PTBP3 contributes to colorectal cancer growth and metastasis via translational activation of HIF-1α

J Exp Clin Cancer Res. 2019 Jul 10;38(1):301. doi: 10.1186/s13046-019-1312-y.

Abstract

Background: Colorectal cancer (CRC) remains the fourth most common cause of cancer-related mortality worldwide. We aimed to identify key molecules and signalling pathways mediating CRC growth and metastasis. Polypyrimidine tract-binding protein 3 (PTBP3) is a member of PTB family. A prooncogenic role for PTBP3 has also been discovered in several kinds of tumors. However, the expression and biological functions of the PTBP3 are still unknown in CRC.

Methods: We analysed the expression levels of PTBP3 using tissue microarray containing 568 CRC tissues and corresponding non-tumor adjacent tissues. The correlations between the PTBP3 expression level and clinicopathological features were evaluated using the chi-square test. The functional characterization for the role and molecular mechanism of PTBP3 in CRC was investigated through a series of in vitro and in vivo experiments.

Results: We showed that PTBP3 expression was increased in human CRC, and high PTBP3 expression was correlated with poor five-year overall survival and disease-free survival. Moreover, PTBP3 promoted tumor cell proliferation, migration and invasion in vitro and tumor growth and metastasis in vivo. PTBP3 enhanced HIF-1α protein expression by directly binding to the 5'UTR HIF-1α mRNA and activated translation of HIF-1α. Furthermore, HIF-1α was responsible for PTBP3-induced cell migration and invasion.

Conclusions: PTBP3 appears to be a novel oncogene of CRC through binding to the IRES region of HIF-1α mRNA, which regulates HIF-1α translation. PTBP3 can serve as a promising predictive biomarker for recurrence and prognosis in patients with CRC.

Keywords: Colorectal cancer; HIF-1α; PTBP3; Protein translation; Tumor metastasis.

MeSH terms

  • Adult
  • Aged
  • Cell Line, Tumor
  • Cell Movement / genetics
  • Cell Proliferation
  • Colorectal Neoplasms / genetics*
  • Colorectal Neoplasms / metabolism*
  • Colorectal Neoplasms / mortality
  • Colorectal Neoplasms / pathology
  • Female
  • Gene Expression Regulation, Neoplastic
  • Genes, Reporter
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / genetics
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism*
  • Kaplan-Meier Estimate
  • Male
  • Middle Aged
  • Models, Biological
  • Neoplasm Grading
  • Neoplasm Metastasis
  • Neoplasm Staging
  • Neovascularization, Pathologic / genetics
  • Neovascularization, Pathologic / metabolism
  • Polypyrimidine Tract-Binding Protein / genetics*
  • Polypyrimidine Tract-Binding Protein / metabolism
  • Prognosis
  • Protein Biosynthesis*
  • Y-Box-Binding Protein 1 / metabolism

Substances

  • Hypoxia-Inducible Factor 1, alpha Subunit
  • PTBP3 protein, human
  • Y-Box-Binding Protein 1
  • YBX1 protein, human
  • Polypyrimidine Tract-Binding Protein