Tissue eosinophilia is characteristic of human atopic allergic inflammation, although the mechanism is largely unknown. In this study we test the hypothesis that eosinophil infiltration during allergen-provoked rhinitis in hayfever sufferers may occur as a consequence of activation of a population of cells having a characteristic cytokine profile equivalent to the murine Th lymphocyte Th2 subset. Biopsies of the nasal inferior turbinate were obtained from 10 grass pollen-sensitive patients 24 h after local nasal provocation with allergen and after a control challenge with the allergen diluent. Biopsies were divided into two and subsequently processed for in situ hybridization using 35S-labeled RNA probes for selected cytokines and for immunohistology using an eosinophil granule mAb (EG2) which recognizes secreting eosinophils. At allergen-challenged sites compared with control sites there were significant increases in mRNA+ cells for IL-3 (p less than 0.04), IL-4 (p = 0.01), IL-5 (p = 0.02) and granulocyte/macrophage-CSF (p = 0.03). In contrast, only occasional hybridization signals were observed for IL-2 and IFN-gamma at both allergen and control sites. After allergen there was an increase (p = 0.01) in EG2+ eosinophils and significant correlations were observed between EG2+ cells and mRNA expression for "Th2-type" cytokines, particularly IL-5 (r = 0.90, p less than 0.0001). These results demonstrate that recruitment of eosinophils during human allergen-induced rhinitis is associated with cells expressing mRNA for IL-3, IL-4, IL-5, and granulocyte/macrophage-CSF.