Simulated space radiation-induced mutants in the mouse kidney display widespread genomic change

PLoS One. 2017 Jul 6;12(7):e0180412. doi: 10.1371/journal.pone.0180412. eCollection 2017.

Abstract

Exposure to a small number of high-energy heavy charged particles (HZE ions), as found in the deep space environment, could significantly affect astronaut health following prolonged periods of space travel if these ions induce mutations and related cancers. In this study, we used an in vivo mutagenesis assay to define the mutagenic effects of accelerated 56Fe ions (1 GeV/amu, 151 keV/μm) in the mouse kidney epithelium exposed to doses ranging from 0.25 to 2.0 Gy. These doses represent fluences ranging from 1 to 8 particle traversals per cell nucleus. The Aprt locus, located on chromosome 8, was used to select induced and spontaneous mutants. To fully define the mutagenic effects, we used multiple endpoints including mutant frequencies, mutation spectrum for chromosome 8, translocations involving chromosome 8, and mutations affecting non-selected chromosomes. The results demonstrate mutagenic effects that often affect multiple chromosomes for all Fe ion doses tested. For comparison with the most abundant sparsely ionizing particle found in space, we also examined the mutagenic effects of high-energy protons (1 GeV, 0.24 keV/μm) at 0.5 and 1.0 Gy. Similar doses of protons were not as mutagenic as Fe ions for many assays, though genomic effects were detected in Aprt mutants at these doses. Considered as a whole, the data demonstrate that Fe ions are highly mutagenic at the low doses and fluences of relevance to human spaceflight, and that cells with considerable genomic mutations are readily induced by these exposures and persist in the kidney epithelium. The level of genomic change produced by low fluence exposure to heavy ions is reminiscent of the extensive rearrangements seen in tumor genomes suggesting a potential initiation step in radiation carcinogenesis.

MeSH terms

  • Animals
  • Carcinogenesis / radiation effects
  • Chromosomes / chemistry
  • Chromosomes / radiation effects*
  • Cosmic Radiation / adverse effects
  • Epithelium / radiation effects*
  • Female
  • Genetic Loci / radiation effects
  • Heavy Ions
  • Iron Radioisotopes / adverse effects*
  • Kidney / radiation effects*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Inbred DBA
  • Photons / adverse effects*
  • Space Simulation
  • Tissue Culture Techniques
  • Translocation, Genetic / radiation effects*

Substances

  • Iron Radioisotopes

Grants and funding

This work was supported by NASA grants NNX10AC12G, NNX14AC97G, NNJ12HB88I, and NNJ16HP23I, Murdock Scholar Fellowships to Gwen Hryciw and Sorrel Johnson, and an Oregon Institute of Occupational Health Sciences summer fellowship to Bradley Eckelmann, and the Ted. R. Lilley Cancer Cure fellowship for high school students. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.