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J. Biol. Chem., Vol. 278, Issue 31, 29048-29056, August 1, 2003

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Regulation of Blastocyst Migration, Apposition, and Initial Adhesion by a Chemokine, Interferon -inducible Protein 10 kDa (IP-10), during Early Gestation^*

Kentaro Nagaoka  , Hisashi Nojima , Fumiko Watanabe ¶, Kyu-Tae Chang ||, Ronald K. Christenson **, Senkiti Sakai  and Kazuhiko Imakawa  

From the Laboratory of Animal Breeding, Faculty of Agriculture, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan, the ^¶R&D Department, Higeta Shoyu Co., Ltd, 2-8 Chuo, Choshi, Chiba 288-8680, Japan, the ^||Korea Research Institute of Bioscience & Biotechnology, Oun-dong 52, Yusong-ku, Daejon 305-333, Korea, and the ^**United States Meat Animal Research Center, USDA-ARS, Clay Center, Nebraska 68933-0166

For a pregnancy to be established, initial apposition and adhesion of the blastocyst to maternal endometrium must occur in a coordinated manner; however, a key factor(s) that mediates the trophoblast cell migration and attachment to the apical surface of the endometrium has not been identified. In this study, we examined the effect of an endometrial chemokine, interferon--inducible protein 10 kDa (IP-10), on conceptus migration to the endometrial epithelium. We first studied endometrial IP-10 mRNA expression, which was localized in the subepithelial stromal region, and detected the protein in the uterine flushing media during early pregnancy. Expression of IP-10 mRNA by the endometrium of cyclic animals was stimulated by the addition of a conceptus factor interferon-tau (IFN-). Immunofluorescent analysis revealed that IP-10 receptor, CXCR3, was localized in the trophoblast cells, to which biotinylated-recombinant caprine IP-10 (rcIP-10) bound. Chemotaxis assay indicated that rcIP-10 stimulated the migration of trophoblast cells, and the effects of rcIP-10 were neutralized by the pretreatment with an anti-IP-10 antibody. Adhesive activity of trophoblast cells to fibronectin was promoted by rcIP-10, and the effect was inhibited by the use of anti-IP-10 antibody. Further adhesion experiments demonstrated that binding of trophoblast cells to fibronectin was completely inhibited by a peptide of the Arg-Gly-Asp (RGD) sequence, which binds to integrins ₅₁, _V1, _V3, and _V5, whereas non-binding peptide containing Arg-Gly-Glu (RGE) had minimal effects. More importantly, rcIP-10 promoted the adhesion of trophoblast cells to primary cells isolated from endometrial epithelium. Furthermore, rcIP-10 stimulated the expression of integrin ₅, _V, and ₃ subunit mRNA in trophoblast cells. These findings suggest that endometrial IP-10 regulates the establishment of apical interactions between trophoblast and epithelial cells during early gestation.

Received for publication, January 16, 2003 , and in revised form, April 23, 2003.

^* This work was supported by a Grants-in-aid for Scientific Research (13556050 and 14206032) (to K. I.) from the Japan Society for the Promotion of Science and by the Program for Promotion of Basic Research Activities for Innovative Bioscience (BRAIN). 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.

Supported by Research Fellowships of the Japan Society for the Promotion of Science for Young Scientists.

To whom correspondence should be addressed: Laboratory of Animal Breeding, Faculty of Agriculture, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan. Tel.: 81-3-5841-5382; Fax: 81-3-5841-8180; E-mail: akaz{at}mail.ecc.u-tokyo.ac.jp.

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