The role of hepatitis B virus (HBV) in the development of
hepatocellular carcinoma
Eberhard Hildt, Peter Hans Hofschneider and Stephan Urban
Based on epidemiological data and experimental results,
mammalian hepadnaviruses, in particular hepatitis B virus
(HBV) and woodchuck hepatitis virus (WHV), have to be
considered as a causative factor in the development of
hepatocellular carcinoma (HCC), despite the fact that they
lack a complete viral oncogene. Integrated viral DNA is
found regularly in woodchuck and human HCC. In
woodchucks an activation in cis of c-myc and N-myc is
almost always observed. By contrast, in humans, a
pleiotropic activation in trans of cellu lar gen es by in tegrated
genes encoding HBV transactivators, namely the X protein
(HBx) and the PreS2 activators (the large surface protein
(LHBs) and truncated middle surface proteins (MHBs
t
)),
has been described as a general mechanism. Mimicking
chemical tumour promoters, i.e. TPA, the viral
transactivators trigger PKC/ Raf-controlled signalling
pathways, finally activating transcription factors such as
AP-1 and NF- κB which con trol gen es relevant for
proliferation. Moreover, ‘HBV-transactivated’ hepatocytes
may give rise to a new epigenetic situation in the form of an
‘immortalized’ inflammatory process which may then pave
the way for further critical events such as mutations and
chromosomal aberrations.
Key words: hepadnaviruses / oncogenesis / viral
transactivators / PKC/ Raf-controlled signalling pathways
©1996 Academic Press Ltd
V IRUS- ASSOCIATED TUMOURS comprise approximately
15% of all tumours in humans worldwide.
1
Assu m in g
the implicated viruses play a causative role in oncoge-
nesis, then viruses are among the most important
oncogenic agents worldwide. Among the virus-asso-
ciated tumours, approximately 30% are HBV-asso-
ciated hepatocellular carcinomas, which means 4.5%
of all tumours worldwide.
From an epidemiological viewpoint, the risk for
males with chronic HBV infection, i.e. HBsAg carriers
and those with chronic persistent and chronic aggres-
sive hepatitis, of developing HCC increases by a factor
of ~ 100.
2,3
For chronically infected males living in
Taiwan this means a lifetime risk of dying of HCC of
almost 50%. Apart from a few exceptions (Greece, for
example) the geographical correlation between
HBsAg prevalence and the incidence of HCC is very
high. At present more than 200 million people
worldwide are chronically infected; every year two
million die as a result of the infection, approximately
700,000 of whom die of HBV-associated HCC
(reviewed in ref 4). Although an HBV vaccine exists,
the WHO estimates that 400 million people will be
chronically infected by the year 2000. Since the
incubation period for the development of HBV-
associated HCC is as long as 30 years or more, this
means that this tumour will remain a major public
health problem for decades, if better therapies cannot
be found to supplement those now in existence. At
present, as curative therapies, only liver resection,
orthotopic liver transplantation and, in Asia, ethanol
injection into the tumour are available. This situation
alone is serious enough to warrant further intensive
studies into the causal relationship between HBV
infection and the development of HCC.
Intensive studies were started very soon after the
cloning of HBV DNA in the late 1970s, which until
then had been difficult to obtain. In addition, animal
model systems were developed, and here in particular
the woodchuck hepatitis virus (WHV) is worth men-
tioning. As is well known, in newborn American
woodchucks WHV induces the development of HCCs
with a frequency of almost 100% within two to three
years.
As pointed out in a review by Rogler and Chisari,
5
many new facts have been discovered but no unifying
concepts could be established: in tumours from
infected woodchucks activation in cis of two cellular
proto-oncogenes, namely c-myc and N-myc, by the
insertion of WHV DNA into these genes or their
flanking regions, including the so-called WIN locus, is
almost always observed (reviewed in refs 5,6, and M.
Buendia, personal communication). In HBV-positive
human as in woodchuck HCCs, viral DNA is almost
From the Abteilung Virusforschung, Max-Planck-Institut f¨ ur
Biochemie, 82152 Martinsried, Germany
seminars in VIROLOGY, Vol 7, 1996: pp 333–347
©1996 Academic Press Ltd
1044-5773/96/050333 + 15 $25.00/0
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