Rap1 translates chemokine signals to integrin activation, cell polarization, and motility across vascular endothelium under flow

doi:10.1083/jcb.200301133

Published online 21 April 2003. doi:10.1083/jcb.200301133

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© The Rockefeller University Press, 0021-9525/2003/4/417 $5.00
The Journal of Cell Biology, Volume 161, Number 2, 417-427

Article

Rap1 translates chemokine signals to integrin activation, cell polarization, and motility across vascular endothelium under flow

Mika Shimonaka¹^,2, Koko Katagiri¹, Toshinori Nakayama³, Naoya Fujita⁴, Takashi Tsuruo⁴, Osamu Yoshie⁵ and Tatsuo Kinashi¹

¹ Bayer-chair, Department of Molecular Immunology and Allergy
² Department of Dermatology, Graduate School of Medicine, Kyoto University, Kyoto 606-8501, Japan
³ Department of Molecular Immunology, Graduate School of Medicine, Chiba University, Chiba 263-8522, Japan
⁴ Institute of Molecular and Cellular Biosciences, University of Tokyo, Tokyo 113-8654, Japan
⁵ Department of Microbiology and Internal Medicine III, Kinki University School of Medicine, Osaka 589-0014, Japan

Address correspondence to Dr. Tatsuo Kinashi, Bayer-chair, Dept. of Molecular Immunology and Allergy, Graduate School of Medicine, Kyoto University, Yoshida-konoe, Sakyo-ku, Kyoto 606-8501, Japan. Tel.: 81-75-771-8159. Fax: 81-75-771-8184. E-mail: tkinashi{at}mfour.med.kyoto-u.ac.jp

Chemokines arrest circulating lymphocytes within the vasculaturethrough the rapid up-regulation of leukocyte integrin adhesiveactivity, promoting subsequent lymphocyte transmigration. However,the key regulatory molecules regulating this process have remainedelusive. Here, we demonstrate that Rap1 plays a pivotal rolein chemokine-induced integrin activation and migration. Rap1was activated by secondary lymphoid tissue chemokine (SLC; CCL21)and stromal-derived factor 1 (CXCL4) treatment in lymphocyteswithin seconds. Inhibition of Rap1 by Spa1, a Rap1-specificGTPase-activating protein, abrogated chemokine-stimulated lymphocyterapid adhesion to endothelial cells under flow via intercellularadhesion molecule 1. Expression of a dominant active Rap1V12in lymphocytes stimulated shear-resistant adhesion, robust cellmigration on immobilized intercellular adhesion molecule 1 andvascular cell adhesion molecule 1, and transendothelial migrationunder flow. We also demonstrated that Rap1V12 expression inlymphocytes induced a polarized morphology, accompanied by theredistribution of CXCR4 and CD44 to the leading edge and uropod,respectively. Spa1 effectively suppressed this polarizationafter SLC treatment. This unique characteristic of Rap1 maycontrol chemokine-induced lymphocyte extravasation.

Key Words: chemokines; LFA-1; ICAM-1; lymphocyte; transmigration

The online version of this article includes supplemental material.

^* Abbreviations used in this paper: HUVEC, human umbilical vascularendothelial cells; ICAM-1, intercellular adhesion molecule 1;LFA-1, lymphocyte function–associated antigen 1; LN, lymphnode; PTX, pertussis toxin; SDF-1, stromal-derived factor 1;SLC, secondary lymphoid tissue chemokine; VCAM-1, vascular celladhesion molecule 1; VLA-4, very late antigen 4.

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