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J. Biol. Chem., Vol. 282, Issue 8, 5378-5388, February 23, 2007

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Cumulus Oophorus-associated Glycodelin-C Displaces Sperm-bound Glycodelin-A and -F and Stimulates Spermatozoa-Zona Pellucida Binding^*

Philip C. N. Chiu, Man-Kin Chung, Riitta Koistinen^¶, Hannu Koistinen^¶, Markku Seppala^¶, Pak-Chung Ho, Ernest H. Y. Ng, Kai-Fai Lee, and William S. B. Yeung¹

From the Department of Obstetrics and Gynaecology, University of Hong Kong, Queen Mary Hospital, Pokfulam Road, Hong Kong SAR, China and the Departments of Obstetrics and Gynaecology and ^¶Clinical Chemistry, University of Helsinki and Helsinki University, Central Hospital, 00029 HUS Helsinki, Finland

Spermatozoa have to swim through the oviduct and the cumulus oophorus before fertilization in vivo. In the oviduct, spermatozoa are exposed to glycodelin-A and -F that inhibit spermatozoa-zona pellucida binding. In this study, we determined whether these glycodelins would inhibit fertilization. The data showed that the spermatozoa without previous exposure to glycodelin-A and -F acquired glycodelin immunoreactivity during their passage through the cumulus oophorus. On the other hand, when glycodelin-A or -F-pretreated spermatozoa were exposed to the cumulus oophorus, the zona pellucida binding inhibitory activity of glycodelin-A and -F was not only removed, but the spermatozoa acquired enhanced zona pellucida binding ability. These actions of the cumulus oophorus were due to the presence of a cumulus isoform of glycodelin, designated as glycodelin-C. The cumulus cells could convert exogenous glycodelin-A and -F to glycodelin-C, which was then released into the surrounding medium. The protein core of glycodelin-C was identical to that in other glycodelin isoforms, as demonstrated by mass spectrum, peptide mapping, and affinity to anti-glycodelin antibody recognizing the protein core of glycodelin. In addition to having a smaller size and a higher isoelectric point, glycodelin-C also had lectin binding properties different from other isoforms. Glycodelin-C stimulated spermatozoazona pellucida binding in a dose-dependent manner, and it effectively displaced sperm-bound glycodelin-A and -F. In conclusion, the cumulus cells transform glycodelin-A and -F to glycodelin-C, which in turn removes the spermatozoazona binding inhibitory glycodelin isoforms and enhances the zona binding capacity of spermatozoa passing through the cumulus oophorus.

Received for publication, August 7, 2006 , and in revised form, November 1, 2006.

^* This work was supported in part by grants from the Committee on Research and Conference Grant; The University of Hong Kong; Hong Kong Research Grant Council Grants HKU7261/01M, HKU7408/03M, and HKU7647/06M, Helsinki University Central Hospital Research Funds; Federation of the Finnish Life and Pension Insurance Companies; the Cancer Society of Finland; the Academy of Finland; and the University of Helsinki. 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: Dept. of Obstetrics and Gynaecology, University of Hong Kong, Queen Mary Hospital, Pokfulam Road, Hong Kong SAR, China. Tel.: 852-28553405; Fax: 852-28175374; E-mail: wsbyeung{at}hkucc.hku.hk.

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