Smart Nanovesicle-Mediated Immunogenic Cell Death through Tumor Microenvironment Modulation for Effective Photodynamic Immunotherapy

ACS Nano. 2020 Jan 28;14(1):620-631. doi: 10.1021/acsnano.9b07212. Epub 2019 Dec 30.

Abstract

Combination therapy that could better balance immune activation and suppressive signals holds great potential in cancer immunotherapy. Herein, we serendipitously found that the pH-responsive nanovesicles (pRNVs) self-assembled from block copolymer polyethylene glycol-b-cationic polypeptide can not only serve as a nanocarrier but also cause immunogenic cell death (ICD) through preapoptotic exposure of calreticulin. After coencapsulation of a photosensitizer, 2-(1-hexyloxyethyl)-2-devinyl pyropheophorbide-a (HPPH) and an indoleamine 2,3-dioxygenase inhibitor, indoximod (IND), pRNVs/HPPH/IND at a single low dose elicited significant antitumor efficacy and abscopal effect following laser irradiation in a B16F10 melanoma tumor model. Treatment efficacy attributes to three key factors: (i) singlet oxygen generation by HPPH-mediated photodynamic therapy (PDT); (ii) increased dendritic cell (DC) recruitment and immune response provocation after ICD induced by pRNVs and PDT; and (iii) tumor microenvironment modulation by IND via enhancing P-S6K phosphorylation for CD8+ T cell development. This study exploited the nanocarrier to induce ICD for the host's immunity activation. The "all-in-one" smart nanovesicles allow the design of multifunctional materials to strengthen cancer immunotherapy efficacy.

Keywords: combination therapy; melanoma cancer immunotherapy; nanovesicle mediated immunogenic cell death; photodynamic therapy; tumor microenvironment modulation.

Publication types

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

MeSH terms

  • Animals
  • Antineoplastic Agents / chemistry
  • Antineoplastic Agents / pharmacology*
  • Apoptosis / drug effects
  • Cell Line, Tumor
  • Drug Carriers / chemistry
  • Drug Carriers / pharmacology
  • Hydrogen-Ion Concentration
  • Immunogenic Cell Death / drug effects*
  • Immunogenic Cell Death / immunology
  • Immunotherapy*
  • Melanoma / immunology
  • Melanoma / pathology
  • Melanoma / therapy*
  • Mice
  • Molecular Structure
  • Nanoparticles / chemistry*
  • Particle Size
  • Peptides / chemistry
  • Peptides / pharmacology
  • Photochemotherapy*
  • Photosensitizing Agents / chemistry
  • Photosensitizing Agents / pharmacology*
  • Polyethylene Glycols / chemistry
  • Polyethylene Glycols / pharmacology
  • Surface Properties
  • Tumor Microenvironment / drug effects
  • Tumor Microenvironment / immunology

Substances

  • Antineoplastic Agents
  • Drug Carriers
  • Peptides
  • Photosensitizing Agents
  • Polyethylene Glycols