
Two CCAAT/enhancer binding protein sites in the cytochrome
P4503A1 locus
Potencial role in the glucocorticoid response
Elsa Rodrigues
1
, Marie-Jose
´Vilarem
2
, Vera Ribeiro
1,
*, Patrick Maurel
2
and Maria C. Lechner
1
1
Molecular Biology Unit, Faculty of Pharmacy, University of Lisbon, Portugal;
2
Unite
´128 INSERM, Montpellier, France
Induction of CYP3A genes by the ligand-activated preg-
nane-X-receptor (PXR) involves the interaction of other as
yet unidentified liver transcription factors. Here we show
that the CYP3A1 promoter contains two active sites con-
trolled by the CCAAT/enhancer-binding protein a(C/
EBPa), previously shown to regulate a number of liver stress
response genes. We have identified two functional C/EBP
binding sites at the CYP3A1 promoter that confer luciferase
activity to C/EBPacotransfected CHO cells. When inserted
upstream of a thymidine kinase promoter, oligonucleotides
corresponding to these elements ()350/)311 and )628/
)608), increase reporter gene expression when cotransfected
with a C/EBPaexpression vector. Point mutations in the
most conserved nucleotides in either element prevent binding
of C/EBPaand abolish transactivation of the CYP3A1
promoter. Moreover, we demonstrate that C/EBPaaccu-
mulates in the rat liver nuclei in response to dexamethasone,
and that under these conditions C/EBPabinds to the
CYP3A1 promoter elements. Our results suggest a correla-
tion between transcription of C/EBPa, nuclear protein
function and induction of CYP3A1 by dexamethasone in the
liver. They also support the notion that C/EBPaparticipates
in the up-regulation of the CYP3A1 gene in response to
synthetic glucocorticoids.
Keywords: cytochrome P450; CYP3A1 locus; C/EBP; regu-
latory elements; glucocorticoid induction.
Mammalian hepatic phenotypes are controlled through the
concerted action of a number of liver-enriched transcription
factors that act in cooperation with a number of ubiquitous
and ligand-activated factors to direct the selective expression
of liver-specific genes. The activity of each target gene is
modulated by dynamic arrays of counterpart transcription
factors that act upon liver differentiation and that are
stimulated by endogenous as well as by exogenous ligands [1].
Cytochrome P450 genes, members of the CYP1–4 fami-
lies, are abundantly expressed in the liver and are subjected
to complex regulatory networks that depend markedly on
the ontological development, and on the hormonal and
nutritional status of the animals [2]. Moreover, P450 mono-
oxygenases, as major body interfaces, are adaptive enzymes
highly responsive to induction and repression by environ-
mental and xenobiotic agents in general.
Recently, important advances have been made in under-
standing the mechanism of action of prototype inducers that
control the expression of hepatic P450 enzymes, namely
those mediated by the nuclear receptors AhR, CAR, PPAR
and PXR (reviewed, [3]). However, the role of these ligand-
activated receptors can be enhanced, reduced or inhibited by
the availability of other transcription factors that participate
in the organization of the transcription initiation complexes
in the native DNA context of each CYP locus. Such func-
tional interactions have not been fully defined, but their elu-
cidation is essential to understand the molecular basis of the
marked physiological variations often observed in the in vivo
response of each CYP gene to common inducing agents.
CYP3A1 has been widely investigated as a model of a
xenobiotic up-regulated liver expressed gene. Transcription
of CYP3A1 is virtually undetected in the adult rat liver, but
markedly induced by structurally diverse agents, including
the synthetic glucocorticoid agonist dexamethasone [4] and
the antagonist pregnenolone 16a-carbonitrile [5]. Such
paradoxical behaviour of the rat CYP3A1, and of other
orthologous genes, was shown to involve the pregnane X
receptor (PXR) [6–8], a member of the steroid hormone
receptor family. The mechanism of the glucocorticoid-
mediated activation of CYP3A1 relies on a dexamethasone
responsive unit in the promoter region of this gene [9,10].
This unit comprises elements that are targeted by the
activated PXR, as well as by COUP-TFs and HNF4 [11,12].
However, in vitro experiments have shown that mouse [6],
Correspondence to M. C. Lechner, Molecular Biology Unit,
Faculty of Pharmacy, University of Lisbon,
Av. Prof Gama Pinto, 1649–003 Lisbon, Portugal.
Fax: + 351 21 7946491, Tel.: + 351 21 7946490,
E-mail: clechner@ff.ul.pt
Abbreviations: C/EBP, CCAAT/enhancer binding protein; C/EBP
cons, C/EBP consensus oligonucleotide; CYP, cytochrome P450;
PXR, pregnane-X-receptor; AhR, aryl hydrocarbon receptor; CAR,
constitutive androstane receptor; PPAR, peroxisome proliferator-
activated receptor; RXR, retinoid-X-receptor; COUP-TF, chicken
ovalbumin upstream promoter transcription factor; HNF4, hepato-
cyte nuclear factor 4; TK, thymidine kinase; EMSA, electrophoretic
mobility-shift assay.
*Present address: Biochemistry Laboratory, Chemistry Departmental
Area, Faculty of Sciences and Technology, University of Algarve,
Campus de Gambelas 8000-117 Faro, Portugal.
(Received 30 September 2002, revised 14 November 2002,
accepted 5 December 2002)
Eur. J. Biochem. 270, 556–564 (2003) FEBS 2003 doi:10.1046/j.1432-1033.2003.03413.x