Targeting Insulin Receptor in Breast Cancer Using Small Engineered Protein Scaffolds

Mol Cancer Ther. 2017 Jul;16(7):1324-1334. doi: 10.1158/1535-7163.MCT-16-0685. Epub 2017 May 3.

Abstract

Insulin receptor (InsR) and the type I insulin-like growth factor (IGF1R) are homologous receptors necessary for signal transduction by their cognate ligands insulin, IGF-I and IGF-II. IGF1R mAbs, intended to inhibit malignant phenotypic signaling, failed to show benefit in patients with endocrine-resistant tumors in phase III clinical trials. Our previous work showed that in tamoxifen-resistant cells, IGF1R expression was lacking, but InsR inhibition effectively blocked growth. In endocrine-sensitive breast cancer cells, insulin was not growth stimulatory, likely due to the presence of hybrid InsR/IGF1R, which has high affinity for IGF-I, but not insulin. Combination inhibition of InsR and IGF1R showed complete suppression of the system in endocrine-sensitive breast cancer cells. To develop InsR-binding agents, we employed a small protein scaffold, T7 phage gene 2 protein (Gp2) with the long-term goal of creating effective InsR inhibitors and diagnostics. Using yeast display and directed evolution, we identified three Gp2 variants (Gp2 #1, #5, and #10) with low nanomolar affinity and specific binding to cell surface InsR. These Gp2 variants inhibited insulin-mediated monolayer proliferation in both endocrine-sensitive and resistant breast cancer, but did not downregulate InsR expression. Gp2 #5 and Gp2 #10 disrupted InsR function by inhibiting ligand-induced receptor activation. In contrast, Gp2 #1 did not block InsR phosphorylation. Notably, Gp2 #1 binding was enhanced by pretreatment of cells with insulin, suggesting a unique receptor-ligand-binding mode. These Gp2 variants are the first nonimmunoglobulin protein scaffolds to target insulin receptor and present compelling opportunity for modulation of InsR signaling. Mol Cancer Ther; 16(7); 1324-34. ©2017 AACR.

MeSH terms

  • Animals
  • Antigens, CD / genetics*
  • Breast Neoplasms / drug therapy*
  • Breast Neoplasms / genetics
  • Breast Neoplasms / pathology
  • Cell Proliferation / drug effects
  • Humans
  • Insulin-Like Growth Factor I / genetics
  • Insulin-Like Growth Factor II / drug effects
  • Mice
  • Nuclear Matrix-Associated Proteins / administration & dosage
  • Nuclear Matrix-Associated Proteins / genetics
  • Protein Binding
  • Receptor, IGF Type 1
  • Receptor, Insulin / antagonists & inhibitors
  • Receptor, Insulin / genetics*
  • Receptors, Somatomedin / antagonists & inhibitors
  • Receptors, Somatomedin / genetics*
  • Repressor Proteins / administration & dosage*
  • Repressor Proteins / genetics
  • Signal Transduction / drug effects
  • Xenograft Model Antitumor Assays

Substances

  • Antigens, CD
  • IGF1R protein, human
  • Nuclear Matrix-Associated Proteins
  • Receptors, Somatomedin
  • Repressor Proteins
  • gene 2 product, bacteriophage T7
  • Insulin-Like Growth Factor I
  • Insulin-Like Growth Factor II
  • INSR protein, human
  • Receptor, IGF Type 1
  • Receptor, Insulin