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Toxic. in Vitro Vol. 8, No. 4, pp. 609-61 I, 1994
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IN VITRO EFFECTS OF THALLIUM ON MOUSE
NEUROBLASTOMA CELLS
G. REPETTO*, P. SANZ and M. REPETTO
National Institute of Toxicology, PO Box 863. 41080--Sevilla, Spain
Abstract--To compare the effects of thallium at different cellular levels, cultured mouse neuroblastoma
cells (Neuro-2A) were exposed for 24 hr to thallium(I) acetate. The following toxic indicators were assessed
in the in vitro test system: cell proliferation by quantification of total protein content of the culture;
cytoplasmic membrane integrity to cytosolic lactate dehydrogenase (LDH) leakage; lysosomal hexosamin-
idase release; lactate dehydrogenase activity; mitochondrial succinate dehydrogenase activity; relative
neutral red uptake by lysosomes; lysosomal hexosaminidase sphingolipid degradation activity; acetylchol-
inesterase activity. The effects of thallium on the various indicators differed. Neural acetylcholinesterase
activity was extremely sensitive to TI inhibition. In contrast, hexosaminidase, an enzyme involved in
glycosphingolipid degradation, was stimulated prior to cytoplasmic membrane disruption detected as
LDH leakage. Relative neutral red uptake was slightly more sensitive than cell growth inhibition and the
reduction in hexosaminidase release suggests an interaction with lysosomes. The low degree of sensitivity
of cell proliferation, as judged by the protein content of the cultures, may reflect inhibition of protein
degradation. LDH glycolytic activity was severely inhibited, but succinate dehydrogenase activity in the
citric acid cycle was increased, probably owing to the mitochondrial accumulation of thallium.
INTRODUCTION
The aim of this study was to compare the effects of
thallium on mouse neuroblastoma cells at different
cellular levels, including cell proliferation, cyto-
plasmic membrane permeability, metabolism,
lysosomal and mitochondrial functions and acetyl-
cholinesterase activity. Thallium is the most highly
toxic cumulative cation (Venugopal and Luckey,
1978). Despite legal restrictions on the use of thal-
lium-based rodenticides, its use has been increasing in
recent years because of growing resistance to the less
toxic dicoumarol-based products. In addition, thal-
lium has been found to be a useful biochemical tool
(Douglas et al., 1990). Thallotoxicosis still occurs
worldwide, therefore, and remains one of the most
frequently occurring types of acute toxicity caused by
any metal. Concern has also been recently expressed
over the chronic consequences of excessive thallium
release into areas surrounding cement plants (Manzo
and Sabbioni, 1988).
Thallium produces a distal (dying back type) and
predominantly sensory, rapidly progressive neuropa-
thy, with some involvement of the central nervous
system. There is considerable evidence to suggest that
the intracellular accumulation of thallium in nervous
tissue is associated with alterations in biochemical
*To whom correspondence should be addressed.
Abbreviations: AChE = acetylcholinesterase; ECs0= med-
ian effective concentration; HEX=hexosaminidase;
LDH = lactate dehydrogenase; RNRU = relative neu-
tral red uptake; SDH = succinate dehydrogenase.
activities related to transmembrane ion transport,
protein metabolism and energy-producing reactions,
because of its tendency to form insoluble complexes
with riboflavin. However, the precise mechanism of
action is not well understood (Manzo and Sabbioni,
1988).
MATERIALS AND METHODS
Neuro-2A cells were plated at a density of 10,000
cells per well in 96-well tissue culture plates. After
24 hr, the culture medium was replaced with 0.2 ml
medium containing thallium(I) acetate in solution (0,
0.1, l, 10, 100 and 1000 mg/litre) and incubated for
another 24 hr. Cytotoxic determinations were carried
out in the same 96-well tissue culture plates in which
exposure took place, as previously described (Repetto
et al., 1993). Cell proliferation, as judged by total
cellular protein, was quantified in situ using
Coomassie Brilliant Blue G-250 as previously de-
scribed (Repetto and Sanz, 1993). Other indicators
studied were LDH (EC 1.1.1.27) activity and leakage
to the medium; hexosaminidase (HEX, N-acetyl-fl-o-
hexosaminidase, EC 3.2.1.30) activity and release;
relative neutral red uptake (RNRU) (Repetto and
Sanz, 1993); succinate dehydrogenase (SDH, EC
1.3.99.1) activity in intact cells, determined by adding
1 mM KCN and antimycin A to the tetrazolium salt
incubation medium in order to inhibit other dehydro-
genases; acetylcholinesterase (ACHE, acetylcholine
acetylhydrolase, EC 3.1.1.7) activity was quantified
on intact cells (Repetto et al., 1994).
609