miR-375 is involved in Hippo pathway by targeting YAP1/TEAD4-CTGF axis in gastric carcinogenesis

Cell Death Dis. 2018 Jan 24;9(2):92. doi: 10.1038/s41419-017-0134-0.

Abstract

miR-375 is a tumor-suppressive microRNA (miRNA) in gastric cancer (GC). However, its molecular mechanism remains unclear. The aim of this study is to comprehensively investigate how miR-375 is involved in Hippo pathway by targeting multiple oncogenes. miR-375 expression in gastric cancer cell lines and primary GC was investigated by qRT-PCR. The regulation of YAP1, TEAD4, and CTGF expression by miR-375 was evaluated by qRT-PCR, western blot, and luciferase reporter assays, respectively. The functional roles of the related genes were examined by siRNA-mediated knockdown or ectopic expression assays. The clinical significance and expression correlation analysis of miR-375, YAP1, and CTGF were performed in primary GCs. TCGA cohort was also used to analyze the expression correlation of YAP1, TEAD4, CTGF, and miR-375 in primary GCs. miR-375 was down-regulated in GC due to promoter methylation and histone deacetylation. miR-375 downregulation was associated with unfavorable outcome and lymph node metastasis. Ectopic expression of miR-375 inhibited tumor growth in vitro and in vivo. Three components of Hippo pathway, YAP1, TEAD4 and CTGF, were revealed to be direct targets of miR-375. The expression of three genes showed a negative correlation with miR-375 expression and YAP1 re-expression partly abolished the tumor-suppressive effect of miR-375. Furthermore, CTGF was confirmed to be the key downstream of Hippo-YAP1 cascade and its knockdown phenocopied siYAP1 or miR-375 overexpression. YAP1 nuclear accumulation was positively correlated with CTGF cytoplasmic expression in primary GC tissues. Verteporfin exerted an anti-oncogenic effect in GC cell lines by quenching CTGF expression through YAP1 degradation. In short, miR-375 was involved in the Hippo pathway by targeting YAP1-TEAD4-CTGF axis and enriched our knowledge on the miRNA dysregulation in gastric tumorigenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / metabolism*
  • Animals
  • Base Sequence
  • Carcinogenesis / genetics*
  • Cell Line, Tumor
  • Connective Tissue Growth Factor / metabolism*
  • DNA-Binding Proteins / metabolism*
  • Down-Regulation / genetics
  • Gene Expression Regulation, Neoplastic
  • Gene Knockdown Techniques
  • Hippo Signaling Pathway
  • Humans
  • Mice, Inbred BALB C
  • Mice, Nude
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Models, Biological
  • Muscle Proteins / metabolism*
  • Phosphoproteins / metabolism*
  • Protein Serine-Threonine Kinases / metabolism*
  • RNA, Small Interfering / metabolism
  • Signal Transduction*
  • Stomach Neoplasms / genetics*
  • Stomach Neoplasms / pathology
  • TEA Domain Transcription Factors
  • Transcription Factors / metabolism*
  • YAP-Signaling Proteins

Substances

  • Adaptor Proteins, Signal Transducing
  • DNA-Binding Proteins
  • MIRN375 microRNA, human
  • MicroRNAs
  • Muscle Proteins
  • Phosphoproteins
  • RNA, Small Interfering
  • TEA Domain Transcription Factors
  • TEAD4 protein, human
  • Transcription Factors
  • YAP-Signaling Proteins
  • YAP1 protein, human
  • Connective Tissue Growth Factor
  • Protein Serine-Threonine Kinases