The roles of Y-box-binding protein (YB)-1 and C-X-C motif chemokine ligand 14 (CXCL14) in the progression of prostate cancer via extracellular-signal-regulated kinase (ERK) signaling

Bioengineered. 2021 Dec;12(2):9128-9139. doi: 10.1080/21655979.2021.1993537.

Abstract

The cold-shock protein Y-box-binding protein (YB)-1 regulates the expression of various chemokines and their receptors at the transcriptional level. Expression of the orphan chemokine CXCL14 is repressed by EGF induced signaling. The possible links between EGF-mediated YB-1 and CXCL14 as well as the functions of critical kinase pathways in the progression of prostate cancer have remained unexplored. Here we examined the correlation between YB-1 and CXCL14, and the ERK/AKT/mTOR pathways in prostate cancer. Knockdown of YB-1 decreased cyclinD1 expression with an upregulation of cleaved-PARP in human prostate cancer cells. EGF treatment upregulated phospho-YB-1 expression in a time-dependent manner, while treatment with an ERK inhibitor completely silenced its expression in prostate cancer cells. EGF treatment stimulates CyclinD1 and YB-1 phosphorylation in an ERK-dependent pathway. Positive and negative regulation of YB-1 and CXCL14 was observed after EGF treatment in prostate cancer cells, respectively. EGF rescues cell cycle and apoptosis via the AKT and ERK pathways. Furthermore, YB-1 silencing induces G1 arrest and apoptosis, while knockdown of CXCL14 facilitates cell growth and inhibits apoptosis in prostate cancer cells. YB-1 and CXCL14 were inversely correlated in prostate cancer cells and tissues. A significant association between poor overall survival and High YB-1 expression was observed in human prostate cancer patients. In conclusion, our data reveal the functional relationship between YB-1 and CXCL14 in EGF mediated ERK signaling, and YB-1 expression is a significant prognostic marker to predict prostate cancer.

Keywords: CXCL14; EGF; ERK pathway; Prostate cancer; YB-1.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis / drug effects
  • Cell Cycle / drug effects
  • Cell Line, Tumor
  • Chemokines, CXC / metabolism*
  • Cyclin D1 / metabolism
  • Disease Progression*
  • Epidermal Growth Factor / pharmacology
  • ErbB Receptors / metabolism
  • Gene Expression Regulation, Neoplastic / drug effects
  • Gene Knockdown Techniques
  • Gene Silencing
  • Humans
  • MAP Kinase Signaling System* / drug effects
  • Male
  • Middle Aged
  • Phosphorylation / drug effects
  • Poly(ADP-ribose) Polymerases / genetics
  • Poly(ADP-ribose) Polymerases / metabolism
  • Prostatic Neoplasms / genetics
  • Prostatic Neoplasms / metabolism*
  • Prostatic Neoplasms / pathology*
  • Signal Transduction
  • Up-Regulation / drug effects
  • Y-Box-Binding Protein 1 / metabolism*

Substances

  • CXCL14 protein, human
  • Chemokines, CXC
  • Y-Box-Binding Protein 1
  • YBX1 protein, human
  • Cyclin D1
  • Epidermal Growth Factor
  • Poly(ADP-ribose) Polymerases
  • EGFR protein, human
  • ErbB Receptors

Grants and funding

This work was supported by Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology of Japan; and the Scientific Research Funds project of Science and Technology Department of Sichuan Province (grant no. Scientific Research Funds Project of Science and Technology Department of Sichuan Province 21YYJC1616 to Yang Liu), the Scientific Research Project of Sichuan Province (grant no. S2002 to Yang Liu).