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Cornelia Berlin-Rufenach^*,||, Florian Otto, Meg Mathies^*, Juergen Westermann, Michael J. Owen, Alf Hamann^||,¶, and Nancy Hogg^*

From the ^* Leukocyte Adhesion Laboratory and the Lymphocyte Molecular Biology Laboratory, Imperial Cancer Research Fund, London WC2A 3PX, United Kingdom; the Center of Anatomy, Medical School of Hannover, D-30623 Hannover, Germany; the ^|| Department of Immunology, Medical Clinic, University Hospital Eppendorf, D-20246 Hamburg, Germany; and ^¶ Charité Clinic, Humboldt University, D-10117 Berlin, Germany

Using lymphocyte function-associated antigen (LFA)-1^–/– mice, we have examined the role of LFA-1 and other integrins in the recirculation of lymphocytes. LFA-1 has a key role in migration to peripheral lymph nodes (pLNs), and influences migration into other LNs. Second, the 4 integrins, 4β7 and 4β1, have a hitherto unrecognized ability to compensate for the lack of LFA-1 in migration to pLNs. These findings are confirmed using normal mice and blocking LFA-1 and 4 monoclonal antibodies. Unexpectedly, vascular cell adhesion molecule (VCAM)-1, which is essential in inflammatory responses, serves as the ligand for the 4 integrins on pLN high endothelial venules. VCAM-1 also participates in trafficking into mesenteric LNs and Peyer's patch nodes where mucosal addressin cell adhesion molecule 1 (MAdCAM-1), the 4β7-specific ligand, dominates. Both 4β1, interacting with ligand VCAM-1, and also LFA-1 participate in substantial lymphocyte recirculation through bone marrow. These observations suggest that organ-specific adhesion receptor usage in mature lymphocyte recirculation is not as rigidly adhered to as previously considered, and that the same basic sets of adhesion receptors are used in both lymphocyte homing and inflammatory responses.

Key Words: adhesion • integrin • homing • bone marrow • lymphocyte

C. Berlin-Rufenach was supported by an EMBO Fellowship. F. Otto was supported by Deutsche Forschungsgemeinschaft fellowship Ot 134/1-1. M. Mathies was supported by The Claremont Colleges, Claremont, CA. This work was funded by the Deutsche Forschungsgemeinschaft (A. Hamann) and the Imperial Cancer Research Fund.

F. Otto's present address is University of Freiburg Medical Center, 79106 Freiburg, Germany, and M. Mathies's is Joint Science Department, Claremont Colleges, Claremont, CA 91711.

C. Berlin-Rufenach, F. Otto, and M. Mathies contributed equally to this manuscript.

Abbreviations used: CT, CellTracker^TM; ES, embryonic stem; HEV, high endothelial venule; HUVEC, human umbilical vein endothelial cell; ICAM, intercellular adhesion molecule; MAdCAM-1, mucosal addressin cell adhesion molecule 1; pLN, peripheral lymph node; PNAd, peripheral node addressin; PP, Peyer's patch; VCAM, vascular cell adhesion molecule.

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