NATURE REVIEWS | UROLOGY ADVANCE ONLINE PUBLICATION | 1
Introduction
The androgen receptor (AR) is an impor-
tant therapeutic target in the treatment of
metastatic prostate cancer, as evidenced
by the life-prolonging effects of androgen
deprivation therapy (ADT). Despite the
initial efficacy of ADT, tumour regrowth
will eventually occur in nearly all patients,
resulting in so-called castration-resistant
prostate cancer (CRPC). For decades,
the cytotoxic agent docetaxel has been the
only known life-prolonging drug for
patients with CRPC. Of note, docetaxel also
affects androgen signalling, as it interferes
with the nuclear translocation of the AR.
1
Surprisingly, the AR remains a driver of
tumour growth and a useful target in the
castration-resistant and even the docetaxel-
resistant setting as proven by the effi-
cacy of second generation AR-targeting
therapeutics, such as enzalutamide
and abiraterone.
Abiraterone acetate prevents testicu-
lar, adrenal and intratumoural androgen
synthesis resulting in a survival benefit
both before and after chemotherapeutic
treatment.
2
However, a major drawback of
this drug is the need for simultaneous treat-
ment with prednisone, mainly to prevent
excessive production of mineralocorticoids
and the concomitant adverse effects.
Another big step forward in this field was
the introduction of enzalutamide, which is
a second generation AR antagonist with a
higher affinity to the AR compared with
the first generation antiandrogens bicalu-
tamide and hydroxyflutamide. In 2012, the
AFFIRM study demonstrated an average
increase in overall survival of 4.8 months in
the enzalutamide versus the placebo group
in patients with CRPC.
3
Unfortunately,
although this new drug has only been
available in clinical practice for 2 years,
development of resistance has already been
noted in the majority of patients.
3
Clearly,
defining the unde rlying mechanisms of
resistance should lead to the optimization
of the treatment, as well as the identifica-
tion of new therapeutic targets and pos-
sible cross-resistances of prostate tumours
to other treatments. In this Perspectives
article, we provide a critical review of the
recently reported mechanisms of enzalu-
tamide resistance in preclinical models of
prostate cancer and the clinical setting.
Enzalutamide resistance
ADT and treatment with AR antagonists
have the same goal: lowering AR signal-
ling either indirectly by depriving the
receptor of its ligand or directly by block-
ing receptor activity. Frequently observed
mechanisms of resistance to ADT and
first-generation antagonists involve the
AR. AR gene amplification and resulting
increased protein levels, receptor muta-
tion and truncation, intracrine synthesis
of androgens by the tumour cells, changes
in AR cofactor balance, as well as multiple
receptor-unrelated mechanisms have been
described (Figure 1).
4
Some of these mecha-
nisms have also been identified during
enzalutamide treatment and various other
new mechanisms have been suggested.
AR truncations
The AR consists of a central DNA-
binding domain (DBD), a carboxytermi-
nal ligand-binding domain (LBD) and an
aminoterminal activation domain (NTD)
(Figure 2).
5
In 2009, AR variants that lack
the LBD were reported in patients with
advanced prostate cancer.
6,7
Loss of the
LBD was caused by somatic mutations that
introduce stop codons in the AR gene by
intragenic deletions or by alternative spli-
cing of the primary transcript.
8
Alternative
splicing is a naturally occurring mechanism
that can generate functionally diverse pro-
teins from the same gene. In cancer cells,
this mechanism can increase the variations
in oncogenic as well as tumour suppressor
proteins. However, truncated ARs can also
arise through somatic mutations that intro-
duce stop codons or through rearrange-
ments in the AR gene. Transgenic mice
that overexpress truncated ARs (alongside
nonmutated variants) in prostate epithelia
develop adenomas, demonstrating that the
mutant receptor can aid carcinogenesis.
9
Structure–function analyses of the
AR protein revealed that truncations of
the LBD result in a highly active, ligand-
independent receptor mutant. Not surpris-
ingly, these truncated forms are unaffected
by AR agonists or antagonists since they lack
the LBD.
7,10
Moreover, the genes that are
induced by truncated ARs are very similar
to those of a full-length receptor that is acti-
vated by levels of androgens that support
OPINION
Emerging mechanisms of enzalutamide
resistance in prostate cancer
Frank Claessens, Christine Helsen, Stefan Prekovic, Thomas Van den Broeck,
Lien Spans, Hendrik Van Poppel and Steven Joniau
Abstract | The majority of prostate cancers are hormone-dependent at diagnosis
highlighting the central role of androgen signalling in this disease. Surprisingly, most
forms of castration-resistant prostate cancer (CRPC) are still dependent on the
androgen receptor (AR) for survival. Therefore, the advent of new AR-targeting drugs,
such as enzalutamide, is certainly beneficial for the many patients with metastatic
CRPC. Indeed, this compound provides a substantial survival benefit—but it is
not curative. This Perspectives article describes the different ways through which
cancer cells can become resistant to enzalutamide, such as AR truncation and other
mutations, as well as by-pass of the AR dependence of prostate cancer cells through
expression of the glucocorticoid receptor. The clinical relevance of these mechanisms
and emerging questions concerning new therapeutic regimens in the treatment of
metastatic CRPC are being discussed.
Claessens, F. et al. Nat. Rev. Urol. advance online publication 16 September 2014;
doi:10.1038/nrurol.2014.243
Competing interests
The authors declare no competing interests.
PERSPECTIVES
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