Although the recruitment of macrophages to the lung is a central feature of airway inflammation, its function in ongoing T_h2 cell-mediated eosinophilic airway inflammation remains controversial. Here, we have demonstrated that the allergen-induced CD11b⁺ CD11c^int macrophage expressing CC chemokine receptor 3 (CCR3) in the lung performs a crucial function in the induction of eosinophilic asthma in a murine model. In the lungs of normal mice, residential cells evidencing high granularity phenotypically evidenced CD11b^int CD11c⁺ or CD11b⁺ CD11c^int cells, appearing at a 2:1 ratio. After allergen challenge, however, this reverses dramatically, up to a ratio of one to six. Approximately 91% of increased CD11b⁺ CD11c^int cells evidenced the expression of the CCR3 eotaxin receptor, but not other chemokine receptors, such as CCR5 and CXCR4. Interestingly, the CD11b⁺ CD11c^int cells purified from the lungs of OVA (ovalbumin)-sensitized and challenged mice evidenced higher antigen-presenting activity than was observed in CD11b^int CD11c⁺ cells. In order to investigate the in vivo function of CD11b⁺ CD11c^int cells, the cells were isolated from the lungs of OVA-sensitized and challenged mice and then adoptively transferred prior to the allergen challenge of normal mice. In the CD11b⁺ CD11c^int-transferred mice airway hyperresponsiveness, eosinophilic inflammation in the lung and T_h2 cytokine secretion in the bronchoalveolar lavage fluids were significantly enhanced as the result of OVA challenge, as compared with the mice that received OVA-primed CD90⁺ T cells or CD11b^int CD11c⁺ cells. These findings show that CD11b⁺ CD11c^int macrophages expressing CCR3 as key pro-inflammatory cells are both necessary and sufficient for allergen-specific T cell stimulation during ongoing eosinophilic airway inflammation.