[CANCER RESEARCH 48, 3607-3612, July 1. 1988|
Increased Antitumor Effect of Immunoconjugates and Tumor Necrosis Factor
in Vivo
Mark J. Smyth, Geoffrey A. Pietersz, and Ian F. C. McKenzie
Research Centre for Cancer and Transplantation, Department of Pathology, University of Melbourne, Parkville, Victoria, 3052, Australia
ABSTRACT
The potential of specifically targeting antineoplastic drugs and toxins
to tumors with the use of monoclonal antibodies (MoAbs) reactive with
tumor-associated antigens is currently being examined. JV-Acetyl-mel-
phalan-MoAb (N-AcMEL-MoAb) conjugates have previously been
shown to have greater antitumor activity than N-AcMEL, melphalan, or
MoAb alone against both subcutaneous and ascites murine thymomas in
mice (1). Although this conjugate is also a highly selective tumor inhibitor
in vitro, it may not reach all the tumor cells in a high concentration, and
consequently larger tumors (>0.4 cm2) cannot be eradicated. This con
jugate is representative of many drug-MoAb conjugates in that they are
unable to gain adequate access to the tumor site to exert their cytotoxic
effect. To potentiate the antitumor effect of the N-AcMEL-MoAb con
jugate, studies were undertaken to analyze its action in combination with
recombinant human tumor necrosis factor a (rTNF-a), a monokini-,
capable of causing acute necrosis of syngeneic tumor transplants in mice.
Treatment of mice with murine thymomas (0.4 to 0.6 cm2 in size)
demonstrated that 30% of the tumors in mice receiving conjugate and
rTNF-a partially or completely regressed, while no regressions were
observed in the tumors of mice receiving N-AcMEL-anti-Ly-2.1 conju
gate or rTNF-a alone. This and other experiments indicated that the
antitumor effect and tumor localization of N-AcMEL-MoAb conjugates
can be enhanced in vivo by rTNF-a, thereby enabling successful eradi
cation of lai HITestablished subcutaneous murine tumors.
INTRODUCTION
There are many problems associated with the use of immu-
noconjugates, such as the complexity of coupling relatively
Hydrophobie and bifunctional drugs to antibody (1), the potency
(2) and nonspecific toxicity (3) of drug/toxin-MoAb1 conju
gates, and the heterogeneity of tumor cells (4, 5), which have
all been addressed. Successful treatment of subcutaneous tu
mors by intratumor immunotoxin therapy (6) suggests that the
relative inaccessibility of solid tumor to drug/toxin-MoAb con
jugates is a major limitation of the more widely applicable i.v.
route of administration. One method of partially overcoming
this problem is to use vasoactive agents. By their selective action
on normal blood vessels, vasoactive drugs can alter the tumor/
normal tissue perfusion ratio, thereby enhancing the access of
drug-MoAb conjugates to tumors and increasing the effective
ness of tumor therapy (7). However, it is clear from these
studies that other methods have to be found to get more
antibody out of the circulation and into the tumor. It is apparent
that antibodies produced in response to bacterial infection
require a local inflammatory response (with vasodilation and
increased permeability of vessels) to permit the antibodies to
reach their target, and on the basis of these observations, we
have used TNF-a, a monokine capable of inducing hemorrhagic
necrosis and a subsequent inflammatory response in tumors, to
Received 12/15/87; revised 3/23/88; accepted 3/31/88.
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1The abbreviations used are: MoAb, monoclonal antibodies; N-AcMEL, N-
acetyl-melphalan; MEL, melphalan; rTNF-a, recombinant tumor necrosis factor
a; rll-N -), recombinant -y-interferon; PBS, phosphate-buffered saline; DME,
Dulbecco's modified Eagles medium; TNF-a, tumor necrosis factor a; TNF,
tumor necrosis faeton %T/C, therapeutic index.
increase the potential antitumor effect and tumor access of
immunoconjugates.
In partially purified form, TNF-a is cytostatic or cytotoxic
for a variety of tumor cells in vitro (8) while having a number
of noncytotoxic effects on normal cells (9). Recently, rTNF-a
protein (10) has confirmed the selective cytotoxic effects in vitro
on tumor cells previously observed with the natural TNF-a.
TNF-a binds to specific receptors on the membrane of target
cells (11) and is subsequently internalized and degraded (12),
although the presence or absence of TNF receptors, however,
is not correlated with sensitivity or resistance to the cytolytic
effects of TNF-a (13). The overall spectrum of the antitumor
activity of TNF-a is not yet understood, and in addition to a
direct cytostatic or cytocidal effect on tumor cells, TNF-a is
also capable of eliciting an antitumor effect by a direct cytotoxic
effect on capillary endothelial cells, thereby leading to vascular
damage and subsequent hemorrhagic tumor necrosis (14).
Studies analyzing the effect of TNF-a in combination with
other lymphokines (murine -y-interferon) and immunochemo-
therapy in an in vivo model system are also a prerequisite for
exploring the full potential of TNF-a given that TNF-a has a
very narrow therapeutic range. We now present evidence that
the antitumor effect of N-AcMEL-MoAb conjugates can be
enhanced by recombinant TNF-a, enabling improved therapy
of larger established murine thymomas.
MATERIALS AND METHODS
Tumor Growth. The E3 clonal variant of the murine thymoma
ITT(1)7SNS (1) was maintained in vitro in DME, supplemented with
10% heat-inactivated newborn calf serum (Flow Laboratories, Sydney,
Australia), 2 niM glutamine (Commonwealth Serum Laboratories, Mel
bourne, Australia), 100-11' of penicillin/ml (Commonwealth Serum
Laboratories), and 100 ¿tg/mlof streptomycin (Glaxo Laboratories,
Melbourne). For in vivo experiments E3 was maintained by serial
passage in the ascites form in CS7BL/6 x BALB/c !•', (hereafter called
B6CF|) mice; cells from the ascites fluid were washed and centrifugea
(400 x g, 5 min) twice in DME and PBS (pH 7.3), resuspended in PBS,
and injected s.c. into mice. Tumor cells were injected s.c. into the
abdominal wall and were allowed to develop into palpable tumors
before commencing treatment. Mice were then subjected to a series of
i.p. and i.v. treatments, and the size of the tumors was measured daily
with a caliper square measuring along the perpendicular axes of the
tumors; the data were recorded as the mean tumor size [product of two
diameters ±SE (<5%)]. Experimental groups of 10 to 20 mice, all of
the same sex and age, were used while a number of parameters were
recorded during the course of experiment for each group, including: (a)
the number of deaths due to rTNF-a toxicity (determined by histopa-
thology); (b) %T/C tumor size = the mean tumor size of a treated group
of mice relative to the mean tumor size of PBS treated mice on Day
20; (c) the proportion of tumors which remained completely regressed
100 days after tumor inoculation; and (d) the proportion of partial
(>50% reduction in original tumor size) and complete tumor regres
sions combined.
Mice. B6CFi mice were produced in the Department of Pathology,
University of Melbourne.
MoAb. The MoAb used in this study was anti-Ly-2.1, a murine
MoAb reactive with the murine Ly-2.1 specificity (IgG2a) (15). This
MoAb was isolated from ascitic fluid by precipitation with 40% am-
3607
Research.
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