Ultrasound-mediated delivery of doxorubicin to the brain results in immune modulation and improved responses to PD-1 blockade in gliomas

Nat Commun. 2024 Jun 6;15(1):4698. doi: 10.1038/s41467-024-48326-w.

Abstract

Given the marginal penetration of most drugs across the blood-brain barrier, the efficacy of various agents remains limited for glioblastoma (GBM). Here we employ low-intensity pulsed ultrasound (LIPU) and intravenously administered microbubbles (MB) to open the blood-brain barrier and increase the concentration of liposomal doxorubicin and PD-1 blocking antibodies (aPD-1). We report results on a cohort of 4 GBM patients and preclinical models treated with this approach. LIPU/MB increases the concentration of doxorubicin by 2-fold and 3.9-fold in the human and murine brains two days after sonication, respectively. Similarly, LIPU/MB-mediated blood-brain barrier disruption leads to a 6-fold and a 2-fold increase in aPD-1 concentrations in murine brains and peritumoral brain regions from GBM patients treated with pembrolizumab, respectively. Doxorubicin and aPD-1 delivered with LIPU/MB upregulate major histocompatibility complex (MHC) class I and II in tumor cells. Increased brain concentrations of doxorubicin achieved by LIPU/MB elicit IFN-γ and MHC class I expression in microglia and macrophages. Doxorubicin and aPD-1 delivered with LIPU/MB results in the long-term survival of most glioma-bearing mice, which rely on myeloid cells and lymphocytes for their efficacy. Overall, this translational study supports the utility of LIPU/MB to potentiate the antitumoral activities of doxorubicin and aPD-1 for GBM.

MeSH terms

  • Animals
  • Antibodies, Monoclonal, Humanized / administration & dosage
  • Antibodies, Monoclonal, Humanized / pharmacology
  • Antibodies, Monoclonal, Humanized / therapeutic use
  • Blood-Brain Barrier* / drug effects
  • Blood-Brain Barrier* / metabolism
  • Brain / drug effects
  • Brain / metabolism
  • Brain Neoplasms* / drug therapy
  • Brain Neoplasms* / immunology
  • Brain Neoplasms* / pathology
  • Cell Line, Tumor
  • Doxorubicin* / administration & dosage
  • Doxorubicin* / analogs & derivatives
  • Doxorubicin* / pharmacology
  • Doxorubicin* / therapeutic use
  • Drug Delivery Systems
  • Female
  • Glioblastoma / drug therapy
  • Glioblastoma / immunology
  • Glioblastoma / pathology
  • Glioma / drug therapy
  • Glioma / immunology
  • Glioma / pathology
  • Humans
  • Immune Checkpoint Inhibitors / administration & dosage
  • Immune Checkpoint Inhibitors / pharmacology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Microbubbles*
  • Microglia / drug effects
  • Microglia / metabolism
  • Polyethylene Glycols
  • Programmed Cell Death 1 Receptor* / antagonists & inhibitors
  • Programmed Cell Death 1 Receptor* / metabolism
  • Ultrasonic Waves

Substances

  • Doxorubicin
  • Programmed Cell Death 1 Receptor
  • liposomal doxorubicin
  • pembrolizumab
  • Antibodies, Monoclonal, Humanized
  • Immune Checkpoint Inhibitors
  • PDCD1 protein, human
  • Polyethylene Glycols