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J. Biol. Chem., Vol. 281, Issue 29, 20303-20314, July 21, 2006

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SHAP Potentiates the CD44-mediated Leukocyte Adhesion to the Hyaluronan Substratum^*

Lisheng Zhuo, Akiko Kanamori^¶, Reiji Kannagi^¶, Naoki Itano, Jiwen Wu, Michinari Hamaguchi^||, Naoki Ishiguro^**, and Koji Kimata¹

From the Institute for Molecular Science of Medicine, Aichi Medical University, Nagakute, Aichi 480-1195, the ^¶Program of Molecular Pathology, Aichi Cancer Center Research Institute, Nagoya, Aichi 464-8681, the CREST, Japan Science and Technology Agency, Kawaguchi, Saitama 560-0082, and the ^||Department of Molecular Pathogenesis, and ^**Department of Orthopedic, Nagoya University Graduate School of Medicine, Nagoya, Aichi 466-8550, Japan

CD44-hyaluronan (HA) interaction is involved in diverse physiological and pathological processes. Regulation of interacting avidity is well studied on CD44 but rarely on HA. We discovered a unique covalent modification of HA with a protein, SHAP, that corresponds to the heavy chains of inter--trypsin inhibitor family molecules circulating in blood. Formation of the SHAP·HA complex is often associated with inflammation, a well known process involving the CD44-HA interaction. We therefore examined the effect of SHAP on the CD44-HA interaction-mediated lymphocyte adhesion. Under both static and flowing conditions, Hut78 cells (CD44-positive) and CD44-transfected Jurkat cells (originally CD44-negative) adhered preferentially to the immobilized SHAP·HA complex than to HA. The enhanced adhesion is exclusively mediated by the CD44-HA interaction, because it was inhibited by HA, but not II, and was completely abolished by pretreating the cells with anti-CD44 antibodies. SHAP appears to potentiate the interaction by increasing the avidity of HA to CD44 and altering their distribution on cell surfaces. Large amounts of the SHAP·HA complex accumulate in the hyperplastic synovium of rheumatoid arthritis patients. Leukocytes infiltrated to the synovium were strongly positive for HA, SHAP, and CD44 on their surfaces, suggesting a role for the adhesion-enhancing effect of SHAP in pathogenesis.

Received for publication, June 20, 2005 , and in revised form, April 19, 2006.

^* This work was supported in part by a grant-in-aid for Scientific Research (B) from Japan Society for the Promotion of Science, by a grant from the CREST of Japan Science & Technology Agency, and by a special research fund from Seikagaku Corp. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ To whom correspondence should be addressed. Tel.: 81-52-264-4811 (ext. 2088); Fax: 81-561-63-3532; E-mail: kimata{at}amugw.aichi-med-u.ac.jp.

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