NATURE REVIEWS | GASTROENTEROLOGY & HEPATOLOGY ADVANCE ONLINE PUBLICATION | 1
Department of Surgery,
NUTRIM School of
Nutrition, Toxicology
and Metabolism,
Maastricht University,
PO Box 616, 6200 MD,
Maastricht, Netherlands
(F. G. Schaap). Division
of Gastroenterology
and Hepatology,
Department of Internal
Medicine III, Medical
University of Vienna,
Waehringer Guertel
18–20, 1090 Vienna,
Austria (M. Trauner).
Department of
Gastroenterology and
Hepatology, Academic
Medical Centre,
Meibergdreef 9,
1105 AZ, Amsterdam,
Netherlands
(P. L. M. Jansen).
Correspondence to:
P. L. M. Jansen
p.l.jansen@amc.uva.nl
Bile acid receptors as targets for drug
development
Frank G. Schaap, Michael Trauner and Peter L. M. Jansen
Abstract | The intracellular nuclear receptor farnesoid X receptor and the transmembrane G protein-coupled
receptor TGR5 respond to bile acids by activating transcriptional networks and/or signalling cascades. These
cascades affect the expression of a great number of target genes relevant for bile acid, cholesterol, lipid and
carbohydrate metabolism, as well as genes involved in inflammation, fibrosis and carcinogenesis. Pregnane X
receptor, vitamin D receptor and constitutive androstane receptor are additional nuclear receptors that
respond to bile acids, albeit to a more restricted set of species of bile acids. Recognition of dedicated bile
acid receptors prompted the development of semi-synthetic bile acid analogues and nonsteroidal compounds
that target these receptors. These agents hold promise to become a new class of drugs for the treatment
of chronic liver disease, hepatocellular cancer and extrahepatic inflammatory and metabolic diseases. This
Review discusses the relevant bile acid receptors, the new drugs that target bile acid signalling and their
possible applications.
Schaap, F. G. et al. Nat. Rev. Gastroenterol. Hepatol. advance online publication 27 August 2013; doi:10.1038/nrgastro.2013.151
Introduction
Traditional Chinese medicine recognized the therapeutic
value of bear bile long before the era of modern medicine.
Bear bile is replete with ursodeoxycholic acid (UDCA),
a bile acid encountered in appreciable amounts only in
Ursidae.
1
Although bear bile gained scientific interest at
the turn of the previous century with the isolation of a
theretofore unknown bile acid (that is, UDCA) from bile
of the polar bear by Olof Hammersten of the University of
Uppsala in Sweden,
1
it would last nearly eight more decades
before the therapeutic potential of bile acids for dissolv-
ing gallstones and the treatment of bile acid biosynthesis
defects and primary biliary cirrhosis (PBC) was realized.
2–4
An early observation was made in 1938 by Nobel laureate
Philip Hench. He observed that rheumatic symptoms
alleviated when patients with rheumatoid arthritis become
jaundiced.
5
Elevation of serum bile acids has been a candi-
date to explain this phenomenon ever since, and suggests
an anti-inflammatory effect of bile acids. The discovery of
receptors with affinity for bile acids, and subsequent X-ray
crystallography studies of their ligand-binding sites, has
given the development of natural, semi-synthetic and fully
synthetic drugs targeting these receptors and associated
pathways a strong impetus and molecular base. These new
agents offer novel therapeutic possibilities for the treatment
and prevention of liver disease, atherosclerosis, obesity and
type 2 diabetes mellitus (T2DM). However, before this
new approach can be fully appreciated, a more complete
understanding is needed of the complex networks that link
bile acids and metabolism.
In reading this Review, one has to appreciate that much
of the research in this area has been undertaken in mice,
which often does not translate directly to humans. Working
with human cell systems only partially remedies this situ-
ation, as effects of bile acid signalling often rely on interac-
tions between tissues rather than responses in single-cell
systems. The final proof for the therapeutic value of bile
acid analogues has to come from carefully planned, ran-
domized human studies with clear end points. In this
Review, we focus on bile acid signalling in humans, albeit
it has to be acknowledged that much of the data and ideas
are based on evidence from mouse models.
Bile acids
Excellent in-depth reviews covering the synthesis, metab-
olism, transport and physicochemical functions of bile
acids have been published elsewhere.
6–9
We will, therefore,
only mention some elemental knowledge.
Bile acids are a diverse class of water-soluble, cholesterol-
derived, amphipathic molecules that are formed in the liver
(primary bile acids) with microbial transformation in the
gut (secondary bile acids) greatly expanding the molecu-
lar repertoire. Bile acids typically occur as conjugates with
either glycine or taurine, and are negatively charged over
most of the physiological pH range. Although the term ‘bile
salt’ would be more appropriate from a chemical perspec-
tive, the expression ‘bile acid’ is mostly used throughout
this Review for congruence with colloquial terminology
(such as UDCA and obeticholic acid). These chemical fea-
tures necessitate dedicated transport proteins for efficient
cellular permeation and largely confine intracellular bile
Competing interests
M. Trauner declares associations with the following companies:
Falk Pharma, Intercept, Phenex. See the article online for full
details of the relationships. F. G. Schaap and P. L. M. Jansen
declare no competing interests.
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