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J Biol Chem, Vol. 273, Issue 5, 2738-2746, January 30, 1998
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From the Departments of The subendothelial aggregation and retention of
low density lipoprotein (LDL) are key events in atherogenesis, but the
mechanisms in vivo are not known. Previous studies have
shown that treatment of LDL with bacterial sphingomyelinase (SMase)
in vitro leads to the formation of lesion-like LDL
aggregates that become retained on extracellular matrix and stimulate
macrophage foam cell formation. In addition, aggregated human lesional
LDL, but not unaggregated lesional LDL or plasma LDL, shows evidence of
hydrolysis by an arterial wall SMase in vivo, and several
arterial wall cell types secrete a SMase (S-SMase). S-SMase, however,
has a sharp acid pH optimum using a standard in vitro
SM-micelle assay. Thus, a critical issue regarding the potential role
of S-SMase in atherogenesis is whether the enzyme can hydrolyze
lipoprotein-SM, particularly at neutral pH. We now show that S-SMase
can hydrolyze and aggregate native plasma LDL at pH 5.5 but not at pH
7.4. Remarkably, LDL modified by oxidation, treatment with
phospholipase A2, or enrichment with apolipoprotein CIII,
which are modifications associated with increased atherogenesis, is
hydrolyzed readily by S-SMase at pH 7.4. In addition, lipoproteins from
the plasma of apolipoprotein E knock-out mice, which develop extensive
atherosclerosis, are highly susceptible to hydrolysis and aggregation
by S-SMase at pH 7.4; a high SM:PC ratio in these lipoproteins appears
to be an important factor in their susceptibility to S-SMase. Most
importantly, LDL extracted from human atherosclerotic lesions, which is
enriched in sphingomyelin compared with plasma LDL, is hydrolyzed by
S-SMase at pH 7.4 10-fold more than same donor plasma LDL, suggesting that LDL is modified in the arterial wall to increase its
susceptibility to S-SMase. In summary, atherogenic lipoproteins are
excellent substrates for S-SMase, even at neutral pH, making this
enzyme a leading candidate for the arterial wall SMase that hydrolyzes LDL-SM and causes subendothelial LDL aggregation.
Anatomy and Cell Biology and
¶ Medicine, and the College of Physicians and Surgeons, Columbia
University, New York, New York 10032, the ** Wallenberg Laboratory,
Göteborg Universitet, S-413 45, Göteborg, Sweden, the
Institut Pasteur de Lille, 59019 Lille, France, the Department of Surgery, University of
California, San Francisco and the San Francisco Veterans Affairs
Medical Center, San Francisco, California 94121, and the
§§ Dorrance H. Hamilton Research Laboratories,
Division of Endocrinology, Diabetes, and Metabolic Diseases, Thomas
Jefferson University, Philadelphia, Pennsylvania 19107
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M.-L. Wong, B. Xie, N. Beatini, P. Phu, S. Marathe, A. Johns, P. W. Gold, E. Hirsch, K. J. Williams, J. Licinio, et al. Acute systemic inflammation up-regulates secretory sphingomyelinase in vivo: A possible link between inflammatory cytokines and atherogenesis PNAS, July 18, 2000; 97(15): 8681 - 8686. [Abstract] [Full Text] [PDF]
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