NFYB-induced high expression of E2F1 contributes to oxaliplatin resistance in colorectal cancer via the enhancement of CHK1 signaling

Cancer Lett. 2018 Feb 28:415:58-72. doi: 10.1016/j.canlet.2017.11.040. Epub 2017 Dec 22.

Abstract

As a third-generation platinum drug, oxaliplatin has been widely applied in colorectal cancer (CRC); however, acquired resistance to oxaliplatin has become a major obstacle. In the present study, we found that the nuclear transcription factor Y subunit beta (NFYB) and E2F transcription factor 1 (E2F1) expression levels were significantly higher in oxaliplatin-resistant DLD1 and RKO CRC (OR-CRC) cells than in non-resistant cells. Additionally, highly expressed NFYB transactivated the E2F1 gene, which is important to maintain oxaliplatin resistance in OR-CRC cells. And Sirt1-dependent deacetylation suppresses the proapoptotic activity of E2F1 in OR-CRC cells. Through profiling the transcriptome of OR-CRC cells following E2F1 knockdown, CHK1 was identified as a target of E2F1. Deprivation of CHK1 sensitized OR-CRC cells to oxaliplatin. In vitro and in vivo phenotype experiments confirmed that an intact NFYB-E2F1-CHK1 axis was required to suppress oxaliplatin-induced apoptosis and maintain the tumorigenicity in OR-CRC cells. Knockdown of E2F1 in OR-CRC cells also decreased the expression of Pol κ, which was essential for CHK1 activation. Consistently, a high level of NFYB, E2F1, or CHK1 predicted poor survival in CRC patients, especially with oxaliplatin treatment. Collectively, the NFYB-E2F1 pathway displays a crucial role in the chemoresistance of OR-CRC by inducing the expression and activation of CHK1, providing a possible therapeutic target for oxaliplatin resistance in CRC.

Keywords: CHK1; Colorectal cancer (CRC); E2F1; NFYB; Oxaliplatin resistance.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Animals
  • Antineoplastic Agents / pharmacology
  • CCAAT-Binding Factor / genetics*
  • CCAAT-Binding Factor / metabolism
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Cell Survival / genetics
  • Checkpoint Kinase 1 / genetics*
  • Checkpoint Kinase 1 / metabolism
  • Colorectal Neoplasms / genetics*
  • Colorectal Neoplasms / metabolism
  • Colorectal Neoplasms / pathology
  • Drug Resistance, Neoplasm / genetics*
  • E2F1 Transcription Factor / genetics*
  • E2F1 Transcription Factor / metabolism
  • Female
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Male
  • Mice, Inbred BALB C
  • Mice, Nude
  • Middle Aged
  • Organoplatinum Compounds / pharmacology*
  • Oxaliplatin
  • RNA Interference
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Survival Analysis
  • Transplantation, Heterologous

Substances

  • Antineoplastic Agents
  • CCAAT-Binding Factor
  • E2F1 Transcription Factor
  • E2F1 protein, human
  • NFYB protein, human
  • Organoplatinum Compounds
  • Oxaliplatin
  • Checkpoint Kinase 1