VIROLOGY 167,630-633 (1988)
The Glucocorticoid Receptor Recognizes a Specific Nucleotide Sequence in Hepatitis B
Virus DNA Causing Increased Activity of the HBV Enhancer
RAN TUR-KASPA,*'I- YOSEF SHAUL,# DAVID D. MOORE,§ ROBERT D. BURK, *Ji SAM OKRET,¶
LORENZ POELLINGER,¶ AND DAVID A. SHAFRiTZ *'**'1
*Marion Bessin Liver Research Center and Department of Medicine, Albert Einstein College of Medicin~ Bronx, New York 10461; tLiver Unit,
Department of Medicine A, Hadassah University Hospital, Jerusalem, Israel; t-Departmentof Virology, The Weizmann Institute of Science,
Rehovot, Israel,"§Department of Molecular Biology, Massachusetts Genera/Hospital and Department of Genetics, Harvard Medical School,
Boston, Massachusetts 02138; IIDepartments of Pediatrics and Microbiology and Immunology, Albert Einstein College of Medicine,
Bronx, New York 10461;¶Department of Medical Nutrition, Karolinska Institute, Stockholm, Sweden; and **Department of Cell Biology,
Albert Einstein College of Medicine, Bronx, New York 10461
Received May 2, 1988; accepted September 8, 1988
The hepatitis B virus (HBV) genome contains a specific DNA binding site for the glucocorticoid receptor. Using DNase
footprinting, this binding site was localized at HBV map positions 341-370 clockwise from the EcoRI site. The DNA
sequence protected in the footprint contains two tandem copies of the G RE core hexanucleotide 5'-TGTTCT-3 '. Deletion
analysis and reconstruction experiments in plasmid expression vectors demonstrated that this glucocorticoid receptor
binding sequence serves as a signal for augmenting glucocorticoid-dependent activity of the HBV enhancer, which is
located ~730 nucleotides downstream in the HBV genome. Even though it does not serve as an independent enhancer
element, the HBV glucocorticoid receptor domain can therefore be categorized as a functional GRE. © 1988 Academic
Press,Inc.
Several clinical reports have demonstrated that corti-
costeroid treatment of patients with chronic HBV infec-
tion causes elevation of HBsAg in the serum (1) and
increased expression of HBcAg in liver cells (2). Corti-
costeroid treatment also stimulates expression of
HBsAg in transgenic mice into which the HBsAg gene
has been introduced (3) and in hepatocellular carci-
noma cell lines containing integrated HBV DNA (4, 5).
Many previous studies have shown that steroid hor-
mones regulate expression of a substantial number of
viral and cellular genes (for review see Ref. 6), and
DNasel footprint analysis has shown that purified, acti-
vated glucocorticoid receptor protein binds to several
specific sites in the mouse mammary tumor virus
(MMTV) LTR (7, 8), as well as in human growth hor-
mone (hGH) (9), human metallothionein-llA (hMT-IIA)
(10), chicken lysozyme (11), Moloney murine sarcoma
virus (MSV) LTR (12), tryptophan oxygenase (TO) (13),
and tyrosine aminotransferase (TAT) (14). Nearly all of
these glucocorticoid receptor binding sites share a
common DNA consensus sequence, 5-GGTACAN-
NNTGT~CT-3'(10, 14, 6).
Previously, we demonstrated that dexamethasone
(Dex) stimulates chloramphenicol acetyltransferase
(CAT) expression in cells transfected with plasmids
containing specific fragments of the HBV genome
1To whom requests for reprints should be addressed,
linked to CAT (15). Dex stimulation of CAT expression
was observed with a 1.4-kb BamHI fragment of HBV
DNA, map positions (m.p.) 30-1402, and only con-
structs containing both the HBV enhancer region at
m.p. 1080-1234 (16) and sequences upstream of m.p.
735 were induced by Dex (15). Examination of this up-
stream region revealed a nucleotide sequence at m.p.
356-366 with extensive homology to several known
glucocorticoid receptor binding sites or so called glu-
cocorticoid responsive elements (GREs), which have
been shown in functional studies to augment expres-
sion of specific reporter genes in a glucocorticoid-de-
pendent manner(10, 12-14, 17-20).
The present study demonstrates that purified gluco-
corticoid receptor protein binds to a restriction frag-
ment of the HBV genome containing the GRE consen-
sus sequence. A 29-nucleotide basepair sequence in
the resulting DNA-protein complex (located at viral
m.p. 341-370)is protected from DNase I digestion and
contains two tandem copies of the GRE core sequence
5'-TGTCCT-3'. CAT plasmids containing both the glu-
cocorticoid receptor binding region of the HBV genome
and the HBV enhancer show increased expression of
CAT in response to Dex. However, when the HBV en-
hancer (m.p. 1080-1234) is deleted, no CAT activity is
observed in the presence or absence of Dex. When the
HBV GRE sequence is added to a CAT plasmid contain-
ing only the HBV enhancer, Dex-mediated enhance-
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