Transcriptional Coactivator PRIP, the Peroxisome Proliferator-activated Receptor
(PPAR
)-interacting Protein, Is Required for PPAR
-mediated Adipogenesis*
Chao Qi,
Sailesh Surapureddi,
Yi-Jun Zhu,
Songtao Yu,
Papreddy Kashireddy,
M. Sambasiva Rao and
Janardan K. Reddy
From the
Department of Pathology, Northwestern University, The Feinberg School of
Medicine, Chicago, Illinois 60611-3008
Received for publication, April 23, 2003
 |
ABSTRACT
|
---|
Nuclear receptor coactivator PRIP (peroxisome proliferators-activated
receptor (PPAR
)-interacting protein) appears to serve as a linker
between cAMP response element-binding protein-binding protein
(CBP/p300)anchored and PBP (PPAR
-binding protein)-anchored coactivator
complexes involved in the transcriptional activity of nuclear receptors.
Disruption of PRIP and PBP genes results in embryonic lethality between
embryonic day 11.5 and 12.5 (postcoitum), indicating that PRIP and PBP are
essential and nonredundant coactivators. Both PRIP and PBP were initially
identified as PPAR
coactivators, suggesting a role for these molecules
in PPAR
-induced adipogenesis.
PBP/ mouse embryonic
fibroblasts fail to exhibit PPAR
-stimulated adipogenesis indicating
that PBP is a downstream regulator of PPAR
-mediated adipogenesis. We
now show that PRIP/ mouse
embryonic fibroblasts are also refractory to PPAR
-stimulated
adipogenesis and fail to express adipogenic marker aP2, a
PPAR
-responsive gene. Chromatin immunoprecipitation assays reveal
reduced association in PRIP/
cells of PIMT (PRIP-binding protein) and PBP with aP2 gene promoter,
suggesting that PRIP is required for the linking of CBP/p300-anchored cofactor
complex with PBP-anchored mediator complex. These data indicate that PRIP,
like PBP, is a downstream regulator of PPAR
-mediated adipogenesis and
that both these coactivators are required for the successful completion of
adipogenic program.
 |
INTRODUCTION
|
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Peroxisome proliferator-activated receptor
(PPAR)1 isoforms,
and
, function as important coregulators of energy (lipid)
homeostasis
(13).
PPAR
regulates energy combustion by serving as a key regulator of
transcriptional pathways controlling fatty acid oxidation, whereas PPAR
functions as an important regulator of adipocyte differentiation and lipid
storage (2,
3). PPAR
is present in
two major isoforms, PPAR
1 and PPAR
2, resulting from alternate
promoter usage (4).
PPAR
2 contains additional 30 amino acids at the N-terminal end relative
to PPAR
1, with PPAR
2 expression limited exclusively to adipose
tissue where it plays a key role in adipogenesis
(5). Recent studies have
established that forced expression of PPAR
2 or PPAR
1 can
stimulate the differentiation of fibroblasts to adipocytes, and in the process
transcriptional pathways essential for the expression of adipocyte specific
genes are activated resulting in lipid accumulation
(6). Overexpression of
PPAR
1 in mouse liver has also been shown to be sufficient for the
induction of adipogenic transformation of hepatocytes with adipose
tissue-specific gene expression and lipid accumulation
(7). In addition to
PPAR
, CCAAT/enhancer binding family of transcription factors
C/EBP
, -
, and -
, also direct fibroblasts to differentiate
into adipocytes (2). The
C/EBP-directed adipocyte conversion is mediated through down-stream regulator
PPAR
(2).
Transcriptional activity of PPAR
and of other nuclear receptors is
regulated by the binding of specific ligands and by the recruitment of nuclear
receptor coactivators or coregulators
(8,
9). The binding of ligands to
nuclear receptors influences the recruitment of initial complex of coactivator
proteins such as members of p160/SRC-1 family, and CREB-binding protein (CBP),
which exhibit histone acteyltransferase activity necessary for remodeling
chromatin (8,
9). Docking of other
coactivators, either sequentially or combinatorially, manifests as a second
multiprotein complex, variously referred to as TRAP-DRIP-ARC mediator complex,
which facilitates interaction with RNA polymerase II complexes of the basal
transcription machinery
(1012).
This second complex, devoid of histone acetyltransferase activity, is anchored
by PPAR
-binding protein (PBP), which was initially cloned as
PPAR
-binding nuclear receptor coactivator
(13). PPAR
also binds
to PPAR
-interacting protein (PRIP/ASC2/RAP250/NRC/TRBP)
(1418),
which is also capable of interacting with several other nuclear receptors and
with CBP/p300 and TRAP130 of the PBP-anchored TRAP-DRIP-ARC complex. In
addition, PRIP-interacting protein with RNA methyltransferase activity,
designated PIMT (19), forms a
complex with CBP/p300, and PBP
(20). Thus, the interactions
of PRIP with CBP and TRAP130, and of PIMT with PRIP, CBP, and PBP raise the
possibility that two major multiprotein cofactor complexes anchored by
CBP/p300 and PBP, respectively, merge into one mega-complex on DNA template
(21).
Evidence obtained from gene knock-out studies has established that both PBP
and PRIP null mutations lead to embryonic lethality, implying that these
coactivators influence the physiological functions of many nuclear receptors
and possibly other transcription factors
(2226).
Recent studies have also established the critical role for PBP/TRAP220 in
PPAR
-stimulated adipogenesis in that
PBP/ mouse embryonic
fibroblasts (MEFs) were found refractory to adipocyte differentiation
(27). Since PRIP is also a
PPAR
coactivator and the disruption of the PRIP gene resulted in lethal
phenotype, it appeared necessary to investigate the role of this coactivator
in PPAR
-stimulated adipogenesis. Here we show that
PRIP/ MEFs fail to exhibit
PPAR
1-stimulated adipogenesis even in the presence of PBP, suggesting
the need for the presence of both PBP and PRIP for PPAR
-directed
adipogenesis.
 |
MATERIALS AND METHODS
|
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Construction of Retrovirus VectorThe retroviral vector
expressing PPAR
1 was constructed by inserting mouse PPAR
1 cDNA
isolated from PCMV-PPAR
1 into pMSCVneo and the construct was verified
by sequencing. Pheonix ecotropic retrovirus packaging cells and PT67 cells
(Clontech) were cultured in Dulbecco's modified Eagle's medium with 10% fetal
bovine serum. Recombinant retroviruses were produced by transfecting Pheonix
cells seeded at a density of 6 x 106 cells per 10-cm dish
with 15 µg of retrovirus vector by LipofectAMINE 2000 reagent (Invitrogen).
Twenty-four hours after transfection, the cells were changed to fresh medium
and cultured for another 24 h. Virus-containing medium was then filtered
through 0.45-µm membrane and added to 1 x 105 PT67 cells
with 5 µg/ml polybrene (Sigma). Twenty-four hours after virus infection,
the cells were selected with 200 µg/ml G418 containing medium for 8 days.
Surviving PT67 cells were grown into confluence.
Immortalization of Wild-type and
PRIP/
Embryonic Fibroblasts Wild type and
PRIP/ primary MEFs
were isolated from E11.5 littermate embryos as described
(24). Self-immortalization of
the MEFs was achieved by re-plating the cells every 3 days at a density of 2.6
x 106 continuously for more than 5 months.
PBP/ MEFs were obtained as
described previously (22).
Cell Culture, Retrovirus Infection of MEFs, and Induction of
AdipogenesisMEF cell lines were grown in Dulbecco's modified
Eagle's medium with 10% fetal bovine serum. To infect MEFs with PPAR
retrovirus, 1 x 105 cells were grown for 24 h and changed to
the medium collected from 10-cm plate of virus producing PT67 cells. Cells
were incubated with retrovirus for 24 h and then cultured in fresh medium.
Forty-eight hours after infection, cells were selected with 200 µg/ml G418
for 8 days. Induction of adipogenesis was carried out as described
(5). Briefly, after cells grew
into confluence, they were treated with culture medium containing 0.5
mM 3-isobutyl-1-methyl-xanthine (Sigma), 1 µM
dexamethasone (Sigma), 5 µg/ml insulin (Sigma), and 0.5 µM
rosiglitazone or Me2SO for 48 h. Cells were then changed to the
medium containing 5 µg/ml insulin (Sigma) and 0.5 µM
rosiglitazone or Me2SO. The induction lasted for 8 days with the
medium being replaced every 2 days. The fat droplets in cells that exhibited
adipogenesis were revealed by Oil Red staining.
Northern Analysis and RT-PCRTotal RNA was extracted from
cultured cells using TRIzol (Invitrogen) according to the manufacturer's
instructions. For Northern blotting, 20 µg of total RNA was used for each
sample. To detect PBP mRNA in wild type and
PRIP/ MEFs, RT-PCR was carried
out with primers 5'-TGTATCTGGCTCTCCAATCC-3' and
5'-AGTGATGAGTTCATACAGGGG-3'
(4). To detect PRIP mRNA in
wild type and PBP/ MEFs, RT-PCR
was performed with primers 5'-TTTCATGGTGATGCAGCAGC-3' and
5'-CATCATATTTGGTGGCCCGT-3'
(15). Total RNA (1 µg) was
used for each sample for RT-PCR analysis using One-Step RT-PCR kit
(Invitrogen).
Chromatin Protein Association AssaysFor chromatin
immunoprecipitation (ChIP) assay, cells were cross-linked with 1%
formaldyehyde at room temperature for 10 min and processed for the isolation
of nuclei, which were then sonicated on ice to shear chromosomal DNA
(28). After centrifugation,
the supernatant was diluted 10-fold with dilution buffer (16.7 mM
Tris-Cl, pH 8.1, 1.1% Triton X-100, 1.2 mM EDTA, 167 mM
NaCl) and precleared with preimmune serum-coupled protein A beads and salmon
sperm DNA. Immunoprecipitation was performed by incubating the precleared cell
lysate with specific antibody at 4 °C for 12 h. Immune complexes were
pulled down by protein A-agarose beads and washed sequentially for 10 min each
with washing buffer I (0.1% SDS, 1% Triton-X100, 2 mM EDTA, 20
mM Tris-Cl, pH 8.1, 150 mM NaCl), buffer II (0.1% SDS,
1% Triton X-100, 2 mM EDTA, 20 mM Tris-Cl, pH 8.1, 500
mM NaCl), and buffer III (0.25 M LiCl, 1% Nonidet P-40,
1% deoxycholate, 10 mM Tris-Cl, pH 8.1). DNA in the immune
complexes was extracted and used as the template in PCR reaction.
Immunoprecipitation and Immunoblot AnalysisCells were
infected with His-tagged adenovirus PIMT as described previously
(21). Cells were collected 48
h after virus infection and lysed in lysis buffer (50 mM Tris-Cl,
pH 8.0, 150 mM NaCl, 1% Nonidet P-40, 1 mM DTT, 1
mM EDTA, 0.5 mM PMSF). Immunoprecipitation with anti-His
tag and immunoblotting were carried out as described previously
(20).
 |
RESULTS
|
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PPAR
1-induced Adipogenesis in
PRIP/
MEFsPPAR
plays an essential role in the transcriptional
regulation of adipocyte-specific genes during adipogenesis
(2,
5). Introduction of PPAR
into either primary or immortalized MEFs stimulates adipogenesis
(5,
27). Both PPAR
isoforms, PPAR
1 and PPAR
2, have been shown to have the similar
adipogenic capacity (28). To
test the requirement of PRIP in PPAR
-mediated adipogenesis,
immortalized MEF cell lines were established from E11.5
PRIP/ embryos and their wild
type littermates. PRIP/ mouse
embryos die between E11.5 and E12.5 (postcoitum) due in most part to defects
in the development of placenta, heart, liver, nervous system, and retardation
of embryonic growth
(2426).
Wild type and PRIP/ MEF cell
lines were infected with retroviruses expressing PPAR
1 and then induced
with differentiation medium containing PPAR
ligand rosiglitazone to
maximize cell differentiation or vehicle (dimethyl sulfoxide) alone. Wild type
MEFs expressing PPAR
1 and treated with rosiglitazone exhibited
adipocyte conversion (Fig. 1, A
and C). In contrast, retroviral expression of
PPAR
1 failed to induce adipogenesis in
PRIP/ MEFs even in the presence
of rosiglitazone (Fig. 1, B and
D). Consistent with the morphological changes, mRNA and
protein levels of adipocyte specific gene aP2 were markedly induced in wild
type MEFs exhibiting adipogenesis, whereas aP2 mRNA and protein were not
detectable in PRIP/ MEFs that
failed to reveal adipogenesis (Fig. 2,
A and C). On Northern blotting, PPAR
1
mRNA level in PRIP/ MEFs were
at a higher level than that noted in the wild type MEFs showing the
differentiated morphology (Fig.
2A). These results demonstrated that PPAR
1 was
unable to stimulate adipogenesis in the absence of PRIP. Primary
PRIP/ MEFs also showed defects
in PPAR
1-stimulated adipogenesis (data not shown).

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FIG. 2. Analysis for adipogenic gene expression. A, Northern
analysis for aP2 gene expression. Wild type (+/+) and
PRIP/ MEFs were infected with
retroviral PPAR 1 in the presence (+) or absence () of ligand
rosiglitazone. 28 S RNA used as loading control. B, RT-PCR analysis
to demonstrate PBP mRNA levels in
PRIP/ and
PRIP+/+ MEFs and PRIP mRNA levels in
PBP/ and
PBP+/+ MEFs. C, Immunoblot analysis
to show aP2 expression in differentiated wild type adipocytes. Catalase
immunostaining is used as protein loading control.
|
|
Expression of PBP in
PRIP/
CellsRecently, PPAR
-coactivator PBP, the anchor protein
for TRAP-DRIP-ARC-PRIC complex
(13,
14), has been shown to be
essential for adipogenesis
(27). Since
PBP/ MEFs have been shown to be
defective in PPAR
2-stimulated adipogenesis, it was important to
ascertain the relative levels of PBP mRNA in wild type and
PRIP/ MEFs
(Fig. 2B). PBP mRNA
levels, as assessed by RT-PCR, were essentially similar in wild type and
PRIP/ MEFs. There was also no
difference in the level of PRIP mRNA expression in
PBP/ MEFs
(Fig. 2B). These
results indicate that the defects in PPAR
1-induced adipogenesis caused
by the absence of PRIP and PBP are independent of each other.
Recruitment of PBP, CBP, and PIMT to aP2 Gene Promoter in
PRIP/ MEFs
during AdipogenesisTranscriptional activation by PPAR
requires recruitment of nuclear receptor coactivator complexes to remodel
chromosome structure and facilitate transcriptional initiation
(8,
9). To investigate the impact
of the absence of PRIP on the ability of PPAR
to recruit coactivator
complexes, ChIP assay was utilized to examine the association of aP2 gene
promoter with coactivators in wild type and
PRIP/ MEFs that received
adipogenesis treatment (Fig.
3). Using antibodies against PPAR
, PRIP, CBP, PIMT, or PBP,
protein-DNA immune complexes were pulled down from cell lysates, and the DNA
fragments in the complexes analyzed by PCR with primers
(5'-AAATTCAGAAGAAAGTAAACACATTATT-3' and
5'-ATGCCCTGACCATGTGA-3') spanning the PPAR
-responsive
element (AGGTCAAATGTGT) in the aP2 gene promoter region
(29). The presence of
endogenous PPAR
was detected on the aP2 promoter in wild type and
PRIP/ cells, and this
association was prominent in the presence of ligand. PPAR
occupancy was
increased by expressing exogenous PPAR
and addition of PPAR
ligand. Recruitment of CBP, and PBP to the aP2 promoter by PPAR
, was
not visibly altered in PRIP/
MEFs in response to retroviral expression of PPAR
1, whereas the
recruitment of PIMT to the aP2 promoter in response to exogenous PPAR
1
was less robust in PRIP/ cells
(Fig. 3), suggesting that PRIP
is needed for PIMT recruitment and for the formation of a large multiprotein
transcriptional complex (20,
21).
Interaction of Coactivators in
PRIP/
CellsNuclear receptor coactivators CBP/p300, PBP, PRIP, and
PIMT function in concert to promote transcriptional activation
(8,
9). It appears that PRIP and
PRIP-binding protein PIMT serve as important linkers between CBP/p300- and
PBP-anchored coactivator complexes
(20,
21). To investigate the
interaction of these coactivators in
PRIP/ cells, wild type and
PRIP/ MEFs were infected with adenovirus
expressing His-tagged PIMT
(20). PIMT and its putative
associated proteins were immunoprecipitated with anti-His antibodies, and the
presence of CBP, p300, and PBP in the immunoprecipitate was detected by
immunoblotting (Fig. 4). While
the interaction of PIMT with PBP or p300 was not altered in
PRIP/ cells, binding of PIMT to
CBP was weaker in PRIP/ cells
compared with wild type cells.

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FIG. 4. Immunoprecipitation and immunoblotting to identify PIMT-interacting
proteins in PRIP/ MEFs.
Cell lysates from adeno-PIMT infected wild type and
PRIP/ MEFs were
immunoprecipitated with anti-His tag. The immunoprecipitates were
immunoblotted with anti-PBP, anti-CBP, anti-p300, and anti-HIS (for PIMT). CBP
is barely detected in PIMT immunoprecipitate derived from
PRIP/ cells.
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 |
DISCUSSION
|
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In this study, we have examined the role of nuclear receptor coactivator
PRIP in the PPAR
1-directed adipogenesis using wild type and
PRIP/ MEFs. Our findings
provide evidence that PRIP is required for adipocyte differentiation and for
the expression of adipocyte specific aP2 gene. The refractoriness of
PRIP/ MEFs to
PPAR
-stimulated adipogenesis is similar to that described for
PBP/TRAP220/ MEFs
(27), suggesting that both
PRIP and PBP play important roles in mediating the adipocyte differentiating
effects of PPAR
. These two coactivators were isolated using PPAR
as bait in the yeast two-hybrid screen and were identified as coactivators for
PPAR
and other nuclear receptors
(1318).
PBP has emerged as a central piece in large TRAP-DRIP-ARC-PRIC multiprotein
cofactor complex
(1012,
21), whereas PRIP and
PRIP-binding protein PIMT have been found recently to serve as linkers between
CBP- and PBP-anchored cofactor complexes
(18,
20). The embryonic lethality
observed with the disruption of PBP and PRIP genes and the failure of MEFs
derived from the PBP and PRIP null mutants to differentiate into adipocytes
under PPAR
stimulation suggest that both PBP and PRIP are vital for the
successful completion of transcriptional activity of several genes involved in
adipogenesis and possibly in the development and differentiation necessary for
ontogeny.
The mechanism for the failure of
PRIP/ MEFs to undergo
PPAR
1-stimulated adipogenesis may involve inadequate docking or linkage
between CBP/p300-anchored coactivators with PBP-anchored TRAP-DRIP-ARC-PRIC
multiprotein complex. Since PRIP binds CBP/p300 and TRAP/DRIP130, a component
of TRAP complex, the absence of PRIP most likely interferes with linkage of
CBP/p300-anchored coactivator complex with PBP-anchored complex, thus
curtailing the transcriptional signaling
(18,
20). Absence of PRIP might
further interfere with these protein-protein interactions because PRIP binding
protein PIMT directly binds with both CBP/p300 and PBP
(20). Interestingly, ChIP
assays revealed reductions in PIMT recruitment to the aP2 promoter in response
to exogenous PPAR
1, implying that PRIP is needed to recruit PIMT to the
coactivator complex. ChIP assays also revealed reduction in exogenous
PPAR
1 recruitment to aP2 promoter in
PRIP/ MEFs
(Fig. 3). This may be due to
the requirement of PRIP for the stable formation of PPAR
1-RXR
heterodimers on the aP2 promoter or reduced amount of RXR in
PRIP/ MEFs in that
PRIP/ MEFs were shown to
exhibit marked repression of RXR-mediated transcriptional activity
(24). Immunoprecipitation and
immunoblotting data reveal that in
PRIP/ MEFs the binding of CBP
to PIMT is reduced, and this may also have functional implications.
It is now well established that PPAR
and C/EBP
are critical
transcription factors in adipogenesis
(1,
2). Genetic analysis of
adipogenesis has revealed that PPAR
promotes adipogenesis in
C/EBP
-deficient cells, but the converse is not true in that
C/EBP
has no ability to promote adipogenesis in the absence of
PPAR
(2). The studies of
Ge and co-workers (27) with
PBP/ MEFs, and the observations
reported here using PRIP/ MEFs
clearly establish the importance of these two coactivators in
PPAR
-stimulated adipogenesis. These two coactivators appear to function
as downstream effectors of PPAR
, and both are required for the
successful completion of the adipogenic program. This assumption is based on
the observation that PRIP/ MEFs
used in this study express PBP (Fig.
2B). Likewise
PBP/ MEFs also express PRIP
mRNA to the same level as wild type MEFs, and the absence of either one of
these coactivators interferes with PPAR
-stimulated adipogenesis. In
essence, lack of PBP may result in the disruption of TRAP-DRIP-ARC-PRIC
complex formation and absence of PRIP may interfere with the linkage and
passage of transcriptional signal through the combined CBP/p300- and
PBP-anchored complex. Additional studies are needed to assess the role of PRIP
in in vivo adipogenesis using PRIP conditional null mice.
 |
FOOTNOTES
|
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* This work was supported by National Institutes of Health Grants GM23750 (to
J. K. R.), CA84472 (to M. S. R.), and CA64239 and K08 ES00356 (to Y.-J. Z.)
and by the Joseph L. Mayberry Sr. Endowment Fund. The costs of publication of
this article were defrayed in part by the payment of page charges. This
article must therefore be hereby marked "advertisement"
in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. 
To whom correspondence should be addressed: Dept. of Pathology, Northwestern
University, Feinberg School of Medicine, 303 East Chicago Ave., Chicago, IL
60611-3008. Tel.: 312-503-8144; Fax: 312-503-8249; E-mail:
jkreddy{at}northwestern.edu.
1 The abbreviations used are: PPAR, peroxisome proliferators-activated
receptor; SRC-1, steroid receptor coactivator-1; PBP, PPAR-binding protein;
PRIP, PPAR-interacting protein; PIMT, PRIP-interacting protein with
methyltransferase activity; RXR, retinoid X receptor; CBP, cAMP response
element-binding protein-binding protein; TRAP, thyroid hormone
receptor-associated protein(s); ARC, activator-recruited cofactor; DRIP,
vitamin D3 receptor-interacting protein(s); PRIC,
PPAR
-interacting cofactor complex; ChIP, chromatin immunoprecipitation;
MEFs, mouse embryonic fibroblasts; RT, reverse transcriptase. 
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