Recruitment of lymphocytes to the lung through vaccination enhances the immunity of mice exposed to irradiated schistosomes

Abstract

The effector mechanism, which operates against challenge parasites in the lungs of C57BL/6 mice vaccinated once with irradiated cercariae of Schistosoma mansoni, is mediated by CD4+ T helper lymphocytes. However, adoptive transfer of immunity from vaccinated donors to naive recipients by using sensitized T cells has not proved successful. One explanation may be that the recruitment of sensitized T lymphocytes to the lungs by vaccinating parasites to arm that organ is not reproduced by transfer protocols. We have used the technique of parabiosis, as a means of adoptive transfer, to demonstrate the relevance of pulmonary T cells to protection. Sensitized and naive partners were joined surgically for a 28-day period, coincident with priming of the immune system. A vascular union rapidly developed, and sensitized T cells were detected in the spleens of the naive partners. When parabionts were challenged percutaneously 10 days after separation, the level of immunity transferred to the naive partners was approximately two-thirds that of their vaccinated counterparts. The naive partners, unlike the vaccinated animals, did not recruit lymphocytes to the lungs during the priming period. In contrast, after percutaneous challenge, schistosome-specific lymphocytes were recruited to the lungs of both separated parabionts. The importance of lymphocytes recruited to the lungs during the primary response was revealed by an intravenous challenge with lung schistosomula; this eliminates the opportunity for secondary immune responses prior to parasite arrival in the lungs. In this situation, the vaccinated partners showed 47% immunity while the naive partners were not protected. We conclude that the presence of specific T cells in the lungs at the time of challenge confers a significant advantage, permitting a more effective recall response than in animals lacking such resident cells.