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Electromagnetic Fields Act Similarly in Plants as in Animals: Probable Activation of Calcium Channels via Their Voltage Sensor

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It has been shown that low intensity microwave/lower frequency electromagnetic fields (EMFs) act in animals via activation of voltage-gated calcium channels (VGCCs) in the plasma membrane, producing excessive intracellular calcium [Ca²⁺]i, with excessive [Ca²⁺]i leading to both pathophysiological and also in some cases therapeutic effects. The pathophysiological effects are produced largely through excessive [Ca2+]i signaling including excessive nitric oxide (NO), superoxide, peroxynitrite, free radical formation and consequent oxidative stress. The activation of the VGCCs is thought to be produced via EMF impact on the VGCC voltage sensor, with the physical properties of that voltage sensor predicting that it is extraordinarily sensitive to these EMFs. It is shown here that the action of EMFs in terrestrial, multicellular (embryophyte) plants is probably similar to the action in animals in most but not all respects, with calcium channel activation in the plasma membrane leading to excessive [Ca²⁺]i, leading in turn to most if not all of the biological effects. A number of studies in plants are briefly reviewed which are consistent with and supportive of such a mechanism. Plant channels most plausibly to be involved, are the so-called two pore channels (TPCs), which have a voltage sensor similar to those found in the animal VGCCs.
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Electromagnetic Fields Act Similarly in Plants as in Animals:
Probable Activation of Calcium Channels via Their Voltage Sensor
Martin L. Pall*
Professor Emeritus of Biochemistry and Basic Medical Sciences, Washington State Universi-
ty, 638 NE 41st Ave., Portland, OR 97232-3312, USA
Abstract: It has been shown that low intensity microwave/lower frequency electromagnetic
fields (EMFs) act in animals via activation of voltage-gated calcium channels (VGCCs) in
the plasma membrane, producing excessive intracellular calcium [Ca2+]i, with excessive
[Ca2+]i leading to both pathophysiological and also in some cases therapeutic effects. The
pathophysiological effects are produced largely through excessive [Ca2+]i signaling includ-
ing excessive nitric oxide (NO), superoxide, peroxynitrite, free radical formation and conse-
quent oxidative stress. The activation of the VGCCs is thought to be produced via EMF impact on the VGCC
voltage sensor, with the physical properties of that voltage sensor predicting that it is extraordinarily sensitive
to these EMFs. It is shown here that the action of EMFs in terrestrial, multicellular (embryophyte) plants is
probably similar to the action in animals in most but not all respects, with calcium channel activation in the
plasma membrane leading to excessive [Ca2+]i, leading in turn to most if not all of the biological effects. A
number of studies in plants are briefly reviewed which are consistent with and supportive of such a mecha-
nism. Plant channels most plausibly to be involved, are the so-called two pore channels (TPCs), which have a
voltage sensor similar to those found in the animal VGCCs.
Keywords: Microwave frequency non-thermal effects, calcium signaling, ion channel evolution, EMFs as
an environmental stressor, free radicals including hydroxyl, carbonate and NO2 radicals.
Received: March 3 2016 Revised: March 3 2016 Accepted: March 16’ 2016
INTRODUCTION
Microwave and lower frequency EMFs have
been found in animals, to work via activation of
voltage-gated calcium channels (VGCCs) [1-4].
Various EMF effects were found to be blocked or
greatly lowered by calcium channel blockers [1-3].
Five different calcium channel blockers have been
used in these studies, which differ from one anoth-
er in their structures and sites of action, but are all
thought to have high specificity as calcium chan-
nel blockers [1-3]. These and other data [1-4],
*Address correspondence to this author at the Professor Emeritus of
Biochemistry and Basic Medical Sciences, Washington State Uni-
versity, 638 NE 41st Ave., Portland, OR 97232-3312, USA; Tel:
503-232-3883; E-mail: martin_pall@wsu.edu
argue for the centrality of VGCC activation in
producing effects of EMFs in animal cells. VGCC
activation is thought to act primarily via increased
intracellular calcium [Ca2+]i, and a wide variety of
effects of EMFs in animals are thought to be pro-
duced as a consequence of increased [Ca2+]i in an-
imal cells [1-4] as diagrammed in Fig. 1. The ther-
apeutic effects of EMFs, such as stimulation of
bone growth, are thought to be produced by ele-
vated nitric oxide (NO) and NO signaling [1,5,6].
The pathophysiological effects of EMFs (Fig. 1)
are thought to be produced both via excessive
[Ca2+]i signaling (Fig. 1, center) and also via ex-
cessive NO, superoxide, peroxynitrite, free radi-
cals and oxidative stress (Fig. 1, lower right). It
will be argued below that pathophysiological EMF
Martin L. Pall
2 Current Chemical Biology, 2016, Vol. 10, No. 1 Martin L. Pall
effects in plants are probably produced as a conse-
quence of very similar mechanisms.
One of the puzzles of the action low intensity
microwave frequency EMFs has been how can
such very low intensities produce substantial bio-
logical effects? The current safety guide-
lines/standards are based on arguments that there
cannot be such effects and only heating effects
need be considered. However those arguments
have been contradicted by a literature made up of
thousands of primary literature citations showing
that there are many such non-thermal effects [4],
going all the way back to the 1950’s and 1960’s.
Nevertheless, it has been puzzling for many years
how such low intensity EMFs can produce biolog-
ical effects.
Pilla [7] showed that low intensity pulsed mi-
crowave EMFs can produce an almost instantane-
ous increase in Ca2+-calmodulin-dependent NO
production, all occurring in less than 5 seconds.
These observations strongly suggest that low in-
tensity EMFs act directly to activate the VGCCs,
because the almost instantaneous increases in both
[Ca2+]i and NO leave no time for indirect activa-
tion mechanisms. It is known that the VGCCs and
also other voltage gated ion channels are con-
trolled by a structure called the voltage sensor
[8,9], a structure that contains multiple charges
(thought to be 20 charges in the VGCCs [9]). Each
of these 20 charges are found on alpha helixes
within the lipid bilayer section of the plasma
membrane [8.9]. The voltage sensor opens the ion
channel due to the action of changes in the electri-
cal force across the plasma membrane acting di-
rectly on these 20 voltage sensor charges [8]. The
structure of the VGCC voltage sensor is discussed
in more detail in the Discussion section below. It
is plausible, therefore, that the electrical forces of
these low intensity EMFs act through their electri-
cal effects on the voltage sensor to activate the
VGCCs. It is predicted that the forces on the 20
charges in the VGCC voltage sensor are highly
amplified because of two important factors [2].
The law of physics called Coulomb’s law predicts
that forces on charged groups are inversely propor-
tional to the dielectric constant of the medium in
which the charges occcur. Because the dielectric
constant of the aqueous phases in the cell or extra-
cellular medium are about 120 times higher than
the dielectric constant of the lipid bilayer [2], this
predicts that forces on the each of the 20 charges
of the voltage sensor are about 120 times higher
than are electrical forces on singly charged groups
in the aqueous phases. In addition, Sheppard et al.
[10], predicted that the electrical forces produced
by EMFs across the plasma membrane are ampli-
fied about 3000-fold compared with the forces in
the aqueous phases because of the high electrical
resistance of the plasma membrane. It follows
from this, that the forces on the voltage sensor are
estimated to be vastly increased as compared with
Fig. (1). How Increased Intracellular Ca2+ Produces Both Pathophysiological and Therapeutic Responses in Animals
following EMF Exposure. [Ca2+]i, Intracellular calcium levels; NO, nitric oxide; cGMP = 3’,5’- guanosine mono-
phosphate; Protein kinase G = cGMP dependent protein kinase; Peroxynitrite (ONOO(-)); Oxidative Stress, an imbal-
ance between free radicals and other oxidants and antioxidants. Fi
g
ure taken with
p
ermission from Ref.
[
2
]
.
Electromagnetic Fields Act Similarly in Plants as in Animals Current Chemical Biology, 2016, Vol. 10, No. 1 3
forces on aqueous phase single charges, where
most if not all charged groups occur:
20(# of charges in voltage sensor) X 120 (from
the dielectric constant) X 3000 (amplification at
the plasma membrane) = 7.2 million
Because of this, the electrical forces placed on
the voltage sensor by these EMFs is calculated to
be approximately 7.2 million times higher than are
the forces placed on singly charged groups located
elsewhere in the cell because these singly charged
groups are predominantly in the aqueous phase
[2]. It is highly plausible, therefore, that this ex-
traordinary sensitivity of the voltage sensor to such
weak electrical effects is the final answer to this
long puzzle of how such low intensity EMFs can
produce biological effects in many animals, in-
cluding humans.
While there are much fewer data on low inten-
sity microwave EMF effects in plants, what data
we have show important similarities both in terms
of the probable target in plants and in terms of the
consequences of exposure in plants. It is those
similarities and the apparent role in plants of cal-
cium channels controlled by a voltage sensor that
are the main foci of this paper.
Low Intensity Microwave Frequency EMF Ef-
fects in Multicellular Embryophyte Plants
Perhaps the best place to start with plants, is by
considering the Beaubois et al. study of tomato
plants [11]. They [11] looked at the mechanism of
microwave EMF-induced stress responses, follow-
ing up on earlier studies showing increased tran-
scription of certain genes following EMF exposure
[11]. Beaubois et al. 11], demonstrated a central role
of increased [Ca2+]i in both direct effects of EMFs
on exposed tomato leaves and also in communica-
tion of stress signals from such exposed leaves to
other shielded parts of the plant. They studied in-
creased transcription of two genes (LebZIP1 and
Pin2), in response to 900 MHz EMF exposure,
where transcription of each of these genes had been
previously shown to increase in response to stressors
that increase [Ca2+]i. When the whole tomato plant
was exposed to 900 MHz radiation, transcript levels
in different leaves all increased at times of 0 to 60
minutes following 10 minute EMF exposure. When
only one leaf was exposed (other leaves being
shielded) the one unshielded leaf responded quickly
with the shielded leaves only responding after a 15
minute delay. When the unshielded leaf was sprayed
with the calcium chelator EGTA plus the calcium
channel blockers LaCl3, transcriptional changes
were blocked, clearly showing that calcium
transport through a calcium channel in the plasma
membrane is essential to both the response to the
EMF exposure in the unshielded leaf, but also to the
delayed response of the shielded leaves as well. The
communication to the shielded leaves was shown to
involve both abscisic acid (ABA) production and
also jasmonic acid (JA) production by the unshield-
ed leaf, communicating the stress to the other
leaves. This was shown both by studying mutant
plants unable to produce either ABA or JA and also
plants treated with naproxen, as specific inhibitor of
ABA production. The shielded leaves produced lit-
tle or no change in gene expression when either
ABA or JA production were prevented. Interesting-
ly, both ABA and JA are known to act, at least in
part, via elevated [Ca2+]i. As stated by Beaubois et
al. [11]The effects of decreasing endogenous cal-
cium levels by using EGTA as a chelating agent
along with LaCl3 as a calcium channel blocker, were
quite remarkable. Under calcium-depleted condi-
tions, no bZIP transcript accumulation occurred, in
either the shielded (distant) leaf or in the directly
exposed leaf. The lack of transcript accumulation in
the directly exposed leaf is very good evidence of an
important role for calcium in gene expression, both
in the local (treated) leaf and in the distant (untreat-
ed) one….” We will return later to the question of
what calcium channel is likely to be activated by
EMF exposure.
Roux et al. [12] showed that non-thermal 900
MHz exposures of tomato plants produced con-
sistent increases in expression of three stress relat-
ed genes at 15 minutes following a 10 minute ex-
posure. One of those transcripts, calmodulin-N6 is
a major [Ca2+]i receptor, causing them to suggest a
linkage to “variations in cytoplasmic Ca2+ con-
centrations.”
In a subsequent study, Roux et al. [13], showed
that a low intensity microwave EMF exposure
produced rapid (5 to 15 minutes following expo-
sure) increases in transcript levels of 3 genes, each
having roles in stress responses in plants. Each of
these transcript increases were prevented by
shielding the plant from the EMF and also by us-
ing either of two calcium chelators (BAPTA or
EGTA) or by the calcium channel blocker La3+.
The chelation and calcium channel blocker studies
4 Current Chemical Biology, 2016, Vol. 10, No. 1 Martin L. Pall
clearly show that Ca2+ influx through the plasma
membrane produces the transcript changes and ar-
gues, therefore, that EMF exposure is acting via
activation of a calcium channel in the plasma
membrane.
Ripoll et al. [14], reviewed evidence for special
roles of calcium in responses to several abiotic
stimuli in plants, including EMFs. They included
in their review, three earlier studies of the same
research group showing that non-thermal EMF
exposures acted via increased calcium influxes
[15-17]. They argued that calcium has a key role
in stimulus sensing, possible storage of infor-
mation and also final expression of effects in the
organism. They further state [14] that “there is
common agreement that plants react to such stimu-
li by an almost immediate elevation of the free
calcium in the cell cytosol.” Additionally “it was
inferred that this elevation of free cytosolic calci-
um (is) derived from the uptake of external calci-
um and/or release from internal Ca2+ stores.” It
should be noted that the above-discussed studies
[11,13,16] show that initial predominant effects of
EMFs are through activation of plasma membrane
calcium channels. Ripoll et al. [14] also note that
“these calcium changes show enormous variability
in their nature (transient, sustained or oscillatory),
amplitude, kinetics and spatial distribution.”
It can be seen from the previous three para-
graphs, that low intensity microwave EMFs act in
terrestrial embryophyte plants via activation of
calcium channels in the plasma membrane, pro-
ducing, in turn, large increases in [Ca2+]i. It has
also been shown, that plants respond to stressors
including elevated sucrose which produce partial
depolarization of the plasma membrane which ac-
tivate voltage regulated calcium channels [18],
again producing large increases in [Ca2+]i. Each of
these suggest similarities to mechanisms involved
in producing the EMF effects, to those found in
animal cells -- mechanisms centered on VGCC
activation.
Among the important studies cited by Ripoll et
al. [14] is the study of Kaplan et al. [19] showing
that in Arabidopsis, there are 230 calcium respon-
sive genes, with 162 being upregulated and 68 be-
ing downregulated by [Ca2+]i increases.
It will be argued in the Discussion section, that
the most plausible targets of EMFs in plants are
the so-called two pore channels (TPCs) [18], with
these channels having many similarities to but also
differences from the VGCCs in animals (see be-
low).
Other Studies Consistent with Calcium In-
creases Include the Following
Pazur and Rassadina [20] used a transgenic Ar-
abidopsis thaliana strain carrying the aequorin
gene, a gene producing the calcium-dependent bio-
luminescent protein aequorin to measure increased
[Ca2+]i in response to low level 50 Hz sinusoidal
EMF exposure. They found rapid increases in cy-
toplasmic [Ca2+]i levels following exposure onset.
Although these increases may have occurred al-
most instantaneously following exposure, they
were only readily apparent after about 2 minutes,
possibly because of efficient concentration of Ca2+
into the vacuole. This study shows that calcium
changes in plants are not limited to microwave
frequency exposures but also occur from extreme-
ly low (50Hz) exposures. This shows another simi-
larity to animals, where many studies have shown
that extremely low frequency field, including 50
Hz exposures, are blocked by calcium channel
blockers, demonstrating that 50 Hz EMFs in ani-
mal cells act via VGCC activation [1]. Pazur and
Rassadina suggest that [20] such exposures can
produce important Ca2+ regulatory (“second mes-
senger”) effects.
Shckorbatov et al. [21] showed that low intensi-
ty 36.6 GHz microwave exposure produced sub-
stantial increases in [Ca2+]i in pea root cells,
measured via calcium-dependent fluo-3 fluores-
cence, following exposure.
A number of plant studies showed that plants
respond to low intensity microwave EMF expo-
sures in similar ways to the responses in animals,
including both cellular DNA damage (genotoxici-
ty) where plants can often be studied more easily
than are animals and also oxidative stress (see
Gustavino et al. [22] for review). Studies have
shown that Vicia faba (fava bean) [22], Vigna ra-
diata (mung bean) [23] and Lemna minor (duck-
weed) [24,25], respond to low intensity exposures
to various microwave EMFs by producing oxida-
tive stress responses, similar to those found in an-
imals following EMF exposures [21], suggesting a
possibly similar mechanism. In animals oxidative
stress responses are thought to be produced by ex-
Electromagnetic Fields Act Similarly in Plants as in Animals Current Chemical Biology, 2016, Vol. 10, No. 1 5
cessive peroxynitrite and free radical formation
both produced as downstream consequences of
excessive [Ca2+]i [1,2,]; see Fig. 1.
In terms of DNA damage (genotoxicity), simi-
lar changes in plants including single and double
stranded DNA breaks and other DNA changes
have been widely found in animals [1,2,27-31],
and are also found in plants [32-36] where such
markers of DNA double strand breaks including
chromosomal breaks and micronucleus formation
can often be much more easily studied than in an-
imals. These chromosomal changes have been
found to occur following low intensity microwave
exposures in Vicia faba (fava beans) [32], in Trad-
escantia [33], in allium (that is onion) root tips
[34,35], in Zea mays (corn) [35] and in Lens culi-
naris (lentils) [36]. Similar changes in cellular
DNA, are thought to be produced in animals via
downstream effects of increased [Ca2+]i including
free radical formation [1,2,27-31] and may, there-
fore be produced by similar mechanisms in plants.
DISCUSSION
In animals, low intensity microwave/lower fre-
quency EMFs have been shown to act via activa-
tion of voltage-gated calcium channels (VGCCs).
This produces excessive [Ca2+]i and the down-
stream effects of such excessive [Ca2+]i are
thought to produce a variety of pathophysiological
effects (Fig. 1). While microwave frequency expo-
sures are of the most environmental concern be-
cause of their ever increasing exposure intensities
all over the world, low intensity, extremely low
frequency EMFs as well as other
EMFs/electrical/magnetic fields can also act via
VGCC activation [1]. While most of the plant
studies involve microwave EMFs, one study
showed that 50 Hz (extremely low frequency)
EMFs can act in plants via [Ca2+]i increases and
subsequent calcium effects [20]. As shown above,
plants resemble animals by having microwave and
extremely low frequency EMFs acting via exces-
sive [Ca2+]i and by having such excessive [Ca2+]i
produced by activation of calcium channels in the
plasma membrane. In animals, pathophysiological
effects of such EMF exposures often involve ex-
cessive calcium signaling (Fig. 1) and the same
thing is also true in plants. In animals, EMF expo-
sures produce oxidative stress and also single
strand and double stranded breaks in cellular DNA
(with the double stranded breaks often being moni-
tored via formation of micronuclei and occasional-
ly via chromosomal rearrangement; these DNA
strand breaks are thought to be produced in ani-
mals by free radicals produced as breakdown
products of peroxynitrite (Fig. 1) [2,27-30]. Plants
are similar to animals in that low intensity EMF
exposures also produce oxidative stress and mi-
cronuclei and chromosomal changes. It is argued
here that it is plausible that the mechanisms for
generating these in plants as downstream effects of
excessive [Ca2+]i may be similar if not identical to
the mechanisms involved animals (Fig. 1).
Another critically important observation with
regard to the animal studies, is that the activation
of the VGCC voltage sensor apparently finally ex-
plains how such low intensity EMFs can produce
biological effects [2-4]. The reason that this is so
important, is that it has long been argued by indus-
try supporters, that there cannot be a biophysical
mechanism by which low intensity EMFs can pro-
duce biological effects. They acknowledge that it
has long been known that microwave EMFs place
forces on charged groups and that microwave ov-
ens cook our food by joggling charged groups in
our foods back and forth, heating the food and
therefore cooking it. However they argue that low
intensity EMFs are too weak to produce biological
effects because they claim that the forces on such
charged groups produced by such low intensity
EMFs are too weak to produce biological changes.
It is important to note, therefore, that with 20
(there have been some questions whether the actu-
al charge number may be as low as 16 or as high
as 24 but I will stay with the 20 figure used earlier
[2,9]) positive charges being found in the voltage
sensor of the VGCCs and with these charges being
found in the lipid bilayer section of the plasma
membrane [8], the force of such low intensity
EMFs on the voltage sensor is about 7.2 million
times the force on individual charged groups found
elsewhere in the cell [2; see Introduction, above].
Because of this, the force on the voltage sensor is
about 7.2 million times stronger than expected
based on industry calculations and consequently
we finally have a plausible explanation of how
such weak EMFs can produce biological effects. It
must be pointed out here, that others have suggest-
ed other possible targets for low intensity EMFs.
However, with the VGCCs, we have direct, empir-
ical data from the calcium channel blocker studies
that these are the actual targets producing EMF
6 Current Chemical Biology, 2016, Vol. 10, No. 1 Martin L. Pall
effects, whereas with other proposed targets, there
is no such empirical evidence (an exception to this
may be the role of magnetite in migrating birds). It
seems clear, therefore that in animal cells, we not
only have strong empirical evidence that the
VGCCs are targets of EMFs, but we have a theo-
retical basis that provides strong support for why
these are the targets the extraordinary sensitivity
of the VGCC voltage sensor to such low intensity
EMFs. One of the questions that we will return to
later is why it seems to be the VGCCs that are in-
volved in producing the biological effects in ani-
mals, when there are similar voltage sensors in
voltage-gated sodium, potassium and chloride
channels but we see little evidence that activation
of those channels have any substantial roles in
producing biological responses to low intensity
EMFs? This predominance of Ca2+ ions over other
ions also is apparent in plants.
The evidence discussed above in plants pro-
vides a similar argument for a very similar mecha-
nism by which low intensity microwave frequency
EMFs produce biological effects in multicellular,
embryophyte terrestrial plants. There is, however,
a difference in the calcium channels in plants as
opposed to the VGCCs in animals and there is also
a type of confirming information that we have in
animals where there is no comparable information
for plants.
Monselise et al. [37] suggested using alanine
accumulation in plants as a measure of cell stress
in response to microwave frequency EMFs. How-
ever it is the author’s view that using transgenic
Arabidopsis or other plants containing the ae-
quorin gene can allow much easier monitoring of
[Ca2+]i which can be used a marker of EMF action
(see Pazur and Rassadina [20]). It is the author’s
view, that using plants rather than animals or ani-
mal cells in culture [2,4] as a measure of biologi-
cal activity of different EMF exposures has sub-
stantial merit, as suggested previously [37], given
the fact that plants tolerate well a much wider
range of temperature and also function well in air,
unlike animal cells in culture. However such plant
assays must be compared to those of animal cells
in culture to determine whether these responses are
sufficiently similar to each other for the plants to
serve well as a surrogate measure of biological ac-
tivity in animal cells. Currently, devices producing
microwave EMFs are never tested biologically for
safety, before they are put out and expose the un-
suspecting public, a major flaw in the whole regu-
latory system [4].
The apparent central role of the voltage sensor
in responding to low intensity, non-thermal EMFs
in animals, raises the question of how these volt-
age sensor-containing four domain channels
evolved, how they relate to each other and what
these things say about their mechanism of action.
There are a number of reviews that have consid-
ered the structure and evolution of voltage sensor
controlled channels [38,39]. Single domain poly-
peptides which presumably act as tetrameric struc-
tures, occur in bacteria, animals, plants and fungi
(including yeasts) [38,39]. This suggests that the
domain structure that is essential for both voltage
sensor activity and the opening of an ion channel
evolved very early in the evolution of life on earth.
The two domain and four domain genes and poly-
peptides, however, occur only in eukaryotic organ-
isms and are presumed to have evolved through
tandem duplication within a gene that originally
encoded only a one domain peptide. Somewhat
surprisingly, four domain polypeptides (and of
course genes) occur in a variety of algae, fungi and
animals, but have been completely lost in multicel-
lular terrestrial embryophyte plants, such as the
plants considered in this review. Thus the plants
considered here, evolved from algae containing
such four domain peptides and genes, but these
have been completely lost in these plants [38,39].
It is the author’s view, that the voltage sensor of
these channels may play a unique central role in
producing biological responses to low intensity
microwave/lower frequency EMFs because the
special structure of the voltage sensor, causes it to
be uniquely sensitive to these weak EMFs, as dis-
cussed above. This view needs to be further tested
experimentally, of course.
An additional puzzle that must be considered, is
why Ca2+ fluxes have such an important role in
both animals and plants in responding to such
EMFs? I think that part of the answer is that
[Ca2+]i is so important in calcium signaling and
that [Ca2+]i is normally maintained at very low
levels in most cell types under most conditions,
except when brief signaling is needed. In addition,
the electrochemical driving force driving Ca2+ into
the cell is very high it is composed of both the
roughly 104 higher external than internal Ca2+
(chemical driving force) plus the much higher
Electromagnetic Fields Act Similarly in Plants as in Animals Current Chemical Biology, 2016, Vol. 10, No. 1 7
electrical driving force because Ca2+ is a divalent
cation, as compared with the other monovalent
ions. It is very important for most organisms and
tissues to maintain very low [Ca2+]i over extensive
time periods to prevent calcium toxicity.
A study providing important information on a
channel that probably has a central role in mediat-
ing such Ca2+ fluxes into plants, identified the
AtTPC1 channel in Arabidopsis thaliana as the
main mediator of Ca2+ influx through the plasma
membrane of leaf cells [18]. In this study, trans-
genic Arabidopsis plants were used expressing the
calcium sensor protein aequorin, a protein that
binds Ca2+ to produce an easily measured blue lu-
minescence which serves, then, as a measure of
Ca2+ concentration in the cytoplasm (“cytosol”) of
the cell. In this study, the Ca2+ fluxes were pro-
duced by depolarization of the plasma membrane
produced in turn by high sucrose levels. In Fig. 4
of Furuichi et al. [18], they showed that increased
expression of the AtTPC1 gene produced greater
sucrose-induced Ca2+ aequorin luminescence and
that greatly lowered AtTPC1 expression produced
a ten-fold decrease in such luminescence; both of
these observations show that AtTPC1 channel is
central to producing the [Ca2+]i cytoplasmic in-
crease. Furuichi et al. [18] also showed that the
AtSUC1 and 2 sucrose symporters each have roles
in producing the depolarization causing the [Ca2+]i
increases. There are similar genes occurring in
other plants as well as similar depolarization-
activated Ca2+ channels in other plants and these
are often collectively referred to as TPC channels
[38.39]. The AtTPC1 channel in Arabidopsis is
universally expressed across various tissues in the
plant [18].
What can we say about the structure of the
AtTPC1 gene and the protein that it encodes? The
overall structure of the protein is [18] “similar to
half of the general structure of the a-subunits of
voltage-activated (that is gated) Ca2+ channels.”
The VGCCs have four very similar domains, each
containing 6 transmembrane alpha helixes, with
the 4th helix out of the 6 each containing 5 positive
charges [9]. The 4th helixes in these 4 domains col-
lectively making up the voltage sensor. However
the AtTPC1 protein only contains two domains
[18], making up half of the structure for the
VGCCs but such proteins are thought to act as di-
mers in the membrane, such that the two identical
subunits may act together to function much like a
single VGCC a-subunit does in animals. The se-
quence of the AtTPC1 protein (shown in Fig. 1A
of [18]), predicts that the first domain 4th helix
contains 4 positive charges and the second domain
4th helix contains 5 positive charges. This predicts
that the voltage sensor of the AtTPC1 protein (act-
ing as a dimer), has a total of 18 positive charges,
similar but not identical to the 20 positive charges
thought to be in the voltage sensor of the animal
VGCCs [9]. There is a 4 domain VGCC-like pro-
tein occurring in the yeast Saccharomyces cere-
visiae, which when knocked out in yeast produces
a mutant that grows much more slowly and has
less Ca2+ uptake compared with the wild type. Ex-
pression of the AtTPC1 cDNA in the mutant yeast,
allows the yeast to grow at almost normal rates
and to accumulate Ca2+ from the medium more
normally [18]. Thus apparently, expression of the
AtTPC1 cDNA sequence in yeast can allow the
plant protein to function almost normally in place
the missing VGCC-like protein. While the
AtTPC1 protein has not yet been directly tested to
determine if it is the main target of these weak
EMFs in plants, it seems highly plausible that in
plants, as in animals, the unique properties of the
voltage sensor causes such Ca2+ channels to be the
main targets of weak EMFs in plants. There is a
possibility that cyclic nucleotide gated channels
encoded by single domain genes may be a target of
EMFs leading to Ca2+ influx in plant cells; howev-
er, these have only weak voltage gating [40] and
therefore seem to be unlikely to be effective tar-
gets of these EMFs.
In summary, plants resemble animals in their
responses to low intensity microwave frequency
EMFs as follows:
1. Plants resemble animals in that low intensity
microwave EMFs activate one or more plasma
membrane calcium channels, allowing calcium
influx into the cell, raising [Ca2+]i.
2. Plants resemble animals in that agents which
block calcium channels can block responses
produced by low intensity EMF exposure.
3. Plants resemble animals in that extremely low
frequency EMFs act like microwave EMFs, al-
so by raising [Ca2+]i.
4. Plants resemble animals in that they undergo
both oxidative stress and DNA strand breaks,
with those strand breaks leading to both for-
8 Current Chemical Biology, 2016, Vol. 10, No. 1 Martin L. Pall
mation of micronuclei and to chromosomal re-
arrangements.
5. Plants resemble animals in that increased
[Ca2+]i levels following microwave EMF expo-
sure produce many (possibly most) of the bio-
logical effects of such EMF exposure.
6. Plants resemble animals in that candidate chan-
nels in plants for possibly producing this effect,
the TPC channels, contain a voltage sensor that
is activated by partial depolarization of the
plasma membrane and is predicted to be ex-
tremely sensitive to low intensity EMFs be-
cause of its structure and physical location in
the plasma membrane.
However, the plant channels in #5 above are
candidate channels, and have not been clearly
shown to have an essential role in producing the
[Ca2+]i increases following EMF exposure. There
is a simple type of experiment which should be
done to determine whether this is correct or not.
There are mutants of Arabidopsis which are com-
pletely deficient in its TPC function (mutants in
the AtTPC1 gene). If the channel protein encoded
by this gene is essential to producing responses to
EMFs, than those mutants should be unresponsive
to EMF exposure.
CONFLICT OF INTEREST
There is no conflict of interest concerning the
materials presented in the article.
ACKNOWLEDGMENTS
Declared None.
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This review considers a paradigm shift on microwave electromagnetic field (EMF) action from only thermal effects to action via voltage-gated calcium channel (VGCC) activation. Microwave/lower frequency EMFs were shown in two dozen studies to act via VGCC activation because all effects studied were blocked by calcium channel blockers. This mode of action was further supported by hundreds of studies showing microwave changes in calcium fluxes and intracellular calcium [Ca2+]i signaling. The biophysical properties of VGCCs/similar channels make them particularly sensitive to low intensity, non-thermal EMF exposures. Non-thermal studies have shown that in most cases pulsed fields are more active than are non-pulsed fields and that exposures within certain intensity windows have much large biological effects than do either lower or higher intensity exposures; these are both consistent with a VGCC role but inconsistent with only a heating/thermal role. Downstream effects of VGCC activation include calcium signaling, elevated nitric oxide (NO), NO signaling, peroxynitrite, free radical formation, and oxidative stress. Downstream effects explain repeatedly reported biological responses to non-thermal exposures: oxidative stress; single and double strand breaks in cellular DNA; cancer; male and female infertility; lowered melatonin/sleep disruption; cardiac changes including tachycardia, arrhythmia, and sudden cardiac death; diverse neuropsychiatric effects including depression; and therapeutic effects. Non-VGCC non-thermal mechanisms may occur, but none have been shown to have effects in mammals. Biologically relevant safety standards can be developed through studies of cell lines/cell cultures with high levels of different VGCCs, measuring their responses to different EMF exposures. The 2014 Canadian Report by a panel of experts only recognizes thermal effects regarding safety standards for non-ionizing radiation exposures. Its position is therefore contradicted by each of the observations above. The Report is assessed here in several ways including through Karl Popper's assessment of strength of evidence. Popper argues that the strongest type of evidence is evidence that falsifies a theory; second strongest is a test of "risky prediction"; the weakest confirms a prediction that the theory could be correct but in no way rules out alternative theories. All of the evidence supporting the Report's conclusion that only thermal effects need be considered are of the weakest type, confirming prediction but not ruling out alternatives. In contrast, there are thousands of studies apparently falsifying their position. The Report argues that there are no biophysically viable mechanisms for non-thermal effects (shown to be false, see above). It claims that there are many "inconsistencies" in the literature causing them to throw out large numbers of studies; however, the one area where it apparently documents this claim, that of genotoxicity, shows no inconsistencies; rather it shows that various cell types, fields and end points produce different responses, as should be expected. The Report claims that cataract formation is produced by thermal effects but ignores studies falsifying this claim and also studies showing [Ca2+]i and VGCC roles. It is time for a paradigm shift away from only thermal effects toward VGCC activation and consequent downstream effects.
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The direct targets of extremely low and microwave frequency range electromagnetic fields (EMFs) in producing non-thermal effects have not been clearly established. However, studies in the literature, reviewed here, provide substantial support for such direct targets. Twenty-three studies have shown that voltage-gated calcium channels (VGCCs) produce these and other EMF effects, such that the L-type or other VGCC blockers block or greatly lower diverse EMF effects. Furthermore, the voltage-gated properties of these channels may provide biophysically plausible mechanisms for EMF biological effects. Downstream responses of such EMF exposures may be mediated through Ca(2+) /calmodulin stimulation of nitric oxide synthesis. Potentially, physiological/therapeutic responses may be largely as a result of nitric oxide-cGMP-protein kinase G pathway stimulation. A well-studied example of such an apparent therapeutic response, EMF stimulation of bone growth, appears to work along this pathway. However, pathophysiological responses to EMFs may be as a result of nitric oxide-peroxynitrite-oxidative stress pathway of action. A single such well-documented example, EMF induction of DNA single-strand breaks in cells, as measured by alkaline comet assays, is reviewed here. Such single-strand breaks are known to be produced through the action of this pathway. Data on the mechanism of EMF induction of such breaks are limited; what data are available support this proposed mechanism. Other Ca(2+) -mediated regulatory changes, independent of nitric oxide, may also have roles. This article reviews, then, a substantially supported set of targets, VGCCs, whose stimulation produces non-thermal EMF responses by humans/higher animals with downstream effects involving Ca(2+) /calmodulin-dependent nitric oxide increases, which may explain therapeutic and pathophysiological effects.