Proteomic comparison of 3D and 2D glioma models reveals increased HLA-E expression in 3D models is associated with resistance to NK cell-mediated cytotoxicity

J Proteome Res. 2014 May 2;13(5):2272-81. doi: 10.1021/pr500064m. Epub 2014 Apr 17.

Abstract

Three-dimensional cell culture techniques can better reflect the in vivo characteristics of tumor cells compared with traditional monolayer cultures. Compared with their 2D counterparts, 3D-cultured tumor cells showed enhanced resistance to the cytotoxic T cell-mediated immune response. However, it remains unclear whether 3D-cultured tumor cells have an enhanced resistance to NK cell cytotoxicity. In this study, a total of 363 differentially expressed proteins were identified between the 2D- and 3D-cultured U251 cells by comparative proteomics, and an immune-associated protein-protein interaction (PPI) network based on these differential proteins was constructed by bioinformatics. Within the network, HLA-E, as a molecule for inhibiting NK cell activation, was significantly up-regulated in the 3D-cultured tumor cells. Then, we found that the 3D-cultured U251 cells exhibited potent resistance to NK cell cytotoxicity in vitro and were prone to tumor formation in vivo. The resistance of the 3D-cultured tumor cells to NK cell lysis was mediated by the HLA-E/NKG2A interaction because the administration of antibodies that block either HLA-E or NKG2A completely eliminated this resistance and significantly decreased tumor formation. Taken together, our findings indicate that HLA-E up-regulation in 3D-cultured cells may result in enhanced tumor resistance to NK cell-mediated immune response.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Blocking / immunology
  • Antibodies, Blocking / pharmacology
  • Blotting, Western
  • Cell Culture Techniques / methods*
  • Cell Line, Tumor
  • Chromatography, Liquid
  • Cytotoxicity, Immunologic / drug effects
  • Cytotoxicity, Immunologic / immunology*
  • Gene Expression / immunology
  • Glioma / immunology*
  • Glioma / metabolism
  • Glioma / pathology
  • HLA-E Antigens
  • Histocompatibility Antigens Class I / genetics
  • Histocompatibility Antigens Class I / immunology*
  • Histocompatibility Antigens Class I / metabolism
  • Humans
  • Killer Cells, Natural / immunology*
  • Killer Cells, Natural / metabolism
  • Mice, Inbred BALB C
  • Mice, Nude
  • Models, Biological*
  • NK Cell Lectin-Like Receptor Subfamily C / immunology
  • NK Cell Lectin-Like Receptor Subfamily C / metabolism
  • Protein Binding / drug effects
  • Protein Binding / immunology
  • Protein Interaction Maps / immunology
  • Proteomics / methods*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Tandem Mass Spectrometry
  • Xenograft Model Antitumor Assays / methods

Substances

  • Antibodies, Blocking
  • Histocompatibility Antigens Class I
  • NK Cell Lectin-Like Receptor Subfamily C