that microsomal HSact conversion activity predominantly
reflects the level of a 3-O-sulfotransferase that converts
HSact precursor into HSact. The kinetic
parameters of purified 3-O-sulfotransferase were determined
for modification of HSact precursor and HSinact
precursor. The apparent
KM* and
Vmax* with respect to PAPS
concentration for sulfation of HSact precursor and
HSinact precursor were 2.4 µM and 23 fmol of
sulfate/min/ng of enzyme and 2.1 µM and 38 fmol of
sulfate/min/ng of enzyme, respectively. There was substrate inhibition
of the sulfation reaction at elevated HS concentration. The apparent
KM* and
Vmax* with respect to GAG
concentration for sulfation of HSact precursor and
HSinact precursor were 16 nM and 120 fmol of
sulfate/min/ng of enzyme and 17 nM and 240 fmol of
sulfate/min/ng of enzyme, respectively. The observation that purified
3-O-sulfotransferase catalyzes sulfation of
HSact precursor and HSinact precursor in
conjunction with a documented discordant regulation of
3-O-sulfate content in HSinact and
HSact suggests that two discrete forms of the enzyme may
exist.
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