[CANCER RESEARCH 41, 2103-2108, June 1981]
0008-5472/81 /0041-OOOOS02.00
Effects of Protease Inhibitors on Radiation Transformation in Vitro1
Ann R. Kennedy2 and John B. Little
Laboratory of Radiobiology, Harvard University School of Public Health. Boston, Massachusetts 02115
ABSTRACT
We have investigated the effects of three protease inhibitors,
antipain, leupeptin, and soybean trypsin inhibitor, on the induc
tion of oncogenic transformation in mouse C3H10T'/2 cells by
X-rays. The patterns of inhibition by the three protease inhibi
tors were different. Antipain was the most effective, having the
ability to suppress completely radiation transformation as well
as radiation transformation enhanced by the phorbol ester
promoting agent 12-O-tetradecanoylphorbol-13-acetate. The
fact that antipain could suppress transformation when present
for only 1 day following irradiation suggests that an effect on
a DNA repair process might be important in its action. Leupep
tin was less effective than antipain in its inhibition of radiation
transformation. Soybean trypsin inhibitor suppressed only the
promotional effects of 12-O-tetradecanoylphorbol-13-acetate
on transformation. Our results suggest that there may be more
than one protease involved in carcinogenesis.
INTRODUCTION
In an attempt to gain more information about the mechanisms
of carcinogenesis, we have been studying the effects of various
agents on radiation transformation in vitro. It has been shown
previously that the development of malignant transformation in
mammalian cells irradiated in vitro can be thought of as involv
ing at least 2 steps: (a) the induction and fixation of the
transformed state as a heritable cellular property; and (b) its
subsequent expression in terms of morphologically altered
cells (14). We have shown previously that incubation with a
nontoxic concentration of TPA3 during the expression period
will greatly enhance X-ray transformation in mouse C3H10T1/2
cells (9, 10) as it has been shown to enhance tumor formation
in vivo in "2-stage" (initiation-promotion) carcinogenesis ex
periments (5).
Our interest in the effects of protease inhibitors on radiation
transformation was stimulated by the reports that some of these
agents could inhibit error-prone DNA repair and mutagenesis
in bacteria (16, 30) as well as inhibit TPA-enhanced carcino
genesis in vivo (6, 26). Thus, protease inhibitors might influence
both the fixation and expression steps in in vitro transformation.
It is our hypothesis that much of the transformation observed
in rodent cell lines in culture may result from the action of an
error-prone DNA repair process such as has been shown to
exist in bacterial cells. Supportive evidence for such a mech
anism in 1OT'/2 cells was found in previous experiments (14,
24).
We have investigated the effects of 3 protease inhibitors,
antipain, leupeptin, and SBTI, which specifically inhibit different
' This research was supported by NIH Grants CA-22704 and ES-00002.
2To whom requests for reprints should be addressed.
3 The abbreviations used are: TPA, 12-O-tetradecanoylphorbol-13-acetate;
SBTI, soybean trypsin inhibitor.
Received January 29, 1980; accepted February 25, 1981.
proteolytic enzymes. The enzymes known to be inhibited by
each agent include: antipain-papain, trypsin, thrombokinase,
cathepsin A and B, plasmin, and plasminogen activator (1, 33);
leupeptin-papain, trypsin, plasmin, cathepsin B, and plasmin
ogen activator (1, 33); and SBTI-trypsin, chymotrypsin, throm-
oplastin, plasmin, and elastase (11, 13). SBTI is of particular
interest, as it is a naturally occurring protease inhibitor found
in the normal diet. It may thus play a role in the prevention of
cancer in humans (29). It has been found recently that carci
nogenesis in 3 organ systems can be inhibited in animals kept
on a soybean diet rich in protease inhibitors (29).
Antipain and leupeptin are small-molecular-weight (M.W.
approximately 500 to 600) natural products isolated from ac-
tinomycetes. They have been characterized by Aoyagi and
Umezawa (1 ). Effective concentrations of these 2 inhibitors are
nontoxic, either with or without radiation exposure, and have
been shown to have no effect on growth, RNA, or protein
synthesis in bacteria (16) or mammalian cells (3, 7, 31). SBTI
is a high-molecular-weight (M.W. approximately 24,000) mac-
romolecular-type protease inhibitor (11 ), which is also nontoxic
to C3H10TV2 cells at the concentrations used. We report here
the effects of protease inhibitors, added at different times in
radiation transformation experiments with and without promo
tion induced by TPA. A preliminary report of our results has
been published (8).
MATERIALS AND METHODS
We used a C3H mouse embryo-derived cell line (1 OTVzclone
8) isolated and characterized by Reznikoff ef al. (21, 22) and
adapted for studies of radiation transformation (14, 24, 25).
Stock cultures were maintained in 60-mm Petri dishes and
were passaged by subculturing at a 1:20 dilution every 7 days.
The cells used were in passages 9 to 14. They were grown in
a humidified 5% CO2 atmosphere at 37° in Eagle's basal
medium supplemented with 10% heat-inactivated fetal calf
serum and antibiotics. Cells were irradiated 24 hr after seeding
and incubated in fresh medium containing the protease inhibi
tors. When the cells reached confluence, the serum concentra
tion in the medium was changed to 5% for the duration of the
transformation assay.
Irradiation was carried out at room temperature with a 100-
kV constant potential Philips industrial X-ray generator oper
ating at 10 ma and yielding a dose rate to the cells of 78 rads/
min. There were 100 to 400 viable cells/dish; plating efficien
cies were determined from plates seeded with a cell density
one-fifth that of the plates for the transformation assay and
terminated 10 days after irradiation. Type II and III foci were
scored as transformants. Details of radiation transformation
experiments have been described previously (25).
TPA treatment at 0.1 jug/ml was begun 48 hr after irradiation
and maintained for the entire 6-week expression period as
described previously (9, 10), TPA, Lot Nos. 007 and 016, was
obtained from Consolidated Midland Co., Brewster, N. Y. Pro-
JUNE 1981
2103
Research.
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