[CANCER RESEARCH 5l. 612-618, January 15, 1991]
In Vivo Acquisition of FcTRH Expression on Polyoma Virus-transformed Cells
Derived from Tumors of Long Latency1
M. Ran, B. Katz, N. Kimchi, E. Halachmi, J-L. Teillaud, J. Even, Y. Berko-Flint, E. Atlas, W. H. Eridman,
and I. P. Witz
Department of Microbiology and the Moise and Frida Eskenasy Institute for Cancer Research, The (Jeorge S. Wise Faculty of Lije Sciences, Tel Aviv University . Tel
Aviv 69978, Israel ¡M.R., B. A'., A/. A'., E. H., Y. B-F, E. A., I. P. W.], and Laboratoire d'Immunologie Cellulaire et Clinique, INSERM ('. 255, Institut Curie, Paris,
France ¡J-L.T., J. E., W. H. F.]
ABSTRACT
BALB/c 3T3 cells transformed in vitro with polyoma virus »erecloned
and passaged once in syngeneic mice. Resulting tumors from each clone
were explanted and recultured. Expression of receptor for Fc of IgG
(FcfRII) in the original in vitro maintained clones and in cells derived
from tumors elicited by the respective cells was measured at the protein
level as well as at the mRNA level. Clones were assayed in pairs. The
ancestor in vitro maintained clones (designated cultured cells (C)| were
compared with cells derived from the same clones after a single passage
in vivo followed by cxplantation and reculturing [designated cultured-
tumor-cultured cells (CTC)|. C cells of any of the tested clones did not
express FcyRII. On the other hand, certain CTC cells were positive. The
FcTRH-positive cells were derived from tumors appearing after a long
precancer latency period (>140 days). CTC cells derived from tumors
that appeared after shorter latency periods (<80 days) were !•'(•-> RII
negative. These results were obtained both by using radioimmunoassay
and monoclonal antibodies against mouse I i-~jRl1 as well as by Northern
blot analysis using the I o KlI complementary DNA probe. The involve
ment of macrophages as the Fc-yRII-expressing cells in CTC cells was
excluded.
1 e->RII expression was down-regulated in CTC cells as a function of
time following their explantation into culture. Io RII expression could
be up-regulated in these cells and induced on C cells by maintaining the
cultured cells in the presence of normal mouse serum or recombinant
Interferon. We also tested the expression of Fc-yRII on CTC cells
following their inoculation into syngeneic mice for a second time (CTCx2
cells). The results showed a positive correlation between FcfRII expres
sion in the inoculated ancestor CTC cells and on the CTCx2 cell progeny.
INTRODUCTION
In experimental tumor systems the length of the precancer
latency period can be precisely determined because it separates
2 measurable events. The First event is the exposure of the
animal to an oncogenic agent or to an inoculum of transformed
cells. The second event is the appearance of a tumor. In human
cancer patients or in spontaneous animal tumor systems the
duration of the precancer latency period cannot be determined
because only the second event can be monitored. In both types
of tumor systems the duration of the precancer latency period
is primarily determined by the ability of the transformed cells
to proliferate as well as by the fraction of proliferating cells and
by their proliferation rate.
The proliferation of transformed cells beyond a subthreshold
mass may be halted due to intrinsic properties and/or to lack
Received 5/30/90; accepted 10/26/90.
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.
1 This work has been supported by the Israel Cancer Association. Tel Aviv: the
National Council for Research and Development. Jerusalem; Association pour la
Recherche sur le Cancer, Paris; Concern Foundation. Los Angeles: The Fainbarg
Family Fund, Orange County; and the Mary A. Pikovski Fund, Jerusalem.
Yehudit Berko-Flint is a fellow of the Israel Cancer Research Fund and Isaac P.
Witz is the incumbent of Ihe David Furman Chair in Immunobiology of Cancer.
of growth-promoting host-derived factors. The presence of
growth-inhibiting host factors may also retard their prolifera
tion. The persistence of transformed cells for prolonged periods
of time without progressing toward a frank and overt tumor
has been termed tumor dormancy (1, 2). Transformed cells may
remain dormant until they acquire altered intrinsic properties
and/or until the balance between host-derived inhibitory and
growth-promoting factors changes. These cells may now prolif
erate to form a tumor.
Once a cellular variant within a dormant population has
acquired the ability to proliferate in vivo and thus to exit the
dormancy state, the remainder of the precancer latency period
will by and large depend on the proliferation rate of this variant.
In a previous study (3) we inoculated cloned BALB/c 3T3
cells transformed in vitro with PyV2 into syngeneic recipients.
We demonstrated that the length of the precancer latency
periods varied drastically in individual mice inoculated with an
identical cell dose from the same clone (3). This was a general
finding being more pronounced with low tumorigenic clones.
In extreme cases the duration of the precancer latency of the
first and the last tumor appearing in a group of syngeneic mice
inoculated with a certain dose of cells from a particular clone
differed by 8 months or more (3). Southern blot analysis re
vealed identical integration sites of the PyV genome in the
original in vitro transformed cells (that were never passaged in
vivo) and in the cells from tumors which appeared after a short
or a long latency period following the inoculation of the in vitro
transformed cells.3 This clearly indicated that both the early
tumors and late ones originated from the same population of
in vitro transformed ancestor cells. Furthermore, these results
suggested rather strongly that the cells from the late tumors
were in a prolonged state of dormancy, some well over 1 year
(3).
In order to elucidate mechanisms responsible for tumor dor
mancy and for its termination it may be helpful to dissect and
identify genetic and phenotypic properties distinguishing tumor
cells which underwent a long, a short, or no in vivo dormancy.
The availability of cells derived from either early or late tumors
while both types of tumors originated from the same ancestor
clone of transformed cells makes such an analysis feasible.
In previous publications we hypothesized that the "ectopie
expression" of receptors for Fc7R by nonlymphoid tumor cells
may be associated with cellular growth and progression patterns
that may differ from those of similar tumor cells not expressing
such receptors (4-6). In the present study we analyzed Fc7RII
1 The abbreviations used are: PyV, polyoma virus; C cells, cells maintained
only in culture; CTC cells, cultured cells that were passaged once as tumors in
syngeneic mice and recultured after explantation: Fc7R, receptor for Fc of IgG;
GaM antibody, goat anti-mouse Ig antibody; mAb, monoclonal antibody: RIA,
radioimmunoassay: r-IFN-p, recombinant Interferon 7; DMEM, Dulbecco's mod
ified Eagle's medium; FCS. fetal calf serum; PBS, phosphate-buffered saline;
NMS. normal mouse serum.
3 Y. Berko-Flint, personal communication.
612
Research.
on August 17, 2017. © 1991 American Association for Cancer cancerres.aacrjournals.org Downloaded from