Extracellular translationally controlled tumor protein promotes colorectal cancer invasion and metastasis through Cdc42/JNK/ MMP9 signaling

Oncotarget. 2016 Aug 2;7(31):50057-50073. doi: 10.18632/oncotarget.10315.

Abstract

The translationally controlled tumor protein (TCTP) can be secreted independently of the endoplasmic reticulum/Golgi pathway and has extrinsic activities when it is characterized as the histamine releasing factor (HRF). Despite its important role in allergies and inflammation, little is known about how extracellular TCTP affects cancer progression. In this study, we found that TCTP was overexpressed in the interstitial tissue of colorectal cancer (CRC) and its expression correlated with poor survival, high pathological grades and metastatic TNM stage in CRC patients. TCTP expression was greater in metastatic liver tissue than in primary tumors and was increased in highly invasive CRC cells. We demonstrated that the expression of TCTP was regulated by HIF-1α and its release was increased in response to low serum and hypoxic stress. Recombinant human TCTP (rhTCTP) promoted the migration and invasiveness of CRC cells in vitro and contributed to distant liver metastasis in vivo. Furthermore, rhTCTP activated Cdc42, phosphorylated JNK (p-JNK), increasing the translocation of p-JNK from the cytoplasm to the nucleus, as well as the secretion of MMP9. In addition, the expression of TCTP positively correlated with that of Cdc42 and p-JNK in clinical CRC samples. The silencing of Cdc42, JNK and MMP9 significantly inhibited the Matrigel invasion of rhTCTP-enhanced CRC cells. Collectively, these results identify a new role for extracellular TCTP as a promoter of CRC progression and liver metastases via Cdc42/JNK/MMP9 activation.

Keywords: Cdc42; extracellular TCTP; metastasis; p-JNK.

MeSH terms

  • Aged
  • Animals
  • Biomarkers, Tumor / metabolism*
  • Cell Line, Tumor
  • Cell Movement
  • Colorectal Neoplasms / metabolism*
  • Disease Progression
  • Female
  • Gene Silencing
  • Humans
  • Hypoxia
  • Inflammation
  • Liver / metabolism
  • MAP Kinase Kinase 4 / metabolism*
  • Male
  • Matrix Metalloproteinase 9 / metabolism*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude
  • Middle Aged
  • Neoplasm Invasiveness
  • Neoplasm Metastasis
  • Recombinant Proteins / metabolism
  • Signal Transduction
  • Tumor Protein, Translationally-Controlled 1
  • cdc42 GTP-Binding Protein / metabolism*

Substances

  • Biomarkers, Tumor
  • Recombinant Proteins
  • TPT1 protein, human
  • Tpt1 protein, mouse
  • Tumor Protein, Translationally-Controlled 1
  • MAP Kinase Kinase 4
  • MMP9 protein, human
  • Matrix Metalloproteinase 9
  • cdc42 GTP-Binding Protein