474 Current Drug Targets, 2010, 11, 474-481
1389-4501/10 $55.00+.00 © 2010 Bentham Science Publishers Ltd.
The Epithelial-Mesenchymal Transition and the Estrogen-Signaling in
Ovarian Cancer
D. Gallo
*
, C. Ferlini and G. Scambia
Department of Obstetrics and Gynecology, Catholic University of the Sacred Heart, Rome, Italy
Abstract: Epithelial ovarian cancer is the leading cause of death for gynecological cancer in most of the Western world;
lethality ensues from the occurrence of occult metastasis within the peritoneal cavity, a process requiring the acquisition
of capacity for migration and invasiveness by ovarian tumor cells (metastatic phenotype), and characterized by a complex
series of interrelated cellular events. Unlike most carcinomas that dedifferentiate during neoplastic progression with loss
of epithelial E-cadherin (epithelial to mesenchymal transition, EMT), ovarian carcinomas undergo transition to a more
epithelial phenotype, early in tumor progression, with increased E-cadherin expression. Subsequent reacquisition of
mesenchymal features is observed in late-stage tumors, and loss of E-cadherin expression or function is a factor in ovarian
cancer progression. Changes in E-cadherin expression are indicative of the phenotypic plasticity that occurs in ovarian
cancer, with a variety of signal transduction pathways impinging on the regulation of E-cadherin levels or subcellular
distribution. Among them, the Snail transcription family, consisting of members SNAIL and SLUG, is thought to be
mainly involved in the repression of E-cadherin expression, leading to EMT. E-cadherin, SNAIL, and SLUG also
represent crucial targets of estrogen signaling. In this review, we discuss recent advances in the understanding of the role
of estrogen signaling in the complex network underlying the phenotypic plasticity in ovarian cancer. Insight into the
mechanisms involved will allow rational drug designs, aimed at the molecules critical to cellular signaling.
Keywords: Ovarian cancer, estrogens, EMT, E-cadherin, SNAIL, SLUG.
INTRODUCTION
Ovarian cancer is the sixth most common cancer and the
fifth leading cause of cancer death among women in the
USA [1]; in European women, in 2006, it accounted for
about 3.9% of all female cancers [2]. The epithelial tumors
represent 80% to 90% of ovarian malignancies in the United
States and Western Europe [3], and usually dominate the
data from cancer registries. Initial therapy for epithelial ova-
rian cancer consists of surgery; debulking surgery is per-
formed for advanced stage of the disease in order to decrease
tumor burden, and it is followed by chemotherapy, the
current standard of care being platinum plus taxane. Ovarian
cancer is recognized to be one of the most chemotherapy-
sensitive malignancies, with 70–80% of newly diagnosed pa-
tients exhibiting a response to primary platinum plus taxane
chemotherapy; despite this fact, the majority of women who
present with advanced ovarian cancer will experience
recurrence. The probability of response to second-line che-
motherapy depends mostly on the relapse-free interval.
Patients with ovarian cancer that is refractory to a platinum-
based chemotherapy, or that relapse within 6 months after its
discontinuation are considered to be platinum resistant [4].
Unfortunately, regimens used as second-line therapy in such
situations have a low response rate, and are associated with
severe side effects that negatively influence the quality of
life, and necessitate long stays in hospital and intensive
palliative care [4]. Patients ultimately die of complications
associated with progressive disease.
The importance of estrogen signaling in the development
and progression of ovarian cancer has been assumed to be
*Address correspondence to this author at the Department of Obstetrics and
Gynecology, Catholic University of the Sacred Heart, Largo A. Gemelli, 8 –
00168, Rome, Italy; Tel: +39 06 3013337; Fax: +39 06 3051160; E-mail:
d.gallo@rm.unicatt.it
less significant than for breast or endometrial cancers,
although clinical data, animal experiments, and receptor
studies have shown that not only normal ovaries but also
many malignant ovarian tumors can be considered as endo-
crine related, and hormone-dependent. Preclinical studies
have indicated a cancer promoting effects of estrogens on
ovarian cancer growth, mostly by up-regulation of proteins
involved in cell growth and metastasis [5, 6]. In postmeno-
pausal patients with epithelial ovarian cancer, plasma con-
centrations of estradiol, progesterone, androstenedione and
testosterone were directly correlated with tumor volume and
FIGO stage, and changes in hormonal concentrations (with
the exception of testosterone) reflected the response of
ovarian cancer to therapy [7]. Consistently, the use of
exogenous hormones for menopause-related symptoms has
been associated with an increased risk of ovarian cancer
incidence or mortality, with recent studies showing that
prolonged periods of hormone replacement therapy (HRT)
use ( 5–10 years) confer an approximately 1.5–2.0- fold
increase in risk [8]. In contrast, decreased risk of ovarian
cancer follows the use of oral contraceptives (OC), with 5
years of oral OC use conferring a 30–50% reduction in
cancer risk [8]. The protective effect of oral contraceptives
could be interpreted as supportive of the estrogen hypothesis,
as oral contraceptive use decreases ovarian estrogen produc-
tion, and early to midfollicular phase circulating estrogens
are maintained during use. Other Authors, however, suggest
that chronic suppression of ovulation reduces cancer risk by
decreasing recurrent ovarian injury [9].
The significance of anti-estrogenic intervention in the
treatment of ovarian carcinoma has been emphasized by the
fact that these drugs will inhibit the growth of ovarian
carcinoma in vitro and in vivo [10, 11]. Clinical trials with
the aromatase inhibitor letrozole, which acts by depleting
levels of estrogen available to the Estrogen Receptors (ERs),