Multivalent Forms of the Notch Ligand DLL-1 Enhance Antitumor T-cell Immunity in Lung Cancer and Improve Efficacy of EGFR-Targeted Therapy

Cancer Res. 2015 Nov 15;75(22):4728-41. doi: 10.1158/0008-5472.CAN-14-1154. Epub 2015 Sep 24.

Abstract

Activation of Notch signaling in hematopoietic cells by tumors contributes to immune escape. T-cell defects in tumors can be reversed by treating tumor-bearing mice with multivalent forms of the Notch receptor ligand DLL-1, but the immunologic correlates of this effect have not been elucidated. Here, we report mechanistic insights along with the efficacy of combinational treatments of multivalent DLL-1 with oncoprotein targeting drugs in preclinical mouse models of lung cancer. Systemic DLL-1 administration increased T-cell infiltration into tumors and elevated numbers of CD44(+)CD62L(+)CD8(+) memory T cells while decreasing the number of regulatory T cells and limiting tumor vascularization. This treatment was associated with upregulation of Notch and its ligands in tumor-infiltrating T cells enhanced expression of T-bet and phosphorylation of Stat1/2. Adoptive transfer of T cells from DLL1-treated tumor-bearing immunocompetent hosts into tumor-bearing SCID-NOD immunocompromised mice attenuated tumor growth and extended tumor-free survival in the recipients. When combined with the EGFR-targeted drug erlotinib, DLL-1 significantly improved progression-free survival by inducing robust tumor-specific T-cell immunity. In tissue culture, DLL1 induced proliferation of human peripheral T cells, but lacked proliferative or clonogenic effects on lung cancer cells. Our findings offer preclinical mechanistic support for the development of multivalent DLL1 to stimulate antitumor immunity.

Publication types

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

MeSH terms

  • Adoptive Transfer
  • Animals
  • Antineoplastic Agents / pharmacology
  • Blotting, Western
  • Calcium-Binding Proteins
  • Cell Line, Tumor
  • Disease Models, Animal
  • ErbB Receptors / antagonists & inhibitors
  • Erlotinib Hydrochloride / pharmacology
  • Female
  • Flow Cytometry
  • Humans
  • Immunohistochemistry
  • Immunotherapy / methods
  • Intercellular Signaling Peptides and Proteins / pharmacology*
  • Lung Neoplasms / drug therapy
  • Lung Neoplasms / immunology*
  • Lymphocytes, Tumor-Infiltrating / immunology*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Inbred NOD
  • Mice, SCID
  • Receptors, Notch / agonists
  • Recombinant Fusion Proteins / pharmacology
  • T-Lymphocytes / immunology*

Substances

  • Antineoplastic Agents
  • Calcium-Binding Proteins
  • Dlk1 protein, mouse
  • Intercellular Signaling Peptides and Proteins
  • Receptors, Notch
  • Recombinant Fusion Proteins
  • Erlotinib Hydrochloride
  • EGFR protein, mouse
  • ErbB Receptors