Targeted Drug Delivery with an Integrin-Binding Knottin-Fc-MMAF Conjugate Produced by Cell-Free Protein Synthesis

Mol Cancer Ther. 2016 Jun;15(6):1291-300. doi: 10.1158/1535-7163.MCT-15-0881. Epub 2016 Mar 29.

Abstract

Antibody-drug conjugates (ADC) have generated significant interest as targeted therapeutics for cancer treatment, demonstrating improved clinical efficacy and safety compared with systemic chemotherapy. To extend this concept to other tumor-targeting proteins, we conjugated the tubulin inhibitor monomethyl-auristatin-F (MMAF) to 2.5F-Fc, a fusion protein composed of a human Fc domain and a cystine knot (knottin) miniprotein engineered to bind with high affinity to tumor-associated integrin receptors. The broad expression of integrins (including αvβ3, αvβ5, and α5β1) on tumor cells and their vasculature makes 2.5F-Fc an attractive tumor-targeting protein for drug delivery. We show that 2.5F-Fc can be expressed by cell-free protein synthesis, during which a non-natural amino acid was introduced into the Fc domain and subsequently used for site-specific conjugation of MMAF through a noncleavable linker. The resulting knottin-Fc-drug conjugate (KFDC), termed 2.5F-Fc-MMAF, had approximately 2 drugs attached per KFDC. 2.5F-Fc-MMAF inhibited proliferation in human glioblastoma (U87MG), ovarian (A2780), and breast (MB-468) cancer cells to a greater extent than 2.5F-Fc or MMAF alone or added in combination. As a single agent, 2.5F-Fc-MMAF was effective at inducing regression and prolonged survival in U87MG tumor xenograft models when administered at 10 mg/kg two times per week. In comparison, tumors treated with 2.5F-Fc or MMAF were nonresponsive, and treatment with a nontargeted control, CTRL-Fc-MMAF, showed a modest but not significant therapeutic effect. These studies provide proof-of-concept for further development of KFDCs as alternatives to ADCs for tumor targeting and drug delivery applications. Mol Cancer Ther; 15(6); 1291-300. ©2016 AACR.

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cell Survival / drug effects
  • Cell-Free System
  • Cystine-Knot Miniproteins / chemistry*
  • Drug Delivery Systems
  • Humans
  • Immunoconjugates / chemistry
  • Immunoconjugates / pharmacology*
  • Immunoglobulin Fc Fragments / chemistry
  • Integrins / chemistry
  • Integrins / metabolism*
  • Mice
  • Neoplasms / drug therapy*
  • Oligopeptides / chemistry
  • Oligopeptides / pharmacology*
  • Peptides / chemistry
  • Protein Binding
  • Xenograft Model Antitumor Assays

Substances

  • Cystine-Knot Miniproteins
  • Immunoconjugates
  • Immunoglobulin Fc Fragments
  • Integrins
  • Oligopeptides
  • Peptides
  • monomethylauristatin F