Afatinib enhances the efficacy of conventional chemotherapeutic agents by eradicating cancer stem-like cells

Cancer Res. 2014 Aug 15;74(16):4431-45. doi: 10.1158/0008-5472.CAN-13-3553. Epub 2014 Jun 27.

Abstract

Cancer stem cells (CSC) have garnered significant attention as a therapeutic focus, based on evidence that they may represent an etiologic root of treatment-resistant cells. Indeed, expression of the multidrug resistance protein ATP-binding cassette subfamily G member 2 (ABCG2) confers chemoresistance to CSCs, where it serves as a potential biomarker and therapeutic target. Here, we show that afatinib, a small-molecule inhibitor of the tyrosine kinases EGFR, HER2, and HER4, preferentially eliminated side population cells with CSC character, in both cell lines and patient-derived leukemia cells, by decreasing ABCG2 expression. In these cells, afatinib also acted in parallel to suppress self-renewal capacity and tumorigenicity. Combining afatinib with the DNA-damaging drug topotecan enhanced the antitumor effect of topotecan in vitro and in vivo. Mechanistic investigations suggested that ABCG2 suppression by afatinib did not proceed by proteolysis through the ubiquitin-dependent proteosome, lysosome, or calpain. Instead, we found that afatinib increased DNA methyltransferase activity, thereby leading to methylation of the ABCG2 promoter and to a decrease in ABCG2 message level. Taken together, our results advocate the use of afatinib in combination with conventional chemotherapeutic drugs to improve efficacy by improving CSC eradication.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP Binding Cassette Transporter, Subfamily G, Member 2
  • ATP-Binding Cassette Transporters / antagonists & inhibitors
  • ATP-Binding Cassette Transporters / biosynthesis
  • ATP-Binding Cassette Transporters / genetics
  • Afatinib
  • Animals
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology*
  • Cell Line, Tumor
  • DNA Methylation
  • Drug Synergism
  • Humans
  • Leukemia / drug therapy
  • Leukemia / genetics
  • Leukemia / metabolism
  • Leukemia / pathology
  • MCF-7 Cells
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude
  • Neoplasm Proteins / antagonists & inhibitors
  • Neoplasm Proteins / biosynthesis
  • Neoplasm Proteins / genetics
  • Neoplastic Stem Cells / drug effects*
  • Neoplastic Stem Cells / pathology
  • Promoter Regions, Genetic
  • Protein Kinase Inhibitors / pharmacology
  • Quinazolines / administration & dosage
  • Quinazolines / pharmacology*
  • Random Allocation
  • Signal Transduction
  • Topotecan / administration & dosage
  • Topotecan / pharmacology
  • Xenograft Model Antitumor Assays

Substances

  • ABCG2 protein, human
  • ATP Binding Cassette Transporter, Subfamily G, Member 2
  • ATP-Binding Cassette Transporters
  • Neoplasm Proteins
  • Protein Kinase Inhibitors
  • Quinazolines
  • Afatinib
  • Topotecan