Prolonged drug selection of breast cancer cells and enrichment of cancer stem cell characteristics

J Natl Cancer Inst. 2010 Nov 3;102(21):1637-52. doi: 10.1093/jnci/djq361. Epub 2010 Oct 8.

Abstract

Background: Cancer stem cells are presumed to have virtually unlimited proliferative and self-renewal abilities and to be highly resistant to chemotherapy, a feature that is associated with overexpression of ATP-binding cassette transporters. We investigated whether prolonged continuous selection of cells for drug resistance enriches cultures for cancer stem-like cells.

Methods: Cancer stem cells were defined as CD44+/CD24⁻ cells that could self-renew (ie, generate cells with the tumorigenic CD44+/CD24⁻ phenotype), differentiate, invade, and form tumors in vivo. We used doxorubicin-selected MCF-7/ADR cells, weakly tumorigenic parental MCF-7 cells, and MCF-7/MDR, an MCF-7 subline with forced expression of ABCB1 protein. Cells were examined for cell surface markers and side-population fractions by microarray and flow cytometry, with in vitro invasion assays, and for ability to form mammospheres. Xenograft tumors were generated in mice to examine tumorigenicity (n = 52). The mRNA expression of multidrug resistance genes was examined in putative cancer stem cells and pathway analysis of statistically significantly differentially expressed genes was performed. All statistical tests were two-sided.

Results: Pathway analysis showed that MCF-7/ADR cells express mRNAs from ABCB1 and other genes also found in breast cancer stem cells (eg, CD44, TGFB1, and SNAI1). MCF-7/ADR cells were highly invasive, formed mammospheres, and were tumorigenic in mice. In contrast to parental MCF-7 cells, more than 30% of MCF-7/ADR cells had a CD44+/CD24⁻ phenotype, could self-renew, and differentiate (ie, produce CD44+/CD24⁻ and CD44+/CD24+ cells) and overexpressed various multidrug resistance-linked genes (including ABCB1, CCNE1, and MMP9). MCF-7/ADR cells were statistically significantly more invasive in Matrigel than parental MCF-7 cells (MCF-7 cells = 0.82 cell per field and MCF-7/ADR = 7.51 cells per field, difference = 6.69 cells per field, 95% confidence interval = 4.82 to 8.55 cells per field, P < .001). No enrichment in the CD44+/CD24⁻ or CD133+ population was detected in MCF-7/MDR.

Conclusion: The cell population with cancer stem cell characteristics increased after prolonged continuous selection for doxorubicin resistance.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, N.I.H., Intramural

MeSH terms

  • AC133 Antigen
  • ATP Binding Cassette Transporter, Subfamily B
  • ATP Binding Cassette Transporter, Subfamily B, Member 1 / genetics
  • Animals
  • Antibiotics, Antineoplastic / pharmacology*
  • Antigens, CD / metabolism
  • Breast Neoplasms / drug therapy*
  • Breast Neoplasms / pathology*
  • CD24 Antigen / metabolism
  • Cell Line, Tumor
  • Cell Movement
  • Cell Proliferation
  • Cell Survival
  • Collagen
  • Confounding Factors, Epidemiologic
  • Disease Models, Animal
  • Doxorubicin / pharmacology*
  • Drug Combinations
  • Drug Resistance, Multiple / genetics*
  • Drug Resistance, Neoplasm / genetics*
  • Female
  • Flow Cytometry
  • Gene Expression Regulation, Neoplastic
  • Glycoproteins / metabolism
  • Humans
  • Hyaluronan Receptors / metabolism
  • Laminin
  • Lung Neoplasms / drug therapy
  • Mice
  • Mice, SCID
  • Microarray Analysis
  • Neoplastic Stem Cells / immunology
  • Neoplastic Stem Cells / metabolism*
  • Neoplastic Stem Cells / pathology
  • Ovarian Neoplasms / drug therapy
  • Peptides / metabolism
  • Proteoglycans
  • RNA, Messenger / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Transplantation, Heterologous
  • Up-Regulation
  • Uterine Cervical Neoplasms / drug therapy

Substances

  • ABCB1 protein, human
  • AC133 Antigen
  • ATP Binding Cassette Transporter, Subfamily B
  • ATP Binding Cassette Transporter, Subfamily B, Member 1
  • Antibiotics, Antineoplastic
  • Antigens, CD
  • CD24 Antigen
  • Drug Combinations
  • Glycoproteins
  • Hyaluronan Receptors
  • Laminin
  • PROM1 protein, human
  • Peptides
  • Prom1 protein, mouse
  • Proteoglycans
  • RNA, Messenger
  • matrigel
  • Doxorubicin
  • Collagen