Temporal and spatial evolution of therapy-induced tumor apoptosis detected by caspase-3-selective molecular imaging

Clin Cancer Res. 2013 Jul 15;19(14):3914-24. doi: 10.1158/1078-0432.CCR-12-3814. Epub 2013 May 31.

Abstract

Purpose: Induction of apoptosis in tumors is considered a desired goal of anticancer therapy. We investigated whether the dynamic temporal and spatial evolution of apoptosis in response to cytotoxic and mechanism-based therapeutics could be detected noninvasively by the caspase-3 radiotracer [(18)F]ICMT-11 and positron emission tomography (PET).

Experimental design: The effects of a single dose of the alkylating agent cyclophosphamide (CPA or 4-hydroperoxycyclophosphamide), or the mechanism-based small molecule SMAC mimetic birinapant on caspase-3 activation was assessed in vitro and by [(18)F]ICMT-11-PET in mice bearing 38C13 B-cell lymphoma, HCT116 colon carcinoma, or MDA-MB-231 breast adenocarcinoma tumors. Ex vivo analysis of caspase-3 was compared to the in vivo PET imaging data.

Results: Drug treatment increased the mean [(18)F]ICMT-11 tumor uptake with a peak at 24 hours for CPA (40 mg/kg; AUC40-60: 8.04 ± 1.33 and 16.05 ± 3.35 %ID/mL × min at baseline and 24 hours, respectively) and 6 hours for birinapant (15 mg/kg; AUC40-60: 20.29 ± 0.82 and 31.07 ± 5.66 %ID/mL × min, at baseline and 6 hours, respectively). Voxel-based spatiotemporal analysis of tumor-intrinsic heterogeneity suggested that discrete pockets of caspase-3 activation could be detected by [(18)F]ICMT-11. Increased tumor [(18)F]ICMT-11 uptake was associated with caspase-3 activation measured ex vivo, and early radiotracer uptake predicted apoptosis, distinct from the glucose metabolism with [(18)F]fluorodeoxyglucose-PET, which depicted continuous loss of cell viability.

Conclusion: The proapoptotic effects of CPA and birinapant resulted in a time-dependent increase in [(18)F]ICMT-11 uptake detected by PET. [(18)F]ICMT-11-PET holds promise as a noninvasive pharmacodynamic biomarker of caspase-3-associated apoptosis in tumors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antineoplastic Agents, Alkylating / pharmacology*
  • Apoptosis / drug effects*
  • Azides
  • Breast Neoplasms / diagnostic imaging
  • Breast Neoplasms / drug therapy
  • Breast Neoplasms / enzymology
  • Breast Neoplasms / pathology
  • Caspase 3 / metabolism*
  • Colonic Neoplasms / diagnostic imaging
  • Colonic Neoplasms / drug therapy
  • Colonic Neoplasms / enzymology
  • Colonic Neoplasms / pathology
  • Cyclophosphamide / pharmacology*
  • Dipeptides / pharmacology
  • Enzyme Activation
  • Female
  • HCT116 Cells
  • Humans
  • Indoles / pharmacology
  • Lymphoma, B-Cell / diagnostic imaging
  • Lymphoma, B-Cell / drug therapy
  • Lymphoma, B-Cell / enzymology
  • Lymphoma, B-Cell / pathology
  • Mice
  • Mice, Inbred C3H
  • Positron-Emission Tomography
  • Radiopharmaceuticals
  • Xenograft Model Antitumor Assays

Substances

  • (18)F-ICMT11
  • Antineoplastic Agents, Alkylating
  • Azides
  • Dipeptides
  • Indoles
  • Radiopharmaceuticals
  • birinapant
  • Cyclophosphamide
  • CASP3 protein, human
  • Caspase 3