Characterization of plasma-derived protoporphyrin-IX-positive extracellular vesicles following 5-ALA use in patients with malignant glioma

EBioMedicine. 2019 Oct:48:23-35. doi: 10.1016/j.ebiom.2019.09.025. Epub 2019 Oct 15.

Abstract

Background: Malignant gliomas are rapidly progressive brain tumors with high mortality. Fluorescence guided surgery (FGS) with 5-aminolevulinic acid (5-ALA) provides fluorescent delineation of malignant tissue, which helps achieve maximum safe resection. 5-ALA-based fluorescence is due to preferential accumulation of the fluorophore protoporphyrin-IX (PpIX) in malignant glioma tissue. Additionally, gliomas cells release extracellular vesicles (EVs) which carry biomarkers of disease. Herein, we performed animal and human studies to investigate whether 5-ALA dosed glioma cells, in vitro and in vivo, release PpIX positive EVs in circulation which can be captured and analyzed.

Methods: We used imaging flow cytometry (IFC) to characterize PpIX-positive EVs released from 5-ALA-dosed glioma cells, glioma-bearing xenograft models, as well as patients with malignant glioma undergoing FGS.

Findings: We first show that glioma cells dosed with 5-ALA release 247-fold higher PpIX positive EVs compared to mock dosed glioma cells. Second, we demonstrate that the plasma of glioma-bearing mice (n = 2) dosed with 5-ALA contain significantly higher levels of circulating PpIX-positive EVs than their pre-dosing background (p = 0.004). Lastly, we also show that the plasma of patients with avidly fluorescent tumors (n = 4) undergoing FGS contain circulating PpIX-positive EVs at levels significantly higher than their pre-dosing background (p = 0.00009) and this rise in signal correlates with enhancing tumor volumes (r 2 = 0.888).

Interpretation: Our findings highlight the potential of plasma-derived PpIX-positive EV-based diagnostics for malignant gliomas, offering a novel liquid biopsy platform for confirming and monitoring tumor status.

Keywords: 5-ALA; Extracellular vesicles; Fluorescence guided surgery; Imaging flow cytometry; Liquid biopsy; Malignant gliomas.

MeSH terms

  • Adult
  • Aged
  • Aminolevulinic Acid
  • Animals
  • Cell Line, Tumor
  • Cell Survival
  • Disease Models, Animal
  • Extracellular Vesicles / metabolism*
  • Female
  • Fluorescent Dyes / administration & dosage*
  • Glioma / diagnosis
  • Glioma / metabolism*
  • Glioma / surgery
  • Humans
  • Levulinic Acids / administration & dosage*
  • Magnetic Resonance Imaging
  • Male
  • Mice
  • Mice, Transgenic
  • Middle Aged
  • Optical Imaging / methods
  • Photosensitizing Agents / metabolism*
  • Protoporphyrins / metabolism*
  • Surgery, Computer-Assisted

Substances

  • Fluorescent Dyes
  • Levulinic Acids
  • Photosensitizing Agents
  • Protoporphyrins
  • protoporphyrin IX