Early gene expression analysis in 9L orthotopic tumor-bearing rats identifies immune modulation in molecular response to synchrotron microbeam radiation therapy

PLoS One. 2013 Dec 31;8(12):e81874. doi: 10.1371/journal.pone.0081874. eCollection 2013.

Abstract

Synchrotron Microbeam Radiation Therapy (MRT) relies on the spatial fractionation of the synchrotron photon beam into parallel micro-beams applying several hundred of grays in their paths. Several works have reported the therapeutic interest of the radiotherapy modality at preclinical level, but biological mechanisms responsible for the described efficacy are not fully understood to date. The aim of this study was to identify the early transcriptomic responses of normal brain and glioma tissue in rats after MRT irradiation (400Gy). The transcriptomic analysis of similarly irradiated normal brain and tumor tissues was performed 6 hours after irradiation of 9 L orthotopically tumor-bearing rats. Pangenomic analysis revealed 1012 overexpressed and 497 repressed genes in the irradiated contralateral normal tissue and 344 induced and 210 repressed genes in tumor tissue. These genes were grouped in a total of 135 canonical pathways. More than half were common to both tissues with a predominance for immunity or inflammation (64 and 67% of genes for normal and tumor tissues, respectively). Several pathways involving HMGB1, toll-like receptors, C-type lectins and CD36 may serve as a link between biochemical changes triggered by irradiation and inflammation and immunological challenge. Most immune cell populations were involved: macrophages, dendritic cells, natural killer, T and B lymphocytes. Among them, our results highlighted the involvement of Th17 cell population, recently described in tumor. The immune response was regulated by a large network of mediators comprising growth factors, cytokines, lymphokines. In conclusion, early response to MRT is mainly based on inflammation and immunity which appear therefore as major contributors to MRT efficacy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptive Immunity / genetics
  • Adaptive Immunity / radiation effects
  • Animals
  • Brain / immunology
  • Brain / radiation effects
  • Brain Neoplasms / genetics*
  • Brain Neoplasms / immunology
  • Brain Neoplasms / radiotherapy*
  • Cell Line, Tumor
  • Gene Expression / radiation effects
  • Gene Expression Profiling
  • Genes, MHC Class II / radiation effects*
  • Glioma / genetics*
  • Glioma / immunology
  • Glioma / radiotherapy*
  • Immunity, Innate / genetics
  • Immunity, Innate / radiation effects
  • Male
  • Oligonucleotide Array Sequence Analysis
  • Radiotherapy / methods
  • Rats
  • Rats, Inbred F344
  • Signal Transduction / immunology
  • Signal Transduction / radiation effects
  • Synchrotrons

Grants and funding

This work was supported by the French National Institute of Health and Medical Research INSERM (U836), European Synchrotron Radiation Facility and Institut National du Cancer (INCa - Bioresis program). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.