Cell Surface Notch Ligand DLL3 is a Therapeutic Target in Isocitrate Dehydrogenase-mutant Glioma

Clin Cancer Res. 2019 Feb 15;25(4):1261-1271. doi: 10.1158/1078-0432.CCR-18-2312. Epub 2018 Nov 5.

Abstract

Purpose: Isocitrate dehydrogenase (IDH)-mutant glioma is a distinct glioma molecular subtype for which no effective molecularly directed therapy exists. Low-grade gliomas, which are 80%-90% IDH-mutant, have high RNA levels of the cell surface Notch ligand DLL3. We sought to determine DLL3 expression by IHC in glioma molecular subtypes and the potential efficacy of an anti-DLL3 antibody-drug conjugate (ADC), rovalpituzumab tesirine (Rova-T), in IDH-mutant glioma.

Experimental design: We evaluated DLL3 expression by RNA using TCGA data and by IHC in a discovery set of 63 gliomas and 20 nontumor brain tissues and a validation set of 62 known IDH wild-type and mutant gliomas using a monoclonal anti-DLL3 antibody. Genotype was determined using a DNA methylation array classifier or by sequencing. The effect of Rova-T on patient-derived endogenous IDH-mutant glioma tumorspheres was determined by cell viability assay.

Results: Compared to IDH wild-type glioblastoma, IDH-mutant gliomas have significantly higher DLL3 RNA (P < 1 × 10-15) and protein by IHC (P = 0.0014 and P < 4.3 × 10-6 in the discovery and validation set, respectively). DLL3 immunostaining was intense and homogeneous in IDH-mutant gliomas, retained in all recurrent tumors, and detected in only 1 of 20 nontumor brains. Patient-derived IDH-mutant glioma tumorspheres overexpressed DLL3 and were potently sensitive to Rova-T in an antigen-dependent manner.

Conclusions: DLL3 is selectively and homogeneously expressed in IDH-mutant gliomas and can be targeted with Rova-T in patient-derived IDH-mutant glioma tumorspheres. Our findings are potentially immediately translatable and have implications for therapeutic strategies that exploit cell surface tumor-associated antigens.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antibodies, Monoclonal, Humanized / genetics
  • Antibodies, Monoclonal, Humanized / therapeutic use
  • Benzodiazepinones / therapeutic use
  • Brain / pathology
  • DNA Methylation / genetics
  • Female
  • Gene Expression Regulation, Neoplastic / drug effects
  • Genotype
  • Glioma / drug therapy*
  • Glioma / genetics
  • Glioma / pathology
  • Humans
  • Immunoconjugates / genetics
  • Immunoconjugates / therapeutic use
  • Intracellular Signaling Peptides and Proteins / genetics*
  • Isocitrate Dehydrogenase / genetics*
  • Ligands
  • Male
  • Membrane Proteins / genetics*
  • Molecular Targeted Therapy*
  • Mutation
  • Neoplasm Recurrence, Local / drug therapy
  • Neoplasm Recurrence, Local / genetics
  • Neoplasm Recurrence, Local / pathology
  • RNA / genetics
  • Receptors, Notch / genetics

Substances

  • Antibodies, Monoclonal, Humanized
  • Benzodiazepinones
  • DLL3 protein, human
  • Immunoconjugates
  • Intracellular Signaling Peptides and Proteins
  • Ligands
  • Membrane Proteins
  • Receptors, Notch
  • rovalpituzumab tesirine
  • RNA
  • Isocitrate Dehydrogenase