The effect of a single allogeneic pregnancy on females’ responsiveness to paternal alloantigens was investigated using RT1-incompatible rats. Fischer (FI) strain females were grafted at various times after the birth of their first litters by DA males with skin from either DA donors or their own F1 hybrid offspring. Controls were provided by similarly grafting virgin FI females and FI females who had borne syngeneic, i.e., FI, litters. Although allogeneically primiparous females rejected the skin allografts as promptly as controls, their capacity to produce hemagglutinating alloantibodies in response to these grafts was severely depressed compared with that of both virgin and pregnancy controls. The switch from IgM to IgG production in the “primary” response of the allogeneically pregnant females was also affected, being of delayed onset. These lower levels of antibodies detected reflected a true diminished capacity to respond and not a shortcoming in the ability of the test system to reveal agglutinating antibodies in maternal serum. Decreased antibody responses were demonstrable in females grafted at 9 to 12 days of allogeneic gestation, but not before. This hyporesponsiveness was specific for paternal antigens in that it was observed in third-party tests only if the paternal strain and graft donor shared significant alloantibody-inducing RT1 antigens. Thus, a single allogeneic pregnancy in the rat induces consistent, specific hyporesponsiveness to paternal alloantigens at the humoral level of the female’s immune response system without influencing the expression of cellular immunity, i.e., her ability to reject a paternal skin allograft. This dichotomous effect on the maternal immune response system is discussed in terms of the possible mechanism(s) mediating this naturally induced hyporesponsiveness to transplantation antigens.
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