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J. Biol. Chem., Vol. 278, Issue 45, 44874-44885, November 7, 2003

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Cloning and Developmental Analysis of Murid Spermatid-specific Thioredoxin-2 (SPTRX-2), a Novel Sperm Fibrous Sheath Protein and Autoantigen^*

From the ^aCenter for Biotechnology, Department of Biosciences at Novum, Karolinska Institutet, S-14157 Huddinge, Sweden, the ^cDepartment of Anatomy and Cell Biology, Queen's University, Kingston, Ontario K7L 3N6, Canada, the ^eDepartment of Developmental Biology, Tampere University Medical School, and the Department of Pathology, Tampere University Hospital, Fin-33101 Tampere, Finland, the ^gDepartment of Cell Biology, University of Virginia, Charlottesville, Virginia 22908, and the ⁱDepartments of Animal Science and Obstetrics and Gynecology, University of Missouri, Columbia, Missouri 65211-5300

Thioredoxins compose a growing family of proteins that participate in different cellular processes via redox-mediated reactions. We report here the cloning, developmental expression, and location of murid Sptrx-2. Mouse and rat SPTRX-2 proteins display a high homology to their human ortholog in the thioredoxin and NDP kinase domains, and the coding genes are located at syntenic positions. Northern blotting and in situ hybridization confirmed the testis-specific expression of murine Sptrx-2 mRNA, mostly in round spermatids. Immunohistochemical analysis of the 19 steps of rat spermiogenesis showed that SPTRX-2 expression becomes prominent in the cytoplasmic lobe of step 15–18 spermatids and diminishes in step 19 just before spermiation. However, in the spermatid tail, SPTRX-2 immunoreactivity increased from step 15 to 19 and was confined to the principal piece. By immunogold electron microscopy, SPTRX-2 was first detected scattered throughout the cytoplasm of the axoneme in step 14–15 spermatids, but began to be incorporated by step 16 into the fibrous sheath (FS). During steps 17–18, the labeling increased over the ribs and columns of the assembled FS. It peaked in step 19 and remained in the FS of epididymal spermatozoa. Immunoblots of isolated FS obtained from spermatozoa confirmed that SPTRX-2 is an integral component of the FS and a post-obstruction autoantigen in vasectomized rats. Our data indicate that SPTRX-2 incorporation into the FS lags well behind FS assembly, suggesting it is required during the final stages of sperm tail maturation in the testis and/or epididymis, where extensive disulfide bonding of FS proteins occurs.

Received for publication, May 24, 2003 , and in revised form, July 9, 2003.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) AF548543 and AF548544.

^* This work was supported in part by grants from the Canadian Institutes of Health Research and National Sciences and Engineering Research Council of Canada (to R. O.) and by Swedish Medical Research Council Projects 03P-14096, 03X-14041, and 13X-10370 and grants from the Åke Wibergs Stiftelse and the Karolinska Institutet (to A. M.-V.). 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.

^b Both authors contributed equally to this work.

^d Supported by the Fundación Margit and Folke Pehrzon.

^f Supported by the Research Fund of the Tampere University Hospital, Tampere University.

^h Supported by NIDDK Grant P50 DK45179 and NICHD Grant HD U54-29009 from the National Institutes of Health.

^j Supported by the Food for the 21st Century Program of the University of Missouri, United States Department of Agriculture Grants 2002-02069 and 99-35203-7785, and National Institute for Occupational Safety and Health Grant OH07324-01.

^k To whom correspondence should be addressed. Tel.: 613-533-2858; Fax: 613-533-2566; E-mail: ro3{at}post.queensu.ca.

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