Induced phenotype targeted therapy: radiation-induced apoptosis-targeted chemotherapy

J Natl Cancer Inst. 2014 Dec 12;107(2):dju403. doi: 10.1093/jnci/dju403. Print 2015 Feb.

Abstract

Background: Tumor heterogeneity and evolutionary complexity may underlie treatment failure in spite of the development of many targeted agents. We suggest a novel strategy termed induced phenotype targeted therapy (IPTT) to simplify complicated targets because of tumor heterogeneity and overcome tumor evolutionary complexity.

Methods: We designed a caspase-3 specific activatable prodrug, DEVD-S-DOX, containing doxorubicin linked to a peptide moiety (DEVD) cleavable by caspase-3 upon apoptosis. To induce apoptosis locally in the tumor, we used a gamma knife, which can irradiate a very small, defined target area. The in vivo antitumor activity of the caspase-3-specific activatable prodrug combined with radiation was investigated in C3H/HeN tumor-bearing mice (n = 5 per group) and analyzed with the Student's t test or Mann-Whitney U test. All statistical tests were two-sided. We confirmed the basic principle using a caspase-sensitive nanoprobe (Apo-NP).

Results: A single exposure of radiation was able to induce apoptosis in a small, defined region of the tumor, resulting in expression of caspase-3. Caspase-3 cleaved DEVD and activated the prodrug. The released free DOX further activated DEVD-S-DOX by exerting cytotoxic effects on neighboring tumor or supporting cells, which repetitively induced the expression of caspase-3 and the activation of DEVD-S-DOX. This sequential and repetitive process propagated the induction of apoptosis. This novel therapeutic strategy showed not only high efficacy in inhibiting tumor growth (14-day tumor volume [mm(3)] vs radiation alone: 848.21 ± 143.24 vs 2511.50 ± 441.89, P < .01) but also low toxicity to normal cells and tissues.

Conclusion: Such a phenotype induction strategy represents a conceptually novel approach to overcome tumor heterogeneity and complexity as well as to substantially improve current conventional chemoradiotherapy with fewer sequelae and side effects.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibiotics, Antineoplastic / pharmacology*
  • Apoptosis / drug effects*
  • Apoptosis / radiation effects*
  • Blotting, Western
  • Caspase 3 / drug effects
  • Caspase 3 / metabolism*
  • Doxorubicin / administration & dosage
  • Doxorubicin / pharmacology*
  • Gene Expression Regulation, Enzymologic / drug effects
  • Gene Expression Regulation, Enzymologic / radiation effects
  • Gene Expression Regulation, Neoplastic / drug effects
  • Gene Expression Regulation, Neoplastic / radiation effects
  • Immunohistochemistry
  • Mice
  • Mice, Inbred C3H
  • Microscopy, Fluorescence
  • Molecular Targeted Therapy / methods*
  • Peptide Hydrolases / administration & dosage
  • Peptide Hydrolases / pharmacology*
  • Phenotype
  • Prodrugs* / administration & dosage
  • Prodrugs* / pharmacology
  • Radiosurgery*
  • Radiotherapy, Adjuvant

Substances

  • Antibiotics, Antineoplastic
  • Prodrugs
  • Doxorubicin
  • Peptide Hydrolases
  • Caspase 3
  • DEVDase