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(Received for publication, July 1, 1996)
From the ABSTRACT Scavenger receptor BI (SR-BI), a putative high
density lipoprotein (HDL) receptor, mediates the selective uptake of
HDL cholesteryl ester into cells and is highly expressed in adrenal
gland (Acton, S., Rigotti, A., Landschulz, K. T., Xu, S., Hobbs, H. H.,
and Krieger, M. (1996) Science 271, 518-520).
Apolipoprotein A-I knock-out (apoA-I0) mice have decreased HDL
cholesterol, depleted adrenal cholesterol stores and impaired
corticosteroid synthesis (Plump, A. S., Erickson, S. K., Weng, W.,
Partin, J. S., Breslow, J. L., and Williams, D. L. (1996) J. Clin. Invest. 97, 2660-2671). We now show up-regulation of
adrenal SR-BI mRNA and protein in apoA-I0 mice, but not in
apoA-II0, LDL receptor 0, apoE0, or cholesteryl ester transfer protein
transgenic mice. Adrenal SR-BI mRNA and protein are also increased
and cholesterol stores decreased in female mice with knock-out of
hepatic lipase, an enzyme previously shown to increase selective uptake
in cell culture. SR-BI mRNA is increased in stressed wild type mice
and in Y1 adrenal cells treated with adrenocorticotropic hormone; the
latter effect is inhibited by HDL. These findings provide in
vivo evidence showing SR-BI is a functional HDL receptor under
feedback control. The action of hepatic lipase on apoA-I-containing
lipoproteins may facilitate the SR-BI-mediated uptake of HDL lipid.
INTRODUCTION High density protein (HDL)1 metabolism
plays a pivotal role in cholesterol homeostasis and development of
atherosclerosis. Plasma HDL cholesterol levels show a general inverse
relationship with coronary heart disease (1). The normal function of
HDL and the mechanisms underlying the HDL-coronary heart disease
relationship are poorly understood. There is evidence in rodents that
HDL provides cholesterol for adrenal steroid hormone synthesis via
selective cholesterol uptake, a putative receptor-mediated process for
delivery of cholesteryl ester into the cells without degradation of HDL
protein (2). Although long suspected, the molecular identification of a
functional HDL receptor has proven to be elusive. In a major
breakthrough, Acton et al. (3) recently demonstrated that
murine scavenger receptor SR-BI, when expressed in transfected cells,
binds HDL and mediates selective uptake of HDL cholesteryl ester. SR-BI
protein is abundant in adrenal gland, ovary, testis, and, to a lesser
extent, liver, precisely the tissues actively involved in selective
uptake (2, 4). Therefore, SR-BI appears to be an authentic HDL receptor
mediating selective uptake. We now provide in vivo evidence
showing that adrenal SR-BI is a functional receptor for HDL under
feedback regulation in response to changes of cellular cholesterol
stores.
EXPERIMENTAL PROCEDURES All animals used were between 3 and 4 months old.
HL0 mice and wild type C57BL/6 mice were purchased from Jackson
Laboratory (Maine). HL0 mice backcrossed with C57BL/6 mice were kindly
provided by Dr. Nobuyo Maeda, University of North Carolina. ApoA-I0 and
ApoA-II0 mice were created by gene targeting in embryonic stem cells
and detailed characterization will be presented
elsewhere.2,3
Reverse
transcription-polymerase chain reaction was used to obtain murine SR-BI
cDNA from the adrenal gland. Murine SR-BI and Anti-SR-BI antisera were prepared
by immunization of rabbits with a recombinant murine SR-BI fragment
(amino acid 315-412) that was expressed in a bacterial expression
system and purified. Western analysis was performed with the adrenal
membrane preparation and equal quantity of membrane protein (50 µg of
protein/lane) was subjected to 7.5% reducing SDS-polyacrylamide gel.
SR-BI protein immunoreactivity was identified at its anthentic
molecular size (~82 kDa) (3). Tissue cholesterol and cholesteryl
ester content were determined as described (6) using
chloroform/methanol extraction and cholesterol CII and free cholesterol
C kit (Wako, Japan). Cholesteryl ester content was determined by
subtracting free cholesterol from total cholesterol. Rat ACTH was
purchased from Sigma. Human HDL was prepared by
preparative ultracentrifugation between d 1.063 and 1.210 g/ml as described (7). For experiments with murine adrenal Y1 cells,
the cells, obtained from ATCC, were maintained in Ham F-12 media plus
20% horse serum. On the day of experiments, the cells were treated for
8 h with or without horse serum. When indicated, 100 n ACTH and 100 µg of protein/ml human HDL were added
during incubation. The cells were collected and washed with
phosphate-buffered saline twice, and total RNA was prepared.
RESULTS The tissue distribution pattern of SR-BI mRNA in wild type
mice (C57BL/6) was determined by ribonuclease protection assay and is
shown in Fig. 1. Adrenal gland was the richest source of
SR-BI mRNA. Ovary and testis also had relatively abundant SR-BI
mRNA. Liver had the highest SR-BI mRNA content in
nonsteroidogenic tissues. Quantitation of SR-BI mRNA by
phosphorimager indicated that hepatic SR-BI mRNA abundance was
about 1/10 of that in the adrenal gland. These SR-BI mRNA
distribution patterns are generally comparable with the SR-BI protein
distribution patterns (3) and are consistent with the order of
selective cholesterol uptake from HDL by different rodent organs (4).
We hypothesized that adrenal SR-BI expression might be under feedback
control in response to changes in cellular cholesterol stores. Plump
et al. (8) recently show that apolipoprotein A-I knock-out
(apoA-I0) mice have decreased HDL cholesterol, depleted adrenal
cholesterol stores, and impaired corticosteroid syntheses. Thus, we
measured SR-BI mRNA in adrenal gland and liver of apoA-I0 mice and,
as shown in Fig. 2, compared the results with mice with
induced mutations in a variety of other genes affecting lipoprotein
metabolism including apolipoprotein A-I (apoA-I) transgenic,
apolipoprotein A-II knock-out (apoA-II0), apolipoprotein E knock-out
(apoE0), LDL receptor knock-out (LDLR0), hepatic lipase knock-out
(HL0), and cholesteryl ester transfer protein transgenic mice. In
contrast to apoA-I0 mice, the first three strains of induced mutant
mice have relatively normal adrenal cholesterol stores (8). Consistent
with our hypothesis, there was ~3.5-fold increase in adrenal SR-BI
mRNA in apoA-I0 mice, but no change in apoA-II0, apoE0, or LDLR0
mice. Analysis of adrenal SR-BI protein by Western analysis in wild
type and apoA-I0 mice gave analogous results to the mRNA data,
i.e. highest expression in the adrenal gland and ~3-fold
up-regulation of adrenal SR-BI protein in apoA-I0 mice (data not
shown). Somewhat surprisingly, HL0 mice were also found to have a
significant 3.0-fold increase in adrenal SR-BI mRNA (Fig. 2,
A and B). SR-BI protein was also increased in
parallel (data not shown). SR-BI mRNA levels in liver were not
changed in any of the different strains of induced mutant mice (Fig.
2C).
Although the increase in adrenal SR-BI mRNA in HL0 mice was not
anticipated, previous studies have shown that HL enhances selective
uptake of HDL free cholesterol and cholesteryl ester in tissue culture
(9, 10). To further assess these findings, SR-BI mRNA was analyzed
in male and female HL0 mice backcrossed six times with C57BL/6 and with
wild type C57BL/6 mice of the same age. Adrenal SR-BI mRNA content
was increased ~3-fold in female HL0 mice but not in the male HL0
mice, even though SR-BI mRNA abundance was similar in wild type
male and female mice (Fig. 3A). In parallel
with these findings, adrenal cholesteryl ester and free cholesterol
stores were significantly decreased (by ~60% and ~20%
respectively) in female HL0 mice (Fig. 3B). On the other
hand, male HL0 mice showed no change in adrenal cholesterol content
(Fig. 3C). In contrast to the findings in HL0 mice, apoA-I0
mice of both sexes showed up-regulation of adrenal SR-BI mRNA (Fig.
2 shows female mice and data not shown for male mice), which is
consistent with the depletion of adrenal cholesterol store in both male
and female apoA-I0 mice (8).
As an additional test of the hypothesis that SR-BI expression is under
feedback control, mice were stressed by the cold swim test (11), which
is known to stimulate ACTH release and corticosteroid synthesis and to
deplete adrenal cholesterol stores (8, 11). In response to the stress
test, mice showed a significant 2-fold up-regulation of adrenal SR-BI
mRNA (p < 0.01, n = 4).
Next, murine adrenal Y1 cells, which are known to show selective uptake
of HDL cholesteryl ester (10), were grown in low serum medium and
treated with ACTH with or without HDL in medium. ACTH treatment
resulted in a significant increase in SR-BI mRNA expression, which
was completely prevented by inclusion of 100 µg of protein/ml HDL in
medium (Fig. 4).
DISCUSSION Our data show that adrenal SR-BI expression is up-regulated as a
response to depletion of cholesterol stores, whether resulting from
decreased uptake of cholesterol (apoA-I0 and HL0 mice) or increased
cholesterol utilization for corticosteroid synthesis (stress or ACTH
treatment). This suggests a feedback loop that controls SR-BI
expression and thereby helps to maintain adrenal cholesterol stores and
corticosteroid biosynthesis (Fig. 5). Together with the
findings of Acton et al. (3) and Plump et al.
(8), these results imply that HDL containing apoA-I is a
physiological ligand for SR-BI and that SR-BI functions to provide free
and esterified cholesterol to maintain adrenal cholesterol stores.
Moreover, up-regulation of SR-BI in HL0 mice suggests that the action
of HL on HDL is required for efficient selective uptake in the adrenal
gland.
The evidence for the proposed feedback control of SR-BI expression
(Fig. 5) is based on the inverse relationship between adrenal SR-BI
mRNA levels and cholesterol stores in various induced mutant mouse
models, as well as HDL-inhibited up-regulation of SR-BI mRNA by
ACTH in adrenal Y1 cells. Thus, in apoA-I0 mice and female HL0 mice
SR-BI mRNA was increased and cholesterol stores were markedly
decreased. By contrast, in male HL0 mice and in all of the other
induced mutant mouse strains tested, adrenal cholesterol stores and
SR-BI mRNA levels were essentially normal. There was no evidence
that increased HDL levels due to apoA-I overexpression in transgenic
mice or HDL addition to basal cell culture medium resulted in
down-regulation of SR-BI mRNA. Thus, the feedback loop may operate
in times of increased cholesterol need in response to augmented
corticosteroid synthesis.
The sex difference in the up-regulation of SR-BI mRNA in HL0 mice
could indicate an effect of sex steroid hormones on SR-BI gene
expression or the HDL ligand, or, more likely, increased cholesterol
demand for corticosteroid synthesis in female HL0 mice. In female mice,
plasma corticosteroid levels are twice as high as in male mice and the
cholesterol storage defect is more severe in female than male apoA-I0
mice (8). The cholesterol storage defect in female HL0 mice was not as
severe as in apoA-I0 mice of either sex (8). This is consistent with
the idea that HL may act on apoA-I-containing HDL particles to optimize
the selective uptake process in the adrenal gland (Fig. 5). A defect in
cholesterol storage results from both suboptimal delivery of
cholesterol by selective uptake as well as higher utilization in female
mice.
Our data suggesting that HL activity is required for optimal selective
uptake of HDL free cholesterol and/or cholesteryl ester by the adrenal
are consistent with earlier studies of selective uptake in cell culture
(9, 10). HL enhances the selective uptake of both free cholesterol and
cholesteryl ester by hepatocytes in vitro, with a major
effect on free cholesterol and a much smaller effect on cholesteryl
ester. HL action also is required for the conversion of large HDL to
smaller, more dense HDL particles (12, 13). The more dense HDL-3
species, which are deficient in HL0 mice (14), are the optimal
substrates for selective uptake in rodents (15). Further studies will
be required to differentiate whether the action of HL primarily alters
the ligand binding properties of HDL to SR-BI, or acts to enhance
selective uptake after binding has occurred.
The present data suggest that SR-BI is involved in the delivery of HDL
cholesterol to the adrenal and perhaps other steroidogenic tissues and
that a feedback loop governing SR-BI expression helps to increase the
delivery of HDL cholesterol in response to increased need. The lower
expression of SR-BI in the liver and the lack of up-regulation of SR-BI
or change of hepatic cholesterol stores in apoA-I0 mice indicates that
SR-BI plays a less important role in hepatic cholesterol homeostasis
than in the adrenal. However, in apoA-I0 mice bile salt synthesis
appears to be decreased,4 perhaps acting as
a compensatory mechanism to maintain hepatic cholesterol stores. Our
data imply that increased hepatic SR-BI expression by interruption of
the feedback loop controlling SR-BI expression in the liver could
result in enhanced reverse cholesterol transport. However, just as
selective uptake in cell culture is down-regulated by cholesterol
loading (16), our studies show an inverse relationship between SR-BI
expression and cellular cholesterol pools. Thus, it appears unlikely
that SR-BI would be up-regulated in peripheral tissues or arterial wall
foam cells as a response to cholesterol loading.
FOOTNOTES REFERENCES
Volume 271, Number 35,
Issue of August 30, 1996
pp. 21001-21004
©1996 by The American Society for Biochemistry and Molecular Biology, Inc.
COMMUNICATION:
IN VIVO EVIDENCE THAT SR-BI IS A FUNCTIONAL HIGH
DENSITY LIPOPROTEIN RECEPTOR UNDER FEEDBACK CONTROL*
,¶
Division of Molecular Medicine, Department
of Medicine, Columbia University, New York, New York 10032 and the
§ Laboratory of Biochemical Genetics and Metabolism, The
Rockefeller University, New York, New York 10021
-actin antisense
riboprobes were prepared by in vitro transcription using
murine SR-BI and -actin cDNA plasmid constructs. The protected
hybrid fragments for SR-BI and -actin were 290 and 160 bp,
respectively. The RNase protection assay was described in detail
previously (5). In brief, 20 µg of liver total RNA or 5 µg of
adrenal gland total RNA were hybridized with 5×105 cpm
SR-BI and -actin riboprobes at 48 °C overnight in 30 µl of a
buffer consisting of 40 m Pipes, pH 6.4, 400 m NaCl, 1 m EDTA, and 80% formamide. The
hybridization mixture was digested with 20 units of T2
ribonuclease at 37 °C for 1 h, extracted with
phenol/chloroform, precipitated with ethanol, and dissolved in 5 µl
of RNA loading buffer. The protected RNA hybride fragments were
resolved on a 5% polyacrylamide/urea gel and subjected to
autoradiography.
Fig. 1.
Tissue distribution of SR-BI mRNA.
Total RNA was prepared from individual tissues of C57BL/6 wild type
mice. Ribonuclease protection assay (RPA) for SR-BI and
actin mRNAs was performed as described under ``Experimental
Procedures.''
Fig. 2.
SR-BI mRNA expression in adrenal gland
and liver in the wild type mice and induced mutant mice. Panel
A, adrenal glands pooled from 3-4 female mice of each line were
used to prepare total RNA. 10 µg of RNA was subjected to RPA.
Panel B, each protected band was quantitated with a
phosphorimager and normalized to actin content. The histogram
represents mean ± S.D. for three different pools of adrenal gland
(total of 9 mice). The asterisk indicates p < 0.01 by Student's t test. Panel C, RPA of
liver RNA; 20 µg of total RNA was used.
Fig. 3.
Adrenal gland SR-BI mRNA and cholesterol
content in HL0 mice. The open bar (
) denotes C57BL/6
wild type mice and the filled bar (
) represents HL0 mice.
Panel A, the adrenal pooled from 3-4 3-month-old HL0 mice
were used for RNA preparation. The results represent an average of two
RPAs. Panel B, adrenal total and free cholesterol
(FC) of female HL0 mice were determined as described under
``Experimental Procedures.'' Cholesteryl ester (CE)
content was estimated by subtraction of free cholesterol from total
cholesterol. The results represent mean ± S.D. from three pools,
each consisting of 4 female mice. The asterisk indicates
p < 0.01 (**) and p < 0.05 (*),
respectively. Panel C, adrenal cholesterol content of male
HL0 mice.
Fig. 4.
Expression of SR-BI in murine adrenal Y1
cells. Y1 cells were maintained in Ham's F-12 medium plus 20%
horse serum, and, on the day of experiment, the cells were treated as
indicated for 8 h. Total RNA was prepared, and 20 µg of RNA were
subjected to RPA.
Fig. 5.
Schematic representation of the possible
feedback regulation of SR-BI expression. SR-BI mediates selective
uptake of HDL cholesteryl ester and free cholesterol into adrenal
cells. This process is enhanced by hepatic lipase activity. Free
cholesterol or its derivatives down-regulate SR-BI expression via a
feedback loop. Cellular cholesterol ester (CE) stores are in
equilibrium with free cholesterol (FC) stores, and may possibly be
directly replenished as a result of SR-BI activity.
¶
To whom correspondence should be addressed: Div. of Molecular
Medicine, Columbia University, 630 W. 168th St., New York, NY
10032.
1
The abbreviations used are: HDL, high density
lipoprotein; apoA-I0, apolipoprotein A-I knock-out; apoA-II0,
apolipoprotein A-II knock-out; apoE0, apolipoprotein E knock-out;
LDLR0, low density lipoprotein receptor knock-out; apoA-I,
apolipoprotein A-I; HL0, hepatic lipase knock-out; HL, hepatic lipase;
apoA-I, apolipoprotein A-I; SR-BI, scavenger receptor BI; ACTH,
adrenocorticotropic hormone; PIPES, 1,4-piperazinediethanesulfonic
acid.
2
A. S. Plump, T. Hayek, A. Walsh, and J. L. Breslow, submitted for publication.
3
W. Weng, T. Hayek, and J. L. Breslow, manuscript
in preparation.
4
A. S. Plump, N. Azrolan, H. Odaka, L. Wu, X. Jiang, A. Tall, S. Eisenberg, and J. L. Breslow, submitted for
publication.
©1996 by The American Society for Biochemistry and Molecular Biology, Inc.
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S. F. Cai, R. J. Kirby, P. N. Howles, and D. Y. Hui Differentiation-dependent expression and localization of the class B type I scavenger receptor in intestine J. Lipid Res., June 1, 2001; 42(6): 902 - 909. [Abstract] [Full Text]
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H. L. Dichek, S. M. Johnson, H. Akeefe, G. T. Lo, E. Sage, C. E. Yap, and R. W. Mahley Hepatic lipase overexpression lowers remnant and LDL levels by a noncatalytic mechanism in LDL receptor-deficient mice J. Lipid Res., February 1, 2001; 42(2): 201 - 210. [Abstract] [Full Text]
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V. Terpstra, E. S. van Amersfoort, A. G. van Velzen, J. Kuiper, and T. J. C. van Berkel Hepatic and Extrahepatic Scavenger Receptors : Function in Relation to Disease Arterioscler. Thromb. Vasc. Biol., August 1, 2000; 20(8): 1860 - 1872. [Full Text] [PDF]
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G. Lambert, M. J. A. Amar, P. Martin, J. Fruchart-Najib, B. Föger, R. D. Shamburek, H. B. Brewer , Jr., and S. Santamarina-Fojo Hepatic lipase deficiency decreases the selective uptake of HDL-cholesteryl esters in vivo J. Lipid Res., May 1, 2000; 41(5): 667 - 672. [Abstract] [Full Text]
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D. Huszar, M. L. Varban, F. Rinninger, R. Feeley, T. Arai, V. Fairchild-Huntress, M. J. Donovan, and A. R. Tall Increased LDL Cholesterol and Atherosclerosis in LDL Receptor-Deficient Mice With Attenuated Expression of Scavenger Receptor B1 Arterioscler. Thromb. Vasc. Biol., April 1, 2000; 20(4): 1068 - 1073. [Abstract] [Full Text] [PDF]
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E. Reaven, L. Zhan, A. Nomoto, S. Leers-Sucheta, and S. Azhar Expression and microvillar localization of scavenger receptor class B, type I (SR-BI) and selective cholesteryl ester uptake in Leydig cells from rat testis J. Lipid Res., March 1, 2000; 41(3): 343 - 356. [Abstract] [Full Text]
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C. J. Schultz, E. J. Blanchette-Mackie, and R. O. Scow Adrenal and liver in normal and cld/cld mice synthesize and secrete hepatic lipase, but the lipase is inactive in cld/cld mice J. Lipid Res., February 1, 2000; 41(2): 214 - 225. [Abstract] [Full Text]
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D. Lopez and M. P. McLean Sterol Regulatory Element-Binding Protein-1a Binds to cis Elements in the Promoter of the Rat High Density Lipoprotein Receptor SR-BI Gene Endocrinology, December 1, 1999; 140(12): 5669 - 5681. [Abstract] [Full Text]
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Y. Ji, N. Wang, R. Ramakrishnan, E. Sehayek, D. Huszar, J. L. Breslow, and A. R. Tall Hepatic Scavenger Receptor BI Promotes Rapid Clearance of High Density Lipoprotein Free Cholesterol and Its Transport into Bile J. Biol. Chem., November 19, 1999; 274(47): 33398 - 33402. [Abstract] [Full Text] [PDF]
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 T. Arai, F. Rinninger, L. Varban, V. Fairchild-Huntress, C.-P. Liang, W. Chen, T. Seo, R. Deckelbaum, D. Huszar, and A. R. Tall Decreased selective uptake of high density lipoprotein cholesteryl esters in apolipoprotein E knock-out mice PNAS, October 12, 1999; 96(21): 12050 - 12055. [Abstract] [Full Text] [PDF]
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Y. Sun, N. Wang, and A. R. Tall Regulation of adrenal scavenger receptor-BI expression by ACTH and cellular cholesterol pools J. Lipid Res., October 1, 1999; 40(10): 1799 - 1805. [Abstract] [Full Text]
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 G. Cao, L. Zhao, H. Stangl, T. Hasegawa, J. A. Richardson, K. L. Parker, and H. H. Hobbs Developmental and Hormonal Regulation of Murine Scavenger Receptor, Class B, Type 1 Mol. Endocrinol., September 1, 1999; 13(9): 1460 - 1473. [Abstract] [Full Text]
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B. Trigatti, H. Rayburn, M. Vinals, A. Braun, H. Miettinen, M. Penman, M. Hertz, M. Schrenzel, L. Amigo, A. Rigotti, et al. Influence of the high density lipoprotein receptor SR-BI on reproductive and cardiovascular pathophysiology PNAS, August 3, 1999; 96(16): 9322 - 9327. [Abstract] [Full Text] [PDF]
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D. K. Spady, D. M. Kearney, and H. H. Hobbs Polyunsaturated fatty acids up-regulate hepatic scavenger receptor B1 (SR-BI) expression and HDL cholesteryl ester uptake in the hamster J. Lipid Res., August 1, 1999; 40(8): 1384 - 1394. [Abstract] [Full Text]
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W. V. Rodrigueza, S. T. Thuahnai, R. E. Temel, S. Lund-Katz, M. C. Phillips, and D. L. Williams Mechanism of Scavenger Receptor Class B Type I-mediated Selective Uptake of Cholesteryl Esters from High Density Lipoprotein to Adrenal Cells J. Biol. Chem., July 16, 1999; 274(29): 20344 - 20350. [Abstract] [Full Text] [PDF]
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X. Collet, A. R. Tall, H. Serajuddin, K. Guendouzi, L. Royer, H. Oliveira, R. Barbaras, X.-c. Jiang, and O. L. Francone Remodeling of HDL by CETP in vivo and by CETP and hepatic lipase in vitro results in enhanced uptake of HDL CE by cells expressing scavenger receptor B-I J. Lipid Res., July 1, 1999; 40(7): 1185 - 1193. [Abstract] [Full Text]
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G. Lambert, M. B. Chase, K. Dugi, A. Bensadoun, H. B. Brewer , Jr., and S. Santamarina-Fojo Hepatic lipase promotes the selective uptake of high density lipoprotein-cholesteryl esters via the scavenger receptor B1 J. Lipid Res., July 1, 1999; 40(7): 1294 - 1303. [Abstract] [Full Text]
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S. Acton, D. Osgood, M. Donoghue, D. Corella, M. Pocovi, A. Cenarro, P. Mozas, J. Keilty, S. Squazzo, E. A. Woolf, et al. Association of Polymorphisms at the SR-BI Gene Locus With Plasma Lipid Levels and Body Mass Index in a White Population Arterioscler. Thromb. Vasc. Biol., July 1, 1999; 19(7): 1734 - 1743. [Abstract] [Full Text] [PDF]
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K.-i. Hirata, H. L. Dichek, J. A. Cioffi, S. Y. Choi, N. J. Leeper, L. Quintana, G. S. Kronmal, A. D. Cooper, and T. Quertermous Cloning of a Unique Lipase from Endothelial Cells Extends the Lipase Gene Family J. Biol. Chem., May 14, 1999; 274(20): 14170 - 14175. [Abstract] [Full Text] [PDF]
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F. Rinninger, N. Wang, R. Ramakrishnan, X. C. Jiang, and A. R. Tall Probucol Enhances Selective Uptake of HDL-Associated Cholesteryl Esters In Vitro by a Scavenger Receptor B-I–Dependent Mechanism Arterioscler. Thromb. Vasc. Biol., May 1, 1999; 19(5): 1325 - 1332. [Abstract] [Full Text] [PDF]
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K. Fluiter, W. Sattler, M. C. De Beer, P. M. Connell, D. R. van der Westhuyzen, and T. J. C. van Berkel Scavenger Receptor BI Mediates the Selective Uptake of Oxidized Cholesterol Esters by Rat Liver J. Biol. Chem., March 26, 1999; 274(13): 8893 - 8899. [Abstract] [Full Text] [PDF]
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Y. Ueda, L. Royer, E. Gong, J. Zhang, P. N. Cooper, O. Francone, and E. M. Rubin Lower Plasma Levels and Accelerated Clearance of High Density Lipoprotein (HDL) and Non-HDL Cholesterol in Scavenger Receptor Class B Type I Transgenic Mice J. Biol. Chem., March 12, 1999; 274(11): 7165 - 7171. [Abstract] [Full Text] [PDF]
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D. L. Silver, X.-c. Jiang, and A. R. Tall Increased High Density Lipoprotein (HDL), Defective Hepatic Catabolism of ApoA-I and ApoA-II, and Decreased ApoA-I mRNA in ob/ob Mice. POSSIBLE ROLE OF LEPTIN IN STIMULATION OF HDL TURNOVER J. Biol. Chem., February 12, 1999; 274(7): 4140 - 4146. [Abstract] [Full Text] [PDF]
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N. H. Fidge High density lipoprotein receptors, binding proteins, and ligands J. Lipid Res., February 1, 1999; 40(2): 187 - 201. [Abstract] [Full Text]
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T. Arai, N. Wang, M. Bezouevski, C. Welch, and A. R. Tall Decreased Atherosclerosis in Heterozygous Low Density Lipoprotein Receptor-deficient Mice Expressing the Scavenger Receptor BI Transgene J. Biol. Chem., January 22, 1999; 274(4): 2366 - 2371. [Abstract] [Full Text] [PDF]
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N. Bergeron, L. Kotite, M. Verges, P. Blanche, R. L. Hamilton, R. M. Krauss, A. Bensadoun, and R. J. Havel Lamellar lipoproteins uniquely contribute to hyperlipidemia in mice doubly deficient in apolipoprotein E and hepatic lipase PNAS, December 22, 1998; 95(26): 15647 - 15652. [Abstract] [Full Text] [PDF]
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N. Wang, T. Arai, Y. Ji, F. Rinninger, and A. R. Tall Liver-specific Overexpression of Scavenger Receptor BI Decreases Levels of Very Low Density Lipoprotein ApoB, Low Density Lipoprotein ApoB, and High Density Lipoprotein in Transgenic Mice J. Biol. Chem., December 4, 1998; 273(49): 32920 - 32926. [Abstract] [Full Text] [PDF]
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D. V.-v. Bruggen, I. Kalkman, T. van Gent, A. van Tol, and H. Jansen Induction of Adrenal Scavenger Receptor BI and Increased High Density Lipoprotein-Cholesteryl Ether Uptake by in Vivo Inhibition of Hepatic Lipase J. Biol. Chem., November 27, 1998; 273(48): 32038 - 32041. [Abstract] [Full Text] [PDF]
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H. Stangl, G. Cao, K. L. Wyne, and H. H. Hobbs Scavenger Receptor, Class B, Type I-dependent Stimulation of Cholesterol Esterification by High Density Lipoproteins, Low Density Lipoproteins, and Nonlipoprotein Cholesterol J. Biol. Chem., November 20, 1998; 273(47): 31002 - 31008. [Abstract] [Full Text] [PDF]
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X. Gu, B. Trigatti, S. Xu, S. Acton, J. Babitt, and M. Krieger The Efficient Cellular Uptake of High Density Lipoprotein Lipids via Scavenger Receptor Class B Type I Requires Not Only Receptor-mediated Surface Binding but Also Receptor-specific Lipid Transfer Mediated by Its Extracellular Domain J. Biol. Chem., October 9, 1998; 273(41): 26338 - 26348. [Abstract] [Full Text] [PDF]
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S. Azhar, A. Nomoto, S. Leers-Sucheta, and E. Reaven Simultaneous induction of an HDL receptor protein (SR-BI) and the selective uptake of HDL-cholesteryl esters in a physiologically relevant steroidogenic cell model J. Lipid Res., August 1, 1998; 39(8): 1616 - 1628. [Abstract] [Full Text]
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D. K. Spady, L. A. Woollett, R. S. Meidell, and H. H. Hobbs Kinetic characteristics and regulation of HDL cholesteryl ester and apolipoprotein transport in the apoA-I-/- mouse J. Lipid Res., July 1, 1998; 39(7): 1483 - 1492. [Abstract] [Full Text]
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N. R. Webb, P. M. Connell, G. A. Graf, E. J. Smart, W. J. S. de Villiers, F. C. de Beer, and D. R. van der Westhuyzen SR-BII, an Isoform of the Scavenger Receptor BI Containing an Alternate Cytoplasmic Tail, Mediates Lipid Transfer between High Density Lipoprotein and Cells J. Biol. Chem., June 12, 1998; 273(24): 15241 - 15248. [Abstract] [Full Text] [PDF]
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B. Lamarche, K. D. Uffelman, G. Steiner, P. H. R. Barrett, and G. F. Lewis Analysis of particle size and lipid composition as determinants of the metabolic clearance of human high density lipoproteins in a rabbit model J. Lipid Res., June 1, 1998; 39(6): 1162 - 1172. [Abstract] [Full Text]
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E. Reaven, A. Nomoto, S. Leers-Sucheta, R. Temel, D. L. Williams, and S. Azhar Expression and Microvillar Localization of Scavenger Receptor, Class B, Type I (a High Density Lipoprotein Receptor) in Luteinized and Hormone-Desensitized Rat Ovarian Models Endocrinology, June 1, 1998; 139(6): 2847 - 2856. [Abstract] [Full Text] [PDF]
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M. Krieger The "best" of cholesterols, the "worst" of cholesterols: A tale of two receptors PNAS, April 14, 1998; 95(8): 4077 - 4080. [Full Text] [PDF]
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M. L. Varban, F. Rinninger, N. Wang, V. Fairchild-Huntress, J. H. Dunmore, Q. Fang, M. L. Gosselin, K. L. Dixon, J. D. Deeds, S. L. Acton, et al. Targeted mutation reveals a central role for SR-BI in hepatic selective uptake of high density lipoprotein cholesterol PNAS, April 14, 1998; 95(8): 4619 - 4624. [Abstract] [Full Text] [PDF]
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K. Fluiter, D. R. van der Westhuijzen, and T. J. C. van Berkel In Vivo Regulation of Scavenger Receptor BI and the Selective Uptake of High Density Lipoprotein Cholesteryl Esters in Rat Liver Parenchymal and Kupffer Cells J. Biol. Chem., April 3, 1998; 273(14): 8434 - 8438. [Abstract] [Full Text] [PDF]
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B. Jian, M. de la Llera-Moya, Y. Ji, N. Wang, M. C. Phillips, J. B. Swaney, A. R. Tall, and G. H. Rothblat Scavenger Receptor Class B Type I as a Mediator of Cellular Cholesterol Efflux to Lipoproteins and Phospholipid Acceptors J. Biol. Chem., March 6, 1998; 273(10): 5599 - 5606. [Abstract] [Full Text] [PDF]
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A. K. Hatzopoulos, A. Rigotti, R. D. Rosenberg, and M. Krieger Temporal and spatial pattern of expression of the HDL receptor SR-BI during murine embryogenesis J. Lipid Res., March 1, 1998; 39(3): 495 - 508. [Abstract] [Full Text]
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 S. Azhar, L. Tsai, S. Medicherla, Y. Chandrasekher, L. Giudice, and E. Reaven Human Granulosa Cells Use High Density Lipoprotein Cholesterol for Steroidogenesis J. Clin. Endocrinol. Metab., March 1, 1998; 83(3): 983 - 991. [Abstract] [Full Text]
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H. L. Dichek, W. Brecht, J. Fan, Z.-S. Ji, S. P. A. McCormick, H. Akeefe, L. Conzo, D. A. Sanan, K. H. Weisgraber, S. G. Young, et al. Overexpression of Hepatic Lipase in Transgenic Mice Decreases Apolipoprotein B-containing and High Density Lipoproteins. EVIDENCE THAT HEPATIC LIPASE ACTS AS A LIGAND FOR LIPOPROTEIN UPTAKE J. Biol. Chem., January 23, 1998; 273(4): 1896 - 1903. [Abstract] [Full Text] [PDF]
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M. S. C. Johnson, P.-A. Svensson, K. Helou, H. Billig, G. Levan, L. M. S. Carlsson, and B. Carlsson Characterization and Chromosomal Localization of Rat Scavenger Receptor Class B Type I, a High Density Lipoprotein Receptor with a Putative Leucine Zipper Domain and Peroxisomal Targeting Sequence Endocrinology, January 1, 1998; 139(1): 72 - 80. [Abstract] [Full Text] [PDF]
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Z.-S. Ji, H. L. Dichek, R. D. Miranda, and R. W. Mahley Heparan Sulfate Proteoglycans Participate in Hepatic Lipaseand Apolipoprotein E-mediated Binding and Uptake of Plasma Lipoproteins, Including High Density Lipoproteins J. Biol. Chem., December 12, 1997; 272(50): 31285 - 31292. [Abstract] [Full Text] [PDF]
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R. E. Temel, B. Trigatti, R. B. DeMattos, S. Azhar, M. Krieger, and D. L. Williams Scavenger receptor class B, type I (SR-BI) is the major route for the delivery of high density lipoprotein cholesterol to the steroidogenic pathway in cultured mouse adrenocortical cells PNAS, December 9, 1997; 94(25): 13600 - 13605. [Abstract] [Full Text] [PDF]
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A. Rigotti, B. L. Trigatti, M. Penman, H. Rayburn, J. Herz, and M. Krieger A targeted mutation in the murine gene encoding the high density lipoprotein (HDL) receptor scavenger receptor class B type I reveals its key role in HDL metabolism PNAS, November 11, 1997; 94(23): 12610 - 12615. [Abstract] [Full Text] [PDF]
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D. Calvo, D. Gomez-Coronado, M. A. Lasuncion, and M. A. Vega CLA-1 Is an 85-kD Plasma Membrane Glycoprotein That Acts as a High-Affinity Receptor for Both Native (HDL, LDL, and VLDL) and Modified (OxLDL and AcLDL) Lipoproteins Arterioscler. Thromb. Vasc. Biol., November 1, 1997; 17(11): 2341 - 2349. [Abstract] [Full Text]
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F. Benoist, P. Lau, M. McDonnell, H. Doelle, R. Milne, and R. McPherson Cholesteryl Ester Transfer Protein Mediates Selective Uptake of High Density Lipoprotein Cholesteryl Esters by Human Adipose Tissue J. Biol. Chem., September 19, 1997; 272(38): 23572 - 23577. [Abstract] [Full Text] [PDF]
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O. Stein, Y. Dabach, G. Hollander, M. Ben-Naim, G. Halperin, J. L. Breslow, and Y. Stein Delayed loss of cholesterol from a localized lipoprotein depot in apolipoprotein A-I-deficient mice PNAS, September 2, 1997; 94(18): 9820 - 9824. [Abstract] [Full Text] [PDF]
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Y. Ji, B. Jian, N. Wang, Y. Sun, M. d. l. L. Moya, M. C. Phillips, G. H. Rothblat, J. B. Swaney, and A. R. Tall Scavenger Receptor BI Promotes High Density Lipoprotein-mediated Cellular Cholesterol Efflux J. Biol. Chem., August 22, 1997; 272(34): 20982 - 20985. [Abstract] [Full Text] [PDF]
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J. Liu, R. Voutilainen, P. Heikkila, and A. I. Kahri Ribonucleic Acid Expression of the CLA-1 Gene, a Human Homolog to Mouse High Density Lipoprotein Receptor SR-BI, in Human Adrenal Tumors and Cultured Adrenal Cells J. Clin. Endocrinol. Metab., August 1, 1997; 82(8): 2522 - 2527. [Abstract] [Full Text] [PDF]
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K. Murao, V. Terpstra, S. R. Green, N. Kondratenko, D. Steinberg, and O. Quehenberger Characterization of CLA-1, a Human Homologue of Rodent Scavenger Receptor BI, as a Receptor for High Density Lipoprotein and Apoptotic Thymocytes J. Biol. Chem., July 11, 1997; 272(28): 17551 - 17557. [Abstract] [Full Text] [PDF]
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D. S. Ng, O. L. Francone, T. M. Forte, J. Zhang, M. Haghpassand, and E. M. Rubin Disruption of the Murine Lecithin:Cholesterol Acyltransferase Gene Causes Impairment of Adrenal Lipid Delivery and Up-regulation of Scavenger Receptor Class B Type I J. Biol. Chem., June 20, 1997; 272(25): 15777 - 15781. [Abstract] [Full Text] [PDF]
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W. V. Rodrigueza, K. J. Williams, G. H. Rothblat, and M. C. Phillips Remodeling and Shuttling: Mechanisms for the Synergistic Effects Between Different Acceptor Particles in the Mobilization of Cellular Cholesterol Arterioscler. Thromb. Vasc. Biol., February 1, 1997; 17(2): 383 - 393. [Abstract] [Full Text]
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A. Rigotti, E. R. Edelman, P. Seifert, S. N. Iqbal, R. B. DeMattos, R. E. Temel, M. Krieger, and D. L. Williams Regulation by Adrenocorticotropic Hormone of the in Vivo Expression of Scavenger Receptor Class B Type I (SR-BI), a High Density Lipoprotein Receptor, in Steroidogenic Cells of the Murine Adrenal Gland J. Biol. Chem., December 27, 1996; 271(52): 33545 - 33549. [Abstract] [Full Text] [PDF]
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T. Mizutani, K. Yamada, T. Minegishi, and K. Miyamoto Transcriptional Regulation of Rat Scavenger Receptor Class B Type I Gene J. Biol. Chem., July 14, 2000; 275(29): 22512 - 22519. [Abstract] [Full Text] [PDF]
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K. N. Liadaki, T. Liu, S. Xu, B. Y. Ishida, P. N. Duchateaux, J. P. Krieger, J. Kane, M. Krieger, and V. I. Zannis Binding of High Density Lipoprotein (HDL) and Discoidal Reconstituted HDL to the HDL Receptor Scavenger Receptor Class B Type I. EFFECT OF LIPID ASSOCIATION AND APOA-I MUTATIONS ON RECEPTOR BINDING J. Biol. Chem., July 7, 2000; 275(28): 21262 - 21271. [Abstract] [Full Text] [PDF]
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S. Urban, S. Zieseniss, M. Werder, H. Hauser, R. Budzinski, and B. Engelmann Scavenger Receptor BI Transfers Major Lipoprotein-associated Phospholipids into the Cells J. Biol. Chem., October 20, 2000; 275(43): 33409 - 33415. [Abstract] [Full Text] [PDF]
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T. A. Ramsamy, T. A.-M. Neville, B. M. Chauhan, D. Aggarwal, and D. L. Sparks Apolipoprotein A-I Regulates Lipid Hydrolysis by Hepatic Lipase J. Biol. Chem., October 20, 2000; 275(43): 33480 - 33486. [Abstract] [Full Text] [PDF]
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N. Wang, D. L. Silver, P. Costet, and A. R. Tall Specific Binding of ApoA-I, Enhanced Cholesterol Efflux, and Altered Plasma Membrane Morphology in Cells Expressing ABC1 J. Biol. Chem., October 13, 2000; 275(42): 33053 - 33058. [Abstract] [Full Text] [PDF]
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J. Han, A. C. Nicholson, X. Zhou, J. Feng, A. M. Gotto Jr., and D. P. Hajjar Oxidized Low Density Lipoprotein Decreases Macrophage Expression of Scavenger Receptor B-I J. Biol. Chem., May 4, 2001; 276(19): 16567 - 16572. [Abstract] [Full Text] [PDF]
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H. Tsuruoka, W. Khovidhunkit, B. E. Brown, J. W. Fluhr, P. M. Elias, and K. R. Feingold Scavenger Receptor Class B Type I Is Expressed in Cultured Keratinocytes and Epidermis. REGULATION IN RESPONSE TO CHANGES IN CHOLESTEROL HOMEOSTASIS AND BARRIER REQUIREMENTS J. Biol. Chem., January 18, 2002; 277(4): 2916 - 2922. [Abstract] [Full Text] [PDF]
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