Centro di Studi Nucleari della Casaccia, Roma Laboratorio di Radiopatologia, Gruppo CNEN-Euratom di Immunogenetica
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1 Centro di Studi Nucleari della Casaccia, Roma Laboratorio di Radiopatologia, Gruppo CNEN-Euratom di Immunogenetica T CELL INDEPENDENT INDUCTION OF ANTIGEN SPECIFIC SUPPRESSION OF THE ANTIBODY RESPONSE* LUCIANO ADORINI DIANA BORASCHI GINO DORIA The immune system is characterized by a series of very precise regulatory mechanisms in which the interplay and the balance between cells and soluble factors with reciprocally countermanding activities determine the net outcome of the immune response, The existence of a feedback mechanism by which specific antibodies can influence the antibody response is firmly established, albeit not completely defined 19,24 On the other hand, T cell subsets endowed with helper or suppressive properties have a fundamental role in the regulation of the immune response 2I Suppression of the immune response can be achieved by different mechanisms in different experimental conditions. Antibodies or antigen-antibody complexes are known to induce specific suppression of the antibody response in vivo and in vitro 20 and suppressor T cells to play a fundamental role in many forms of suppression 7,22. In some cases suppressor T cells are generated by specific antibodies as in chronic allotype suppression 10 or in idiotype suppression 6,16. To assess the relative contribution of these two regulatory pathways, the antibody mediated and the T cell mediated, we have examined the suppression of the immune response in vitro to a hapten-carrier conjugate. Spleen cells from HRBC 2 immune mice (immunized with 2x10 7 HRBC 14 days before culture) give Key-words: Antibody response; Immune spleen cells; Immune system; Immunosuppression; T cells. * This work was supported by CNEN-Euratom association contract. It is publication no of the Euratom Biology Division. Abbreviations used: anti-t = rabbit anti-rat brain serum; C = guinea pig complement; FCS = fetal calf serum; HRBC = horse red blood ceils; PFC = plaque4orming cells; SRBC = sheep red blood cells; TNP = trinitrophenyl. Accepted for publication on October 8, La Ricerca Clin. Lab. 9, 351,
2 T CELL INDEPENDENT INDUCTION OF ANTIBODY RESPONSE SUPPRESSION a lower anti-tnp response, when challenged in vitro with TNP-HRBC, than spleen cells from HRBC carrier-primed mice (primed with 2x10 s HRBC 3 days before culture). In mixing experiments the immune spleen cell population was shown to suppress the anti-tnp-hrbc response of the carrier-primed ceii population. The results indicate that, in the experimental system used, suppression is induced by antigen specific product of cells other than T cells. MATERIALS AND METHODS Mice - Male (C57BL/6 x DBA/2)F~ mice were used throughout these experiments. Mice were from our breeding colony and used at 3-4 months of age. Irradiation - Mice received 2,000 R total-body x-ray dose 15 rain before spleen removal. Irradiation conditions have been previously described 3. Antigens - SRBC and HRBC were purchased from Sclavo, Italy. TNP-HRBC was prepared according to KETTMAN and DUTTON 14 Immunizations - To induce carrier-primed spleen cells, mice were injected i.v. with 2x10 s HRBC 3 days before in vitro culture 4. Suppressive activity was induced by immunization with a single i.v. injection of 2x107 HRBC 2 weeks before culture. Alternatively, mice were immunized with 10 ~~ HRBC i.p. together with 2x109 killed Bordetella pertussis bacilli, boosted 7 days later with 10 '~ HRBC i.p. and their spleen ceils cultured after 1 week. Cell separations - Spleen ceils were separated by nylon wool column technique as described by JULIUS et al. 13. Briefly, 5x108 spleen cells were loaded on nylon wool columns prepared packing 3.5 g of nylon woot in 50 ml syringes. Non-adherent cells were eluted dropwise with medium whereas adherent cells were harvested by repeated compression of the nylon wool. Cell viability of both populations was >90% as judged by trypan blue exclusion. Non-adherent ceils were 30-35% of the loaded cells and >90% of this population was killed by anti-t serum and complement treatment. Enriched B cell populations were prepared by incubating (60 min at 37"C) 7.5 ml spleen cells (2x107/ml) with 0.5 mi undiluted anti-t serum and 3 ml of agar-adsorbed guinea pig complement diluted 1:3. Anti-T serum adsorbed twice with C3H mouse brain (18 h at 4 "C) was used as control serum. Anti-T serum was rabbit anti-rat brain prepared according to GOLUB 9. This serum and complement treatment killed about 40% of spleen ceils and >95% of thvmocytes. Spleen cell mitotic reactivity to PHA and Concanavalin A (Con A), after the aforementioned treatment, was reduced to < 10% of the control values whereas the LPS response was unaffected. Cell cultures - Mishell and Dutton culture conditions were used's. Culture medium was RPMI 1640 supplemented with 10% FCS, 1 mm sodium pyruvate, 0.1 mm non-essential amino acid mixture, 100 IU/ml penicillin and 100 btg/ml streptomycin sulphate, 2 mm L-glutamine and 20 mm HEPES. Usually 2x107 spleen ceils were cultured in 1 ml of medium in plastic dishes with 2x10 s TNP-HRBC or 107 SRBC, without 2-mercaptoethanot added to the culture. Cultures were fed daily with nutritional cocktail. Duplicate cultures were harvested on days 3 to 6 of culture and tested for direct PFC by the Jerne plaque assay is using TNP-SRBC or SRBC 352
3 L. ADORINI, D. BORASCHI, G. DORIA or HRBC. Results are expressed as PFC per culture and the net anti-tnp response was calculated by subtracting the anti-srbc background from the anti-tnp-srbc PFC response. Background was very low, usually less than 196 of the specific response. RESULTS Suppressive activity of immune spleen cells - Carrier-primed spleen cells were from mice iniected with 2x10 s HRBC i.v. 3 days before culture. This celt population displayed optimal helper activity in the in vitro antibody response to TNP-HRBC 4 and hereafter is designated as helper cell population. Immune spleen cells were from mice primed 14 days before culture with 2x10 s or 2x10 7 HRBC. Helper and immune spleen cells were cultured alone or mixed together in various proportions, with 2x10 s TNP-HRBC and assayed on days 3 to 6 of culture for direct anti-tnp PFC. Results in fig. 1 refer to the anti-tnp response on day 4 of culture of one out of 3 experiments with similar results. Immune spleen ceils give a much lower response as compared to helper cells. Ability of immune spleen cells to suppress the Fig. 1 - Suppressive activity of immune spleen cells. MishelI-Dutton culture conditions, 2x105 TNP-HRBC/culture. Panel A: titration of anti-tnp PFC response. Spleen cells were from mice unimmunized (o o) or primed with 2xI0 s HRBC 3 days before culture (* -) or primed with 2x105 HRBC 14 days before culture (~. A) or immunized with 2x107 HRBC 14 days before culture (A A). Panel B: suppression of anti-tnp PFC response by immune spleen cells. Eight x 106 helper spleen ceils (from mice given 2x105 HRBC 3 days before culture) were cultured alone (o) or mixed with 4, 8, or 12x106 spleen cells from mice unimmunized (D ~) or primed with 2x10 s HRBC 14 days before culture (m -m) or immunized with 2x107 HRBC 14 days before culture (8 g). 353
4 T CELL INDEPENDENT INDUCTION OF ANTIBODY RESPONSE SUPPRESSION immunogen in culture 10 7 helper ~ cells in culture with 10 7 spleen cells from mice days of culture PFC/culture PFC/culture PFC/culture anti-tnp anti-srbc ~nti-tnp anti-srbc anti-tnp anti-srbc TNP-HRBC Or" SRBC normal immune b 4, ,900 3, ,490 5,060 3, ,830 TNP-HRBC and SRBC normal immune b 2,990 1, ,730 8,940 1,920 1,160 8,760 4,960 1, ,970 Misheli-Dutton culture conditions, 2x10 5 TNP-HRBC or 10 7 SRBC/culture. Spleen cells from mice primed with 2x10 s HRBC i.v. 3 days before culture; b spleen cells from mice primed with 2x10 7 HRBC i.v. 14 days before culture. Tab. 1 - Antigen specificity of the suppressive activity of immune spleen cells. response of the helper cell population was tested by adding to 8x10 6 helper cells 4, 8 or 12x10 6 normal spleen ceils or spleen ceils from mice immunized with 2x10 s or 2x10 7 HRBC 14 days before culture. Suppression is present only when the relatively high dose (2x10 7) was used for priming. Under our conditions 2x10 7 spleen ceils per culture gave the best response and this cell dose was chosen for further experiments. Since a good and reproducible suppression was obtained by immunizing with 2x10 7 HRBC 2 weeks before culture, this schedule of immunization was selected to study in some detail the suppressive activity of immune spleen cells. Antigen specificity o/suppression - To ascertain antigen specificity of suppression, a mixture of 10 7 HRBC immune spleen cells and 10 7 helper ceils was cultured with TNP-HRBC and SRBC in the same dish or with each immunogen in separate dishes. Cultures were assayed for anti-tnp and anti-srbc PFC. The results demonstrate that suppression is carrier specific because only the anti-tnp and not the anti-srbc response is suppressed by immune spleen cells (tab. 1). The suppressive effect exerted by HRBC-immune spleen ceils could not be ascribed to partial coating of TNP-HRBC by anti-hrbc antibodies secreted in culture, because suppression was unchanged, and even slightly increased, by adding 5 times the standard dose of TNP-HRBC to cultures (data not shown). T cells are not required ~or suppression - Helper spleen cells (2x10 s HRBC 3 days before culture) were mixed with immune (2x10 7 HRBC 14 days before culture) spleen ceils pretreated with anti-t serum and C and cuttured with TNP-HRBC or SRBC (tab. 2, exp. 1). Suppression induced by HRBC immune spleen cells is exerted on both anti-tnp and anti-firbc PFC responses. Suppressive activity persists after anti-t treatment of immune spleen cells, indicating that suppression is not mediated by T cells present in the immune population. Non-specific cytotoxicity of anti-t serum treatment was ruled out by the similar primary anti-srbc response. The same experiment was repeated using two different protocols to obtain immune spleen cells (tab. 2, exp. 2A). In addition to the standard protocol 354
5 L. ADORINI~ D. BORASCHI~ G. DORIA mice were immunized with 10 l~ I-IRBC together with 2x109 Bordetella pertussis i.p. 14 days before culture and boosted with 10 m HRBC 7 days before culture. The results demonstrate that in neither case is suppressive activity mediated by T cells of the immune population and that the level of suppression is similar in both priming regimens. Efficiency of anti-t serum treatment is demonstrated by the reduction of the primary response of normal spleen cells to SRBC (tab. 2, exp. 2B). To ascertain if suppressive activity could be mediated by thymocytes, mice were immunized with 2x107 HRBC i.v. 14 days before culture and their thymic or spleen cells were mixed with HRBC-primed helper ceils (2x10 ~ HRBC 3 days before culture). Cell mixtures were cultured with TNP-HRBC and assayed for direct anti-tnp PFC response on day 4 and 5 (tab. 3). Immune thymocytes do not appear 107 helper cells ~ in culture with 107 spleen ceils from mice days of culture 4 5 PFC/culture PFC/culture anti-tnp anti-hrbc anti-srbc anti-tnp anti-hrbc anti-srbc normal 13,740 10,5t ,440 16,360 5,350 immune (2x107) ~ 1, , ,620 immune (2x107) anti-t+c 1, , ,080 immune (2x10 r) anti-t adsorbed + C 2,930 1, , ,380 2A normal 4,765 4,650 3,875 4,160 1,870 1,380 normal anti-t+c 4,385 2,190 n.t. 3,540 1,750 n.t. immune (2x107) 3,680 2,620 2,510!, ,280 immune (2x107) anti-t+c n.t. 1,060 1,160 n.t. immune (2x10 ~~ = 1,630 1, ,260 immune (2x10 m) anti-t+c n.t n.t. 2B 2x107 normal x107 normal anti-t + C x107 normal anti-t adsorbed + C 98O 650 Mishell-Dutton culture conditions, 2xi0 s TNP-HRBC or 107 SRBC/culture. All ceil mixtures are 107 helper normal or immune spleen ceils. Helper ceils are from mice primed with 2x105 HRBC i.v. 3 days before culture; b s)ieen ceils from mice primed with 2x107 HRBC i.v. 14 days before cuiture; c spleen cells from mice primed with 10 ~ HRBC and 2x109 Bordetella pertussis i.p. and boosted with 10 l~ HRBC 7 days before culture; n.t. = not tested. Tab. 2 - Persistence of suppressive activity after anti-t treatment of the immune spleen cells irrespectively of the priming regimen. 355
6 T CELL INDEPENDENT INDUCTION OF ANTIBODY RESPONSE SUPPRESSION i0 v helper ~ spleen ceils in culture with 10 v day 4 PFC anti-tnp/cuhure day 5 normal spleen ceils 2,820 2,330 immune b spieen celis 1, normal thymus cells 3,190 2,660 immune thymus cells 2,420 3,220 Mishell-Dutton culture conditions, 2x10 s TNP-HRBC/cuhure. SpIeen cells from mice primed with 2x10 s HRBC i.v. 3 days before culture; b spleen cells from mice primed with 2x107 HRBC i.v. 14 days before culture. Tab. 3 - Absence of suppressive activity in thymocytes from immune mice. PFC anti-tnp/cuhure 10 7 helper ~ spleen cells in culture with 10 7 days of culture exp. I exp. 2 exp. 1 exp. 2 exp. 1 exp. 2 normal ceils 4,020 2,480 13,000 2,970 n.t. 1,490 nylon non-adherent normal cells 1,790 n.t. 8,020 n.t. 3,970 n.t. nylon adherent normal ceils immune b cells 1,770 n.t. 1, ,520 n.t. 3, ,800 n.t. 700 i45 nylon non-adherent immune cells 2,050 1,400 5,I80 1,930 3,600 1,230 nylon adherent immune ceils 1, , Mishell-Dutton culture conditions, 2x10 s TNP-HRBC/cuhure. Spleen cells from mice primed with 2x105 HRBC i.v. 3 days before culture; b spleen ceils from mice primed with 2x107 HRBC i.v. 14 days before culture; n.t. = not tested. Tab. 4 - Presence of suppressive activity in nylon adherent immune spleen ceils. to exert any suppressive activity, whereas this is clearly displayed by immune spleen ceils obtained from the same mice. Presence of suppressive activity in nylon zvool adherent immune spleen cells - Nylon wool cell separation was performed on normal or immune (2x days before culture) spleen cells. Adherent as well as non-adherent normal or immune spleen cells were mixed with helper cells, cultured with TNP-HRBC and direct anti-tnp PFC evaluated on clays 3 to 5 of culture in 2 separate experiments (tab. 4). The resuhs indicate that suppressive activity is primarily exerted by the nylon wooi-adherent immune cell populations. Suppressive activity is very radioresistant - Radiosensitivity of suppressive activity was examined by irradiation of normal or immune mice with 2,000 R x-ray dose 15 rain before spleen removal. Spleen cells from irradiated mice were mixed 356
7 L. ADORINI, D. BORASCHI, G. DORIA with helper spleen cells and cultured, in separate dishes, with TNP-HRBC or SRBC. Data in tab. 5 demonstrate that specific suppressive activity is not impaired by x-ray doses as large as 2,000 R. Although irradiation of normal mice had a detrimental effect on the PFC response, probably due to a lower number of viable cells in culture, suppression is evident, specific, and radioresistant. Two other experiments performed under the same conditions gave similar results. Suppressive activity of supernatants from cultures of immune spleen cells - Two x 107 normal spleen ceils or 2x107 immune spleen cells were cultured for 3 days with or without TNP-HRBC. Two x 107 helper ceils were resuspended in undiluted cell-free supernatants and cultured together with TNP-HRBC or, in separate dishes, SRBC. From days 3 to 5 of culture direct anti-tnp and anti-srbc PFC responses were measured in 2 separate experiments. As demonstrated in tab. 6, when supernatants from normal spleen ceils are added to helper cells the anti-tnp and anti-srbc PFC responses are increased, as compared to control values, because supernatant is a 'conditioned' medium. On the other hand, when supernatants from immune spleen ceils are added to helper ceils the anti-tnp PFC response is specifically suppressed. No difference is observed comparing the suppressive activity of supernatants from cultures of immune spleen cells with or without TNP-HRBC. DISCUSSION We have examined a model of antigen specific suppression in which spleen cells from HRBC immune mice are able to suppress the response of HRBC carrier-primed spleen cells to the TNP-HRBC conjugate. This suppression could not be ascribed to suppressor T cells in the immune spleen cell population for the following reasons: a. suppression is not eliminated by anti-t treatment of the immune population; b. suppression is resistant to a 2,000 R in vivo x-irradiation. Suppressor T cells have been found to be very radiosensitive, doses as low as 400 R in vitro 5 or 150 R in vivo t7 being sufficient to inactivate them; c. suppression 10? helper ~ cells in culture with 10 7 spleen cells from mice days of culture PFC/culture PFC/culture PFC/culture anti-tnp anti-srbc anti-tnp anti-srbc anti-tnp anti-srbc normal 13, ,440 5,350 17,280 9,410 normal irradiated b 5, ,520 2,410 7,550 5,350 immune c 1, ,100 7, ,850 immune irradiated 1, ,030 3, ,040 Mishell-Dutton culture conditions, 2x10 s TNP-HRBC or 107 SRBC/cutture. Spleen cells from mice primed with 2x105 HRBC i.v. 3 days before culture; b spleen ceils from mice exposed to 2,000 R total body x-ray dose 15 rain before sacrifice; spleen cells from mice primed with 2x107 HRBC i.v. 14 days before culture. Tab. 5 - Radioresistance of the suppressive activity in spleen ceils from immune mice. 357
8 T CELL INDEPENDENT INDUCTION OF ANTIBODY RESPONSE SUPPRESSION days ok culture spleen cells in culture PFC/culture PFC/cuhure PFC/culture anti-tnp anti-srbc anti-tnp anti-srbc anti-tnp anti-srbc 2x107 normal 2x107 helper a 2x107 immune b 107 helper normal 107 helper+ 107 immune 2x107 helper + SN (without TNP-HRBC) 2x107 helper + SN (with TNP-HRBC) 2x10 v helper+si d (without TNP-HRBC) 2x10 v helper + SI (with TNP-HRBC) 1, , , , , , , , , ,460 3,780 8,790 10,900 4,080 8,760 10,800 8, ,000 18,160 I8,260 22,080 15, , ,080 1,200 6,120 2,970 13, ,420 2,610 25, ,780 6,300 34,380 5,460 21, , ,370 Mishell-Dutton culture conditions, 2x10 s TNP-HRBC or 107 SRBC/culture. = Spleen ceils from mice primed with 2x105 HRBC i.v. 3 days beeore culture; b spleen ceils from mice primed with 2x107 HRBC i.v. 14 days before culture; c supernatant from day 3 culture of normal spleen ceils (cultured with or without TNP-HRBC); a supernatant from day 3 culture of immune spleen ceils (cultured with or without TNP-HRBC). Tab. 6 - Suppressive activity of supernatant from cultures of immune spleen calls. is exerted by nylon wool-retained but not by nylon wool-passed spleen cells. In most suppressive systems studied suppressor T cells have been found to be not adherent to nylon wool. However, there are exceptions 1,; d. suppression is mediated by spleen ceils but not by thymocytes. Usually, when suppressor ceils are induced they are present both in the thymus and the spleen. As an example, OKUMURA and TADA iv demonstrated, in an adoptive transfer system, that thymocytes and spleen ceils from mice primed with HRBC contain specific suppressor T cells able to transfer suppression; e. an antigen specific suppressive factor is present in culture supernatants of immune spleen cells. The production of this suppressive factor by ceils other than T cells is also compatible with the finding that no suppressive activity has been detected in culture supernatants during the induction of SRBC-specific suppressor T cells 5 The same evidence that stands against a T cell induced suppression could be construed as indication for an antibody-secreting cell-mediated phenomenon. As a matter of fact, the cells inducing suppression were found to be T negative, radioresistant, adherent to nylon wool, present in the spleen but not in the thymus and actively secreting their products. Others have reported the existence of antibodymediated, T cell independent suppression of the antibody response. TAKaTSU et al. 23 have shown that anti-carrier antibodies can suppress the anti-hapten and the anti-carrier responses without affecting specific helper T ceils. Thus, regulation by antibody feedback seems to be restricted to B cells only. OI~DAL et al. as have found 358
9 L. ADORINI, D. BORASCHI, G. DORIA that C3H mice, genetically non responder to the synthetic polypeptide poly(l-tyrosine-l-glutamic acid)-poly(d,l-alanine)-poly(l-lysine), (T,G)-A--L, can produce a primary IgM response to this antigen. After challenge, the switch to IgG production was found to be suppressed by antibody (IgM) mediated feedback. This mode of suppression has been interpreted as T cell independent. In the experiments described in the present paper, T cells were not found to be involved in the induction of suppression even when high doses of carrier were injected. This result is at variance with reports of suppressor T cell induction after high doses of carrier priming s,2s. The reason for this discrepancy is not clear but it is possible that both antibody mediated and T cell mediated mechanisms are inducible and that subtle variation in experimental conditions may favour activation and/or detection of one of them. Secretion in culture of antibodies with suppressive properties has been recently confirmed. In a modified Marbrook-type culture system, using Nuclepore membrane, the presence of immunoadsorbents in the reservoir continuously removing antibodies and antigen-antibody complexes being formed, was able to significantly increase the response over control values 1. The experiments presented here were not directly aimed at sorting out the mechanism of antibody mediated suppression and more information is needed before reaching a firm conclusion. In the experimental system examined suppression does not appear to result from antigen masking by antibody nor to involve suppressor T cells in its induction. Thus, it is conceivable that anti-carrier antibodies can suppress hapten-specific and carrier-specific B ceils by means of hapten-carrier conjugate bound to B cell receptors. This could represent one of the many mechanisms through which the immune system regulates antibody production. SUMMARY Immune spleen cells (from mice given 2x107 HRBC 14 days earlier) when mixed in vitro with carrier-primed syngeneic spleen cells (from mice given 2x10 s HRBC 3 days earlier) are able to suppress the anti-tnp and anti-hrbc PFC response to TNP-HRBC. If immune thymocytes are substituted for spleen cells suppression is not observed. This suppression is antigen specific, resistant to anti-t treatment or x-irradiation, and is exerted by nylon wool-retained ceils of the immune spleen cell population. An antigen specific suppressive factor is released from immune spleen cells in culture. Under these experimental conditions, suppression appears to be mediated by a specific product of B rather than T ceils present in the immune spleen cell population. REFERENCES 1. ADORINI L., EIPERT E.F., COUD~C J.: Immunoadsorbent removal of antibodies produced during in vitro culture relieves inhibition of the response - Cell. Immunol. 47, 356, CHIORAZZI N., FOX D.A., KATZ D.H.: Hapten-specific IgE antibody responses in mice. VII. Conversion of IgE 'non responder' strains to IgE 'responders' by elimination of suppressor T cell activity - J. Immunol. 118, 48, DORIA G., AGAROSSI G.: Thymus dependence of adoptive immunity in irradiated mice - Transplantation 6, 218, DORIA G., AGAROSSI G., BORASCHI D., AMENDOLEA M.A.: Effects of carrier priming on antibody avidity in the in vivo and in vitro immune response - Immunology 32, 539, EARDLEY D. D., GERSHON R. K.: Induction of specific suppressor T cells in vitro - J. Immunol. 117, 313, EICHMANN K.: Idiotype suppression. II. Amplification of a suppressor T ceil with anti-idiotypic activity - Europ. J. Immunol. 5, 511, GERSHON R.K.: T cell control of antibody production - Contemp. Top. Immunobiol. 3, 1,
10 T CELL INDEPENDENT INDUCTION OF ANTIBODY RESPONSE SUPPRESSION 8. GERSHON R.K., KONDO K.: Cell interactions in the induction of tolerance: the role of thymic lymphocytes - Immunology 18, 723, GOLUs E.S.: Brain associated antigen: reactivity of mouse anti-brain with mouse lymphoid cells - Cell. Immunol. 2, 353, HERZENBERG L.A., OKUMURA K., METZLER C.M.: Regulation of immunoglobulin and antibody production by allotype suppressor T cells in mice - Transplant. Rev. 27, 57, HODES R.J., HATHCOCK K.S.: In vitro generation of suppressor cell activity: suppression of in vitro induction of cell-mediated cytotoxicity - J. Immunol. 116, 167, JERNE N.K., NORDIN A.A.: Plaque formation in agar by single antibody-producing ceils - Science 140, 405, JULIUS H. M., SIMPSON E., HERZENBERG L.A.: A rapid method for the isolation of functional thymus-derived murine lymphocytes - Europ. J. Immunol. 3, 645, KETTMAN J., DUTTON R.W.: An in vitro primary response to 2,4,6-trinitrophenyl substituted erythrocytes. Response against carrier and hapten - J. Immunoi. 104, 1558, MISHELL R. I., DUTTON R. W,: Immunization of dissociated spleen cell cultures from normal mice - J. exp. Med. 126, 423, NISONOr~ A., Ju S.-T., OWEN F.L.: Studies of structure and immunosuppression of a cross reactive idiotype in strain A mice - Immunol. Rev. 34, 89, OKUMURA K., TADA T.: Suppression of hapten-specific antibody response by carrier specific T ceils - Nature (New Biol.) 245, 180, ORnAL J., SMITH S., NESS D., GERSHON R,K., GRUMET F.C.: IgM-mediated, T cell-independent suppression of humoral immunity - J. Immunol. 116, 1182, ROWLEu D.k., FITCH F. W., STUART F. P., KOHLER H., COSENZA I~I.: Specific suppression of immune responses - Science 182, 1133, SINCLAIR N.R. St. C.: Immunoregulation by antibody and antigen-antibody complexes - Transplant. Proc. 10, 349, SNELL G.D.: T cells, T ceil recognition structures, and the major histocompatibility complex - tmmunoi. Rev..38, I, TADA T., TANIOUCHI M., TAKEMORI T.: Properties of primed suppressor T cells and their products - Transplant. Rev. 26, 106, TAKATSt,r K., HAMAOKA T., KITAGAWA M.: Antibody production in mice. VI. Effect of anticarrier antibody on cellular cooperation in the primary anti-hapten antibody response - Immunology 26, 233, UHR J.W., MOILER G.: Regulatory effect of antibody on the immune response - Advanc. Immunol. 8, 81, WEITZMAN S., SHEN F.W., CANTOR H.: Maintenance of hyporesponsiveness to antigen by a distinct subclass of lymphocytes - J. Immunol. 117, 2209, Requests for reprints should be addressed to: LUCIANO ADORINI Centro di Studi Nucleari della Casaccia Laboratorio di Radiopatologia Gruppo CNEN-Euratom di Immunogenetica S.P. Anguillarese km , Roma - Italia 360
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