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The Oncogenic Transforming Potential of the Passage of Single Particles

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The Oncogenic Transforming Potential of the Passage of Single Particles Proc. Natl. Acad. Sci. USA Vol. 96, pp. 19–22, January 1999 Applied Biological Sciences The oncogenic transforming potential of the passage of single a particles through mammalian cell nuclei RICHARD C. MILLER,GERHARD RANDERS-PEHRSON,CHARLES R. GEARD,ERIC J. HALL, AND DAVID J. BRENNER* Center for Radiological Research, Columbia University, 630 West 168th Street, New York, NY 10032 Communicated by Richard B. Setlow, Brookhaven National Laboratory, Upton, NY, November 3, 1998 (received for review June 2, 1998) ABSTRACT Domestic, low-level exposure to radon gas is cell at risk will be traversed by more than one a particle in a considered a major environmental lung-cancer hazard involv- lifetime (1). ing DNA damage to bronchial cells by a particles from radon Even in the laboratory, there has until now been no direct progeny. At domestic exposure levels, the relevant bronchial way of measuring the oncogenic transforming effects of exactly cells are very rarely traversed by more than one a particle, one a particle without the confounding effects of a significant whereas at higher radon levels—at which epidemiological fraction of exposed cells being subject to multiple a-particle studies in uranium miners allow lung-cancer risks to be traversals, and this has led to significant uncertainty in low- quantified with reasonable precision—these bronchial cells dose radon risk estimates (2). are frequently exposed to multiple a-particle traversals. Mea- In recent years, several groups have developed charged- suring the oncogenic transforming effects of exactly one a particle microbeams, in which cells on a dish are individually particle without the confounding effects of multiple traversals irradiated by a predefined exact number of a particles, thus has hitherto been unfeasible, resulting in uncertainty in allowing the effects of exactly one (or more) a particle extrapolations of risk from high to domestic radon levels. A traversals to be assessed (3–8). However, earlier microbeam technique to assess the effects of single a particles uses a irradiation systems have been too slow to measure oncogenic charged-particle microbeam, which irradiates individual cells transformation frequencies, because the low probabilities in- ' 5 or cell nuclei with predefined exact numbers of particles. volved require that many cells ( 10 ) be individually irradi- Although previously too slow to assess the relevant small ated. Specifically, the current overall irradiation throughput ' oncogenic risks, recent improvements in throughput now for the microbeam experiments described here is 3,000 cells permit microbeam irradiation of large cell numbers, allowing per hr, which may be compared with earlier microbeam system ' the first oncogenic risk measurements for the traversal of throughputs of 120 cells per hr (6). In practice, the earlier low ' 5 exactly one a particle through a cell nucleus. Given positive throughput precluded the irradiation of the 10 cells neces- controls to ensure that the dosimetry and biological controls sary for measurements of oncogenic transformation frequen- were comparable, the measured oncogenicity from exactly one cies. This increased microbeam throughput, made possible by a particle was significantly lower than for a Poisson- developments in both hardware and software, now permits a sufficient numbers of cells to be irradiated, and we report here distributed mean of one particle, implying that cells tra- a versed by multiple a particles contribute most of the risk. If the direct measurement of the oncogenic risk of exactly one this result applies generally, extrapolation from high-level particle. a The goal of this study was to investigate the oncogenic radon risks (involving cellular traversal by multiple parti- a cles) may overestimate low-level (involving only single a effects produced by exactly one particle traversing cell nuclei. particles) radon risks. Specifically, we have investigated whether the oncogenic ef- fects of exactly one a particle are similar to the effects of a (Poisson) mean of one a particle, with the latter’s attendant Domestic exposure to radon gas in homes generally is consid- proportion of cells traversed by more than one a particle. ered to be the single largest naturally occurring environmental Because it is much less likely that there would be a difference hazard (1). The basic mechanism involves DNA damage to a between the effects of, say, exactly four and a Poisson-mean of bronchioepithelial cells by particles emitted by radon prog- four a particles, we have made such comparisons to act as eny. The most recent report (1) from the U.S. National positive controls. Equality in these positive controls for mul- Academy of Sciences on the health effects of environmental tiple a-particle traversals would imply that any differences seen exposure to radon gas (BEIR VI) estimated that 10–14% of all between the effects of exactly one a particle and a Poisson- lung cancer deaths—amounting to central estimates of about mean of one a particle are not artifacts of any differences in 15,400–21,800 per year in the United States—are linked to irradiation conditions between the microbeam and the broad- radon gas exposure from the environment. beam systems—although we have striven to make the irradi- The BEIR VI (1) estimates (and others) of the risks of ation conditions as similar as possible. domestic radon exposure were made by extrapolating risks The layout and irradiation procedure of the Columbia from underground miners who received radon exposures that University microbeam have been described in detail elsewhere were, on average, many times larger than those of people in (3, 8). Briefly, each cell attached in a monolayer to the thin most homes. The problem inherent in this extrapolation is that, polypropylene base of a cell culture dish is identified and at these high exposures, the cells at risk in the bronchial located by using an image analysis system, and its coordinates epithelium of miners may be traversed by several a particles are stored in a computer; the cell dish is then moved under during a short period, whereas for individuals exposed in computer control such that the centroid of each cell nucleus in homes at normal domestic radon levels, it is unlikely that any the dish is in turn positioned over a highly collimated shuttered beam of a particles. The nucleus of each cell is exposed to a a The publication costs of this article were defrayed in part by page charge predetermined exact number of particles having an energy payment. This article must therefore be hereby marked ‘‘advertisement’’ in that simulates the emission from radon progeny, and a particle accordance with 18 U.S.C. §1734 solely to indicate this fact. © 1999 by The National Academy of Sciences 0027-8424y99y9619-4$2.00y0 *To whom reprint requests should be addressed. e-mail: djb3@columbia. PNAS is available online at www.pnas.org. edu. 19 Downloaded by guest on September 26, 2021 20 Applied Biological Sciences: Miller et al. Proc. Natl. Acad. Sci. USA 96 (1999) detector above the cell signals to close the accelerator shutter when the desired number of particles (e.g., 1) are recorded, after which the next cell is moved under the beam. In parallel with these microbeam studies, we have conducted ‘‘broad beam’’ a-particle exposures by using different fluences of a particles such that cell nuclei were traversed by mean numbers of 0, 1, 2, 4, 6, and 8 particles. In this case, Poisson statistics determine the probability that any given cell nucleus is traversed by a given number of a particles. For example, if the fluence is chosen such that the mean number of particles traversing nuclei is 1, then 37% are not traversed at all, 37% are traversed once, and the remaining 26% are traversed by 2 or more a particles. Groups of cell nuclei traversed by a given exact number of a particles, and by the same (Poisson- a 1 distributed) mean number of particles can be considered to FIG. 2. Detail of C3H10T ⁄2 cells attached to the polypropylene have received the same average dose. surface of the mini-well, as detected by the automated microbeam 1 C3H10T ⁄2 cells were used in this study, which can be quanti- image analysis system. The cells were stained with a low concentrations tatively assayed for in vitro oncogenic transformation (9). of Hoechst 33342 fluorescent dye as described in the text, which is Transformed cells can be identified by their altered morphol- preferentially taken up by the cell nucleus. The cell dish is moved ogy, and extensive prior studies have shown that such trans- under computer control such that the centroid of every cell nucleus as determined by the image analysis system (marked by the image analysis formed cells produce tumors when injected into animals (10). system as crosses) is sequentially situated under the collimated mi- crobeam for irradiation with a predetermined number of a particles. METHODS AND MATERIALS For illustrative purposes, the cells shown here also were stained with orange fluorescent probe (CellTracker orange CMTMR, Molecular Microbeam Irradiations. A schematic of the microbeam Probes), which is preferentially taken up in the cytoplasm and is used system is shown in Fig. 1. a particles accelerated by a 4-MV when microbeam irradiation of only the cytoplasm is required. The bar 5 illustrates the overall spatial precision of the a particle microbeam of Van de Graaff accelerator to an energy of 5.3 MeV (1 eV 6 m 5 m 1.602 3 10219 J; stopping power 90 keVymm) were used for the 3.5 m. (Bar 7 m.) microbeam irradiations. As described below, the cells to be 1 ing C3H10T ⁄2 cells (11)—that the particle beam would miss irradiated were attached to the bottom of thin-bottomed the targeted nucleus at a rate of ,0.3%.
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