[CANCER RESEARCH 48, 1798-1802, April 1, 1988]
Potential Intracellular Target Proteins of the Anticarcinogenic Bowman Birk
Protease Inhibitor Identified by Affinity Chromatograph}1
Paul C. Billings, William St. Clair, Albert J. Owen,2 and Ann R. Kennedy
Department of Cancer Biology, Harvard School of Public Health, Boston, Massachusetts 021 IS
ABSTRACT
The soybean-derived Bowman Birk inhibitor (BBI) has been shown to
inhibit carcinogenesis in both in vitro and in vivo model systems. In the
present study, we have utilized a BBI affinity column to determine
whether cellular enzymes, present in C3H/10T'/2 cells, specifically inter
act with this inhibitor. Using this technique, we have identified three
proteins with masses of about 70, 60, and 50 kilodaltons. Cell fractiona-
tion experiments demonstrate that the 60- and 50-kilodalton proteins are
present in the 10,000 x g pellet (lysosomal/golgi fraction) of C3H/10T'/2
cell homogenates. We have also identified two proteins with masses of
60 and SO kilodaltons which bind to the BBI affinity column in fibroblasts
from patients having Bloom syndrome. BBI as well as several other
protease inhibitors has been shown previously to reduce the frequency of
spontaneous chromosomal aberrations in these cells. Our results indicate
that the 50- and 60-kilodalton proteins we have identified by affinity
Chromatograph) are present in both mouse and human cells and further
suggest that these proteins are potential intracellular targets of the BBI
in these cells.
INTRODUCTION
Protease inhibitors are effective suppressors of carcinogenesis
i/i vivo and carcinogen-induced transformation in vitro (1-8).
Although much is known about the specific types of protease
inhibitors which are potent suppressors of carcinogenesis, rel
atively little is known about the precise mechanism(s) by which
these compounds exert their anticarcinogenic effects. We hy
pothesize that protease inhibitors exert their anticarcinogenic
effects by inhibiting cellular enzymes involved in the induction
and/or expression of the transformed phenotype. Our labora
tory has studied the anticarcinogenic activity of the soybean-
derived protease BBI3 both in vivo and in vitro (5, 7, 8). The
BBI is an 8000-dalton protein which effectively inhibits both
trypsin and chymotrypsin (9). This inhibitor has been shown
to suppress dimethylhydrazine-induced colon carcinogenesis
in mice when present in the diet (7) and dimethyl-
benz(a)anthracene-induced cheek pouch carcinogenesis when
topically applied (5). Additionally, BBI has been shown to
suppress radiation-induced transformation of C3H/10T'/2 cells
at nanomolar concentrations (8).
BS is an autosotnal recessive genetic disease characterized by
high levels of chromosomal aberrations and sister chromatid
exchanges which are thought to predispose affected individuals
to a higher than normal incidence of cancer (10).
We have demonstrated that the BBI, as well as several other
protease inhibitors, will reduce the frequency of chromosomal
abnormalities in BS cells when the cells are grown in the
presence of the inhibitor (11). Therefore, protease inhibitors
have been shown to suppress specific chromosomal abnormal-
Received8/24/87;revised12/15/87;accepted12/31/87.
The costs of publication of this article were defrayed in part by the payment
of page charges. This article must therefore be hereby marked advertisement in
accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
1Supported by NIH Grants CA45734, CA40214, CA22704, and ES00002.
1 Present address: Department of Nutrition, Harvard School of Public Health,
Boston, M A 02 US.
3 The abbreviations used are: BBI, Bowman Birk inhibitor, BS, Bloom syn
drome; DFP, diisopropylfluorophosphate; FITC, fluorescein isothiocyanate; kDa,
kilodaltons; MCA, methylcholanthrene.
¡tieswhich are thought to be involved in human cancer devel
opment.
Previously, defined substrates have been used to identify two
enzymatic activities in C3H/10T'/2 cells which are inhibited by
several protease inhibitors processing anticarcinogenic activity
(12, 13).4 Using the thrombin substrate Boc-Val-Pro-Arg-
MCA, our laboratory has identified a 70-kilodalton cytosolic
serine protease (12) which is inhibited by several anticarcino
genic protease inhibitors. Yavelow et al. (13) and Carew and
Kennedy4 have identified a BBI-inhibitable activity which
cleaves the chymotrypsin substrate Suc-Ala-Ala-Pro-Phe-
MCA. In both of these studies ( 13)4the enzyme was not purified
and hence, from the data presented, it is not clear whether this
activity represents single or multiple activities. The use of
defined substrates is an indirect approach to identifying "target
enzymes" of the anticarcinogenic protease inhibitors. This strat
egy is inherently limited because it allows one to determine only
whether the cleavage of a particular substrate is affected by a
specific protease inhibitor and does not directly address the
broader and more important question of which cellular proteins
actually interact with these inhibitors in the cell.
Affinity chromatography represents a more direct approach
to identifying those cellular enzymes which interact with the
anticarcinogenic protease inhibitors. This technique will poten
tially enable us to isolate functionally intact enzymes in large
enough quantities for biochemical characterization. In addition,
affinity chromatography should allow us to identify all of the
cellular proteins which interact with BBI. In the current series
of experiments, we have utilized a BBI affinity column as a tool
to identify cellular enzymes from C3H/10T'/2 and BS cells
which interact with BBI. In this report we describe the results
of these experiments.
MATERIALS AND METHODS
Chemicals. The BBI was obtained as a crude extract from Technion
Testing and Research Laboratory, Inc. (Belleville, NJ), and purified by
DEAE ion exchange chromatography as previously described (9). S-35
methionine was obtained from New England Nuclear. CNBr-activated
sepharose and chymotrypsin (type II) were obtained from Sigma. En
lighten was obtained from New England Nuclear. Suc-Ala-Ala-Pro-
Phe-MCA was obtained from Peninsula Laboratories, Belmont, CA,
and was made up as a 1-mg/ml (1.51 HIM)stock solution in spectrograde
dimethylsulfoxide and stored at 4*C.
Cells. C3H/10T'/2 cells were grown in basal minimal Eagle's medium
containing 10% heat-inactivated fetal calf serum as described (1, 3). BS
cells were grown in minimal essential Eagle's medium containing 20%
fetal calf serum (11).
S-35 Labeling of Cellular Proteins. Log-phase C3H/10T'/2 or BS
cells were grown in methionine-free medium containing 10% heat-
inactivated fetal calf serum and [3SS]methionine (50 ¿tCi/ml)for 12 h.
After labeling, the medium was removed, the cell monolayers were
washed twice with ice-cold Earle's balanced salt solution, and the cells
were removed from the dishes with a rubber policeman. The cells were
pelleted by centrifugation at 800 x g for 5 min.
Subcellular Fractionation. Cells were resuspended in 5 ml of ice-cold
4J. A. Carew, and A. R. Kennedy. Identification of a metaloprotease which
may be involved in transformation of C3H/10T'/2 cells, submitted for publication.
1798
Research.
on November 25, 2021. © 1988 American Association for Cancer cancerres.aacrjournals.org Downloaded from