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The Journal of Immunology, 2003, 170: 4638-4648.
Copyright © 2003 by The American Association of Immunologists

Naive T Cell Recruitment to Nonlymphoid Tissues: A Role for Endothelium-Expressed CC Chemokine Ligand 21 in Autoimmune Disease and Lymphoid Neogenesis1

Wolfgang Weninger2,*,{dagger}, Hege S. Carlsen{ddagger},§, Mahmoud Goodarzi*,{dagger}, Farzad Moazed*, Maura A. Crowley*, Espen S. Baekkevold{ddagger}, Lois L. Cavanagh*,{dagger} and Ulrich H. von Andrian2,*,{dagger}

* The Center for Blood Research and {dagger} Department of Pathology, Harvard Medical School, Boston, MA 02115; and {ddagger} Institute of Pathology and § Department of Surgery, University of Oslo, Rikshospitalet, Norway

Naive T cells are usually excluded from nonlymphoid tissues. Only when such tertiary tissues are subjected to chronic inflammation, such as in some (but not all) autoimmune diseases, are naive T cells recruited to these sites. We show that the CCR7 ligand CC chemokine ligand (CCL)21 is sufficient for attracting naive T cells into tertiary organs. We performed intravital microscopy of cremaster muscle venules in T-GFP mice, in which naive T cells express green fluorescent protein (GFP). GFP+ cells underwent selectin-dependent rolling, but no firm adherence (sticking). Superfusion with CCL21, but not CXC chemokine ligand 12, induced integrin-dependent sticking of GFP+ cells. Moreover, CCL21 rapidly elicited accumulation of naive T cells into sterile s.c. air pouches. Interestingly, a second CCR7 ligand, CCL19, triggered T cell sticking in cremaster muscle venules, but failed to induce extravasation in air pouches. Immunohistochemistry studies implicate ectopic expression of CCL21 as a mechanism for naive T cell traffic in human autoimmune diseases. Most blood vessels in tissue samples from patients with rheumatoid arthritis (85 ± 10%) and ulcerative colitis (66 ± 1%) expressed CCL21, and many perivascular CD45RA+ naive T cells were found in these tissues, but not in psoriasis, where CCL21+ vessels were rare (17 ± 1%). These results identify endothelial CCL21 expression as an important determinant for naive T cell migration to tertiary tissues, and suggest the CCL21/CCR7 pathway as a therapeutic target in diseases that are associated with naive T cell recruitment.


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