Honokiol Affects Stem Cell Viability by Suppressing Oncogenic YAP1 Function to Inhibit Colon Tumorigenesis

Cells. 2021 Jun 26;10(7):1607. doi: 10.3390/cells10071607.

Abstract

Honokiol (HNK) is a biphenolic compound that has been used in traditional medicine for treating various ailments, including cancers. In this study, we determined the effect of HNK on colon cancer cells in culture and in a colitis-associated cancer model. HNK treatment inhibited proliferation and colony formation while inducing apoptosis. In addition, HNK suppressed colonosphere formation. Molecular docking suggests that HNK interacts with reserve stem cell marker protein DCLK1, with a binding energy of -7.0 Kcal/mol. In vitro kinase assays demonstrated that HNK suppressed the DCLK1 kinase activity. HNK also suppressed the expression of additional cancer stem cell marker proteins LGR5 and CD44. The Hippo signaling pathway is active in intestinal stem cells. In the canonical pathway, YAP1 is phosphorylated at Ser127 by upstream Mst1/2 and Lats1/2. This results in the sequestration of YAP1 in the cytoplasm, thereby not allowing YAP1 to translocate to the nucleus and interact with TEAD1-4 transcription factors to induce gene expression. However, HNK suppressed Ser127 phosphorylation in YAP1, but the protein remains sequestered in the cytoplasm. We further determined that this occurs by YAP1 interacting with PUMA. To determine if this also occurs in vivo, we performed studies in an AOM/DSS induced colitis-associated cancer model. HNK administered by oral gavage at a dose of 5mg/kg bw for 24 weeks demonstrated a significant reduction in the expression of YAP1 and TEAD1 and in the stem marker proteins. Together, these data suggest that HNK prevents colon tumorigenesis in part by inducing PUMA-YAP1 interaction and cytoplasmic sequestration, thereby suppressing the oncogenic YAP1 activity.

Keywords: apoptosis; cancer stem cells; colitis associated cancer; colonospheres; doublecortin-like kinase 1; hippo signaling; leucine-rich repeat-containing G-protein coupled receptor 5; spheroids.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adaptor Proteins, Signal Transducing / metabolism*
  • Animals
  • Apoptosis / drug effects
  • Apoptosis Regulatory Proteins / metabolism
  • Biomarkers, Tumor / metabolism
  • Biphenyl Compounds / pharmacology*
  • Carcinogenesis / drug effects
  • Carcinogenesis / pathology*
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cell Survival / drug effects
  • Colitis / complications
  • Colonic Neoplasms / pathology*
  • Doublecortin-Like Kinases
  • Down-Regulation / drug effects
  • Hippo Signaling Pathway
  • Humans
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Lignans / pharmacology*
  • Male
  • Mice
  • Mice, Inbred ICR
  • Models, Biological
  • Neoplastic Stem Cells / drug effects
  • Neoplastic Stem Cells / pathology*
  • Protein Binding / drug effects
  • Protein Serine-Threonine Kinases / metabolism
  • Proto-Oncogene Proteins / metabolism
  • Signal Transduction / drug effects
  • Transcription Factors / metabolism*
  • Tumor Stem Cell Assay
  • YAP-Signaling Proteins

Substances

  • Adaptor Proteins, Signal Transducing
  • Apoptosis Regulatory Proteins
  • BBC3 protein, human
  • Biomarkers, Tumor
  • Biphenyl Compounds
  • Intracellular Signaling Peptides and Proteins
  • Lignans
  • Proto-Oncogene Proteins
  • Transcription Factors
  • YAP-Signaling Proteins
  • YAP1 protein, human
  • honokiol
  • DCLK1 protein, human
  • Doublecortin-Like Kinases
  • Protein Serine-Threonine Kinases