Ratiometric activatable cell-penetrating peptides label pancreatic cancer, enabling fluorescence-guided surgery, which reduces metastases and recurrence in orthotopic mouse models

Ann Surg Oncol. 2015;22(6):2082-7. doi: 10.1245/s10434-014-4144-1. Epub 2014 Oct 16.

Abstract

Background: The aim of this study was to evaluate the efficacy of using matrix metalloproteinase-2 (MMP-2) and matrix metalloproteinase-9 (MMP-9)-cleavable ratiometric activatable cell-penetrating peptides (RACPPs) conjugated to Cy5 and Cy7 fluorophores to accurately label pancreatic cancer for fluorescence-guided surgery (FGS) in an orthotopic mouse model.

Methods: Orthotopic mouse models were established using MiaPaCa-2-GFP human pancreatic cancer cells. Two weeks after implantation, tumor-bearing mice were randomized to conventional white light reflectance (WLR) surgery or FGS. FGS was performed at far-red and infrared wavelengths with a customized fluorescence-dissecting microscope 2 h after injection of MMP-2 and MMP-9-cleavable RACPPs. Green fluorescence imaging of the GFP-labeled cancer cells was used to assess the effectiveness of surgical resection and monitor recurrence. At 8 weeks, mice were sacrificed to evaluate tumor burden and metastases.

Results: Mice in the WLR group had larger primary tumors than mice in the FGS group at termination [1.72 g ± standard error (SE) 0.58 vs. 0.25 g ± SE 0.14; respectively, p = 0.026). Mean disease-free survival was significantly lengthened from 5.33 weeks in the WLR group to 7.38 weeks in the FGS group (p = 0.02). Recurrence rates were lower in the FGS group than in the WLR group (38 vs. 73 %; p = 0.049). This translated into lower local and distant recurrence rates for FGS compared to WLR (31 vs. 67 for local recurrence, respectively, and 25 vs. 60 % for distant recurrence, respectively). Metastatic tumor burden was significantly greater in the WLR group than in the FGS group (96.92 mm(2) ± SE 52.03 vs. 2.20 mm(2) ± SE 1.43; respectively, χ (2) = 5.455; p = 0.02).

Conclusions: RACPPs can accurately and effectively label pancreatic cancer for effective FGS, resulting in better postresection outcomes than for WLR surgery.

Publication types

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

MeSH terms

  • Animals
  • Cell-Penetrating Peptides / administration & dosage*
  • Cell-Penetrating Peptides / metabolism
  • Female
  • Fluorescence
  • Green Fluorescent Proteins / metabolism
  • Humans
  • Matrix Metalloproteinase 2 / chemistry
  • Matrix Metalloproteinase 2 / metabolism*
  • Matrix Metalloproteinase 9 / chemistry
  • Matrix Metalloproteinase 9 / metabolism*
  • Mice
  • Mice, Nude
  • Microscopy, Fluorescence
  • Neoplasm Metastasis
  • Neoplasm Recurrence, Local / prevention & control*
  • Optical Imaging / methods
  • Pancreatic Neoplasms / pathology*
  • Pancreatic Neoplasms / surgery*
  • Surgery, Computer-Assisted*
  • Tumor Burden

Substances

  • Cell-Penetrating Peptides
  • Green Fluorescent Proteins
  • Matrix Metalloproteinase 2
  • Matrix Metalloproteinase 9