BATF2 inhibits chemotherapy resistance by suppressing AP-1 in vincristine-resistant gastric cancer cells

Cancer Chemother Pharmacol. 2019 Dec;84(6):1279-1288. doi: 10.1007/s00280-019-03958-4. Epub 2019 Sep 23.

Abstract

Purpose: Chemotherapy remains the primary treatment used to improve overall survival and quality of life for patients with gastric cancer (GC); however, multidrug resistance is a major reason underlying failure of chemotherapy. Drug resistance (DR) can arise because of molecular changes inhibiting drug-target interactions; for example, overexpression of drug efflux pumps, such as P-gp, mediated by the activation of AP-1. BATF2 is a suppressor of AP-1; therefore, this study aimed to determine how BATF2 interacts with AP-1to inhibit DR in GC cells.

Methods: Expression of BATF2 in drug-responsive and non-responsive GC tumor tissues was evaluated by quantitative PCR and western blotting. Further, expression levels of BATF2- and AP-1-related genes were confirmed in vincristine-resistant SGC7901/VCR cells treated with cisplatin or 5-fluorouracil. A BATF2 overexpression system was established in SGC7901/VCR cells, and then AP-1 also overexpressed in the cells with upregulated BATF2 levels. Further, an AP-1 knockdown system was generated in SGC7901/VCR cells. MTT and flow cytometry assays were performed in the BATF2/AP-1 overexpression system, to evaluate cell proliferation, cell cycle effects, and apoptosis, and the expression of various proteins was detected by western blotting in AP-1/BATF2 overexpression cells. Finally, the effects of BATF2 overexpression in an in vivo nude mouse GC model were evaluated.

Results: We found that BATF2 was overexpressed in tissues from patients with non-responsive GC and the VCR resistance cell line, SGC7901/VCR, while levels of c-Fos and c-Jun were reduced in the SGC7901/VCR cell line. BATF2 overexpression suppressed levels of AP-1 and P-gp. Further, our data demonstrate that cell proliferation is suppressed, and the cell cycle and apoptosis are induced in SGC7901/VCR cells overexpressing both AP-1 and BATF2. Overexpression of AP-1 restored levels of genes downstream of AP-1 in BATF2 overexpressing cells. Compared with controls, tumor growth of SGC7901/VCR cells in nude mice was suppressed in the BATF2 overexpression group.

Conclusion: AP-1 down-regulation by BATF2 overexpression or AP-1 knockdown can inhibit DR in GC cells. These findings suggest that BATF2 inhibits DR in SGC7901/VCR GC cells by down-regulating AP-1 expression.

Keywords: AP-1; BATF2; Drug resistance; Inhibit; Knockdown; Overexpression.

MeSH terms

  • Animals
  • Basic-Leucine Zipper Transcription Factors / genetics
  • Basic-Leucine Zipper Transcription Factors / metabolism*
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cell Proliferation / genetics
  • Chemotherapy, Adjuvant / methods
  • Drug Resistance, Neoplasm / genetics*
  • Female
  • Gastrectomy
  • Gene Expression Regulation, Neoplastic
  • Gene Knockdown Techniques
  • Humans
  • Inhibitory Concentration 50
  • Mice
  • Proto-Oncogene Proteins c-fos / genetics
  • Proto-Oncogene Proteins c-jun / genetics
  • Stomach / pathology
  • Stomach Neoplasms / genetics
  • Stomach Neoplasms / pathology
  • Stomach Neoplasms / therapy*
  • Transcription Factor AP-1 / genetics*
  • Transcription Factor AP-1 / metabolism
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / metabolism*
  • Vincristine / pharmacology*
  • Vincristine / therapeutic use
  • Xenograft Model Antitumor Assays

Substances

  • Basic-Leucine Zipper Transcription Factors
  • Batf2 protein, human
  • Proto-Oncogene Proteins c-fos
  • Proto-Oncogene Proteins c-jun
  • Transcription Factor AP-1
  • Tumor Suppressor Proteins
  • Vincristine