ARTICLE IN PRESS

Progress in Biophysics and Molecular Biology 87 (2005) 213223

www.elsevier.com/locate/pbiomolbio

Effects of static magnetic elds at the cellular level

Junji Miyakoshi
Department of Radiological Technology, School of Health Sciences, Faculty of Medicine, Hirosaki University,
66-1 Hon-Cho, Hirosaki 036-8564, Japan
Available online 19 October 2004

Abstract
There have been few studies on the effects of static magnetic elds at the cellular level, compared to those
of extremely low frequency magnetic elds. Past studies have shown that a static magnetic eld alone does
not have a lethal effect on the basic properties of cell growth and survival under normal culture conditions,
regardless of the magnetic density. Most but not all studies have also suggested that a static magnetic eld
has no effect on changes in cell growth rate. It has also been shown that cell cycle distribution is not
inuenced by extremely strong static magnetic elds (up to a maximum of 10 T). A further area of interest is
whether static magnetic elds cause DNA damage, which can be evaluated by determination of the
frequency of micronucleus formation. The presence or absence of such micronuclei can conrm whether a
particular treatment damages cellular DNA. This method has been used to conrm that a static magnetic
eld alone has no such effect. However, the frequency of micronucleus formation increases signicantly
when certain treatments (e.g., X-irradiation) are given prior to exposure to a 10 T static magnetic eld. It
has also been reported that treatment with trace amounts of ferrous ions in the cell culture medium and
exposure to a static magnetic eld increases DNA damage, which is detected using the comet assay. In
addition, many studies have found a strong magnetic eld that can induce orientation phenomena in cell
culture.
r 2004 Elsevier Ltd. All rights reserved.

Tel.: +81 75 753 4412; fax: +81 192 332830.

E-mail address: miyakosh@cc.hirosaki-u.ac.jp (J. Miyakoshi).

0079-6107/$ - see front matter r 2004 Elsevier Ltd. All rights reserved.
doi:10.1016/j.pbiomolbio.2004.08.008

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1. Cell proliferation and cell cycle distribution

Wiskirchen et al. (1999) reported that no statistically signicant differences could be detected in
population doublings and cumulative population doublings between exposed and control cell
groups following exposure to a static magnetic eld of 1.5 T for a period of 3 weeks. Clonogenic
activity, DNA synthesis, cell cycle, and proliferation kinetics were not altered by exposure to the
magnetic eld and repetitive exposure to a static magnetic eld of 1.5 T exerted no effects on
proliferation of human fetal lung broblast (HFLF) cells.
Raylman et al. (1996) reported that a 64 h exposure to a 7 T magnetic eld produced a reduction
in viable cell numbers in melanoma, (HTB 63), ovarian carcinoma, (HTB 77 IP3) and lymphoma
(CCL 86) cell lines. Prolonged exposure to the 7 T eld appeared to inhibit growth of the three
human tumor cell lines in vitro. Alterations in cell growth cycle and gross fragmentation of DNA
were excluded as possible contributory factors. Buemi et al. (2001) examined the effects of a static
magnetic eld of 0.5 mT on the cell proliferation/cell death balance in renal cells (VERO) and
cortical astrocyte cultures from rats. After 2, 4 and 6 days of exposure to a magnetic eld, they
observed a gradual decrease in apoptosis and proliferation and a gradual increase in cells with a
necrotic morphology compared to the control group. These reports suggest that the effect of
exposure to static magnetic elds varies depending on the cell type.
Cell cycle analysis of synchronized and non-synchronized HFLFs cells did not reveal
statistically signicant differences between the cells exposed to 0.2, 1.0, or 1.5 T for 1 h/day for 5
consecutive days and control cells (Wiskirchen et al., 2000). The population doublings did not
indicate any growth modulation during exposure. Proliferation kinetics did not provide any hint
of modulating effects of repetitive magnetic eld exposure. HL60 and EA2 cells were exposed to
static magnetic elds of 1.5 and 7.05 T, for periods ranging from 1 to 24 h (Schiffer et al., 2003).
Cell cycle analysis did not reveal differences between the exposed and control cells.

2. Genotoxic effects
2.1. Mutation
Ikehata et al. (1999) examined possible mutagenic and co-mutagenic effects of strong static
magnetic elds using the bacterial mutagenicity test. No mutagenic effect of static magnetic elds
up to 5 T (1 T=10,000 G) was detected using four strains of Salmonella typhimurium (TA98,
TA100, TA1535 and TA1537) and Escherichia coli (E. coli) WP2 uvrA. The mutation rate in the
exposed group was signicantly higher than in the non-exposed group when cells were treated
with N-ethyl-N0 -nitro-N-nitrosoguanidine, N-methyl-N0 -nitro-N-nitrosoguanidine, ethylmethanesulfonate, 4-nitroquinoline-N-oxide, 2-amino-3-methyl-3H-imidazo[4,5-f]quinoline or 2-(2-furyl)3-(5-nitro-2-furyl) acrylamide.
An E. coli mutation assay was used to assess the mutagenic effects of strong static magnetic
elds (Zhang et al., 2003). Various mutant strains of E. coli were exposed up to 9 T for 24 h and
the frequencies of rifampicin-resistant mutations were then determined. The expression of the
soxS::lacZ fusion gene was assessed by measuring b-galactosidase activity. The results for survival
or mutation obtained with the wild-type E. coli strain GC4468 and its derivatives defective in

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DNA repair enzymes or redox-regulating enzymes showed no effect of exposure. On the other
hand, the mutation frequency was signicantly increased by exposure to a static magnetic eld of
9 T in soxR and sodAsodB mutants, which are defective in defense mechanisms against oxidative
stress.
2.2. Sister chromatid exchanges
The effects of static homogeneous magnetic elds of 0.5 and 1.0 T on cells from human blood
were investigated by examining their inuence on the frequency of gross lesions, sister chromatid
exchanges and on the proportion of amodal cells (Cooke and Morris, 1981). Neither treatment
had a signicant effect on any of the parameters measured.
2.3. Micronucleus formation
Long-term exposure to a 10-T static magnetic eld for up to 4 days did not affect cell growth
rate or cell cycle distribution in Chinese hamster ovary CHO-K1 cells (Nakahara et al., 2002).
Exposure to the static magnetic eld alone did not affect micronucleus formation. In X-rayirradiated cells, exposure to a 1-T static magnetic eld also did not affect micronucleus formation,
but exposure to a 10-T static magnetic eld resulted in a signicant (po0:05) increase in
micronucleus formation induced after a 4-Gy exposure.
The effects of a 4.7 T static eld on the frequency of micronucleated cells in CHL/IU cells
induced by mitomycin C (MMC) were studied in vitro (Okonogi et al., 1996). The cells were
simultaneously exposed to the static eld and MMC for 6 h, and then the cells were cultured in
normal condition for the micronucleus expression up to 66 h. Exposure to the static magnetic eld
for 6 h signicantly decreased the frequency of MMC-induced micronucleated cell expression after
culture periods of 18, 42, 54 and 66 h. These results suggested that a 4.7 T static magnetic eld
might have exerted an inuence on the DNA damage stage produced by MMC rather than on the
formation of micronuclei during the stage following MMC-induced DNA damage.
2.4. DNA damage
Lymphocyte exposure to a static magnetic eld of 7 mT did not affect the number of cells with
DNA damage in the comet assay (Zmyslony et al., 2000). Incubation of lymphocytes with FeCl2
(10 mg/ml) also did not produce detectable damage of DNA. However, when the FeCl2-incubated
lymphocytes were simultaneously exposed to a 7 mT static magnetic eld, the number of damaged
cells increased signicantly and reached to approximately 20%. Exposure of the cells to static
magnetic elds and simultaneous treatment with a known oxidant, ferrous chloride, may therefore
affect oxidative damage of DNA molecules (Zmyslony et al., 2000).
3. Ca2+ and ion transport
Exposure to a 120 mT static magnetic eld resulted in a slight reduction in the peak
calcium current amplitude and shift in the currentvoltage relationship in cultured GH3

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cells using the whole-cell patch clamp technique (Rosen, 1996). Absorbance measurements at 660 nm of calmodulin-dependent cyclic nucleotide phosphodiesterase activity
under cell free conditions indicated that 30-min exposure to a weak static magnetic eld
(20 mT) intensity altered this activity compared to zero magnetic eld exposure (Liboff et al.,
2003).
Human lymphocytes were simultaneously exposed to 4.75 T for static component and
0.7 mT for the pulsed component at 500 MHz generated by an NMR apparatus for 1 h. Exposure
to the static magnetic eld together with a pulsed electromagnetic eld increased the Ca2+ inux
without any proliferative, activating or proinammatory effect on either unstimulated or
phytohemagglutinin (PHA)-stimulated lymphocytes (Aldinucci et al., 2003a). On the other
hand, exposure of Jurkat cells decreased Ca2+ inux and proliferation signicantly. These
effects were consistent with the low levels of IL-2 measured in supernatants of the cells after
exposure. It was also reported that exposure of Jurkat cells signicantly decreased the
proliferation indexes, which were 0.770.29 and 0.8770.12 24 and 48 h after exposure,
respectively. Moreover, in Jurkat cells, the Ca2+ inux, which was higher than in human
peripheral blood mononuclear cells, was reduced signicantly by about 50% after exposure
(Aldinucci et al., 2003b).
Exposure to strong homogeneous magnetic elds with various magnetic ux densities of less
than 1.6 T had no signicant effect on either active or passive Rb+ inuxes into HeLa cells
(Miyamoto et al., 1996). Exposure to a magnetic eld of 2 T at different temperatures (1045 1C)
also did not cause any change in active or passive Rb+ inux, and no evidence was obtained for
the presence of a phase transition point of the cell membrane between 10 and 37 1C. The patchclamp method was used to measure transmembrane Na+ and K+ currents in SH-Sy5Y
neuroblastoma cells exposed to static magnetic elds of 0.1, 0.5, and 7.5 mT (Sonnier et al., 2003).
Application of the magnetic elds did not result in detectable changes in any of the action
potential parameters chosen for this study.
There was a slight shift in the currentvoltage relationship and a less than 5% reduction in peak
current during magnetic eld exposure to 125 mT in voltage-activated Na+ channels in
proliferating GH3 cells (Rosen, 2003). More pronounced was the increase in the activation time
constant, tm ; during and for at least 100 s following exposure to the eld. The temperature
dependence of this phenomenon was probably due to the greater ease with which the liquid crystal
membrane was deformed. The experimental threshold gradient and the calculated threshold eld
intensity for blockade of action potentials by these arrays were estimated to be approximately
0.02 mT/mm and 0.02 mT, respectively. These ndings suggested that spatial variation of the
magnetic eld was the principal cause of action potential blockade in dorsal root ganglia (DRG)
in vitro (Cavopol et al., 1995).

4. Metabolic activity
Onodera et al. (2003) reported that exposure to a magnetic eld of 10 T reduced the viability of
PHA-activated T cells in both the CD4(+) and CD8(+) subclasses. The susceptibility of
lymphocytes to magnetic eld exposure differed among activated T-cell subtypes. The
magnetic eld exposure signicantly increased the death of PHA-stimulated lymphocytes by

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apoptosis. These results suggested that a 10 T magnetic eld had acute effects on immune cells
during cell division, while the eld exposure had a minimal effect on immune cells in non-dividing
phases.
Sabo et al. (2002) reported that the metabolic activity was reduced in human leukemic cell line
HL-60 exposed to a 1 T static magnetic eld for 72 h. The inhibitory effect was also observed in
the presence of the mixture of the antineoplastic drugs, 5-uorouracil, cisplatin, doxorubicin and
vincristine.
The rate of cell proliferation of human gingival broblasts, histogram of the nuclear DNA
content, rates of lactate production and glucose consumption and the ATP content were
determined and cell morphology was investigated by both light- and electron-microscopy in a
static 0.2 T magnetic eld for 6 or 8 months (Yamaguchi et al., 1993). The results showed no
signicant differences between exposed and control cells.

5. Morphology
Pacini et al. (1999) examined morphological changes caused by exposure to a 0.2 T magnetic
resonance tomograph on a normal human neuronal cell culture (FNC-B4). The results showed
dramatic changes in morphology: vortexes of cells were formed and exposed branched neurites
featuring synaptic buttons. Control (sham-exposed) or non-neuronal cells (mouse leukemia, and
human breast carcinoma cells) did not show any alteration following exposure. Endothelin-1
release from FNC-B4 cells was also dramatically reduced after 5 min exposure. They also reported
that human skin broblast cell morphology was modied with a concomitant decrease in the
expression of some sugar residues of glycoconjugates after 1 h exposure to a 0.2 T static magnetic
eld (Pacini et al., 2003). However, cell viability, assessed by the colony-forming assay, was
unaffected.
HeLa cells grew at a normal rate for 96 h in the magnetic eld of 1.5 T and showed no
signicant change in shape that could be detected by scanning electron microscopy (Sato et al.,
1992). The growth of HeLa cells was not inuenced by exposure to the magnetic eld. Similarly,
exposure for 48 h to the magnetic eld had no effect on growth of normal human gingival
broblasts (Gin-1).
Gradient magnetic elds of 6 T with 60 T/m affected the convection of oating cell aggregations
in the cell culture ask, and reversibly changed the direction of convectional ow (Iwasaka et al.,
2003a). HeLa cells exhibited stream-like cell distribution patterns in the direction of the applied
magnetic eld gradient.
Dubey et al. (1999) developed an in vitro assay to study neurite elongation of DRG explants
placed onto one end of magnetically aligned collagen gel rods. The extent of neurite elongation
from chick embryo DRG neurons into the rods was found to be substantially greater than that
observed in controls and increased with magnetic eld strength, as did the collagen gel rod
birefringence, indicative of collagen bril alignment along the rod axis. These results may
translate into an improved method of entubulation repair of transected peripheral nerves by
directing and stimulating axonal growth through a tube lled with magnetically aligned collagen
gel.

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6. Gene expression
Miyakoshi and co-workers used a static magnetic eld exposure system, to expose cells to a
spatially inhomogeneous 6 T with a strong magnetic eld gradient (41.7 T/m) or to a spatially
homogeneous 10 T (Hirose et al., 2003a). HL-60 cells exposed to either a 6 or 10 T static magnetic
eld for periods of 148 h did not exhibit signicant differences in the levels of c-Myc and c-Fos
protein expression, as compared to sham-exposed cells. In contrast, c-Jun protein expression
increased in HL-60 cells after exposure to the 6 T static magnetic eld for 24, 36, 48, and 72 h.
Exposure to a strong magnetic eld gradient induced c-Jun expression, which suggested that
strong magnetic eld gradients may have signicant biological effects, particularly regarding
processes related to an elevation of c-jun gene expression.
Hirai et al. (2002) reported that brief exposure (15 min) to a static magnetic eld of 100 mT led
to a marked but transient potentiation of binding of a radiolabeled probe for activator protein-1
(AP-1) in immature cultured rat hippocampal neurons with high expression of growth-associated
protein-43. Exposure to the static magnetic eld increased AP-1 DNA binding through expression
of Fra-2, c-Jun and Jun-D proteins in immature cultured hippocampal neurons.
Hiraoka et al. (1992) reported that c-fos mRNA in the HeLaS3 cells was undetectable in
untreated cells, but the expression was induced in cells by the magnetic eld exposure of
0.180.2 T for 224 h. Expression of mRNA changed as a function of time with a peak at a 6 h
exposure. c-fos was expressed following heat treatment at 45 1C for 10 and 15 min, and its
expression was further enhanced by treating the cells with heat followed by 4 h of exposure to the
magnetic eld.
Human peripheral blood mononuclear cells were exposed to a 0.5 T eld generated by a
superconducting MRI unit for 24 h. The exposed and sham-exposed cells were maintained at the
same temperature of 2470.2 1C. The 0.5 T eld produced a reduced expression of CD69 from
human peripheral blood mononuclear cells in vitro, which was enhanced after PHA stimulation
(Salerno et al., 1999). An increased release of IFN-g and IL-4 was also found, which was reduced
after PHA stimulation. The release of TNF-a, IL-6 and IL-10 was not modied.

7. Apoptosis
HL-60 cells were exposed to a static magnetic eld of 6 mT with or without DNA
topoisomerase I inhibitor, camptothecin for 5 h. The static magnetic eld alone did not produce
any apoptogenic or necrogenic effect in HL-60 cells (Teodori et al., 2002). Static magnetic elds
alone or in combination with camptothecin did not affect overall cell viability, but they
accelerated the rate of cell transition from apoptosis to secondary necrosis after induction of
apoptosis by camptothecin.
Simultaneous exposure of rat lymphocytes to a 7 mT static magnetic eld and ferrous chloride
(FeCl2) caused an increase in the number of cells with DNA damage (Jajte et al., 2002). The
damage of DNA molecules by simultaneous exposure to a 7 mT static magnetic eld and iron ions
may lead to cell death by apoptosis or necrosis. No signicant differences were observed between
unexposed lymphocytes and lymphocytes exposed to a 7 mT static magnetic eld. A 3-h
incubation with FeCl2 (10 mg/ml) did not affect cell viability. However, when lymphocytes were

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exposed to a 7 mT static magnetic eld and simultaneously treated with FeCl2, there was a
signicant increase in the percentage of apoptotic and necrotic cells accompanied by signicant
alterations in cell viability.
Flipo et al. (1998) observed that exposure to a static magnetic eld of 0.0250.15 T increased
intracellular Ca2+ levels and decreased mitogenic responses in C57BL/6 murine macrophages,
splenic lymphocytes or thymic cells. Exposure to the static magnetic eld produced markedly
increased apoptosis of thymic cells, as determined by ow cytometry.
Static magnetic elds above 600 mT were found to decrease the extent of cell death by apoptosis
induced by several agents in different human cell systems of U937 and CEM cells in an intensitydependent fashion, reaching a plateau at 6 mT (Fanelli et al., 1999). The protective effect was
found to be mediated by the ability of the elds to enhance Ca2+ inux from the extracellular
medium; accordingly, it was limited to those cell systems where Ca2+ inux was shown to have an
antiapoptotic effect.

8. Orientation
Murayama (1965) rst reported that the sickled erythrocytes were oriented perpendicular to the
magnetic eld at 0.35 T. Higashi et al. (1993) assessed the inuence of a uniform static magnetic
eld (8 T maximum) on normal erythrocytes. The erythrocytes were oriented with their disk
planes parallel to the magnetic eld direction. This effect on erythrocytes was detectable at 1 T
and almost 100% of the cells were oriented when exposed to 4 T. They also reported that the
intact erythrocytes were oriented with their disk planes parallel to the magnetic eld because of
the diamagnetism of the cell membrane components, particularly the transmembrane proteins
(e.g., Band III, glycopholin) and the lipid bilayer (Higashi et al., 1995). In addition, Higashi et al.
(1996) observed that the paramagnetism of membrane-bound hemoglobin was thought to
contribute signicantly to this orientation. The observation of magnetic orientation was directed
toward understanding the fundamental microstructural aspects of the erythrocyte.
Bull sperm and paramecium cilium were exposed to uniform static magnetic elds to determine
effects on their orientations and measure their anisotropic diamagnetic susceptibility (Dw) (Emura
et al., 2003). The whole bull sperm and the bull sperm heads became oriented perpendicular to the
magnetic elds (1.7 T maximum), while the paramecium cilia became parallel to the magnetic
elds (8 T maximum).
It has been reported that exposure to strong static magnetic elds on the order of 1 T can result
in the orientation of macromolecules such as collagen (Torbet and Ronziere, 1984) and of animal
cells in vitro. Human foreskin rboblasts were also oriented using the magnetic orientation of
collagen with static magnetic elds of 4.0 and 4.7 T (Guido and Tranquillo, 1993). Furthermore,
osteoblast cells have been shown to be oriented under exposure to a strong static magnetic eld of
8 T in the absence of collagen (Kotani et al., 2000).
Guido and Tranquillo (1993) showed that the degree of bril orientation, and consequently the
elicited contact guidance, could be controlled by independently varying the magnetic eld strength
or temperature during brillogenesis. They presented the rst quantitative correlation of contact
guidance (based on cell orientation) with collagen bril orientation (based on birefringence) for

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human foreskin broblasts cultured in a collagen gel, by using gels of varying orientation resulting
from different magnetic eld strengths and temperatures during brillogenesis.
Hirose et al. (2003b) reported that human glioblastoma A172 cells embedded in collagen gels
were oriented perpendicular to the direction of the static magnetic eld at 10 T. A172 cells
cultured in the absence of collagen did not exhibit any specic orientation pattern after 7 days of
exposure to the static magnetic eld. Eguchi et al. (2003) observed that after 60 h of magnetic eld
exposure, cultured Schwann cells from dissected sciatic nerves of neonatal rats were
oriented parallel to the magnetic eld at 8 T. In contrast, Schwann cells, suspended in a medium
with collagen, oriented in the direction perpendicular to the magnetic eld after 2 h of magnetic
eld exposure. In this case, Schwann cells aligned along the collagen ber oriented by magnetic
elds.
The morphological effects of strong static magnetic elds on adherent cells are less well
understood than the effects of magnetic elds on red blood cells. Iwasaka et al. (2003b)
reported that a high-intensity magnetic eld of 14 T affected the morphology of smooth
muscle cell assemblies and that the cell colonies were extended along the direction of the magnetic
ux. The speculated mechanism was that a diamagnetic torque force acts on cytoskeleton
bers, which are dynamically polymerizing and depolymerizing during cell division and cell
migration. They also detected the intracellular macromolecule behavior under 14 T eld by
linearly polarized light (Iwasaka and Ueno, 2003). The change in polarized light intensity
through the lamellar cell assembly under magnetic elds corresponds to behavioral changes
in cell components. They speculated that intracellular macromolecules rotated and showed
a displacement due to diamagnetic torque forces during 23 h of magnetic eld exposure
at 14 T.

9. Conclusions
There have been few studies on the effects of static magnetic elds at the cellular level,
compared to those of extremely low frequency electromagnetic elds; therefore, a clear evaluation
cannot yet be made. Articles cited here varied with respect to magnetic ux density of static
magnetic elds and exposure times (from minutes to months) and it is difcult to compare them
directly. Considering these articles comprehensively, the conclusions are as follows: exposure to
static magnetic elds alone has no or extremely small effects on cell growth and genetic toxicity
regardless of the magnetic density. However, in combination with other external factors such as
ionizing radiation and some chemicals, there is evidence to strongly suggest that a static magnetic
eld modies their effects. A static magnetic eld may have effects on intracellular ion control,
especially Ca2+. Regarding gene expression, although not a consistent view, static magnetic elds
and strong magnetic eld gradients have an effect on c-Jun expression. Effects of static magnetic
elds on apoptosis are a potentially interesting phenomenon but the data are denitive. Many
studies report orientation by high magnetic ux densities on cells and collagen bers, which have
been conrmed as effects of static magnetic elds. However, these effects often depended on a cell
type and were not found in various types of cells. MRI has gained widespread use for diagnosis
and its magnetic ux densities used are increasing. Studies of the effects of static magnetic elds at
the cellular level should therefore be continued.

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