PERGAMON Micron 31 (2000) 165–181

www.elsevier.com/locate/micron
Review

Radiation response of cell organelles

Z. Somosy*
“Fodor József” National Centre of Public Health, National “Frédéric Joliot-Curie” Research Institute for Radiobiology and Radiohygiene, Anna St. 5, 1221
Budapest, Hungary
Received 15 March 1999; received in revised form 20 August 1999; accepted 25 August 1999

Abstract
The cellular responses to various form of radiation, including ionizing- and UV-irradiation or exposure to electromagnetic fields is
manifested as irreversible and reversible structural and functional changes to cells and cell organelles. Moreover, beside the morphological
signs related to cell death, there are several reversible alterations in the structure of different cell organelles. The radiation-induced changes in
the supramolecular organization of the membranes, including plasma membrane, and different cell organelle membranes, play a significant
role in the development of acute radiation injury. These signs of radiation-induced reversible perturbation biological membranes reflect
changes in the organization and/or composition of the glycocalix, modified activity and/or distribution of different membrane domains,
including enzymes and binding sites. The observed changes of the cell surface micromorphology and the alteration of intercellular connec-
tions are closely related to the reorganization of the cytoskeletal elements in the irradiated cells. The mitochondria, endoplasmic reticulum,
Golgi-complex, the lysosomal system have long been considered to be direct intracellular targets of irradiation. The listed morphological
alterations of nuclear chromatin (e.g. changes of fine structure, altered number of nucleolar organizing regions and micronuclei, development
of chromosome aberrations) may originate from the radiation-induced damage to the supramolecular organization of DNA and/or nucleus
specific proteins. These endpoints of radiation effects resulted as direct consequence(s) of absorbed radiation energy, and indirectly altered
intra-, intercellular communication or modified signal transduction. Some complementary data suggest that all these effects are not strictly
specific to radiation and may be best considered as general stress responses, similar to those observed after application of various injurious
agents and treatments to cells. Moreover, they may be equally responsible for direct degradation of supramolecular component of cells,
altered signal transduction, or changes in the amount or ratio of any extracellular mediators upon irradiation. Nevertheless, qualitative and/or
quantitative evaluation of any changes of chromosomes by different techniques (morphological analysis of metaphase chromosomes,
fluorescent in situ hybridization, development of micronuclei etc.) are useful biological indicators as well as “biological dosimeters” of
radiation injury. It is suggested, that some modern methods such as immunohistochemical detection of different proteins, specific markers of
cell organelles and cytoskeleton, inspection of distribution of cell surface charged sites and different membrane domains and application of
tracer substances may all be included into protocols for evaluation of cell alterations induced by different types and intensities of radiation.
q 1999 Elsevier Science Ltd. All rights reserved.

Keywords: Ionizing-irradiation; Ultraviolet-irradiation; Electromagnetic field; Response; Fine structure; Cell organelles; Biological membranes

Contents
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 166
2. Cell death . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 167
2.1. Apoptosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 167
2.2. Necrosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 168
2.3. Giant cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 168

* Tel.: 136-1 226-0144; fax: 136-1-226-0144.

E-mail address: somosy@hp.osski.hu (Z. Somosy)
Abbreviations: bCOP, Non-clatrin coated vesicles containing coat protein; CF, Cationized ferritin; CHO, Chinese hamster ovary cell; CHO K1, Chinese
hamster ovary cell line; Con A, Concanavalin A lectin; C3H 101/2, Murine fibroblast; DNA, Deoxyribonucleic acid; ELF, Extremely low frequency; EMF,
Electromagnetic field; GSM, Global system for mobile communication; Gy, Gray, 1 J/kg adsorbed radiation energy of medium; HT-29, Colon carcinoma cell;
L-929, Murine fibroblast cell-line; NIEHS, National Institute of Environmental Health Sciences; NINH 3T3, Murine fibroblast cell line; MOLT-4, T
lymphocyte line; pre-mRNA, Pre-messenger ribonucleic acid; pre-rRNA, Pre-ribosome ribonucleic acid; p58, Microtubule binding protein on the Golgi
apparatus; rEr, Rough endoplasmic reticula; SAR, Specific adsorption rate; UV-B, Ultraviolet B; SCLII, Human epidermal cell line; TUNEL assay, Method of
detecting in situ DNA fragmentation; VIP, Vasointestinal peptide; V79, Chinese hamster fibroblast; WGA, Wheat germ agglutinin

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166 Z. Somosy / Micron 31 (2000) 165–181

3. Morphology of cells surviving irradiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 168

3.1. Radiation response of plasma membrane and cytoplasmic organelles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 168
3.1.1. Plasma membrane . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 168
3.1.1.1. Membrane domains . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 168
3.1.1.2. Membrane-bound calcium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 169
3.1.1.3. Cell surface micromorphology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 170
3.1.1.4. Intercellular contacts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 170
3.1.2. Cytoskeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 172
3.1.3. Mitochondria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 172
3.1.4. Endoplasmic reticulum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 173
3.1.5. Golgi apparatus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 173
3.1.6. Lysosomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 173
3.2. Reversible forms of nuclear alteration in irradiated cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 174
3.2.1. Nuclear swelling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 174
3.2.2. Changes in the structure of chromatin and nucleolus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 174
3.2.3. Chromosome aberrations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 175
3.2.4. Changes in nuclear envelope . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 176
3.2.5. Micronucleated cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 176
4. Concluding remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 176
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 177
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 177

1. Introduction free radicals. The energy transfer is accomplished by simple

thermal conversion. However, line of evidences suggested,
The forms of radiation consist of energetic particles and that ELF EMF exposures can also lead to non-thermal rever-
electromagnetic waves (Table 1). These radiation types can sible and irreversible effects. Thus, the non-thermal inter-
penetrate into living tissue or cells and result in the transfer action of cellular membrane surfaces with ELF EMF is a
of radiation energy to the biological material. The absorbed well-known phenomenon. During this process, this type of
energy of the ionizing radiation can break chemical bonds EMF can disturb the electric double layer of the cell surface
and cause ionization of different atoms and molecules, membrane, and/or modify the intrinsic conformational equi-
including water and different biologically essential macro- librium of membrane domains. The possible mechanism(s)
molecules, as DNA (Schulte-Frohlinde and Bothe, 1991; of these interactions and its biological consequences (e.g.
Lett, 1992) membrane lipids and proteins (Köteles, 1979;
Cramp et al., 1994; Daniniak and Tann, 1995). Moreover Table 1
the ionization effect of ultraviolet radiation, especially, the Types and characteristic features of radiation (according to Livesey et al.
ultraviolet B (UV-B), can be absorbed by nucleic acids, and (1985))
by some aromatic amino acids and may cause breaks and/or
Type Sources I/NI a
perturbation of molecular structures (Shimmura and
Tsubota, 1997; Caricchio et al., 1998; Hollósy, 1999). Particulate
Besides the above-mentioned direct energy transfers the Electrons (b 2 particles) Radioactive decay I
indirect energy transfers via free radicals are also essential Positrons (b 1 particles) Radioactive decay I
Protons Cyclotron, Van de Graff I
in the radiation damage of organic molecules during the
generator
energy-absorption process. Thus, the radiolysis of water Neutrons Nuclear fission, Cyclotron I
and other molecules to hydroxy radicals is important in Helium nuclei (a particles) Radioactive decay I
the genesis of radiation damage of living systems as Nuclei of heavier elements Particle accelarators I
reviewed by Livesey et al. (1985). The endogen and exogen Electromagnetic
Cosmic rays …5 × 1025 nm† Stars I
factors which can influence the amount and stability of the
g-rays …5 × 1024 –1:4 ×21 nm† Radioactive decay I
radiation-produced free radicals, including molecular X-rays …1 × 1022 –10 nm† X-ray machine I
oxygen, thiols, vitamin E and other antioxidants can alter Ultraviolet (280–400 nm) Sunlight, artificial sources Int
the radiosensitivity of living material (Livesey et al., 1985). Microwave (0.3–300 cm) Radio, television and other NI
The radioprotection of organisms by chemical agents is also transmitters, other
artificial EM fields
based on radical scavenging reactions.
Radiowaves (.0.3 cm) Communications, cosmic NI
Opposite to ionizing radiation the energy of microwave sources
and radiofrequency do not transfer to biological macromo-
a
lecules by the formation of chemically reactive ion pairs and I, ionizing; NI, non-ionizing; Int, intermediate.
 Z. Somosy / Micron 31 (2000) 165–181
alteration of different cellular signal transduction systems
and in intercellular communication have recently been
reviewed in the NIEHS Working Group Report (1998).
The investigation of acute and longer term effects of
low doses of ionizing radiation on cells and tissues have
exceptional importance in radiotherapy, as well as in the
management of accidental radiation exposure. Recently,
considerable effort has been taken to clarify the biological
consequences of non-ionizing radiation, in addition to UV-
B irradiation and the effects of exposure to weak (non-
thermal) low-frequency EMFs (Shimmura and Tsubota,
1997; Caricchio et al., 1998; NIEHS Working Group
Report, 1998; Hollósy, 1999).
According to their time course, the post-irradiation events
of in vivo systems upon radiation exposition can be classi-
fied as acute-, delayed-, and late-phase responses, occurring
a few hours or days, a few weeks and some months after
irradiation (Berthrong and Fajardo, 1981; Rubio and Jalnäs,
1996). Acute- and delayed-phase responses are also
observed in vitro (in cell cultures). Acute-phase events
occurs within a few hours or days after irradiation in the
irradiated cells, while delayed-phase responses may be
observed in their later descendants (Kadhim et al., 1995;
Morgan et al., 1996; O’Reilly and Mothersil, 1997). The
effects may be long lasting, i.e. they can be observed up
to 45 cell doublings after radiation exposure, as a conse-
quence of the radiation-induced genomic instability. This
phenomenon, as shown by several authors is also observable
following UV-B irradiation (O’Reilly and Mothersil, 1997).
At the cellular level the radiation response may be mani-
fested in irreversible changes, such as mutations, malignant
transformation, development of abnormal cell forms and the
death of cells, or as minor reversible structural and func-
tional alterations of biological systems. Both the irreversible
and reversible damage of cells are manifested at the sub-
cellular level as structural and functional changes in cell
organelles, including plasma membrane, intercellular
contacts, nuclear membranes, Golgi-complex, mitochon-
dria, endoplasmic reticulum, lysosomes, cytoskeletal
system etc.
In this review we summarize some data on the morpho-
logical aspects of radiation-induced cell death as well as on
reversible changes of cell shape, cell surface micromorphol-
ogy and in the ultrastructure of cell constituents after expo-
sure to ionizing, ultraviolet irradiation and following
exposure to weak, low-frequency electromagnetic fields.
2. Cell death
Cell death can be the ultimate consequence of cellular
radiation injury (Okada, 1970a; Harms-Ringdahl et al.,
1996; Blank et al., 1997; Hendry and West, 1997). Know-
ledge of the type or mechanisms leading to radiation-
induced cell killing is especially important in practice
because therapeutic application of irradiation is frequently
167
directed towards killing of target malignant cells. Cell death
caused by ionizing irradiation has previously been categor-
ized into two main classes, based upon the time of disinte-
gration of cells after exposure, namely into as interphase
death and reproductive or mitotic death (Okada, 1970a).
Interphase death is defined as an irreversible impairment
of cellular metabolism and breakdown of cellular structures
before entering into the first mitosis after irradiation. Repro-
ductive or mitotic death occurs during mitosis and one or
even several divisions after the irradiation (Okada, 1970b).
Both interphase and reproductive death can be manifested as
apoptosis and/or necrosis (Akagi et al., 1993; Nakano and
Shinohara, 1994; Szumiel, 1994; Harms-Ringdahl et al.
1996).
2.1. Apoptosis
Apoptosis is expressed as an active, intrinsic mechanism
based on the concerted action of specific proteases
(caspases) and endonucleases (Khodarev et al., 1998).
Necrosis is the consequence of irreversible destruction of
cell membranes, followed by collapse of cellular meta-
bolism resulting from extrinsic damage to the cell.
The category of cell death depends on the type of cells
and tissues and on the conditions and types of ionizing
irradiation (Harms-Ringdahl et al., 1996; Blank et al.,
1997; Hendry and West, 1997; Olive and Durand, 1997;
Meng et al., 1998). Many observations suggest that apopto-
sis is the main form of ionizing radiation-induced cell death
in lymphocytes, thymocytes, lymphoid and myeloid cell
lines. However, some cell types show a slow and delayed
apoptotic response (Hendry and West, 1997; Olive and
Durand, 1997). The process starts within minutes following
irradiation and lasts for several hours. On the other hand,
other types of cells such as cultured fibroblasts (V79,
L-929), Chinese hamster ovary (CHO) cells, as well as
many human tumour cell lines, appear in practice unable
to undergo apoptosis in vitro and they generally die by
necrosis Time- and cell position-dependent variations in
the apoptotic response have been observed in several tissues
(Hendry and West, 1997). For example, a rapidly evolving
wave of apoptosis was seen in irradiated lymphoid organs
and in salivary gland parenchyma. Other tissues (e.g. small
intestine, epidermis) showed a slower and ordered apoptotic
response, during which the number of apoptotic cells
increased only in a well determined zone of the tissue, in
stem cell zones of small intestinal crypts (Ijiri and Potten,
1987). The dose of irradiation may also play a role in deter-
mining the type of cell death. As reported by Payne et al.
(1992), high doses may cause cell destruction by necrosis in
lymphoid cells, while lower doses induce apoptosis.
UV-B irradiation may also induce apoptosis in several
cell systems (Caricchio et al., 1998; Gniadecki et al.,
1998; Meng et al., 1998). Dose (energy) dependent forms
of apoptotic cell death were observed in keratinocytes,
which responded to the low energy UV-B irradiation
168 Z. Somosy / Micron 31 (2000) 165–181
(50 mJ/cm 2) by producing apoptosis, while very high
energy (300 mJ/cm 2) exposition resulted in typical necrosis
(Gniadecki et al., 1998)
There are only few data concerning the effects of EMF on
the mechanism of cell death and apoptosis. Simkó et al.
(1998) examined morphological changes in two human
cell lines exposed to 0.1–1.0 mT 50 Hz AC magnetic fields.
In the SCLII transformed squamous-cell line, a dose-
dependent increase in apoptosis was seen after 48 and
72 h continuous exposure to 50 Hz (0.8 and 1.0 mT). In
contrast, in a non-transformed amniotic fluid cell line, no
significant changes were noted, suggesting that various cell
lines react differently to the same electromagnetic field.
Ismael et al. (1998) applied the TUNEL assay to observe
apoptotic events in mouse thymocytes treated with dexa-
methasone and magnetic fields. An increase was observed
in the number of apoptotic thymocytes but not in splenic
T-cells of animals exposed to a 0.4–1.0 mT 60 Hz magnetic
field. The number of apoptotic thymocytes and apoptotic
spleen cells from mice exposed to an 8–20 mT DC
magnetic field were similar to that of the controls.
As a rule, apoptosis and necrosis can be easily distin-
guished by morphological criteria.
Shrinkage and fragmentation of nuclei are the main
morphologic features of cells dying by apoptosis. Condens-
ation and clumping of chromatin, redistribution of nuclear
pores, dissolution of nuclear laminae accompanies this
process. The chromatin fragments may appear scattered in
the cytoplasm in the form of so called micronuclei. The cell
as a whole shrinks and finally breaks up into fragments
which become engulfed by neighbouring cells (DiPietro et
al., 1994; Falcieri et al., 1994). Alterations in mitochondrial
structure (swelling and disappearance of cristae) and func-
tion (drop in mitochondrial transmembrane potential) occur
in early stages of apoptosis and may precede and/or accom-
pany nuclear changes (Petit et al., 1995). Disintegration of
Golgi complex and dilatation of endoplasmic reticulum as
well as disappearance of microvilli (Kondo et al., 1997) and
cell contacts (Brancolini et al., 1997) and formation of blebs
(Mills et al., 1998) are commonly observed in apoptotic
cells. These changes are in close relationship with reorgan-
ization of the cytoskeleton and an altered phosphorylation
state of the cytoplasmic myosin light chains and regulatory
proteins of the microfilament system (Brancolini et al.,
1997; Kondo et al., 1997; Mills et al., 1998).
2.2. Necrosis
On the other hand, mitochondrial swelling, dilatation and
degranulation of endoplasmic reticule, vacuolization of
Golgi complex, lysosomal rupture, disorganization of cyto-
skelatal system, dilatation and dissolution of nuclear-lami-
nae, and appearance of breaks in the plasma membrane are
the morphologic hallmarks of necrotic process, which ends
in irreversible swelling and lysis of cells (Stefani et al.,
1977; Falcieri et al., 1994).
2.3. Giant cells
Ionizing irradiation may induce morphological altera-
tions such as development of giant cells, which cells prior
to death (Olive and Durand, 1997). Giant cell formation
occurs in vivo and in vitro in a variety of mammalian
cells after exposure to high doses of ionizing irradiation
(Tolmach and Marcus, 1960; Hurwitz and Tolmach, 1969;
Rubio and Jalnäs, 1996; Olive and Durand 1997). As
reported by Rubio and Jalnäs (1996) the appearance of
giant cells is a dose-dependent event in irradiated small
intestine and these cells can be detected after moderate
and/or high dose irradiation. These cells probably retain
the capacity to grow, but are unable to synthesize DNA
and divide. Mono- and bi-nucleated and multi-nucleated
forms appear frequently in cell cultures Okada, 1970b;
Kura et al., 1978). According to Kura et al. (1978), the bi-
or multi-nucleated giant forms develop by fusion from
mono-nucleated cells. An increased frequency of apoptotic
cell death can develop as a consequence of radiation
induced genomic instability (Kadhim et al., 1995; Morgan
et al., 1996).
3. Morphology of cells surviving irradiation
3.1. Radiation response of plasma membrane and
cytoplasmic organelles
The radiation-induced alterations to the supramolecular
organization and function of cell membranes play a signifi-
cant role in the development of acute radiation injury. Non-
lethal doses of ionizing and non-ionizing radiation perturb
the plasma membrane reversibly and this might be a direct
or indirect cause of non-stochastic effects observed in cells
and tissues.
3.1.1. Plasma membrane
3.1.1.1. Membrane domains. The main signs of radiation-
induced membrane perturbation are the changes in the
organization and/or composition of the glycocalyx, mani-
fested as alterations in the amount and/or distribution of the
negatively charged membrane components (i.e. sialic acid),
lectin-, and calcium-binding sites. It is well known that the
exposition to ionizing radiation is followed by reversible
decrease of surface negative charges in several cell types
(Somosy et al., 1986; Köteles et al., 1987). According to our
data based on the cationized ferritin-binding technique, the
number and density of negative charged sites available on
the surfaces of human fibroblasts dropped significantly
within 1 min after X-irradiation, in the dose range from
0.25 to 2.5 Gy, then recovered within 1 h (Fig. 1 and
Table 2) (Somosy et al., 1986). UV light exposition can
also cause decrease in amount of net negative charges on
the cell surface (Krylenkov et al., 1984).
 Z. Somosy / Micron 31 (2000) 165–181
Fig. 1. Binding of CF on (a) non-exposed primary human fibroblasts and
after (b) 10 min; (c) 1 h 2.5 Gy X-irradiation. Bar: 0.5 mm.
Electromagnetic field expositions may also modify the
amount of cell surface negative charges. However, the
magnitude this effect is dependent on the physical para-
meters and/or type of the field applied (Marron et al.,
1988; Smith et al., 1991; Somosy et al., 1991). Thus, as
shown in the aqueous partition chromatography data of
Marron et al. (1988), sinusoidal modulated electric and
magnetic field exerted different effects on the cell surface
of Physarum polycephalum. For instance, exposure to an
electric field increased the negative charge on the cell
surface while the magnetic field decreased it.
Changes of lectin-binding capacity of cell membranes
following ionizing and nonionizing radiation have been
observed by many authors (Köteles et al., 1976; Köteles et
al., 1983; Kubasova et al., 1984; Hodges et al., 1985;
Somosy et al., 1985a; Somosy et al., 1986; Somosy et al.,
1987; Nievergelt-Edido et al., 1993; Traikov et al., 1994;
Condaminet et al., 1997). According to Köteles et al. (1976),
2 Gy dose X-irradiation induced a 20–25% increase in the
binding of Concanavalin A (Con A) to human fibroblast
after 30–60 min, which then returned to the control level
after 3 h. Taking into consideration that the observed
169
Table 2
Change of cationized ferritin binding to unfixed human fibroblast after X-
irradiation with 2.5 Gy (Somosy et al., 1986) (primary human fibroblast
cultures were irradiated by X-ray with 2.5 Gy dose. Cationized ferritin
(Sigma) was used for the visualization of the negative charges on the cell
surface according to Danon et al. (1972). Cell cultures were incubated for
1 min in phosphate buffered saline containing 0.3 mg/ml CF)
Time after irradiation Number of Cationized ferritin
particles per mm 2 (CF) coverage
(per cent a) (percent of total
apical surface b)
Unirradiated control 4030 ^ 250 (100) 42 ^ 14
1 min 2250 ^ 270 (56) 25 ^ 11
10 min 1660 ^ 121 (41) 24 ^ 9
1h 3840 ^ 235 (95) 58 ^ 11
4h 4210 ^ 276 (104) 56 ^ 14
a
Ferritin particles were counted in tangential section through the cell
surface, on micrographs at 100 000 × final magnification at 50 × 1 mm2
area per sample.
b
CF coverage was estimated on perpendicular section of cellular
surfaces on micrographs at 34 500 × magnification.
changes of lectin binding were dose- and cell type-depend-
ent, this phenomenon was even proposed as a biological
indicator of radiation injury (Köteles, 1979; Köteles et al.,
1983; Kubasova et al., 1984; Köteles et al., 1987).
Transient, dose-dependent changes in wheat germ agglu-
tinin (WGA) binding were observed in X-ray irradiated
lymphocytes (Moullier et al., 1986). An increased WGA
binding was explained by elevation of the number of bind-
ing sites found up to 1 Gy, while between 2 and 7 Gy an
opposite effect, i.e. a decrease in WGA binding was
observed, which was probably due to the loss of sialic
acid residues from cell surface. Our data show, that changes
in the amount of lectin- or charged sites are frequently
accompanied by redistribution of these ligands on the
surface of irradiated cells (Somosy et al., 1987; Somosy et
al., 1989).
Ionizing radiation and EMF exposure directly modify the
number and/or response of several receptors, because of
perturbation of the plasma membrane. For example,
Griffiths et al. (1996) found a rapid eight-fold decrease in
vasointestinal peptide (VIP) receptor affinity and an
increased receptor number in pig enterocytes at 6 Gy
X-ray or neutron irradiation. EMFs may also effect cell
surface receptors. A reduced ability to produce cyclic
AMP in response to parathyroid hormone by interaction of
EMFs was observed in mouse osteoblast-like cells (Luben et
al., 1982). Modified distribution and activity of membrane
bound enzymes, including adenylate cyclase and calcium
ATPase, following radiation exposure was reported by
several authors (Wattel et al., 1977; Köteles, 1979; Somosy
et al., 1988; Somosy et al., 1994; Cramp et al., 1994; Dani-
niak and Tann, 1995).
3.1.1.2. Membrane-bound calcium. Several lines of
evidence based on the detection of calcium in the electron
170 Z. Somosy / Micron 31 (2000) 165–181
Fig. 2. Confluent culture of (a): non-exposed primary human fibroblasts.
The cell shape after (b) 30 min; (c) 4 h; and (d) 24 h 2.5 Gy X-irradiation.
Bar: 4 mm.
microscopic show that the localization of the membrane-
bound calcium is altered both after X-ray radiation and
EMF exposure in the small intestine (Somosy et al., 1993;
Somosy et al., 1994). Calcium pyroantimonate precipitates
were localized within intercellular space in the lateral
regions of intact small intestinal epithelial cells, including
intermediate junctions and desmosomes. (Fig. 3a), (Somosy
et al., 1993). Ionizing radiation (X-ray, 1–3 Gy doses)
induced a prominent and rapid decrease of plasma
membrane-bound calcium in the small intestine. On the
other hand, modulated microwave exposure (16 Hz, 0.5
and 1 mW/cm 2 power densities, 1.6 mW/g specific
adsorption rate [SAR] leads to a reversible redistribution
of calcium from the outer surface of small intestinal
epithelial cells (Fig. 3b), (Somosy et al., 1993). In another
study, we observed changes in the localization of calcium in
neural regions (in the habenula and cortex) after modulated
microwave exposition (16 Hz, 0.5 and 1 mW/cm 2 power
densities and 1.6 mW/g SAR). According to our findings,
microwave irradiation caused a redistribution of loosely
bound calcium at synapses, i.e. induced the appearance
of precipitates in the synaptic cleft and on the external
side of neuronal plasma membrane, while the calcium
content of synaptic vesicles decreased (Kittel et al., 1996).
In contrast, GSM modulated RF field (900 MHz, 271 Hz,
1/8 duty-cycle), did not cause unambiguous effect on the
distribution of calcium in the cerebral cortex (Somosy et al.,
1998).
3.1.1.3. Cell surface micromorphology. A wide spectrum
of the changes in cell surfaces micromorphology (e.g.
changes in the number and size of microvilli, development
of surface blebs, membrane ruffling, retraction of
pseudopods) have been observed in a variety of cells
following irradiation. Ionizing irradiation may induce
rapid retraction of cell protrusions and rounding up of
flattened cells, e.g. endothelial cells (Kantak et al., 1993)
primary human fibroblasts (Somosy et al., 1983, 1987),
(Fig. 2), glial cells (Hamberg et al., 1977), Ehrlich ascites
cells (Skog et al., 1983). The rate and reversibility of
radiation-induced micromorphological changes depends
on the type of cell and on the conditions of irradiation
(Hamberg et al., 1977; Kantak et al., 1993; Somosy et al.,
1983, 1987, 1989, 1991, 1995). Data on the effect of UV-B-
radiation on shape and cell surface morphology are few.
Daniniak and Tann (1995) showed, that lymphocytes
treated for a brief period of time with UV-B (1200 J/m 2),
responded by blunting of microvilli and impaired
exfoliation of surface membrane-derived vesicles.
Weak (non-thermal) low-frequency electromagnetic
fields may also induce shape and surface changes in cultured
cells. Uniform field exposure influence the direction of
migration and formation of cell protrusions (Patel and
Poo, 1982; Onuma and Hui, 1988; Ross et al., 1988). As
reported by Patel and Poo (1982), the number of filopodia
facing the cathode increased within 5 min of field exposure
in fibroblasts, with a concomitant decrease on the anodic
side. Cell surface changes upon magnetic field exposure
were also observed by Paradisi et al. (1993). According to
their scanning electron microscopic data, magnetic field
exposure of 2.0–2.5 mT caused smoothing of the cell
surface and formation of blebs from the K562 erythroleu-
kemic cell line. The number of injured cells was directly
related to the duration of treatment (Paradisi et al., 1993).
Induction of neurite outgrowth was observed in different
experimental systems following exposition to ELF EMF
(Blackman et al. 1996; NIEHS Working Group Report,
1998).
3.1.1.4. Intercellular contacts. A characteristic cellular
response to ionizing radiation is the alteration of structure
and function of intercellular contacts (Durand and
Sutherland, 1972; Hamberg et al., 1977; Somosy et al.,
1983, 1987, 1993; Trosko et al., 1990; Kantak et al.,
1993). The ionizing radiation-induced morphological and
functional changes of the gap-junctions in the radiation
response lead to altered cell communication and may
result in the tumorous transformation of cells (Trosko et
al., 1990, 1996). The importance of the gap-junction
response of cells is demonstrated by the so-called contact
effect (Durand and Sutherland, 1972; Kwok and Sutherland,
 Z. Somosy / Micron 31 (2000) 165–181 171

Fig. 3. Distribution of calcium in the junctional complexes of (a) unirradiated and (b) modulated microwave irradiated small intestine. The histochemical
reaction product is localized in the intercellular space within the control cells (arrow) (a). After microwave exposure (b), the reaction product can be seen at the
cytoplasmic side of lateral membranes (arrow). Double empty arrowheads, tight junction; double marked small arrowhead, intermediate junction; large
arrowhead, desmosome. Bars: (a,b) 0.5 mm; insets, 0.1 mm.

1991; Ishii and Watanabe, 1996). This term is based on the
data from comparative investigations of radiation effects on
spheroids and monolayer cultures of the same cell type. The
multicellular spheroids are more resistant to killing by
ionizing radiation, than the monolayers. This behaviour is
explained by the presence of a well-developed junctional
system between the cells of spheroids (Durand and
Sutherland, 1972). According to our unpublished results,
based on the scrape loading technique (McKarns and
Doolite, 1992), X-irradiation at 1–3 Gy doses resulted in
biphasic change of dye transfer between HT-29 cells.
First, we found a rapid increase in the intercellular
communication a few minutes after irradiation, followed
later by a decrease in the number of communicating cells.
Alteration of gap-junction-mediated intercellular
communication following UV irradiation was also observed
in V79 Chinese hamster fibroblasts (Bånrud et al., 1994).
This effect was strongly depended on the wavelength and
was not related to modification on distribution of the gap
junctional protein connexin-43 (Bånrud et al., 1994). Ubeda
et al. (1995) investigated changes in gap-junctional perme-
ability by dye-coupling technique in C3H 10T1/2 cells
exposed to magnetic field of 50 Hz at 1.6 mT from a Helm-
holtz coil pair. According to their data, exposure to the
magnetic field blocked the up-regulation of coupling caused
by melatonin treatment. Conversely, dye microinjection
studies in NIH 3T3 cells showed that a 50 Hz field could
up-regulate intercellular coupling (Schimmelpfeng et al.,
1995). Exposure to the field for 5 min caused 1.6-fold
increase in the average number of coupled cells in the
monolayer configuration in these experiments. According
to our unpublished data, based on the scrape loading tech-
nique and connexin-43 immuohistochemistry, magnetic
field exposure leads to a decrease of dye coupling in con-
fluent HT-29 colon carcinoma- and rat glia-cell cultures.
The cellular localization of connexin-43 in HT-29 cells
also changed upon the exposure to magnetic field.
Radiation-induced morphological abnormalities of cell
shape and surface micromorphology may persists in several
cell generations after exposure, as shown by Lyng et al.
(1996) using the hamster cell line (CHO K1) and on virus
immortalized keratinocytes. According to these authors, the
altered phenotype of descendants of irradiated cells is a
consequence of radiation induced genetic instability.
A characteristic feature of acute phase response to ioniz-
ing radiation in vitro is due to the damage of intercellular
contacts, including desmosomes, adherents junctions and
tight junctions. Significant reversible widening of inter-
cellular spaces following X- or gamma-ray irradiation was
observed in oral mucosa, kidney and in intestinal and in
vascular epithelium as the consequence of altered contact
region (Liu et al., 1977; Lieb et al., 1977; Evans et al.,
1986). As a rule, the irradiated epithelial sheets became
leaky due to the destruction of junctional complexes.
Increased vascular permeability, penetration of lanthanum
and ruthenium red tracers and loss of barrier functions for
bacteria, bacterial toxins and proteolytic enzymes in the
intestine were observed in several studies (Quasler, 1956;
Lieb et al., 1977; Porvaznik 1979; Evans et al., 1986;
Somosy et al., 1993, 1999a).
Alteration of tight junctions in epithelial sheets of the
small intestine following ionizing irradiation has been
172 Z. Somosy / Micron 31 (2000) 165–181

Table 3
Changes in morphometrical parameters of tight junction after X-ray and modulated microwave irradiation (Somosy et al., 1999a) (Male CFLP mice were used
in experiments. The mice were whole body irradiated by X-ray at 4.0 Gy and by amplitude-modulated (16 Hz) 2450 MHz microwave for 3 h at a 1 mW/cm 2
power density. The glutaraldehyde fixed intestinal samples were freeze-fractured by standard method. Carbon–platinum replicas were photographed in a JEOL
100CX transmission electron microscope at 20 000 × magnification and the electron micrographs (negatives) were enlarged 100 000 × final magnification.
Morphologic features of tight junctions were evaluated on 20 micrographs from each experimental group. The break index and number of the breaks in the most
apical and the most basal strands were calculated according to Wolburg et al. (1994). For the morphometrical evaluation of samples the Fenestra Vision image
processing software (Kinetic Imaging Ltd., Liverpool, UK) was used)

Morphometrical parameters Control X-ray Microwave

1h 24 h 1h 3h

BI a (1/mm) 1.434 ^ 0.782 6.279 ^ 2.577 3.993 ^ 1.690 0.788 ^ 0.270 1.029 ^ 0.451
Nb b (1/mm) 1.130 ^ 0.866 3.807 ^ 2.250 2.424 ^ 1.530 0.619 ^ 0.582 0.927 ^ 0.935
Na c (1/mm) 0.430 ^ 0.665 3.359 ^ 2.065 3.474 ^ 1.930 0.335 ^ 0.473 0.334 ^ 0.530

a
BI, break index: number of free strand terminals/total strand length.
b
Nb: number of basal breaks/axis.
c
Na: number of apical breaks/axis.

investigated by freeze-fracturing. In an early study, Porvaz-
nik (1979) observed a significant shift in the mean depth of
the tight junction zonule between epithelial cells on the third
day after 3 and 5 Gy X-irradiation in ileal epithelium. Also,
the tight junctions of some of the goblet cells were focally
disrupted.
We have carried out a detailed morphometric analysis of
tight junctions of X-ray and microwave irradiated mouse
jejunal cells on freeze-fractured replicas. X-irradiation
induced an increase of the break indexes (BI, Nb, Na)
suggesting that the structure of the tight junctions was
altered (Table 3). On the other hand, intestinal epithelial
cells react to microwave exposure with an apparent increase
in the structural integrity of their tight junctions, as indi-
cated by the dramatic decrease of break indexes (Table 3)
(Somosy et al., 1999a).
3.1.2. Cytoskeleton
The changes of cell surface micromorphology and the
alteration of intercellular junctions are closely related to
the reorganization of the cytoskeletal elements within the
irradiated cells. Disorganization of actin network and
disruption of intermediate filaments have been observed in
different types of cells exposed to irradiation (Friedman et
al., 1986; Kobayashi, 1988; Anniko et al., 1989; Kantak et
al., 1993; Kasper et al., 1993; Somosy et al., 1995). In our
experiments, we found that X-irradiation at 0.5 and 1.0 Gy
doses caused rapid disruption of the actin and intermediate
filaments and their components appeared as clumps of actin
and cytokeratin aggregates in the cytoplasm of HT-29 cells
(Somosy et al., 1995). Unlike actin and cytokeratin fila-
ments, the microtubules were resistant to irradiation in
HT-29 cells, as well as in endothelial cells and lymphocytes
(Rubin et al., 1988; Raciu et al., 1993; Somosy et al., 1995).
Some observation suggest that radiation may modulate the
expression of genes encoding cytoskeletal proteins (Anniko
et al., 1989; Woloschak and Chang-Liu, 1991).
Similarly to ionizing-radiation, UV exposition also
disrupted the cytoskeleton of cultured keratinocytes
(Zamansky et al., 1992) and lens epithelial cells (Rafferty
et al., 1977). Changes in cell shape and surface micro-
morphology related to alteration of cytoskeleton following
electromagnetic field exposure have been also described
(Popov et al., 1991; Santoro et al., 1997). However, the
cytoskeleton was not totally disrupted by the electromag-
netic field in these experiments. Moreover, as suggested by
Bras et al. (1998) the assembly of microtubules was
promoted and their orientation might be modulated by
high magnetic fields in vitro. Some of the available experi-
mental data the suggest that radiation-induced reorganiza-
tion and breakdown of different cytoskeletal elements is
related to modified calcium homeostasis or altered phos-
phorylation/dephosphorylation state of proteins in the irra-
diated cells (Onuma and Hui, 1988; Zamansky et al., 1992;
Kantak et al., 1993; Somosy et al., 1995; Santoro et al.,
1997).
3.1.3. Mitochondria
Mitochondria have long been considered to be direct
intracellular targets of ionizing radiation. Reactive oxygen
species are continually produced at a relatively high amount
in mitochondria during physiological conditions, however,
their concentration greatly increases following irradiation
and the products of lipid peroxidation accumulate. As a
consequence, alterations in the structure and function of
mitochondria are commonly observed in irradiated cells
(Kergonou et al., 1981; Erickson and Koppenol, 1987).
Elongation and branching of the mitochondria, and a revers-
ible increase of their size and the development of giant
forms are the most frequently reported changes in irradiated
mitochondria (Yago et al., 1972; Liu et al., 1977; Maeda,
1982; Betzold et al., 1992). Shen et al. (1989) showed that
the increase of the mitochondrial volume in alveolar type II
cells was accompanied by a great variance in their size and
distribution caused by irradiation following action of inhal-
ing 239PuO2. The total number of mitochondria also changed
 Z. Somosy / Micron 31 (2000) 165–181
dynamically in adrenal cortical cells, as reported by Yago et
al. (1972) in whole body X-ray irradiated rats. Vacuoliza-
tion and disruption of outer and inner membranes of mito-
chondria are also frequently observed upon irradiation in a
wide variety of cells (Hendee et al., 1963; Montgomery et
al., 1964; Jordan, 1967; René and Evans, 1970; Yago et al.,
1972; Shen et al., 1989; Kim and Shin, 1994). Radiation-
induced loss of mitochondrial matrix was observed in
mouse hepatocytes after receiving a 5.3 Gy dose of mixed
neutron–gamma irradiation (René and Evans, 1970)
Humoral factors, such as radiation-induced increase of
corticosterone secretion may also play a role in the struc-
tural and functional changes of mitochondria (Yago et al.,
1972).
3.1.4. Endoplasmic reticulum
As a rule, the effect of irradiation is manifested as the
dilatation, vesicularization and fragmentation of endoplas-
mic reticulum cisternae (Sobel, 1964; René and Evans,
1970; Conti et al., 1974; Hamberg et al., 1977; Skog et
al., 1983; Rosen et al., 1989). In addition, ionizing radia-
tion-induced degranulation of rER membranes is also a
well-known phenomenon in a wide variety of cells
(Cammarano et al., 1969; Unger and Hidvégi, 1971; Conti
et al., 1974; Mukerjee and Goldfeder, 1974; Skog et al.,
1983). The shift from membrane-bound ribosomes to free
forms was accompanied by an increase in the relative
number of polysomes 5 h after irradiation with 5 Gy, in S
and G1 phases of a synchronized Ehrlich ascites cell-line
(Skog et al., 1983). Chedid and Nair (1975) described the
development of large polysomal aggregates in rat hepato-
cytes upon prenatal X-irradiation at a 0.5 Gy dose.
3.1.5. Golgi apparatus
The Golgi apparatus is a specific intracellular membrane
system responsible for sorting, packaging and modification
of proteins synthesized in the rough endoplasmic reticulum,
as part of the secretory apparatus of the cell. Fragmentation
and rearrangement of the Golgi cisternae are commonly
observed in various cell types of upon irradiation (René
and Evans, 1970; Ostenda, 1973; Chedid and Nair, 1975;
Christozova et al., 1977; Hamberg et al., 1977; Liu et al.,
1977; Wattel et al., 1977; Somosy et al., 1991; Betzold et al.,
1992). This phenomenon may be accompanied by an
increase of fractional volume of the Golgi apparatus (Liu
et al., 1977) and perturbation of its functions (Kubasova et
al., 1975, 1976). According to our data, the disorganization
of Golgi architecture is accompanied by redistribution of the
protein p58 (it probably acts as microtubule-binding site on
the Golgi) and coat protein bCOP (it is localized on the
surface of tubulo-vesicular elements of the rough endoplas-
mic reticulum–Golgi interface as well as on the Golgi
membranes and it is involved in the traffic between these
compartments (Somosy et al., 1999b). The Golgi complexes
of the intact HT-29 and L928 cells investigated in this study
are situated at the periphery of the nucleus and consisted of
173
stacks of narrow and/or slightly dilated cisterns, surrounded
by small vesicles and vacuoles (Fig. 4a and c). After irradia-
tion, the Golgi apparatus breaks up into small vesicles,
which become scattered throughout the cytoplasm (Fig. 4b
and d). Accordingly, the bCOP protein which accumulates
around the nucleus of control cells, show weak diffuse stain-
ing in distant parts of the cell body of the exposed cells
(inserts of Fig. 4a and c). Irradiation (X-ray, 1–4 Gy), also
resulted in a changed staining pattern of the other Golgi
marker p58. In irradiated HT-29 cells this protein appears
as randomly distributed bright spots appeared in the
cytoplasm around the nucleus. In irradiated fibroblasts
(Fig. 4b insert), similar spots can also be observed in cyto-
plasmic protrusions of the cells (Fig. 4d insert). Our data
suggest that alteration of the Golgi complex may be
connected with the radiation-induced destruction of the
cytoskeletal system.
3.1.6. Lysosomes
Following ionizing radiation the number and the volume
fraction of lysosomes increase in the cells (Table 4) and
elevated lysosomal enzyme activity can be detected by
biochemical measurements (Brandes et al., 1967; Hamberg
et al., 1977; Hamberg, 1983; Piao et al., 1983). At the same
time, lysosomal enzymes may appear in the cytosol and in
the extracellular fluid (Brandes et al., 1967; Harris, 1970;
René et al., 1971; Conti et al., 1974; Snyder and Eklund,
1978). These data were interpreted in the framework of the
“enzyme release” hypothesis of post-radiational cell death
(Alexander and Bacq, 1961), which suggests that cell death
is a consequence of the unregulated release of digestive
enzymes from lysosomes after irradiation. This is may be
true in the case of radiation-induced necrosis.
Some of the observations suggesting increased lysosomal
enzyme activity in the irradiated cells are based on the fact
that the volume fraction of lysosomes/autophagic vacuoles
is increased in these cells. However, these data must be
interpreted with caution because the expansion of the lyso-
somal/autophagic compartment may be due to a decreased
rate of digestion of the segregated material, which may
these cause the overload and expansion of the lysosomal
compartment. In fact, in a comparative study we found
that the rate of protein degradation measured by the release
of amino acids from 14C pre-labelled proteins decreased in
irradiated HT-29 cells, as compared to controls. At the same
time, we found an increase in the volume fraction of lyso-
somal/autophagic vacuole compartment of these cells.
These data suggest that the expansion of lysosomal
compartment was due to the accumulation of undegraded
material as a consequence of the decreased rate of lysosomal
protein degradation in the irradiated cells (Somosy et al.,
1996). Other data suggest that cells such as macrophages
and glial cells may respond to irradiation by elevated pino-
cytotic and phagocytic activity (Ostenda, 1973; Hamberg et
al., 1974; Piao et al., 1983).
174 Z. Somosy / Micron 31 (2000) 165–181

Fig. 4. Morphology of the Golgi apparatus and distribution of bCOP in (a,c) control and (b,d) irradiated (a,b) HT-29 cells and (c,d) L929 fibroblast. The
irradiation induces moderate vacuolization and fragmentation of Golgi complex in the HT-29 cell, which is more pronounced in (arrow) L929 fibroblasts.
Perinuclear staining bCOP is seen in the control cells (a,c inserts). 4 h after 1 Gy dose of irradiation randomly arranged bright spots appear in the cytoplasm of
HT-29 cells (b insert), and in the cytoplasmic projections of irradiated fibroblasts (d, insert). Bars: (a–c), 0.5 mm; (d), 0.4 mm; insets, 2 mm.

3.2. Reversible forms of nuclear alteration in irradiated
cells
3.2.1. Nuclear swelling
Low doses of irradiation may induce a rapid and revers-
ible swelling of nuclei in a variety of cells, including Chang
liver cells (Montgomery et al., 1964), guinea pig gastric
parietal cells (Capoferro, 1973), Ehrlich ascites cells
(Skog et al., 1983), MXT mouse mammary carcinoma
cells (Gasperin et al., 1992) and human and mice lympho-
cytes (Anderson et al., 1975; Somosy et al., 1985b),
irradiated in vivo and in vitro. Cells with enlarged nuclei
appear within 30–60 min after irradiation and persist for
several days or weeks. The effective dose range is from
0.25 to 4 Gy (Capoferro, 1973; Anderson et al., 1975;
Somosy et al., 1985b).
3.2.2. Changes in the structure of chromatin and nucleolus
Several reports show that cells respond to low doses of
irradiation by marginal condensation of chromatin onto the
nuclear lamina (Jordan, 1967) and formation of large dense
chromatin clumps in the nuclear matrix (Klein-Szanto et al.,
 Z. Somosy / Micron 31 (2000) 165–181 175

Table 4
Ionizing radiation-induced alteration of autophagic vacuole/lysosomal compartments in various cells (compiled data according to Somosy et al. (1996))

Cell type Irradiation Compartments (increased in volume)

Rat lung X-ray Lysosomes a

Granular pneumocytes X-ray, 15, 20 Gy, 3–6 h Small autophagic vacuoles a
Membranous pneumocytes Autophag vacuoles, multivesicular bodies a
Endothelial cells Large autophagic vacuoles a
Rat alveolar macrophages Thermalized neutron Lysosomes b
Epithelium of duodenal crypt X-ray Lysosomes a
Mouse hepatocytes X-ray, mixed g–neutron Lysosomes, myelin figures a
131
Thyroid I Autophagic vacuoles a
Cultured neuroblastoma cells X-ray Autophagic vacuoles a; multivesicular bodies a;
heterophag vacuoles a
Mouse gland carcinomas X-ray Lysosome a
Oral epithelium (rat) X-ray, 50 Gy, 26–50 h Autophagic vacuoles a
Jejunum (Rhesus monkey) 32 MeV protons Giant lysosomes a
Rat dorsal ganglia neurons X-ray Autophagic vacuoles a
Pituitary adenomas Radiotherapy Autophagic vacuoles a
60
Hippocampus Co, 1 Gy prenatal irradiation Autophagic vacuoles a
Cultured BHK cells X-ray Autophagic vacuoles a
Chang liver cells X-ray or gamma-irradiation Autophagic vacuoles a; lysosomes a
Cultured KB cells X-ray Lysosomes a
HeLa cells X-ray Lysosomes a
Glial cells Gamma-rays Autophagic vacuoles a
Splenic macrophage from rat Gamma-rays Hetero- and autophagic vacuoles a
HT-29 cell X-ray Whole lysosome compartment b
Macrophages Incorporated 241Pu particles Autophagic vacuoles a
Cochlea of guinea pig Fast neutron Autophagic vacuoles a

a
Quantitative evaluation.
b
Qualitative evaluation.

1974; Barham and Walters, 1978; Skog et al., 1983; Somosy
et al., 1985a; Gasperin et al., 1992).
Low doses of irradiation are frequently followed by the
formation of the so-called nuclear bodies, which appear
ring-like chromatin aggregates surrounded by a less dense
halo (Klein-Szanto et al., 1974; Barham and Walters, 1978;
Orkisz and Bartel, 1981; Skog et al., 1983; Somosy et al.,
1985a). Their development may be accompanied by an
increase in the processing or transport of pre-mRNA and/
or pre-rRNA (Roth, 1995). The number of nucleoli and the
average volume of nucleolar organizer regions may increase
significantly upon irradiation, as reported by Schwint et al.
(1993); Morales et al. (1996). These phenomena may be
related to the radiation-induced elevation of trascriptional
activity of the nucleus. Irradiation may cause the formation
of patches of dense substances in the nucleoli (Mironescu
and Dragomir, 1967; Orkisz and Bartel, 1981). Nucleolar
segregation was also observed in irradiated cells (Klein-
Szanto et al., 1974; Skog et al., 1983; Somosy et al., 1985a).
3.2.3. Chromosome aberrations
Ionizing radiation produces many types of DNA lesion,
including DNA base alterations, DNA–DNA cross-links,
and single-and double-strand breaks (Schulte-Frohlinde
and Bothe, 1991; Lett, 1992). Gaps and breaks within the
chromatid strands and chromosomes are the most frequently
observed radiation-induced chromosomal lesions (Evans,
1962; Yu, 1971; Brecher, 1977). Combined light and elec-
tron microscopic studies by several authors (Humphrey and
Brinkley 1969; Brinkley and Hittelman, 1975; Brecher,
1977) revealed that radiation-induced gap-formation were
a result of the physical loss of DNA–protein complexes
rather than decondensation of the chromatin. Chromosome
abnormalities, such as translocations, fragile tips and dele-
tions were detected by high resolution scanning electron
microscopy in canine chromosomes after whole-body irra-
diation (Niiro and Seed, 1988). Several studies on homo-
logous chromosomes in the prophase of the first meiotic
division showed the presence of breaks and rearrangements
of synaptonemal complexes in irradiated cells (Backer et al.,
1991; Allen et al., 1994; Johannisson et al., 1994). The
ultraviolet radiation, especially UV-B absorbed by nucleic
acids may also cause breaks or perturbation of the molecular
structures of nucleic acids, manifested as chromosome aber-
rations (Shimmura and Tsubota, 1997; Caricchio et al.,
1998; Hollósy, 1999).
A marked increase in the frequency of chromosome aber-
rations and formation of micronuclei was also observed in
human blood lymphocytes upon 2450 MHz microwave
exposure (Maes et al., 1993). This cytogenetical effect
seems to be dependent on the frequency used, because it
was absent in cells exposed to 935.2 MHz microwave irra-
diation (Maes et al., 1997).
These lesions can be caused directly by radiation energy
176 Z. Somosy / Micron 31 (2000) 165–181
and they can develop as a consequence of radiation induced
genomic instability (Kadhim et al., 1995; Morgan et al.,
1996) in the surviving cells. Measurement of chromosome
aberrations is an informative and widely used technique for
studying the genetic risk of ionizing radiation and is a useful
biological indicator of radiation exposure.
3.2.4. Changes in nuclear envelope
The nucleo-cytoplasmic compartmentation is maintained
by the nuclear envelope, which is formed by an inner and an
outer nuclear membrane that are periodically joined to the
nuclear pore complexes and the internal nuclear lamina. The
nuclear membranes are generally considered to be the prin-
cipal targets of radiation (Alper, 1971; Sato et al., 1975;
McClain et al., 1990). Sato et al. (1975) observed radia-
tion-induced alteration of the net negative charge of nuclear
membranes, determined by electrophoretic mobility assay.
McClain et al. (1990) found dose-dependent differences in
the membrane fluidity between irradiated and non-irradiated
nuclear membranes. Doses from 1.25 to 7.5 Gy produced a
dose-dependent increase of membrane fluidity, lasting up to
15 h in the MOLT-4 cells. Dilation of the perinuclear space
has been observed in a wide variety of cells following differ-
ent types of irradiation (Montgomery et al., 1964; Hurwitz
and Tolmach, 1969; Djaczenko et al., 1973; Liu et al., 1977;
Barham and Walters, 1978; Kubasova et al., 1984; Somosy
et al., 1991). Szekely and Copps (1976) observed a
pronounced dose-dependent decline in the nuclear pore
number in irradiated HeLa and CHO cells and in regenerat-
ing rat liver by using freeze-fracture method.
3.2.5. Micronucleated cells
The micronuclei are formed from chromosome fragments
and whole chromosomes and are found in the cytoplasm of
cells subjected to physical or chemical treatments which
destruct DNA or mitotic spindle apparatus (Geraud et al.,
1989; Müller et al., 1995; Huber et al., 1996).
Elevation of the number of micronucleated cells is
frequently observed in cell cultures exposed to ionizing
radiation (Heddle, 1973; Almássy et al., 1987; Geraud et
al., 1989; Cornforth and Goodwin 1991; Müller et al.,
1995). The appearance of micronuclei was also observed
in UV-B irradiated cells (Weller et al., 1996). These authors
found that caffeine potentate the induction of micronuclei
by UV-B, however, this drug did not influence the frequency
of micronuclear formation after gamma irradiation. Data
about the effects of EMF exposure on micronuclei are
conflicting. Scarfi et al. (1991) showed that the formation
of micronuclei in human lymphocytes was not affected by
exposure to a pulsed magnetic field of 2.5 mT (peak pulse)
at 50 Hz and this field did not influence mitomycin
C-induced micronucleus formation. This finding was
consistent with that of a previous study from the same
laboratory (Cossarizza et al., 1989), in which the same
pulsed magnetic field did not produce a change in cell survi-
val or unscheduled DNA synthesis in human lymphocytes,
with or without additional treatment with ionizing radiation.
Tofani et al. (1995) reported a synergistic effect on micro-
nucleus formation in human peripheral lymphocytes after
concurrent exposure to mitomycin C and EMF (32 Hz,
75 mT AC field with a 42 mT static field). In these studies,
neither a 75 nor a 150 mT AC field affected micronucleus
formation in the absence of mitomycin C or an applied static
magnetic field. Lagroye and Poncy (1997) observed no
change in micronucleus formation in a spontaneously trans-
formed tracheal epithelial cell line exposed to EMF alone
(50 Hz, 100 mT, sinusoidal), but when the cells were
exposed to EMF plus 6 Gy of ionizing (gamma) radiation,
the number of binucleated cells containing micronuclei
increased by approximately 10% …p , 0:05†: Simkó et al.
(1998) examined micronucleus formation in two human cell
lines exposed to 0.1–1.0 mT 50 Hz AC magnetic fields. In
the SCLII transformed squamous-cell line, a dose-depen-
dent increase of the number of micronuclei was seen after
48 and 72 h continuous exposure to 50 Hz (0.8 and 1.0 mT).
Monitoring of micronuclei is a simple and useful cyto-
genetic technique for quantitative analysis of chromosomal
lesions induced by ionizing radiation or other genotoxic
agents on different cell types (Heddle, 1973; Müller et al.,
1995; Almássy et al., 1987).
4. Concluding remarks
Data reviewed here indicate that the cellular responses to
various forms of radiation, including ionizing and UV irra-
diation and exposure to low-frequency electromagnetic
fields have many common elements. They are not strictly
specific and may be best considered as general stress
responses similar to those observed after application of
various injurious agents and treatments of the cells.
Development of common endpoints such as apoptosis,
may be caused by diverse initial injurious events, e.g. by
direct destruction of DNA, altered signal transduction
(Ojeda et al., 1994, 1995; Blank et al., 1997; Caricchio et
al., 1998; Khodarev et al., 1998; Meng et al., 1998), and
radiation-induced genetical instability (Kadhim et al.,
1995). In addition to the listed biological indicators of radia-
tion exposure (micronucleus test, cytogenetical studies) the
qualitative and quantitative evaluation of different morpho-
logic changes developing in the irradiated cells has great
importance in radiobiology and in the management of
radiation exposition accidents. Measurement of different
morphologic parameters is a useful tool to characterize the
sensitivity of tissues to radiation injury and dependence of
histological/ultrastructural alteration Several approaches
were proposed to fulfil this task (Eriksson et al., 1982;
Carr et al., 1996; Langberg et al., 1996; Rubio and Jalnäs
1996). According to Carr’s procedure (Carr et al., 1996), the
volume of various cell types, submucosal arterioles, outer
and inner muscle nuclei, Auerbach’s and Meissner’s nerve
plexuses, villi, and crypts are measured and the mitotic
 Z. Somosy / Micron 31 (2000) 165–181
figures are counted and the structure of villi and organiza-
tion of various cell organelles are evaluated by electron
microscopy. Rubio and Jalnäs (1996) used another evalua-
tion system which takes into consideration cell necrosis,
loss of granulation of cells, mucosal ulceration, changes
of lymphocyte margination, collagen content, ectopic
glands, capillary congestion and morphology of altered
cells. Langberg et al. (1996) have proposed a protocol for
the characterization of fibrosis.
We suggest, that additional methods such as immuno-
histochemical detection of various proteins, specific
markers for cell organelles and cytoskeleton, and inspection
of the distribution of cell surface charged sites and different
membrane domains, application of tracer substances and
other cell or molecular biological probe, may be included
into generalized protocols for evaluation of cellular altera-
tions induced by radiation.
Acknowledgements
The author gratefully acknowledges the interest and
support of Prof. Dr G.J. Köteles (Director of the National
“Frédéric Joliot-Curie” Research Institute for Radiobiology
and Radiohygiene) and Prof. Dr J. Kovács (Department of
General Zoology of Eötvös Lóránd University, Budapest).
This work was partially supported by the Hungarian Minis-
try of Health ETT Grant no. 060/96.
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