Mechanisms of enhanced cell killing at low doses: Implications for radiation risk

B. Marples, P. Johnston, S.D. Scott, G.D. Wilson and M.C. Joiner
Gray Laboratory CRT, Mount Vernon Hospital, Northwood, Middlesex, HA6 2JR, UK

Over the last decade we have demonstrated that radiation sensitivity can be dose-dependent with small acute exposures (typically below ~50 cGy) being more lethal per unit dose than larger exposures (> 1 Gy). This change in radiosensitivity has given rise to the descriptive terms low dose hyper-radiosensitivity (HRS) and increased radioresistance (IRR). HRS may be the constitutive response to low-dose radiation exposures of all normal and malignant cell systems (both in vivo and in vitro) since it is found in ~80% of cell lines we have investigated. Evidence suggests that IRR reflects an induced 'protective' repair response triggered by accumulated DNA damage, as evidenced by our dose-rate experiments.

We are investigating the underlying mechanism of HRS/IRR. In a panel of 10 cell lines of differing HRS/IRR response, we have established that DNA-PK activity, and not the amount of DNA-PK present, may dictate the IRR response. This observation is supported by work using the MO59 family of cell lines that express disparate DNA-PK status. MO59J cells, that lack DNA-PK, did not show an IRR response. In contrast, MO59K and MO59J/FUS1 cells that contain DNA-PK both exhibited distinct IRR responses. The HRS response was indistinguishable in the three MO59 cell lines.

The specific poly (ADP-ribosyl) transferase (PARP) inhibitor NU1025 prevented the development of IRR. In contrast, NU1025 did not affect the survival response in U373 cells that lack an HRS/IRR response. These data confirm our earlier observations with the less specific PARP inhibitor 3-aminobenzamide. It is likely therefore that DNA damage detection via a PARP-mediated process is involved in the initiation of the IRR response. To test this hypothesis, we have recently generated a functional PARP specific ribozyme.

The involvement of DNA strand breaks in HRS/IRR has recently been confirmed with our preliminary observations that HRS/IRR can be detected using the micronuclei assay. Of the cell lines we have investigated to date, a correspondence exists between the presence of HRS/IRR scored by clonogenic survival or the micronuclei assay. Our in-house developed high-resolution comet assay is being used to measure DNA strand breaks in the dose region characterising HRS/IRR. This has required modifications and improvements to both cell lysis protocols and comet scoring algorithms. The measurement of DNA damage after 0-2 Gy doses is currently in progress.

While the precise mechanism underlying HRS/IRR has yet to be fully determined the balance of evidence is now indicating that DNA repair activity involving PARP signalling and DNA-PK transduction is critical.