The regulatory role of APE1 in epithelial-to-mesenchymal transition and in determining EGFR-TKI responsiveness in non-small-cell lung cancer

Cancer Med. 2018 Sep;7(9):4406-4419. doi: 10.1002/cam4.1717. Epub 2018 Aug 14.

Abstract

Background: Epithelial-to-mesenchymal transition (EMT) plays a pivotal role in resistance to EGFR tyrosine kinase inhibitors (TKIs) in non-small-cell lung cancer (NSCLC). Our previous study revealed that in osteosarcoma, human apurinic/apyrimidinic endonuclease 1 (APE1) regulates transforming growth factor-β (TGF-β), an important player in EMT. We therefore hypothesized a link between APE1 and EGFR-TKI responsiveness in NSCLC.

Methods: The protein levels of APE1 were analyzed in tumors of NSCLC patients receiving EGFR-TKI treatment. The correlation between APE1 expression and progression-free survival (PFS), overall survival (OS), or response rate were analyzed. The impact of APE1 on the response to EGFR-TKIs was measured by exogenous manipulation of APE1 in EGFR-TKI-sensitive and EGFR-TKI-resistant cells.

Results: We indicate that low expression of APE1 in tumors is associated with a significantly longer PFS (20.8 months vs 8.4 months, P = 0.008) and a preferential OS (39.0 months vs 17.0 months, P = 0.001), with no difference in initial response rate to EGFR-TKIs. We observed that APE1 protein level was significantly increased in EGFR-TKI-resistant cells and was associated with downregulated E-cadherin and upregulated vimentin. The EMT phenotype, as well as the levels of TGF-β, was suppressed in APE1 knockdown HCC827/IR and PC-9/ER cells, while the EMT phenotype was promoted in APE1-overexpressed HCC827 and PC-9 cells. Furthermore, a specific APE1 redox inhibitor (ie, E3330) effectively reversed the EMT phenotype and further sensitized the cells to EGFR-TKIs.

Conclusion: This study revealed a significant role of APE1 in EGFR-TKI resistance via novel regulatory effects on the EMT phenotype in NSCLC.

Keywords: EGFR-TKI resistance; apurinic/apyrimidinic endonuclease 1; epithelial-to-mesenchymal transition; non-small-cell lung cancer; transforming growth factor-β.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Animals
  • Antineoplastic Agents / pharmacology
  • Biomarkers
  • Carcinoma, Non-Small-Cell Lung / drug therapy
  • Carcinoma, Non-Small-Cell Lung / genetics*
  • Carcinoma, Non-Small-Cell Lung / pathology*
  • DNA-(Apurinic or Apyrimidinic Site) Lyase / genetics*
  • Epithelial-Mesenchymal Transition / genetics*
  • ErbB Receptors / antagonists & inhibitors*
  • ErbB Receptors / genetics
  • Female
  • Gene Deletion
  • Genomics / methods
  • High-Throughput Nucleotide Sequencing
  • Humans
  • Lung Neoplasms / drug therapy
  • Lung Neoplasms / genetics*
  • Lung Neoplasms / pathology*
  • Male
  • Mice
  • Middle Aged
  • Neoplasm Staging
  • Protein Kinase Inhibitors / pharmacology
  • Signal Transduction

Substances

  • Antineoplastic Agents
  • Biomarkers
  • Protein Kinase Inhibitors
  • ErbB Receptors
  • APEX1 protein, human
  • DNA-(Apurinic or Apyrimidinic Site) Lyase