Protein–protein interactions (PPIs) form the molecular
bases of many physiological processes in health and dis-
ease. In cancer, PPIs can have important regulatory roles;
for example, in the cell division cycle or in cell signalling.
The specificity and affinity of these interactions are criti-
cally important — changes in them can lead to cellular
malfunctions, such as the uncontrolled cell growth that
typifies cancer. Thus, it is not surprising that modulators
of PPIs, whether as biological agents (such as antibodies)
or as small-molecule synthetic compounds, are urgently
being sought and developed by the pharmaceutical
industry to treat an unmet medical need.
This interest in PPIs as drug targets has historically
been tempered by the pervasive view that finding mol-
ecules, particularly small synthetic molecules (those
<500 Da), that will modulate PPIs is irredeemably
hampered by the large, flat, featureless areas of protein
surfaces that form the interface — an interface that is
thought to be ‘undruggable’ (REFS 1–4). This has often
been in spite of compelling evidence from molecular,
cellular and animal studies that such targets have an
excellent potential for drug development. Nevertheless,
major inroads into discovering such molecules have
been made in recent years, with more than 12 small-
molecule PPI modulators currently in clinical develop-
ment (TABLE 1) and sales worldwide predicted to be in
excess of US$800 million within 5 years
5
.
As with other areas of drug discovery, a major chall-
enge is to identify and validate physiologically relevant
PPIs as cancer-related targets; this task is particularly chall-
enging for many PPIs, as they can be transient in nature.
The most common tools for identifying PPIs have
been genetic approaches, such as yeast two-hybrid,
synthetic lethal, systematic RNA interference and
co-evolution analyses; cell biology approaches, includ-
ing the localization of proteins with fluorescent mark-
ers; proteomic approaches, such as affinity purification
and mass spectrometry (MS) of complexes and pro-
tein arrays; and direct protein co-purification and
immunoprecipitation. The past couple of years have
also seen the development of highly sophisticated
approaches to genome-wide prediction of interacting
proteins, including studies that have identified more
than 300,000 potential interaction pairs encoded in
the human genome
6
. Of particular relevance to can-
cer is the genome-wide profiling of tumour samples by
initiatives such as The Cancer Genome Atlas and the
International Cancer Genome Consortium.
Validating the physiological relevance of a PPI to
cancer facilitates the initiation of a drug discovery
programme. The pathways in a typical drug discov-
ery programme are outlined in FIG. 1; the nature of the
protein target and the available resources will dictate
which pathways are followed. FIGURE 2a illustrates how
different approaches are being applied to a single pro-
tein target in the hunt for PPI modulators. As well as
traditional high-throughput chemical screening (HTS),
structure-based discovery approaches are now com-
mon. In addition to the challenges described above,
these approaches face another challenge that is specific
to PPIs. There is a wide gulf between the number of
experimentally determined protein structures and the
1
Australian Cancer Research
Foundation Rational Drug
Discovery Centre and Biota
Structural Biology
Laboratory, St. Vincent’s
Institute of Medical Research,
9 Princes Street, Fitzroy,
Victoria 3065, Australia.
2
Department of Medicine,
University of Melbourne,
41 Victoria Parade, Fitzroy,
Victoria 3065, Australia.
3
Department of Biochemistry
and Molecular Biology,
Bio21 Molecular Science and
Biotechnology Institute,
University of Melbourne,
Parkville, Victoria 3052,
Australia.
Correspondence to M.W.P.
e‑mail: mparker@svi.edu.au
doi:10.1038/nrc3690
Published online
13 March 2014
High-throughput chemical
screening
(HTS). A systematic way to
measure the modulation of an
interaction or a biological
function against a given protein
target by a large number of
individual compounds.
Oncogenic protein interfaces:
small molecules, big challenges
Tracy L. Nero
1
, Craig J. Morton
1
, Jessica K. Holien
1
, Jerome Wielens
1,2
and Michael W. Parker
1,3
Abstract | Historically, targeting protein–protein interactions with small molecules was not
thought possible because the corresponding interfaces were considered mostly flat and
featureless and therefore ‘undruggable’. Instead, such interactions were targeted with larger
molecules, such as peptides and antibodies. However, the past decade has seen
encouraging breakthroughs through the refinement of existing techniques and the
development of new ones, together with the identification and exploitation of unexpected
aspects of protein–protein interaction surfaces. In this Review, we describe some of the latest
techniques to discover modulators of protein–protein interactions and how current drug
discovery approaches have been adapted to successfully target these interfaces.
REVIEWS
248 | APRIL 2014 | VOLUME 14 www.nature.com/reviews/cancer
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