[CANCER RESEARCH 39, 2923-2927, August 1979]
0008-5472/79/0039-0000$02.0O
Collagen Synthesis in Capsules Surrounding Dimethylbenzanthracene
induced Rat Breast Tumors and the Eftect of Pretreatment
with fJ-Aminopropionitrile1
I. Kelman Cohen, Charles W. Moncure, Raphael J. Wltorsch, and Robert F. Dlegelmann2
Departments of Surgery (I. K. C., R. F. Di, Pathology (C. W. M.j, and Physiology (R. J. W.j, MCV/VCU Cancer Center (R. F. DI, Medical College of Virginia,
Virginia Commonwealth University, Richmond, Virginia 23298
ABSTRACT MATERIALSAND METHODS
Collagen synthesis is increased over three-fold in capsules
surrounding dimethylbenzanthracene-induced rat breast tu
mors compared to the tumor parenchyma and over six-fold
compared to normal breast connective tissue. Increased col
lagen synthesis is independent of the rate of tumor growth and
final tumor size. Pretreatment of animals with $-aminopropio
nitrile to inhibit collagen cross-linking caused an 82% decrease
in tumor formation and a significant reduction in tumor volume
(approximately 0.4 cu cm) compared to controls (approxi
mately 10 cu cm). The four small tumors that did develop in the
lathyritic animals had increased collagen synthesis in the inte
nor tumor stroma and reduced collagen synthesis in the tumor
capsule. These findings suggest that the collagenous capsule
surrounding dimethylbenzanthracene tumors functions as a
physical barrier to protect the tumor from the immune system
of the host. The apparent antitumor effects of $-aminopropio
nitrile may be due to immunopotentiation and/or cytotoxic
actions of the drug.
INTRODUCTION
Most benign and malignant neoplasmsare associated with
a collagenousstroma. The variable quantityand quality of this
collagenous tissue in and surrounding tumors has never been
correlated with tumor virulence. For example, both scirrhous
carcinoma and benign fibroadenoma of the breast are com
posed of a dense collagenous matrix while other benign and
malignant neoplasms may be mainly cellular with a scant col
lagenous stroma.
As an initialstudy to define some of the basic parametersof
collagenmetabolismin malignanttumorand the significanceof
a tumor capsule, the DMBA3-induced rat mammary carcinoma
model was chosen because it has a well-defined collagen
capsule and does not metastasize (8). The objective of this
study was to measure collagen and total protein synthesis
within the tumor parenchyma compared to tumor capsule and
to correlate these findings with the histological appearance of
the tumor. Moreover, we sought to determine if alteration in
the collagenous stroma by inhibition of collagen cross-linking
with BAPN (9) would inhibit capsule formation and allow the
DMBA rat breast tumor to metastasize.
I This investigation was supported by Grant CAl 7297, awarded by the Na
tlonal Cancer Institute, Department of Health, Education, and Welfare. A prelim
mary report of a portion of this work was presented (4).
2 To whom requests for reprints should be addressed, at Box 756, Medical
College of Virginia, Richmond, Va. 23298.
3 The abbreviations used are: DMBA, dimethylbenzanthracene; BAPN. fl-aml
nopropionitrile.
Received January 15, 1979; accepted April 24, 1979
Induction of DMBA Rat Breast Tumors by a Multiple Dose
RegImen. Breast tumors were induced in female Sprague
Dawley rats by jugular i.v. pulse doses of a lipid emulsionof
DMBA (2 mg/dose) at 50, 53, and 60 days of age (8).
Collagen Synthesis Measurements. Collagen synthesis was
measured in vitro (5) by incubating finely minced (0.5 mm)
fresh biopsies (100 mg) of normal connective tissue, tumor
capsule, and tumor in 3 ml of Krebs-Ringer medium containing
10 @Ci of 5-[3Hjproline (49 Ci/mM; Schwarz/Mann, Orange
burg, N. V.). After a 2-hr incubation at 37°,the samples were
frozen, sonicated, and homogenized.
Unincorporated [3H]proline was removed by repeated 5%
tnchloroacetic acid precipitation at 4°,and the radioactive
substrate was then washed twice with ethanol:ether(3:1 , v/v)
and once with absolute ether to remove the trichloroacetic
acid. The precipitated protein was dried slowly to a powder
and desiccated under vacuum to a constant dry weight. The
dried protein was weighed, dissolved in sodium hydroxide,
neutralized, and digested with purified bacterial collagenase as
described previously (5, 10). After 90 mmat 37°,the digestion
with purified bacterial collagenase was stopped by the addition
of an equal volume of 10% trichloroacetic acid:0.5% tannic
acid and centnfugation (10). Collagen digestion products in the
supernatant fluid and radioactive noncollagen protein in the
precipitate were each analyzed by liquid scintillation spectrom
etry. All samples were counted in the presence of 1.5 ml of 5%
trichloroacetic acid:0.25% tannic acid and were completely
dissolved in 10 ml of Triton:Liquifluor(1 :2, v/v) prior to analysis
(10).
Radioactivity released by collagenase was used as a meas
ure of collagen synthesis, and the remaining, undigested pro
tein was a measure of noncollagen protein synthesis. Collagen
and noncollagen protein synthesis were quantitated per mg
tissue dry weight.
Measurement of DNA. The procedure of Webb and Levy
(1 1) was used for DNA quantitation.
AnimalExperiments. Ininitialexperiments, collagenbiosyn
thesis was measured in the capsule and parenchyma of estab
lished DMBA rat breast tumors and compared to nontumorous
breast connective tissue. In subsequent studies, the effect of
BAPN on the inductionof DMBA tumors was evaluated in the
following treatment groups. Four groups of 12 female Sprague
Dawley rats (190 g) were treated as follows:Group 1, 0.5 to
1% fumarate in their diet (control); Group 2, 1 to 2% BAPN:
fumarate in their diet (BAPN supplied by Aldrich Chemical Co.,
Inc., Milwaukee, Wis.); Group 3, 0.5 to 1% fumarate in their
diet 2 months prior to tumor initiation; Group 4, 1 to 2% BAPN
in their diet 2 months prior to tumor initiation. Animals were
AUGUST 1979
2923
Research.
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