Mechanism of the Antitumor and Radiosensitizing Effects of a Manganese Porphyrin, MnHex-2-PyP

Antioxid Redox Signal. 2017 Nov 10;27(14):1067-1082. doi: 10.1089/ars.2016.6889. Epub 2017 Mar 30.

Abstract

Aims: Cationic manganese (Mn)-substituted N-pyridylporphyrin-based potent mimics of the family of superoxide dismutases (SODs) protect normal tissues from injury related to ionizing radiation (IR) by reducing levels of reactive oxygen and nitrogen species (ROS/RNS). Furthermore, Mn-porphyrins have demonstrated antitumor and radiosensitizing effects on cancer cells by promoting IR-induced tumor vasculature damage and apoptotic processes. In this study, we explored the underlying mechanisms of Mn-porphyrin-mediated tumor radiosensitization using murine mammary carcinoma 4T1 and melanoma B16 cells in vitro and in vivo.

Results: Combination treatment with MnTnHex-2-PyP and IR substantially reduced cell viability, clonogenic cell survival, and DNA damage repair and synergistically increased IR-induced apoptosis of 4T1 and B16 cells. MnTnHex-2-PyP in combination with IR caused a significant delay in growth of 4T1 and B16 xenograft tumors. MnTnHex-2-PyP dose-dependently enhanced IR-mediated production of H2O2-derived species, but not superoxide. Catalase overexpression reversed MnTnHex-2-PyP-enhanced ROS production and apoptosis. Demonstrated suppression of phosphorylation of several mitogen-activated protein (MAP) kinases and activation of NF-κB by MnTnHex-2-PyP/IR, which presumably inhibited activation of the antiapoptotic pathway, are in agreement with our other data on the apoptosis of cancer cells. Innovation and Conclusions: MnTnHex-2-PyP exerted a radiosensitizing effect on 4T1 and B16 tumor models in vitro and in vivo via pro-oxidative actions and therefore bears a large therapeutic potential. When combined with IR, it attenuated DNA damage repair and triggered a shift from prosurvival pathways to apoptotic cell death, likely due to increased ROS production and disturbed cellular redox balance, acting at the level of nuclear factor κB (NF-κB). Antioxid. Redox Signal. 27, 1067-1082.

Keywords: MnTnHex-2-PyP; SOD mimic; manganese porphyrin; radiation therapy; radiosensitization; reactive oxygen species.

MeSH terms

  • Animals
  • Breast Neoplasms / metabolism
  • Breast Neoplasms / therapy*
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cell Proliferation / radiation effects
  • Cell Survival / drug effects
  • Cell Survival / radiation effects
  • Female
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • MAP Kinase Signaling System / drug effects
  • Melanoma, Experimental / metabolism
  • Melanoma, Experimental / therapy*
  • Metalloporphyrins / administration & dosage*
  • Metalloporphyrins / pharmacology
  • Mice
  • Phosphorylation / drug effects
  • Phosphorylation / radiation effects
  • Radiation-Sensitizing Agents / administration & dosage*
  • Radiation-Sensitizing Agents / pharmacology
  • Xenograft Model Antitumor Assays

Substances

  • Metalloporphyrins
  • Mn(III) meso-tetrakis(N-n-hexylpyridinium-2-yl)porphyrin
  • Radiation-Sensitizing Agents