[CANCER RESEARCH 39, 2390-2399, July 19791
studies, decreased cytoplasmic spreading on substrata was
characteristic of neoplastic rodent embryo fibroblast lines com
pared with normal cell lines (5, 7, 10, 11). Transformation
related changes in cell shape have also been identified by
scanning electron microscopy in rodent liver cells (2, 15) and
embryonic fibroblasts (4, 7, 17, 30). In chick embryo fibroblasts
infected with a temperature-sensitive Rous sarcoma virus,
changes in cell shape occurred rapidly after a shift to the
permissive temperature (3, 16).
In addition, scanning electron microscopic studies of normal
and transformed fibroblasts have provided evidence for in
creased surface activity in transformed cells, in the form of
prominent microvilli (4, 17, 23) or ruffles (3). In comparisons of
normal and oncogenically transformed rat liver cells, the latter
also exhibited increased degrees of surface activity (2, 15).
However, a recent comparison of tumorigenic and nontumori
genic cell lines derived from a single clone of mouse embryo
cells showed no consistent alterations in surface features,
although greater variability of surface morphology was typical
of the tumorigenic lines (30). In a similar study of tumorigenic
and nontumorigenic rat fibroblasts in vitro, no universal pattern
of surface morphology was found to be associated with tumor
igenicity (6). In general, disturbances of cell shape appeared
to be more characteristic of oncogenically transformed cells
than were changes in surface architecture.
It is important to determine whether morphological alterations
are correlated with oncogenic transformation in cells from the
lining epithelia, which constitute the major sites of cancer
incidence in humans. In an experimental model of respiratory
carcinogenesis, cell lines derived from carcinogen-exposed
respiratory airway epithelium showed anchorage independ
ence and tumorigenicity after varying lengths of time in culture
(19). The characteristics of populations similar in origin but
differing in tumorigenicity have been studied in cells from
sequential passages of these lines. To accomplish the present
objectives, we have compared cell shape and microvillar den
sity in cells from populations derived before and after the time
at which anchorage independence and tumorigenicity were
expressed. Since cell shape and surface morphology vary
considerably among cells of the lining epithelia in vivo (1, 14,
25), significant morphological variability was expected in the
cells studied. Therefore, the approach taken was to assess the
variability of shape and surface features in cells from small
colonies, predominantly of clonal derivation. By this approach,
a range of variability could be defined for preoncogenic popu
lations; thus, the appearance of new characteristics or chang
ing frequencies of expression of existing characteristics could
be detected.
MATERIALS AND METHODS
Cell Culture. All of the cell lines used were derived from
specific-pathogen-free, inbred female Fischer 344 rats. Two
ABSTRACT
The purpose of the present studies was to determine whether
changes in cell shape and microvillar density accompanied
oncogenic transformation of rat respiratory tract epithelial cells.
Two cell lines which became oncogenic during in vitro culture
(1000 W and 165 S) were studied. In relatively late passages,
but not in early passages, the lines produced keratinizing
squamous cell carcinomas when tested in syngeneic hosts.
Small colonies, predominantly of clonal origin, were obtained
at early and late times after initiation of the lines into in vitro
culture. Scanning electron microscopic studies showed that
preoncogenic and oncogenic populations differed with respect
to the shapes of cells within colonies. Differences in cell shape
were further analyzed by estimation of the height and the ratio
of length to width for 20 cells sampled from each colony. Each
cell was assigned to one of nine classes of cell shape. The
frequency with which spindle-shaped cells were observed in
colonies increased 3-fold with oncogenic transformation of the
1000 W and 165 S lines. The frequency did not increase during
in vitro culture of a third highly oncogenic cell line, BP 3-0. The
frequency of observation of spindle-shaped cells in the 1000
W line was not decreased by in vivo growth and rederivation.
In fact, the tumor-derived subline, 1000 WT, had a 5-fold
greater frequency of expression than did an early passage of
the 1000 W line. The number of colonies in which this cell
shape was observed also increased 5-fold and came to include
nearly one-half of the colonies analyzed. Therefore, expression
of spindle shape became prevalent in clonal subpopulations of
the line. In early passages of the 1000 W and 165 S lines, most
spindle-shaped cells were found at the edges of colonies. This
observation suggested that the spindle shape was assumed in
response to forces generated during colony expansion. In
general, the 1000 W line, which was more oncogenic than the
165 S line, also showed more pronounced morphological al
terations. The prevalence of ruffles was well correlated with
oncogenicity in the 1000 W line. However, the cell lines differed
with respect to the density of microvilli at the cell surface, and
this feature did not seem well correlated with oncogenicity. The
results suggested that cytoskeletal and/or adhesive mecha
nisms implicated in shape maintenance were altered in parallel
with oncogenic transformation of epithelial cells originating
from the respiratory tract.
INTRODUCTION
Previous comparisons of normal and transformed cells in
vitro have shown that certain morphological features are cor
related with oncogenic transformation. In light microscopic
, Research sponsored by the Division of Biomedical and Environmental Re
search, United States Department of Energy, under contract w-7405-eng-26
with the Union Carbide Corporation.
2 To whom requests for reprints should be addressed.
Received October 12. 1978; accepted March 21, 1979.
CANCERRESEARCHVOL. 39
2390
Morphological Markers of Oncogenic Transformation in Respiratory Tract
Epithelial Cells1
C. A. Heckman2 and A. C. Olson
Biology Division. Oak Ridge National Laboratory. Oak Ridge. Tennessee37830
Research.
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