Oxidative stress in malignant melanoma enhances tumor necrosis factor-α secretion of tumor-associated macrophages that promote cancer cell invasion

Antioxid Redox Signal. 2013 Oct 20;19(12):1337-55. doi: 10.1089/ars.2012.4617. Epub 2013 Mar 28.

Abstract

Aims: Malignant melanoma is well known for abundant reactive oxygen species (ROS) that exist in the primary tumor environment. Within this microenvironment, tumor-associated macrophages (TAMs) play substantial roles in multiple steps of tumor development in terms of tumor growth, invasion, and metastasis. We therefore aimed to determine whether this high-level ROS in primary melanoma is capable to promote tumor invasiveness by influencing TAM properties. Moreover, we wanted to further investigate probable underlying mechanisms.

Results: We characterized malignant melanoma TAMs as a heterogeneous phenotype, which possesses both M1 and M2 markers. We also revealed a role for high-level intracellular ROS in enhancing proinvasion signature of TAMs by strongly increasing their tumor necrosis factor α secretion, which is possibly attributed to ROS-enhanced peroxisome proliferator-activated receptor γ (PPARγ) translocation mediated by MAPK/ERK kinase 1.

Innovation: This is the first study demonstrating that high levels of ROS in the primary melanoma environment can influence TAM behaviors. Furthermore, we are also the first to indentify that nucleus-to-cytoplasm translocation of PPARγ is significantly upregulated by ROS and responsible for the proinvasiveness capacity of melanoma TAMs.

Conclusion: Taken together, our data describe how a high level of ROS plays a critical role in enhancing the proinvasion characteristic of TAMs in malignant melanoma.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Nucleus / metabolism
  • MAP Kinase Kinase 1 / metabolism
  • Macrophages / metabolism*
  • Melanoma, Experimental / immunology
  • Melanoma, Experimental / metabolism*
  • Melanoma, Experimental / pathology
  • Mice
  • Neoplasm Invasiveness
  • Neoplasm Transplantation
  • Oligonucleotide Array Sequence Analysis
  • Oxidative Stress*
  • PPAR gamma / metabolism
  • Protein Transport
  • Reactive Oxygen Species / metabolism
  • Transcriptome
  • Tumor Necrosis Factor-alpha / metabolism*

Substances

  • PPAR gamma
  • Reactive Oxygen Species
  • Tumor Necrosis Factor-alpha
  • MAP Kinase Kinase 1