[CANCER RESEARCH 54, 6344-6347, December 15, 1994]
Advances in Brief
Molecular Characterization of Prostate-specific Antigen Messenger RNA
Expressed in Breast Tumors1
Maria Monne, Carlo M. Croce,2 He Yu, and Eleftherios P. Diamandis
Department of Microbiology-Immunology and Jefferson Cancer Institute, Jefferson Medical College, Thomas Jefferson University. Philadelphia. Pennsylvania 19107
(M. M., C. M. C.], and Department of Clinical Biochemistry. University of Toronto, Toronto, Ontario M5G 11.5. Canada [H. Y., E. P. D.J
Abstract
Prostate-specific antigen (PSA) Is considered a highly specific blochem
Ical marker of the prostate gland and is currently used for prostate cancer
diagnosis and monitoring of patients with prostate adenocarcinoma. We
recently demonstrated, however, that about 30% of female breast tumors
produce a Mr 33,000 protein that has striking similarities to seminal PSA.
In this study we characterized the presence ofPSA in 6 breast tumors and
in the testosterone-stimulated T47D breast cancer cell line at the mRNA
level. Using reverse transcriptase-polymerase chain reaction and DNA
sequencing techniques we identified PSA mRNA In Immunoreactive PSA
positive breast tumors but not in immunoreactive PSA-negative breast
tumors. The sequence of the generated polymerase chain reaction prod
ucts was identical to the sequence of the PSA complementary DNA
derived from prostate tissue. The data presented here support the notion
that breast tumors produce a Mr 33,000 protein which is identical to PSA
produced by the prostate gland. Our study suggests that the presence of
PSA in breast tumors may be used as a new additional biochemical
marker for breast cancer prognosis, for the spreading of hematogenous
micrometastases, and/or for response to adjuvant treatment.
Introduction
PSA3 is a Mr 33,000 glycoprotein produced almost exclusively by
the epithelial cells of the prostate and is currently used as a marker for
diagnosis and monitoring of prostate cancer (1—3).PSA detection in
tumors of nonprostatic origin has been reported as a rare event, in a
few instances, using immunohistochemical techniques (4).
We have recently reported that PSA immunoreactivity can be
detected in about 30% of breast tumors and that breast cancer cells in
culture can produce IRPSA after stimulation by steroid hormones
(5—7). This immunoreactive PSA was shown to be associated with the
presence of steroid hormone receptors, early disease stage, and
younger patient age (5). Although the results from previous studies
suggested that IRPSA in breast cancer cells seems identical to the
seminal PSA, a final proof has not yet been provided. In this study we
report the molecular characterization of the PSA detected in breast
tumors and in the testosterone-stimulated T47D breast cancer cell line.
Six breast tumors were tested for PSA immunoreactivity and then
analyzed for PSA gene expression by reverse transcriptase-PCR and
DNA sequence was determined on the PCR fragments. DNA se
quence analysis demonstrated that PSA mRNA derived from breast
tumors is identical to the PSA from prostate tissue.
The PSA production by 30% of breast tumors underscores the
Received 9/6/94; accepted 11/2/94.
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.
I This work was supported by a NIH Outstanding Investigator Grant CA39860
to C. M. C.
2 To whom requests for reprints should be addressed, at Department of Microbiology
and Immunology, Jefferson Cancer Institute, Jefferson Medical College, Thomas
Jefferson University, 1ith and Walnut Streets, Philadelphia, PA 19107.
3 The abbreviations used are: PSA, prostate-specific antigen; IGFBP, insulin growth
factor-binding protein; IRPSA, immunoreactive PSA; eDNA, complementary DNA PCR,
polymerase chain reaction.
similarities between breast and prostate tissues and holds promise of
being used in breast cancer for prognosis, in selection of therapy, or
for devising new therapeutic interventions.
Materials and Methods
Tissue Specimens. Six breast cancer specimens were obtained from
women undergoing surgery for primary breast cancer. The breast tumor tissue
was stored in liquid nitrogen immediately after surgical resection, transported
to the laboratory, and subsequently stored at —70°C until protein and R.NA
extraction was performed. Frozen surgical specimens from various other
tumors were obtained from the Toronto Hospital, Toronto, Ontario, Canada
(3 ovarian and 2 lung carcinomas), from the Hospital of Padova, Padua, Italy
(1 gastric and 1 colon carcinomas), and from the Jefferson Hospital, Philadel
phia, PA (1 melanoma). All tumors were primary lesions except for one
ovarian carcinoma, which was metastatic from breast cancer, and one lung
carcinoma, which was metastatic from prostate cancer. One normal breast
tissue specimen was obtained from a woman undergoing breast cosmetic
surgery, and peripheral blood leukocytes obtained from a healthy volunteer
were prepared from 10 ml venous blood.
Tissue Culture and Stimulation with Steroids. The steroid hormone
receptor-positive breast carcinoma cell line T47D was obtained from the
American Type Culture Collection, Rockville, MD. The cell line was grown in
flasks at 37°C and 5% CO2 in RPMI 1640 supplemented with 0.2 Hi of bovine
insulin/ml, 29 g/liter glutamine, and 10% FCS. When the cells were grown to
90% confluencythey were washedwith isotonic saline and maintainedin the
medium as above but without the presence of FCS. Stimulation experiments
with steroids were performed by adding in the culture medium various steroids
in alcoholatfinalconcentrationsof iO@ M.Thefinalconcentrationof alcohol
was always <0.1% of the total volume. Control experiments with alcohol alone
were performed in parallel. In this work we used T47D cells stimulated with
either solvent or testosterone.
T47D cells stimulated with testosterone produce PSA which is secreted in
the tissue culture supernatant and which is measurable by the immunofluoro
metric procedure. After 4 days of stimulation the cells were detached by
trypsin-EDTA treatment and were kept frozen at —70°C until RNA extraction
was performed.
Preparation ofTumor CytosolicExtracts. Approximately0.5goftumor
tissue was weighed out, fragmented with a hammer if necessary, and pulver
ized in a Thermovac tissue pulverizer at liquid nitrogen temperature. The
resulting powder was transferred into 50-mi plastic tubes along with 10 ml of
extraction buffer [10 mmol/liter Tris-HC1 (pH 7.40), 1.5 mmol/liter EDTA,
5 mmol/liter sodium molybdate]. The suspendedtissue powder was solubilized
on ice with a single 5-s burst of a Polytron homogenizer. The particulate
material was pelleted by centrifugation at 105,000 X g for 1 h. The interme
diate layer (cytosol extract) was collected without disturbing the lipid or
particulate layers. The cytosols were then assayed for PSA with the immun
ofluorometric procedure.
PSA Assay in Tumor Cytosols and Tissue Culture Supernatants. PSA
in the cytosolic breast extracts and tissue culture supernatants was measured
with a highly sensitive and specific immunofluorometric technique described
in detail elsewhere (7). Briefly, the PSA assay uses a mouse monoclonal
anti-PSA capture antibody coated to polystyrene microtiter wells, a biotiny
lated polyclonal rabbit detection antibody, and alkaline phosphatase-labeled
streptavidin. In the assay 50 ml of sample are first incubated with the coating
antibody in the presence of 50 ml of assay buffer. After 3 h incubation and 6
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