MEK5/ERK5 signaling inhibition increases colon cancer cell sensitivity to 5-fluorouracil through a p53-dependent mechanism

Oncotarget. 2016 Jun 7;7(23):34322-40. doi: 10.18632/oncotarget.9107.

Abstract

The MEK5/ERK5 signaling pathway is emerging as an important contributor to colon cancer onset, progression and metastasis; however, its relevance to chemotherapy resistance remains unknown. Here, we evaluated the impact of the MEK5/ERK5 cascade in colon cancer cell sensitivity to 5-fluorouracil (5-FU). Increased ERK5 expression was correlated with poor overall survival in colon cancer patients. In colon cancer cells, 5-FU exposure impaired endogenous KRAS/MEK5/ERK5 expression and/or activation. In turn, MEK5 constitutive activation reduced 5-FU-induced cytotoxicity. Using genetic and pharmacological approaches, we showed that ERK5 inhibition increased caspase-3/7 activity and apoptosis following 5-FU exposure. Mechanistically, this was further associated with increased p53 transcriptional activation of p21 and PUMA. In addition, ERK5 inhibition increased the response of HCT116 p53+/+ cells to 5-FU, but failed to sensitize HCT116 p53-/- cells to the cytotoxic effects of this chemotherapeutic agent, suggesting a p53-dependent axis mediating 5-FU sensitization. Finally, ERK5 inhibition using XMD8-92 was shown to increase the antitumor effects of 5-FU in a murine subcutaneous xenograft model, enhancing apoptosis while markedly reducing tumor growth. Collectively, our results suggest that ERK5-targeted inhibition provides a promising therapeutic approach to overcome resistance to 5-FU-based chemotherapy and improve colon cancer treatment.

Keywords: 5-fluorouracil; MEK5/ERK5; apoptosis; chemosensitization; p53.

MeSH terms

  • Animals
  • Antimetabolites, Antineoplastic / pharmacology*
  • Apoptosis / drug effects
  • Apoptosis Regulatory Proteins / metabolism
  • Benzodiazepinones / pharmacology
  • Caspase 3 / metabolism
  • Caspase 7 / metabolism
  • Cell Line, Tumor
  • Cell Proliferation
  • Colonic Neoplasms / drug therapy*
  • Colonic Neoplasms / genetics
  • Enzyme Activation / drug effects
  • Fluorouracil / pharmacology*
  • HCT116 Cells
  • Humans
  • MAP Kinase Kinase 5 / antagonists & inhibitors
  • MAP Kinase Kinase 5 / metabolism*
  • MAP Kinase Signaling System / drug effects
  • Mice
  • Mice, Inbred BALB C
  • Mice, SCID
  • Mitogen-Activated Protein Kinase 7 / antagonists & inhibitors
  • Mitogen-Activated Protein Kinase 7 / metabolism*
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins p21(ras) / metabolism
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism*
  • Xenograft Model Antitumor Assays

Substances

  • Antimetabolites, Antineoplastic
  • Apoptosis Regulatory Proteins
  • BBC3 protein, human
  • Benzodiazepinones
  • Proto-Oncogene Proteins
  • Tumor Suppressor Protein p53
  • XMD 8-92
  • MAPK7 protein, human
  • Mitogen-Activated Protein Kinase 7
  • MAP Kinase Kinase 5
  • MAP2K5 protein, human
  • Caspase 3
  • Caspase 7
  • Proto-Oncogene Proteins p21(ras)
  • Fluorouracil