[CANCER RESEARCH 53. I630-I6.16. April 1. ITO|
Transforming Growth Factor-a Production and Autoinduction in a Colorectal
Carcinoma Cell Line (DiFi) with an Amplified Epidermal Growth Factor
Receptor Gene1
Scema Untawale, Mark A. Zorbas, Clague P. Hodgson, Robert J. Coffey, Gary E. Gallick, Susan M. North,
David M. Wüdrick,Matilde Olive, Mark Blick, Lynn C. Yeoman, and Bruce M. Boman2
on Cancer Center. Creighton University School of Medicine. Omaha. Nebraska 68178 IB. M. B.. D. M. W.. C. P. H.f; Department of Tumor Biology. The Universitv of
Texan M. D. Anderson Cancer Center. Houston. Texas 77030 ¡G. E. G.. S. M. N.]: Department of Human Oncologv K4/3I9, University of Wisconsin Hospital, University' of
Wisconsin Clinical Cancer Center. Madison. Wisconsin 53792 ¡S. U.¡:Section of Gastrointestinal Oncolog\ and Digestive Diseases. The University of Texas M. D. Anderson
Cancer Center. Houston. Texas 77030 ¡M. O.I: Molecular Analysis. Inc.. Houston. Texas 77054 ¡M. fi./. Department of Pharmacology. Baylor College of Medicine, Houston.
Texas 77030 ¡M. A. Z.. L C. Y./: and Vanderbill University School of Medicine. Departments of Medicine and Cell Biology. Nashville. Tennessee 37232 IR. J. CI
ABSTRACT
The DiFi colorectal carcinoma cell line, derived From a patient with
familial adenomatous polvposis. was examined for gene expression and
production of the autocrine growth factor transforming growth factor a
(TGF-«) and for epidermal growth factor receptor (EGFR) gene expres
sion and gene copy number. DiFi cells expressed TGF-a transcripts as
identified on Northern (RNA) blots. Addition of TGF-a ( 10 ng/ml) or EOF
110 ng/ml) to DiFi cell cultures (lacking I <.1 or serum) up-regulated DiFi
cell basal T(iF-» mRNA levels, suggesting that autoinduction of TGF-a
occurs in these cells. DiFi cell cultures in log phase growth secreted mea
surable amounts of TGF-u (347 pg/10* cells/24 h) into their culture me
dium, as determined by radioimmunoassay. DiFi cells showed strong over-
expression of the EGFR gene on Northern blots relative to three other
colon cancer cell lines examined. Immunoperoxidase staining showed en
hanced I I.I K expression in a cell subpopulation among the original (un
cultured) ascitic fluid cells from which the DiFi cell line was established.
This cell subpopulation was observed to expand dramatically between
passages 1 and 25. Immune complex kinase assay of DiFi cells showed that
EGFR were functional as determined by their ability to autophosphory-
late. The EGFR gene in these cells was not found to be rearranged or
genetically altered using Southern blot analysis. Dot blot analysis of DiFi
cell DNA revealed EGFR gene amplification in the range of 60-80 copies/
cell, which is approximately twice the copy number seen in A-431 epider-
moid carcinoma cells. To our knowledge DiFi cells represent the first
example of EGFR gene amplification in a colorectal adenocarcinoma.
Because Ilili colorectal cancer cells uniquely show production and auto-
induction of TGF-a in addition to amplification and overexpression of the
EGFR gene, these cells represent a valuable tool for studying the role(s) of
the EGFR in the regulation of tumor cell growth.
INTRODUCTION
EOF' is a polypeptide growth factor produced by many normal
human tissues and is present in normal serum. TGF-a, a homologue
of EOF. is produced by a variety of malignant and normal cell types.
Both TGF-a and EOF are known to bind to the same cell surface
receptor, the EGFR. and they produce a similar biological response
(reviewed in Refs. I and 2).
Received 9/8/92; accepted 1/14/93.
The costs of publication of this article were defrayed in part by the payment of page
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18 U.S.C. Section 1734 solely to indicate this fact.
1 Support for these studies was provided by Health Future Foundation Funds. Creigh-
ton University Department of Medicine Research Fund. The University of Texas M. D.
Anderson Cancer Center New Program Funds, and NIH grant CA5039I (L. C. Y.).
Preliminary data were presented at the proceedings of the Fourth International Symposium
on Colorectal Cancer. Kobe. Japan. November 1989.
2 To whom requests for reprints should be addressed, at Creighton Cancer Center.
Creighton University School of Medicine. 24th and California Street. Omaha. NE 68178.
1The abbreviations used are: EGF. epidermal growth factor; TGF-a, transforming
growth factor-a; EGFR. epidermal growth factor receptor(s); RIA, radioimmunoassay:
ATCC, American Type Culture Collection: FBS. fetal bovine serum; SSC. standard
sodium citrate: 10F medium, McCoy's 5A medium (GIBCO) containing UK? FBS;
SF-EGF medium. McCoy's 5A medium containing 4 ug/ml transferrin and 20 ug/ml
insulin but lacking serum and EGF: DMSO. dimethyl sulfoxide; TPA, 12-O-tetrade-
canoylphorbol-l3-acetate; cDNA, complementary DNA.
Alterations in EGFR number or structure in a given cell may
influence the growth properties of that cell. For example, when NIH
3T3 cells were transfected with a vector containing the full-length
EGFR gene (which induces EGFR overproduction), they became fully
transformed (3). Additionally, in subclones of A-431 cells having
different degrees of EGFR gene amplification and expression, the
level of EGFR observed is reported to be proportional to the ability of
the cells to grow both in vivo and in vitro (4). The oncogenic prop
erties of \-erhB. which encodes a truncated version of the EGFR (5).
indicate that an altered EGFR can directly lead to tumorigenesis.
Overproduction of EGFR has been reponed for squamous cell
carcinomas (lung, skin, oral cavity, and esophagus), brain tumors
(glioblastomas and meningiomas). breast adenocarcinomas (90%),
and colon adenocarcinomas (moderately well differentiated but not
poorly differentiated) (6-13). In some tumors, the overproduction of
EGFR is correlated with amplification of the number of copies of the
EGFR gene (7. 10. II). In gliomas, the amplified EGFR gene is
frequently rearranged, suggesting that this gene mutation may be
associated with development of the tumor ( 10). Yet. in the majority of
cancers that overproduce EGFR, such overproduction appears to oc
cur through mechanisms other than gene amplification. An analysis of
101 cancers, including carcinomas, sarcomas, lymphomas, and leu-
kemias. showed that only one squamous cell carcinoma had amplifi
cation of the EGFR gene (14). Whereas some primary colonie ade
nocarcinomas and colon carcinoma cell lines showed enhanced EGFR
expression, none displayed gene amplification (12, 14, 15).
The initial purpose of our study was to determine EGFR gene copy
number and expression (mRNA) in the DiFi colorectal carcinoma cell
line, which was established from a patient with familial adenomatous
polyposis (16). Because these studies revealed dramatic EGFR gene
amplification/overexpression in DiFi cells ( 17), we conducted further
studies on cell surface EGFR expression, EGFR kinase activity.
TGF-a production, and potential TGF-a autoinduction in these cells
to determine their value in understanding the role of the EGFR in
human colon tumor cell growth.
MATERIALS AND METHODS
Cell Culture. DiFi cells and SW403 colon cancer cells (ATCC CCL 230)
were routinely cultured (without udded EGF or TGF-a) in a 50:50 mixture of
L-15:Dulbecco's modified Eagle's culture medium (both from GIBCO. Grand
Island. NY) containing lO'/r FBS plus insulin (5 ug/ml; Sigma Chemical
Company, St. Louis, MO), transferrin (5 ug/ml; Sigma), and sodium selenite
(5 ng/ml: Collaborative Research. Waltham. MA) and plated into standard
75-cm- plastic tissue culture flasks or 850-cnr plastic roller bottles (Coming
Glass, Corning. NY). The three remaining SW lines. SW480. SW620 (ATCC
CCL 228 and CCL 227). and SW742 (from Dr. Benjamin Drewinko, The
University of Texas M. D. Anderson Cancer Center. Houston. TX), were grown
in L-15 medium (modified) containing i-glutamine. supplemented with \07c
FBS. insulin (5 ug/ml). and glutathione (16 ug/ml). A-431 cells (ATCC CRL
1555) used for EGFR gene amplification comparison with DiFi cells were
maintained in Dulhecco's modified Eagle's medium with 4.5 g/liter glucose
1630
Research.
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