Published online before print July 12, 2002, 10.1148/radiol.2243011300
(Radiology 2002;224:817-822.)
© RSNA, 2002
Effects of Exposure of CHO-K1 Cells to a 10-T Static Magnetic Field1
Takehisa Nakahara, PhD,
Hiroko Yaguchi, PhD2,
Masami Yoshida, BSci and
Junji Miyakoshi, PhD
1 From the Department of Radiation Genetics, Graduate School of Medicine, Kyoto University, Yoshida-Konoe-cho, Sakyo-ku, Kyoto 606-8501, Japan. Received July 30, 2001; revision requested September 9; final revision received March 18, 2002; accepted March 26. Supported in part by a grant-in-aid from the Ministry of Education, Culture, Sports, Science and Technology, Japan, and by a grant-in-aid from the Research for the Future Program, Japanese Society for the Promotion of Science. Address correspondence to J.M. (e-mail: miyakosh@mfour.med.kyoto-u.ac.jp).
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ABSTRACT
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PURPOSE: To evaluate whether exposure to strong static magnetic fields (SMFs), of up to 10 T, affects the growth and cycle distribution of and the micronucleus formation in monolayered Chinese hamster ovary CHO-K1 cells.
MATERIALS AND METHODS: The authors developed a system to expose cultured cells to strong SMFs immediately after the cells are seeded. Cell growth rate was evaluated according to cell number count. Cell cycle distribution experiments were performed by using flow cytometric analysis. In these experiments, the cells were exposed to SMFs for up to 4 days. The frequency of micronucleus formation with only SMF exposure at x-ray irradiation was analyzed at microscopic observation.
RESULTS: Long-term exposure to a 10-T SMF for up to 4 days did not affect cell growth rate or cell cycle distribution. Exposure to SMFs alone did not affect micronucleus frequency. In x-ray–irradiated cells, exposure to a 1-T SMF did not affect micronucleus frequency, but exposure to a 10-T SMF resulted in a significant (P < .05) increase in micronucleus frequency.
CONCLUSION: Strong (10-T) SMFs have no effect on cell growth, cell cycle distribution, or micronucleus frequency, but they may cause an increase in the micronucleus formation induced by 4-Gy x rays.
© RSNA, 2002
Index terms: Experimental study • Magnetic resonance (MR), experimental studies, **.12143 • Magnetic resonance (MR), high-field-strength imaging, **.1214 • Magnetic resonance (MR), safety, **.1214
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INTRODUCTION
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Due to recent developments in electronic technologies, daily exposure to strong static magnetic fields (SMFs) is increasing. An example is the increasing use of magnetic resonance (MR) imaging for medical diagnoses. The intensity of SMFs used at MR imaging, in addition to the development of MR imaging systems, also is becoming higher (1). Such strong-SMF exposure systems have great potential to improve medical and research applications. However, this also means that SMF exposure levels will increase. The U.S. Food and Drug Administration and International Electrotechnical Commission have established guidelines for the safety of MR systems (2,3). Despite these guidelines, there are still important safety issues regarding exposure to strong SMFs. Several investigators (4–9) have reported that the effects of strong SMFs—of greater than 1 T—are too weak for measurement of a biological response. Therefore, more biological data are needed to evaluate the safety of human exposure to strong SMFs.
We have designed and manufactured a system for the long-term, high-field-strength exposure of cells to SMFs. With such a system, the mean temperature of the incubator can be varied from 20° to 37°C ± 0.2° (SD) and the cultured cells can be exposed to a 10-T SMF. Thus, the purpose of our study was to evaluate whether strong SMFs have an effect on mammalian cells.
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MATERIALS AND METHODS
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SMF Exposure System
Figure 1 shows a diagram and photographs of the SMF exposure system, which consists of a magnet with a built-in CO2 incubator (Fig 1c), a direct current power supply and cryocooler unit for the magnet, a sham exposure unit with a built-in CO2 incubator, and a condition control unit for both incubators. The electric power supply (model 622; Lake Shore Cryotronics, Westerville, Ohio) can be output by means of a direct current at ±30 V, ±125 A (current), and 1,000 W (maximum power). The condition control unit (Fig 1b) consists of a gas compressor and a thermocontroller. A gas mixture of 5% CO2 and 95% air is supplied to both incubators by the gas compressor for SMF and sham exposures. The thermocontroller supplies warm water to the incubators to maintain the temperature of the incubation space. A cryocooler unit is used for the magnet (model CSA-71A; Sumitomo Heavy Industries, Kobe, Japan). The sham exposure unit (Fig 1d) has a CO2 incubator that is similar to that of the SMF exposure unit, but the sham unit is covered by a high-nickel-content soft alloy (Permalloy C, JIS C 2531; Nakano Permalloy, Tokyo, Japan) for protection against SMFs from the magnet.
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Figure 1a. (a) Schematic diagram of the SMF exposure system, which consists of a magnetic field generator with a CO2 incubator, a direct current (DC) power supply, a gas compressor, a thermocontroller for the incubator, and a cooling unit for the magnets. Photographs of the (b) condition control unit, (c) magnet with a built-in CO2 incubator, and (d) sham exposure unit also are shown.
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Figure 1b. (a) Schematic diagram of the SMF exposure system, which consists of a magnetic field generator with a CO2 incubator, a direct current (DC) power supply, a gas compressor, a thermocontroller for the incubator, and a cooling unit for the magnets. Photographs of the (b) condition control unit, (c) magnet with a built-in CO2 incubator, and (d) sham exposure unit also are shown.
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Figure 1c. (a) Schematic diagram of the SMF exposure system, which consists of a magnetic field generator with a CO2 incubator, a direct current (DC) power supply, a gas compressor, a thermocontroller for the incubator, and a cooling unit for the magnets. Photographs of the (b) condition control unit, (c) magnet with a built-in CO2 incubator, and (d) sham exposure unit also are shown.
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Figure 1d. (a) Schematic diagram of the SMF exposure system, which consists of a magnetic field generator with a CO2 incubator, a direct current (DC) power supply, a gas compressor, a thermocontroller for the incubator, and a cooling unit for the magnets. Photographs of the (b) condition control unit, (c) magnet with a built-in CO2 incubator, and (d) sham exposure unit also are shown.
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We measured the very low magnetic fields by using a gauss meter (model 5060; F. W. Bell, Orlando, Fla). With the exception of the SMFs caused by geomagnetism, the SMFs in the sham-exposure space were lower than 5.0 µT. In Japan, the average geomagnetism level is about 50 µT.
Generator, Incubator, Magnetic Flux Density, and Magnetic Gradient
Figure 2 shows the CO2 incubator of the SMF exposure system and the rack for the culture plates (100 mm in diameter). The incubator is made of acrylic resin. The CO2 incubators are inserted into the bore of the magnet or the soft alloy pipe for sham exposure. The maximum magnetic flux density is 10 T, as indicated by the rack position of 0 (Fig 2). To maintain high humidity in the incubator, steam with 5% CO2, which is provided from a bubbling tank in the control unit, is supplied through small holes at the front end of the incubator. Warm water is supplied from a thermocontroller and flows into the water jacket that is attached to the outside of the incubator. The graphs in Figure 3 depict the distributions of magnetic flux density and magnetic field gradient in the magnet bore. The magnetic flux density was highest at the center of the magnet and decreased gradually with increasing distance from the center. The magnetic field gradient was strongest at the position of 17.5 cm from the magnet center and was zero at the center.
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Figure 2. The CO2 incubator of the SMF exposure system. The incubator is made of acrylic resin. The numbers (-3 to +5) are the places for the plates from position 0. Position 0 is the center of the magnet bore. The plus and minus symbols are used to distinguish these positions.
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Cell Growth at SMF Exposure
We chose Chinese hamster ovary CHO-K1 cells for the experiments because they grow faster than other cells of human origin and are suitable for observations of the micronucleus. CHO-K1 cells were cultured in a medium (HAM F-12; Nikken Bio Medical Laboratory, Kyoto, Japan) that was supplemented with 10% fetal bovine serum (Invitrogen, Carlsbad, Calif). The cells were exposed to SMFs for up to 4 days. When we used a horizontal superconducting magnet with high gradient fields, the surface of the water near the center of the magnet parted (10). To avoid this effect (Fig 4), we exposed the cultured cells to SMFs immediately after they were seeded for the cell growth and cell cycle distribution experiments. CHO-K1 cells that were exposed to 3-Gy x rays at a rate of 1.2 Gy/min and incubated in a conventional CO2 incubator for up to 4 days served as controls. After exposure to SMFs, the cells were treated with trypsin and counted by using a particle counter (Coulter Z1; Beckman Coulter, Fullerton, Calif).
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Figure 4. Influence of the parted water phenomenon on the SMF exposure system. Ten milliliters of melted 0.5% agarose was seeded onto culture plates (100 mm in diameter). The plates were then exposed to an SMF in the exposure system. The numbers (-3 to +5) are plate positions. sham represents incubation in the sham-exposure unit.
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Cell Cycle Distribution Assay
To estimate the effects of SMFs on the cycle distribution of CHO-K1 cells, one of the authors (T.N.) performed flow cytometric analysis, as has been described previously (11,12). Briefly, the cells were labeled with 20-µM bromodeoxyuridine (Nacalai Tesque, Kyoto, Japan) for 30 minutes. They were then harvested, fixed in 70% ethanol at 4°C for more than 20 hours, and incubated in the following solutions: 4 N hydrochloric acid with 0.5% polyethylene glycol mono-p isoocthyl ether (Triton X-100; Nacalai Tesque) for 30 minutes at room temperature, fluorescein isothiocyanate–conjugated anti-bromodeoxyuridine antibody (Becton Dickinson, Mountain View, Calif) for 1 hour at room temperature, and 5 µg/mL of propidium iodide in phosphate-buffered saline (pH 7.4) for 1 hour at room temperature. Subsequently, flow cytometric analysis was performed by using a cytometry system (FACSCalibur; Becton Dickinson). The fluorescence data were displayed as dot plots for estimation of the percentages of cell cycle phases G0, G1, S, and G2/M by using computer software (ModFit LT; Varity Software House, Topsham, Maine), and the difference in percentage of cell cycle phases was determined by means of visual affirmation. We did not evaluate the effect of SMFs on apoptosis.
Micronucleus Assay
CHO-K1 cells with an average doubling time of approximately 12 hours were used in the study. CHO-K1 cells were seeded at a density of 5 x 104 cells per plate (60 mm in diameter). After a 24-hour incubation, the cells were irradiated with 1-, 2-, and 4-Gy x rays at a rate of 1.2 Gy/min. The nonirradiated and irradiated cells were then either sham exposed or exposed to 1-and 10-T SMFs for 18 hours. After being treated with trypsin, the cells were harvested and centrifuged (Southern 3 Cytospin; Thermo Shandon, Pittsburgh, Pa) onto microscopic slides at 900 rpm for 5 minutes. The cells were fixed in absolute methanol for 20 minutes, stained with 1 µg/mL of 4'-6-diamidino-2-phenylindole (Nacalai Tesque), and observed at phase-contrast and fluorescence microscopy. We analyzed at least 1,000 cells per culture to determine the micronucleus frequency. Micronuclei were identified (by H.Y.) on the basis of the following criteria: The structures were clearly surrounded by a nuclear membrane, they had a diameter of less than one-third that of the main nucleus, they were not touching the nucleus, and they were located within the cytoplasm of the cells (13–15).
Statistical Analyses
Statistical analyses were performed by using analysis of variance for intergroup differences with computer software (StatView version 4.5-J for Macintosh; SAS Institute, Cary, NC). When a significant F value was observed (P < .05), the Fisher protected least significant difference test for multiple comparisons was used to compare the number of micronucleated cells in SMF-exposed samples with that in the sham-exposed control samples.
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RESULTS
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We investigated the influence of strong SMFs on cell growth. The graphs in Figure 5 depict the growth curves of CHO-K1 cells at all positions in the incubator. No significant difference in growth rate was observed at any position in the SMF exposure unit. The growth rate of the cells in the sham exposure unit and in the conventional CO2 incubator placed in a separate room was similar to that of the cells exposed to SMFs, whereas x-ray irradiation caused an inhibition of cell growth.
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Figure 5a. Graphs depict the growth curves of CHO-K1 cells exposed to (a) a 10-T SMF and (b) a sham system. Plate positions (-3 to +5) are described in Figure 2. control refers to incubation in the conventional CO2 incubator with no magnetic field exposure. x-ray refers to 3-Gy x-ray irradiation followed by incubation in the conventional CO2 incubator. The data points represent the mean values in three separate experiments. The error bars represent the standard errors of the means in duplicate studies.
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Figure 5b. Graphs depict the growth curves of CHO-K1 cells exposed to (a) a 10-T SMF and (b) a sham system. Plate positions (-3 to +5) are described in Figure 2. control refers to incubation in the conventional CO2 incubator with no magnetic field exposure. x-ray refers to 3-Gy x-ray irradiation followed by incubation in the conventional CO2 incubator. The data points represent the mean values in three separate experiments. The error bars represent the standard errors of the means in duplicate studies.
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The graph in Figure 6 depicts the cycle distributions of CHO-K1 cells at positions 0, +1, and +3 in the incubator for SMF exposure, in the incubator for sham exposure, and in the conventional CO2 incubator, all for up to 4 days. The cycle distribution of cells exposed to the SMF was similar to that of the sham-exposed cells and to that of the control cells in the conventional CO2 incubator.
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Figure 6. Graph depicts cell cycle distribution analyzed by using a flow cytometer. Plate positions 0, +1, and +3 are described in Figure 2. S represents sham exposure, and C represents incubation in the conventional CO2 incubator. Gray bars represent the G2/M cell growth phase; white bars, the S cell growth phase; and black bars, the G0/G1 cell growth phase. The data points represent the mean values in three separate experiments.
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When the micronucleus frequency in the CHO-K1 cells following sham exposure or 10-T SMF exposure for 18 hours was measured, no significant difference between these two conditions was observed (Fig 7). The micronucleus frequency in x-ray–irradiated cells increased in a dose-dependent manner. To investigate the effects of SMFs on x-ray–induced micronucleus formation, we irradiated the cells with x rays and then exposed them to the sham unit or to 1- and 10-T SMFs. The graph in Figure 7 depicts the results of duplicate studies of the cells that were exposed to SMFs, as compared with those of studies of the cells that were sham exposed, following x-ray irradiation. After x-ray irradiation with 1 and 2 Gy, the cells exposed to SMFs showed small increases in x-ray–induced micronucleus formation compared with the sham-exposed cells. However, there was no statistically significant difference in micronucleus frequency between the sham- and SMF-exposed cells. Exposure to a 10-T SMF also did not significantly affect the frequency of micronucleus formation induced by 1- and 2-Gy x rays. However, exposure to SMFs did cause a statistically significant increase in micronucleus frequency after 4-Gy x-ray irradiation (P < .05).
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Figure 7. Graph depicts induced micronucleus (MN) formation in CHO-K1 cells exposed to 1- and 10-T SMFs and to a sham system. Black bars indicate cells containing one micronucleus; gray bars, cells containing two micronuclei; and white bars, cells containing more than two micronuclei. Error bars indicate the standard errors of the means in duplicate studies. * indicates significant difference between the cells exposed to the sham system and those exposed to SMFs (P < .05, Fisher protected least significant difference test).
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DISCUSSION
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Long-term exposure to a 10-T SMF for up to 4 days did not affect the growth rate or cycle distribution of CHO-K1 cells. Previous reports have indicated that exposure to a 7-T SMF has no significant effect on the growth rate of P-388 and V-79 cells (16) and that repeated exposure to a 1.5-T SMF has no significant effect on the growth rate of cultured human fetal lung fibroblasts (17). These data suggest that exposure to strong SMFs—of up to 10 T at least—may not affect cell growth and will not induce cell death. On the other hand, effects of SMFs on mammalian cells have been observed in biochemical studies. These effects include induction of c-fos gene expression (18), changes in the intracellular concentration and membrane flux of Ca2+ (19–21), and inhibition of poly–adenosine 5'-diphosphate ribosylation of proteins (22).
We investigated whether strong SMFs affect the frequency of micronuclei that are induced either spontaneously or by x-irradiation in CHO-K1 cells. Our study results show that exposure to a 10-T SMF alone does not affect micronucleus frequency and that a 1-T SMF does not affect the frequency of micronucleus formation induced by x-ray irradiation. To our knowledge, there has been only one previous report of the effects of SMFs on micronuclei. Okonogi et al (23) reported that exposure to a 4.7-T SMF for 6 hours significantly decreased the frequency of mitomycin C–induced micronuclei in Chinese hamster lung intrauterine cells. In the present study, exposure to SMFs caused statistically significant increases in micronucleus frequency after 4-Gy doses of x-ray irradiation. Findings at comparison of the present experiments with those conducted by Okonogi et al (23) suggest that the differences may be due to differences in the field strengths, exposure times, and cell lines used in the two studies and to the different processes by which micronuclei were induced by chemicals and ionizing radiation.
It is generally assumed that the micronuclei found in interphase cells can arise from acentric chromosome or chromatid fragments or from whole chromosomes that lag behind at anaphase and are not incorporated into the daughter nuclei during division (24). However, Nusse et al (24) argued that although it has been assumed that radiation-induced micronuclei are produced mainly by single acentric fragments, in radiation-induced micronuclei there are not only single acentric fragments but also whole chromosomes. Therefore, radiation-induced micronuclei can result from both clastogenic effects and spindle-damaging effects. We observed that exposure to SMFs increased the micronucleus formation that was induced by 4-Gy x rays. These results suggest that strong SMFs may inhibit the repair of DNA damage or worsen the spindle apparatus damage induced by x rays. However, because an increased frequency of x-ray–induced micronuclei was not observed with low (1- and 2-Gy) doses of x-ray irradiation, we suggest that SMFs have only a weak effect on overcoming the cell defense systems against x-ray irradiation. Our study results indicate that strong (10-T) SMFs have no effect on cell growth, cell cycle distribution, or micronucleus frequency but can cause an increase in the frequency of micronucleus formation induced by 4-Gy x rays.
The chances of exposure to strong SMFs may increase in the future because of, for example, the use of MR imaging for medical diagnoses and the development of superconducting, magnetically levitating vehicles for public transportation. However, very few biological experimental data on the effects of SMFs at the cellular level have been reported, and the existing data are insufficient for the evaluation of human safety. Further studies are needed to evaluate the biological effects of SMFs.
Practical application: In this study, we examined the biological effects of strong SMFs at the cellular level. A strong SMF—for example, 10-T maximum field strength during a maximum exposure time of 4 days—had no effect under our experimental conditions. However, the current results suggest that x rays combined with a strong SMF may have an effect. To investigate this theory, more detailed experiments are required.
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ACKNOWLEDGMENTS
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The authors thank Gui-Rong Ding of the Department of Radiation Medicine, The Fourth Military Medical University, China, for helpful assistance during this study.
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FOOTNOTES
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2 Current address: Growth Factor Division, National Cancer Center Research Institute, Tokyo, Japan. 
3 **.Multiple body systems
Abbreviation: SMF = static magnetic field
Author contributions: Guarantor of integrity of entire study, J.M.; study concepts and design, J.M.; literature research, T.N.; experimental studies, T.N., M.Y., H.Y.; data acquisition and analysis/interpretation, T.N.; statistical analysis, H.Y.; manuscript preparation and definition of intellectual content, T.N.; manuscript editing, revision/review, and final version approval, J.M.
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ABSTRACT
INTRODUCTION
