[CANCER RESEARCH 41, 3840-3843, October 1981]
0008-5472/81 /0041-OOOOS02.00
Reversal of Resistance to Methotrexate by Hyperthermia in Chinese
Hamster Ovary Cells1
Terence S. Herman, Anne E. Cress, Cynthia Sweets, and Eugene W. Gerner
Departments of Internal Medicine [T. S. H., C. S.], and Radiology [A. E. C., E. W. G.], University oÃ-Arizona College of Medicine, Tucson, Arizona 85724
ABSTRACT
Our Chinese hamster ovary cells are extremely resistant to
methotrexate (MIX) (100% survival after 500 /ig/ml for 13 hr).
However, exposure to 43° (but not 41° or 42°) for 1 hr
sensitizes the cells to MIX so that a 50% cell kill in excess of
that due to hyperthermia occurs. Treatment of cells at 43°
increases net MIX uptake by about 30% at 30 min but causes
a substantial reduction after 1 hr. This negative effect is greater
in cells continually heated at 43° than in those exposed for
only 1 hr. Treatment at 43°for 1 hr also markedly increases
efflux of MTX out of cells over the first 2 hr. Dihydrofolate
reducÃ-ase activity was found to decrease to about 50% of
control values by 4 to 5 hr after exposure to 43°.The biological
half-life of dihydrofolate reductase in Chinese hamster ovary
cells was determined to be about 4.5 hr, indicating that hyper-
thermia-induced cessation of protein synthesis may explain
both the decrease in dihydrofolate reductase activity and the
sensitization to MTX observed with heat exposure. In sched
uling experiments, lethality due to exposure to 43°for 1 hr in
conjunction with MTX was maximum when 1-hr drug exposure
began just at the end of heat treatment.
INTRODUCTION
There is now considerable clinical interest in the treatment
of cancer with a combination of chemotherapeutic drugs and
hyperthermia (9,13). In general, however, early clinical results
have been less than outstanding when patient morbidity and
the difficulties in delivering the hyperthermia (at least whole
body) are considered (4, 16, 19). In vitro and in vivo studies
conducted in this laboratory and others (9,17) have suggested
that the scheduling of chemotherapeutic drugs with heating
may be critical to maximization of cellular lethality. Better
clinical results might be anticipated if these factors were un
derstood. Because other studies had shown that exposure to
temperatures greater than 43°could transiently shut off protein
synthesis, causing significant decreases in the levels of impor
tant intracellular enzymes (8, 10), we chose to investigate the
interaction between exposure of cells to hyperthermia and
MTX,2 since MTX acts by inhibiting one such enzyme, DHFR
(1 ). Our strain of CHO cells proved an excellent model because
it is resistant to MTX due to high levels of this enzyme (11 ). We
further attempted to define the best scheduling of this drug
with heat to better plan for eventual clinical application.
MATERIALS AND METHODS
Method of Cell Culture. CHO cells, originally obtained in 1974 from
' Supported in part by Grants CA 26220 and CA 17343 and in part by
Research Advisory Group, Veterans Administration, Tucson, Ariz. 85723.
2 The abbreviations used are: MTX, methotrexate; DHFR, dihydrofolate reduc
tase: CHO, Chinese hamster ovary.
Received October 23. 1980; accepted June 29. 1981.
Dr. Ronald M. Humphrey, University of Texas Cancer Center, M D.
Anderson Hospital, Houston, Texas, and RT9 cells, originally obtained
in 1975 from Dr. Kenneth Wheeler, University of Rochester, Rochester,
N. Y., were both grown in McCoys' Medium 5A supplemented with
20% (v/v) fetal calf serum, penicillin (11 units/ml), streptomycin (100
fig/ml), and Fungizone (0.25 /ig/ml) (all from Grand Island Biological
Co., Grand Island, N. Y.). Cells were maintained in logarithmic growth
phase at 37°in a 5% CO?-95% air atmosphere. Doubling time was 13
to 14 hr for the CHO cells and 15 to 16 hr for the RT9 cells. Cell
numbers were determined with an electronic particle counter (Coulter
Electronics, Hialeah, Fla.). Cells were replated approximately 12 hr
before experimental manipulation.
Cell Viability Measurements. Cell viability was measured by the
ability of single cells to form colonies in vitro. For this assay, known
numbers of cells were plated in plastic Falcon No. 3002 Petri dishes
(Falcon Plastics, Oxnard, Calif.) containing 5 ml of fresh medium. Three
dilutions of the known cell number were made for each drug concen
tration, and each was plated in triplicate. After incubation for 7 to 8
days, colonies were fixed and stained with 0.5% crystal violet (Fisher
Scientific Co., Fair Lawn, N. J.) in 95% ethanol. Viable cells were those
that produced colonies of more than 50 cells upon examination under
a dissecting microscope. The plating efficiencies of control cultures of
CHO cells were between 80 and 90%. The results from colony forma
tion experiments, described in Charts 1 and 6, represent 3 to 5
replicate experiments per data point.
Heat Treatments. Exponentially growing cells were grown in T2S
flasks (Falcon Plastics). Flasks were then immersed in a specially
designed plexiglass water tank with continuous flow of heated water
for a Haake Model FK water circulator (temperature variability, ±0.1")
(Haake, Inc., Saddle Brook, N. J.). Five ml of fresh media or media
plus drug were added directly prior to heating. Thermometry was
accomplished with mercury and glass thermometers calibrated by the
method of Cetas and Conner (6).
Drug Treatments. Exponentialiy growing cells were exposed to
varying concentrations of MTX (Lederle Laboratories, Pearl River,
N. Y.) in 60-mm Petri dishes for 1 hr at 37°, or in T25 flasks as above
at 41 °,42°,or 43°.Drug solutions were always prepared immediately
prior to use by dissolving the drug in sterile water. Appropriate dilutions
of drugs were added to fresh medium, with the volume of drug solution
never exceeding 20% (1 ml) of the total volume of 5 ml. After treatment,
the medium was removed, and the cultures were washed twice with
warmed Puck's Saline A (Grand Island Biological Co.) and trypsinized
(0.05% for 2 to 3 min). Following this, known numbers of cells were
plated into plastic Petri dishes for colony growth as described above.
Measurement of DHFR. The activity of DHFR was measured by the
method of Mathews and Huennekens (18). Twenty million cells were
used for each determination. CHO and RT9 cells were removed from
monolayer cultures by scraping with a rubber policeman. These cells
were suspended (1 .Ox 10' cells/ml) in 0.1 M Tris HCI buffer, pH 7.4,
and were disrupted by sonication (E/MC Corp. ultrasonic cell disruptor;
4.5-in probe, 20-sec pulse). The resulting cell homogenate was cen-
trifuged at 12,000 x g for 10 min. The pellet was discarded, and the
supernatant extract was placed on ice. The reaction mixture included
40 mM potassium phosphate (pH 7.4), 8 rriM 2-mercaptoethanol, 0.08
HIMdihydrofolate, 0.08 rnw NADPH, and 0.20 ml of sample supernatant
in a total volume of 1.00 ml. DHFR activity was then determined at 37°
by measuring the decrease in absorbance at 340 nm of the solution as
3840 CANCER RESEARCH VOL. 41
Research.
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