[CANCER RESEARCH 47, 4160-4164, August 1. 1987]
Expression of the Gene Encoding a Prolactin-inducible Protein by Human Breast
Cancers in Vivo: Correlation with Steroid Receptor Status1
Leigh C. Murphy,2 Matthew Lee-Wing,3 Gerald J. Goldenberg, and Robert P. C. Shiu4
Departments of Physiology [L. C. M., M. L-W, K. P. C. S.J and Medicine [G. J. GJ, University of Manitoba and the Manitoba institute of Cell Biology,
Winnipeg. Manitoba, Canada, R3E OWi
ABSTRACT
We have previously reported the identification and characterization of
a prolactin-inducible protein (PIP) as well as the cloning of the gene
encoding PIP in cultured human breast cancer cells. We now present
three lines of evidence that the gene encoding PIP is also expressed by
some human breast cancers in vivo: (a) detection of PIP immunoreactivity
in the serum of some breast cancer patients; (b) imntunohistochemical
detection of PIP in breast cancer sections; and (<•) the presence of PIP
mRNA, detected by complementary DNA hybridization in human breast
biopsy samples.
In a preliminary study using Western blot analysis authentic PIP was
detected in the serum of some patients with breast cancer. Subsequently
the sera of 234 unselected patients with breast cancer were assayed for
the presence of PIP using a specific radioimmunoassay. Thirty-five % of
these sera contained detectable PIP (i.e., > 3 ng/ml). As well we were
able to show by immunohistochemical techniques that PIP immunoreac
tivity was present in some human breast biopsy specimens. Levels of
estrogen receptor, progesterone receptor, and PIP mRNA were deter
mined in an unselected population of 51 human breast tumor biopsies.
Sixty-one % of these tumors had detectable PIP mRNA; a positive
correlation (r = 0.52; /' < 0.01) was found between PIP mRNA levels in
breast biopsy samples and estrogen receptor content, a known prognostic
indicator in human breast cancer.
INTRODUCTION
A PIP5 secreted by the HBC cell line T-47D has been de
scribed previously (1), and recently its cDNA was cloned.6
Maximum expression of this gene occurs when T-47D cells are
treated with human prolactin in the presence of hydrocortisone
for 4-5 days (I).6 While not all HBC cell lines were found to
express the PIP gene,5 those that did were both prolactin and
estrogen receptor positive. The data suggested a potential value
of PIP as a marker of prolactin action in HBC. However, before
this question could be addressed it was first necessary to deter
mine if the PIP gene was expressed in vivo and if so to investi
gate the relationship of PIP expression to known prognostic
indicators in HBC such as ER and PgR.
Since PIP is a secreted protein (1) we approached the above
questions by first investigating the presence of PIP in the serum
of breast cancer patients by Western blot analysis and radioim
munoassay. Next we investigated the expression of PIP by HBC
Received 1/20/87; revised 4/14/87; accepted 5/1/87.
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
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1The work was supported by the Medical Research Council of Canada, the
Manitoba Health Research Council, the St. Boniface Hospital Research Foun
dation, and the Faculty of Medicine of the University of Manitoba.
2 Medical Research Council (Canada) Fellow. To whom requests for reprints
should be addressed.
* Recipient of a Terry Fox Cancer Research Clerkship Award from the National
Cancer Institute of Canada.
' Medical Research Council (Canada) Scientist.
9 The abbreviations used are: PIP. prolactin-inducible protein; HBC, human
breast cancer; PBS, phosphate-buffered saline; TBS, Tris buffered saline; ER,
estrogen receptor; PgR, progesterone receptor; cDNA, complementary DNA;
BSA, bovine serum albumin; SDS, sodium dodecyl sulfate; SSC. standard saline
citrate.
6 L. C. Murphy, D. Tsuyuki. and R. P. C. Shiu. Cloning and regulation of a
prolactin-inducible gene in human breast cancer, submitted for publication.
biopsies using both immunohistochemical techniques and spe
cific cDNA hybridization techniques.
MATERIALS AND METHODS
Serum Samples. Coded blood samples were obtained from an unse
lected population of breast cancer patients attending the Manitoba
Cancer Treatment and Research Foundation. Normal human blood
samples were obtained from healthy volunteers. Blood samples were
clotted, centrifuged, and the serum stored at —20°C until assay.
Human Tumor Samples. Breast tumor biopsies sent frozen to the
laboratory for routine ER and PgR assay were the source of breast
tumor tissue used for either immunohistochemical studies or RNA
extraction and cDNA hybridization. Other human tumor samples were
kindly provided by Dr. A. Alguacil of the Department of Pathology,
Health Sciences Centre, Winnipeg, Canada. Dr. R. Matusik, Depart
ment of Physiology, University of Manitoba, generously donated sam
ples of RNA extracted from a range of human benign prostatic and
prostaiic carcinoma specimens. All tissues had been frozen as quickly
as possible following surgery and pathological examination and stored
at -70°C.
ER and PgR Assays. Samples weighing between 0.2 and 0.3 g were
taken for ER and PgR assay. Available steroid receptors were assayed
using a single saturating dose and a charcoal-dextran method (2) for
separation of bound from free hormone. ER and PgR concentrations
were expressed as fmol of steroid bound per mg of cytosol protein.
RNA Isolation and Hybridization Analysis. RNA was isolated by the
guanidinium thiocyanate/cesium chloride method (3). For Northern
blot analysis RNA isolated as described above was denatured in 50%
(v/v) formamide and 2.2 M formaldehyde, size fractionated on a 1%
(w/v) agarose-2.2 M formaldehyde gel (4) and then blotted onto nitro
cellulose paper (5). Filters were baked for 2 h at 80°Cunder vacuum
and then prehybridized in hybridization solution for at least 3 h. The
filters were then hybridized with nick-translated "P-labeled purified
PIP cDNA insert, cPIP-8-3 (specific activity, 1-5x10* cpm/Mg DNA).
Hybridizations, usually for 24 h, were performed at 42°C in the presence
of 50% (v/v) deionized formamide, 5x Denhardt's solution (Ix Den-
hardt's = 0.02% w/v each of BSA, Ficoll, and polyvinylpyrrolidine),
5x SSPE (Ix SSPE = 0.15 M NaCl-0.01 M NaH2PO4-l mM EDTA),
250 Mg/ml denatured salmon sperm DNA, and 0.1% SDS. At the end
of the hybridization period the blots were washed twice in 0.1% SDS-
2x SSC (Ix SSC = 0.15 M NaCl-0.015 M sodium citrate) for 15-30
min at room temperature, followed by one wash in O.lx SSC-0.1%
SDS for 45-60 min at 65°C.Blots were then exposed to Kodak XAR
film at —70°C with an intensifying screen.
For dot-blot analysis RNA extracted as described above was dena
tured according to the protocol of White and Bancroft (6) and spotted
in varying concentrations (30-0.25 Mg for tumors and MCF-7 HBC
cells or 2-0.0625 Mgfor T-47D HBC cells) onto nitrocellulose filters
using a BRL dot-blot manifold. Filters were treated as described above.
Quantitation of serially diluted RNA samples was achieved by den-
sitometric scanning of various exposures of the dot-blot autoradi-
ographs. The line of best fit obtained by least squares regression analysis
of the integrated peak areas of the signal intensity versus the amount
of RNA loaded was compared to that obtained from a standard serial
dilution of hormone treated T-47D RNA, arbitrarily given a value of
100, present on each dot-blot. A negative control of MCF-7 human
breast cancer cell RNA was also included on each dot-blot. Consistently
we have been unable to detect the presence of PIP mRNA in this cell
line by Northern analysis.6
4160
Research.
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