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,3
*
Departamentos de Alimentos e Nutrição Experimental e
**
Análises Clínicas e Toxicológicas, Faculdade de Ciências Farmacêuticas and Departamentos de
Medicina Preventiva e
Patologia, Instituto de Medicina Tropical de São Paulo (LIM/38), Faculdade de Medicina, Universidade de São Paulo, São Paulo, SP, Brasil;
Departamento de Ciências Exatas, Escola Superior de Agricultura Luis de Queiroz-ESALQ, Universidade de São Paulo, Piracicaba, SP, Brasil; and
Karolinska Institute, Stockholm, Sweden
3To whom correspondence should be addressed.
 |
ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • casein • soy protein isolate • lipoprotein oxidation • atherosclerosis • rabbits.
|
INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, Witztum 1993
, Yla-Hertuala et al. 1989
). The exact
mechanism by which modified lipoproteins contribute to the disease
progression is still not fully understood. The profound biological
effect of oxLDL, ranging from direct toxicity on cells to induction of
cytokine production, promoting chemotaxis and modulation of cellular
receptors and functions (Berliner et al. 1990
,
Chisolm 1993
, Cushing et al. 1990
,
Esterbauer et al. 1997
, Frostegård et al. 1990
and 1991
, Kim et al. 1994
, Kume et al. 1992
, Lehr et al. 1993
,
Rajavashisth et al. 1990
), is compatible with the
proposed tissue injury hypothesis (Ross and Glomset 1976
, Ross 1993
). However, more recent studies
suggest that part of the atherosclerotic process may involve a specific
immune response because B and T lymphocytes and immunoglobulin have
been detected in the atherosclerotic plaque (Sohma et al. 1995
, Stemme et al. 1995
). Moreover, oxLDL can
upregulate the major histocompatibility complex (MHC) class II
molecules on monocytes, making the monocyte more immune competent
(Frostegård et al. 1990
). In addition, oxLDL can be
antigenic itself as demonstrated by the presence of higher levels of
autoantibodies against oxLDL in groups with carotid atherosclerosis
than in the normal population (Salonen et al. 1992
) and
can induce potential autoantigens such as heat-shock proteins on
monocytic cells (Frostegård et al. 1996
).
Overwhelming evidence shows that nutritional factors are of prime
importance in preventing and modifying the ongoing atherosclerotic
process [for further references see Arntzenius et al. (1985)
, Drew and Tipping (1995)
and
Hegsted et al. (1965)
]. Epidemiologic studies have
shown a positive correlation between an animal protein–rich diet and
mortality from ischemic coronary heart disease. In contrast,
populations that consume large amounts of plant protein have a lower
incidence of stroke and ischemic coronary heart disease (Feldman and Kuske 1987
). Furthermore, a number of dietary trials in
humans and animals have provided evidence that the level of plasma
cholesterol and the development of atherosclerosis can be modified by
replacing animal protein with plant protein in the diet (Carroll 1978
, Kurowska et al. 1990
, Samman et al. 1990
). Even though the physiologic, biochemical and immunologic
variables associated with atherosclerosis have been studied
intensively, the link between these variables and nutritional factors
remains unclear. This is particularly true for the influence of
immunologic events associated with the progression of atherosclerosis.
In this study, we compared the effect of casein (CAS) or soy protein
isolate (SPI) on the induction of atherosclerosis in
cholesterol-fed rabbits (Finking and Hanke 1997
).
|
MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Adult male New Zealand rabbits (n = 20)
weighing 2.5–3.0 kg were purchased from CRIEX (Sao Paulo, Brazil); the
protocol for the study complied with NIH guidelines (NRC 1985
). Throughout the experiment, rabbits were maintained in
individual metal cages and were allowed free access to food and water.
The room temperature were maintained at 
22°C. All procedures in
this study complied with the ethical guidelines of the institution for
experiments with animals. The rabbits were divided at random into two
groups. A group of 10 rabbits (CAS group) were fed a nonpurified diet
(Nutri-coelhos Especial Purina, Sao Paulo, Brazil) supplemented with
10.0 g/kg cholesterol (Sigma Chemical, St. Louis, MO) and 270.0 g/kg
casein (Casein 2S, Rodoma S/A, Sao Paulo, Brazil), and a group of 10
rabbits (SPI group) was fed the same commercial diet supplemented with
10.0 g/kg cholesterol and 270.0 g/kg soy protein isolate (Samprosoy 90
NB, Ceval Alimentos S/A, Sao Paulo, Brazil). To prepare the
supplemented diets, commercial nonpurified diet was triturated,
homogenized with prehydrated casein or soy protein isolate, and
repelleted and dried at 50°C for 12 h. Ether-diluted
cholesterol was pulverized on the diets, which were maintained under
the hood for 12 h for ether to evaporate. The diets were prepared
weekly and maintained at -20°C to reduce the oxidative
modifications. The chemical compositions of the commercial nonpurified
and supplemented diets were appropriate to maintain the health of the
rabbits. Protein, amino acid, total lipid, mineral, water and fiber
contents were analyzed by the methods indicated by the
Association of Official Analytical Chemists (1980)
after
addition of casein or soy protein isolate to a commercial nonpurified
diet (Table 1
).
|
Variation in body weights and food intakes was monitored daily. CAE was determined during treatment in each experimental group. The CAE is the ratio of the difference in body weight between d 60 and 0 (T60 - T0) and the amount of food consumed throughout the experimental period.
Purification of LDL from plasma.
Rabbits were deprived of food for 12 h and blood samples were collected into tubes containing 1.0 g/L EDTA at d 0, 15, 30, 45 and 60 of treatment. Immediately after plasma separation, 1.0 mmol/L phenylmethylsulfonyl fluoride, 2.0 mmol/L benzamidine, 2.0 mg/L aprotinin and 20.0 mmol/L BHT were added to the samples. All of these reagents were purchased from Sigma Chemical.
LDL were purified from rabbit plasma by sequential ultracentrifugation
as previously described (Havel et al. 1955
). LDL (1.020
< d < 1.063 kg/L) were dialyzed extensively
against 150.0 mmol/L sodium chloride, 1.0 mmol/L EDTA, 10.0 mmol/L
Trizma base and 3.0 mmol/L sodium azide at 4°C for 12 h. All
samples (plasma and LDL) were maintained at -80°C until analysis.
Protein concentrations in plasma and LDL were determined according to
the method of Lowry et al. (1951)
.
Analysis of cholesterol levels.
The concentration of cholesterol was determined in plasma and LDL using an enzymatic analysis kit for cholesterol determination (# 11 5050, BioSystem, Barcelona, Spain).
Detection of oxidized LDL by ELISA.
The oxidized LDL (oxLDL) in blood plasma were detected by ELISA using
anti-oxLDL monoclonal antibodies (mAb) as described by
Gidlund et al. (1996)
. Three mAb with different
specificities were used; mAb 23 and 24 were specific for highly
oxidized lipoprotein and mAb 28 was reactive with minimally oxidized
lipoprotein (Gidlund et al. 1996
). Ninety-six–well
plates (EIA/RIA, Costar, Cambridge, MA) were coated with plasma samples
(10.0 mg protein/L) in carbonate-bicarbonate buffer, pH 9.4, and
incubated overnight at 4°C. The plates were washed once with 0.01
mol/L PBS, pH 7.4, and further blocked with 5.0 g/L fat-free milk
(Molico, Nestlé, Araçatuba, SP, Brazil) in PBS for 2 h. After washing with PBS, the respective mAb were added at a final
concentration of 2.0 mg/L in PBS, and the antibodies were allowed to
react for 3 h at room temperature. The plates were then washed
four times with PBS containing 0.2 mL/100 L Tween 20 (PBS-T; Fluka
Chemie AG, Sao Paulo, Brazil). Horseradish peroxidase–conjugated
polyclonal rabbit anti-mouse immunoglobulin (Ig) antibody (Dako
A/S, Carpinteria, CA) diluted 1:2000 (v/v) in PBS was added. The plates
were maintained at room temperature for 1 h, washed four times
with PBS-T and the reaction was developed by the addition of
o-phenylenediamine (Sigma) in 0.1 mol/L
citrate-phosphate buffer pH 5.0. The reaction was stopped by the
addition of 2.0 mol/L sulfuric acid and the optical density (OD)
measured with a microplate reader (Spectra Count, Canberra Company,
Meriden, CT) at 490 nm. The samples were analyzed in duplicate
at the same time. The data are presented as reactivity index (RI)
calculated for each rabbit considering the entire experimental period.
RI = (X - L):(H
- L), where X is the OD value at
the defined time point, L is the lowest OD value during
the experimental period and H is the highest OD value
during the experimental period.
Detection of anti-oxLDL antibodies.
Human LDL (1.0 g/L) were oxidized in vitro with 50.0 µmol/L copper sulfate for 8 h at 37°C. Plates were coated with 10.0 mg oxLDL protein/L in carbonate/bicarbonate buffer, pH 9.4, and kept overnight at 4°C. Then, the plates were blocked with 50.0 g/L fat-free milk (Molico, Nestlé, Araçatuba, SP, Brazil) in PBS for 2 h and washed with PBS-T; the plasma samples, diluted 1:50 in PBS (v/v), were added and kept at room temperature for 2 h. The plates were then washed four times with PBS-T, and a horseradish peroxidase–conjugated polyclonal swine anti-rabbit IgG antibody (Dako A/S) diluted 1:1000 in PBS (v/v) was added. The plates were incubated for 40 min, washed and developed as above. The data are presented as % increase = [(value at defined time point - baseline value at d 0): baseline value at d 0] x 100.
Analysis of hydroperoxides.
The content of lipid hydroperoxides present in LDL was evaluated by
HPLC at 235 nm, according to the method of Terao and Fukino (1993)
, using a C8 Inertsil column (GL Sciences, Tokyo, Japan).
The cholesteryl ester and trilinolein hydroperoxides were extracted
with methanol/hexane (1:3, v/v) (Folcik and Cathcart 1994
) and phosphatidylcholine hydroperoxides were extracted
with methanol/chloroform (1:2, v/v). The quantification of cholesteryl
linoleate (CL-OOH), trilinolein (TL-OOH) and phosphatidylcholine
(PL-OOH) hydroperoxides present in the samples was done using external
standards calibrated at multiple levels using the chromatographic
software Class LC-10, LC Work Station (Shimadzu, Tokyo, Japan).
Analysis of atherosclerotic lesions.
The rabbits were anesthetized with an intramuscular injection of 5
mg/kg body weight Rompun (Bayer S.A, Sao Paulo, Brazil) and 50 mg/kg
body weight Ketalar (Parke-Davis, Sao Paulo, Brazil) and then killed;
the thorax was opened and the heart and aorta removed. The intact aorta
was removed from each rabbit, fixed in 0.01 mol/L phosphate buffered 37
g/L formaldehyde and opened longitudinally. Because the major incidence
of lesions occurs in the aortic arch, a 0.5-cm long longitudinal
fragment, 1.0 cm from the coronary ostium, was taken randomly from each
rabbit. The fragment was dehydrated in increasing ethanol
concentrations, cleared in propylene oxide and embedded in paraffin.
Consecutive semi-thin sections (n = 20; 5
µm) were taken serially from each fragment, mounted on
glass slides, stained with hematoxylin/eosin and examined under the
light microscope at X100 magnification. Quantitative measurements were
made in each section using the Optima imaging analysis system (BioScan,
Edmonds, WA). Area and the volume were calculated by the method of
Daley et al. (1994)
. The area
(µm2) was calculated as the sum of linear
length of the lesions in the 20 sections multiplied by 5 (thickness of
each section). The volume (µm3) was
calculated as the sum of the lesion area in 20 sections multiplied by 5
(thickness of each section). The data were presented as the percentage
of lesions in relation to the total area and volume of the sections
from the segment of aortic arch analyzed. These analyses were done in
samples from 8 CAS-fed rabbits and 10 SPI-fed rabbits due to
accidental loss of two samples from the CAS group.
Statistical analysis.
Statistical analysis was done using the SAS statistical package (version 6.03, 1995) developed by the SAS Institute (Cary, NC). ANOVA was used for intragroup analysis and multivariate ANOVA (MANOVA) with repeated measurements to compare intergroup differences. MANOVA was applied to the data resulting after subtracting the basal values from d 0. Intra- and intergroup differences were analyzed by Tukey’s studentized range test. Student’s t test was applied to analyze differences in atherosclerotic lesions. Differences were considered significant when P < 0.05. Values are means ± SD.
|
RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The concentrations of lipids, protein, fiber, minerals, vitamins and
water were similar in the CAS and SPI diets (Table 1)
. The amino acid
composition is shown in Table 2
. The sum of the concentrations of hypocholesterolemic amino acids
(arginine and glycine) in the CAS and SPI diets was 119.20 and 133.90
g/kg protein, respectively, and the sum of the concentrations of
hypercholesterolemic amino acids (lysine, valine, leucine and
isoleucine) in the CAS and SPI diets was 250.10 and 260.10 g/kg of
protein, respectively. The ratio of the sum of the concentration of
hyper- and hypocholesterolemic amino acids was 2.1 and 1.9, in the CAS
and SPI groups, respectively. When the arginine/lysine ratio was
calculated, the differences between the diets were more evident, i.e.,
the arginine/lysine ratio was 1.57 in the SPI diet and 1.22 in the CAS
diet. In spite of the significant difference in amino acid composition
between diets, no significant differences in protein concentrations
were observed in plasma or the LDL fraction, except for the LDL
fraction at d 60 (Table 3). The changes in body weight were not significantly different between
the CAS and SPI groups (data not shown). Throughout the experimental
period, rabbits in the CAS and SPI groups were healthy and the CAE did
not differ between groups: 0.13 ± 0.05 for CAS and 0.11 ± 0.06 for SPI.
|
|
The cholesterol content of the diets promoted a significant increase in
concentrations of plasma and LDL cholesterol in the CAS and SPI groups.
However, plasma cholesterol was significantly higher in CAS- than in
SPI-fed rabbits at d 15, 30 and 45 of treatment (Fig. 1A
). The concentration of LDL cholesterol was higher in the CAS group than
in the SPI group at d 15 and 30 of treatment (Fig. 1B
).
Triglyceride concentration did not differ in the CAS and SPI groups
throughout the experimental period, and a significant increase relative
to d 0 was observed only after 60 d of treatment in both groups
(data not shown).
|
The addition of cholesterol to the diet given to the rabbits induced an
increase in the formation of lipid hydroperoxides that differed between
the CAS and SPI groups. PL-OOH levels were significantly higher in
the CAS group than in the SPI group from d 15 through d 45 d of
treatment. Furthermore, PL-OOH levels did not increase
significantly in the SPI group until d 60 (Fig. 2A
). CL-OOH levels increased in both groups, but it was only at d 60
of treatment that the SPI-fed rabbits had a significantly higher
level than that of the CAS group (Fig. 2B
). TL-OOH
levels increased significantly in both groups but levels were
significantly higher at d 15, 30 and 60 in the CAS group than in the
SPI group (Fig. 2C
).
|
). Similarly, mAb 24-reactive oxLDL did not change significantly in the
CAS group during the experiment, whereas the SPI group showed decreases
at d 15, 45 and 60 relative to d 0 (Fig. 3B
). A
significantly higher level of mAb 24-reactive oxLDL was observed at d
60 in the CAS group than in the SPI group (Fig. 3B
). mAb
28-reactive oxLDL had increased in both groups by d 60 and a
significantly higher level was reached in the SPI group than in the CAS
group at d 45 (Fig. 3C
).
|
Because there was substantial variability within groups, we evaluated
the oxLDL autoantibody concentration considering the baseline value at
d 0 for each rabbit. The cholesterol-rich diet caused a very rapid
increase in anti-oxLDL antibodies from d 15 of treatment in the CAS
group, whereas in the SPI group, the increase occurred only at d 60 of
treatment (Fig. 4
). Autoantibodies against oxLDL were significantly higher in the CAS
group than in the SPI group at d 15, 30 and 45 of treatment.
|
The volume of the lesions did not differ between groups but the lesion
area was significantly greater in the CAS group than in the SPI group
(P < 0.05), (Fig. 5
).
|
|
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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), was higher in the SPI diet (1.57) than in the CAS diet
(1.22). Soybeans and soy protein isolate contain isoflavones
(Anderson et al. 1995
, Anthony et al. 1997
, Kerry and Abbey 1998
), which have
antioxidant effects, but the soy protein isolate used in this study was
obtained by a hydroalcoholic extraction process that removes major
isoflavones. Therefore, we can study the differences in rabbits fed
different protein supplements, focusing essentially on amino acid
composition.
CAS-fed rabbits generally had greater concentrations of plasma and LDL
cholesterol, lipid hydroperoxides and oxLDL species than SPI-fed
rabbits. Because the only difference between groups was in the protein
supplement and apparently only in amino acid composition, our data
suggest that the amino acid composition of the diet initially causes a
greater increase in the level of plasma and LDL cholesterol in
CAS-fed rabbits than in those fed SPI by mechanisms such as
increased cholesterol absorption in the gut (Beynen et al. 1983
) and downregulation of apolipoprotein B/E receptors on
cells (Vahouny et al. 1985
). The generation of different
lipid hydroperoxides and different species of oxidized LDL could be a
consequence of increased plasma and LDL cholesterol because reduction
in lipoprotein clearance is associated with increased susceptibility of
LDL to oxidation (Deigner et al. 1992
, Ling et al. 1997
, Usynun et al. 1999
).
Differences in the variables analyzed above may be related to the
development of atherosclerosis, but the main purpose of this study was
to analyze the immunologic mechanism involved in the process. Our
approach was based on the fact that antigenic particles from LDL are
generated during the process of oxidation. LDL particles undergo a
large range of modifications from generation of lipid hydroperoxides to
complete fragmentation of the particle (Esterbauer et al. 1992
), and some of these components generated become
immunogenic as indicated by the presence of autoantibodies against
oxLDL in some patients (Salonen et al. 1992
). The degree
of oxidation of LDL is usually evaluated by the detection of
thiobarbituric acid-reactive substances; however, we recently
developed monoclonal antibodies against oxLDL that recognize oxLDL with
various degrees of oxidative modifications. For this purpose,
hybridomas were generated against oxLDL and were selected using LDL
oxidized by copper for either 1 or 18 h, i.e., for generation of
minimally or highly oxidized LDL. Three mAb were selected according to
reactivity to these oxLDL preparations, i.e., mAb 23 and 24,
recognizing highly oxidized LDL, and mAb 28, recognizing minimally
oxidized LDL (Gidlund et al. 1996
). These mAb were used
to detect oxLDL species by immunologic assay (ELISA), and we observed
the predominance of highly oxidized LDL (mAb 24-reactive oxLDL) in the
CAS group, whereas minimally oxidized LDL (mAb 28-reactive oxLDL) were
predominant in the SPI group.
The oxLDL presence in the circulation remains a controversial issue.
Witzum (1993)
and Jansen et al. (1995)
suggested that oxLDL are not detectable in the circulation because they
are rapidly removed by the scavenger receptors in the hepatic sinusoid.
However, other reports (Hodis et al. 1994
) show both the
presence of circulating oxLDL and a positive correlation between levels
of circulating oxLDL and progression of atherosclerosis. Much of this
discrepancy may result from the difficulty in measuring oxLDL and the
fact that oxidation of LDL particles leads to a wide spectrum of oxLDL
species. Even though a large portion of the oxLDL species are rapidly
eliminated by phagocytes in the liver, some may remain either as free
entities or associated with other serum components. Our results using
mAb that detect oxLDL with different degrees of oxidation actually
showed the generation of a variety of oxLDL during the process,
confirming the validity of this type of approach.
Oxidatively modified lipoproteins are immunogenic (Witztum 1993
), and the presence of autoantibodies against oxLDL has
been considered a risk factor in coronary heart disease. However, there
are conflicting reports showing the absence of or low titers (1:5) of
autoantibodies in risk groups (Vijver et al. 1996
) or
the beneficial effect of high titers (>1:100,000) of
antimalonyldealdehyde-lysine (an epitope of oxLDL) antibodies
achieved by active immunization in induced atherosclerosis
(Palinski et al. 1995
). Our data revealed that all
rabbits had a basal level of anti-oxLDL antibodies compatible with
the presence of oxLDL detected by monoclonal anti-oxLDL antibodies
before the beginning of the diet treatments. With the diet, the rabbits
in the CAS group showed a very sharp and an early increase in
anti-oxLDL antibodies, whereas in the SPI group, we could detect
changes only during the late phase of the experiment at d 60. The
reason for this significant difference between the CAS and SPI groups
could be the predominance of highly oxidized LDL in the CAS group,
whereas in the SPI group, a higher level of only minimally oxidized LDL
was observed.
At the end of the diet period, rabbits were killed and the extent of
the atherosclerotic lesion was assessed. Atherosclerotic lesion area
was greater in the CAS group than in the SPI group. From the different
variables analyzed, we cannot define the direct cause of the more
extensive atherosclerosis in the CAS group, which had high lipid
hydroperoxide levels and sustained highly oxidized LDL levels and high
anti-oxLDL antibody levels. OxLDL is chemotactic for monocytes
(Frostegård et al. 1990
, Yla-Hertuala et al. 1991
) and may have favored this process in the CAS group,
leading to more intense inflammation. The presence of high levels of
anti-oxLDL antibody may also have contributed to the development of
the lesion. It is possible that anti-highly oxidized LDL antibodies
are atherogenic because the oxLDL used as the antigen in the test in
this study were oxidized for 8 h, as suggested by our findings,
and that, in contrast, the anti-minimally oxidized LDL antibodies,
which were not evaluated in this study, are protective.
At present, it is accepted that dietary interventions in lipids can
modify the susceptibility of lipoproteins to oxidation and consequently
the progression of atherosclerosis (Bakhit et al. 1994
,
Krosla et al. 1989
, Vahouny et al. 1985
).
Here we have shown that the amino acid composition of dietary protein
is an important factor and that the SPI diet was efficient in
counteracting the oxidative stress of a cholesterol-rich diet. This
dietary intervention altered differently the pattern of lipoprotein
oxidation and immunologic variables. In the long term, the apparently
beneficial effect of SPI supplement is nullified by continuous
consumption of a cholesterol-rich diet, as seen at d 60 of the
experimental period. The data suggest that, in addition to biochemical
alterations, immunologic alterations with the generation of
autoantibodies are important in the pathogenesis of atherosclerosis. We
thus suggest that in conjunction with classical biochemical and
physiologic markers, oxLDL levels and anti-oxLDL autoantibodies
should be considered in the follow-up of atherosclerosis in general
and also when dietary intervention is indicated.
|
ACKNOWLEDGMENTS |
|---|
|
FOOTNOTES |
|---|
2 Presented in part at the XI International Symposium on Atherosclerosis, Abbaye de Royamont, France [Abdalla, D.S.P., Rodrigues, F.M.D. & Damasceno, N.R.T. (1997) Effect of soy protein on lipoprotein oxidation and atherosclerotic lesion progression in experimental atherosclerosis. P1]; and at the IX International Symposium of Molecular Medicine, Brazil [Damasceno, N.R.T., Rodrigues, F.M.D., Gidlund, G., Goto, H. & Abdalla, D.S.P. (1997) Anti-OxLDL autoantibodies in experimental atherosclerosis. OC13/P135].
4 Abbreviations: CAS, nonpurified diet supplemented with 10.0 g/kg cholesterol plus 270.0 g/kg casein; CAE, coefficient of alimentary efficacy; CL-OOH, cholesterol linoleate hydroperoxides; Ig, immunoglobulin; mAb, monoclonal antibody; MHC, major histocompatibility complex; OD, optical density; OxLDL, oxidized LDL; PBS-T, PBS-Tween 20; PL-OOH, phosphatidylcholine hydroperoxides; RI, reactivity index; SPI, nonpurified diet supplemented with 10.0 g/kg cholesterol plus 270.0 g/kg soy protein isolate; TL-OOH, trilinolein hydroperoxides.
Manuscript received March 30, 2000. Initial review completed July 6, 2000. Revision accepted August 4, 2000.
|
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