Cancer Immunol Immunother (1989) 29: 185-192 ancer
mmunolggy
mmunotherapy
© Springer-Verlag 1989
Blocked and not blocked whole-ricin-antibody immunotoxins:
Intraperitoneal therapy of human tumour xenografted
in nude mice*
P. Brusa 1, F. Pietribiasi 2, G. Bussolati 2, F. Dosio 1, R. Arione 3, P. M. Comoglio 2, M. Prat 2, and L. Cattel 1
Applied Medicinal Chemistry Institute, University of Turin, Italy
2 Department of Biomedical Sciences and Oncology, University of Turin, Italy
• 3 Microbiology Institue, University of Turin, Italy
Summary. A blocked immunotoxin, consisting of ricin
and AR-3 monoclonal antibody joined by a short thioether
bond, was previously synthesized. This conjugate had lost
the ability to bind the galactosidic residues of Sepharose
6B, probably because of the steric restraint of the antibody
molecule on the ricin B chain. In in vitro assays immuno-
toxin was active only on cells expressing the correspond-
ing AR-3 epitope. The in vivo activity of our blocked im-
munotoxin was assessed by injecting it directly into the
peritoneal cavity of tumour-bearing nude mice. The ani-
mals were i.p. grafted with the HT-29 cell line, which was
derived from a human colorectal adenocarcinoma express-
ing the antigen CAR-3, against which the AR-3 monoclo-
nal antibody is directed. The best protocol tested, to arrive
at the optimal regimen for the i.p. blocked immunotoxin
therapy, required the administration of the immunotoxin
(2 lxg) on days 4 and 6 after the graft. The mice were killed
on different subsequent days to determine the therapeutic
effects. Histological sections of the different organs were
prepared and stained with haematoxylin/eosin and were
also examined by an immunocytochemical method with
AR-3 monoclonal antibody to confirm the presence of the
relating antigen on the tumour cell surface. The blocked
immunotoxin substantially suppressed tumour growth of
the grafted HT-29 cells, without showing any undesirable
ricin toxicity. Most importantly, established transplanted
HT-29 tumour cells treated with blocked immunotoxin al-
most completely regressed, while under the same condi-
tions the not blocked immunotoxin, an irrelevant immu-
notoxin, ricin, and the AR-3 alone failed to inhibit tumour
growth.
Introduction
Immunotoxins are conjugates of highly active protein tox-
ins and monoclonal antibodies [2, 12, 36, 37]. The aim of
using immunotoxins in cancer therapy is to concentrate
the toxin within tumour tissue causing the specific killing
of the neoplastic cells [14].
* This work was supported by grants from the Ministry of Public
Education, the Regione Piemonte and the Associazione Italiana
per la Ricerca sul Cancro
Offprint requests to: L. Cattel, Istituto di Chimica Farmaceutica
Applicata, corso Raffaello 31, I-10125, Torino, Italy
Ricin is a toxic plant glycoprotein composed of two
subunits (A and B) linked by a disulphide bond [26]. The
A chain catalytically inhibits protein synthesis by inactivat-
ing 60S ribosomal subunits, so that very few A chain mole-
cules are sufficient to kill a cell [7, 8, 25]. The B chain
binds the toxin to a cell-surface galactosidic receptor and
facilitates A chain translocation [34, 42, 43].
Linkage of a tumour-cell-specific monoclonal antibody
to the A chain alone or to the whole ricin molecule gener-
ates a hybrid molecule which, in theory, combines the
cancer specificity of the antibody with the extreme cyto-
toxicity of the toxin. However, A-chain conjugates are not
as toxic as whole-ricin conjugates and may even be inac-
tive [24, 34]. Nevertheless intact ricin immunotoxins have
non-specific effects, since the B-chain galactose-binding
site is active [2]. This non-specific binding can be limited
in vitro with high concentrations of lactose or galactose
[26, 41]; such intact ricin-antibody conjugates have been
successfully used in vitro to treat bone marrow cells, prior
to transplantation, for the removal of T cells [9] or
leukemic cells [22].
Recently a disulphide-linked whole-ricin-antibody
conjugate was prepared, which failed to bind to lactose-
Sepharose, implying the blocking of the galactose-binding
site on the B chain [27]. This conjugate showed cytotoxicity
in vitro equal to that of native ricin, while in vivo it was
only moderately effective against tumours (growing s.c. in
mice), since it caused some liver and kidney damage.
However, injection of the immunotoxins directly into the
tumours resulted in regression of the tumours [28]. Another
approach, to reduce the non-specific binding, was to pre-
pare intact ricin immunotoxins, thioether-linked; the
B-chain galactose-binding site appeared to be sterically
hindered by the antibody [33]. This immunotoxin, al-
though highly specific to target cells in vitro [2, 5], has not
so far been tested in vivo.
Following the same strategy we prepared [4] a new
thioether-linked ricin-antibody immunotoxin in which the
galactose-binding site of the ricin was sterically hindered.
The immunotoxin was synthesized by linking the AR-3
monoclonal antibody, previously derivatized with N-hy-
droxysuccinimidyl-S-acetyl thioacetate (SATA), to ricin
iodoacetylated with the N-hydroxysuccinimidylester of
iodoacetic acid (SIA). After the last step of purification on
Sepharose 6B, we obtained two populations of immuno-
toxins; one, referred to as blocked, which had lost the abil-
ity to bind the galactosidic residues of the Sepharose 6B,