delayed-type hypersensitivity [T cell (thymus-derived)/macrophlage/ir gene/cell-mediated immunity/altered self]
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1 Proc. Natl. Acad. Sci. USA Vol. 73, No. 7, pp , July 1976 Immunology Role of major histocompatibility complex gene products in delayed-type hypersensitivity [ (thymus-derived)/macrophlage/ir gene/cell-mediated immunity/altered self] J. F. A. P. MILLER, M. A. VADAS, ALISON WHITELAW, AND JENNIFER GAMBLE The Walter and Eliza Hall Institute of Medical Research, P.O. Royal Melbourne Hospital, Victoria 3050, Australia Communicated by Baruj Benacerraf, May 7, 1976 ABSTRACT Sensitized thymus-derived (I) lymphocytes can transfer delayed-type hypersensitivity (DTH) to naive mice only if there is identity at the major histocompatibility complex (MHC). The MHC region responsible differs according to the antigen used for sensitization. For transfer of DTH to fowl gamma globulin identity at I-A is necessary; for dinitrofluorobenzene, however, identity at either K, D, or I region is sufficient. s of one genotype, sensitized in a chimeric environment, transferred DTH to both parental strains even though these were MIC incompatible. However, s from F1 hybrid mice, sensitized not in the F1 but in one parental strain, transferred DTH only to that parental strain, not to the other, in contrast to F1 s sensitized in the F1 which could transfer DTH to both parental strains. Macrophages pulsed with antigen in vitro could be used to sensitize syngeneic or semi-allogeneic mice for the transfer of DIH. Transfer was, however, successful only in the strain syngeneic to that from which the macrophages were derived. Evidence is also presented that genetically lowresponder mice can be made to exhibit DTH provided they are pretreated with cyclophosphamide two days before sensitization. When considered in toto these results strongly argue in favor of the notion that there are receptors on activated s which recognize antigenic determinants and MHC gene products. The implications of these findings are discussed in relation to the role of macrophages in antigen presentation and to the possible parallel evolution of MHC gene products and of receptors for antigen. Many activities of thymus-derived (T) cells are regulated by genes of the major histocompatibility complex (MHC). Thus, in the guinea pig, compatibility at the MHC was required for macrophage-associated antigen initiation of proliferation of sensitized lymphocytes (1). In the mouse, cooperative interactions between helper s and antibody-forming precursor (B) cells or macrophages required identity at the I region of the MHC, both in vivo (2) and in vitro (3). Specific lysis of virusinfected or chemically modified target cells occurred effectively only when the cytotoxic T lymphocytes and their targets were MHC compatible, the genes required for this interaction mapping in the K or D, but not I, regions (4, 5). By contrast, transfer of delayed-type hypersensitivity (DTH) to protein antigens by sensitized s was successful only in I-A compatible recipients (6). The inability to transfer DTH in incompatible recipients could not be attributed to rejection of the injected cells, to their total recruitment into areas such as the spleen, nor to their engagement in a mixed lymphocyte reaction (6). Thus, for example, DTH was successfully transferred from Abbreviations: T lymphocytes, thymus-derived lymphocytes; B cell, bone-marrow-derived lymphocyte; DNFB, 2,4-dinitro-1-fluorobenzene; DTH, delayed-type hypersensitivity; FGG, fowl gamma globulin; 125I-dUrd, 5-[12Iliodo-2'-deoxyuridine; L/R l25i-durd uptake, ratio of radioactivity of left ear to radioactivity of right ear; MHC, major histocompatibility complex; TBMC, tetraparental bone marrow chimera. sensitized F1 mice to naive mice of the parental strain that are competent to reject the F1 cells. The requirement for compatibility at some genes of the MHC for DTH transfer may be taken to indicate that effective interaction between sensitized lymphocytes and cells presenting antigen (probably macrophages) are governed by cell surface structures coded by MHC genes. The genetic constraints imposed on this interaction may be explained in one of two ways. (1) It is possible that the antigen binding receptor on the has a combining site directed towards a structure on the macrophage that represents an antigen-associated modification of the I region determinant or, alternatively, an I region modification of the processed antigen. This, represented diagrammatically in model I of Fig. 1, is based on the model favored by Doherty, Blanden, and Zinkernagel (4) to explain the genetic constraints imposed by the K and D regions of the MHC for cytotoxic T lymphocytes. (2) An alternative possibility envisages the receptor as a compound, with one part being the combining site directed towards the antigen and the other part consisting of a cell interaction molecule coded by the I region which is not a receptor for antigen. The would become effective only if two reactions occurred at its surface: one would be the binding of the antigen to the combining site, and the other would be some conformational change induced in the cell interaction molecule after matching another identical molecule on the surface of the macrophage. This model (shown as model II in Fig. 1) is based on the postulate by Katz and Benacerraf (2) of the existence of cell interaction molecules to explain the failure of cooperative interactions between allogeneic T and B cells in secondary antibody responses. We report here experiments, using three different approaches, that indicate that s involved in DTH perceive both MHC-coded cell surface molecules and processed antigen. MATERIALS AND METHODS Mice. Female mice (2- to 3-month-old) were used for sensitization and as recipients of sensitized cells. Highly inbred specific pathogen-free CBA/CaH Wehi, C57BL/6JWehi, and BALB/cAnBrWehi, and F1 hybrids between CBA and C57BL and between CBA and BALB/c mice were maintained in conventional rooms for the duration of the experiments. The.congenic lines of A.TH and A.TL were bred in conventional rooms in our Institute. Male and female athymic CBA.nu and BALB/c.nu mice derived from the seventh to eighth backcross generation of nude (nu/nu) mice to CBA or BALB/c were used. T Cell Reconstitution of nu/nu Mice. The mice were given, on three occasions 1 week apart, a mixture of syngeneic or (CBA X BALB/c)Fl thymus and lymph node cells intraperitoneally. During this interval the mice were no longer in the specific 2486
2 Immunology: Miller et al. Proc. Natl. Acad. Sci. USA 73 (1976) 2487 Table 1. Identity at the D and K regions allows DTH transfer to DNFB but not to FGG MHC of recipients* L/R '25I-dUrd uptaket Source of sensitized cells Recipients K I-A I-B I-C S D DNFB FGG A.TL A.TL s k k k k d 3.70 ± ± 0.12 A.TL A.TH s s s s s d 2.58 ± ± 0.04 A.SWt A.TL s k k k k d 2.03 ± ± 0.07 A.SW A.TH s s s s s d 2.78 ± ± 0.16 C57BL C57BL b b b b b b 5.50 ± ± 0.26 C57BL B1O.A(2R) k k k d d b 3.21 ± ± 0.03 CBA CBA k k k k k k 2.06 ± ± 0.16 CBA A.TL s k k k k d 2.72 ± ± 0.28 * Letters in italic bold face point to region of difference between donor and recipient mice. t Values are arithmetic mean + 1 SEM. Five to six mice per group. t TheMHCofA.SWmiceisssssss. pathogen free unit but were kept in sterile cages and given sterile food and water. Tetraparental Bone Marrow Chimeras (TBMC). TBMC were obtained by injecting lethally irradiated (950 roentgens, coulombs/kg) (CBA X C57BL)F1 hybrids with 107 anti-thy-l-treated bone marrow cells from both parental strains. These mice were kept, in specific pathogen free environment, for 2 months before use. Sensitization. Two days before sensitization mice were given 200 mg/kg (reduced to 150 mg/kg for nu/nu mice) of cyclophosphamide (Endoxan-Asta) subcutaneously to allow maximal levels of sensitization to all forms of antigen. Sensitization to fowl gamma globulin (FGG) and dinitrofluorobenzene (DNFB) have been described previously (6). For sensitization to the B isoenzyme of porcine lactic dehydrogenase, the antigen was emulsified in complete Freund's adjuvant and 0.1 ml (containing 20,ug of the isoenzyme) was injected into the two hind footpads and subcutaneously into the abdominal region. For sensitization with macrophage-associated antigen, 107 mouse peritoneal exudate cells (75-85% macrophages) were incubated at 370 for 60 min in 1 ml of Hanks' balanced salt solution containing 10% fetal calf serum and 100lug of FGG. The cells were washed four times in cold medium and counted. The residual antigen has been estimated to be ug/3 X 106 macrophages. Viable antigen-pulsed macrophages (3 X 106) were then injected intravenously into cyclophosphamide pretreated mice. Transfer of Sensitized State. For transfer, peripheral lymph 1 cen receptor for gfta.ed sew MM00L It Compound * weptn (Strain X) (stroin X) (Trui.X -Ag CI * A combining ind wcde combining site site O rin I(Strin)I vmi -A^9 FIG. 1. Hypothetical models used to explain genetic constraints imposed on T lymphocyte-macrophage interactions (see text). X and Y indicate hypothetical MHC- incompatible strains of mice. I, I-region determinant "a" or "b"; MO, macrophage; Ag, antigen "1". A third model, mentioned in the text, is not shown here. node cells and spleen cells were taken from mice 5 days after sensitization and injected intravenously into naive mice (6). Test for DTH. The sensitized mice and naive recipients of sensitized cells were tested for DTH by the radioisotopic ear method with use of 5-['25I]iodo-2'-deoxyuridine ('25I-dUrd) and radiometry as described previously (6). Briefly, the mice were challenged with antigen in the left ear and then injected intraperitoneally with 0.1 ml of 1 mm 5-fluorodeoxyuridine followed by 2 1ACi of 125I-dUrd (specific activity AiCi/g, Radiochemical Centre, Amersham, U.K.). The mice were killed 24 hr later and the ears removed and counted in a Packard Gamma Spectrometer. The results are expressed as the ratio of the radioactivity in the left ear to the radioactivity in the right ear (L/R '25I-dUrd uptake). It is unusual to obtain a ratio greater than 1.2 in nonsensitized miceor in naive mice not receiving sensitized cells. Antisera. Anti-Thy-i and anti-h-2 sera of appropriate specificities were prepared as described before (7). RESULTS Previous work establishing that the transfer of DTH required I-A identity at the MHC, at least for protein antigens such as FGG (6), is confirmed with mice used in an experiment reported in Table 1. In addition, whereas I-A identity alone was sufficient for DTH transfer to FGG, either I, K, or D identity alone could permit DTH transfer to DNFB (Table 1). This difference in genetic constraints imposed on the transfer of sensitivity to protein antigens and to reactive contact chemical agents may be related to different subsets of s, some reacting to antigens processed and presented by macrophages, and others reacting to compounds able to modify a variety of MHC gene products on cell surfaces. The work establishing the details of these interactions will be described elsewhere. DTH transfer with cells sensitized in chimeric environments To create an environment where a given antigen may be presented on macrophages of two different genotypes, we used tetraparental bone marrow chimeras (TBMC) of the type used by von Boehmer and Sprent (8) in their studies on T and B cell collaboration in antibody responses. Cells from such TBMC are unresponsive in both the mixed lymphocyte reaction and cell mediated lysis to either parent's histocompatibility antigens but have unimpaired reactivity to third party determinants (8). The cells of the TBMC do, however, express K and D serological specificities of the MHC since they can be lysed by specific alloantisera, and also express I determinants since they can be
3 2488 Immunology: Miller et al. Proc. Nati. Acad. Sci. USA 73 (1976) Table 2. s sensitized in chimeric environment transfer DTH to MIC-incompatible parental recipients L/R 125I-dUrd Source of sensitized cells* Recipients uptaket - Cells from sensitized CBA C57BL TBMC CBAt 1.45 ± 0.03 treated with anti-c57bl H-2 serum (CBA x C57BL)F, 1.82 ± 0.12 C57BL 1.91 ± 0.10 CBA cells from sensitized CBA CBA 1.98 ± 0.06 (CBA x C57BL)F, 1.89 ± 0.05 C57BL 1.01 ± 0.05 * Lymphoid cells (10 x 106) were transferred. t The response to FGG in recipients not given cells was CBA: 1.10 i 0.04; (CBA x C57BL)F1: ; C57BL: t Arithmetic mean X 1 SEM. Five mice per group. used as stimulator cells in the mixed lymphocyte reaction (8). TBMC made from CBA and C57BL mice and containing roughly 50% CBA cells and 50% C57BL cells in their hemopoietic system, were sensitized to FGG. Lymph node cells were taken 5 days later, and separated into CBA and C57BL cells by appropriate incubation with relevant anti-h-2 sera able to kill either CBA or C57BL cells. The remaining cells were then washed and tested for their capacity to transfer DTH to naive recipients. For simplicity, we show here the results obtained with the transfer of CBA cells sensitized to FGG in the chimeric environment (Table 2). The cells transferred DTH as effectively to allogeneic C57BL as to syngeneic or F1 mice. This contrasts with the failure of CBA cells, sensitized in normal nonchimeric CBA mice, to transfer DTH to allogeneic C57BL mice. These findings argue in favor of the notion that s, primed in a,chimeric environment made up of two different strains, are primed to antigen 1 and I region gene product a (Fig. 2) as well as to antigen 1 and I region gene product b. Thus, in the TBMC environment, as suggested by von Boeheer and Sprent (8), CBA s would be composed of two different subsets of primed s, one with specificity towards the antigen and the I region of CBA and another with specificity towards the antigen and the I region determinant of C57BL. Alternatively, the s could utilize two receptors, one recognizing antigen, the other an I-region gene product. DTH transfer with F1 cells sensitized in parental strain It was previously shown (6) that primed s from F1 mice will successfully transfer DTH to both parental strains as well as to the syngeneic F1. The question was therefore asked: can F1 s sensitized, not in the F1 animal, but in one of the parental strains (say X) transfer DTH to both parental strains (X and say Y) or only to that in which they were originally sensitized, namely X. To sensitize F1 cells not in the F1 but in one of the parental strains, we made use of the athymic nude mice which are available on several congenic backgrounds. DTH could not be elicited in these mice unless they were first *- TBMC X*OY-- -- jr'i0 Ag-. combining (stram X) M I(strainY)I M 0-0 A (stroln X) (strain X) 2 subsets of primed X s & 2 subsets of primed Y s -Ag sombining FIG. 2. Possible different types of reactive s in sensitized tetraparental bone marrow chimeras (TBMC) (see text). Abbreviations as in Fig. 1. reconstituted with thymus cells or a mixture of thymus and lymph node cells (Table 3). To sensitize F1 s in the parental environment, s from naive, nonsensitized, (CBA X BALB/c)F1 mice were used to reconstitute BALB/c.nu and CBA.nu, and these were then sensitized to FGG. We then transferred lymph node cells from such reconstituted mice to naive BALB/c and CBA mice to test for their ability to transfer DTH. It is evident that F1 cells sensitized in BALB/c.nu could transfer DTH successfully only to BALB/c, not to CBA. On the other hand, F1 s sensitized in CBA.nu could transfer DTH successfully only to CBA, not to BALB/c (Table 4). These results strongly support the notion that sensitization of s in an F1 mouse leads to the activation of two subsets of F1 s with respect to the specificity of their antigen combining sites: one with sites directed towards the antigen and the I-A. region gene product of one parental strain, the.other with sites directed towards the antigen and the I-A region gene product of the other parental strain (Fig. 3). Sensitization of F1 s in the parental environment would thus lead to the activation of only one of these two subsets of s. The model (model II, Fig. 1) which demands matching of identical I-A region gene products can be substantiated only if these products were subject to allelic exclusion, for which there is no evidence. DTH transfer with cells from mice sensitized by antigen-pulsed macrophages Macrophages from CBA or BALB/c mice were pulsed with FGG in vitro, washed and injected into cyclophosphamidepretreated (CBA X BALB/c)F1 mice. High levels of sensitivity were achieved in this manner with doses of antigen that were calculated (using radiolabeled FGG) to be 100 to 1000 less than is needed for aggregated antigen. Lymphoid cells from mice sensitized with such macrophage preparations were tested for their ability to transfer DTH into parental naive recipients. The results shown in Table 5 indicate that cell transfer of DTH was possible provided the macrophages used for sensitization were Table 3. DTH to FGG in athymic- nude mice Strain of L/R '2SI-dUrd nude mice s given* uptaket' BALB/c.nu None 1.05 ± 0.11 BALB/c.nu BALB/c 4.10 ± 0.06 BALB/c.nu (CBA x BALB/c)F, 3.82 ± 0.16 CBA.nu None 0.94 ± 0.08 CBA.nu CBA 3.23 ± 0.50 CBA.nu (CBA x BALB/c)F, 3.70 ± 0.30 * Mice were given a mixture of 4 X 108 thymus and lymph node cells in two doses 1 week apart. t Arithmetic mean 4 1 SEM. Five to six mice per group.
4 Table 4. Immunology: Miller et al. Effect of transfer of sensitized lymph node cells from reconstituted nude mice Donors of sensitized L/R '25I-dUrd lymph node cells* Recipients uptaket CBA.nu CBA 1.65 ± 0.08 (5) CBA.nu BALB/c 1.18 ± 0.13 (5) BALB/c.nu CBA 1.01 ± 0.15 (4) BALB/c.nu BALB/c 1.73 ± 0.14 (4) CBA 1.17 ± 0.09 (6) BALB/c 1.15 ± 0.04'(6) * Donors were reconstituted by 3 weekly injections of 108 (CBA x BALB/c)Fi thymus + mesenteric lymph node cells before sensitization. Lymph node cells (17 x 106) were injected intravenously into each recipient. t Mean + SlM. Number of mice per group shown in brackets. of the same genotype as the recipients. This again strongly supports the notion that sensitization is directed not to the antigen as such but to cell surface structures on the macrophage determined partly by an MHC gene product (I-A) and partly by the processed antigen. Similar observations have recently been made by Pierce et al. (9) who demonstrated restriction in macrophage- interaction in the secondary response induced by the primary response. DTH in responder and nonresponder mice The above results suggest that one possible mechanism of Ir gene control of -dependent responses is that low responders may lack the appropriate I region gene that is essential to produce (in the macrophage) the product with which a particular antigenic determinant can become associated after the antigen is processed by that cell. The defect in the low responder may thus depend on an inadequate repertoire of I-A region gene products expressed in macrophages. Alternatively, the defect could be in the scope of the receptor dictionary in the s. It was, therefore, of interest to study the responsiveness of mice to the B isoenzyme of lactic dehydrogenase which is under genetic control (10). As shown in Fig. 4, a good DTH response was obtained in responder C57BL mice but none, at any time, in nonresponder CBA mice. If, however, the mice were pretreated 2 days prior to antigen sensitization with 200 mg/kg of cyclophosphamide, DTH could be elicited from CBA mice, but the period of sensitivity was short lived. The low responder strain cannot therefore lack s with appropriate specificities, nor the mechanism by which stimulator cells or macrophages effectively present antigen to s (presumably in association with the I-A region gene product). Under normal conditions however, this stimulation potential is suppressed by Proc. Natl. Acad. Sci. USA 73 (1976) 2489 I (X/Yb)Fi I a l A 9 T oell (anti-bl) (XaYbF (anti-cl) (Xa/Yb) Fi 2 sub se ts of anti-i reactive s In primed Fh FIG. 3. Possible different types of reactive s in sensitized F1 (see text). Abbreviations as in Fig. 1. a cyclophosphamide-sensitive mechanism, the nature of which remains to be elucidated. Candidates for such a suppressive mechanism are, of course, suppressor s but their role in this particular system has yet to be established unequivocally. DISCUSSION Taken in toto, the findings obtained in the experiments with TBMC, with F1 s sensitized in parental strains, and with cells sensitized by semi-allogeneic macrophages, argue strongly in favor of the notion that sensitized s have antigen receptors predominantly directed to cell surface components. These are determined partly by genes coding for the K, I, or D products and partly by the antigenic determinant as it appears on the cell surface after macrophage processing. It would appear from our previous work with DTH to FGG (6) and from the work of Erb and Feldmann with helper s in antibody production (3), that the Ly-1, which is responsible for both DTH and helper functions (11), can be activated only by antigen associated with macrophages and can discriminate variation in antigenic pattern associated with I region gene products. On the other hand, the Ly-2, responsible for direct cytotoxicity, has a dictionary restricted to variations of the pattern of antigen in association with molecules coded by the K or D genes of the MHC (4). From the data obtained here (Table 1), it is therefore tempting to postulate that two subsets of s may be responsible for the transfer of DTH to DNFB. A basic difference in the mechanisms of antigen activation of primed B and s was suggested by previous work performed here with the collaboration of Prof. Basten (7) in which entirely different conditions were shown to be essential for inactivation or "suicide" of primed T and B lymphocytes by radiolabeled antigen. First, suicide, unlike B cell suicide, could be achieved only if antigen was presented, not in soluble form, but in association with other cell types, probably macrophages. Second, suicide occurred with s only if incu- Table 5. Transfer of DTH with lymphoid cells from mice sensitized with macrophage associated antigen Naive recipient of 6 X 107 sensitized Source of FGG Mice sensitized with (CBA X BALB/c)F1 pulsed macrophages FGG pulsed macrophages* spleen cells L/R 125I-dUrd uptaket CBA (CBA x BALB/c)F, CBA 1.62 ±.0.09 CBA (CBA X BALB/c)F, BALB/c 1.11 ± 012 BALB/c (CBA X BALB/c)F1 CBA 1.12 ± 0.05 BALB/c (CBA X BALB/c)F1 BALB/c 1.63 ± 0.17 * The L/R 1251-dUrd uptake in (CBA x BALB/c)F1 when sensitized with CBA macrophage-associated FGG was while with BALB/c-associated FGG, it was on the day of cell transfer. t Arithmetic mean + 1 SEM. Six mice per group.
5 2490 Immunology: Miller et al. : J L Ī r- lo0.' Po a I a I a I I a 1- i I a I J 3 S 7 9 it 13 Is 17 19,2 DAYS AFTER SENSITIZATION TO LDH B FIG. 4. DTH response in C57BL and CBA mice sensitized with the B isoenzyme of lactic dehydrogenase (LDHB). 0-0, response in CBA mice not pretreated with cyclophosphamide; A-A, response in CBA mice pretreated with cyclophosphamide; *-*, response in C57BL mice not pretreated with cyclophosphamide; A-A, response in C57BL mice pretreated with cyclophosphamide. Controls were not sensitized. Proc. Natl. Acad. Sci. USA 73 (1976) bation was at 370, not at 4 even though 40 was effective for B cell suicide. Third, s could be protected from suicide by preincubation with alloantiserum directed against relevant MHC components whereas anti-immunoglobulin had no protective effect. By contrast, B cell suicide could be prevented by anti-immunoglobulin, not by anti-h-2 pretreatment. Finally, certain inhibitors of metabolism, such as azide, had no effect on B cell suicide but prevented suicide. These findings support the notion that components of the MHC must somehow be intimately involved in primed activation. In addition, these observations may explain why so-called "T-independent" antigens (12) or antigens composed of D-amino acids (13) do not induce T helper cells or allow DTH, although they can elicit IgM responses from B cells. Such antigens are either poorly metabolized or nondegradable and hence may be unable to activate s since this appears to require antigen processing by metabolically active macrophages. Since macrophages are essential for the activation of some subsets, it is possible that the lesion of genetic nonresponsiveness resides in the macrophage which could display an inadequate repertoire of I-A region gene products. This idea does not appear to be supported by the results obtained with the B isoenzyme of lactic dehydrogenase in which low responders could be made to respond after cyclophosphamide treatment. Alternatively, cyclophosphamide may temporarily allow macrophages to process antigen in a more immunogenic form, irrespective of the responder status. There is increasing evidence that evolution of cell surface components occurred so that recognition of nonself in the process of fertilization in hermaphrodite species and of self in the process of cell association for the growth of particular tissues was possible. The basis for such diversity of cell surface structures in the colonial tunicate, Botryllus, is a single genetic locus with multiple alleles (14). Such a gene locus is the logical precursor of the 4 loci on chromosome 17 of the mouse, Tit, H-2K, H-2D, and TL, each of which specifies surface glycoproteins *of similar nature and molecular weight and enables cell recognition either in embryogenesis or later (15). IfMHC gene products did evolve to enable cell recognition for allofertilization and for tissue growth and development, there must have been an associated parallel evolution of complementary recognition elements. It is tempting to suggest that from these elements evolved the receptors for antigen. The possibility that at least part of this receptor is coded by V genes similar or identical to those responsible for immunoglobulin diversity has received support from the recent work of Eichmann and Rajewsky (16) and Binz and Wigzell (17). This suggests, as an alternative to the "altered self" hypothesis (model I, Fig. 1), that s may utilize a dual recognition system, i.e., two separate receptors, one for antigen, the other for a particular MHC give product (18). The results reported here do not discriminate between these two hypothesis, but they do exclude the mechanism illustrated by model II of Fig. 1. This work was supported by the National Health and Medical Research Council of Australia and by U.S. Public Health Service Research Grant no from the National Cancer Institute. 1. Rosenthal, A. S., Lipsky, P. E. & Shevach, E. M. (1975) Fed. Proc. 34, Katz, D. H. & Benacerraf, B. (1975) Transplant. Rev. 22, Erb, P. & Feldmann, M. (1975) J. Exp. Med. 142, Doherty, P. C., Blanden, R. V. & Zinkernagel, R. M. (1976) Transplant. Rev Shearer, G. M., Rehn, G. R. & Garbarino, C. A. (1975) J. Exp. Med. 141, Miller, J. F. A. P., Vadas, M. A., Whitelaw, A. & Gamble, J. (1975) Proc. Nati. Acad. Sci. USA 72, Basten, A., Miller, J. F. A. P. & Abraham, R. (1975) J. Exp. Med. 141, von Boehmer, H. & Sprent, J. (1976) Transplant. Rev. 29, Pierce, C. W., Kapp, J. A. & Benacerraf, B. (1976) J. Exp. Med., in press. 10. Melchers, I., Rajewsky, K. & Shreffler, D. C. (1973) Eur. J. Immunol. 3, Vadas, M. A., Miller, J. F. A. P., McKenzie, I. F. C., Chism, S. E., Shen, F.-W., Boyse, E. A., Gamble, J. R. & Whitelaw, A. M. (1976) J. Exp. Med. 144, in press. 12. Sela, M., Mozes, E. & Shearer, G. M. (1972) Proc. Nati. Acad. Sd. USA 69, Benacerraf, B. & Katz, D. H. (1974) J. Immunol. 112, Burnet, F. M. (1971) Nature 232, Vitteta, E. S., Artzt, K., Bennett, D., Boyse, E. A. & Jacob, F. (1975) Proc. Natl. Acad. Sd. USA 72, Eichmann, K. & Rajewsky, K. (1975) Eur. J. Immunol. 5, Binz, H. & Wigzell, H. (1975) J. Exp. Med. 142, Doherty, P. C., Gotze, D., Trinchieri, G. & Zinkernagel, R. M. (1976) Immunogenetics, in press.
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