From the Vollum Institute, Oregon Health Sciences University, Portland, Oregon 97201
CREB1-binding
protein (CBP) and p300 are believed to participate in the activities of
hundreds of different transcription factors (see Fig.
1). Current models suggest that the
binding of these coactivators to transcription factor activation
domains positions histone acetyltransferases (HATs) near specific
nucleosomes in target gene promoter regions (for review, see Ref. 1).
Interactions with components of the general transcriptional machinery,
such as TFIID, TFIIB, and the RNA polymerase II holoenzyme (RNAPII) have also been suggested to contribute to CBP/p300 function. The simultaneous interaction of multiple transcription factors with CBP/p300 has been proposed to contribute to transcriptional synergy. Conversely, competition for CBP/p300 binding has been suggested to
mediate some examples of signal-induced transcriptional repression. An
overview of CBP/p300 in cellular growth and differentiation has
recently been published (2), but many questions regarding their role in
transcriptional regulation remain unanswered. This review deals with
some of the more controversial aspects of CBP/p300 function. In
particular, we will ask whether CBP and p300 have distinct functions,
review the evidence for their regulation by phosphorylation, and ask
whether they function primarily by acetylating histones or other
proteins. We will also revisit the evidence for the role of CBP/p300 as
transcriptional "integrators." Finally, we will attempt to localize
CBP/p300 function within the complex series of processes involved in
transcriptional activation.
Although CBP and p300 are highly related and share many functional
properties, there is evidence that these factors are not really
interchangeable. Subtle differences in the expression of CBP and p300
during development (3) may explain why knockouts of the two
coactivators in mice result in somewhat distinct phenotypes. For
example, heterozygosity for CBP causes certain hematological defects
and a predisposition to cancer that is not seen in mice lacking one
allele of p300 (4). Studies of specific transcription factor pathways
provide additional evidence of differences between the functions of CBP
and p300. For example, fibroblasts derived from homozygous p300
knockouts are defective for retinoic acid receptor but not CREB
signaling (5). Similarly, ribozyme-mediated ablation of p300, but not
CBP, blocks the retinoic acid receptor response (6). Other differential
functions of CBP and p300 have been revealed by their distinct
interactions with viral transforming proteins. For example, the Kaposi
sarcoma-associated herpesvirus protein vIRF has been reported to be
stimulated by CBP and repressed by p300 (7). Distinct roles for CBP and
p300 have also been suggested in the differentiation of muscle and F9
teratocarcinoma cells (8, 9). On the other hand, homozygous mutations
in CBP and p300 both result in lethality and a similar constellation of
phenotypic defects (4, 5). Moreover, CBP/p300 double heterozygotes are
invariably lethal, suggesting that functions of CBP and p300 must
overlap, at least to some degree. This complexity is not shared by
simpler metazoans, such as Drosophila and
Caenorhabditis elegans, which express only a
single isoform of CBP/p300 (reviewed in Ref. 2).
Although cell cycle-dependent phosphorylation of p300
was reported almost a decade ago (10), it is still not entirely clear how phosphorylation regulates CBP/p300 function. In large part, this
lack of understanding is because of the fact that the specific phosphorylation sites in CBP/p300 have never been precisely identified. Phosphorylation of p300 and CBP by cyclin E/Cdk2 was reported by
Perkins et al. (11) and Ait-Si-Ali et al. (12),
respectively. In the case of p300, cyclin E/Cdk2 was shown to
negatively regulate coactivator function in a manner that can be
blocked by the cyclin-dependent kinase inhibitor, p21. In
this model, p21 was proposed to participate in a positive feedback
loop, whereby activators such as p53, which depend upon p300 for
function, induce p21, which then alleviates the block in p300 action
mediated by cyclin E/Cdk2. In contrast, cyclin E/Cdk2 was reported to
increase the intrinsic HAT activity of CBP, potentially activating
expression of S-phase genes that are repressed in early G1
(12). Because the phosphorylation sites in p300 and CBP have not been
mapped, however, it may be premature to conclude that the two
coactivators are differentially regulated by
cyclin-dependent kinases.
CBP and p300 both contain a consensus protein kinase A (PKA) site
adjacent to their third zinc finger domains, and several groups have
proposed that phosphorylation by PKA may contribute to CBP/p300
regulation. For example, Xu et al. (13) have argued that
phosphorylation of CBP is responsible for the PKA-mediated augmentation
of the transcription factor Pit-1. This is an intriguing model because
Pit-1 itself cannot be phosphorylated by PKA. Using microinjection
assays, these workers demonstrated that the activation of Pit-1 by PKA
was lost in the presence of CBP containing a point mutation at the
consensus PKA site. This model was not confirmed by Zanger et
al. (14), however, and Swope et al. (15) have suggested
that the PKA-responsive domain in CBP resides near its amino terminus.
At this point, the mechanism of PKA activation of CBP/p300 remains enigmatic.
Other kinases proposed to regulate CBP/p300 function include
calcium/calmodulin (CaM) kinase IV, MAPK, and pp90Rsk. Although several
reports suggested that CBP cannot mediate its transcriptional functions
in the absence of CaM kinase IV stimulation (16-18), later studies
showed that recruitment of CBP by itself was sufficient for
transcriptional activation (19, 20). It remains possible, however, that
phosphorylation of CBP/p300 by CaM kinase IV could contribute to
signaling by augmenting the transcriptional response.
Phosphorylation and activation of CBP by MAPK was first reported by
Janknecht and Nordheim (21). Activation of MAPK through the Ras pathway
by insulin or nerve growth factor was reported to recruit pp90Rsk to
the third zinc finger domain of CBP in a manner that prevents the
binding of essential CBP effectors such as RNAPII (22). Interestingly,
modulation of CBP by pp90Rsk does not appear to require its catalytic
kinase activity. This inhibitory effect of pp90Rsk has not been seen by
other investigators, however, so it is possible that it is cell
type-specific (23). Clearly, the understanding of CBP/p300 regulation
by phosphorylation remains a major topic for future study.
In addition to their intrinsic acetyltransferase functions, CBP
and p300 are known to associate with additional HATs, including P/CAF,
SRC-1, and p/CIP. Why so many different HATs are required for
transcriptional regulation is unknown, but the answer may lie in the
differing preferences of these enzymes for free histones as compared
with nucleosomes and their distinct targets within the histone
substrates (for review, see Ref. 24). Although it has been suggested
that the HAT domains in CBP/p300 are highly related to those in P/CAF
and GCN5 (25), the primary sequences of these domains are actually
quite different. Moreover, these differences are significant enough to
allow the development of specific inhibitors of the P/CAF and CBP/p300
enzymatic activities (26). Kraus et al. (27) have shown that
the p300-mediated activation of estrogen receptor (ER) function on
reconstituted chromatin depends upon the intrinsic acetyltransferase
activity of the coactivator, demonstrating that this enzymatic function is essential in the context of chromatin. Because histone acetylation is not required for transcription of naked DNA templates, these results
imply that some component of chromatin is the acetylation target. These
conclusions are supported by the results of Ludlam et
al.,2 which show that
flies containing an acetyltransferase-deficient form of CBP are
incapable of activating specific target genes in vivo.
Although confirming the importance of the CBP enzymatic function, these
studies do not identify the acetylation target. Recent studies have
shown that the HAT activity of CBP/p300 is directed toward nucleosomes
through interactions with the histone chaperone, RbAp 48 (28).
Moreover, Ito et al. (29) have found that histone
acetylation by p300 facilitates the transfer of H2A-H2B from
nucleosomes to the chaperone protein NAP-1. In this model, the
recruitment of p300 and the subsequent histone acetylation follow a
chromatin remodeling step mediated by ATP-dependent
proteins in the ISWI family. These results are consistent with
in vivo chromatin immunoprecipitation experiments in yeast
showing that the association of SWI/SNF components on the HO
promoter is required for the subsequent HAT recruitment (30, 31).
Whether the release of H2A-H2B results from the acetylation of these
proteins directly or whether other nucleosomal components are the
primary targets of the acetyltransferases remains to be determined.
Acetylation of transcription factors (through FAT, factor
acetyltransferase activities) by CBP/p300 may
provide an equally important mode of regulation. First identified in
the context of the tumor suppressor p53 (32), acetylation of
transcription factors has been increasingly recognized as a mechanism
of gene regulation. In some instances, acetylation has clearly been
shown to increase the binding of transcription factors to DNA (32). In
most cases, however, the mechanism of activation is unknown. Recent
evidence suggests that coactivator acetyltransferases might also serve
to disrupt activator and repressor complexes. For example, Evans and
co-workers (33) have shown that the recruitment of p300 to the
ligand-activated ER leads to the acetylation of ACTR (an associated
acetyltransferase), disruption of the ACTR-p300-ER complex, and the
termination of transcription. Another possibility, consistent with the
multistep model of transcription proposed by Roeder (reviewed in Refs.
34 and 35), is that CBP/p300-mediated acetylation of the complex may
promote the transition from a CBP/p300-dependent to a
mediator-dependent stage of transcription (see below). A converse mechanism was proposed by Zhang et
al.3 In these studies,
interaction of the histone deacetylase-binding corepressor, CtBP
(carboxyl-terminal binding
protein), to a variety of transcriptional repressors was
shown to be blocked by acetylation of the CtBP interaction sites. In
this instance, as in the classical histone acetylation model,
acetylation is proposed to activate transcription by disrupting protein
complexes involved in repression. Paradoxically, acetylation by CBP can
also cause transcriptional repression in some systems. For example, in
flies, CBP has been shown to inhibit wingless signaling by acetylating
the Drosophila homologue of the high mobility group protein,
LEF/TCF-1 (36). Acetylation of a specific residue in LEF/TCF-1 is
believed to block the binding of the coactivator It is somewhat surprising that CBP and p300, which mediate the
activities of so many different transcription factors, might be present
in the cell at limiting concentrations. Nonetheless, there is
considerable evidence that this is the case. Even discounting experiments involving transcription factor overexpression, which would
perhaps be expected to exceed the capacity of the endogenous CBP/p300,
studies have shown that relatively small decreases in the
concentrations of coactivator are deleterious. For example, in the
human Rubinstein-Taybi syndrome, loss of a single CBP allele results in
severe developmental defects (37). The idea that CBP/p300 levels are
limiting is also supported by tissue culture experiments, as
exemplified by the studies of Hottiger et al. (38), which
examined the ability of interferon- The idea that CBP/p300 contributes to transcriptional synergy is
probably best supported by studies of the IFN- Transcriptional processes are regulated through the sequential
interactions of a large number of modulatory multiprotein complexes. Assembly of basal transcription factors at the promoter represents the
end result of these interactions. Regulation is imparted by additional
components such as enhanceosomes and mediator complexes which, along
with coactivators, integrate specific extracellular events and
intracellular signals.
Enhanceosomes are stable multiprotein complexes that promote the
cooperative recruitment of coactivators and the RNAPII complex to
active sites of transcription. In one well characterized example, formation of the enhanceosome involves recruitment of NF
INTRODUCTION
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INTRODUCTION
Are CBP and p300...
How Does Phosphorylation...
Are CBP and p300...
Does CBP/p300 Function as...
How Does CBP/p300 Fit...
Summary and Future Perspectives
REFERENCES
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Fig. 1.
Organization of CBP/p300-binding
proteins. Association of CBP/p300 with transcriptional
activators (top) and basal transcription factors and HATs
(bottom) is shown. The zinc fingers (Zn),
CREB-binding domain (KIX), bromodomain (Bromo),
HAT domain, and glutamine-rich domain (Q) are indicated.
TBP, TATA-binding protein.
Are CBP and p300 Redundant?
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INTRODUCTION
Are CBP and p300...
How Does Phosphorylation...
Are CBP and p300...
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How Does CBP/p300 Fit...
Summary and Future Perspectives
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How Does Phosphorylation Regulate CBP/p300 Function?
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INTRODUCTION
Are CBP and p300...
How Does Phosphorylation...
Are CBP and p300...
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Summary and Future Perspectives
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Are CBP and p300 Primarily HATs or FATs?
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INTRODUCTION
Are CBP and p300...
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Are CBP and p300...
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-catenin/Armadillo,
one of the intermediates in the wingless signaling pathway. In support of this model, CBP loss-of-function mutants have been found to suppress
the effects of an Armadillo mutation.
Does CBP/p300 Function as a Transcriptional Integrator?
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INTRODUCTION
Are CBP and p300...
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(IFN-
) to inhibit tumor
necrosis factor-
-stimulated human immunodeficiency virus gene
expression. This inhibition was shown to be mediated by competition
between STAT-2 (stimulated by IFN-
) and the p65 subunit of NF-
B
(stimulated by tumor necrosis factor-
) for a shared binding site
within the first zinc finger domain of CBP/p300. It is not certain that
two transcription factors must compete for the same binding site to be
mutually antagonistic, however. If CBP/p300 levels are truly limiting,
it is possible that they could be directed toward specific genes to the
exclusion of others. Testing this hypothesis will require the use of
experimental paradigms that do not involve the overexpression of
exogenous transcription factors.
enhanceosome (see
below), but other complex promoters have also been shown to contain
binding sites for multiple CBP/p300-interacting transcription factors.
(Indeed, given the large number of factors that bind CBP/p300, it is
difficult to imagine a promoter where this would not be the case.)
Nonetheless, although transcriptional synergy through CBP/p300 is an
appealing model, it has not been shown conclusively that these
coactivators interact with multiple transcription factors
simultaneously. In addition, although the recruitment of coactivators
to the enhanceosome appears to be required for synergistic activation,
tethering CBP/p300 to the promoter through a heterologous DNA-binding
domain is not sufficient. As suggested by Merika et al.
(39), the activation domains of the individual transcription factors
comprising the enhanceosome may contribute critical interactions with
basal factors. Alternatively, CBP/p300 may only participate in a
transient (albeit required) step in the transcriptional process. It may
be equally important for CBP/p300 to be replaced by other factors, such
as the mediator complex, for transcription to proceed. In support of
this idea, Kraus and Kadonaga (40) have demonstrated that although both
the ER and p300 are necessary for transcriptional initiation from
chromatin templates, only the ER is required for reinitiation.
How Does CBP/p300 Fit into the Complex Series of Events That
Mediate Transcriptional Activation?
TOP
INTRODUCTION
Are CBP and p300...
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Are CBP and p300...
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B,
ATF-2/c-Jun, interferon regulatory factors, and HMG1(Y) to
enhancer elements in the IFN-
promoter to create stereospecific
interaction surfaces between the enhancer binding proteins and the
CBP/p300-associated RNAPII complex (Fig.
2) (41, 42). The critical role of
CBP/p300 in this context is to promote the rapid formation of the
preinitiation and reinitiation complex to facilitate multiple rounds of
transcription (43). Depletion of CBP/p300 from this complex decelerates
the rate of transcription (44). CBP/p300 may also participate in terminating IFN-
gene transcription by acetylating HMG1(Y),
decreasing its affinity for DNA and disrupting the enhanceosome (43,
45, 46). Whether enhanceosomes actually rely on the HAT activity of
CBP/p300 has not been determined, however. Recent evidence demonstrating an intrinsic, phosphorylation-dependent HAT
activity in ATF-2, one of the DNA-binding proteins found in the IFN-
enhanceosome, suggests that the CBP/p300 HAT function could be
redundant (47).
View larger version (24K):
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Fig. 2.
The IFN-
enhanceosome complex. Assembly of the IFN-
enhanceosome
creates a stereospecific interaction surface for recruitment of
CBP/p300 and the basal transcription machinery to allow multiple rounds
of transcription. GTFs indicate general transcription
factors. p160 refers to the SRC/TIF/pCIP family of
coactivators.
Mediator complexes provide the penultimate step in the activation
process, leading to the recruitment of the general transcriptional machinery (Fig. 3). These mediators,
ARC/DRIP/TRAP/SMCC, NAT, CRSP, SRB/Med, and mouse Mediator,
share a subset of common components (reviewed in Refs. 48 and 35). The
relationships between these complexes and CBP/p300 have not been
entirely resolved, however. TRAP, the first of the mammalian
mediators to be characterized, does not contain CBP/p300 and lacks
detectable HAT activity (49, 50). Consistent with its absence of
associated HAT activities and with its relationship to the yeast
Mediator, TRAP shows potent coactivator functions with diverse
activators on naked DNA templates, whereas additional functions with
chromatin templates remain to be tested. In contrast, ARC- and
DRIP-mediated transcription has been observed on chromatin templates,
possibly reflecting the presence of some TRAP components in the assays
with DNA templates and/or the loose association or copurification of
CBP/p300 (or other HATs) with ARC and DRIP complexes (51, 52). Might
TRAP components also exhibit additional essential (or enhanced)
functions with chromatin templates, indicating a potential need for
additional protein-protein interactions for formation of the
preinitiation complex in this context? What is the role of CBP/p300 in
ARC and DRIP? Does CBP/p300 bridge transcriptional activators to the
mediator complex, or is its role to alter nucleosome structure in a
manner that allows the mediators to function at a subsequent stage of transcription?
|
Part of the ambiguity regarding the association of CBP/p300 with mediator complexes may stem from the different methods used to purify these mediators. TRAP was purified using a functional assay (49), whereas ARC and DRIP were identified through their binding to activated transcription factors (52). It is likely that the fusion proteins used to purify ARC and DRIP interact with CBP/p300 and the mediators in a mutually exclusive manner. This explanation would be consistent with the multistep interaction model proposed by Roeder (35). In this model, activated transcription factors have the capacity to interact with both CBP/p300 and the mediator complexes, but the mediator interactions might be nonfunctional until appropriate nucleosomal modifications have been induced by CBP/p300.
Nonetheless, it may be premature to conclude that mediators do not
contain HATs. Lorch et al. (53) have determined that the
yeast Mediator forms direct interactions with nucleosomes and contains
a subunit, Nut1, that specifically acetylates nucleosomal histone H3.
Therefore, at least in yeast (which does not contain CBP/p300),
mediator complexes do have intrinsic HAT activity. These studies reopen
the issue of whether the mammalian mediator complexes might also
contain loosely associated HATs or whether this activity must be
provided by a distinct complex containing CBP/p300.
![]() |
Summary and Future Perspectives |
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![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
In the sequential step model of transcriptional regulation,
coactivator HATs such as CBP/p300 are key regulators in the assembly and mobilization of the basal transcription machinery. Precisely how
CBP/p300 prepares the template for subsequent steps in the transcriptional process remains to be determined. Understanding the
positioning, timing, activation, and termination of CBP/p300 functions
will shed light on how cells use common transcriptional complexes to
mediate specific genetic responses to diverse cellular signals.
![]() |
ACKNOWLEDGEMENTS |
---|
We thank Robert Roeder, Yoshihiro Nakatani, and W. Lee Kraus for helpful comments.
![]() |
FOOTNOTES |
---|
* This minireview will be reprinted in the 2001 Minireview Compendium, which will be available in December, 2001.
To whom correspondence should be addressed: Vollum Inst., Oregon
Health Sciences University, 3181 S.W. Sam Jackson Park Rd., Portland,
OR 97201. Tel.: 503-494-5078; Fax: 503-494-4353; E-mail: goodmanr@ohsu.edu.
Published, JBC Papers in Press, March 8, 2001, DOI 10.1074/jbc.R000025200
2 W. Ludlam, R. H. Goodman, and S. Smolik, submitted for publication.
3 Zhang, Q., Yao, H., Vo, N., and Goodman, R. H. (2000) Proc. Natl. Acad. Sci. U. S. A. 97, 14323-14328.
![]() |
ABBREVIATIONS |
---|
The abbreviations used are:
CREB, cAMP-response
element-binding protein;
CBP, CREB-binding protein;
HAT, histone
acetyltransferase;
RNAPII, RNA polymerase II holoenzyme;
PKA, protein
kinase A;
CaM, calmodulin;
MAPK, mitogen-activated protein kinase;
FAT, factor acetyltransferase;
ER, estrogen receptor;
IFN-, interferon-
;
ARC, activator-recruited cofactor;
DRIP, vitamin D
receptor-interacting protein;
TRAP, thyroid receptor-associated
protein.
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