Endoplasmic reticulum-targeting photosensitizer Hypericin confers chemo-sensitization towards oxaliplatin through inducing pro-death autophagy

Int J Biochem Cell Biol. 2017 Jun:87:54-68. doi: 10.1016/j.biocel.2017.04.001. Epub 2017 Apr 6.

Abstract

Hypericin is an endoplasmic reticulum (ER)-located photosensitizer, which causes oxidative damage to ER during photodynamic therapy (PDT). Hypericin-mediated PDT (HY-PDT) has been confirmed to enhance chemo-sensitivity of oxaliplatin (L-OHP) in colon cancer cells. The present study reveals that autophagy plays a key role in chemosensitization during HY-PDT. We proved pro-death autophagy was required for sensitization and HY-PDT/L-OHP antitumor synergism. High dosage of HY-PDT induced autophagic cell death; while low dose of HY-PDT predominantly triggered protective autophagy and promoted cell proliferation. Low dose of HY-PDT reduced the cytotoxicity of L-OHP in oxaliplatin-resistant colon cancer cells. Different level of autophagy therefore contributed to the opposite effect of HY-PDT on cell fate and chemo-sensitivity. Furthermore, we revealed the role of CHOP as a regulator connecting pro-survival and pro-death autophagy under ER damage. High dose of HY-PDT induced massive ROS generation and severe ER stress, which then led to induction of CHOP. CHOP thereby activated CHOP/TRIB3/Akt/mTOR cascade and triggered autophagic cell death. Additionally, when apoptotic pathway was blocked, cells treated with high dose of HY-PDT preferentially underwent death through autophagic pathway. On the other hand, suppression of autophagy made cells more vulnerable to apoptosis under low dose of HY-PDT. These results provided new evidences for the clinical application of ER-targeting PDT in modifying chemosensitivity of colorectal cancer therapy.

Keywords: Autophagic cell death; Chemo-sensitization; Endoplasmic reticulum (ER); Photodynamic therapy (PDT).

MeSH terms

  • Animals
  • Anthracenes
  • Apoptosis / drug effects
  • Autophagy / drug effects*
  • Dose-Response Relationship, Drug
  • Drug Resistance, Neoplasm / drug effects
  • Drug Synergism
  • Endoplasmic Reticulum / drug effects*
  • Endoplasmic Reticulum / metabolism*
  • Endoplasmic Reticulum Stress / drug effects
  • Female
  • HCT116 Cells
  • Humans
  • Mice
  • Organoplatinum Compounds / pharmacology*
  • Oxaliplatin
  • Perylene / analogs & derivatives*
  • Perylene / pharmacology
  • Photosensitizing Agents / pharmacology*
  • Reactive Oxygen Species / metabolism
  • Xenograft Model Antitumor Assays

Substances

  • Anthracenes
  • Organoplatinum Compounds
  • Photosensitizing Agents
  • Reactive Oxygen Species
  • Oxaliplatin
  • Perylene
  • hypericin