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256 Current Cancer Drug Targets, 2015, 15, 256-269
Cancer Stem Cells in Solid and Liquid Tissues of Breast Cancer Patients:
Characterization and Therapeutic Perspectives
Rena Chiotaki, Hara Polioudaki and Panayiotis A. Theodoropoulos
*
Department of Biochemistry, School of Medicine, University of Crete, Heraklion, Greece
Abstract: Breast cancer stem cells (BCSCs) represent a heterogeneous subpopulation of rare cells
within breast cancer tumors, displaying an enhanced tumor initiating capability and underlying
disease progression and therapy resistance. Unraveling their phenotypic, biological and functional
profile is a major challenge in the context of diminishing patient mortality. In this review, following a
brief description on how cancer stem cells (CSCs) and their microenvironment contribute to tumor
preservation and heterogeneity, we summarize the current literature regarding the molecular
signature of BCSCs either localized in the primary tumor or circulating in the blood of breast cancer
patients. We present recent data on specific stem and epithelial-to-mesenchymal transition (EMT)
markers designating the BCSC subpopulation and underline their pathogenic significance. The molecular characterization
of BCSCs has promoted the design of novel therapeutic approaches targeting the BCSC subpopulation which are currently
being experimentally and clinically evaluated. We highlight recent advances on the development of novel BCSC-targeting
therapeutic strategies including the inhibition of cell signaling pathways, differentiation therapy, metabolic interference
and nucleotide-, bio- and nano-technology based approaches. Eliminating the chemo- and radio-resistance properties of
breast cancer tumor cells via BCSC-directed therapies, combined to conventional therapeutic approaches, will augment
the effectiveness of breast cancer treatment and improve the clinical outcome of breast cancer patients.
Keywords: Breast cancer, cancer stem cells, circulating tumor cells, epithelial-to-mesenchymal transition, targeting of cancer
stem cells.
INTRODUCTION
The existence of CSCs was originally demonstrated
twenty years ago, when research in the field of blood cancer
revealed [1] that a cell exhibiting the CD34
+
/CD38
-
phenotype
initiates acute myeloid leukemia after transplantation into
SCID mice. Not many years later, a pioneering study [2]
confirmed that CSCs can also be identified in breast cancer
solid tumors and demonstrated that a small subpopulation of
BCSCs bearing the molecular signature CD44
+
/CD24
-/low
/Lin
-
initiated tumor formation when implanted into immunodeficient
NOD/SCID mice. In a series of following studies, the
identification and characterization of CSCs with tumor
generating capacity, also designated as tumor initiating cells,
tumor propagating cells or cancer initiating cells, progressed
in the area of brain [3], liver [4], colorectal cancer [5] and
melanoma [6, 7]. In addition to the origination and
preservation of the neoplastic tissue, CSCs are also
implicated in metastasis formation, the main cause of
decease among cancer patients (reviewed in [8]). In order for
cancer cells to disseminate from a primary tumor mass and
enter the bloodstream, they have to acquire mesenchymal
features, promoting their motility and invasiveness, via their
engagement into an EMT genetic program. Circulating tumor
cells (CTCs) in the blood of cancer patients have long been
considered to be the source of metastasis, the major cause of
*Address correspondence to this author at the University of Crete, School of
Medicine, P.O. Box 2208, 71003 Heraklion, Greece; Tel: +30 2810 394546;
Fax: +30 2810 3945430; E-mail: takis@med.uoc.gr
treatment failure and mortality in cancer patients and are
proposed to have clinical utility in all cancers of epithelial
origin ([9] and references therein). The use of liquid
biopsies, non-invasive blood tests that enable the detection
of CTCs and free nucleotide (DNA or RNA) fragments [10-
16], has offered valuable insight into tumor diagnosis and
treatment. The induction of EMT has been shown to generate
undifferentiated cells with CSC properties [17-20], thus
providing a link between EMT and cancer cell stemness.
Over the last years, a plethora of review and research articles
have emerged on the rapidly evolving field of CSC biology.
Although the role of CSCs in breast cancer, one of the
leading causes of mortality among women, has been
thoroughly highlighted in many stimulating studies,
collective data on the expression of EMT and stem cell
markers on both primary breast cancer tumors and breast
cancer CTCs (BCTCs) are rather lacking. In this review, we
will summarize the current knowledge regarding the
molecular characterization of BCSCs based on data
extrapolated from the study of both solid tumors and BCTCs
(Fig. 1) and we will describe recent advances on the
development of novel anti-cancer strategies specifically
targeting the BCSC subpopulation.
THE CONTRIBUTION OF CSCs AND MICRO-
ENVIRONMENT IN TUMOR PRESERVATION AND
HETEROGENEITY
CSCs are identified based on their capability of self-
renewing, differentiating, forming and sustaining tumors in
mice and propagating as non-adherent tumorspheres ex vivo
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