MERTK Inhibition Induces Polyploidy and Promotes Cell Death and Cellular Senescence in Glioblastoma Multiforme

PLoS One. 2016 Oct 26;11(10):e0165107. doi: 10.1371/journal.pone.0165107. eCollection 2016.

Abstract

Background: MER receptor tyrosine kinase (MERTK) is expressed in a variety of malignancies, including glioblastoma multiforme (GBM). Our previous work demonstrated that inhibition of MERTK using RNA interference induced cell death and chemosensitivity in GBM cells, implicating MERTK as a potential therapeutic target. Here we investigate whether a novel MERTK-selective small molecule tyrosine kinase inhibitor, UNC2025, has similar anti-tumor effects in GBM cell lines.

Methods: Correlations between expression of GAS6, a MERTK ligand, and prognosis were determined using data from the TCGA database. GBM cell lines (A172, SF188, U251) were treated in vitro with increasing doses of UNC2025 (50-400nM). Cell count and viability were determined by trypan blue exclusion. Cell cycle profiles and induction of apoptosis were assessed by flow cytometric analysis after BrdU or Po-Pro-1/propidium iodide staining, respectively. Polyploidy was detected by propidium iodide staining and metaphase spread. Cellular senescence was determined by β-galactosidase staining and senescence-associated secretory cytokine analysis.

Results: Decreased overall survival significantly correlated with high levels of GAS6 expression in GBM, highlighting the importance of TAM kinase signaling in GBM tumorigenesis and/or therapy resistance and providing strong rationale for targeting these pathways in the clinic. All three GBM cell lines exhibited dose dependent reductions in cell number and colony formation (>90% at 200nM) after treatment with UNC2025. Cell cycle analysis demonstrated accumulation of cells in the G2/M phase and development of polyploidy. After extended exposure, 60-80% of cells underwent apoptosis. The majority of surviving cells (65-95%) were senescent and did not recover after drug removal. Thus, UNC2025 mediates anti-tumor activity in GBM by multiple mechanisms.

Conclusions: The findings described here provide further evidence of oncogenic roles for MERTK in GBM, demonstrate the importance of kinase activity for MERTK tumorigenicity and validate UNC2025, a novel MERTK inhibitor, as a potential therapeutic agent for treatment of GBM.

MeSH terms

  • Adenine / analogs & derivatives*
  • Adenine / pharmacology
  • Antineoplastic Agents / pharmacology
  • Cell Death / drug effects*
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cellular Senescence / drug effects*
  • Enzyme Activation / drug effects
  • Gene Expression Regulation, Neoplastic / drug effects
  • Glioblastoma / pathology*
  • Humans
  • Intercellular Signaling Peptides and Proteins / metabolism
  • Neural Stem Cells / drug effects
  • Neural Stem Cells / pathology
  • Piperazines / pharmacology*
  • Polyploidy*
  • Prognosis
  • Protein Kinase Inhibitors / pharmacology*
  • Proto-Oncogene Proteins / antagonists & inhibitors*
  • Receptor Protein-Tyrosine Kinases / antagonists & inhibitors*
  • c-Mer Tyrosine Kinase

Substances

  • Antineoplastic Agents
  • Intercellular Signaling Peptides and Proteins
  • Piperazines
  • Protein Kinase Inhibitors
  • Proto-Oncogene Proteins
  • UNC2025
  • growth arrest-specific protein 6
  • MERTK protein, human
  • Receptor Protein-Tyrosine Kinases
  • c-Mer Tyrosine Kinase
  • Adenine