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Induction of Macrophage-Mediated Tumor Lysis by the Lectin Wheat Germ Agglutinili1

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Induction of Macrophage-Mediated Tumor Lysis by the Lectin Wheat Germ Agglutinili1 (CANCER RESEARCH 40, 3798-3803. October 1980] 0008-54 72/80/0040-0000$02.00 Induction of Macrophage-mediated Tumor Lysis by the Lectin Wheat Germ Agglutinili1 Manko Kurisu,2 3 Masatoshi Yamazaki,3 and Den'ichi Mizuno Faculty ol Pharmaceutical Sciences. University of Tokyo. Tokyo. Japan ABSTRACT syngeneic tumor system (23, 30-32). The first step in this type of cytolysis also involves interaction between the macrophages The first step in macrophage-mediated tumor lysis, effector- and the tumor cells, which is induced by antitumor antibody target contact, was studied in a C3H/He mouse-MM46 syn- (20). However, an important question remains to be answered. geneic tumor system in which antibody-dependent tumor lysis Is the contact of macrophages with tumor cells that results in by macrophages (ADMC) was observed in vitro. Various lectins cytolysis mediated only by antitumor antibody, or can any other were tested for the ability to mediate the contact between agents induce the binding of effector macrophages to target effector macrophages and target tumor cells. Several lectins, tumor cells to provoke the cytolysis? such as wheat germ agglutinin (WGA), concanavalin A, phyto- To investigate this question, we examined the ability of plant hemagglutinin, and pokeweed mitogen, were found to induce lectins to act as 'ligand" substances between effector and this contact, but only WGA also induced tumor lysis by mac target cells. The present report shows that several lectins serve rophages. Both this lectin-dependent cytolysis by macro as ligand substances and that one of these, WGA, can phages (LDMC) and the cytoadherence between macrophages induce cytolysis after mediating the binding of effector to target and tumor cells induced by WGA were inhibited by W-acetyl- cells. This new type of WGA-dependent tumor lysis mediated glucosamine, a sugar specifically recognized by WGA. In the by macrophages (LDMC) is compared with ADMC and is dis LDMC reaction, macrophages in the presence of WGA could cussed as a possible candidate in vivo. kill other syngeneic and allogeneic tumor cells but not normal thymus or spleen cells. These findings suggest that WGA is a ligand in macrophage-mediated cytolysis, inducing the binding MATERIALS AND METHODS of effector cells to target cells that triggers off lysis of the target Mice. Male C3H/He mice, free from mouse mammary tumor cells. virus, were obtained from breeding colonies in the Institute of Comparative studies on the mechanisms of cytolysis involved Medical Science, University of Tokyo. in LDMC and ADMC showed that ADMC, but not LDMC, was Tumor Cells. MM46, a transplantable ascites tumor from a inhibited by aggregated ¡mmunoglobulin and by protease pre spontaneous mammary carcinoma in a C3H/He mouse, was treatment of macrophages. Thus, the mechanisms of recogni used for immunization and as a target of effector cells. MM48 tion in LDMC and ADMC are different, but both ligands can mammary carcinoma and MH134 hepatoma cells were also induce the lytic reaction. used as target cells. These tumors were passaged weekly in the peritoneal cavity of syngeneic C3H/He mice. INTRODUCTION Macrophage Monolayers. Glycogen-stimulated macro phages were used as effector cells. They were obtained 1 day Macrophage-mediated cytotoxicity against tumor cells has after i.p. injection of 4 mg of glycogen into C3H/He mice. been studied to clarify the mechanism of cytotoxicity involved Peritoneal cells were suspended in medium (Nissui Seiyaku in tumor rejection in vivo (1, 14). Thus far, 2 mechanisms of Co., Tokyo, Japan) supplemented with 10% heat-inactivated macrophage-mediated cytotoxicity of syngeneic tumor cells fetal calf serum (Grand Island Biological Co., Grand Island, N. have been reported: (a) macrophages activated by various Y.), 100 units of penicillin per ml and 100 jug of streptomycin stimuli or by tumor cell growth can provoke direct cytotoxicity per ml (RPMI-FCS). Samples of 7.5 x 10b cells were incubated of tumor cells (15, 16); and (b) stimulated macrophages can in flat-bottomed glass tubes (7 x 90 mm) at 37° for 2 hr to do so in the presence of antitumor antibody (12, 31). Nothing allow the cells to adhere to the glass. The medium was re is known about the mechanism by which activated macro moved, and the adherent cells (about 2 to 3 x 10'' cells/tube) phages recognize and kill tumor cells in either type of cytotox were washed 3 times with warm RPMI-FCS. These cells were icity, but it has been emphasized that the cytotoxicity requires cultured overnight in 0.5 ml of RPMI-FCS and then were used close contact between the macrophages and target cells (8, for cytolysis and cytoadherence assays. These adherent cells 14). We have investigated the mechanism of ADMC1 in a murine were macrophages by more than 95%, as determined by Giemsa stain, nonspecific esterase stain (18), and phagocyto Received December 26. 1979; accepted June 25. 1980 sis of carbon particles. 1This work was supported by a Grant-in-Aid for Scientific Research from the Antitumor Antibody. The immunization procedure used was Ministry of Education, Science and Culture, Japan. as described previously (30). Briefly, mice resistant to synge ' To whom requests for reprints should be addressed. ' Present address: Faculty of Pharmaceutical Sciences, Teikyo University, neic MM46 tumor were obtained by inoculation of tumor cells Sagamiko. Kanagawa 199-01, Japan. attenuated with mitomycin C (Kyowa Hakko Co., Tokyo, Japan) " The abbreviations used are: ADMC. antibody-dependent macrophage-me diated cytolysis; WGA. wheat germ agglutinin; LDMC, lectin-dependent macro penicillin (100 units/ml), and streptomycin (100 fig/ml); PHA. phytohemaggluti- phage-mediated cytolysis; RPMI-FCS, Roswell Park Memorial Institute Tissue nin; Con A. concanavalin A; UEA, Ulex europaeus agglutinin; SBA, soybean Culture Medium 1640 (Nissui Seiyaku Co . Tokyo. Japan) containing 10% heat- agglutinin; PWM. pokeweed mitogen; GlcNAc, N-acetylglucosamine: NANA, N- inactivated fetal calf serum (Grand Island Biological Co.. Grand Island. N.Y.), acetylneuraminic acid; LDCC, lectin-dependent cell-mediated cytotoxicity. 3798 CANCER RESEARCH VOL. 40 Downloaded from cancerres.aacrjournals.org on September 25, 2021. © 1980 American Association for Cancer Research. Lectin-dependent Macrophage-mediated Tumor Lysis and then by 4 challenges with fresh tumor cells. Immune serum Aggregated IgG. Human aggregated IgG was prepared as of resistant mice was purified first by gel filtration and then by described previously (5). Briefly, 20 mg of Cohn Fraction II chromatography on 2 types of ion-exchange column to obtain human IgG (Miles Laboratories, Inc., Elkhart, Ind.) were dis solved in 1 ml of Dulbecco's phosphate-buffered saline (0.01 the IgG 2a fraction with activity in ADMC (31). Reagents. PWM, UEA II, SBA, and PHA were purchased M sodium and potassium phosphate/0.14 M NaCI/0.003 M from E. Y. Laboratories, San Mateo, Calif. Con A, Bauhinia KCI) and heat aggregated at 63°for 20 min. The aggregates purpurea agglutinin, and UEA I were gifts from Dr. T. Osawa were precipitated by centrifugation at 150,000 x g for 60 min, homogenized in Dulbecco's phosphate-buffered saline, and (University of Tokyo). WGA was a gift from Dr. T. Terao (Uni versity of Tokyo) and was also purchased from E. Y. Labora centrifuged at 600 x g for 15 min before use. As a control, 20 tories. (All of the lectin preparations were purified by affinity mg of human IgG per ml without heat treatment were centri chromatography and showed a single band by disc gel electro- fuged at 150,000 x g for 60 min, and the supernatant was phoresis, except for PWM and UEA II which showed several used for assays. bands by disc gel electrophoresis.) Neutral sugars were prod Protease Treatment of Macrophages. Various concentra ucts of Wako Pure Chemical Industries, Ltd., Osaka, Japan, tions of trypsin (Difco Laboratories, Detroit, Mich.) or Protein- and /V-acetylneuraminic acid was a product of Sigma Chemical ase K (Boehringer Mannheim GmbH, Mannheim, West Ger Co., St. Louis, Mo. many) were added to macrophage monolayers in the flat-bot Cytolysis Assay. Antibody-dependent or lectin-dependent tomed tubes in 0.5 ml of Roswell Park Memorial Institute Tissue cytolytic activity of macrophages was measured by determining Culture Medium 1640 without fetal calf serum. The mixtures 51Cr release from labeled target cells, essentially as described were incubated at 37° for 30 min, and then protease was previously (30). Briefly, 7.5 x 103 target cells were added to removed by decanting the supernatant and by washing the the macrophage monolayers in the flat-bottomed glass tubes monolayers 3 times. These treated macrophages were used in 0.5 ml of RPMI-FCS with antitumor antibody or lectins. The for cytolysis and Cytoadherence assays. mixtures were cultured at 37°for 8 hr, and then the radioactiv ity of the supernatant was measured. Cytolysis was defined as RESULTS follows: Lectin-dependent Cytoadherence and Cytolysis. In an at Experimental count i of 6'Cr release = x 100 tempt to determine whether lectins as well as antitumor anti Maximum releasable count body can induce macrophage-mediated tumor lysis, 8 lectins Experimental count - control count were tested for their ability to induce the binding of effector to % of cytolysis = x 100 Maximum releasable count - control count target cells and lysis of the target cells. Results showed that the lectins WGA, Con A, PHA, and PWM could cause the Maximum release of b'Cr was measured after freezing and marked Cytoadherence of macrophages to tumor cells (Chart thawing labeled tumor cells 3 times; it was equivalent to 70 to 1). SBA and UEA II also caused Cytoadherence, but B. purpu 80% of the total cell-associated isotope. The control count was rea agglutinin and UEA I had no effect even at a concentration measured as the radioactivity released spontaneously from of 90 /ig/ml.
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