ABSTRACT: We identified and quantified the hydroperoxides,
hydroxides, epoxides, isoprostanes, and core aldehydes of the
major phospholipids as the main components of the oxophos-
pholipids (a total of 5–25 pmol/μmol phosphatidylcholine) in a
comparative study of human atheroma from selected stages of
lesion development. The developmental stages examined in-
cluded fatty streak, fibrous plaque, necrotic core, and calcified
tissue. The lipid analyses were performed by normal-phase
HPLC with on-line electrospray MS using conventional total
lipid extracts. There was great variability in the proportions of
the various oxidation products and a lack of a general trend.
Specifically, the early oxidation products (hydroperoxides and
epoxides) of the glycerophosphocholines were found at the ad-
vanced stages of the plaques in nearly the same relative abun-
dance as the more advanced oxidation products (core alde-
hydes and acids). The anticipated linear accumulation of the
more stable oxidation products with progressive development
of the atherosclerotic plaque was not apparent. It is therefore
suggested that lipid infiltration and/or local peroxidation is a
continuous process characterized by the formation and destruc-
tion of both early and advanced products of lipid oxidation at
all times. The process of lipid deposition appears to have been
subject to both enzymatic and chemical modification of the
normal tissue lipids. Clearly, the appearance of new and dis-
proportionate old lipid species excludes randomness in any ac-
cumulation of oxidized LDL lipids in atheroma.
Paper no. L9428 in Lipids 39, 97–109 (February 2004).
Oxidative modification of LDL is now recognized as a neces-
sary condition for foam-cell formation. Oxidized LDL, in
contrast to native LDL, is taken up avidly by macrophages,
which can cause foam-cell formation and eventual develop-
ment of atherosclerosis. Although a great variety of oxidized
LDL components have been identified, only a few have been
recovered from atheroma. In most instances, the isolations
from atheroma have been confined to the neutral lipids, oxo-
cholesterol and oxidized cholesteryl esters, the concentration
of which has been shown to increase dramatically with pro-
gressive atherosclerotic disease (1–3). Hoppe et al. (4)
showed that oxidation products of cholesteryl linoleate are re-
sistant to hydrolysis by macrophages, whereas Huber et al.
(5) showed that oxidation products of cholesteryl linoleate
(cholesteryl [9-oxo]linoleate and hydroperoxylinoleate) stim-
ulate human umbilical vein endothelial cells to specifically
bind human peripheral blood mononuclear cells.
Other studies have recognized both isoprostanes (6,7) and
hydroxides (8–11) of FA released by saponification from oxi-
dized phospholipids of atherosclerotic plaques. The estimates
of the hydroperoxides were found to exceed those of the iso-
prostanes by more than 20 times.
In parallel, a degradation of the PUFA in the sn-2-position
of phosphatidylcholine (PtdCho) by oxidation has been rec-
ognized as essential for binding oxidized LDL to macrophage
scavenger receptors, indicating that oxidized phosholipids are
involved in the initial binding process (12–16). The reactive
oxidation products derived from phospholipids, such as the
core aldehydes, can form covalent adducts with apolipopro-
tein B. These adducts retain the intact phosphorylcholine
headgroup (17,18) and have been demonstrated by immuno-
histochemical methods to accumulate in atherosclerotic le-
sions (18). The oxidized PtdCho-containing phospholipid ap-
pears to be an immunodominant epitope (19–21). Steinberg
(22) has suggested that oxidized phospholipids could be the
missing initiating factor(s) in atherosclerosis. Uchida (23) has
discussed the role of reactive low-M.W. aldehydes in cardio-
vascular diseases, although little is known about the effects
of oxidative stress on the development of atherosclerosis.
Although the presence of oxo-PtdCho in atherosclerotic le-
sions has been demonstrated previously (16,24–26), no com-
parative investigation has been reported on the composition of
the native and oxophospholipids at different stages of devel-
opment of atherosclerosis. By means of normal-phase liquid
chromatography/electrospray ionization-mass spectrometry
(LC/ESI-MS), we have tentatively identified and quantified
the hydroperoxides, hydroxides, epoxides, isoprostanes, and
core aldehydes bound to the common phospholipids as the
major components of the oxophospholipids. Oxidation prod-
Copyright © 2004 by AOCS Press 97 Lipids, Vol. 39, no. 2 (2004)
Present address of the seventh author: Midori Health Care Foundation,
3-22-5 Tarumi-cho, Suita, Osaka, 564-0062 Japan
*To whom correspondence should be addressed.
E-mail: arnis.kuksis@utoronto.ca
Abbreviations: DNPH, 2,4-dinitrophenylhydrazones; GroPCho, glycero-
phosphocholine; GroPEtn, glycerophosphoethanolamine; GroPIns, glyc-
erophosphoinositol; LC/ESI-MS, liquid chromatography/electrospray ion-
ization-mass spectrometry; lysoPtdCho, lysophosphatidylcholine; lysoPtd-
Etn, lysophosphatidylethanolamine; lysoPtdIns, lysophosphatidylinositol;
PAF, platelet-activating factor; PtdCho, phosphatidylcholine; PtdEtn, phos-
phatidylethanolamine; PtdIns, phosphatidylinositol; PtdSer, phosphatidylser-
ine; SM, sphingomyelin.
ARTICLES
Phospholipids and Oxophospholipids in Atherosclerotic
Plaques at Different Stages of Plaque Development
Amir Ravandi
a,b
, Saeid Babaei
b
, Ramsey Leung
b
, Juan Carlos Monge
b
,
George Hoppe
c
, Henry Hoff
c
, Hiroshi Kamido
a
, and Arnis Kuksis
a,
*
a
Banting and Best Department of Medical Research, University of Toronto, Toronto, Canada M5G 1L6,
b
Terrence Donnelly Heart Center, St. Michael’s Hospital, University of Toronto, and
c
Department of Cell Biology, Lerner Research Institute, The Cleveland Clinic Foundation, Cleveland, Ohio