(CANCER RESEARCH 50, 159-163. January I. 1990]
Enhancement of Monoclonal Antibody Uptake in Human Colon Tumor Xenografts
following Irradiation1
H. Kalofonos, G. Rowlinson, and A. A. Epenetos2
Imperial Cancer Research Fund Oncology Group, Royal Postgraduate Medical School, Hammersmith Hospital, London W120HS, England
ABSTRACT
Indium-Ill-labeled Al Al tumor-associated monoclonal antibody
raised against an antigen of colon adenocarcinoma was used to evaluate
the effect of ionizing radiation on antibody uptake by the LoVo adeno
carcinoma cell line grown as a xenograft in nude mice. Tumors were
exposed to single doses of external X-irradiation of between 400 and
1600 cGy followed, 24 h later, by administration of specific or nonspecific
antibody. Animals were sacrificed 3 days after antibody administration.
At doses higher than 400 cGy, tumor uptake with both specific and
nonspecific antibody was significantly increased. No difference in changes
in tumor volume was observed between the groups receiving irradiation
and the controls. Specific antibody uptake by tumors was always signif
icantly higher than nonspecific having an approximate 4-fold binding
advantage. Vascular permeability and the vascular volume of irradiated
and control tumors was measured 24 and 72 h after irradiation, using
iodine-125-labeled nonspecific antibody and labelling of the red blood
cells in vivo with "TcO.t. At doses higher than 400 cGy, vascular
permeability in the tumor 24 h after irradiation was significantly in
creased (P < 0.05), while the vascular volume decreased (P < 0.001)
compared to control values. However at 72 h after irradiation there was
no difference between treated and control groups.
The results obtained in this study suggest a potential value of external
irradiation to increase monoclonal antibody uptake by tumors governed
mainly by the increased vascular permeability of the tumor vasculature
soon after the irradiation exposure.
INTRODUCTION
The usefulness of radiolabeled monoclonal antibodies for
diagnosis (1) and therapy (2) of human tumors has been rec
ognized, but a significant limitation for their application in vivo
is the low absolute amount reaching the target (3). The local
ization of monoclonal antibodies on the solid tumors is assumed
to be governed by passive diffusion and binding on tumor cells.
This depends on many factors such as antibody affinity, binding
of the injected antibody by circulating antigen, density of the
antigen expressed on tumor cells, vascular content of the tumor
and accessibility of the antibody to solid tumors (4-6).
It has been previously shown that a single dose of external
irradiation can increase monoclonal antibody uptake by tu
mors such as colorectal carcinoma (7), melanoma (8), and
hepatoma (9), grown in mice and in an anecdotal hepatoma
case reported by Order et al. (10). Ionizing radiation has been
shown to change the vascular volume and the vascular perme
ability to macromolecules in tumors. Paradoxically increased
and decreased vascular volume have been observed depending
upon the study and the time of observation after the irradiation
(11, 12). The exposure of several different tissues to ionizing
irradiation leads to a disruption of the vascular endothelium
(13-15) and a quantitative increase in vascular permeability
(15-18).
The purpose of this study was to conduct a comprehensive
evaluation of the effect of a single dose of external irradiation
Received 3/20/89; revised 7/31/89; accepted 10/2/89.
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.
1This work was supported by the Imperial Cancer Research Fund.
2To whom requests for reprints should be addressed, at ICRF Oncology
Group, Hammersmith Hospital, DuCane Road, London W120HS. England.
on the uptake of specific and nonspecific monoclonal antibody
by a human colon adenocarcinoma xenograft in nude mice. A
further aim was to assess and correlate the vascular volume and
vascular permeability in this tumor model following irradiation.
MATERIALS AND METHODS
Animals and Tumors
Twelve-week-old male athymic nu/nu (nude) mice, from a colony of
mixed genetic background, were bred in the ICRF Animal Breeding
Unit (South Mimms, Hertfordshire, UK). The mice were housed in
sterile cages and maintained on irradiated diet and acidified water (pH
2.8). Xenografts were established s.c. by the inoculation under the skin
of the flank of a single cell suspension of 5.106 cells in 0.1-ml medium
of a human tumor cell line of a colon carcinoma designated LoVo (19).
Tumor cells were grown in large tissue culture flasks in RPMI 1640
medium supplemented with 10% FCS.3 Cells were harvested by incu
bation with 0.02% EDTA for 5 min and washed with serum free
medium. Dimensions of tumors were measured before the irradiation
as well as at the day of dissection to determine whether irradiation had
a detectable effect on tumor volume. Tumor volume was determined
from orthogonal measurements of three diameters using the formula:
y = (4ir/3) x (dl x d2 x d3)/8
where V is the tumor volume, dl, d2, and d3 are the three different
diameters. Mice were randomly allocated to treatment groups of five
to six. The mean tumor volume in each group of mice was not signifi
cantly different from the others.
Monoclonal Antibodies
AUA1. This is a murine IgG, raised in the conventional fashion by
immunising BALB/c mice with the colon adenocarcinoma cell line
LoVo (20). It recognizes a M, 35,000 antigen located on basolateral
aspect of the cell membrane of a wide variety of neoplastic cells and a
limited set of normal epithelial tissues (21). AUA1 is an epithelial
specific antibody and reacts with the majority of human gastrointes
tinal, ovarian and breast carcinomas, as well as proliferating epithelial
cells in tissues such as normal colon.
HMFG1. This is a murine IgG, and defines a tumor-associated
antigen on a high molecular weight glycoprotein which is strongly
expressed in lactating breast as well as in a range of neoplasms such as
breast cancer, ovarian, and nonsmall cell lung cancer (22). This antibody
does not react with LoVo adenocarcinoma and was used as a negative
control.
Radiolabeling of Antibodies
Monoclonal antibodies were radiolabeled with '"In (0.04 M, carrier
free, INS. 1; Amersham International, Amersham, UK) using DTPA,
the cyclic anhydride (Sigma), as described by Hnatowich et al. (23). In
the vascular studies the HMFG1 was labeled with '"I (IBS.3, Amer
sham International, Amersham, UK), in order to determine the perme
ability of tumor vasculature to IgG. lodination was carried out in
iodogen coated tubes using an established technique (24). lodinated
antibody was purified before each experiment by passage through a
column with Sephadex G50 (Pharmacia, Sweden) to remove the free
' The abbreviations used are: PCS, fetal calf serum; FACS. fluorescence-
activated cell sorting; FPLC, fast protein liquid chromatography: Ht. haematocrit;
PBS, phosphate buffered saline: SDS-PAGE, sodium dodecyl sulfate-polyacryl-
amide gel electrophoresis; VV, vascular volume; VP, vascular permeability.
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