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Role of CXC Chemokine Ligand 13, CC Chemokine Ligand (CCL) 19, and CCL21 in the Organization and Function of Nasal-Associated Lymphoid Tissue¹

Javier Rangel-Moreno^*, Juan Moyron-Quiroz^*, Kim Kusser^*, Louise Hartson^*, Hideki Nakano and Troy D. Randall^2,*

^* Trudeau Institute, Saranac Lake, NY 12983; and Department of Medicine, Duke University Medical Center, Durham, NC 27710

Nasal-associated lymphoid tissue (NALT) orchestrates immune responses to Ags in the upper respiratory tract. Unlike other lymphoid organs, NALT develops independently of lymphotoxin- (LT). However, the structure and function of NALT are impaired in Lt^–/– mice, suggesting a link between LT and chemokine expression. In this study we show that the expression of CXCL13, CCL19, CCL21, and CCL20 is impaired in the NALT of Lt^–/– mice. We also show that the NALT of Cxcl13^–/– and plt/plt mice exhibits some, but not all, of the structural and functional defects observed in the NALT of Lt^–/– mice. Like the NALT of Lt^–/– mice, the NALT in Cxcl13^–/– mice lacks follicular dendritic cells, BP3⁺ stromal cells, and ERTR7⁺ lymphoreticular cells. However, unlike the NALT of Lt^–/– mice, the NALT of Cxcl13^–/– mice has peripheral node addressin⁺ high endothelial venules (HEVs). In contrast, the NALT of plt/plt mice is nearly normal, with follicular dendritic cells, BP3⁺ stromal cells, ERTR7⁺ lymphoreticular cells, and peripheral node addressin⁺ HEVs. Functionally, germinal center formation and switching to IgA are defective in the NALT of Lt^–/– and Cxcl13^–/– mice. In contrast, CD8 T cell responses to influenza are impaired in Lt^–/– mice and plt/plt mice. Finally, the B and T cell defects in the NALT of Lt^–/– mice lead to delayed clearance of influenza from the nasal mucosa. Thus, the B and T cell defects in the NALT of Lt^–/– mice can be attributed to the impaired expression of CXCL13 and CCL19/CCL21, respectively, whereas impaired HEV development is directly due to the loss of LT.

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