Knockdown of NIK and IKKβ-Binding Protein (NIBP) Reduces Colorectal Cancer Metastasis through Down-Regulation of the Canonical NF-κΒ Signaling Pathway and Suppression of MAPK Signaling Mediated through ERK and JNK

PLoS One. 2017 Jan 26;12(1):e0170595. doi: 10.1371/journal.pone.0170595. eCollection 2017.

Abstract

Background: Despite the identification of many signaling pathways involved in colorectal cancer (CRC) tumorigenesis, metastatic CRC still remains one of the major causes of cancer related death. NIK and IKKβ-binding protein (NIBP) is one of the key regulators of the NF-κB signaling pathway, which has been implicated in CRC metastasis. The aim of this study was to investigate the possible role of NIBP in CRC metastasis through its regulation of NF-κΒ and extracellular regulated kinase/c-Janus kinase (ERK/JNK) signaling pathways.

Methods: In this study NIBP, phosphorylated (p)-p65, p-ERK1/2, and p-JNK1/2 expression was examined in 130 CRC, and 25 adenoma tissue samples were studied by immunohistochemistry. NIBP shRNA knockdown was performed in HCT116 cells, and NF-κB and ERK/JNK pathway activity was measured after TNF-α stimulation in vitro and in vivo.

Results: We found that NIBP, p-p65, p-ERK1/2, and p-JNK1/2 expression was higher in late stages of CRC compared to early stages or adenomas. Expression of p-p65, p-IκBα, p-IκBβ, p-ERK1/2, and p-JNK1/2 was inhibited in TNF-α stimulated HCT116 cells following NIBP knockdown. Nevertheless, p-ERK1/2 expression in un-transfected and NIBP knockdown HCT116 cells remained the same in the absence of TNF-α stimulation. Furthermore, cell motility and invasion were reduced in HCT116 cells following NIBP knockdown even after TNF-α treatment. Finally, primary tumor weight and liver metastasis were reduced in nude mice with orthotopically transplanted NIBP knockdown of HCT116 cells.

Conclusion: In conclusion, we demonstrated that NIBP knockdown reduces colorectal cancer metastasis through down-regulation of canonical NF-κΒ signaling and suppression of ERK and JNK signaling.

MeSH terms

  • Animals
  • Carcinogenesis / genetics*
  • Carrier Proteins / antagonists & inhibitors
  • Carrier Proteins / genetics*
  • Colorectal Neoplasms / genetics*
  • Colorectal Neoplasms / pathology
  • Gene Expression Regulation, Neoplastic
  • Gene Knockdown Techniques
  • HCT116 Cells
  • Humans
  • Intercellular Signaling Peptides and Proteins
  • MAP Kinase Kinase 1 / genetics
  • MAP Kinase Kinase 4 / genetics
  • MAP Kinase Signaling System / genetics
  • Mice
  • NF-kappa B / genetics*
  • Neoplasm Metastasis / genetics
  • Neoplasm Metastasis / pathology
  • Transcription Factor RelA / genetics
  • Transfection
  • Xenograft Model Antitumor Assays

Substances

  • Carrier Proteins
  • Intercellular Signaling Peptides and Proteins
  • NF-kappa B
  • RELA protein, human
  • TRAPPC9 protein, human
  • Transcription Factor RelA
  • MAP Kinase Kinase 1
  • MAP Kinase Kinase 4

Grants and funding

This work was supported by grants from the National Natural Science Foundation of China (No. 81260365).