Carcinogenesis vol.18 no.7 pp.1365–1370, 1997
Power frequency magnetic fields do not contribute to
transformation of JB6 cells
Jeffrey D.Saffer1,4, Guang Chen2, Nancy H.Colburn3 and
Sarah J.Thurston1
1Molecular
Biosciences Department and 2Engineering and Analytic Sciences
Department, Pacific Northwest National Laboratory, Richland, WA 99352
and 3Gene Regulation Section, Laboratory of Biochemical Physiology,
National Cancer Institute, Frederick, MD 21702–1201, USA
4To
whom correspondence should be addressed
The potential for power frequency magnetic fields to
enhance neoplastic transformation has been investigated
in vitro using promotion-sensitive mouse epidermal JB6
cells. In a soft agar assay, 60-Hz magnetic fields of 0.01,
0.1, 1.0, or 1.1 mT flux density did not induce anchorageindependent growth. In addition, these magnetic fields
did not enhance tumor promoter-induced transformation
showing no increase in the maximum number of transformed colonies and no shift in the dose–response curve.
Thus, these data do not support the notion that environmental exposures to magnetic fields contribute to transformation.
Introduction
The possibility of a link between 60-Hz magnetic fields and
cancer incidence has caused much scientific controversy, as
well as public concern. Since the epidemiological studies have
been often contradictory and for the most part inconclusive
(1–5), bioeffects have been sought in animal and cell culture
studies as a means for demonstrating biological plausibility
for the potential of magnetic fields to increase cancer risk.
Although these studies have suggested a wide range of effects
(for example, 6–11), the reported responses have been small
and difficult to repeat. Thus, none has provided a plausible
mechanism for a magnetic field role in carcinogenesis.
Because power frequency magnetic fields do not damage
DNA directly (12) and do not alter the ability of cells to repair
DNA damage (13,14), it is unlikely that they initiate tumor
formation through mutations. Therefore, if magnetic fields
contribute to tumorigenesis it is likely that they do so through
non-genotoxic mechanisms during what are operationally
defined as the promotion and progression phases. The potential
of magnetic fields to contribute to transformation directly can
be readily tested using the JB6 mouse epidermal cell model
system. The preneoplastic JB6 cells, comprised of variant
Balb/c mouse epidermal lines, are immortalized but are not
capable of anchorage-independent growth or forming tumors
in syngeneic or nude mice (15). Treatment of JB6 promotionsensitive (P1) cells with tumor promoters induces anchorageindependent growth and tumorigenic transformation (16).
Transformation of these cells does not require agents referred
to as complete carcinogens, i.e. those having both tumor
initiating and tumor promoting activity in vivo. Anchorage*Abbreviations: MEM, minimal essential medium; AC, alternating-current;
TPA, O-tetradecanoylphorbol-13-acetate.
© Oxford University Press
independent transformation of JB6 P1 cells is completely
dependent on exposure to agents known to have tumor promoting activity in vivo and has been used to detect promoting
activity of a number of classes of agents including phorbol
diesters, non-phorbol diterpenes, polypeptide hormones, oxidants, drugs and environmental agents such as cigarette smoke
(17). Although these studies make no presumptions about
activity in humans, with this broad responsiveness and sensitivity to tumor promoting agents, JB6 cells provide an ideal
in vitro system for assessing potential transformation by
magnetic fields.
Materials and methods
Cell culture and standardized cell handling
Mouse epidermal P1 JB6 cells (clone 41.5a) were grown at 37°C in Eagle’s
minimal essential medium (MEM*) supplemented with 5% fetal calf serum
and penicillin/streptomycin (100 U and 100 µg/ml, respectively). Cells from
the same expansion were used for all experiments. A fresh vial (P93) was
thawed for each experiment and used on day 3 (40–50 % confluence) without
passaging. Cells were maintained at all times in a low alternating-current
(AC) field (,3 µT) by defining the lowest field regions within the incubator
(Forma Model 3033) and in the laminar flow hood.
Transformation assay
The over-agar transformation assay was performed as described (18) except
that organ culture dishes (Falcon #3037) were used with proportional volumes
of soft agar and cells in media in the outer annulus (5.53103 cells) and central
well (1.253103 cells). These two regions of the organ culture dishes have
different induced electric currents in the presence of a vertical magnetic field,
providing an opportunity to discern potential electric field effects. For a 1mT magnetic field, the induced electric field (Ei) would be 0–1.8 mV/cm in
the inner well and 3.2–4.7 mV/cm in the outer annulus. Fetal bovine serum
(Gibco, Grand Island, NY, lot 11112205 or JRH Biosciences, Lenexa, KS, lot
4M2224) was at 8%. O-Tetradecanoylphorbol-13-acetate (TPA, Sigma, lot
92H0233) was added at concentrations of 0.03, 0.1, 0.3 and 1 ng/ml (5310–11–
1.6310–9 M) from a stock of 1 or 10 µg/ml. Within each experiment, each
TPA concentration was tested in triplicate or quadruplicate. Dishes were
placed and positioned randomly in one of two identical chambers. The
exposure conditions were unknown to the experimenter until after all analysis
was completed. The two exposure chambers were maintained under identical
conditions by a rapidly recirculating atmosphere; and to prevent drying of the
agar plates the edge of each dish was wrapped with Parafilm. Dishes were
removed from fields on Day 14, coded for blind analysis and colonies were
scored using an inverted microscope. Colonies were classified as ‘large’
(.60 µm in diameter) or ‘small’ (,60 µm) to differentiate between possible
growth rate differences as opposed to changes in transformation rate.
Magnetic field exposure
The magnetic field exposure system is a double-wound square 4-coil configuration generating a vertical 60-Hz magnetic field. This exposure system provides
several features of importance including control of non-field effects of
energized coils, exposure and control chambers with identical environments,
an ability to do blind exposures, and high field uniformity (variation within
culture area ,0.5%). Two identical chambers could share atmosphere from a
remote incubator and two identical coil sets could be assigned randomly for
exposure and sham-exposure. The 60-Hz fields at each culture dish location
were measured before and after exposure using a power frequency field meter
(Electrical Field Measuring Company, model 111). Field strengths used were
0.01, 0.1, 1.0, or 1.1 mT as indicated. For sham exposures, background fields
were ø0.1 µT. The static geomagnetic field measured with a gaussmeter
(Model 610, F. W. Bell, Inc., Orlando, FL) with a Hall effect probe (Bell
Model HTB1–0608) was 30.7 µT, angle of inclination 30° in one chamber
and 32.8 µT, angle of inclination 12° in the other. All exposures were carried
out in a blinded fashion. Other details of the exposure system have been
1365
J.D.Saffer et al.
described (19,20). Uniformity of temperature in the two chambers was
confirmed, and CO2 levels were measured periodically throughout the exposure period.
Statistical methods
The number of resulting colonies out of the total number of cells under
inspection, n, can be modeled as a Binomial random variable with parameters
n and p, where p represents the frequency of colony formation. In this study,
we are interested in the effects of magnetic field exposure on the formation
frequency, p, at each TPA dose. Based on the theory of generalized linear
models, these effects can be described using a logit model. The statistical
analysis addresses whether the magnetic field exposure has a significant
impact on p.
In addition to the magnetic field, there are two other factors that may affect
p, the specific chamber used and potential differences between experiments.
Under the current experiment setting, the chamber effect will not influence
comparisons because all combinations of magnetic field levels and TPA doses
were tested using both chambers, and, therefore, any potential bias of a
chamber would be eliminated in comparisons. The experiment effect, however,
was included in the model since transformation can be affected by factors
such as cell density during the cell expansion. The choice of serum could
also have a profound effect, thus separate analyses were conducted for
experiments using different sera.
Let Cijk denote the number of colonies observed out of n cells with certain
magnetic field and TPA dose combination. Then Cijk has a binomial (n,pijk)
distribution. The logit model for pijk is log(pijk/(1 – pijk)) 5 u 1 Expi 1 MFj
1 TPAk 1 MF*TPAjk, where u is an overall mean, Expi is the effect of ith
experiment, MFj is the effect of jth magnetic field level, TPAk is the effect of
kth TPA concentration level and MF*TPAjk is the interaction of jth magnetic
field and kth TPA concentration.
To identify the contribution of magnetic fields to the colony formation rate,
the effect of magnetic fields at each exposure level was compared with the
effect with sham exposure through the following hypothesis tests:
(a)
versus
Ho: MF1 5 MF2 5 MF3
Ha: Mfj ,. MFj’ for at least one j ,. j’
(b) Ho: Mfj 1 TPAk 1 MF*TPAjk 5 Mfj’ 1 TPAk 1 MF*TPAj’k for all j at each k
versus
Ha: at least one equality does not hold.
Test (a) compares the magnetic field effects over all TPA levels, while test
(b) compares the effects at each of the TPA levels. Insignificant results of
these tests would indicate the lack of impact of magnetic field exposure on
the colony formation rate.
The procedure GENMOD of the statistical software package SAS (Release
6.09, SAS Institute Inc., Gary, NC), was used to fit this logit model based on
the observed counts of colonies in the dishes. Considering that the triplicate
or quadruplicate dishes for each TPA concentration were prepared out of a
single stock of cells and were exposed to certain level of magnetic field in
the same chamber, these triplicate or quadruplicate dishes were not treated as
independent samples, but multiple observations, with respect to a magnetic
field–TPA combination. A scale factor was also included in the model-fitting
to adjust the over-dispersion of the model.
Results
Do magnetic fields contribute to transformation in JB6 cells?
To determine whether 60-Hz magnetic fields were capable of
transforming JB6 cells or augmenting their transformation by
a chemical tumor promoter, a dose–response paradigm was
used in a series of assays for anchorage-independent growth.
JB6 cells were grown for 14 days over soft agar in the presence
of 0, 0.03, 0.1, 0.3, or 1.0 ng/ml TPA. These TPA doses were
chosen based on preliminary dose ranging experiments (data
not shown) that defined a maximal transformation response
around 1.0 ng/ml. Six or eight dishes were set up for each
TPA concentration and randomly assigned to one of two
identical magnetic field exposure chambers (19,20). The two
chambers share a circulating atmosphere and maintain the cells
under identical conditions. A vertical magnetic field was
applied to either one of the chambers with the other remaining
below background (,0.1 µT). Transformation of JB6 cells by
chemical agents such as TPA and EGF require continuous
1366
exposure for at least 4 days (21); thus, the magnetic field
was applied over the entire 14-day soft-agar growth period.
Experimental series included both configurations of chambers
being used for exposure, as well as assays for which neither
chamber was activated (sham–sham), with the specific configuration and the magnetic field flux density unknown to the
experimenter. Since a vertical magnetic field induces an electric
current proportional to the radius of the dish, cells were grown
in organ culture dishes using both the inner well (radius 5 0–
0.9 cm) and the outer annulus (radius 5 1.6–2.4 cm) to assess
contribution of the induced electric current.
JB6 cells were grown over agar in the presence of a 60-Hz
magnetic field at 0.01 mT or at 1 mT, the latter flux density
representing the high end of what might be encountered
transiently in the home or workplace. These experiments used
a serum lot that had been shown in preliminary experiments
to allow a strong response to chemical promoters. After 14
days, the number of colonies, representing cells that became
transformed, were counted. The number that were large (.60
µm diameter) or small (,60 µm) were noted. As expected, in
the absence of TPA and at the 0.03 ng/ml dose few (~30%)
of the colonies were large. An increasing percentage of large
colonies was observed with increasing TPA dose: ~45% at 0.1
ng/ml, ~70% at 0.3 ng/ml, and reaching ~80% at the 1 ng/ml
dose. No significant differences in colony numbers were
observed between magnetic field-exposed and control cells at
any TPA concentration (Figure 1; Table I, serum A). Overall,
the results of the likelihood ratio test for the contribution of
each factor in the statistical model gave a P-value of 0.40 for
magnetic field exposure and 0.56 for the interaction between
magnetic field and TPA dose. Furthermore, the magnetic fields
had no significant effect on colony formation at each TPA
dose (hypothesis b) with P-values of 0.60, 0.52, 0.48, 0.35
and 0.85 at TPA concentrations of 0, 0.03, 0.1, 0.3 and 1.0
ng/ml, respectively.
The potential effect of a 1 mT field on transformation by
epidermal growth factor (EGF) was also examined. Again no
shift of the dose–response was observed in either the inner
well or the outer annulus of the organ culture dishes (Figure 2).
Does the serum affect magnetic field responsiveness?
Several in vitro transformation experiments have suggested a
dependence on specific serum lots. For the assays with JB6
cells in particular, the low background transformation rate may
suggest a low responsiveness of the cells in the serum used.
Thus, background and TPA-induced transformation rates were
assessed in 11 different lots of serum from four suppliers.
Higher background transformation rates (2- to 3-fold) were
observed for two of the tested sera and a high induction by
TPA although normal background transformation was observed
for another serum (data not shown). Each of these three sera
were then used in transformation assays with magnetic field
exposure (1 mT) using zero or 1 ng/ml of TPA. Two of these
showed no indication of a magnetic field effect in an initial
assay, whereas one showed a slight inhibition of TPA-induced
colony formation in the presence of the field (data not shown).
This serum was further tested in a more rigorous series of
three experiments (sham–sham, exposed–sham and sham–
exposed) using a complete dose range of TPA. No effect of
the magnetic field was found (data not shown).
The complete lack of a field effect in any of these experiments
was contrary to suggestions of a promoting effect of magnetic
fields on JB6 cells reported by West et al. (22,23). Thus, an
Power frequency magnetic fields
Fig. 1. Magnetic fields do not alter the dose–response of JB6 cells to TPA-induced transformation. The effect of magnetic fields on transformation by TPA
was assessed in JB6 cells grown over-agar in organ culture dishes, three or four for each data point. Colonies in the inner well and outer annulus were
counted. For each experiment, the colony counts in field-exposed dishes are shown in black and the sham-exposed in gray. The hatched lines are for the inner
wells and the solid lines are for the outer annulus. Since each dish represents a separate observation rather than an independent experiment, the error bars
represent the standard deviations associated with the experimental variation in cell plating and colony growth, and not the confidence interval for
transformation obtained from analysis of the results in full.
1367
J.D.Saffer et al.
Table I. Colony formation of JB6 cells in soft agar in the presence of
magnetic fields only (no TPA)
Cell chambera
Serum
Field
Experimentb
Right
A
sham
S–S
S–S
E–S
E–S
S–E
S–E
E–S
E–S
S–E
S–S
E–S
S–E
E–S
S–E
1
7
5
3
3
1
5
14
26
7
32
2
8
14
1 mT
Fig. 2. Magnetic fields do not alter the dose–response of JB6 cells to EGFinduced transformation. The effect of magnetic fields on transformation by
EGF was assessed in JB6 cells grown over-agar in organ culture dishes,
four for each data point. The data are presented as in Figure 1.
0.01 mT
B
additional series of experiments was carried out with the lot
of serum (JRH, lot 4M2224) used by West. In contrast to the
experiments described above using a 0.01 or 1.0 mT flux
density, experiments using this lot of serum were carried out
using flux densities of 0.1 or 1.1 mT as used previously by
West (22,23). As observed with other sera, magnetic field
exposure alone did not promote JB6 cells to a transformed
phenotype (Table I, serum B) nor did they affect the transformation response of JB6 cells to TPA (Figure 3). Specifically, with
this serum, the results of the likelihood ratio test for the
contribution of each factor in the statistical model gave a Pvalue of 0.59 for magnetic field exposure and 0.93 for the
interaction between magnetic field and TPA dose. For each
sham
1.1 mT
0.1 mT
6
6
6
6
6
6
6
6
6
6
6
6
6
6
Left
1
3
2
1
1
1
5
4
7
2
16
1
3
2
2
16
6
3
3
3
7
21
21
10
25
1
7
8
6
6
6
6
6
6
6
6
6
6
6
6
6
6
aMean
number of colonies (inner well plus outer annulus) per dish
(6.753103 cells) from triplicate or quadruplicate assays 6 SD. (Each dish is
a separate observation, but not an independent sample; hence, the standard
deviation here reflects the experimental variation in cell plating and colony
growth and not the confidence interval for transformation obtained from
analysis of the results in full.)
bS–S indicates both chambers had no field, E–S indicates the right chamber
was used for field exposure, and S–E indicates the left chamber was used
for field exposure.
Fig. 3. The inability of magnetic fields to contribute to JB6 transformation is independent of serum lot. JB6 cells were grown and TPA-induced
transformation were assessed using a lot of fetal bovine serum previously reported (22,23) to support magnetic field effects. The data are presented as in
Figure 1.
1368
1
4
1
1
2
1
2
8
5
3
9
1
4
2
Power frequency magnetic fields
TPA dose the magnetic field effect P-values were 0.54, 0.77,
0.97, 0.75 and 0.76 at concentrations of 0, 0.03, 0.1, 0.3 and
1.0 ng/ml, respectively.
The transformation assays described thus far were carried
out using the over-agar method (18), in contrast to the
soft agar assays used by West et al. (22,23). Although the
responsiveness of JB6 cells to induction of transformation by
TPA is similar in both assays (18), the ambient temperature
cell suspension is mixed with melted (42°C) 0.5% agar medium
in the soft-agar method, whereas in the over-agar method the
cells never receive a potential heat shock. Although a number
of in-agar assays in our lab also failed to indicate a magnetic
field effect, the potential heat shock could be a confounder.
Thus, an experiment was conducted in which the JB6 cells
were held at 42°C for 60 min. As before, there was no
difference in colony formation between magnetic field-exposed
and sham-exposed cells at any TPA concentration (0 to 1 ng/
ml) (data not shown).
a circulating atmosphere, and blind assignment of field conditions. The magnetic field conditions were confirmed at each
assay dish location for each experiment. Multiple dishes
were set up for each assay condition and several replicate
experiments were performed covering each field exposure
condition (exposed–sham, sham–exposed and sham–sham)
with the arrangement and flux density unknown to the experimenter. Importantly, a dose–response with TPA or EGF in each
experiment provided a positive control demonstrating the
responsiveness of the cells to tumor promoting agents. In
addition, heat shock of the cells, as might occur in some
assays, was ruled out as a potential confounder. This experimental design provides as much confidence as possible in the
negative data obtained for magnetic field effects.
The negative results obtained are specific for JB6 cells
under the specific conditions tested. However, the failure to
detect transformation activity by magnetic fields in this relatively sensitive cell culture system argues against those fields
contributing to cancer risk.
Discussion
Acknowledgements
The data presented indicate that in well-controlled experiments
power frequency magnetic fields do not induce transformation
of JB6 cells, nor do they influence tumor promoter-induced
transformation. In a number of assays at a 0.01 and 1.0 mT
flux density, the number of anchorage-independent colonies in
the presence or absence of the field were remarkably similar,
with the largest difference occurring in a sham–sham comparison. Similarly, there was no evidence in any experiment for
an increase in colony numbers or a shift in the dose-response
of JB6 cells concomitantly treated with TPA and the magnetic
field. Magnetic field exposure also had no effect on EGFinduced transformation. Furthermore, the lack of a magnetic
field effect was not due to the presence or absence of induced
electric currents, since each experiment allowed discernment
of a potential effect under both low and high induced currents.
Since several transformation assay systems are sensitive to
specific lots of serum used to supplement the medium, additional experiments were carried out with other batches of
serum in an attempt to find a lot that would make the JB6
cells the most sensitive for transformation by EMF. Although
three lots of serum were found to give higher background
transformation rates, and potentially more sensitivity to tumor
promoting agents, none resulted in the cells becoming responsive to magnetic fields. In addition, no magnetic field response
was evident using a serum lot previously reported (22,23) to
give a ‘significantly increased’ number of cells capable of
anchorage-independent growth.
It remains a question as to why the negative results reported
here differ from those of West et al. (22,23). Both sets of
experiments used the same subclone of JB6 cells (clone 41a)
at similar passage numbers, similar fields (vertical, 60 Hz, 0.1
or 1.1 mT, 14 d exposure), and in some cases the same serum
lot. Although the source of the discrepancy is difficult to
assign, in the work of West et al. the effect was variable (1.0to 10-fold), no positive control was used, separately regulated
incubators were used for control and exposed cells, and zero
field controls used unenergized coils rather than an active
antiparallel double-wound arrangement. In the work described
here, the assays were conducted in a magnetic field exposure
system that allowed true sham controls (coils active, but zero
field), identical conditions in the two culture chambers through
This work was supported by the National Institute of Environmental Health
Science grant R01-ES07122.
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Received on January 3, 1997; revised on April 9, 1997; accepted on April
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