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(Received for publication, January 9, 1997, and in revised form, March 28, 1997)
From the Division of Preventive Medicine, Department of Medicine,
Columbia University College of Physicians and Surgeons,
New York, New York 10032 and ¶ Department of Comparative
Medicine, Bowman Gray School of Medicine,
Winston-Salem, North Carolina 27157
A unique feature of lipoprotein lipase (LpL), the
rate-limiting enzyme in the hydrolysis of circulating triglycerides, is its movement from its cell of synthesis, adipocyte or myocyte, to its
site of action, the luminal endothelial surface. This involves processes that allow LpL to be released from the adipocyte cell surface
and transferred against the flow of interstitial fluid to the luminal
surface of endothelial cells. LpL, an unstable enzyme, must retain its
activity during this process. Whether a chaperone-like molecule is
involved in LpL stabilization and transport is unclear. In the present
study, we tested the hypothesis that endothelial cells secrete factors
that release LpL and promote its transfer to the luminal
endothelial surface. Incubation of adipocytes with endothelial cell
conditioned medium (ECCM) led to release of about 2-fold more LpL
activity than control medium. Medium from endothelial cells exposed to
lysophosphatidylcholine (lyso-ECCM), a product of LpL lipolysis of
lipoproteins, released approximately 3-fold more LpL than ECCM.
Concomitant with the release of LpL, adipocyte cell surface heparan
sulfate (HS) proteoglycans were degraded suggesting that lyso-ECCM
contained a heparanase-like activity. More heparanase was found in
media from the basolateral than the apical side of
lysolecithin-stimulated polarized endothelial cells. In coculture
experiments, lipolysis and lysolecithin stimulation of endothelial
cells increased LpL release from adipocytes. LpL released by lyso-ECCM
remained stable and did not lose enzymatic activity at 37 °C for
1 h. LpL activity was also stabilized by heparanase-digested
fragments of HS (HS oligosaccharide) and by purified LpL binding
decasaccharide. Moreover, LpL·HS oligosaccharide complexes crossed
endothelial cell monolayers and bound to the apical side of the
cells. Thus, an endothelial heparanase may play a critical role in
releasing subendothelial HS bound proteins, and specific HS
oligosaccharides produced by this enzyme may serve as extracellular
chaperones.
Volume 272, Number 25,
Issue of June 20, 1997
pp. 15753-15759
©1997 by The American Society for Biochemistry and Molecular Biology, Inc.
EVIDENCE THAT HEPARAN SULFATE OLIGOSACCHARIDE IS AN
EXTRACELLULAR CHAPERONE
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