Image-Based Modeling Reveals Dynamic Redistribution of DNA Damage into Nuclear Sub-Domains

Costes, Sylvain V.; Ponomarev, Artem; Chen, James L.; Nguyen, David; Cucinotta, Francis A.; Barcellos-Hoff, Mary Helen

doi:10.1371/journal.pcbi.0030155

Image-Based Modeling Reveals Dynamic Redistribution of DNA Damage into Nuclear Sub-Domains

Journal Article · Fri Aug 03 00:00:00 EDT 2007 · PLoS Computational Biology (Online)

DOI:https://doi.org/10.1371/journal.pcbi.0030155· OSTI ID:1627183

Costes, Sylvain V. ^[1]; Ponomarev, Artem ^[2]; Chen, James L. ^[3]; Nguyen, David ^[3]; Cucinotta, Francis A. ^[4]; Barcellos-Hoff, Mary Helen ^[3]

Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Life Sciences Division; DOE/OSTI
NASA Johnson Space Center, Houston, TX (United States); Universities Space Research Association, Houston, TX (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Life Sciences Division
NASA Johnson Space Center, Houston, TX (United States)

Several proteins involved in the response to DNA double strand breaks (DSB) form microscopically visible nuclear domains, or foci, after exposure to ionizing radiation. Radiation-induced foci (RIF) are believed to be located where DNA damage occurs. To test this assumption, we analyzed the spatial distribution of 53BP1, phosphorylated ATM, and cH2AX RIF in cells irradiated with high linear energy transfer (LET) radiation and low LET. Since energy is randomly deposited along high-LET particle paths, RIF along these paths should also be randomly distributed. The probability to induce DSB can be derived from DNA fragment data measured experimentally by pulsed-field gel electrophoresis. We used this probability in Monte Carlo simulations to predict DSB locations in synthetic nuclei geometrically described by a complete set of human chromosomes, taking into account microscope optics from real experiments. As expected, simulations produced DNA-weighted random (Poisson) distributions. In contrast, the distributions of RIF obtained as early as 5 min after exposure to high LET (1 GeV/amu Fe) were non-random. This deviation from the expected DNA-weighted random pattern can be further characterized by ‘‘relative DNA image measurements.’’ This novel imaging approach shows that RIF were located preferentially at the interface between high and low DNA density regions, and were more frequent than predicted in regions with lower DNA density. The same preferential nuclear location was also measured for RIF induced by 1 Gy of low-LET radiation. This deviation from random behavior was evident only 5 min after irradiation for phosphorylated ATM RIF, while cH2AX and 53BP1 RIF showed pronounced deviations up to 30 min after exposure. These data suggest that DNA damage–induced foci are restricted to certain regions of the nucleus of human epithelial cells. It is possible that DNA lesions are collected in these nuclear sub-domains for more efficient repair.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1627183

Journal Information:: PLoS Computational Biology (Online), Journal Name: PLoS Computational Biology (Online) Journal Issue: 8 Vol. 3; ISSN 1553-7358

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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