(CANCER RESEARCH 43, 5718-5724, December 1983]
Effects of Dimethyl Sulfoxide and Thiourea upon Intercalator-induced
DMA Single-Strand Breaks in Mouse Leukemia (L1210) Cells
Yves Pommier,1 Leonard A. Zwelling, Michael R. Mattern, Leonard C. Erickson, Donna Kerrigan,
Ronald Schwartz, and Kurt W. Kohn
Laboratory of Molecular Pharmacology. Developmental Therapeutics Program, Division of Cancer Treatment, National Cancer Institute, NIH, Bethesda. Maryland 20205
ABSTRACT
The free radical scavengers, dimethyl sulfoxide (MezSO) and
thiourea, were used to assess the role of free radicals in the
production of intercalator-induced DNA breaks and cytotoxicity
in mouse leukemia L1210 cells. Both agents decreased X-ray
break production, and this decrease was comparable in magni
tude to the degree of inhibition of X-ray-induced cell killing. By
contrast, Me2SO increased the DNA breaks produced by the
intercalators, Adriamycin, 5-iminodaunorubicin, and 4'-(9-acridi-
nylamino)methanesulforHn-anisidide. This was not due to an
enhancement of Adriamycin or 4'-(9-acridinylamino)methane-
sulfon-m-anisidide uptake by Me2SO. Strand break production
by intercalators was decreased by thiourea. This was not due to
an inactivation of the intercalators or to a decrease of Adriamycin
or 4'-{9-acridinylamino)methanesulfon-/n-anisidide uptake by thi
ourea. Experiments using nudeokJ sedimentation to assess the
DNA linking number and domain size from cells treated with
Me2SO and thiourea indicated that these chemicals alter chro-
matin structure in a fashion which may account for effects on
intercalator-induced DNA scission. The alterations in intercalator-
induced DNA scission were not accompanied by corresponding
alterations in cytotoxicity, thus dissociating intercalator-induced
strand break production from lethality and the mechanism of X-
ray break production.
INTRODUCTION
A variety of DNA intercalating agents cause single- and double-
strand DNA scission in mammalian cells (25-27, 33-37). This
DNA scission differs from the DNA breakage produced by other
DNA damaging agents in several respects, (a) The intercalator-
induced DNA breaks are associated with an approximately stoi-
chiometric amount of covalently bound protein which dissociates
at the same time the breaks are reseated (27, 36). (b) The
formation of the DNA breaks is saturable and is inhibited at low
temperature but wilt occur subsequently in the presence of drug
when the temperature is raised (36). (c) The formation and
resealing of the breaks is not accompanied by stimulation of
poly(adenosine diphosphoribose) synthesis (35). (d) The break
resealing can occur in isolated nuclei and permeabilized cells in
the absence of nucleoside triphosphates (24, 35). These findings
taken together suggest a mechanism of DNA scission coordi
nated with protein-DNA binding having its origins in an enzyme
constituent of the cell nucleus, perhaps a topoisomerase (27,
36).
Some DNA damaging agents, such as ionizing radiation and
bleomycin, generate free radical species which produce DNA
breaks (5, 6), and it has been proposed that some intercalating
agents also break DNA by a free radical mechanism. In particular,
ADM2 can generate free radicals during NADPH and O2 reaction
with reducÃ-aseenzymes (2, 3, 14), and DNA strand breaks can
be generated by this mechanism (4).
Free radical formation depends on reductive reactions which
are most likely to occur in those intercalating agents, incuding
ADM, which contain quinone groups. However, several interca
lating agents, such as ellipticine, 2-Me-9-OH-E+, 5-ID, or m-
AMSA, do not contain quinone groups and exhibit relatively little
free radical production (19, 23) yet still stimulate the formation
of protein-associated DNA strand breaks in cells (27,33,36,37).
Thus, intercalating agents could produce DNA strand breaks by
2 distinct mechanisms, but it is not dear whether the free radical
mechanism may make an appreciable contribution in living cells.
Therefore, we investigated the effects of the free radical
scavengers, Me2SO and thiourea, on intercalator-induced DNA
breakage and cytotoxicity. These compounds reduce the extent
of DNA breakage in cells exposed to ionizing radiation or hydro
gen peroxide (5, 22). In the course of these experiments, we
found unexpectedly that Me2SO actually increased the interca
lator-induced DNA breakage. We propose that this phenomenon
may involve an effect on chromatin structure.
MATERIALS AND METHODS
Materials. [2-'4C]Thymidine (58 mCi/mmol) and [mef/jy/-3H]thymidine
(20 Ci/mmol) were purchased from New England Nuclear, Boston, Mass.
MejSO and thiourea were purchased from Fisher Scientific Co., Fairtawn,
N. J. and from Eastman Organic Chemicals, Rochester, N. Y., respec
tively. ADM (NSC 123127) and m-AMSA (NSC 249992) were obtained
from the Drug Synthesis and Chemistry Branch, Division of Cancer
Treatment, National Cancer Institute; m-AMSA was dissolved in 100%
M62SO at 10 mM, and ADM was dissolved in glass distilled water at 1
mg/ml. 5-ID (NSC 254681) was a gift from Dr. Robert I. Glazer, Applied
Pharmacology Section, Laboratory of Medical Chemistry and Biology,
National Cancer Institute, who obtained the compound from Dr. E. Acton,
Stanford Research Institute. 5-ID was dissolved in glass distilled water
at 1 mM. 2-Me-9-OH-E+ was a gift from Dr. J. B. Le Pecq, Laboratoire
de Pharmacologie Moléculaireau Centre National de la Recherche Scien
tifique, Institut Gustave-Roussy, Villejuif, France, and was dissolved in
glass distilled water at 8.25 mw. [14C]m-AMSA (19.6 mCi/mmol) and
[MC]ADM (17.2 mCi/mmol) were synthesized by SRI International, Menlo
Park, Calif., and were obtained through the Chemical Resources Section,
National Cancer Institute. [14C]m-AMSA and [14C]ADM were dissolved
in 100% Me2SO and in glass-distilled water, respectively. ADM, 5-ID, m-
1To whom requests for reprints should be addressed, at Building 37, Room
5D17, 9000 Rockvilte Pike, Bethesda, Md. 20205.
Received May 26,1983; accepted August 25,1983.
2The abbreviations used are: ADM, Adriamycin; 2-Me-9-OH-E+, 2-methyl-9-
hydroxyellipticinium; 5-ID, 5-iminodaunorubicin; m-AMSA, 4'-(9-acridinylam-
ino)methanesulfon-m-aniskJ"tde; Me^O, dimethyl sulfoxide; [14C]m-AMSA, 4'-(9-
acridinyl-[9-'4C]amino)methanesulfon-m-anisidide; [14C]ADM, Adriamycin hydro-
chloride-(14-"C]; RPMI 1630, Roswell Park Memorial Institute tissue culture Me
dium 1630; DPC, DNA-protein cross-links; SSB, single-strand breaks; SDS, sodium
dodecyl sulfate.
5718 CANCER RESEARCH VOL. 43
Research.
on November 27, 2021. © 1983 American Association for Cancer cancerres.aacrjournals.org Downloaded from